Advances In Psychology Volume 86 Applications of Parallel Processing in Vision

APPLICATIONS OF PARALLEL PROCESSING IN VISION ADVANCES IN PSYCHOLOGY 86 Editors: G. E. STELMACH P. A. VROON NORTH-...

Author: Brannan J. R.

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APPLICATIONS OF PARALLEL PROCESSING IN VISION

ADVANCES IN PSYCHOLOGY 86 Editors:

G. E. STELMACH

P. A. VROON

NORTH-HOLLAND AMSTERDAM * LONDON NEW YORK TOKYO

APPLICATIONS OF PARALLEL PROCESSING IN VISION

Edited by

Julie R. BRANNAN Departments of Neurohiology and Neurology The Mount Sinai Medical Center N e w York, NY, U.S.A.

I992 NORTH-HOLLAND AMSTERDAM LONDON NEW YORK TOKYO 9

NORTH-HOLLAND ELSEVIER SCIENCE PUBLISHERS B.V. Sara Burgerhartstraat 25 P.O. Box 2 I I, 1000 AE Amsterdam, The Netherlands

Distributors for the United States and Canada: ELSEVIER SCIENCE PUBLISHING COMPANY. INC. 655 Avenue of the Americas New Y0rk.N.Y. 10010. U.S.A.

ISBN: 0 444 88651 6 01992 ELSEVIER SCIENCE PUBLISHERS B.V. All rights reserved.

No part of this publication may be reproduced, stored in a retrieval system. or transmitted, i n any form or by any means, electronic. mechanical, photocopying, recording or otherwise. without the prior written permission of the publisher, Elsevier Science Publishers B.V., Permissions Department, P.O. Box 521, 1000 AM Amsterdam, The Netherlands. Special regulations for readers in the U.S.A. - This publication has been registered with the Copyright Clearance Center Inc. (CCC), Salem, Massachusetts. Information can be obtained from the CCC about conditions under which photocopies of parts of this publication may be made in the U.S.A. All other copyright questions, including photocopying outside of the U.S.A., should be referred to the copyright owner, Elsevier Science Publishers B.V., unless otherwise specified. No responsibility is assumed by the publisher for any injury and/or damage to persons or property as a matter of products liability, negligence or otherwise, or from any use or operation of any methods, products. instructions or ideas contained in the material herein. Printed in The Netherlands

Table of Contents List of Contributors

vii

Preface

ix

INTRODUCTION TO PARALLEL PROCESSING 1.

2.

Parallel Retinocortical Channels: X and Y and P and M Robert Shapley Parallel Processing in Human Vision: History, Review, and Critique Bruno G. Breitmeyer

3

37

PARALLEL PROCESSING AND VISUAL DEVELOPMENT

3.

4.

Parallel Processes in Human Visual Development Adriana Fiorentini Changes in Temporal Visual Processing in Normal Aging Julie R. Brannan

81

119

PARALLEL PROCESSING IN HIGHER-ORDER PERCEPTION 5.

6.

7.

M and P Pathways and the Perception of Figure and Ground Naorni Weisstein, William Maguire, a n d Julie R. Brannan

137

Cooperative Parallel Processing in Depth, Motion and Texture Perception Douglas Williams

167

Parallel and Serial Connections Between Human Color Mechanisms Qasim midi

227

CONTENTS

vi

PARALLEL PROCESSING AND VISUAL ABNORMALITIES 8.

9.

Sensory and Perceptual Processing in Reading Disability M a y C. Williams and William Lovegrove

263

How Can the Concept of Parallel Channels Aid Clinical Diagnosis? M. Felice Ghilardi, Marc0 OnOfrJ, and Julie R. Brannan

303

Author Index

327

Subject Index

337

List of Contributors Julie R. Brannan Box 1052 Departments of Neurobiology and Neurology The Mount Sinai Medical Center One Gustave Levy Place New York, NY 10029

Bruno G. Breitmeyer Department of Psychology University of Houston Houston, TX 77204

Adriana Norentini Istituto di Neurofisiologia CNR Via S. Zen0 51 1-56127 Pisa. Italy M. Felice Ghilardi College of Physicians and Surgeons Columbia University Center for Neurobiology and Behavior 722 W. 168th Street Research Annex, Room 819 New York. NY 10032 William Lovegrove Department of Psychology University of Wollongong Wollongong, New South Wales Australia. 2500 William Maguire Department of Radiology Long Island Jewish Medical Center New Hyde Park, NY 11042 Marco Onofrj Clinica Neurologica Universita G. d ' h n u n z i o Ospedale Ex-Pediatric0 66100 Chieti Italy

viii

CONTRIBUTORS

Robert Shapley Center for Neural Science Departments of Psychology and Biology New York University New York. NY 10003 Naoml Weisstein State University of New York at Buffalo (on leave) 890 West End Avenue #8B New York. NY 10025

Douglas Williams Rockefeller University The Neurosciences Institute 1230 York Avenue New York. NY 10021 Mary C. Williams Department of Psychology University of New Orleans Lakefront Campus New Orleans, LA 70148

Qasim Z d d i Department of Psychology Columbia University New York. NY 10027

Preface A fundamental property of the human visual system is that information is processed in parallel. That is. visual sensory information is analyzed simultaneously along two or more independent pathways. This insight originated in the area of color perception, with an idea first expressed by Thomas Young in 1801 and later reformulated by Hermann Helmholtz in 1909. Their theory states that our perception of color depends solely on the response of three different pigments. These three color pathways, together with their opponent interaction, are sufficient to perceive the entire chromatic continuum. It has also been argued that, based on limitations of neural timing, massive parallel processing becomes the only biologically plausible mode of operation. For example, the "100 step rule" of Feldman and Ballard (Cognltiue Science, 1982) is a criterion which demonstrates the necessity of processing our complex visual world in parallel. The maximum rate of neuronal firing is 1000 Hz. and simple perceptual tasks require approximately 100 milliseconds. Given these parameters, biologically feasible phenomena could include no more than 100 steps - unless parallel processing occurs. In the past two decades, researchers have extensively used the concept of parallel visual channels as a framework to direct their explorations of human vision. Based initially on the discovery of functionally different sets of ganglion cells in cat retina, this concept has evolved over time to encompass the psychophysically based notion of a "transient-sustained'' dichotomy, and (more recently) a division based on magnocellular and parvocellular layers in the monkey LGN. What these various conceptualizations have in common is a "division of labor" based on temporal, spatial, chromatic, and contrast attributes of the visual world. Perhaps the controversy regarding the absolute validity of a strict functional dichotomy in humans is ultimately less important than the usefulness of such a dichotomy in guiding and directing vision research. For example, many researchers (and some clinicians) have found such a dichotomy applicable to the way we organize our knowledge of visual development, higher order perception, and visual disorders, to name just a few. This volume attempts to provide a forum for gathering these different perspectives. Robert Shapley opens the volume with an overview of the anatomical and physiological data in the cat and monkey which underlie our understanding of parallel channels, and how they may relate to human perception. Bruno Breitmeyer then provides a historical perspective on the concept of parallel processing in human visual perception. The next section deals with the development of parallel pathways in vision. Adriana Fiorentini describes what we know about this process in infancy, followed by a chapter describing temporal processing changes in the aging visual system (Brannan). Next, the implications of parallel processing to higher order perception are explored. Naomi Weisstein and colleagues report recent data and a qualitative model which suggest that the activity of parallel systems may

X

PREFACE

underlie our perception of figure and ground. Douglas Williams describes depth, motion, and texture perception in the context of parallel processing, while Qasim Zaidi's chapter provides a comprehensive review of parallel color mechanisms. Finally, the potential of using this concept to improve our understanding of visual disorders is discussed by Mary Williams and William Lovegrove (reading disability) and M.F.Ghilardi and associates (clinical diagnosis). Julie R. Brannan New York, New York

Introduction to Parallel Processing

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Applications of Parallel Processing in Vision J. B r m a n (Editor) @ 1992 Elsevier Science Publishers B.V. All rights reserved

3

Parallel Retinocortical Channels: X and Y and P and M ROBERT SHAPLEY

Multiple parallel neural mechanisms There has been a great advance in our understanding of the neural basis of vision in mammals. Different types of retinal ganglion cells, the output neurons of the retina, project in parallel, separately and independently, from the retina to the brain. The ganglion cells filter visual stimuli, sending on to the brain responses to those stimuli to which they are tuned. Furthermore, each of these cell types, or classes, is distributed throughout the retina. Therefore, activity across the population of cells in each one of the classes forms a representation of the world as "seen" by that type of cell. Previously, one might have conceived of the eye as an optical device with a sensitive film (the retina) from which neural images were transmitted to the brain. Now this scheme must be modified to include the idea that the retina is made up of many neural "films" overlaid on each other. Each neural "film" transmits a separate filtered version of the optical image formed by the eye. There h a s also been some excitement lately in relating psychophysical properties of visual sensitivity to neural mechanisms in the retina and in cerebral cortex, and this interest is connected to the concept of parallel retinocortical pathways. The focus of interest is the degree to which color vision and achromatic vision may be thought of as parallel and independent sensory analyses of the visual scene. There was a tradition for many years in theories of color vision to consider responses to black and white as being the result of a different neural mechanism from the one that can discriminate among wavelengths or wavelength distributions (see for example Hurvich and Jameson. 1957). This dualistic approach was reinforced by neurophysiological work by De Valois and Gouras and their colleagues in an earlier era of visual neurophysiology (reviewed in DeValois and DeValois. 1975: Gouras. 1984). The idea arose of a separate set of color blind retinal ganglion cells that were sensitive to a broad band of the visible spectrum and responsible for the visibility of black and white patterns. The numerous class of color opponent ganglion cells was supposed to be the sole vehicle for signals about color to travel from eye to brain. Then opinions changed and hypotheses were formulated about how all of vision, both

4

CHAPTER 1

achromatic and chromatic, could be derived from the spatiotemporal and chromatic response characteristics of the color opponent type of neuron (see for example, DeValois and DeValois. 1975; Ingling and Martinez Uriegas, 1983; Kelly, 1983; Derrington. Krauskopf. and Lennie, 1984; Rohaly and Buchsbaum, 1988, 1989). More recently, among neurophysiologists there has been some return to the dual, parallel channels point of view (Shapley and Perry, 1986; Livingstone and Hubel. 1987. 1988; Lee, Martin, and Valberg. 1988; Kaplan. Lee, and Shapley, 1990). This is still an unresolved controversy (cf. Lennie, Trevarthen, Wassle, and Van Essen. 1989).The neurophysiological. retinocortical channels probably do not correspond exactly with the achromatic and chromatic channels of psychophysics, and they probably interact more than some theories predict. Nevertheless, there is good reason to believe that there are two separate retinocortical pathways carrying different kinds of signals about the appearance of the outside world, one referring more to achromatic contrast, the other concentrating more on color contrast. In discussing the data, I will begin by considering the evidence for parallel retinocortical processing in the cat. Then, the focus will shift to the monkey visual pathway, its relation to the cat's, and functional roles of primate visual channels. One question for present research in this field is whether primates, including humans, have visual pathways organized, like the cat's. into X and Y and other similar retinocortical channels. This question has been studied most extensively in the retina of macaque monkeys. Macaque retinal ganglion cells fall naturally into different cell classes which form parallel anatomical and functional channels to the brain (Gouras. 1968; Schiller and Malpeli. 1978; DeMonasterio. 1978a). The crucial point is whether or not the macaque's ganglion cell classes are functionally similar to the cat's X and Y classes. Several lines of evidence indicate that primate M cells, the retinal ganglion cells that project to the magnocellular layers of the LGN, are functionally similar to X cells. The P cells, ganglion cells that form the input to parvocellular E N . seem to be functionally different from cat X cells and appear to be a primate specialization for color vision.

X and Y cells and the concept of parallel channels In the cat, two of the known functional classes of retinal ganglion cells, denoted the X and Y types (Enroth-Cugell and Robson, 1966) are believed to be of the greatest importance for pattern perception. This is because of their high sensitivity to spatial patterns (Derrington and Lennie. 1982; Enroth-Cugell and Robson. 1984; Shapley and Perry, 1986) and because of their direct connection to the lateral geniculate nucleus which relays visual information to primary visual cortex (Cleland, Dubin and Levick. 1971; Stone and Hoffmann. 1972: So and Shapley. 1979). The X cells are most sensitive to fine detail. sharply defined borders of objects, and small light or dark spots on a background. The Y cells respond most vigorously to coarse patterns. abrupt changes in diffuse illumination, and to large objects moving a t high velocities. The function of these neurons can be understood by considering how they act as filters of spatial and temporal stimuli from the environment. The differences in filtering

PARALLEL CORTICAL CHANNELS

5

characteristics imply that the different cell types are connected to basically different retinal neural pathways. This fact means that the retina is constructed to provide separate and independent views of the world to the brain. The cat's X and Y filters are not the only retinocortical channels. There are many other functional classes, but their visual functions are less well understood than those of X and Y cells.

Spatial and temporal filtering and the X/Y classification The initial discovery of the X and Y classes of cat retinal ganglion cells was made by Enroth-Cugell and Robson (1966. 1984).Their finding was a consequence of their investigation of these cells as spatial and temporal filters of visual signals. The activity of a ganglion cell, the modulation of its impulse rate up and down from a resting level, is strictly controlled by variations of the external visual stimulus. Therefore, each ganglion cell may be considered to be reacting to the visual environment, and passing through to the brain those stimuli to which the cell is tuned. Man-made devices of this general type are called filters. There is a general procedure for studying filters: it is known as systems analysis. In general, any neuron which can be described as having a receptive field can be conceived to be a spatial and temporal filter. Neurophysiologists who study the receptive fields of neurons are always performing a kind of systems analysis (Rodieck, 1973). One experimental test of whether a ganglion cell is acting as a linear or nonlinear filter is to combine steady and time-varying signals at the ganglion cell and to measure whether the average impulse rate depends on the presence of the time-varying signal, as Enroth-Cugell and Robson (1966)did initially. This is a special test of the property of superposition, a necessary condition for a linear system. Superposition means that if the system responds to stimulus A(t! with response a(t), and to stimulus B(t) with response b(t). then it must respond to stimulus A(t)+B(t) with response a(t)+b(t) rather than with some nonlinear combination like a+b+2ab. One particular test of superposition is to see the effect of a time varying stimulus on the response to a steady state stimulus. Enroth-Cugell and Robson used a drifting pattern to cause a time-varying signal in the retina. The pattern was presented on a background of steady light which provided a source of steady input to the ganglion cells. The retinal ganglion cells in which the average impulse rate did not vary when the time-varying signal was present, that is the cells which behaved like linear filters and obeyed superposition, they called X cells. They found many cells in which the average impulse rate increased when a time-varying stimulus was present, behavior which is characteristic of a particular kind of nonlinear filter, and these they called Y cells. To understand the visual function of the retina, it is not enough to know that some cells resemble linear filters and others nonlinear. One needs to know how ganglion cells combine signals from different photoreceptors. A way to answer this question is to examine the linearity of spatial summation of neural signals. A useful tool for this test is a sinusoidal grating pattern. This is a visual stimulus in which the variation in retinal illumination in the direction perpendicular to the

6

CHAPTER 1

bars of the grating is a sinusoidal function of position. The retinal illumination of a sinusoidal grating may be represented formally as

I(x) = 10 + 11 sin(2xkx + 01. where x is position on the retina. 10 is the mean illumination of the grating. 11 is the amplitude of the variation of illumination with position; it is also the maximum illumination minus the mean. The ratio I 1 /I0 is the contrast of the grating, and it indicates how bright or dark the bars of the grating are compared to the mean level of illumination. The fineness or coarseness of the pattern is determined by k, the spatial frequency in cycles/degree of visual angle. 0 is the spatial phase of the grating. The spatial phase is equivalent to the position of the grating on the retina. Since the grating is periodic, all possible positions of the grating are specified by a value of spatial phase between 0 and 271. If a ganglion cell is simply adding u p neural signals from different spatial locations in its receptive field, and there is no difference in the time course of the response from the different signal sources, then positions can be found at which introduction and withdrawal of the grating produce no response (Enroth-Cugell and Robson. 1966). These so-called "null positions" exist because the sine grating may be placed so that the zero crossing of the sine function lies over an axis of symmetry of the receptive field. Then introduction of the pattern produces a s much net positive signal from one side of the field as it produces net negative signal from the other side of the field, and the two signals of equal magnitude but opposite sign cancel when added. Null positions can be found for X cells, but there are no null positions for Y cells (Enroth-Cugell and Robson. 1966). This strengthens the hypothesis that X cells act like linear spatial filters, while Y cells behave like nonlinear spatial filters. Hochstein and Shapley (1976a.b) probed the functional differences between X and Y cells by studying how their sensitivities depended on the spatial phase of a sine grating not just at null positions but a t a whole range of positions of the grating with respect to the cells' receptive fields. In order to study the problem systematically, they introduced the use of the contrast reversing sine grating into visual neurophysiology. This stimulus can be written formally as I(x.t) = 10

+ 11 sin(2xkx + 0) *

M(ft)

where x is position on the retina, t is time, 10 is mean luminance, 11 is the modulation depth, 11/10 is the peak contrast of the contrast reversing grating, and M(ft) is the temporal modulation signal, usually which is modulated between the values of + 1 and - 1, usually a sine wave or a square wave with a temporal frequency f. The responses of X cells follow a sinusoidal function of spatial phase in response to a contrast reversing sine grating (Hochstein and Shapley, 1976a). This is illustrated in Figure 1. The reason for a sinusoidal dependence on spatial phase is a s follows. When spatial frequency and contrast are held fixed and only spatial phase is vaned, the local illumination at a point on the retina is proportional to the sine of the spatial phase. Therefore, because the receptor's response is proportional to the local illumination from the grating pattern and thus


7

is a locally linear transduction, each photoreceptor's response also is a sinusoidal function of spatial phase. The sum of such Jmctions from all the photoreceptors which converge on the ganglion cell will also be a sinusoidal function of spatial phase. This is a crucial mathematical point worth emphasizing. A summation of sine functions that have as a argument the sum of a fixed term and a variable term can be written as a product of the sine of the fixed term multiplied by another sinusoidal function. This is a consequence of the fact that sinusoidal functions may be viewed as complex exponential functions. This reasoning works for X cells and not Y cells because the process of signal transduction is locally linear, and summation is simple linear addition only in X cells. Null positions are the spatial phases at which the sinusoidal function of spatial phase equals zero.

Fundamen&-'

0 0

E l-

z

0 0

-200

!

-180

I

-120

-60

0

60

I I

I

120

180

SPATIAL PHASE

Figure 1. Spatial phase dependence of the response of a cat X ganglion cell. The amplitudes of the fundamental component, and the second harmonic component, in response to sinusoidal contrast reversal, are graphed as a function of spatial phase of the contrast reversing pattern. The spatial frequency of the grating was near optimal for this cell. It is clear that the fundamental amplitude data are well fit by a sinusoidal function of spatial phase, while the second harmonic data are in the noise. Redrawn from Hochstein and Shapley (1976a). The responses of cat Y cells to contrast reversing sine gratings have a complicated and peculiar dependence on spatial phase. To understand it, one can analyze the modulation of the ganglion cell's impulse rate in response to sinusoidal modulation of the contrast reversing stimulus. An X cell's impulse rate modulation is a t the temporal frequency of modulation of the contrast reversal (Hochstein

CHAPTER 1

8

and Shapley 1976a; Victor and Shapley, 1979a; Enroth-Cugell and Robson. 1984). A Y cell's response, however, contains two frequency components: one at the temporal modulation frequency of the stimulus, the fundamental frequency, and one a t twice the frequency of the stimulus, the second harmonic frequency. The fundamental, linear component of the Y cell's response varies sinusoidally with spatial phase like the X cell's, and thus appears to come from a single linear spatial summation mechanism. However, the nonlinear harmonic component is invariant in amplitude when the spatial phase of the grating pattern is varied. The linear component of the Y cell resolves patterns less well than X cells in its vicinity on the retina, usually two to four times less well (Hochstein and Shapley. 1976b; So and Shapley, 1979). However, the nonlinear component of the Y cell's response has a spatial frequency resolution two to four times higher than the linear component, comparable to that of the X cells in the neighborhood (Hochstein and Shapley. 1976b; So and Shapley. 1979). Furthermore, the peak of the nonlinear response is usually a t a spatial frequency a t which the linear component has vanished into the noise. If one graphs linear and nonlinear response components vs spatial frequency, the two curves intersect (as in Figure 2 redrawn from So and Shapley, 1981). This intersection is what has been called the "Y cell signature" (Spitzer and

al m t

0 Q

m

0

a l ! 0.01

I

0.10

I

1.oo

I

10.00

Spatial Frequency (c/deg)

Figure 2. Responses of a Y cell to gratings of different spatial frequency: the "Y cell signature." These are data from two experiments on one cat Y cell. The empty circles are the fundamental amplitudes to drifting sine gratings, as a function of spatial frequency. The filled diamonds are second harmonic amplitudes of responses to contrast reversal, also as a function of the spatial frequency of the grating pattern. The Y cell signature is the crossing of these two curves at high spatial frequency.


9

Hochstein. 1985). The spatial phase invariance and the high spatial frequency resolution of the nonlinear response imply that there must be many spatially dispersed mechanisms contributing to the nonlinear response in Y cells. Therefore, the hypothesis was advanced that there are many receptive field subunits, each of which pools photoreceptor signals over a small area. Then subunit signals are summed by the Y cell after a nonlinear transduction (Hochstein and Shapley. 1976b; Victor and Shapley, 1979b). Perhaps the most immediate question about the nonlinear subunits is, where is the nonlinearity located? Some have speculated that the photoreceptors might be intrinsically nonlinear, while others have guessed that the nonlinearity might be in the Y ganglion cell itself. Nonlinear systems analysis of Y cells has revealed that the Y subunit nonlinearity must be embedded in the network of the retina between photoreceptors and ganglion cells (Victor and Shapley, 1979b). The results on Y cells are consistent with the idea that the nonlinear transduction in the cat retina is located a t the bipolar-amacrine connection (Shapley and Perry, 1986). Such amacrine cells would have to serve as a major input to Y cells, but not X cells. It is important to note that the X/Y dichotomy a s presented here and previously (Hochstein and Shapley. 1976ab) is not based on a single property of linear or nonlinear filtering, but rather on evidence of linear spatial filtering measured across a wide range of spatial frequencies, in the case of the X cells, or of the Y cell "signature." as described above and shown in Figure 2. in the case of the Y cells. The procedure for determining whether a cell is X or Y thus requires the measurement of a cluster of spatial filtering properties (cf. Shapley and Perry, 1986). The different receptive field mechanisms of X and Y cells must contribute to their different roles in the cat's perception. Nonlinear subunits provide an excitatory signal to Y cells. That is why there is a burst of impulse firing in a Y cell at each contrast reversal of a grating pattern, and why the Y cell's firing rate is increased when a pattern drifts across the retina. The widely dispersed array of subunits excites a Y cell whenever a pattern moves or changes at any locus within a wide area of the retina. Y cells therefore send an increased signal to the brain whenever a pattern is present, but they indicate in an imprecise manner the location of the pattern. X cells are accurate about location. X cells in the center of the cat retina can give a maximally modulated response when a grating pattern is moved from a null position by as little as 0.1 degree of visual angle, which is a change in position of about 20 microns on the retina (Shapley and Victor, 1986). In the process of pattern perception, Y cells could signal "object present" while X cells could be used for pattern recognition by their very precise responses to fine detail and the relative locations of borders.

Other physiological properties of X and Y cells There are several other physiological and anatomical properties of cat X cells which differentiate them from cat Y cells, besides the spatial filtering characteristics stressed so far. One physiological trait is the more transient nature of a Y cell's response to a bright step of light on a dim background (Cleland et al.. 1971). However, this "sustained-transient" distinction seems to be much more apparent at

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CHAPTER 1

high contrast than low (Lennie. 1980; Shapley and Victor, 1981). Y cells respond better to large targets and to higher target velocities than X cells (Cleland et al.. 1971: Stone and Fukuda. 1974); this is due, at least qualitatively, to the larger receptive field centers of Y cells. The average conduction velocity of Y cell axons in the optic nerve and tract is considerably higher than that of X cell axons (Cleland et al.. 1971; Fukada. 1971; Stone and Hoffmann. 1972). There is a wide distribution of conduction velocities within each class, but the two distributions are distinct. Several studies agree that the average conduction velocity for X cell axons between optic nerve and chiasm is about 18 m/sec (Fukada, 1971; So and Shapley. 1979).The estimated average velocity for Y cell axons is somewhat more variable because of measurement difficulty: values between 30 and 70 m/sec have been reported (Fukada, 1971; So and Shapley. 1979). These velocity differences cause rather small latency differences a t the lateral geniculate nucleus between X and Y afferent input --- about 1 to 2 msec in comparison to a common visual latency for both X and Y cells of 30-40 msec (Shapley and Victor, 1981) in the light adapted state, and even longer in the dark adapted state.

"W-cells" The "W cells" (Cleland and Levick. 1974a.b; Stone, 1983). which are all the cat ganglion cells not classifiable a s X or Y, are probably composed of several classes of cells. Many of these cells have axons with a slow conduction velocity. Some however have axons with conduction velocities close to that of X cells. Evidence about spatial filtering in these ganglion cells is fragmentary, except for one class: the suppressed-by-contrast cells. These cells behave, crudely speaking, like off-center Y cells with inhibitory instead of excitatory subunits (Troy, Einstein, Schuurmans. Robson, and Enroth-Cugell, 1989). Suppressed-by-contrast cells are very sensitive to contrast. Many of the other 'W cells" are quite unresponsive to contrast, however. One particular class of rarely encountered ganglion cell in the cat is especially interesting for trans-species comparisons with macaque monkeys. This is the class of color-coded units discovered by Daw and Pearlman (1970). These cells react to visual stimuli in a manner similar to blue-on, yellow-off color-opponent cells in the monkey. In the cat the color-coded cells project to the C laminae of the LGN (Daw and Pearlman, 1970; Cleland and Levick. 1974b). and to superior colliculus. The corresponding cell type in the monkey projects only to the parvocellular layers of the LGN (Schiller and Malpeli, 1977, 1978).

Morphology of cat ganglion cells The morphology of the dendritic trees of cat ganglion cells has been found to correlate well with the physiological classifications (Boycott and Wassle. 1974: Leventhal. 1982). The large ganglion cells denoted alpha cells are certainly Y cells. Probably most of the ganglion cells with medium sized cell bodies and smaller dendritic trees, denoted beta cells, are X cells. The variation of dendritic field size with retinal eccentricity of the alpha and beta cells (Boycott and Wassle, 1974) is just like the variation in receptive field center size of Y and X


11

cells although the correspondence of the receptive field center to dendritic field is not exact. The gamma cell class of Boycott and Wassle was recognized initially to be heterogeneous and while it is clear that there is considerable diversity among this population, it is not known whether these cells form a continuum of morphological types or discrete subsets. They probably correspond to some of the ganglion cells usually referred to as "W cells." Another anatomical property which correlates with physiological classification is the central destination of the cell's axon. The following picture of connectivity is derived from electrophysiological studies and horseradish peroxidase (HRP) labelling. X cells connect primarily with the A or A1 layer of the lateral geniculate nucleus though a small fraction may connect to the C laminae of the LGN. Y cell axons typically have many collaterals and most if not all project to the A or Al. and C laminae of the LGN, as well as to the superior colliculus (Wassle and Illing, 1980; Illing and Wassle. 1981). There is also a massive Y cell projection to the medial interlaminar nucleus (MIN) (Stone, 1983).The central projections of "W cells" are very diverse, including the C laminae of the LGN. the superior colliculus, the accessory optic nuclei in the midbrain (Stone, 1983).None project to where the X cells project, the A and A1 laminae of the LGN.

P (Parvocellular) and M (Magnocellular) pathways Visual neurophysiological study of the macaque monkey is especially interesting to students of human vision because the visual performance of macaques is very similar to that of humans, and the anatomy of the retinocortical pathway is similar in macaque and human. The visual performance of cats and humans is similar on some psychophysical tasks but there are significant differences also. As shown in Figure 3. the contrast sensitivity function for sine gratings has a similar shape in human and cat but the human function is higher and shifted to the right, meaning that the human has a somewhat higher peak contrast sensitivity and higher spatial frequency resolution. The spatial frequency at the peak of the light-adapted cat contrast sensitivity function is about 0.6 c/deg while for the human it is about 3 c/deg: a five-fold smaller spatial scale in human than in cat. The monkey contrast sensitivity function peaks at a slightly lower spatial frequency than human, so that the ratio of space scales of monkey and cat may be closer to 1:4. Besides the spatial difference, the monkey like the human has the capability of color vision: fine wavelength discrimination and color categorization. While the cat may be trained to perform some crude wavelength discriminations, its color vision is much poorer than a primate's. These visual functional differences between cat and monkey should be kept in mind when comparing the visual properties of ganglion cells from the different species. The parallelism of functional pathways begins in the retina, so we begin our consideration of parallel processing in the monkey with retinal ganglion cells. There are clearly some similarities between X and Y ganglion cell classes in cat, and ganglion cell classes in monkey, but there is an ongoing debate about which monkey ganglion cells are most like cat X cells and which like Y cells.

12

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There are three clear subdivisions of monkey ganglion cells. One class of cells has been called "tonic" (Gouras. 1968; Schiller and Malpeli. 1978; DeMonasterio. 1978a). These cells have very small receptive fields and are usually selective for the wavelength of the visual stimulus. Such a cell will give sustained responses to light when the wavelength is a t the peak of the cell's spectral sensitivity curve. These cells respond phasically, however, to white light or other broad-band illumination (DeMonasterio, 1978a). They have a concentric center-surround organization, and the surround has a different action spectrum from that of the center, giving the cell color-opponent properties in response to stimuli that cover center and surround. Some "tonic" cells are blue-excitatory, yellow inhibitory cells like the color-opponent ganglion cells in the cat retina which project to the C laminae of the cat's LGN. In the monkey, the "tonic" cells send axons only to the four, dorsalmost parvocellular laminae of the LGN (Schiller and Malpeli. 1977, 1978; Kaplan and Shapley, 1986).

loo0l

Cat \

\

I! 0.1

1.o

10.0

1 100.0

SPATIAL FREQUENCY (c/deg)

Figure 3. Human and feline contrast sensitivity compared. These are photopic contrast sensitivities to sinusoidal grating patterns. Redrawn from Pasternak and Merigan (1981). Another major class of monkey ganglion cells is the group called "phasic" (Gouras, 1968). These ganglion cells have concentric center-surround receptive fields. They respond in a transient manner to a step of broad-band illumination, in this way resembling the "tonic" cells. The time course of their response to monochromatic or highly colored light has been little investigated, but may be transient or sustained. "Phasic" cells show little overt wavelength selectivity though recent work suggests that they may receive antagonistic signals from different cones (Shapley and Kaplan. 1989; Reid and Shapley, 1990) like their LGN targets, the Type IV cells of Wiesel and Hubel (1966; cf.


13

Derrington, Krauskopf, and Lennie, 1984). The axons of "phasic" ganglion cells project mainly to the Magnocellular layers of the LGN (Schiller and Malpeli, 1977; Kaplan and Shapley. 1986),though there is a small fraction of "phasic" cells which projects also to the superior colliculus. Because the tonic-phasic nomenclature puts too much emphasis on the initially discovered differences in the dynamics of response and not enough on the subsequently discovered differences in chromatic and spatial properties, Shapley and Perry (1986) referred to "phasic" cells as M cells because they project mainly to the Magnocellular layers of the LGN, and "tonic" cells as P cells because their only projection is to the Parvocellular layers in the LGN. A third catch-all class contains all those ganglion cells that are neither M nor P and has been referred to as the "rarely-encountered'' class (DeMonasterio. 1978b). The cells in this group resemble some of the cells classified a s "rarely-encountered'' in the cat (Cleland and Levick, 1974b). None have been found to be wavelength selective (DeMonasterio. 1978b). This group provides the bulk of the retinal input to the midbrain, particularly the superior colliculus. Presumably the "rarely-encountered'' class in the monkey actually Is composed of several distinct classes (or subclasses) of ganglion cell, as is thought to be the case for the "W-cells"in the cat (Stone, 1983).

Functional significance of parallel channels in primate The story about parallel channels for color and brightness acquired a new force in the attempts to explain the layering of the monkey's Lateral Geniculate Nucleus (LGN). For many years there was a mystery about the multi layered structure of the LGN of Old World primates, including humans (Walls. 1942). In the main body of the Old World primate's LGN there are six clearly segregated layers of cells. The four more dorsal layers are composed of small cells and are named the Parvocellular layers. The two more ventral layers, composed of larger neurons, are called Magnocellular layers. Recent work on functional connectivity and the visual function of single neurons has revealed that the different types of cell layers in the LGN receive afferent input from different types of retinal ganglion cells. The evidence on functional connectivity of retina to LGN comes from Leventhal. Rodieck and Dreher (1981) and Perry, Oehler. and Cowey (1984) who labeled axon terminals in specific LGN layers of the macaque monkey with Horseradish Peroxidase (HRP) and looked back in the retina to see which ganglion cells were labeled retrogradely. Direct electrophysiological evidence about retinogeniculate connectivity comes from Kaplan and Shapley ( 1986) who recorded excitatory synaptic potentials (from retinal ganglion cells) extracellularly in different LGN layers and who found that different types of retinal ganglion cell drove different LGN layers. For example, LGN cells that are excited by red light but inhibited by green light (so called red green color opponent neurons) are only found in the Parvocellular layers. These "Red-Green Opponent" LGN cells receive excitatory synaptic input from "Red-Green Opponent" ganglion cells: "Red-Green Opponent" ganglion cells only provide direct excitatory input to Parvocellular LGN neurons of the "RedGreen Opponent" type. The specificity of ganglion cell types exactly

14

CHAPTER 1

matches that of their LGN targets (Kaplan and Shapley. 1986: Shapley and Kaplan, 1989). Our direct evidence about this issue confirmed the earlier correlative results of DeValois. Abramov. and Jacobs (1966) and Wiesel and Hubel (1966) in the LGN, and Gouras (1968). DeMonasterio and Gouras (1975). and Schiller and Malpeli (1977) on retinal ganglion cells. As we will discuss in more detail, Parvocellular neurons are color opponent. This means that their responses, to stimuli which fill their entire receptive fields, change sign from excitatory to inhibitory contingent on the wavelength of the stimulating light (DeValois et al., 1966). The property of color opponency is conferred on them by their ganglion cell inputs, the P cells (Gouras. 1968: Malpeli and Schiller. 1977: Kaplan and Shapley. 1986). From the neuroanatomical work, one may infer that P cells are very numerous and densely packed, with small cell bodies and dendritic trees. Magnocellular neurons are generally thought to give the same sign of response to all wavelengths of light: this property is referred to as broad band spectral sensitivity (Gouras, 1968: Malpeli and Schiller. 1977). However, only some (about half) of the Magnocellular cells are truly broad band: the other Magnocellular neurons are color opponent by the above definition. These are the cells Wiesel and Hubel (1966) called Type lV. cells which have an excitatory receptive field center mechanism that is broad band, and a n antagonistic inhibitory surround mechanism that is selectively sensitive to long wavelength red light. The properties of the Magnocellular neurons, both broad band and Type IV. are determined almost completely by their retinal ganglion cell inputs (Kaplan and Shapley. 1986). The HRP experiments of Leventhal et al. (1981) and Perry et al. (1984) showed that Magnocellular cells receive input from a class of retinal ganglion cells, the M cells, that are somewhat larger in cell body size and dendritic extent than P cells.

Spatial summation in primate ganglion cells The first experiments on spatial summation in monkey ganglion cells produced results which were interpreted to mean that P cells were linear and therefore like X cells in the cat, while M cells were nonlinear and were like Y cells (DeMonasterio. 1978a). However, for various reasons I believe these interpretations were erroneous. The major problem with these experiments was that the stimulus contrast was very high, around 0.6. Even in cat X cells, one can elicit second harmonic responses when such contrasts are used (Hochstein and Shapley. 1976a). This is because the contrast gain of the neural networks that drive cat X cells, and monkey M cells, is very high. Such high gain networks must saturate and create response distortion at relatively low contrast. This brings up the main distinction between the monkey's M and P cells when examined as spatial and temporal filters: the gain of the M cells is much higher than for P cells. I will deal with this topic below. To return to experiments on the X/Y distinction in monkey, it is reasonable to test for linear signal summation a t low contrasts where the cell's response is proportional to contrast. When this is done, as many as 80% of the M cells behave like X cells in response to grating contrast reversal. Their response amplitudes vary sinusoidally with


15

spatial phase, and their response is predominantly at the fundamental temporal modulation frequency of the stimulus (Kaplan and Shapley, 1982, 1986).In this way, many M cells resemble cat X cells. This result is consistent with the earlier finding that about 80% of Magnocellular neurons, the targets of M cells in the LGN, also are X-like in this respect (Shapley. Kaplan and Soodak, 1981; Kaplan and Shapley, 1982; Blakemore and Vital Durand. 1986). A small fraction of M ganglion cells and their magnocellular target cells were found to behave like Y-cells; they had the same "Y-cell signature" a s Y cells in the cat (Kaplan and Shapley, 1982. 1986). When tested for linear signal summation, almost all P ganglion cells are X-like as are their LGN targets, the parvocellular neurons. However, P cells are very unlike cat X-cells in their contrast gain and other visual characteristics.

Conduction velocity of M and P axons The conduction velocity of the axons of monkey ganglion cells, between optic chiasm and optic tract, h a s been measured with the following results. The average conduction velocity of M cells is 21 m/sec. The conduction velocity of P cells on the average is 13 m/sec. The distributions of velocity are broad and there is considerable overlap of the velocity distributions (Schiller and Malpeli. 1977). Comparing average velocities with the cat, one finds that no monkey ganglion cells have been found that have the very fast conduction speed of Y cells (often more than 50 m/sec). The M cell conduction velocity is close to that of cat X cells (18 m/sec). The P cell conduction velocity is significantly lower than that of cat X cells.

Trans-species comparisons There are two main proposals for grouping monkey ganglion cells in a correspondence with cat ganglion cells. The original idea was that P cells were functionally similar to X cells and M cells were similar to Y cells. This idea originated from experimental results on Parvocellular and Magnocellular LGN neurons (Dreher, Fukada and Rodieck, 1976) and was then applied to their retinal inputs (Schiller and Malpeli. 1978; DeMonasterio. 1978a). This hypothesis was based on the following considerations: (1) the P cells and the X cells were the ganglion cells with the smallest receptive fields. and dendritic trees, at each retinal locus in each retina; (2) the M cells and the Y cells had the axons which were the fastest for their respective species: (3) the response of P cells was more sustained that of M cells, just as the response of X cells was more sustained than that of Y cells. In each case, the argument is based on relative properties between the two cell classes. A somewhat different proposal has been based on visual and spatial filtering characteristics (Shapley. Kaplan and Soodak. 1981; Kaplan and Shapley, 1982; Shapley and Perry, 1986). The proposal is that M cells and their Magnocellular targets actually are composed of two subgroups which correspond to X and Y cells. The more numerous MX variety projects to the Magno-X cells, while the less numerous MY type cell projects to the Magno-Y cells. Part of this proposal is that the

16

CHAFTER 1

monkey P cell group has no exact functional equivalent in the cat, but is a hyperplasic enlargement of the color-coded class of cat ganglion cells that project to the C-laminae. This proposal is based on the following considerations: (1) a large majority of Magnocellular neurons and their M cell inputs are X-like in terms of spatial summation and spatial filtering; (2)a small fraction of Magnocellular neurons and M cells have "the Y-cell signature"; (3)all monkey ganglion cells have transient responses to white light and most have more or less sustained (4) the contrast gain of responses to monochromatic light: Magnocellular neurons and M cells is about ten times greater than that of Parvocellular neurons and P cells, and the contrast gain of M cells is comparable to that of X and Y cells in the cat (see below); (5)the P cells a n d their L G N targets, t h e Parvocellular n e u r o n s , a r e wavelength-selective while cat X cells are not; (6) most M cells make synaptic contacts only with Magnocellular neurons in the LGN, while almost all cat Y cells bifurcate and contact geniculate and superior colliculus neurons. The arguments for the second proposed trans-species comparison rest mainly on absolute comparisons of the visual capabilities of neurons from monkey and cat and detailed comparisons of neural connectivity. There are some more recent findings that support this second version of trans-species comparison. For example, the degree of rod input to near peripheral M cells seems much stronger than to nearby P cells (Purpura, Kaplan and Shapley, 1988); the cell type that most strongly resembles cat X cells in this respect is the MX type. Sustained inhibition or excitation from the receptive field surround is strong in P cells but weak or nonexistent in M ganglion cells, a s in cat X cells (Shapley and Kaplan. 1990; Enroth-Cugell, Lennie. and Shapley. 1975). Whether or not one can make assignments of functional equivalence between monkey and cat, we believe the weight of the evidence is against one proposed functional equivalence: monkey P cells and cat X cells. These two classes differ in the following important ways: the receptive field size distribution with eccentricity; the dendritic tree diameter's dependence on eccentricity, contrast gain, wavelength selectivity, and conduction velocity; and degree of rod input. There is no visually significant way in which these two cell classes are similar.

Contrast gain in M and P pathways Besides their spectral sensitivities, the other property that distinguishes Parvocellular from Magnocellular neurons is contrast gain. To make this clear I provide the technical definition of contrast, then proceed to define contrast gain. Contrast is used technically in vision research to mean the variation in the amount of light in a stimulus, normalized by the mean amount of light. For example, in a periodic grating pattern in which the peak amount of light is P and the least amount of light is T (for trough), then contrast is defined as

C = (P - T)/(P + T).


17

This definition goes back to Rayleigh (1889), and Michelson (1927). and is equivalent to our earlier definition for sine grating patterns. Contrast is the stimulus variable that the retina responds to under photopic conditions (Robson, 1975; and many others reviewed in Shapley and Enroth-Cugell. 1984). I t is thought that such response dependence on contrast evolved because the contrasts of reflecting objects are invariant with changes in illumination occasioned by shadows, weather, or the passage of the sun. The retina thus sends signals to the brain that are more closely linked to surface properties of reflecting objects than they are to variations in illumination. Contrast gain is defined as the change in response of the neuron per unit change in contrast, in the limit as the contrast goes to zero. Contrast gain is thus the differential responsiveness of the neuron to contrast around the operating point of the mean illumination. The different contrast gains of Parvocellular and Magnocellular LGN neurons are illustrated in Figure 4 (Shapley and Kaplan. unpublished; compare with retinal ganglion cells in Kaplan and Shapley. 1986). As can be seen from the figure, the response as a function of contrast grows much more steeply for the Magnocellular neuron than for the Parvocellular, especially a t low contrast near the behavioral detection threshold. This is a general finding. The ratio of the average contrast gains of the population of Magnocellular neurons to the population average of Parvocellular neurons is approximately eight under midphotopic

n

0

8o

T

e al

E

;3.

w u)

z

0

Q v)

W

U

--II

0.00

0.20

0.40

0.60

0.80

1.oo

CONTRAST

Figure 4. Responses of macaque LGN neurons and a cat X ganglion cell as a function of contrast. One on-center Magnocellular neuron and one off-center (+M-L) Parvocellular neuron are shown, together with the data from an on center cat X cell. Mean luminance was 60cd/m2. Responses were calculated a s the best fitting Fourier component a t 4 Hz. the temporal frequency of the drift. Spatial frequency was chosen to be optimal for each neuron.

18

CHAPTER 1

conditions (Kaplan and Shapley, 1982; Hicks, Lee, and Vidyasagar. 1983; Derrington and Lennie. 1984). Subsequently, Dr. Ehud Kaplan and I showed that this contrast gain difference in LGN neurons is already set up in the retina. The retinal ganglion cells that innervated Magnocellular neurons had about eight times the contrast gain of ganglion cells that provided the excitatory drive for Parvocellular LGN neurons (Kaplan and Shapley. 1986). We still do not know the mechanistic reason for the substantial differences in contrast gain for cells in the two pathways. There are various possible factors that may contribute. The receptive field centers of P cells are smaller than those of M cells, and if the local contrast gains from points in each field are equal, then the larger summing area of the M cells would lead to a higher contrast gain for an optimal sine grating pattern (see Enroth-Cugell and Robson, 1966). Though this factor must contribute something, it does not seem to account for all the difference between M and P. Then there is the possibility that in P cells, but not M cells, there are antagonistic interactions between cone types within the receptive field center. Though this may be the case in many neurons, it is possible to find some P cells in which the center is driven predominantly by one cone type only. Both these hypotheses are considered in the review by Kaplan. Lee, and Shapley (1990). There is still a puzzle here because neither mechanism mentioned above is sufficient to account for all the difference between M and P contrast gains. Whatever the complete explanation is. it must involve retinal mechanisms since the M and P differences in contrast gain begin in the retina. Next, we must consider in more detail the responses neurons in the P and M pathways to chromatic stimuli. This discussion requires a prior analysis of the three cone photoreceptors in the Old World primate retina. and the effect of the properties of the cones on chromatic responses.

Three photoreceptors and spectral sensitivity There are three cone photoreceptor types in human and macaque retinas. The spectral sensitivities of these photoreceptors have been determined for macaque retina by Baylor et al. (1987) and for human retina by Schnapf et al. (1987). using suction electrodes to measure cone photocurrent directly. These direct measurements of photoreceptor spectral sensitivities are in generally good agreement with microspectrophotometric measurements of cone absorption spectra (Bowmaker and Dartnall. 1980: Bowmaker. Dartnall, and Mollon, 1980). The photocurrent measurements agree even more closely with estimates of cone spectral sensitivity based on human psychophysics (Smith and Pokorny, 1975). The Smith and Pokorny fundamentals (estimated cone spectral sensitivities a s measured at the retina after the light has been pre filtered by the lens) are three smooth functions of wavelength peaking at 440 nm (S cones). 530 nm (M cones) and 560 nm (L cones). Please note that the historically older nomenclature about cones denotes the Middle wavelength cones as M cones b u t this is unrelated to the designation of Magnocellular projecting ganglion cells as M cells.


19

Human sensitivity to light across the visible spectrum under photopic, daylight conditions is called the photopic luminosity function. denoted Vx. It might be thought that the easiest way to determine Va would be to measure psychophysically the sensitivity for increments of light of different wavelength on a photopic background. However, the photopic luminosity function is not measured in this way, mainly because such measurements are variable between and within observers because of the complexity of the visual system (H. Sperling and Harwerth. 1971; King-Smith and Carden. 1976). Rather. the procedure known a s heterochromatic flicker photometry (HFP) h a s been employed. Monochromatic light of a given wavelength is flickered against a white light at a frequency of 20 Hz or above, and the radiance of the monochromatic light is adjusted until the perception of flicker disappears or is minimized (Coblentz and Emerson, 1917). This technique exploits the fact that neural mechanisms that can respond to the color of the monochromatic light are not able to follow fast flicker. The photopic luminosity function has been measured more recently using contour distinctness (Wagner and Boynton, 1972) and minimal motion (Cavanagh. MacLeod, and Anstis. 1987) as response criteria. These measurements agree remarkably well with the luminosity function determined by flicker in the same subjects. The agreement is remarkable because these are such different spatiotemporal stimuli. The luminance of a light source is its effectiveness in stimulating the visual neural mechanism that has as its spectral sensitivity the photopic luminosity function. Thus, the luminance of any light may be computed by multiplying its spectral radiance distribution, wavelength M and L cones and the Photopic Luminosity Function

" "T

Wavelength (nm) Figure 5 . Spectral sensitivity functions of the M and L cones, and the photopic luminosity function (labelled LUM). Data are redrawn from Smith and Pokorny (1975).

20

CHAPTER 1

by wavelength, by the photopic luminosity function and summing the products from all the wavelengths. The spectral sensitivities of the M (530 nm) and L (560 nm) cones and the photopic luminosity function are graphed in Figure 5. The purpose of this graph is to show the degree of overlap of the two longer wavelength cones with the photopic luminosity function, and also to demonstrate the closeness of the luminosity function to the L cone sensitivity especially at longer wavelengths. This becomes significant in the consideration of cone contrasts in chromatic, equiluminant stimuli. I will emphasize later the importance of variation in the photopic luminosity function, VI,. The photopic luminosity curve graphed in Figure 5 is an average of curves from many subjects. There is substantial variation in the normal population in the peak wavelength and particularly in the long wavelength limb of the VI, curve (Coblentz and Emerson, 1917: Crone, 1959). For example, some people who have normal color vision can have half a log unit less relative sensitivity to 620 nm light than the average observer (Coblentz and Emerson, 1917). There is variance also in the reported spectral sensitivity of cones (Baylor et al.. 1987) and in the pigments’ spectral absorption (Bowmaker et al., 1980).

Color exchange and equiluminance Color exchange, or silent substitution (Estevez and Spekreijse (1974. 1982) is a technique for identifying contributions from photoreceptors or other spectral response mechanisms. For any spectral sensitivity function, and two light sources with different spectral distributions within the band of the sensitivity function, one can perform a color exchange experiment that will provide a characteristic color balance for that particular spectral sensitivity. For example, if one chooses two monochromatic lights with wavelengths such that they are equally effective at stimulating the L (560 nm) cone, then temporal alternation between these two lights a t equal quantum flux should cause no variation in the response of the L cone. The same argument works for the photopic luminosity function which presumably is the spectral sensitivity of a neural mechanism that receives additive inputs from M and L cones. Two lights that, when exchanged, produce no response from the luminance mechanism are called equiluminant. The results of a simulated color exchange experiment on cones and a broad band cell with a VI, spectral sensitivity are illustrated in Figure 6. The calculations are based on the spectral sensitivities of the M and L cones and the photopic luminosity function as graphed in Figure 5. The spectral distributions of the light sources were those of the red and green phosphors on standard color television sets, designated P22 phosphors. The red phosphor is narrow band centered around 630 nm. The green phosphor is more broad band centered around 530 nm. Such colored lights have been used in many experiments on color vision (Derrington et al.. 1984; DeValois and Switkes. 1983: Kaplan. Shapley. and Purpura. 1988; Livingstone and Hubel. 1987: Tootell. Silverman, Hamilton, DeValois, and Switkes, 1988). The experiment that is simulated is color exchange between the red (denoted capital R) and green (denoted capital G)phosphors. I have scaled the x axis so that when the G/R ratio is 1.0, the green phosphor


21

has the same luminance as the red phosphor. When the luminance of the green phosphor is approximately 0.4 that of the red (G/R ratio 0.41, the response of the M (530 nm) cones is nulled. When the G/R ratio is about 1.2. the L (560 nm) cone response is nulled. Notice that the shape of each of these spectral mechanisms is similar: near the null the response vs. G/R ratio forms a V. This is based on the assumption of small signal linearity. a good assumption in the case of macaque P and M pathways (Kaplan and Shapley. 1982; Derrington et al., 1984: Blakemore and Vital-Durand, 1986).

a, fn C

0 L1

fn

a, K

G/R Ratio Figure 6. Color exchange response functions for M and L cones and luminance. The predicted response of the cones to different G/R ratios was calculated from the cross product of the G and R phosphors with the spectral sensitivities of the M and L cones from Figure 5. Also plotted in this graph are response amplitudes of a Magnocellular neuron from a macaque monkey, stimulated by 1 c/deg drifting heterochromatic gratings (unpublished observations of Shapley and E. Kaplan). It is clear that this representative Magnocellular neuron's responses fit the responses predicted by the human photopic luminosity function. One can prove that a spectral mechanism that sums the responses of M and L cones will have a null in a color exchange experiment at a G/R ratio between the nulls of the two cones. If the spectral sensitivity of the summing mechanism is K*L+M. where K is a number between zero and infinity, then when K approaches zero, the color exchange null approaches the M cone null from above. When K goes to infinity, the color exchange null approaches the L cone null, from below. The null of the luminosity curve between the cone nulls in Figure 6 is a case in point. For that curve, K is approximately 2. One

22

CHAPTER 1

must qualify the assertion to include the condition that the photoreceptor signals have the same time course, and that in the process of summation their time courses are unaffected. The existence of sharp V's in color exchange experiments on M ganglion cells and Magnocellular cells is reasonably good evidence that M and L cones have similar time courses under the conditions of those experiments (Lee, Martin, and Valberg. 1988; Kaplan et al. 1988; Shapley and Kaplan, 1989).

In the work that we will discuss next, investigators often have applied a neurophysiological result on monkeys to human perception, and vice versa. This requires an assumption that the visual pathways in humans and monkeys function similarly. Support for this assumption comes mainly from the work of R.L. DeValois and his colleagues (DeValois, Morgan, Polson. and Hull, 1974; DeValois, Morgan, and Snodderly, 1974). They showed that for Old World monkeys, such as rhesus or cynomolgus monkeys which are the usual species studied in neurophysiological experiments on vision, detailed behavioral measurements of the spectral sensitivity function, wavelength discrimination function, and contrast sensitivity function resemble human performance. It is well known that there is a similarity in the neuroanatomy of the retinocortical pathway between humans and Old World monkeys. More recent evidence on similarities in detailed structure and layout of the retina in human and macaque monkeys strengthens the argument for functional similarity (Rodieck. 1988).

Responses of M and P neurons to equiluminant stimuli One particular color exchange experiment has become crucial, namely measuring responses of P and M neurons to equiluminant color exchange. In their large and influential paper on perceptual effects of parallel processing in the visual cortex, Livingstone and Hubel (1987) assumed that because Magnocellular cells were broad band, their responses would be nulled at equiluminance. As the above discussion was aimed to show, this is a non sequitur. To repeat, there could be a whole family of broad band neurons in the visual pathway that summed signals from L and M cones with different weighting factors Ki, such that spectral sensitivity of the i-th mechanism was Ki*L+M. Each mechanism would have a null a t a different point on the G/R axis. The striking thing about M cells and Magnocellular neurons is that, for stimuli that produce responses from the receptive field center mechanism, the position of the null on the color exchange axis is close to that predicted from the human photopic luminosity function, VI (Lee et al., 1988; Shapley and Kaplan. 1989; Kaplan et al.. 1990). There is no more variability in the position of the color exchange null in the neurophysiological data than there is in psychophysical experiments on the luminosity function in humans (Crone. 1959) or in behavioral experiments on macaques (DeValois et al.. 1974a). There are other experiments that indicate that, under stimulus conditions where the center of the receptive field is not the only response mechanism contributing to t h e response. M a n d Magnocellular neurons do not have a color exchange null a t equiluminance. Lee et al. (1988) reported that large disks that stimulate center and surround have nulls away from equiluminance.


23

Shapley and Kaplan (1989) used heterochromatic sine gratings to study chromatic properties of receptive field mechanisms. Heterochromatic sine gratings are formed by producing a sine grating on, say, the red phosphor of a color monitor, and producing an identical sine grating on the green phosphor except for a n exact 180 degree phase shift. Thus where the red phosphor has a bright red bar the green phosphor has a dark green bar, and vice versa. The sum of these two grating patterns in antiphase yields as a spatial pattern a red green, ergo heterochromatic, grating. Shapley and Kaplan (1989) reported that heterochromatic sine gratings of low spatial frequency may produce no color null in Magnocellular neurons. Derrington et al. (1984), using the technique of modulation in color space, found that many Magnocellular units exhibited properties expected of color opponent cells. Undoubtedly, all these results are related to the earlier work of Wiesel and Hubel (1966) who found that many Magnocellular neurons had a receptive field surround that was more red sensitive than the receptive field center. Such neurons could behave as color opponent cells to stimuli which covered both center and surround if the spectral sensitivities of center and surround were different enough. Similar M ganglion cells were reported by DeMonasterio and Schein (1980).Thus, in psychophysical experiments, if the stimulus is designed to tap the receptive field center of cells in the M pathway, it will elicit a spectral sensitivity function like VL. Such a stimulus will be nulled in a color exchange experiment a t equiluminance. However, should other stimuli be detected by the M-Magnocellular pathway but not isolate the central receptive field mechanism, one might discover a color opponent mechanism driven by M cells. There is another result that indicates a failure of nulling at equiluminance in Magnocellular neurons. This is the second harmonic distortion discovered by Schiller and Colby (1983). In color exchange experiments with large area stimuli, these investigators often found strong frequency doubled responses. Such results were not reported by Derrington et al. (1984) who found frequency doubling rarely (20% of the time) in their experiments. Shapley and Kaplan (1989) reported that frequency doubling was dependent on spatial frequency of the pattern used for color exchange. Center isolating stimuli elicited no frequency doubling but it could be observed when spatial frequency was s o low, less than 0.5 c/deg. that the receptive field surround could contribute to the M cell's response. This also could contribute to failure to achieve sharp psychophysical equiluminance with stimuli of large area or low spatial frequency, even with stimuli that isolated a perceptual mechanism driven only by the M pathway.

Chromatic opponency in P and M cells The basis for wavelength selectivity in the visual pathway is antagonistic (excitatory vs. inhibitory) interactions between signals from different cone types. The simplest type of antagonism is subtraction. There is good evidence for subtractive interactions between M and L cones on P ganglion cells (DeMonasterio and Gouras, 1975; Zrenner and Gouras. 1983) and Parvocellular neurons (DeValois et al.. 1966; Wiesel and Hubel, 1966; Derrington et al.. 1984). The classical evidence is a change in sign of response with wavelength (DeValois et al.. 1966). For

24

CHAPTER 1

example, many P cells that receive opponent inputs from M and L cones have a sign change at a wavelength near 570 nm. The "blue excitatory" cells referred to earlier often have a change from excitation at short wavelengths to inhibition at long wavelengths at around 490 nm. These cells receive excitatory input from S cones and inhibitory input from some combination of M and L cones. The precise mapping of cone types t o receptive field mechanisms is a problem not yet solved, though we have some interesting preliminary results on this problem. Wiesel and Hubel (1966) postulated that color opponent cells received excitatory (or inhibitory) input from one cone type in the receptive field center and antagonistic inputs from a complementary cone type in the receptive field surround. However, the detailed quantitative evidence that would be needed to support or to reject this hypothesis was not available then. One problem is spatially isolating center from surround because receptive fields in the monkey's retina, and presumably in human too, are quite small. Though Wiesel and Hubel's (1966) proposal may be true, there are a number of other possibilities. One alternative hypothesis is that there is mixed receptor input to the receptive field surround, and only or predominantly one cone input to the center of the receptive field (see Paulus and Kroger-Paulus, 1983: Kaplan et al., 1990). However, my own recent research with R. Clay Reid indicates that the chromatic opponent inputs to P cells are specifically wired to individual cone types, for example L+M- and the receptive field surround is just the receptive field mechanism that receives weaker and more spatially diffuse input from one of the cone inputs (Reid and Shapley. 1990).

Comparison of achromatic and chromatic contrast sensitivity The spatial characteristics of vision have been studied for many years by measuring the contrast sensitivity function for sinusoidal gratings (Campbell and Robson. 1968: DeValois, Morgan and Snodderly. 1974b. among many others). These have traditionally been achromatic measurements and the contrast sensitivity has been taken to be the reciprocal of the luminance contrast at psychophysical threshold. More recently, luminance contrast sensitivity has been compared with the spatial frequency dependence of chromatic contrast sensitivity as measured with equiluminant heterochromatic grating patterns (van der Horst, de Weert, and Bouman, 1967: Kelly, 1983: Mullen, 1985). The luminance contrast sensitivity function is band pass while the chromatic contrast sensitivity is low pass and cuts off at a fairly low spatial frequency compared with luminance. In both P and M pathways, response to equiluminant heterochromatic gratings is best a t the lowest spatial frequencies. P cells and Parvocellular neurons respond much better to equiluminant heterochromatic gratings of low spatial frequency because, under those conditions, the antagonistic center and surround become synergistic (DeValois and DeValois. 1975). However, Type IV M cells and their Magnocellular targets in LGN also become more sensitive a t low spatial frequencies of heterochromatic gratings because of their color opponency.


25

The responses to middle and high spatial frequencies are better when luminance than when equiluminant gratings are used a s stimuli. Thus, if the data were plotted as response vs. G/R ratio, one should expect a dip in response near equiluminance at middle to high spatial frequency. Such results were reported by Mullen (1985). It would be important to measure the equiluminant G/R ratio on the same subject with heterochromatic flicker photometry or minimal motion or minimally distinct border to see whether the same or different spectral mechanisms are a t work in detecting the heterochromatic gratings. K.K. DeValois and Switkes (1983) and Switkes et al. (1988) have demonstrated that heterochromatic grating patterns are detected by spatial frequency channels like those involved in achromatic grating detection (Campbell and Robson, 1968; Graham, 1980).Thus, elevation of threshold for detecting an equiluminant grating is produced by pre exposure to an equiluminant grating of the same spatial frequency, and less elevation of threshold is produced by more distant spatial frequencies. Moreover, color gratings mask and adapt color and luminance gratings but, as we will discuss below, luminance gratings may facilitate detection of color gratings. The work on spatial frequency channels in color throws a new light on receptive field models that have sought to explain chromatic and luminance spatial contrast sensitivity functions in terms of single channel receptive field models (Ingling and Martinez-Uriegas. 1983; Kelly, 1983). The chromatic contrast sensitivity function is an envelope of chromatic spatial frequency channels, just a s the luminance contrast sensitivity function is thought to be an envelope of the well studied achromatic spatial frequency channels. Single channel models, though they may be of heuristic value in summarizing a body of data, must be only a first approximation to a true mechanistic model of these multi channel systems.

Possible neural substrates for contrast sensitivity The M and P pathways must be the conduits for signals about detection of contrast. The high gain M system is well suited to handle detection of grating patterns with low to medium spatial frequencies (Shapley and Perry, 1986; Kaplan et al.. 1990). The numerous P cells may be required to represent veridically the spatial waveform for grating patterns near the acuity limit (Lennie et al.. 1989). The neural basis for photopic contrast sensitivity in the primate is still a controversial topic. Derrington and Lennie (1984) claimed that the contrast insensitive Parvocellular neurons might still support contrast sensitivity performance through the mechanism of "probability summation" among the numerous Parvocellular neurons. However, this argument presupposes that there is response independence among Parvocellular neurons, a prerequisite for probability summation. Furthermore, if probability summation is admitted as a mechanism, then it is not clear why Magnocellular neurons do not also contribute to detection by this mechanism. Probability summation can be viewed as fractional power law summation. Threshold will be lowered by some fractional power of the number of summing elements N. A reasonable estimate might be N-114.If one uses the figure of ten times as many Parvocellular neurons as Magnocellular, one can calculate that the relative increase of Parvocellular neurons' contrast sensitivity compared

CHAPTER 1

26

to Magnocellular contrast sensitivity caused by probability summation would be about 1.8. Since Magnocellular neurons are about ten times more sensitive than Parvocellular neurons, neuron by neuron, one would have to conclude that even with probability summation the Magnocellular neurons ought to be the neural system signalling contrast detection. Recent experiments on lesions of the P and M pathways indicate a larger role for the P pathway in photopic achromatic contrast detection. Merigan and Eskin (1986)found that contrast sensitivity was reduced in monkeys poisoned chronically with acrylamide. This toxic substance appeared to cause anatomical damage preferentially in the P pathway in LGN and retina, though its physiological effects on the P and M pathways have not been studied. Schiller. Logothetis and Charles (1990) placed ibotenic acid lesions in the Magnocellular and Parvocellular layers of macaque monkeys and then studied the lesioned animals' visual performance on several tasks. One of these was contrast detection of a checkerboard pattern. Contrast sensitivity in this task was reduced by Parvocellular but not Magnocellular lesions. This finding is unexpected based on our neurophysiological results and remains something of a mystery. One curious feature of the Schiller group's measurements is the low contrast sensitivity for the checkerboard pattern in control monkeys - the highest sensitivity was 0.1, about one log unit below the best contrast sensitivity for sine gratings. Furthermore, the control monkeys had highest contrast sensitivity at the lowest fundamental spatial frequency of the checkerboard, another unexpected finding. There needs to be more research on the relation of neurophysiology with detection thresholds in this system. Recent neurophysiological results by Purpura. Kaplan and Shapley (1988) indicate that the P cells become visually unresponsive to grating patterns when the mean luminance drops below 0.1 cd/m2 at the rod/cone break. M cells become less sensitive progressively as mean luminance is reduced, but they are so much more sensitive in the light that they remain responsive into the scotopic range. We suggested that these results might mean that spatial vision under scotopic conditions would be dependent on M cell signals. Wiesel and Hubel (1966) and Gielen et al. (1982) reported rod driven responses in Parvocellular LGN cells under scotopic adapting conditions, an apparent contradiction to the results of Purpura et al. (1988). However, both these sets of authors reported that a rod driven Parvocellular neurons was rarely encountered, and moreover, they did not test for spatial vision under scotopic conditions. In the Purpura et al. study, we did observe rod driven responses in P cells but only with very low spatial frequency gratings or diffuse light as spatial stimuli.

Cortical target areas for P and M signals

v1

I

There is indirect evidence that Magnocellular and Parvocellular signals are kept somewhat segregated within striate cortex, V1, Hawken and Parker (1984) and Hawken, Parker and Lund (1988) have shown that cortical neurons with high contrast gain, like Magnocellular neurons, can be found in layer lVc alpha of V1. Color opponent neurons


27

are located in layer IVc beta, and these are presumably the targets of the LGN afferents from Parvocellular cells. There are subdivisions within the upper layers of the cortex, layers I1 and 111, that may be preferentially influenced by Magnocellular signals. All of layers I1 and I11 receive inputs from layer IVc beta, so. presumably receive Parvocellular signals filtered through the cortical network. However, from experiments on labelling of active cells with 2 deoxyglucose, Tootell. Hamilton and Switkes (1988)found that there was weak but significant labelling of the cytochrome oxidase blobs in layers I1 and 111 of V1 cortex when stimuli of low achromatic contrast were used. The cytochrome oxidase blobs were shown to contain cortical neurons broadly tuned for orientation by Livingstone and Hubel (1984).This finding may mean that Magnocellular and Parvocellular signals converge onto blob neurons. The cytochrome oxidase blobs have been found to form a network throughout macaque V1 (Horton. 1984;Livingstone and Hubel. 1984)and it has been hypothesized that they form a separate system for the analysis of color (Livingstone and Hubel. 1984, 1987).Many of the cells in the blobs are color selective. A test of this idea is whether cells in the inter blob regions of layers 11, I11 of V1 are not color selective or are substantially less color selective than blob neurons. There are recent single unit data on this question from Lennie, Krauskopf and Sclar (1989)and the results indicate that color selectivity in blob cells is not that different from inter blob cells. Furthermore, Tootell. Silverman et al. (1988)used equiluminant color gratings to label layer 11,111 cells with 2 deoxyglucose and found that labelled cells were found throughout the upper layers, though there was stronger labelling of the blobs with diffuse color patterns. These data are essentially consistent with the findings of Lennie et al. (1989).

v2. Using cytochrome oxidase as a marker, Tootell, Silverman. DeValois and Jacobs (1983)demonstrated stripe like structures in secondary visual cortex V2 in macaque monkeys. Subsequently, Shipp and Zeki (1985)and DeYoe and Van Essen (1985)have shown that distinct anatomical regions within primary visual cortex make characteristic connections with regions in macaque V2. Neurons in the blobs of V1 are connected to one of the sets of darker stripes in V2; neurons in the interblob regions of layers 11,111 are connected to stripe like regions of low cytochrome oxidase staining in V2. Livingstone and Hubel (1987).from their measurements in squirrel monkeys, also propose that layer IVb, which receives Magnocellular signals from layer IVc alpha, projects to the alternating dark cytochrome stripes in macaque V2. The functional consequences of this complex sequence of connection is that parallel functional pathways proceed from V1 to V2. Livingstone and Hubel (1987.1988) have made a very detailed psychophysical linking proposition based on the anatomy and receptive field properties of neurons in V1 and V2. They propose that blob cells, connecting to one set of V2 stripes, constitute a system for color vision. The putative Magnocellular pathway from layer IVc alpha through layer MI to the other set of dark V2 stripes is supposed to be important for responding to objects in depth. The interblob neurons in V1, connected

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CHAPTER 1

to pale stripes in V2. are supposed to be important for form vision, mainly because neurons located in pale stripes in V2 were found to be end stopped, i.e. more strongly responsive to corners and the ends of lines than to long contours (Hubel and Livingstone, 1987). While it is thought provoking, there are problems with the specifics of the Livingstone and Hubel story. One problem is that depth perception seems to depend on both chromatic and achromatic information: this is even indicated in the paper by Livingstone and Hubel (1987). Another problem is that "form" is a poorly defined concept. Certainly the shape of an object may be defined by motion in random dot cinematograms (Braddick, 1974). Even three dimensional shape may be perceived based on dot trajectories in cinematograms (Sperling, Dosher and Landy. 1988). So the assignment of motion perception to one pathway and shape perception to another pathway seems greatly oversimplified. A third problem is, even at the level of detailed neuroanatomy, V1 compartments seem to receive convergent input from Parvocellular and Magnocellular signals. For example, Tootell. Hamilton and Switkes (1988) found that V1 blobs were active not only in response to chromatic equiluminant patterns, but also to patterns of low spatial frequency and low contrast - indicative of input from Magnocellular signals possibly relayed via layer IVc alpha. It is likely from the neuroanatomy that many interblob neurons also receive mixed Magnocellular and Parvocellular inputs. So the rigid segregation of function and simplicity of connectivity between V1 and V2 postulated by Livingstone and Hubel is not likely given the richness of cortical connectivity within V1.

Motion Among the psychophysical proposals of Livingstone and Hubel (1987). the most robust idea is that Magnocellular signals form the basic excitatory drive of the motion pathway. Motion perception is greatly disturbed a t equiluminance. Heterochromatic color gratings appear to move more slowly (Cavanagh. Tyler and Favreau, 1984; Livingstone and Hubel, 1987). Apparent motion is greatly reduced or abolished (Ramachandran and Gregory, 1978; Livingstone and Hubel. 1987). However, Livingstone and Hubel (1987) state that they observed reduction in apparent motion at a G/R ratio that was 20% less than the G / R ratio for equiluminance determined with flicker photometry. This is significant because it may indicate that contrast in a cone mechanism, or some other neural mechanism than the specific V;I mechanism, is being selected in these experiments. There are many experiments on equiluminant vision that have been designed with random dot cinematograms (Ramachandran and Gregory. 1978) or random dot stereograms (Livingstone and Hubel. 1987). These may all be subject to artifacts as a result of chromatic aberration (Flitcroft, 1989). Chromatic aberration may affect spatial frequencies as low a s 4 c/deg, and it certainly may affect experiments with random dot patterns which will be broad band in spatial frequency. Cavanagh et al. (1987) used a minimum motion technique to estimate the cone inputs to the motion mechanism as well a s to determine spatial and temporal tuning of the motion pathway. One of their chief findings was that b cones provide very little input to the


29

motion pathway. Furthermore, minimum motion and flicker photometry give virtually the same equiluminant point for a given pair of colored lights. This is strong evidence for a single pathway with a single spectral tuning curve, as would be the case if M signals were the front end for the motion signal. However, there is a motion response to equiluminant stimuli: the motion system just signifies the wrong velocity. Furthermore, evidence from motion aftereffects (Cavanagh and Favreau. 1985: Mullen and Baker, 1985) indicates there may be some, albeit weaker, inputs from color opponent signals to the motion pathway. There are many sites along the visual pathway at which interactions may occur (see below) and where a Magnocellular signal might be modulated by Parvocellular signals before it reached the site of motion perception. The evidence for Parvocellular inputs involves suprathreshold motion perception.

Interactions between M and P pathways The independence of P and M pathways as they travel in parallel to cortex from the retina, and through visual cortex is remarkable. However, there are several psychophysical experiments on facilitation of detection and on suppression of detection that indicate substantial coupling between chromatic and achromatic signals. First, there are the results of Switkes et al. (1988) on masking and facilitation of color by luminance, and luminance by color. The most interesting in this paper is the facilitation of detection of equiluminant color patterns by luminance patterns even if the latter were substantially suprathreshold. This suggests that one of the functions of the Magnocellular pathway might be to gate Parvocellular signals into the cortex. This concept would also make sense of Kelly's finding that equiluminant chromatic patterns suffer great losses in contrast sensitivity when stabilized on the retina (Kelly, 1983). It is well known that Parvocellular signals are sustained in time when the stimulus is a colored pattern (e.g.. Schiller and Malpeli. 1978). Yet, an image defined solely by color fades faster and more completely than a luminance pattern. Other studies that suggest a role for luminance signals in facilitating or gating chromatic signals are the investigations of the gap effect by Boynton. Hayhoe and MacLeod (1978) and by Eskew (1989). These studies show that luminance steps near the border of colored test object may facilitate chromatic discrimination. The effect is only significant for colored stimuli that are defined by b cone modulation. Yet the effect does indicate the possibility for interaction between M and P pathways. The search for evidence about P-M interaction should prove a s fruitful and challenging as the previous work on P-M parallelism and independence at lower levels of the visual pathway.

Conclusions The retina contains many visual systems within it. In the cat, the X and Y and the many W classes project from the retina to diverse targets within the brain. The different spatially filtered versions of the world presented by these different neurons are obviously used for different visual functions. In the monkey, because of the extraordinary

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CHAPTER 1

importance of color vision, the segregation of function between different retinocortical channels is even more obvious than in the cat. The P pathway, from P ganglion cells through the Parvocellular layers of the LGN to primary visual cortex V1. carries signals about color and location. The M pathway carries signals about contrast and motion. These two pathways are kept separated up to visual cortex, but there are important interactions between the pathways in cortex that remain to be explored. Acknowled cfem e n t a : I would like to thank my colleagues Shaul Hochstein, Jonathan Victor, Ehud Kaplan, Jim Gordon, Keith Purpura, Norman Milkman, Clay Reid, Yuen Tat So, and Michael Hawken for their great help. Preparation of this article was partly supported by NIH grant EY 01472. and NSF grant BNS 870606, and by a grant from the Sloan Foundation.

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Schiller, P.H. and Colby. C.L. (1983).The responses of single cells in the lateral geniculate nucleus of the rhesus monkey to color and luminance contrast. Vision Research, 23, 1631-1641. Schiller, P.H. and Malpeli. J.G. (1977). Properties and tectal projections of monkey ganglion cells. Journal of Neurophysiology, 40, 428-445. Schiller. P.H. and Malpeli, J.G. (1978).Functional specificity of lateral geniculate laminae in the rhesus monkey. Journal of Neurophysiology. 41. 788-797. Schnapf. J.L.. Kraft, T.W. and Baylor, D.A. (1987).Spectral sensitivity of human cone photoreceptors. Nature, 325. 439-441. Shapley, R. and Enroth-Cugell. C. (1984). Visual adaptation and retinal gain controls. In N. Osborne and G. Chader (Eds.), Progress inRetinaZ Research Vol. 3. p. 263-346.Pergamon, Oxford. Shapley, R. and Kaplan, E. (1989).Responses of magnocellular LGN neurons and M retinal ganglion cells to drifting heterochromatic gratings. Investigative Ophthalmology and Visual Science Supplement, 30, 323. Shapley. R. and Perry, V.H. (1986).Cat and monkey retinal ganglion cells and their visual functional roles. Trends ln Neuroscience, 9, 229-235. Shapley, R.. Kaplan. E. and Soodak. R. (1981).Spatial summation and contrast sensitivity of X and Y cells in the lateral geniculate nucleus of the macaque. Nature, 292, 543-545. Shipp, S. and Zeki, S. (1985).Segregation of pathways leading from area V2 to areas V4 and V5 of macaque visual cortex. Nature, 316, 322-325. Smith, V.C. and Pokorny. J. (1975).Spectral sensitivity of the foveal cone photopigments between 400 and 500 nm. Vision Research, 16. 161 - 172. Sperling. H.G and Harwerth, R.S. (1971).Red-green cone interactions in the increment-threshold spectral sensitivity of primates. Science, 172. 180-184. Stromeyer, C.F., Cole, G.R., and Kronauer. R.E. (1987).Chromatic suppression of cone inputs to the luminance flicker mechanism. Vision Research, 27, 1 1 13-1137. Switkes, E.. Bradley, A., and DeValois, K.K. (1988). Contrast dependence and mechanisms of masking interactions among chromatic and luminance gratings. Journal of the Optical Soceity of America A, 7, 1149-1162. Tootell. R.B.H.. Silverman, M.S., DeValois. R.L., and Jacobs, G.H. (1983).Functional organization of the second visual cortical area in primates. Science, 220, 737-739. Tootell, R.B.H.. Silverman. M.S., Hamilton. S.L.. DeValois. R.L.. and Switkes. E. (1988). Functional anatomy of macaque striate cortex 111. Color. Journal of Neuroscience, 8, 1569-1593. Tootell. R.B.H., Hamilton, S.L., and Switkes, E. (1988). Functional anatomy of macaque striate cortex lV. Contrast and magno-parvo streams. Journal of Neuroscience, 8. 1594-1609. Troscianko. T. and Harris, J. (1988). Phase discrimination in chromatic compound gratings. Vision Research, 28. 1041- 1049. Wagner, G. and Boynton, R.M. (1972).Comparison of four methods of heterochromatic photometry. Journal of the Optical Society of America, 62. 1508-1515.

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Wiesel, T.N. and Hubel, D.H. (1966). Spatial and chromatic interactions in the lateral geniculate body of the rhesus monkey. Journal of Neurophysiobgy, 29,1 1 15-1156. Zrenner, E. and Couras. P. (1983).Cone opponency in tonic ganglion cells and its variation with eccentricity in rhesus monkey retina. In J.D. Mollon and L.T.Sharpe (Eds.). Colour Vision, Academic, London. p. 211-224.

A lications of Parallel Processing in Vision ~.Trarman(mitor) 8 1992 Elsevier Science Publishers B.V. All rights reserved

37

Parallel Processing in Human Vision: History, Review, and Critique BRUNO G. BREITMEYER

Introduction We live and move about in a visual world composed of richly varied surfaces, objects and events that can be characterized along a relatively small set of distinct perceptual dimensions or attributes. It would be reasonable to expect efficient information gathering systems like our brains to have incorporated into their functional design distinct subsystems, each specialized to process one ar a few of these limited dimensions and attributes. Hence, the system as a whole would comprise a set of parallel information processing channels. Recently, the existence of parvocellular (P) and magnocellular (M) streams of processing in the monkey visual system has provided a particularly useful and popular basis for models of parallel processing of form/color and depth/motion in primate vision (Livingstone and Hubel. 1987, 1988; DeYoe and Van Essen. 1988). However, the proposal that the visual system performs two broadly separable and parallel types of functions - one concerned with object recognition and identification (figure, form, color), the other with spatial and spatiotemporal relations (ground, position, depth, motion) - has been around for some time (Ingle, 1967; Held, 1968), and the neural and behavioral bases supporting these and related functional distinctions have been increasingly elaborated over the past 25 years (Schneider. 1967; Trevarthen, 1968; Weiskrantz. 1972; Humphrey, 1974; Breitmeyer and Ganz. 1976; Stone, Dreher and Leventhal, 1979; Ungerleider and Mishkin, 1982; Mishkin, Ungerleider and Macko, 1983; Ungerleider, 1985; Previc. 1990; Weisstein et al.. this volume). In particular, recent anatomical and physiological studies of cortical pathways (Shipp and Zeki, 1985; Ungerleider, 1985; Van Essen, 1985; Schiller, 1986; Maunsell, 1987; Livingstone and Hubel. 1988; DeYoe and Van Essen, 1988; Desimone and Ungerleider, 1989: for a review, see also Shapley, this volume) as well as midbrain pathways (Goldberg and Robinson, 1978; Wurtz and Albano, 1980; Schiller, 1986) have increased our understanding of the later processing stages in higher brain centers participating in these functions.

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Over the same time period, related developments also have revealed parallel processing early along afferent visual pathways. As noted by Stone (1983). the concept of parallel processing at early visual levels has had a long history. For instance, the existence of separate rod and cone systems was established during the latter half of the 19th century. More recently, the existences of different chromatic and achromatic (luminance) channels (de Lange. 1958; Kelly and van Norren, 1977) of direction, orientation, and spatial-frequency selective mechanisms (Sekuler and Ganz. 1963; Campbell and Kulikowski, 1966; Pantle and Sekuler, 1968; Blakemore and Campbell, 1969) and of separate pathways for perception of luminance increments (brightness) and decrements (darkness) (Jung. 1961, 1973) also have been established psychophysically and, still more recently, anatomically (Schiller, 1982. 1984; Schiller. Sandell and Maunsell, 1986; Tootell et al.. 1988a,c). While these and other developments already pointed to several forms of parallel processing of visual information, it was not until about two and a half decades ago that the discovery of X and Y ganglion cells in cat retina by Enroth-Cugell and Robson (1966) initiated, in the early and mid 1970s. concerted and extensive efforts among visual psychophysicists and perception psychologists to investigate in humans the existence and properties of analogues of these two neural pathways and their relation to the several other known types of distinct visual mechanisms. Hints of psychophysical analogues of these distinctions already existed a t and prior to this time; however, they were not yet expressed within a n explicitly articulated parallel-processing framework based on plausible neurophysiological substrates such as the X and Y pathways. For instance, in the early 1950s Saucer (1954) hypothesized that the human visual system contains motion-processing analyzers or channels which have properties distinct from channels processing form and pattern detail. In the late 1960s Pantle and Sekuler (1969) empirically supported such a distinction. They demonstrated via selective adaptation techniques that the response of human visual mechanisms sensitive to direction of motion saturated at a low contrast of about 0.2, whereas the response of mechanisms sensitive to orientation of form (Campbell and Kulikowski, 1966) increased monotonically up to a maximal contrast of 1.0. The distinction was given further empirical support in the late 1960s by Robson (1966). van Nes et al. (1967) and in the early 1970s by Tulunay-Keesey (1972). For instance, van Nes et al. (1967) reported separate form and flicker thresholds for drifting stimuli containing low spatial and high temporal frequencies. Similarly, Tulunay-Keesey (1972) showed that one can obtain separate thresholds for detecting the flicker component or else the pattern component of a line flashing on and off at varying temporal frequencies. Tulunay-Keesey (1972) found that flicker detectors were generally more sensitive over the entire range of temporal frequencies she used (0.3 - 30.0 Hz) than were pattern detectors. As we shall see below. the distinctions between flicker/motion perception and form/pattern perception on the one hand and transient and sustained channels on the other played a crucial role in the initial studies of parallel processing in human vision. Although it continues to play a n important role to this day, it has met with criticism and calls for revision (Harris, 1980; Derrington and Henning. 1981; Green, 1981,

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1984: Kelly and Burbeck, 1984) and has been augmented by additional distinctions based on visual latency, various types of masking, and more recent distinctions drawn with respect to the processing of color, texture, as well as depth (Zeki. 1978; Cavanagh. Tyler and Favreau. 1984; Livingstone and Hubel, 1987, 1988; DeYoe and Van Essen, 1988; Cavanagh, 1989. Logothetis et al.. in press; Schiller, Logothetis and Charles, in press; Schiller and Logothetis, in press). In the following we will discuss the early developments in studies of parallel visual processing in humans, their promises and problems, and their more recent and current trends.

Developments in the sustained/transient dual channel approach

Form/pattem andflicker/ motion Despite attendant problems to be discussed below, the sustained/transient terminology used by some physiologists (Cleland et al.. 1971; Cleland and Levick. 1974; Bolz et al., 1982) was initially adopted broadly and extensively by psychophysicists investigating perceptual signs of underlying parallel pathways. Tolhurst (1973) and Kulikowski and Tolhurst (1973) were among the first investigators to adopt the sustained/transient distinction to describe pattern-sensitive and motion- or flicker-sensitive channels in human vision. Tolhurst (1973) compared thresholds for detecting stationary sinusoidal gratings to thresholds for detecting gratings which drifted or were temporally modulated in counterphase at a rate of 5 Hz. For spatial frequencies of 4 c/deg or less, Tolhurst (1973) found threshold sensitivities for temporally modulated gratings to be higher than sensitivities for stationary gratings; above 4 c/deg the two sensitivities were equal. Similar results were reported by Kulikowski and Tolhurst (1973) when comparing flicker to pattern threshold sensitivities for temporally counterphased gratings. Thus the pattern-sensitive sustained channels were characterized by preference for higher spatial frequencies and lack of preference for temporally modulated stimuli over stationary ones. Transient channels, in contrast, were characterized by preference for lower spatial frequencies and temporally modulated or moving stimuli. Moreover, Tolhurst (1973) and Kulikowski and Tolhurst (1973) drew explicit comparisons between these psychophysically defined sustained and transient channels and the X and Y classes of cells studied in cats.

Additional approaches and findings Related approaches and interpretations have been adopted by several other investigators (Breitmeyer and Ganz, 1976: Legge. 1978; Green, 1984). The common feature in these investigations is the repeated finding of differences between the spatiotemporal response characteristics of the visual system at low and high spatial frequencies. Besides being more sensitive to rapid motion and flicker, evidence indicates that the low spatial frequency transient channels, relative to the higher spatial frequency sustained ones, are also characterized by a higher sensitivity to abrupt a s compared to gradual stimulus onset

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(Breitmeyer and Julesz, 1975; Tolhurst. 1975 a.b; Wilson, 1978). briefer temporal summation (Brown and Black, 1976; Breitmeyer and Ganz, 1977; Watson and Nachmias, 1977; Legge, 1978). broader orientational tuning (Burbeck and Kelly, 1981; Gorea, 1979; Kelly and Burbeck. 1987). and a greater susceptibility t o spatiotemporal adaptation (Bowker and Tulunay-Keesey, 1983).

Visual latency In addition, the transient and sustained channels also differ in response latency. Breitmeyer (1975) demonstrated that simple reaction time (RT) to the onset of briefly flashed gratings set at a 60% contrast increased monotonically with spatial frequency. RT was roughly 200 ms at a spatial frequency of 0.5 c/deg and increased to a value ranging between 300 and 350 ms at a spatial frequency of 11.0 c/deg. The monotonic increase in RT with spatial frequency, although somewhat attenuated, was maintained even when the gratings were equated for subjective contrast (Breitmeyer, 1975). Similar RT findings were reported by other investigators for grating onset (Lupp, Hauske and Wolf, 1976; Vassilev and Mitov, 1976; Parker, 1980; Breitmeyer, Levi and Harwerth. 1981a). offset (Parker, 1980; Breitmeyer et al., 1981a: Long and Gildea, 1981). as well as contrast reversal (Parker, 1980).In a somewhat different paradigm, Tolhurst (1975a) showed that the RT distribution to gratings just above contrast threshold differed as a function of spatial frequency. For a 0.2 c/deg grating the RT distribution was bimodal, with each mode corresponding to the onset or offset of the grating. According to Tolhurst (1975a). these modes reflected the probabilistically distributed activities of transient channels to grating on- and offset. For a higher, 3.5 c/deg grating activating predominantly sustained channels the RT distribution was unimodal and, moreover, of longer latency than the onset RTs to the low frequency grating. Similar findings have been reported by Breitmeyer et al. (1981a) a s well a s by Schwartz and Loop (1982, 1983) in their study of transient luminance and sustained color-opponent channels.

Visual masking Various masking paradigms also have been employed to study the properties of, and interactions between, sustained and transient channels. Legge (1978) employed a technique of measuring contrast thresholds when the onsets and offsets of test gratings of variable spatial frequency and duration were transiently masked by the 20-ms presentation of a mask grating. Relative to the no-mask condition the effect of the mask was to increase threshold temporal summation for test gratings having spatial frequencies below but not above 3 c/deg. This was attributed to the transient channels' loss of sensitivity at low spatial frequencies when a transient mask is used; the brief mask failed to affect the higher spatial frequency sustained channels and thus did not alter their temporal summation properties (Legge. 1978). Related findings using uniform field flicker (UFF) masks (Breitmeyer et al., 1981a) and uniform flashes of light (Green 1981. 1984) have been reported. For instance, Breitmeyer et al. (1981a).showed that, relative to a steady background, UFF increased flicker thresholds and on- and

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offset RTs at low but not high spatial frequencies. Similarly, Green (1981) showed that transient masking a t the onset and offset of a uniform conditioning flash (Crawford, 1947) was produced with low but not high spatial frequency test gratings. In both of these studies the transient masking produced by either the UFF or the uniform conditioning flash affected primarily the response of low spatial frequency transient channels while leaving that of the higher spatial frequency sustained channels unaltered. Several theories of visual masking and information processing based on the sustained/transient channel distinction have been proposed (Matin, 1975; Weisstein. Ozog and Szoc, 1975: Breitmeyer and Ganz. 1976). In their particular theory Breitmeyer and Ganz (1976) dealt not only with the masking phenomena discussed above, which tap effects occurring within one or the other of the two types of channels, but also with metacontrast masking (Stigler, 1910: Alpern. 1953; Weisstein, 1972). which indexes interactions between the two channels. According to the sustained/ transient theory of masking. the inverted, U-shaped function relating the magnitude of metacontrast to the onset asynchrony between the target stimulus and the following mask stimulus results from post-retinal inhibition of the target's long-latency sustained channels by the mask's short-latency transient channels. Psychophysical evidence for the reverse inhibition of transient channels by sustained ones has been obtained from studies of target disinhibition in metacontrast (Breitmeyer, 1978: Breitmeyer. Rudd and Dunn, 1981b). inhibition of the transient motion detecting channels by sustained pattern channels (von Gruenau, 1978: Banta and Breitmeyer, 1985) and asymmetric interference between the low and high spatial frequency components of compound gratings (Hughes. 1986). Inhibitory interactions between X and Y cells, the neural analogs of sustained and transient channels, have been reported in the lateral geniculate nucleus (LGN) and cortical area 17 of cat (Hoffmann. Stone and Sherman, 1972: Singer and Bedworth. 1973: Singer, 1976; Tsumoto and Suzuki. 1976). although, as noted by Lennie (1980a). in monkey such interactions probably occur no earlier than visual cortex. A more extensive and detailed discussion of the roles and interactions of sustained and transient channels in visual masking and their neural analogues can be found in Breitmeyer (1984).

Controversies and criticisms The above findings and interpretations are controversial and have met with substantial criticism. In the last 10 years. several articles have appeared which have questioned the validity of the sustained/transient distinction in human vision. The disputes can be regarded a s focusing on two broad and interrelated issues. One concerns the evidence and psychophysically defined properties used to establish the distinction between sustained and transient channels in humans (as well a s subhuman organisms): the second concerns the link between the psychophysics and the neurophysiology of parallel pathways and the attendant problem of naming, identifying and classifying channels or pathways defined via either physiological or psychophysical methods.

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Evidence for the psychophysical distinction between sustained and transient channels Turning to the first issue, several investigators -- among them Lennie ( 1980b), Burbeck ( 1981). Derrington and Henning ( 1981). Panish, Swift and Smith (1983), Green (1984). Kelly and Burbeck (1984) -- have argued that the evidence derived from studies such as Tolhurst's (1973) or Kulikowski and Tolhurst's (1973) provides neither a valid nor a consistent or clear set of criteria for distinguishing between transient and sustained channels. Their objections are based on methodological as well as definitional grounds.

M e thodoLogical controuersies The methodological objection is t h a t Tolhurst (1973). Kulikowski and Tolhurst (1973) and a number of similar studies (Tulunay-Keesey, 1972; Breitmeyer and Julesz, 1975: King-Smith and Kulikowski. 1975: Tolhurst, 1975b: Breitmeyer et al., 1981a) used psychophysical methods which relied on separate subjective threshold criteria for flicker/motion detection and for form/pattern detection. When supposedly "criterion-free'' or forced-choice methods are employed instead, differences between form/pattern and flicker/motion thresholds may be eliminated (Lennie, 1980b: Derrington and Henning. 1981) or, as in Burbeck's (1981) study, reversed a t all but the lowest spatial frequencies. As a first response to this criticism one should note that no psychophysical threshold measuring procedure is truly criterion-free. Perhaps one can reduce the use of two or more subjective criteria to a single detection criterion by using a forced-choice or similar procedure: but the problem inherent in using some criterion is not eliminated. In particular, in Burbeck's (1981) study a test grating, temporally modulated in counterphase a t threshold, was always compared to a reference stimulus which could be either a UFF of the same temporal frequency slightly above threshold or else a stationary grating of the same spatial frequency also slightly above threshold. This procedure hardly eliminates subjective criteria: rather, it forces the observer to substitute subjective or phenomenal criteria reflecting the experimenter's choices or standards of reference percepts for those of his/her own choosing. In addition, as noted by both Bowker and Tulunay-Keesey (1983) and Green (1984). Burbeck (1981) as well as Derrington and Henning (1981) overlook a n alternative interpretation of their data. Burbeck (1981) and Derrington and Henning (1981) argued that the channels most sensitive to low spatial frequency counterphase gratings not only responded to the temporal aspects of the gratings but also encoded their spatial orientation. However, since counterphase modulated gratings can be detected by mechanisms tuned to direction of motion (Levinson and Sekuler. 1975). the orientation discrimination could have been performed by such motion-selective as opposed to orientation-selective mechanisms. I have discussed additional concerns regarding Burbeck's (1981) criterion-free methods elsewhere (Breitmeyer, 1984). For now I would like to proceed to a second, more general consideration of the use of two separate

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subjective criteria, such as flicker/motion and from/pattern. employed in the method of adjustment versus use of a single criterion, whatever it may be, presumably adopted in a forced-choice procedure. First, as shown by Pantle (1983).even when subjects are placed in a forced-choice paradigm, compelling evidence for a distinction between low spatial frequency transient channels and higher spatial frequency sustained channels can be obtained. Similarly, using "objective" forced-choice techniques, Watson and Robson (1981) obtained results consistent with the existence of two distinct sets of mechanisms. One of these mechanisms is selective for low, the other for high temporal frequencies. Watson and Robson (1981)believe these two mechanisms to correspond to the sustained and transient mechanisms investigated by Kulikowski and Tolhurst ( 1973),whose technique relied on observers shifting from one "subjective" threshold criterion to another. A second noteworthy issue is exemplified by Stone's (1983)more fundamental points made in his monograph entitled Parallel Processing in the Visual System. There Stone argues that the psychophysical data obtained with forced-choice methodology used by investigators such as Lennie (1980b)and, by implication, others (e.g., Derrington and Henning, 1981; Green, 1983) is of no direct relevance to the results obtained with adoption of two separate subjective criteria as in, say, KulikowsM and Tolhurst's (1973) study and, again by implication, other studies using similar methods (e.g.. Breitmeyer and Julesz. 1975; Casima. Blake and Lema. 1977: Essock and Lehmkuhle. 1982). Nor, Stone (1983)claims further, do data obtained with forced-choice methods provide alternative explanations to results obtained with the method of adjustment. Rather, they reveal the obvious (but worth repeating) point that different methods yield different results, and more specifically, that the method of adjustment and forced-choice methods do not provide equivalent tests of visual performance. As noted by Essock and Lehmkuhle (1982). this is particularly evident when comparing the pattern task criterion of "spatial structure" (e.g.. the discrimination of the distinct bars of a grating) used in the method of adjustment to, say, the two-alternative forced-choice "pattern" task criterion for detecting any spatial contrast on a n otherwise uniform field. Merely calling both tasks by the same name does not eliminate the fact that the perceptual contents to which the observers attend in the two tasks are not equivalent. Stone (1983) uses the following example to illustrate this important point. In studies of "blind sight." tests relying on subjective, conscious experience render the patient quite blind, whereas forced-choice methods, particularly those relying on visually guided motor responses, reveal residual visual function of which the patient has no subjective, conscious awareness. Although based on a different experimental rationale and patient population, a similar case for the use of subjective criteria can be supported by Brussell et a1.k (1984)study of pattern and flicker sensitivity in normal subjects as compared to multiple sclerosis (MS) patients and by Regan and Neima's (1984)related study comparing visual performance in normal observers to patients with MS, glaucoma, and ocular hypertension. The point raised by such studies, although often forgotten or neglected, is not new. It has been made by Kahneman (1968)and by Breitmeyer and Ganz (1976)with regard to visual masking and by

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Bridgeman et al. (1979) in their study of saccadic suppression. A shift of criterion can be effected not only via a quantitative shift (e g., making the criterion more or less conservative) along a given perceptual dimension but also via the choice of criterion content, Le., the choice of the qualitative informative aspect of a stimulus to which a n observer attends or responds in a detection or discrimination task. The two types of criterion shifts should not be confused. The prohibition of the latter, qualitative shifts when forced-choice procedures are dogmatically employed may compel observers to use a single criteria1 perceptual dimension and thus eliminate measurable differences between tasks such as "flicker" versus "pattern" detection. While the logic of such a procedure can effectively force a disconfirmation of the existence of separate flicker/motion and from/pattern detectors, it also results in an unfortunate loss of useful information. I t is interesting that a trained physiologist like Stone should see the importance for method as well as explanation of the use of subjective criteria based on conscious experience in psychophysical and perceptual investigations in addition to the putatively objective, forced-choice criteria. Along with him, I believe that rather than eliminating them in favor of a single criterion used in forced-choice methods it is far wiser to exploit and explore the richer information inherent in including subjective criteria tapping separate perceptual dimensions.

Controversies concerning the psychophysically defined distinctions between sustained and transient channels However, in choosing subjective criteria I am not claiming that the properties originally used to distinguish psychophysically between sustained and transient channels are not in need of reconsideration or revision. On the contrary, despite aforementioned problems with their own methodological rationale, results of several studies -- among them Burbeck (1981). Derrington and Henning (1981). Green (1983, 1984). Kelly and Burbeck (1984). and Badcock and Sevdalis (1987) -- indicate that such reconsideration and revision may be in order. For instance, while noting that most psychophysical studies of spatiotemporal vision do not require a two-mechanism model, Kelly and Burbeck (1984) concede that the effects of the masking of gratings by uniform conditioning flashes (Stromeyer. Zeevi and Klein. 1979) or UFF (Breitmeyer e t al.. 1981a) cannot be easily predicted by the spatiotemporal threshold function based on a single mechanism. The implication is that recourse to a two-mechanism, sustained/transient approach may be required to account for these data. Hence, the use of masking with either UFF or a uniform conditioning flash to distinguish between sustained and transient channels may be especially critical. Recently, Badcock and Sevdalis (1987)have taken issue with the use of UFF masking to distinguish between transient and sustained channels on the grounds that prior studies, e.g., Breitmeyer et al.(1981a). using this technique introduced a n artifact since the effective contrast of the target grating to be detected flickered in synchrony with the flickering uniform field. After controlling for this artifact, Badcock and Sevdalis (1987) indeed obtained weaker UFF masking than previously reported. However, it was significantly present a t spatial frequencies of 4 c/deg and lower, a finding consistent with

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the existence of flicker sensitive, low spatial frequency transient channels. The sustained/transient channel distinction also survives Green's (1981, 1984) related analysis of masking by a uniform flash of light. A conditioning flash can produce two countervailing effects. On the one hand, it can produce transient masking at its on- and offset (Crawford. 1947): on the other, this effect is confounded with changes in contrast sensitivity accompanying changes of light adaptation level (Patel. 1966). Green's (1981, 1984) results and analysis show that while a uniform conditioning flash produces a facilitation effect on contrast sensitivity a t both high and low spatial frequencies, it additionally produces a masking effect at the on- and offsets of the conditioning flash which is specific to the low spatial frequency transient system. Another problematic issue is the psychophysical relationship and degree of correspondence between flicker/motion and form/pattern detection and separate transient and sustained channels, respectively. For instance, Kelly and Burbeck (1984) argue that although mechanisms for detection of low and high spatial frequencies must have transient and sustained temporal responses, respectively, it does not follow that there must exist two different underlying mechanisms. According to Kelly and Burbeck (1984). such a conclusion would follow only if the two mechanisms display spatiotemporal separability. However, there are problems with the assertion of this criterion. In specifying this criterion Kelly and Burbeck (1984) have posed the following conundrum. While some investigators have reported spatiotemporal decoupling in both X and Y cells in the lateral geniculate nucleus (Lehmkuhle et. al., 1980) and visual cortex (Tolhurst and Movshon, 1975) of cat, a majority (Victor and Shapley, 1979: Lee et. al., 1981; Derrington and Lennie. 1982, 1984: Enroth-Cugell et. al., 1983; Troy, 1983: Dawis et. al.. 1984) report evidence for spatiotemporal coupling in X and Y cells a t retinal and geniculate levels. If the spatiotemporal threshold surface is determined at retinal levels as suggested by Kelly and Burbeck (1984) and if retinal (and geniculate) X and Y cells do not show spatiotemporal separability, then the temporal frequency response of their psychophysical analogues most likely also will depend on spatial frequency. Since the human spatiotemporal frequency response as measured by contrast sensitivity does show this type of interaction, Kelly and Burbeck (1984) may be in the enviable position of 1) asking proponents of separate sustained and transient channels to meet an impossible physiological and, hence, psychophysical criterion while 2) arguing that a single mechanism with properties akin to the retinal X cells investigated by Enroth-Cugell et al. (1983) is sufficient to account for the human spatiotemporal threshold response. Although a single-mechanism account may hold for normal observers, Brussell et al. (1984) have presented data comparing normal observers to M S patients which are hard to reconcile with the existence of a single mechanism determining spatiotemporal vision. The different results obtained by normal observers and M S patients indicate that different mechanisms for processing flicker and pattern exist and that M S patients are specifically deficient in the flicker sensitive mechanism. A comparison of normal observers to a variety of other ophthalmological patients similarly supports the existence of separate form/pattern and flicker/motion channels in human vision (Enoch. 1978: Regan and Neima. 1984; Silverman, Trick and Hart, 1990).

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Another problem with Kelly and Burbeck's (1984) account is that although it has the desirable quality of being parsimonious, it is complicated by Wilson's (1980) finding, based on measures of line-spread rather than contrast sensitivity functions, that the human transient mechanism displays spatiotemporal decoupling. As noted by Wilson (19801, this result indicates that the human spatiotemporal response surface may, at least in part, be determined at cortical levels where spatiotemporal separability holds (Tolhurst and Movshon. 1975) rather than at retinal levels a s assumed by Kelly and Burbeck (1984). Kelly and Burbeck (1984) dismiss Wilson's (1980) finding as inconclusive. Nonetheless, they also point out that the issue of spatiotemporal decoupling within psychophysical and neural channels remains a moot point awaiting resolution. This point is underscored by Lee. Martin and Valberg (1989a), who found that activity of subcortical neurons does not correlate well with certain aspects of spatiotemporal vision and, on that basis, argued that central neural activity must additionally be involved. Besides this problem remaining to be worked out, others also need to be addressed. Burbeck (1981), Derrington and Henning (1981) and Green (1983. 1984) present results indicating that the human visual system cannot be strictly partitioned into sustained (pattern) and transient (flicker/motion) analyzing channels. In particular, Burbeck (1981) and Derrington and Henning (1981) present results indicating that the low spatial frequency transient channels can do some pattern analysis and use these findings a s critical evidence against the sustained-transient distinction. Above, we discussed problems with this interpretation of their results. However, even if it is correct, these investigators, as noted by Green (1984). may have misinterpreted previous authors, such a s Kulikowski and Tolhurst (1973). Tolhurst (1973). and Breitmeyer and Ganz (1976). in claiming that they denied the possibility of form analysis in transient channels. In fact, Breitmeyer and Ganz (1976) are quite explicit in claiming that the transient channels can perform a crude type of pattern analysis, a claim consistent not only with Watson and Robson's (1981) and King-Smith and Kulikowski's (1980) subsequent psychophysical results and interpretations but also with neurophysiological findings (Stone and Dreher, 1973: Lehmkuhle et al., 1980: Frascella and Lehmkuhle, 1984). This, of course, makes use of a stringent motion/pattern dichotomy at both the methodological a s well as explanatory levels impossible (King-Smith and Kulikowski. 1980: Essock and Lehmkuhle. 1982: Murray, MacCana and Kulikowski, 1983): and use of a less stringent dichotomy poses obvious problems if one relies exclusively on it (or any other single perceptual dichotomy) to draw distinctions between sustained and transient channels. A possibly more damaging problem for the sustained-transient channel distinction is Green's (1983, 1984) finding that the high spatial frequency sustained channels are also capable of discriminating flicker and motion at lower rates and velocities than the low spatial frequency transient channels. Although original versions of the sustained-transient distinction (Kulikowski and Tolhurst, 1973: Breitmeyer and Ganz, 1976). based on limited knowledge of underlying physiology, may have claimed that sustained channels respond only to stationary stimuli, more recent versions (Kulikowski. 1978; Murray et al., 1983:

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Breitmeyer, 1984; Raymond & Darcangelo, 1990). taking into account new physiological findings of flicker and motion sensitivity in X as well as Y pathways of cat and monkey (Kulikowski, Bishop and Kato, 1977; Eckhorn and Poepel. 1981; Scobey. 1981: Cleland and Harding. 1983). have incorporated a sensitivity to low-velocity motion in sustained channels. This distinction between high velocity or high temporal frequency transient detectors and low velocity or low temporal frequency sustained detectors has been elaborated psychophysically by a number of investigators in the last decade (Burbeck and Kelly, 1981: Watson and Robson, 1981; Anderson and Burr, 1985: Ferrera and Wilson, 1985: Hess and Plant, 1985: Kelly and Burbeck. 1987). Among other things, these elaborations have revealed noticeable heterogeneity within both the transient as well as sustained systems. In his model of sustained and transient vision, Legge (1978) proposed that the transient system consists of a single, low-pass spatial frequency channel whereas the sustained system consists of multiple band-pass, spatial frequency specific channels (Blakemore and Campbell, 1969) cumulatively spanning a frequency range from as low as .375 c/deg (see also Stromeyer et al.. 1982) to the upper limit of spatial resolution. Wilson and Bergen (1979) and Wilson, McFarlane and Phillips (1983) subsequently were able to derive at least two transient mechanisms from observers' contrast sensitivity functions: and Ferrera and Wilson (1985) have extended the number of transient mechanisms to three. Two other aspects of Ferrera and Wilson's (1985) results are noteworthy. The three transient mechanisms are non-oriented and may correspond to the spatially broad-band transient mechanisms showing little or no orientation selectivity reported by Kelly and Burbeck (1987). Moreover, they possibly may also correspond to the three distinct sets of high temporal frequency, transient detectors reported by Watson and Robson (1981). These detectors, as noted by Watson and Robson (1981). are remarkably poor a t making spatial discriminations, which would be consistent with spatially broad-band and non-oriented response characteristics. Whereas Wilson and Bergen's (1979) data suggest the existence of only two, and Wilson et a1.k (1983) findings suggest the existence of at most four spatial frequency selective sustained channels, Watson and Robson's (1981) data indicate that a s many as seven may exist. The preceding discussions point out some of the problems and controversies that have arisen in attempts to specify psychophysically the response properties of sustained and transient channels. We can summarize the discussion by noting that it is unlikely, if not impossible, to make an unequivocal psychophysical distinction between sustained and transient on the basis of any single criteria1 dimension such as flicker/motion, form/pattern. susceptibility to UFF masking, etc.; rather, a meta-analysis based on a variety of results obtained with the use of several different criterial measures seems to be more informative and telling. This view is similar to that offered by Rowe and Stone (1977) and Stone (1983) in their proposal that neuronal naming and classification be based on as many dimensions as possible. This and related issues will be discussed more fully below.

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Links between the psychophysics and neurophysiology of sustained and transient channels For now, I would like to turn to some of the equally difficult problems (see Teller, 1980. 1984) concerning links between the psychophysics and the neurophysiology of parallel pathways. My opinions here share much in common with those offered by Stone (1983). If one views the correspondence between neurophysiology and psychophysics as tentative hypotheses in need of testing and correcting, then the enterprise of drawing links between the two domains can be fruitful without the danger, as noted by Uttal (1971, 1981),of reducing psychological theory to physiological data. To establish links, one works with the main assumption that the visual neurophysiology of organisms like the cat or monkey can be related to human psychophysics. With regard to the sustained/transient approach this assumption in turn carries with it two criteria that must be satisfied. First, one must find psychophysical indices of sustained and transient channel activities in these organisms which parallel similar indices found in humans; and a second requirement is that the psychophysics indeed relates to the known physiology. The first criterion has been met by several convergent lines of investigation. It has been met in studies of normal, behaving cat (Blake and Casima. 1977) and monkey (Harwerth. Boltz and Smith, 1980) in which psychophysical indices used in human studies -- e.g., threshold sensitivity to flickering and stationary gratings, reaction time to near-threshold and suprathreshold gratings, temporal summation at threshold -- were employed. However, the latter criterion has been challenged by Lennie (1980b) and more recently by Troy (1983) and Frascella and Lehmkuhle (1984). On the basis of their physiological results, they argue that X and Y cells in cat do not subserve the distinct function of fonn/pattern and flicker/motion detection, respectively. As discussed above, one may need to revise the distinction to allow for a crude form of pattern analysis in Y cells and for some sensitivity to motion in X cells. However, Stone (1983) offers a n alternative interpretation of these results. They were obtained from samples of cells, many of which fell outside the area centralis of cat. On the basis of his cat studies, Stone (1983: see also Cleland and Levick, 1974; Hochstein and Shapley, 1976) believes that X cells located in the area centralis will have a significantly poorer sensitivity at low spatial frequencies and high temporal frequencies than peripherally located ones. Hence, a comparison which includes X and Y cell responses outside the area centralis may not show differences that very likely exist for cells in the area centralis. Certainly comparison of responses from cells located in the area centralis would be more relevant for the psychophysics of cat since one would expect that, during training, cats typically learn to direct their gaze and, thus, their area centralis at the test stimuli (Blake and Casima, 1977). Moreover, if Wilson (1980) and Lee et al. (1989a) are correct in claiming that spatiotemporal vision requires cortical as opposed to the subcortical mechanisms suggested by Kelly and Burbeck (1984). then Lennie's (1980b). Troy's (1983) and Frascella and Lehmkuhle's (1984) findings would lose some of their critical impact since they are based on study of subcortical cells. In all fairness. it should be noted, however, that this loss of critical impact

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would also apply to all the physiological studies of subcortical cells which in the past have been used to support the existence of separate flicker/motion and from/pattern channels in humans. Based on the above limited findings, the best we can say is that although the locus of neural substrates for detection is a n important issue (Teller, 1980, 19841, it remains to be resolved. The roles of the two pathways in cat psychophysics also have been investigated by studying the effects of pressure blocking of Y and X optic nerve fibers in cat (Burke, Burne and Martin, 1985; Burke, 1986; Burke et al., 1986.1987). With selective degenerative loss of Y fiber activity, acuity is not impaired. Hence, in cat, acuity and the perception of pattern detail is not mediated by the Y pathway. The X pathway appears to be necessary for visual acuity tasks in cat (see Waessle, 1986) since additional pressure-block induced degeneration of a majority of X fibers reduces acuity substantially (Burke et al., 1987). A visual function which was compromised but not eliminated by selective Y fiber degeneration was the ability to discriminate fast motion. According to Burke (1986) and Burke et al. (1987). this indicates that while the Y pathway is superior in its ability to discriminate fast motion, the X pathway's ability to discriminate such motion nonetheless overlaps considerably with the Y pathway's. While showing that each pathway is specialized for particular visual functions, these and particularly the latter results support Lennie's (1980b) and Frascella and Lehmkuhle's (1984) claim that in cat there are no clear-cut distinctions or sharp restrictions of function between the two pathways. The human visual system is more similar anatomically and physiologically to that of monkey than that of cat; and, as noted, the psychophysical performance of monkey provides evidence consistent with the existence of sustained and transient channels that parallels similar evidence found in humans (Harwerth et al.. 1980).A problem, however, is that the visual systems of monkey and cat are sufficiently different that the properties used to define X and Y cells in cat, which typically have been used to draw parallels with sustained and transient vision in humans, may not be applicable to monkey (Shapley and Lennie, 1985). For example, several investigators (Dreher, Fukuda and Rodieck. 1976; Schiller and Malpeli. 1978: Hicks, Lee and Vidyasagar, 1983; Derrington and Lennie, 1984; Maunsell, 1987) report that the magnocellular (M) and parvocellular (P) cells in monkey LGN have predominantly transient and sustained response characteristics, respectively. Using response latency to electrical stimulation of the optic chiasm and absence or presence of a sustained response to standing contrast a s classification criteria, Dreher et al. (1976) and Sherman et al. (1976) concluded that monkey M and P cells correspond to cat Y and X cells, respectively. However, when linearity of spatial summation is used to classify cells, not only are almost all P cells X-like but s o are many M cells (Blakemore and Vital-Durand, 1981; Shapley, Kaplan and Soodak, 1981; Kaplan and Shapley. 1982; Marrocco. McClurkin and Young, 1982). More recent evidence suggests that many M cells may correspond to X cells, while most P cell do not (see Shapley, this volume), Regarding such classification problems, Rowe and Stone (1977) and Stone (1983) recommend on philosophical and methodological grounds against the use of a single or essentialistic (see Popper, 1962) criterion, such as linear spatial summation across

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the receptive field, to identify cells, b u t rather advocate a multi-criterion classification system. With such a system, which relies on a number of physiological and anatomical criteria, the M and P cells of monkey are by and large transient and sustained (Schiller and Malpeli. 1978; Maunsell and Schiller. 1984). However, as with most analogies this one is imperfect, and it is further complicated by several findings which have questioned the equivalence of the originally proposed X/Y and sustained/ transient distinction. The temporal response characteristics of neurons are influenced by a number of stimulus variables (Shapley and Victor, 1978: Kaplan and Shapley, 1982) such as the wavelength composition of the stimulus (Marroccco, 1976: DeMonasterio, 1978a). the retinal eccentricity of neural receptive fields (Cleland and Levick. 1974; Cleland, 1983). and the state of adaptation (Zacks. 1975; Jakiela, Enroth-Cugell and Shapley. 1976; Saito and Fukuda. 1986).The effects of light or dark adaptation provide a particularly striking example as to why, according to Rowe and Stone (1977) and Stone (1983). a multi-criterion classification system should be employed. With dark adaptation Y cell responses become more sluggish or sustained until at scotopic levels one cannot distinguish between X and Y cells on the basis of absence or presence of a sustained response component (Zacks, 1975; Jakiela et al., 1976: Saito and Fukuda. 1986). However, as noted by Saito and Fukuda (1986). along with giving a sustained response at scotopic levels, Y cells also show linear spatial summation across the receptive field, a property which is absent a t photopic levels (Enroth-Cugell and Robson, 1966; Saito and Fukuda, 1986). Accordingly, not only do Y cells become sustained with dark adaptation but they also become X-like if one takes presence or absence of linear summation a s an absolute or essentialistic identification criterion. Besides raising obvious problems for cell classification, these results suggest a tighter link between absence or presence of a sustained response component on the one hand and linear spatial summation on the other than was previously believed (Zacks. 1975; Jakiela et al.. 1976; Kaplan and Shapley. 1982). It also raises the possibility that other stimulus parameters such as wavelength composition which affect the level of response transience and sustainedness (Marrocco, 1976: DeMonasterio, 1978a) may correspondingly affect linear spatial summation. Visual latency is another temporal response characteristic whose use in distinguishing sustained X from transient Y pathways (Singer and Bedworth. 1973: Ikeda and Wright, 1975; 1976) has been criticized. In particular, using near-threshold stimuli, Lennie (1980b) was able to eliminate response latency differences between X and Y cells. However, as noted by Maunsell (1987). although neither visual response latency nor transience or sustainedness provide absolutely reliable classification criteria, one would expect the most severe deviations from such a classification scheme for near-threshold stimuli and the clearest differences in response characteristics to emerge when suprathreshold stimuli are used. In particular. Maunsell (1987) reports that with clearly suprathreshold stimuli, M-pathway cells have a shorter visual response latency than P-pathway cells not only in LGN and cortical area V1 of macaque monkey but also a t later stages of processing, e.g., when comparing transient cells in area MT and sustained cells in area V4.

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Similar results, when suprathreshold stimuli are used, have been reported in extrastriate regions of owl monkey (Petersen, Miezin and Allman, 1988) a s well as the retina (Bolz et al., 1982; Sestokas et al., 1987) and LGN (Sestokas and Lehmkuhle, 1986: Sestokas et al., 1987) of cat, although the latter results have been qualified by Troy and Lennie (1987).What these and the other findings discussed above point out is that since any single classification criterion may be unreliable it is important to extensively explore several stimulus dimensions and to use many convergent physiological response criteria to classify cells. As noted previously, a similar multidimensional approach should be taken in psychophysically studying human parallel channels.

The role of color-opponent P and broad-band M pathways in vision As Schiller and Malpeli's (1978) and Maunsell's (1987; Maunsell and Schiller, 1984) investigations indicate, it may be time to look increasingly to P and M pathways of monkey rather than X and Y pathways of cat for analogues of human sustained and transient channels. According to Livingstone and Hubel (1987. 1988). cells in the P and M pathways can be differentiated on the basis of color selectivity, contrast sensitivity, spatial resolution and temporal resolution. Specifically. single cell studies as well investigations of the perceptual effects of selectively lesioning the P or M pathway in monkey have revealed the following response properties. The color-opponent P cells are selective in their response to wavelength while the broad-band M cells are not (De Valois et al., 1958; Wiesel and Hubel, 1966: Schiller and Malpeli. 1978). The P pathway, therefore, is involved in visual analysis and coding of color while the M pathway typically is not (Tootell et al., 1988b: Merigan, 1989: Schiller. Logothetis and Charles, 1990). However, although not considered to be color-coded, a large proportion of cells in the M pathway do show some color selectivity in they have red-dominant receptive field surrounds (Wiesel and Hubel, 1966; De Monasterio, 1978a. b; De Monasterio and Schein, 1980: Derrington. Lennie and Krauskopf. 1984; Livingstone and Hubel, 1984: Marroccco. McClurkin and Young, 1988). which may be the basis for tonic suppression of their response by diffuse red light (Wiesel and Hubel. 1966; Dreher et al., 1976; Krueger, 1977; Schiller and Malpeli. 1978). P cells also differ from M cells in their contrast sensitivity, with M cells having a lower contrast thresholds (Kaplan and Shapley, 1982; Hicks et al.. 1983; Derrington and Lennie, 1984; Tootell, Hamilton and Switkes. 1988a). Moreover, although individual M cells can have a spatial resolution as high as that of P cells (Hicks et al.. 1983; Crook et al., 1988). the P pathway is crucial for higher spatial resolution whereas the M pathway is not (Merigan and Eskin. 1986: Tootell et al., 1988~; Merigan. 1989: Schiller and Logothetis. in press; Schiller et al., 1990). Besides these color and spatial response differences, P and M cells also show temporal response differences. In addition to having a longer latency and a sustained as compared to transient response, P cells are characterized by a poorer temporal resolution in that they prefer slow flicker or motion whereas M cells are crucial in visual analysis of fast flicker and motion (Merigan and Eskin. 1986; Schiller and Logothetis, in press: Schiller et al.. 1990).

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The geniculate P and M pathway which begins at the retina with the B and A classes of ganglion cells, respectively (Leventhal. Rodieck and Dreher. 1981). branches into a t least three identifiable cortical pathways which have different laminar and tangential distributions as revealed by patterns of staining for cytochrome oxidase and deoxyglucose (Tootell et al., 1983, 1988a,b,c). In cortical area V1. the P pathway splits into two anatomically distinct, P-blob and P-interblob, streams of processing which in turn project via the thin and pale stripes of area V2 to V4 and subsequently to inferotemporal cortex. The separate cortical M pathway originates in V 1 and projects via V3 and the thick stripes of V2 to area MT and subsequently to the parietal cortex. Interaction exists between the cortical M and the two P pathways. In particular, V 3 projects not only to MT but also to V4. and moreover, V4 is anatomically linked with both area MT and the parietal areas (DeYoe and Van Essen, 1988: Desimone and Ungerleider, 1989). These three cortical streams of processing and their interactions are discussed in greater detail in several reviews and play a prominent role in current models of visual perception (Cavanagh, 1987. 1989a,b; Livingstone and Hubel, 1987, 1988; DeYoe and Van Essen. 1988; Desimone and Ungerleider. 1989; Ramachandran, 1990). While there is general agreement among the various theoretical models and empirical findings that the P and M pathways are closely tied to visual analysis of color and motion, respectively, there is disagreement regarding the specifics of this color/motion distinction as well as the roles of these pathways in the analysis of form and depth. To set the stage for discussion, the approach recently taken by Livingstone and Hubel (1987. 1988) will be outlined and compared to other approaches to visual perception also based on the M and P pathways. According to Livingstone and Hubel (1987, 1988). information about depth and movement appear to be processed mainly by the M pathway whereas information about form and color is processed predominantly by the P system (for similar views, see Ramachandran. 1990).However, they also make the important point that while color and certain high-resolution aspects of form information are processed by the P-blob and P-interblob systems, respectively, other low-resolution and Gestalt-linking aspects of form information are processed by the M system. Although Livingstone and Hubel (1987. 1988) qualify their proposal for distinct M- and P-pathway functions, some investigators suggest that Livingstone and Hubel have proposed a stronger distinction by claiming that " ... the M-cell system alone can support virtually all aspects of vision except for color, and that it provides the exclusive basis not only for motion perception, but also for stereopsis. perception of the three-dimensionality of objects based on perspective and shading, and most of the Gestalt phenomena of 'linking operations'. According to this model, the only contribution of the P-cell system to perception are color and a two-fold increase in the resolution of simple achromatic patterns" (Desimone and Ungerleider, 1989. p. 278). Regardless of whether claims are made for a predominant or an exclusive contribution of a given pathway to a perceptual function, it seems that Livingstone and Hubel's (1987. 1988) proposals are in need of some clarification and revision. The need stems from two considerations. One deals with the anatomical, physiological and psychophysical evidence supporting common as well as distinct roles of

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the M and P pathways in spatial and temporal vision: the other, with the use of isoluminant chromatic stimuli in humans (and monkeys) as a method of supposedly isolating P- from M-pathway functions in perception.

Evidence for shared and distinct spatial and temporal response properties of M and P pathways Based on a review of anatomical, physiological a n d psychophysical studies, DeYoe and Van Essen (1988) propose the following scheme. Although the P-blob pathway performs only analysis of color and the M pathway dominates motion perception, the M pathway has no exclusive or dominant role in stereopsis as proposed by Livingstone and Hubel (1987. 1988). According to DeYoe and Van Essen (1988). the P-interblob system, besides supporting color and form vision, also plays a crucial role in stereopsis. Since the P system additionally plays a critical role in high spatial resolution (Livingstone and Hubel. 1987,1988). one would in turn expect that its role in stereopsis is especially important for tasks requiring high resolution as suggested by DeYoe and Van Essen (1988). These differential roles of the M and P systems a s well as the role of the P system in high-resolution stereopsis has been corroborated by recent results reported by Schiller and co-workers (Schiller and Logothetis. in press; Schiller et al., 1990). These investigators looked a t the effects of selectively lesioning the P- or the M-cell layers of the LGN on the disruption of visual capacities in monkeys. Their findings indicate that the P pathway is essential for the processing of not only color, texture and fine pattern but also fine stereopsis while the M pathway is crucial for the perception of fast flicker and motion. Coarse shape discrimination and stereopsis could be supported by either pathway. Moreover, the P system was found to support flicker and motion perception at low temporal frequencies, indicating that the M pathway, in addition to not dominating all aspects of stereopsis. does not entirely dominate all aspects of flicker or motion perception. These spatiotemporal properties of the M and P pathways and their consequences for perception agree well with t h e updated psychophysical distinction between human transient and sustained channels mentioned above.

The roles of color and isoluminant stimuli in studies of parallel pathways The distinction between the processing of luminance and color has had an important impact on current theoretical and methodological developments in the study of visual perception (Anstis and Cavanagh. 1983; Livingstone and Hubel. 1987, 1988; Cavanagh, 1989a.b; Cavanagh and Mather, 1989; Ramachandran. 1990). However, the claimed effects of luminance and color on responses in the M and P pathways as well as the associated psychophysics in humans and monkeys provide grounds for significant controversy. The above models and findings (e.g., DeYoe and Van Essen, 1988: Schiller et al.. 1990) indicate that the color-opponent P pathway processes color information whereas the

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broad-band M pathway, except for color opponency shown in the receptive field surrounds of mainly type IV M cells (Wiesel and Hubel, 1966; Dreher et al., Krueger, 1977; Schiller and Malpeli. 1978; Livingstone and Hubel, 1984) does not. In view of this, isoluminant stimuli devoid of luminance variations but varying only in wavelength should be processed by the P but not the M pathway. Since the M pathway presumably is color blind, the perceptual functions which it critically supports should be those functions lost or severely compromised when isoluminant stimuli are used. This rationale has been used by several investigators (Livingstone and Hubel, 1987, 1988; Ramachandran. 1990) to supposedly isolate perceptual functions attributable to the P pathway from those attributable to the M pathway. There are several reasons for questioning the validity of such a rationale. Neither physiological nor psychophysical findings clearly support the use of isoluminant stimuli to distinguish M- from P-pathway function at early, precortical levels of visual analysis. Although some investigators report nulling of M-cell responses to isoluminant stimuli (Krueger. 1979; Hicks et al., 1983; Lee, Martin and Valberg, 1988, 1989 b,c) and a maintenance of P-cell responses to the same stimuli (Hicks et al.. 1983; Lee et al.. 1989b). others (Schiller and Colby. 1983) find the converse in that M cells could not be silenced a t any heterochromatic luminance ratios while many P cells, particularly those lacking color selectivity, could be silenced (Logothetis et al., 1990). Even those investigators who report silencing of M cells at isoluminance report that this does not hold under all conditions (Krueger, 1979; Lee et al.. 1988).As noted by Lee et al. (1989~1,a nonlinearity occurring at or before the summation of medium- and long-wavelength cone inputs to the M cells could provide a basis for their responses to red-green isoluminant borders. If responses to isoluminant stimuli occur in the M pathway at early levels of visual analysis, it would be reasonable also to expect such responses a t later cortical levels. Indeed, several investigators have reported responses of direction-selective cells in area MT to moving stimuli made of isoluminant-color or relative-motion borders (Albright. 1987; Charles and Logothetis, 1989; Saito et al.. in press). Even if a given M cell could be perfectly silenced a t isoluminance. among M cells there is significant variation of the luminance ratios at which isoluminance is obtained (Schiller and Colby. 1983; Derrington et al.. 1984; Logothetis et al., 1990). Hence, as noted by Cavanagh (1989b: Cavanagh and Anstis, 1986). in psychophysical studies no single luminance ratio would be expected to silence all cells and, thus, all activity in the M pathway. The residual perceptual abilities a t isoluminance could therefore be attributed to such a weakened residual response in the M pathway. However, a n alternative interpretation based on properties of cells in the P pathway is equally plausible. Schiller and Colby (1983) and Logothetis et al. (1990) report that many P cells also are unresponsive at isoluminance. indicating that impairment or compromise of visual capacities a t isoluminance cannot be attributed to only one of the two pathways. In particular, Logothetis et al. (1990) show that high-resolution form perception in monkey, which presumably can be ascribed to the P (interblob) system (Livingstone and Hubel. 1987, 1988). is compromised a t isoluminance, as are motion and depth perception, which presumably can be ascribed to the M pathway.

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In humans similar ambiguities and inconsistencies exist regarding visual performance with isoluminant stimuli. For instance, while Lu and Fender (1972) and Gregory (1977) found that depth perception was absent in isoluminant random-dot stereograms. de Weert and Sadza (1983)found that observers could judge depth in such stereograms. although their ability to do s o was impaired. On the assumption that the M pathway dominates stereopsis (Livingstone and Hubel. 1987, 19881, such residual abilities could be due to the aforementioned residual activity in the M pathway at isoluminance; however, as Schiller et a1.k (1990) findings suggest, they could also be due to the P pathway's contribution to the processing of random dot stereograms. Similar considerations apply when isoluminant stimuli eliminate or impair the perceptions of shape from shading, of shadow a s part of a spatially unbroken object or surface, of the related Gestalt-linking involved in the perception of subjective contours, and of static pictorial depth based on occlusion or perspective cues (Cavanagh. 1985, 1987. 1989b: Livingstone and Hubel, 1987, 1988; Cavanagh and Leclerc, 1989; Ingling and Grigsby. 1990; Ramachandran, 1990). The fact that the response of a substantial proportion of the P cells can be silenced or minimized at isoluminance (Logothetis et al.. 1990) makes claims such as Livingstone and Hubel's (1987, 1988) about an exclusive or predominant role of the M pathway in these perceptual functions questionable (see also Cavanagh. 1989a; Ingling and Grigsby, 1990). As another instance of ambiguities with the use of isoluminant stimuli, recall that the masking produced by the on- and offsets of a uniform luminance flash (Crawford, 1947) is found in the low spatial frequency transient channels but not the high spatial frequency sustained channels (Green. 1981, 1984). Since the transient M pathway supposedly does not respond well or at all to isoluminant wavelength or hue substitution. suddenly substituting one background hue for another equiluminant one should produce little or no masking of a test flash at the onset of the hue substitution. Although this is true when the background wavelengths differ from each other only slightly, large wavelength differences produce a powerful transient masking effect (Glass and Sternheim. 1973). Similar results hold when target and mask stimuli consisting of hue substitutions against a n isoluminant background are employed in metacontrast: when hue differences between stimuli and background are relatively small (e. g.. orange on white), little or no metacontrast is obtained (Bowen. Pokorny and Cacciato. 1977): however, when the differences are large (red on green), metacontrast is obtained (Reeves, 1981; Breitmeyer, May and Williams, 1989; Breitmeyer. May and Scott, in preparation). If isoluminance eliminated or severely weakened the response in the transient M pathway one should obtain no or only little onset-transient and metacontrast masking. The presence of these two types of masking effects a t isoluminance agrees with Schiller and Colby's (1983) and Derrington et a1.k (1984) finding that M cells are either not silenced at isoluminance or that no isoluminance value silences all M cells. Several lines of investigation have shown that the mechanisms underlying metacontrast may also contribute to motion perception in humans (Kahneman. 1967: Weisstein and Growney, 1969; Breitmeyer, Love and Wepman. 1974; Matin. 1975; Stoper and Banffy, 1977). If so,

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then based on the above findings one would expect motion perception to exist at isoluminance. Although Ramachandran and Gregory (1978) reported a n absence of motion perception in isoluminant random-dot cinematograms (RDCs; Julesz, 1971). subsequent investigations have shown that motion signals can be generated in such RDCs as well as other isoluminant moving stimuli (Cavanagh. Tyler and Favreau. 1984: Cavanagh. Boeglin and Favreau, 1985; Cavanagh and Favreau, 1985: Derrington and Badcock, 1985: Sato. 1988; Cavanagh, 1989b: Cavanagh and Mather, 1989). Cavanagh and Favreau (1985) and Derrington and Badcock (1985) argue on the basis of these findings that a common motion pathway receiving convergent input from luminance and color patterns exists in the human visual system. This is a plausible notion since a significant proportion of simple and complex cells in monkey striate cortex receive convergent inputs form M and P layers of the LGN (Malpeli, Schiller and Colby, 1981). However, the notion of such a common motion pathway in human vision has been challenged recently by Gorea and Papathomas (1989a.b). who propose instead that one can psychophysically identify a t least three distinct mechanisms, a luminance mechanism, a chromatic-plus-luminance mechanism, and a pure chromatic mechanism, each of which independently provides motion information. Further evidence for modulation of motion perception by the addition of color to luminance contrast has been reported in a number of recent studies. For instance, Logothetis et al. (1990) showed that monkeys‘ perceptions of motion and depth were enhanced when color contrasts were added to luminance contrasts. While Cavanagh and Favreau (1985) report that adding chromatic to a constant luminance contrast reduces its ability to generate or null motion after effects in human observers, other studies of humans (Ramachandran. Anstis and Rogers, 1987: Gorea and Papathomas, 1989b: Papathomas, Gorea and Julesz, 1989; Ramachandran. 1990) have shown that adding color to luminance contrast can resolve directional ambiguities in a number of directionally multistable apparent-motion (AM) displays. In addition, aspects of form such a s orientation (Green, 1986: Gorea and Papathomas, 1989 a.b; Mack et al., 1989) and texture (Ramachandran. Rao and Vidyasagar. 1973; Cavanagh. Arguin and von Gruenau. 1989) also can contribute to directional signals and disambiguition in AM displays. Rather than supporting the existence of a common motion pathway onto which form, color and motion information converge as suggested by some investigators (Cavanagh and Favreau. 1985; Derrington and Badcock, 1985; Cavanagh, 1989b). these effects of color or form on motion, a s alternatively proposed by Papathomas et al. (1989), could be due to interactions between the cortical M and P pathways (DeYoe and Van Essen, 1988; Desimone and Ungerleider, 1989). Such interactions may give rise to what DeYoe and Van Essen (1988) have termed a concealed or indirect contribution of color or form to, in this instance, motion perception or vice versa (Desimone and Ungerleider, 1989). They also could provide a basis of what Ramachandran (1987) terms “motion capture”. a phenomenon in which moving, luminance varying RDCs or illusory contours induce a sense of co-directional motion in a stationary isoluminant color border. In addition, they could explain the dependence of the perceived position of motion-segregated edges on the absence a n d presence of luminance-segregated edges (Anstis. 1989).

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An additional property of M neurons, mentioned previously, is the red- or long-wavelength-dominant surround mechanism characterizing many of their receptive fields (Wiesel and Hubel, 1966; De Monasterio, 1978a.b: De Monasterio and Schein, 1980: Livingstone and Hubel, 1984; Marrocco et al., 1982). This property may be the basis for the tonic suppression of activity in M-pathway neurons produced selectively by diffuse red light (Dreher et al., 1976: Livingstone and Hubel, 1984; Van Essen, 1985). Along with several collaborators I have recently looked at the implications of these findings for human psychophysics. Since a red background selectively suppresses the transient M pathway, one would predict, among other things, that stimuli presented against a red as compared to isoluminant green or neutral background should yield weaker metacontrast and motion a s well as longer reaction time to stimulus onset. So far each of these predictions h a s been confirmed (Breitmeyer et al.. 1989, in preparation; Breitmeyer and Williams, in press: Breier and Breitmeyer. in preparation). Of particular significance is the finding (Breitmeyer et al.. 1989, in preparation) that stimuli consisting of green hue substitutions 6n a n isoluminant red background yield weaker metacontrast and motion than red stimuli on green backgrounds. These asymmetries pose obvious problems for claims made by Kelly (1983, 1989) that a single pathway able to carry luminance a s well as opponent-color information, such a s the red-green X-cell channel proposed by Ingling and Martinez-Uriegas (1985). can fully account for spatiotemporal aspects of color vision. It is likely that further exploration of the suppressive effects of diffuse red light on M neurons will reveal additional properties of the M and P pathways and their respective contributions to spatial and temporal aspects of human vision.

Extensions of the parallel pathway approach

The control of visual orienting and attention In their discussion of possible functional aspects of the Y pathway in cat, Waessle. Peichl and Boycott (1981) suggest that any change occurring in the visual environment would initially be signalled by the transient and fast responding cells in that pathway. Hence, they could provide a system for triggering and directing visual orienting and attention. This is consistent with the projection of Y fibers to the superior colliculus (Hoffman, 1973) where, to use Schiller and Koerner's (1971) terminology, recipient Y cells could serve as "event detectors" signalling the events that trigger saccades and shifts of attention (Albano and Wurtz. 1981).In monkey, cells in the M pathway could serve a s event detectors since, as shown by Schiller and Colby (1983). they are particularly well suited by their fast and transient response for detection of any spatially localized change. This role of transient channels was incorporated into Breitmeyer and Ganz's (1976) parallel channel model and has been corroborated by a number of psychophysical studies showing the prepotency of abrupt onsets in triggering and controlling spatial attentional shifts (Todd and Van Gelder. 1979; Jonides, 1981; JSrumhansl. 1982; Yantis and Jonides,

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1984, 1990; Jonides and Yantis. 1988; Yantis and Johnson, in press). Moreover, it is consistent with a number of clinical studies implicating the tectal midbrain areas in triggering and directing the movement of spatial attention (Singer. Zihl and Poeppel. 1977; Zihl and von Cramon, 1979; Posner, Cohen and Rafal. 1982). Deployment of eye movements and spatially selective attention during inspection of the visual environment also requires the posterior parietal cortex, a major recipient site of M-pathway projections (Mountcastle, 1978; Lynch, 1980; Robinson, Bushnell and Goldberg, 1980; Bushnell, Goldberg and Robinson, 1981). Clinical studies of humans have also revealed the crucial role of the posterior parietal cortex in disengaging attention from a current target location so that it can be free to shift to another target locus (Posner et al.. 1984, 1987; Posner. 1988; Farah et al.. 1989; Petersen. Robinson and Cunie, 1989). Moreover, as suggested by Desimone and Ungerleider (1989) and Posner and Petersen (1990). the posterior parietal attentional system may effect spatial selectivity in ventral pattern recognition areas, such as V4 and IT (Desimone and Moran, 1985). via the interactive linkages between the dorsal M and the ventral P pathways. Posner and Petersen (1990) suggest that this particular interaction is communicated through the pulvinar of the thalamus (Petersen. Robinson and Morris, 1987), consistent with the finding that the pulvinar does modulate spatial selectivity of receptive fields in the ventral pattern recognition system (Gross, Bender and Rocha-Miranda. 1974).

The ventral/dorsal cortical streams of processing in object/spatial and farlnear vision Despite linkage between the M and P pathways (DeYoe and Van Essen, 1988; Desimone and Ungerleider. 1989). the two processing streams by and large take separate anatomical routes in visual cortex. The cortical M pathway originating in layer 4C-alpha of area V1 projects dorsally via layer 4B of V1 through area V3 and the thick stripes of area V2 to MT and additional areas in the superior temporal sulcus on its way to area PG in posterior parietal cortex. The cortical P pathway originating mainly in layer 4C-beta of area V1 projects ventrally along the P-blob and P-interblob routes via area V2 to area V4 on its way to area TE in inferotemporal cortex. Mishkin. Ungerleider and coworkers (Ungerleider and Mishkin. 1982; Mishkin et al.. 1983; Ungerleider. 1985; Desimone and Ungerleider, 1989) propose that the anatomically and physiologically distinguishable dorsal and ventral streams of processing comprise two functionally distinct cortical systems. Based on an extensive review of research on the differential impairments to vision produced by selective lesions of the two pathways in monkey and of related visual impairments associated with damage to parietal and temporal cortex in humans, they argue that the dorsal and ventral pathways support various aspects of spatial perception and object perception, respectively. The proposal that the visual system performs separate functions of spatial perception and object recognition is not new (Ingle. 1967; Held, 1968). However, the work of Mishkin. Ungerleider and coworkers elaborates and extends the proposal by showing that the two visual functions, originally relegated to the tectum and cortex, respectively (Schneider. 1967; Trevarthen, 1968). are

59 additionally supported by distinct cortical pathways. More recent investigations of intact a s well as brain-damaged humans not only support the existence of these two distinct cortical pathways (Zihl, Von Cramon and Mai. 1983; Hess. Baker and Zihl. 1989; Lueck et al.. 1989; Vaina, 1989) but also indicate cross-linkage between them (Vaina. 1989). A different proposal for the roles of the two pathways h a s recently been made by Previc (1990). Previc's (1990) proposal rests on review of anatomical, physiological, behavioral and clinical data suggesting anatomical and functional differences between the upper and lower visual field representations in the visual system. In particular, it is argued that the lower visual field is biased toward perception of near or "peripersonal" space whereas the upper visual field is biased toward perception of far or "extrapersonal" space. In so far as near space is involved with manipulative and consumatory behavior and f a r space is involved with exploratory and orienting behavior, this is somewhat of a departure from other schemes, e.g., Trevarthen (1978). in which visual space is partitioned into central focal vision concerned with object recognition and consumatory behavior and ambient peripheral vision concerned with spatial exploration and orientation. By implication, since focal vision is concerned with object recognition, one would expect the ventral P pathway to play a predominant role in near vision whereas the dorsal M pathway would be more crucial in ambient far vision. In contrast to this scheme, Previc (1990) argues that the functional differences between near and far visual space instead are correlated with the disproportionate representations of the lower and upper visual hemifields in the dorsal M and ventral P divisions of the visual association areas. Indeed. the dorsal M pathway in monkey cortex does show a bias not only toward lower hemifield representation (Van Essen. 1985; Maunsell, 1987) but also for near or crossed disparities (Maunsell and Van Essen, 1983; Komatsu, Roy and Wurtz, 1988),which, as hypothesized by Maunsell and Van Essen (1987) may be related to control of hand movements during reaching. Binocular neurons in the ventral P pathway seem to be tuned to stimuli in the fixation plane, i. e., at zero disparity (Burkhalter and Van Essen. 1986). These findings are consistent with the behavioral strategies of primates scanning and fixating objects to be visually identified before being grasped or manipulated by hands reaching along a trajectory typically found in the lower visual field. Similarly, as proposed by Levick (1977) and Pettigrew and Dreher (1987). in the cat the bias of the cortical Y system for crossed disparities may render it particularly useful for analysis of near space whereas the X system is more useful for analysis of objects in the fixation plane. Human vision also shows a bias for crossed disparities in the lower visual field and for uncrossed disparities in the upper visual field (Breitmeyer. Julesz and Kropfl. 1975; Julesz, Breitmeyer and Kropfl, 1976). Such biases would be consistent with Previc's (1990) proposal that the lower and upper fields are in turn biased toward perception of near and far space. However, as noted by Breitmeyer (in press: Breitmeyer, Battaglia and Bridge, 1976). the differences between the disparity biases of the upper and lower hemifields could additionally correlate with locomotion on a horizontal ground plane.

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Sustained and transient channels in reading and reading disability Possible roles of sustained and transient channels in dynamic vision characterized by a variety of eye movements have been discussed by several investigators (Breitmeyer, 1980, 1984: Barlow, 1981). In particular, it has been proposed (Matin. 1974: Breitmeyer. 1980. 1984; Volkmann. 1986) that the inhibition which the transient channels exert on sustained channels in metacontrast and, analogously, which Y cells exert on X cells (Singer and Bedworth. 1973) serves as a mechanism of saccadic suppression. Saccadic suppression clears the retinotopically organized sustained channels between fixations so that the pattern information carried by these channels from a prior fixation does not carry over and mask the pattern information picked up by the same channels during the succeeding fixation. Hence, by inhibiting the sustained channels' response persistence to pattern stimulation from a prior fixation, saccadic suppression expedites the pick-up of information during foveal scanning of spatially extended patterns such as reading material. In addition to this function, Matin (1974) notes that saccadic suppression also prevents the perception of retinal image smear during saccadic eye movements and, additionally, is important in maintaining constancy of visual direction and a stable visual world despite the continually changing retinal images while scanning. Over the past decade a series of studies reported separately by Bill Lovegrove and Mary Williams and their coworkers (see Lovegrove. Martin and Slaghuis. 1986: Williams and LeCluyse, 1990: Williams and Lovegrove. this volume) indicates that about 70% of dyslexic or specifically reading disabled (SRD)subjects suffer from a deficit in transient channel activity. Compared to normal subjects, SRDs have poorer temporal resolution as shown by lower flicker sensitivity and longer visual persistence to low spatial frequency stimuli (Lovegrove et al., 1986: Williams and LeCluyse. 1990) as well as poorer double-flash temporal order judgments (Williams and LeCluyse, 1990). More significantly. as expected from a transient channel deficit, SRDs also show a pronounced attenuation of metacontrast (Williams and LeCluyse, 1990). These findings clearly are relevant to our understanding of SRD. They indicate that saccadic suppression is substantially weaker in SRD than in normal subjects. Although data relying on direct experimental tests of this conjecture are needed, I would like to follow up some of its consequences. First, a weaker saccadic suppression would result in greater persistence of pattern activity generated during a prior fixation. Relative to similar activity generated by the following fixation, this would constitute a source of noise impeding or masking efficient pick-up of sequentially scanned information. In reading tasks, weaker saccadic suppression would thus contribute to a primary visual deficit in SRD subjects. Moreover, following Matin's (1974) reasoning, defective saccadic suppression also would lead to an interrelated set of secondary visual problems in SRD. including retinal image smear, a loss of visual direction constancy, and instability of the visual world. Such deficits have been reported to exist in about 60-70% of dyslexic subjects studied by Stein, Riddell and Fowler (1989). which is also the percentage of transient channel deficits reported to exist in SRDs by

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Lovegrove et al. (1986). Further research is required to determine if this concordance is mere coincidence or reflects a common basis as conjectured here.

Applications of sustained and transient channels to the study of psychological abnormalities Previously I noted that the distinction between sustained, form/pattern channels and transient, flicker/motion channels already has found application to the study of visual abnormalities in multiple sclerosis and other ophthalmological abnormalities such as open-angle glaucoma, ocular hypertension, and optic neuritis (Enoch. 1978; Brussell et al., 1984: Regan and Neima, 1984: Silverman et al., 1990; Ghilardi et al., this volume). In recent years a number of investigators also have reported deficits of visual information processing in schizophrenic and schizotypal subjects (Steronko and Woods, 1978: Saccuzzo and Schubert. 1981: Merritt and Balogh. 1990. in press: Balogh and Merritt, 1985, 1987; Nakano and Saccuzzo. 1985). Specifically, Merritt and Balogh (1990, in press) present and review evidence based on backward masking which is consistent with the hypothesis that schizotypal subjects are characterized by aberrant transient channel activity. However, although these preliminary findings are intriguing and suggestive, the extent to and manner in which transient activity in schizophrenics and schizotypics is abnormal must, a s noted by Merritt and Balogh (1990). still be determined.

Summary and conclusions Although several loosely related lines of research on parallel pathways in human vision can be traced back for decades, it was the discovery of X and Y cells in cat in the 1960s that stimulated a n acceleration of psychophysical investigations specifically focused on defining the properties of analogous pathways in humans. Most of the early research was framed in the context of explicitly a s well as implicitly articulated distinctions hypothesized to exist between sustained and transient channels. These distinctions were incorporated into models of spatiotemporal vision, visual information processing and visual masking. Although a significant portion of this research was subsequently criticized on theoretical and methodological grounds, the main tenets on which the distinctions were based have survived in revised form incorporating some of the major theoretical criticisms and more recent empirical clarifications and elaborations. The revisions of the sustained-transient channel approach have been accompanied by a shift from drawing analogies with the X and Y pathways of cat to more recent analogies with the opponent-color P and broad-band M pathways in monkey. The latter development h a s broadened the psychophysically defined distinctions between parallel pathways in human vision by including, along with temporal and spatial response differences, differences of chromatic sensitivity. These distinctions in t u r n have been criticized on theoretical and methodological grounds and are in need of revision. Nonetheless, they have provided and, in revised form, can continue to provide a useful

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framework for investigating a number of visual functions such as the perceptions of form, color, depth and motion in humans. They also are closely related to recent distinctions made between pathways for object recognition and spatial vision and similarly for visual function in near (peripersonal) and f a r (extrapersonal) space. Moreover, extensions of the parallel-channels approach help inform u s about a number of other phenomena such as selective spatial attention and reading, and they provide a means of investigating a number of visual abnormalities associated with specific reading disability, ophthalmological disorders, and, possibly, also schizophrenia.

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Bolz, J., Rosner. G. & Waessle, H. (1982).Response latency of brisk-sustained (XI and brisk-transient (Y) cells in the cat retina. Journal of Physiology, 328, 171 - 190. Bowen. R. W., Pokorny. J. & Cacciato. D. (1977).Metacontrast masking depends on luminance transients. Vision Research, 17. 971-975. Bowker. D. 0. & Tulunay-Keesey, U . (1983). Sensitivity to countermodulating gratings following spatiotemporal adaptation. Journal of the Optical Society of America, 73. 427-435. Breier. J. & Breitmeyer, B. G. (in preparation). Effects of isoluminant-background color on visual reaction time and bistable motion. Breitmeyer, B. G. (1975).Simple reaction time as a measure of the temporal response properties of transient and sustained channels. Vision Research, 15. 1411-1412. Breitmeyer. B. G. (1978).Disinhibition of metacontrast masking of Vernier acuity targets: Sustained channels inhibit transient channels. Vision Research, 18, 1401-1405. Breitmeyer, B. G. (1980).Unmasking visual masking: A look at the 'why' behind the veil of the 'how'. Psychological Review, 87. 52-69. Breitmeyer, B. G. (1984).Visual Masking: An Integrated Approach. New York: Oxford University Press. Breitmeyer. B. G. (1990).Ups and downs of the visual field: 'Manipulation and locomotion. Behavioral and Brain Sciences, 13,544545. Breitmeyer. B., Battaglia, F. & Bridge, J. (1976).Existence and implications of a tilted binocular disparity space. Perception, 6. 161 - 164. Breitmeyer. B. G. & Ganz. L. (1976): Implications of sustained and transient channels for theories of visual pattern masking, saccadic suppression, and information processing. Psychological Review , 83. 1-36. Breitmeyer, B. G. & Ganz. L. (1977).Temporal studies with flashed gratings: Inferences about human transient and sustained channels. Vision Research, 17. 861-865. Breitmeyer. B. G. & Julesz, B. (1975). The role of on and off transients in determining the psychophysical spatial frequency response. Vision Research, 15,41 1-415. Breitmeyer, B. G..Julesz. B. & Kropfl, W. (1975).Dynamic random-dot stereograms reveal up-down anisotropy and left-right isotropy between cortical hemifields. Science, 187. 269-270. Breitmeyer, B. G.. Levi, D. M. & Harwerth. R. S. (1981a). Flicker-masking in spatial vision. Vision Research, 21, 1377-1385. Breitmeyer. B. G.. Love. R. & Wepman. B. (1974).Contour suppression during stroboscopic motion and metacontrast. Vision Research, 14. 1451- 1456. Breitmeyer, B. G., May, J. G. 81 Williams, M. C. (1989). Asymmetries in metacontrast and motion with red/green isoluminant stimuli. Paper presented at the annual meeting of the Psychonomic Society, Atlanta, Georgia, November 17-19. Breitmeyer, B. G.. May. J. G. & Scott, S.(in preparation). Metacontrast and motion reveal asymmetries at red/green isoluminance. Breitmeyer, B. G.. Rudd. M. & Dunn, K. (1981b).Spatial and temporal

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function in developmental dyslexia. In C. Von Euler, I. Lundberg & G. Lennerstrand (Eds.) Brain and Reading, pp. 139-157. New York: Stockton Press. Steronko, R. J. & Woods, D. J. (1978). Impairment in early stages of visual information processing in nonpsychotic schizotypic individuals. J o ~ n a Ol f Abnormal Psychology, 87,48 1-490. Stigler. R. (1910). Chronotouische S t u d i e n ueber d e n Ukgebungskontrast. Pfluegef s Archiv der gesamten Physiologie, 135, 365-435. Stone, J. (1983). Parallel Processing in the Visual System New York: Plenum. Stone, J. & Dreher, B. (1973). Projection of X- and Y-cells of the cat's lateral geniculate nucleus to areas 17 and 18 of visual cortex. Journal of Neurophysiology, 36, 551-567. Stone, J.. Dreher, B. & Leventhal, A. G. (1979). Hierachical and parallel mechanisms in the organization of the visual cortex. BrainResearch Review, 1. 345-394. Stoper. A. E. & Banffy. S . (1977). Relation of split apparent motion to metacontrast. Journal of Experimental Psychology: Human Perception and Performance, 3, 21 1-227. Stromeyer, C.. Klein. S . , Dawson. B. & Spillmann, L. (1982). Low spatial-frequency channels in human vision: Adaptation and masking. VisionResearch, 22. 225-234. Stromeyer. C.. Zeevi, Y. & Klein. S. (1979). Response of visual mechanisms to stimulus onsets and offsets. Journal of the Optical Society of America, 69. 1350-1354. Teller, D. Y. (1980). Locus questions in visual science. In C. S . Harris (Ed.) Visual Coding and Adaptability, pp. 151- 176. Hillsdale. New Jersey: Erlbaum. Teller, D. Y. (1984). Linking propositions. Vision Research, 24. 1233-1246. Todd, J. T. & Van Gelder, P. (1979). Implications of a transient-sustained dichotomy for the measurement of human performance. Journal of Experimental Psychology: Human Perception and Performance, 5 . 625-638. Tolhurst, D. J . (1973). Separate channels for the analysis of the shape and movement of a moving stimulus. Journal of Physiology, 231. 385-402. Tolhurst, D. J . (1975a). Reaction times in the detection of gratings by human observers: A probabilistic mechanism. Vision Research, 15, 1143-1149. Tolhurst, D. J. (1975b). Sustained and transient channels in human vision. Vision Research, 15. 1151-1155. Tolhurst. D. J. & Movshon, J. A. (1975). Spatial and temporal contrast sensitivity of striate cortical neurones. Nature, 257,674-675. Tootell. R. B. H., Hamilton, S . L. & Switkes, E. (1988b). Functional anatomy of macaque striate cortex. IV. Contrast and magno-parvo streams. Journal of Neuroscience, 8, 1594- 1609. Tootell. R. B. H., Silverman, M. S . & De Valois, R. L. (1983). Topography of cytochrome oxidase patterns in extrastriate cortex of the owl monkey. Society for Neuroscience Abstracts, 7,356. Tootell. R. B. H., Silverman. M. S . . Hamilton, S . L.. De Valois. R. L. & Switkes, E. (1988a). Functional anatomy of macaque striate cortex. 111. Color. Journal of Neuroscience. 8. 1569-1593.

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ganglion cells produced by changes in background illumination. Paper presented at the annual meeting of the Association for Research in Vision and Ophthalmology, Sarasota, Florida, April. Zeki. S. M. (1978).Functional specialization in the visual cortex of the rhesus monkey. Nature, 274, 423-428. Zihl, J. & von Cramon. D. (1979). The contribution of the 'second' visual system to directed visual attention in man. Brain,102. 835-856. Zihl. J., von Cramon, D. & Mai. N. (1983).Selective disturbance of movement vision after bilateral brain damage. Brain, 106. 313-340.

Parallel Processing and Visual Development


Applications of Parallel hocessing in Vision J. Brannan (Editor) 0 1992 Elsevier Science Publishers B.V. All rights reserved

81

Parallel Processes in Human Visual Development ADFUANA FIORENTINI

Introduction It has long been known that the human visual system is largely immature at birth, but until some twenty years ago not much was known about the visual functional properties of the newborn. or about the rate at which the visual system develops in the early period of infant life. The introduction of behavioral and electrophysiological techniques that could successfully be applied to study infant visual capacities has considerably increased our knowledge of the visual improvement that occurs after birth. A number of papers have appeared that review recent achievements in this field (for instance Aslin, 1987; Atkinson and Braddick. in press: Banks and Dannemiller, 1987; Gwiazda et al., 1989a; Teller and Bornstein. 1987). Only recently, however. it has become apparent that the time course of visual development may be quite different for different aspects of vision, even during the first year of life. This fact may reflect the different rates of maturation of classes of neurons which process in parallel various aspects of visual information. Unfortunately it is often impossible to assign the result of a human developmental study, either psychophysical or electrophysiological, to the maturation of a specific neural structure. In addition one has to take into account that visual development occurs both serially, a t various peripheral and central levels, and in parallel for various visual functions. In some cases the factors that limit infant vision are imposed in the eye by the physical and anatomical properties of the photoreceptors. b u t further constraints derive from immaturities of the neural structures in the retina and/or in the brain. In this chapter some recent findings are reviewed which provide the opportunity to speculate about the development of parallel neural pathways in the human visual system both a t peripheral and at central levels. Some inferences will be made regarding the possible contribution of the two major neural streams of the primate visual system, the parvocellular (P) and magnocellular (MIpathways, to some properties of infant vision and of its improvement in the early life period.

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Structural development The infant visual system undergoes profound structural changes in the early postnatal period. Some developmental modification continues during childhood (see Hickey and Peduzzi, 1987,for a recent review). Apart from an obvious increase in the size of the eyeball, there is in the retina a long maturation process, mainly in the macular region (Yuodelis and Hendrickson. 1986). The cones increase dramatically in length after birth and become increasingly thinner and more closely packed in the very center of the macula. At the same time the ganglion cells, a t birth still present in front of the receptors even in the center of the retina, migrate to occupy more eccentric positions allowing the foveal pit to take its adult shape. This process takes a few years to complete. Similar modifications have been reported to occur in the retina of macaque monkeys (Hendrickson and Kupfer, 1976). The optic nerve fibers, almost completely unmyelinated a t birth, acquire a myelin sheet that increases progressively in width. This process proceeds from the orbital portion of the nerve towards the eye. Almost all fibers are myelinated by 7 months of age, but the width of the myelin sheet continues to increase thereafter, especially during the first two years of life (Magoon and Robb, 1981). The Lateral Geniculate Nucleus (LGN)is structurally adultlike at birth, clearly differentiated into six layers, with two magnocellular ventral layers and four parvocellular dorsal layers (Hickey and Guillery, 1979). The cell bodies of the newborn are considerably smaller than those of the adult, both in the ventral and dorsal layers, and about two years are required to complete the process of cell body growth in the human LGN (Hickey, 1977). The rate of maturation is different in the parvo and magnocellular layers: while cells in the parvocellular layers (P cells) approach adult size by the end of the sixth month post term. those of the magnocellular layers (M cells) do not reach a comparable development until the end of the first year. However, the dendritic morphology of LGN cells seems to be mature by the end of the ninth month, both in the parvo and magnocellular layers (Garey and de Courten. 1983). Not much is known about the structural development of the human visual cortex in infancy. Synaptic density increases considerably from around two months after term till around eight months, when it reaches its maximum. Thereafter the number of synapses decreases. to stabilize at about eleven years (Garey and de Courten, 1983). A postnatal growth of dendritic branching has been described in layers 3 and 5 of the striate cortex, with layer 5 neurons maturing earlier (within 5 months from birth) than layer 3 neurons (Becker et al.. 1984). The latter take about two years to complete maturation. There is also some evidence that intracortical horizontal connections between columns develop mainly after birth (Burkhalter and Bernardo. 1989). One of the more important modifications functionally, which is known to occur in the striate cortex of infant monkeys, is the segregation of monocular LGN inputs to layer 4C. underlying the formation of ocular dominance columns. At birth the inputs from the two eyes overlap extensively in layer 4C while in the adult macaque

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monkey there is almost complete segregation (Hubel et al., 1977). Ocular dominance columns are known to be present in the human visual cortex, where they form a pattern similar to the monkey, although the single columns are considerably wider in the human adult than in the macaque (Horton and Hedley-Whyte, 1984). There is some evidence that ocular dominance columns in the human cortex form during the first six months of life. The columns have been found to be well formed in the cortex of 6 month old infants, but only poorly defined in the brain of a 4 month old infant (Hickey and Peduzzi, 1987: Horton and Hedley-Whyte, 1984).

Spatial characteristics: central vision The spatial characteristics of the adult visual system are best described by the contrast sensitivity function (CSF). which relates contrast sensitivity, Le., the reciprocal of the contrast threshold for resolving sinusoidal gratings, to stimulus spatial frequency (Campbell and Robson. 1968). Contrast thresholds can b e evaluated psychophysically or can be extrapolated from visual evoked potentials WEP) (Campbell and Maffei. 1970). A

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Figure 1. A Contrast sensitivity functions obtained from VEP responses to contrast-reversed sinusoidal gratings in one infant at three ages (in months) and in one adult subject (from Pirchio et al.. 1978). Mean luminance: 7 cd/m2; square-wave contrast reversal: 8 Hz. B: Average contrast sensitivity curves of infants of different ages obtained behaviourally with the preferential looking technique. Stimulus: stationary gratings, mean luminance 55 cd/m2. Both psychophysical and electrophysiological methods have been applied to study contrast sensitivity of newborns and its development in early life period (see Banks and Dannemiller. 1987. and Mohn and van Hof-van Duin. in press, for recent reviews). The two methods agree in showing that contrast sensitivity is poor in very young infants, and restricted to a band of low spatial frequencies

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(Figure 1, A and B) (Atkinson et al.. 1977: Banks and Salapatek, 1978; Pirchio et al., 1978; Norcia et al. 1988, 1990). During the first six months of life there is a rapid increase in contrast sensitivity, especially a t medium to high spatial frequencies, with a related improvement in visual acuity and a n increase in the optimal spatial frequency (Figure 1. A). Contrast sensitivity at low spatial frequencies (below 1 c/degl remains relatively unchanged with age. Similar findings have been obtained behaviorally in infant monkeys (Boothe et al.. 1980 and 1988). although the time scale of development is different between the two species: one postnatal week for the monkey corresponds to about 4 weeks for the human infant. In spite of the qualitative agreement between the behavioral and the VEP findings on age related changes in the CSF, there are large quantitative differences among the available sets of data. In particular, VEP contrast sensitivities evaluated recently by Norcia et al. (1988,1990)with the swept-contrast technique (Norcia et al., 1985) are much higher than those obtained by others in VEP experiments (Pirchio et al.. 1978; Morrone and Burr, 1986; Atkinson and Braddick, 1989) or using behavioral techniques (Atkinson et al.. 1974; 1977; Banks and Salapatek. 1978). I t is not clear why the swept-contrast technique yields peak contrast sensitivities that consistently exceed those obtained with other methods: psychophysical thresholds coincide with VEP thresholds obtained in the same infant with the Campbell and Maffei ( 1970) extrapolation technique (Atkinson and Braddick. 1989). One possibility is that the function relating VEP amplitude to log contrast in infants is composed of two regression lines of different slopes and that the swept-contrast technique extrapolates to the lower threshold. The two regression lines could represent the activity of two populations of neurons with different contrast sensitivity and contrast gain as described in the monkey (see Kaplan et al., 1990, for review). Other discrepancies can be ascribed to differences in the temporal properties of the stimuli: stationary stimuli were used in two behavioral experiments (Atkinson et al.. 1977; Banks and Salapatek, 1978) and contrast reversal stimuli in the VEP experiments. A temporal modulation of stimulus contrast can facilitate the detection of low spatial frequency stimuli (thus reducing or eliminating the low-frequency fall off). but impair the detectability of high spatial frequencies. If the same temporally modulated stimuli are used in the same infant, the contrast thresholds evaluated behaviorally and with the VEP contrast extrapolation technique coincide (Atkinson and Braddick, 1989). Differences in optimal contrast sensitivity can also be due to differences in mean luminance of the stimuli employed in different experiments: optimal contrast sensitivity can be expected to increase in proportion to the square root of mean luminance in the photopic range and it does so in the adult. The high contrast sensitivities reported by Norcia et al. (1990) have been obtained at luminances exceeding 200 cd/m2, while most of the previous experiments employed luminances of 10 cd/m2 or less. Early behavioral studies on human infants (Atkinson et al., 1977; Banks and Salapatek. 1978) seemed also to indicate that the CSF of one month olds is a low-pass function and that the low-frequency fall off

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typical of adult CSFs shows up later and becomes steeper with age. The adult CSF is thought to result from the sum of several detecting mechanisms with narrower tuning curves and different preferred spatial frequency (see Braddick et al., 1978. for review). The change in the shape of the infant CSF with age has accordingly been ascribed to the progressive maturation of detectors tuned to higher and higher spatial frequencies. This would be accompanied by an increase in contrast sensitivity of the low spatial frequency detectors present already at an early age and possibly by a change from low-pass to band-pass tuning properties. The low-pass shape of the neonatal CSF. however, seems not to be a firmly established fact, a t least for stationary stimuli. [For temporally modulated stimuli, a s typically employed in VEP experiments, the adult CSF has little or no low-frequency decline (Robson, 19661.1 Note that the infant curves of Figure 1A represent VEP amplitudes normalized a t peak contrast sensitivity. No low-frequency fall off has been found in CSF curves obtained by Norcia et al. (1988, 1990) from VEP extrapolated thresholds (see Figure 4. squares) Movshon and Kiorpes (1988) have reanalyzed contrast sensitivity data of human and monkey infants for stationary stimuli and have argued that the reported change in the shape of the CSF with age is probably a n artifact due to group-averaging. By separately analyzing the CSFs of single subjects of the same age they come to the conclusion that the data can be fitted by a function of constant shape, at each age, and that in order to fit the data at different ages it is sufficient to shift the function horizontally and vertically in a log-log plot. If so, it would be unnecessary to invoke the differential development of mechanisms tuned at different spatial frequencies. The development would consist of a scale change brought about primarily by the increase in focal length of the eye and by the change in the spacing of the foveal cones, accompanied by an increase in sensitivity. A similar hypothesis has been advanced by Wilson (1988). who assumes that the development of cortical inhibition also plays a role in sharpening the spatial frequency tuning of single detectors. During infant development, retinal and cortical acuity appear to have a common limiting factor. This is shown by the data reported in Figure 2. The acuities reported in this figure were evaluated from pattern electroretinograms (PERG) and pattern VEPs recorded simultaneously in infants two to six months old. PERG acuities (Figure 2. open symbols) improve with age in parallel with the improvement of acuities extrapolated from VEPs (Figure 2. closed symbols) (Fiorentini et al., 1984). It is generally accepted that limits to visual acuity in infants are mainly imposed by the maturational state of the fovea, and in particular of the foveal cones (Banks and Bennett, 1988: Wilson, 1988; Brown et al.. 1987). although there is no agreement about whether the size and spacing of cones is the only limiting factor. The disagreement derives from slightly different hypotheses on the quantum efficiency of cones in the infant retina. It is difficult at present to resolve this controversial point, because of the few anatomical data available of infant human retinae. Therefore one h a s to consider the possibility that postreceptoral factors also contribute to limit visual acuity, either in the

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retina or in the brain, or both. The data of Figure 2 indicate that postretinal developmental processes possibly involved in the improvement of spatial resolution proceed at the same rate as retinal development during the first six month of life.

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Figure 2. Infant acuities estimated from pattern ERG (open symbols) and VEP (closed symbols) in nine infants. Different symbols represent different subjects. Stimulus: sinusoidal gratings, mean luminance 50 cd/m2, contrast 50%, square-wave contrgst reversal: 6 Hz. Pattern-reversal VEPs are believed to reflect the activity of cortical neurons. In adults, the amplitude of the potentials in response to gratings depend upon the orientation of the grating: it is larger for vertical and horizontal gratings than for oblique gratings (Maffei and Campbell, 1970). This oblique effect is present also in infants starting from 3 months from birth (Sokol et al.. 1987). Since retinal and geniculate neurons of monkeys are not selective for orientation, it is generally assumed that orientational effects in human visual responses indicate cortical processes. Thus, it seems very likely that at three months of age, and possibly before, pattern-reversal VEPs reflect at least in part the activity of cortical neurons and not merely the LGN input to the visual cortex. If so, then the similar trend in the improvement of acuity evaluated from pattern ERG and VEP indicates that acuity of cortical neurons does not lag behind retinal development of acuity. This is consistent with findings on the monkey reported next. In the monkey LGN. the "acuity" of single cells in the foveal representation is low at birth, not exceeding 5 c/deg. During the first

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year of life there is a gradual increase in the spatial resolution of foveal LGN cells (both in the parvo and magnocellular layers) until the mean "acuity" and the "acuity" of the best cells reach adult values of about 30 c/deg (Blakemore and Vital-Durand. 1986). The changes in spatial resolution of LGN cells seem to be related to a progressive decrease in the size of receptive field centers. Interestingly, the spatial resolution of cells in the monkey striate cortex also improves with age, and the improvement in the cortex parallels the improvement in the LGN (Blakemore and Vital-Durand, 1983).Behavioral visual acuity of infant monkeys (Teller et al., 1978; Boothe et al., 1988) increases at a slightly lower rate compared with the acuity of the best cells during the first three months from birth (Jacobs and Blakemore. 1988). Thus in the infant monkey, like in human infants, the development of cortical acuity seems to not lag behind the improvement proceeding at a more peripheral stage in the visual pathway. No data are available so far for the functional development of the retinal ganglion cells of infant monkeys. It has to be noted that in the LGN of the adult monkey, those M cells that show linear spatial summation seem to have similar spatial resolution (on average) as P cells, although cells with the highest acuities (exceeding 25 c/deg) may be more numerous in parvocellular t h a n in magnocellular layers (Blakemore a n d Vital-Durand, 1986). In the parafoveal region of the monkey retina, ganglion cells with sustained response properties seem not to exceed in acuity the resolution of phasic cells (Crook et al., 1988). which project almost exclusively to the magnocellular layers of the LGN. On the other hand, experiments on monkeys with selective degeneration of P cells suggest that the integrity of the P pathway is crucial for reaching a normal behavioral acuity (Merigan and Eskin. 1986; Merigan, 1989: Schiller et al.. 1990). In the newborn monkey the limits to optimal acuity are largely imposed by peripheral factors. The full development of foveal acuity takes a relatively long time in the monkey, as in humans. If the P pathway is mainly responsible for visual acuity in adult monkeys, it is reasonable to assume that in so far as the improvement in acuity reflects changes in the retino-cortical pathway, these changes should eventually involve the P system. As to the contrast sensitivity of P and M cells in infant monkeys. the data available s o far in the literature (Blakemore and Hawken, 1985) indicate that in the LGN the peak contrast sensitivity of the most sensitive P cells approaches adult values even in the neonate. The best M cells are more sensitive than the best P cells, but the difference is less marked than in the adult. Thus, cells in the magnocellular layers must undergo a relatively greater increase in contrast sensitivity during development than cells in the parvocellular layers. These findings might have a bearing on human visual development, as will be discussed at the end of this chapter.

Spatial characteristics: eccentric vision Static and kinetic perimetry show that the visual field of the young infant is small, compared with the adult. In the human newborn the orienting reaction to an object introduced in its peripheral visual

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field is restricted horizontally to within 20 - 30 deg from the fixation point and the vertical visual field is even narrower. The s u e of the visual field remains practically unchanged during the first two months of life (Schwartz et al.. 1987). then increases rapidly to approach adult levels by the end of the first year (see Mohn and Van Hof-Van Duin. in press). Morphologically, the extrafoveal retina of the newborn is relatively more mature than the fovea and its development seems to be complete by the end of the first year of life (Abramov et a1.,1982; Drucker and Hendrickson, 1989). There is unequivocal evidence, however, that peripheral spatial resolution improves after birth (Spinelli et al.. 1983; Sireteanu et al.. 1984; Sireteanu et al.. 19881, rapidly during the first 3 - 4 months and then more slowly. By 3 months of age, but not earlier, acuity is better in the temporal than in the nasal visual field at 20 deg eccentricity (Courage and Adams. 1990) as it is in adults (Rovamo and Virsu, 1979). In the LGN of the adult monkey, spatial resolution of P and M cell declines with eccentricity (Blakemore and Vital-Durand. 1986).At each eccentricity the mean resolution of X-type P and M cells (those that show linear spatial summation) are similar, while Y-type M cells (with non-linear spatial summation) have lower resolution (Blakemore and Vital-Durand. 1986). It seems therefore that the acuity of single neurons depends more on the functional properties of their receptive field (linear vs non-linear summation) than on the P - M classification. On the other hand one has to consider that the retinal ganglion cells that project to the parvocellular LGN layers (defined morphologically as P-beta cells) form the large majority of ganglion cells, while the cells that project to the magnocellular layers (P-alpha cells), are only lW?o of the total population (Perry and Cowey, 1985). Thus the sampling density of P cells largely exceeds that of M cells, and this may assign a predominant role in pattern resolution to the P system. In the newborn monkey, resolution of U ; N cells varies little with eccentricity. The subsequent improvement in resolution with age is prominent in the foveal and parafoveal LGN region, but small at larger eccentricities (Blakemore and Vital-Durand, 1986). This compares well with the larger increase in visual acuity for central vision than for peripheral vision in human infants during the first year (see above).

Temporal characteristics The temporal characteristics of infant vision have not been extensively investigated. Regal (1981) evaluated behaviorally the critical fusion frequency of infants by a forced-choice preferential looking (FPL) method (Teller, 1979). The stimulus was a uniform field square-wave modulated in luminance a t various temporal frequencies, to be discriminated from a non-modulated field of the same mean luminance. The critical fusion frequency (highest discriminable frequency of modulation) was found to increase with age after birth and to reach adult values within three months of age. This is an interesting finding. since in the monkey the sensitivity for fast flickering lights seems to be subserved by the M system (Schiller et al., 1990). More important for vision in a natural environment is the sensitivity to a temporal modulation of contrast in pattern stimuli.


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There has been so far no systematic study of the development of spatio-temporal contrast sensitivity in infants. Some preliminary reports indicate that contrast sensitivity for a fixed spatial frequency is highly dependent upon the temporal frequency modulation of the pattern contrast. The temporal contrast sensitivity function of young infants, however, differs from the adult function, having both lower peak sensitivity and lower optimal frequency. Moreover, the low-frequency fall off in sensitivity characteristic of adult functions does not appear until 3 - 4 months of age (Hartmann and Banks, 1984; Swanson and Birch, 1989). Again, it is of interest to investigate whether the temporal characteristics of the neonatal visual system are constrained mainly at a retinal or at a higher level. Some information can be obtained from simultaneous recording of the pattern ERG and VEP (Fiorentini and Trimarchi, 1989). Temporal resolution evaluated from the PERG for gratings of low spatial frequency (0.5 c/deg) sinusoidally reversed in contrast, improves with age between 2 and 5 months of age, as it does for the pattern VEP. The function relating PERG amplitude to temporal frequency of contrast reversal is practically low-pass at 6 weeks of age and tends to become more band pass between 2 and 5 months from birth. The same is true for the temporal tuning function of the pattern VEP (Moskovitz and Sokol, 1980). [It has to be noted that these functions do not describe contrast sensitivity, but the dependence of response amplitude from temporal frequency for a constant stimulus contrast.] At each age there is a tendency for the PERG to peak at a higher frequency and to have a hlgher temporal resolution than the pattern VEP (Fiorentini and Trimarchi. 1989) as occurs for the adult (Plant, Hess and Thomas, 1986). Thus the development of temporal frequency characteristics for contrast reversal seems to be constrained by postretinal limiting factors, in addition to the limits imposed by retinal immaturity. If we had better knowledge of the complete spatio-temporal CSF in infants and of its changes with age, it would be possible to compare the development of sensitivity for temporal contrast modulation with the development of visual acuity. This might be relevant to the question of possible differential development of P and M pathways. In view of the findings obtained from behaving monkeys with selective destruction of P-beta ganglion cells (Merigan and Eskin. 1986: Merigan. 1989) and also on t h e basis of electrophysiological properties of P and M cells, there seems to be general consent that contrast sensitivity for temporally modulated patterns of low spatial frequencies is subserved by M cells, while spatial resolution tasks are mediated by P cells (Kaplan et al., 1990: Lennie et al., 1989). Unfortunately the developmental data about temporal frequency characteristics available so far are still incomplete. The data obtained from VEP experiments which typically employ gratings reversed in contrast at 5-8 Hz. indicate that contrast sensitivity for low spatial frequencies matures quite early compared with spatial resolution (Pirchio et al.. 1978. Norcia et al., 1990). It would be of interest to know how these flndings compare with the development of contrast sensitivity at low spatial frequencies for stationary patterns, but the data on psychophysical CSF available so far cover only the earliest postnatal months (Atkinson et al., 1977;

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Banks and Salapatek, 1978) or a much later range of preschool ages (Beazley et al.. 1980; Atkinson et al.. 1981). At what age the CSF for stationary stimuli is fully developed is still unknown. Several studies have been devoted to the development of VEP responses to transient contrast reversal. In the adult, these transient VEPs have a rather complex waveform, with a main positive deflection that peaks with a delay of about 100-110 ms with respect to stimulus reversal. In the newborn infant, the waveform is much simpler and the positive wave peaks with a much longer delay (around 250 ms or more). The peak latency shortens rapidly after birth and for checkerboard patterns with large checks it levels off at adult values towards the end of the first year. For small checks the peak latency decreases at a lower rate and takes longer to reach adult values (Moskowitz and Sokol, 1980). 300

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AGE (weeks) Figure 3. Peak latency of the pattern VEP (solid symbols) and ERG (open and stippled symbols) as a function of age. Different symbols represent different subjects. Stimulus: sinusoidal grating, 0.5 c/deg, contrast 50%. square-wave reversed in contrast a t 1 Hz, mean luminance 50 cd/m2. The long latencies observed in the transient VEPs of young infants are likely to reflect the sluggish response properties of neonatal visual neurons (Blakemore and Vital-Durand, 1986) in addition to the slower conduction velocities of visual nerve fibers. Comparison

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with the PERG in response to transient contrast reversal of low spatial frequency gratings is indicative of both these facts. The peak latencies of the neonatal ERG (Fulton and Hansen, 1982. 1989) and PERG (Fiorentini and Trimarchi. 1989) are also much longer than the adult's, suggesting that the neonatal photoreceptors and retinal neurons are also sluggish. However, PERG latency decreases during early infancy (Figure 3, open and gray symbols) and approaches adult values earlier than the VEP latency (Figure 3,closed symbols) (Fiorentini and Trimarchi, 1989). This suggests that retinal circuitry develops more rapidly than cortical circuitry. Latencies of the responses of single neurons to visual stimulation have been measured in the LGN of macaque monkeys of various ages from birth to adulthood (Blakemore and Vital-Durand, 1986). The latency of the responses is much longer in newborn monkeys compared with adults. It extends u p to 150 ms and even the shortest latencies are longer than the longest latencies of adult LGN

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cells. Then latencies decrease rapidly and consistently and approach adult levels around 70 days of age. There is a tendency for cells in the magnocellular layers to have shorter latencies than parvocellular cells a t all ages. This fact probably reflects the higher conduction velocities of P-alpha cell axons.

Scotopic vision The properties of scotopic vision of young infants indicate that the rods, although not yet morphologically mature (Drucker and Hendrickson. 1989). are functional in the human neonate. The scotopic spectral sensitivity function of 1 and 3 month old infants practically coincides with the adult function and the absolute sensitivity is only 1.7-2 log units below adult sensitivity at 4 weeks and 0.7-1 log unit at 3 months (Powers et al., 1981; Hansen and Fulton, 1987). So far, there has been only one study of infant contrast sensitivity a t low luminance levels (Fiorentini a t al., 1980). These VEP data (Figure 4 B. filled circles) indicate that a t 10 weeks of age, contrast sensitivity for sinusoidal gratings of low luminance (0.06 cd/m2) reversed in contrast at 8 Hz is lower than the adult sensitivity (Figure 4 A. filled circles) and the same is true for acuity. Psychophysical data also show that a t 2 months visual acuity is lower than adult acuity at all luminance levels (Brown et al.. 1987). The difference in contrast sensitivity between infants and adults, however, is rather small (a factor of 2 - 3) and adult values are reached within 4 months from birth (Fiorentini et al., 1980). Figure 4 also compares CSFs obtained in adults and 10 week old infants a t a low photopic (open circles) and a high photopic level (closed squares) with the low-luminance CSF. Interestingly, the optimal contrast sensitivity of adults increases in proportion of the square-root of mean luminance. For infants, the contrast sensitivities of the two extreme sets of data (obtained in different laboratories) are also in agreement with the square-root law, while the data for the intermediate luminance deviate consistently from this law. This point is of interest and will be reconsidered in the Discussion. Summation properties of the infant scotopic visual system are also different from the adult, both in space and time. Area summation is about 12 times the adult's a t 4 weeks and 4 times the adult's a t 11 weeks (Hamer and Schmeck, 1984). Temporal summation also extends over much longer stimulus durations in 10 week old infants than in adults (Hansen and Fulton, 1990) and the temporal summation function is very shallow in young infants, suggesting that the inhibitory components of the temporal response function are delayed or less pronounce than in the adult (Fulton, 1988). In conclusion, receptoral and preneural factors seem insufficient to explain the immaturity of scotopic vision at birth and its subsequent development. Most of the developmental processes are likely to be due to changes occurring in visual structures central to the photoreceptors.

Spatial frequency selectivity In the adult monkey, a large proportion of cells in the LGN and in the striate visual cortex have band pass spatial frequency

93


characteristics (Kaplan and Shapley, 1982: Derrington and Lennie, 1984; Blakemore and Vital-Durand, 1986; Poggio et al., 1977: DeValois et al., 1982: Foster et al. 1985). In human subjects, psychophysical and electrophysiological evidence indicates that visual detectors are selective to limited bands of spatial frequencies (see Braddick et al.. 1978. for review). There are few data that describe the development of spatial frequency tuning of single cells in the monkey visual system. Blakemore and Vital-Durand (1986) report various examples of response curves

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Figure 5 . Spatial frequency channels: effects on the amplitude of the VEP in response to a sinusoidal grating of constant spatial frequency (arrow) and moderate contrast ( 15-20%). square-wave reversed in contrast at 7 Hz. in the presence of a masking grating of high contrast, reversed in contrast at 6 or 9 Hz. Mean luminance: 6 cd/m2. A adult data for 4 different spatial frequencies of the test stimulus. B: data from an infant 1 1/2 months old. C: data from an infant 3 1/2 months old. Different symbols indicate different experimental sessions.

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of LGN cells as a function of stimulus spatial frequency, recorded from infant monkeys at different times from birth. In very young animals the responses of single cells peak at relatively low spatial frequencies and the high frequency cut off does not exceed 5 c/deg. However, the response functions show a clear low-frequency attenuation. Thus at least some LGN neurons have band pass spatial frequency characteristics even in the newborn monkey. The tuning then sharpens with age and the optimal spatial frequency a s well as the cut-off of the best resolving cells move toward higher spatial frequencies. These findings are relative to P cells. No data are available for the tuning characteristics of M cells in the infant monkey. Very little is known of the tuning characteristics of cortical neurons of infant monkeys. There seems to be some indication that in very young animals the spatial frequency tuning characteristics of cortical neurons have little low frequency attenuation (Blakemore and Vital-Durand, 1983). The same is true in young kittens (Derrington and Fuchs, 1981). There have been two attempts to find evidence for spatial frequency channels in human babies, both using a masking procedure. One study (Fiorentini et al., 1983) reported spatial frequency selective effects of masking on the amplitude of VEPs in response to sinusoidal gratings of fxed spatial frequency, reversed in contrast a t 7 Hz. The masking grating had a variable spatial frequency, either lower or higher than the test grating, and was reversed in contrast a t a slightly different temporal rate. The amplitude of the VEP in response to the test stimulus was reduced in the presence of the masking stimulus by a n amount that depended upon the difference in spatial frequency between the two stimuli (Figure 5). The second study (Banks. Stephen and Hartmann. 1985) applied the psychophysical preferential looking technique to investigate the effects of a narrow-band noise masker on the detectability of sinusoidal gratings of three different spatial frequencies. The two studies agree in showing that spatial frequency selectivity is present in infants 3 months old. The bandwidth of tuning at 1 c/deg at this age (Figure 5, C)is comparable to that of adult tuning for higher spatial frequencies (Figure 5, A). This finding can be understood in terms of the different spatial scales in the infant and adult foveae (Wilson, 1988). For younger infants, there is disagreement between the electrophysiological and the psychophysical studies. While in the former the data from one infant 6 weeks old show band pass tuning a t 0.3 c/deg (Figure 5. B). in the latter the average results of five 6 week old infants indicate low pass tuning. Whether this discrepancy is due to the small sample tested, to group averaging or to methodological differences remains to be investigated. One possible reason could be found in the different temporal properties of the test stimuli used in the two experiments. Possibly, band pass spatial frequency tuning may become manifest at an earlier age with temporally modulated than with stationary stimuli because of different developmental rates of mechanisms with different temporal response properties. It has also to be noted that, because of the contrast gain of the visual system (see for instance Figure 8), the effects of a masking stimulus on the contrast threshold (FPL experiment), may be expected to be considerably smaller than the effects on the response to a stimulus of suprathreshold contrast (VEP experiment).


95

Vernier acuity Vernier acuity (the ability to detect the misalignment of two abutting lines or gratings) is a type of hyperacuity. In foveal vision, adults vernier thresholds can be an order of magnitude better than thresholds for grating resolution. In peripheral vision on the contrary, vernier acuity drops much more steeply than grating acuity with increasing eccentricity (Westheimer, 1982: Levi et al., 1985). Having in mind the very small foveal thresholds for hyperacuity tasks in adults, one may be surprised to learn that in young infants vernier acuity evaluated behaviorally is lower than grating acuity (Shimojo and Held, 1987). This situation reverses rapidly, however, because vernier acuity develops at a higher rate than grating acuity (Figure 6. A). Already a t 3 to 4 months of age vernier acuity exceeds grating acuity (see Gwiazda et al.. 1989a for review). A difference in the rate of increase of grating acuity and vernier acuity can be expected merely on the basis of preneural factors, in particular of the quantum efficiency of the photoreceptors (Geisler, 1989: Banks and Bennet, 1988). That this is not the whole story, however, is suggested by two interesting facts about the development of vernier acuity. First, there is a sex difference in the rate of improvement of vernier acuity. Between 3 and 5 months females are better in vernier acuity than males (Held et al.. 1984). No sex difference is observed for the development of grating acuity. Second, vernier acuity continues to improve in children up to 7 years of age (Figure 6B, squares). while grating acuity levels off much earlier (Figure 6B, circles). Apparently, the development of vernier acuity requires the maturation of structures or the development of processes beyond those responsible for the age related increase in grating acuity. Perhaps all these factors mature simultaneously during an early life period, so that grating acuity and vernier acuity appear to have the same limiting factors. A differential time course in the development of vernier acuity and grating acuity has been found also in infant monkeys (Kiorpes and Movshon, 1989).These findings parallel those in human infants, apart from the different time scale.

Binocular function and stereoacuity Like most spatial acuities that develop gradually after birth, stereopsis seems to emerge abruptly between 3 and 4 months of age. After this sudden onset, stereoacuity increases very rapidly during the next few weeks, to reach thresholds as low as 60 arcsec around six months of age (see van Sluyters et al., 1989, for review). Several years seem then to be required for stereoacuity to match adult values (Gwiazda et al.. 1989a). Simultaneously with the onset of stereopsis there is evidence for the onset of another binocular function: infants start to prefer binocularly fusible stimuli to stimuli that in the adult produce binocular rivalry (such as vertical stripes in one eye and horizontal stripes in the other) (Shimojo et al.. 1986: Gwiazda et al., 198913). Other forms

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Figure 6. Development of grating acuity, stereoacuity and vernier acuity in infants (A1 (top panel) and children (B) (bottom panel). Vernier acuity and stereoacuity for some older infants (A). older children and adults (B)were limited by the maximum resolution of the display. Copyright 1989. Canadian Psychology Association. Reprinted by permission.


97

of binocular function have been investigated in infants, for instance the preference for random-dot stimuli correlated in the two eyes with respect to non-correlated stimuli. There is some controversy on whether this preference appears concomitantly with the onset of stereopsis (Smith et al., 1988) or appears earlier (Einzeman et al., 1989).

As for vernier acuity, there is a sex difference for the development of stereoacuity and of fusion preference (Bauer et al. 1986: Gwiazda et al., 1989a). Females show evidence for stereopsis and for fusion preference around 9 - 10 weeks, while males do not before 12 - 13 weeks. The sudden appearance of stereopsis and fusion around 3 months of age has been suggested to reflect the process of segregation of monocular inputs to layer IV in the striate cortex (Held. 1985). There is some evidence that this should occur between 4 and 6 months in human infants (Hickey and Peduzzi. 1987). It seems rather unlikely however that the segregation process is confined to a very brief period of time. Possibly segregation of monocular inputs is a necessary prerequisite for binocular stereopsis, but other factors are involved.

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Figure 7 . VEP responses to orientation reversal of a grating pattern in a 7 weeks old infant (b). The lower trace represent the timing of stimulus reversals. The upper trace (a) represents for comparison VEPs recorded in response to appearance of a pattern. Reprinted by permission from N a t u r e , Vol. 320, p.618. Copyright (C) 1986 Macmillan Magazines Ltd .

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Discrimination of orientation In the newborn monkey, cells in the visual cortex show a considerable degree of orientation specificity a n d a system of orientation columns is already established a t birth (Wiesel and Hubel. 1974). Since in higher mammals specificity for orientation is a property of cortical neurons that is not shared by neurons at lower levels of the visual system, it is of interest to know whether the human visual system also shows some kind of sensitivity for orientation of lines or contours. Two lines of research have been followed to investigate orientation discrimination in infants. Behavioral experiments based on the habituation paradigm (Maurer and Martello. 1980) provide evidence that human neonates can discriminate square wave gratings oriented a t 90 deg from each other (Slater et al., 1988). The selectivity for orientation however is probably rather poor at birth. In the adult it is possible to evaluate the width of orientation channels using a masking procedure (Campbell and Kulikowski. 1966). Experiments applying the masking technique to babies of various ages suggest that tuning for orientation is very poor at one month of age, but that it improves between 2 and 4 months and remains constant thereafter (Held et al.. 1989). On the whole, these behavioral experiments indicate that orientation selectivity is a t least to some degree innate and that it probably reaches adult values much earlier than other visual functions. Somewhat different findings have been obtained following another line, namely by recording VEPs in response to patterns that periodically change in orientation (Braddick et al.. 1986). Responses correlated with 90 deg shifts in orientation of the stimulus grating, occurring 8 times per second (Figure 71, could be recorded in infants 6 weeks old, but not in younger infants. It appears, however, that the age of onset of orientation-specific VEPs depends on the temporal rate of orientation-reversals. For reversals occurring 3 times per second, VEP responses could be obtained in infants 3 weeks old, earlier than for a 8 Hz rate of reversal (Braddick et al., 1989). This was confirmed using the habituation paradigm: at one months of age infants are sensitive to 90 deg shifts of orientation if these occur at a rate of 3 Hz. but not a t a rate of 8 Hz. These findings seem to recompose the apparent controversy between behavioral and electrophysiological studies of orientation discrimination in very young infants. Probably the VEP responses to a change in stimulus orientation reveal the relative immaturity of temporal characteristics of orientation selective neural mechanism. Both sets of results are consistent with the presence of some form of orientation discrimination very early in life. And both provide evidence that orientation selectivity improves rapidly after birth, approaching adult values by 3 - 4 months of age (Atkinson et al.. 1988; Held et al., 1989). It is possible, however, that the psychophysical experiment, based on masking effects, reveals the development of inhibitory interactions that are not necessarily involved in the VEP experiment.


99

Motion Perception Motion perception has been studied in infants both psychophysically and electrophysiologically. Psychophysical studies using the preferential looking procedure indicate that infants of 3 months of age and older show a preference for a moving with respect to a stationary pattern, provided the pattern velocity exceeds a threshold (see Dannemiller and Freedland. 1989). In 3 - 4 months old infants the minimum velocity threshold for drifting gratings of low spatial frequency is of the order of 3 - 5 deg/s (Aslin. 1988: Dannemiller and Freedland. 1989). Infants of 2 months or younger either do not show any preference for a moving stimulus (Dannemiller and Freedland, 1989) or have very poor sensitivity to motion. at least at low velocities (Kaufmann et al., 1985). VEP studies agree with the behavioral findings indicating a relatively late development of motion sensitivity. A VEP response to motion can be obtained by reversing at a fixed temporal frequency the direction of motion of a random dot pattern (which also jumps incoherently a t and between reversals a t a high temporal frequency). Responses time-locked to the reversals of motion direction, and not to the intervening jumps, are considered to reflect the activity of mechanisms sensitive to the direction of motion, and not simply to pattern change (Wattam-Bell, 1987).In adults, motion specific VEPs are recordable in a large range of stimulus velocities (5 to 30 deg/s). and peak around 15 deg/s (Wattam-Bell. in press). In infants younger than 10 weeks, no motion specific responses are recordable, even at low velocities (5 deg/s), although responses to the pattern jumps are clearly present. Motion specific VEPs emerge around 10 weeks of age at low velocities, but still later for stimull of higher velocity. The highest velocity at which a motion-specific VEP is obtained increases with age (Wattam-Bell, in press). Oculomotor responses are also rather immature in very young infants. For instance, smooth pursuit can be observed around 10 weeks of age for linear motion of a target at low velocities (Shea and A s h , 1988) but not at higher velocities, where it is replaced by a series of saccadic eye movements (Aslin. 1987). Optokinetic responses are immature at birth: monocular optokinetic nystagmus (OKN) can be elicited by stimuli moving in the temporal-nasal direction, but not in the opposite direction (Atkinson. 1979). I t is not until after 3 months of age that the monocular OKN can be driven in either direction. The immaturity of smooth pursuit can be explained at least in part by the lack or immaturity of motion perception. The OKN asymmetry has been ascribed to the lack of appropriate cortical inputs to the motor centers responsible for the optokinetic response (Atkinson, 1984; van Hof-van Duin.1978). In conclusion, both sensory and oculomotor responses to moving stimuli seem to be immature a t birth and to emerge somewhat later in comparison with other visual responses. If a longer age span is considered, however, it appears that motion specific responses may complete their maturation years in advance to some pattern specific responses (De Vries et al., 1989).

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Inhibitory interactions Inhibition plays a crucial role in shaping the response of single visual neurons and in controlling the interplay of stimulus evoked activity in different neurons. Signs of inhibitory phenomena in the intact visual system of adult human subjects are found for instance in subthreshold interactions, in masking phenomena and in the low-frequency cut off of the CSF. In cats, surround inhibition in retinal and LGN receptive fields is present, but weak, a t birth and it develops gradually during the early postnatal period (Hamasaki and Flynn. 1977;Rusoff and Dubin. 1977:Berardi and Morrone. 1984). Inhibition must be present at least to some degree in the LGN neurons of the neonatal monkey, because their spatial frequency tuning characteristics are band pass in shape (Blakemore and Vital-Durand, 1986).Apparently, this type of inhibition is less mature in the neonatal visual cortex (Blakemore and Vital-Durand. 1983). 1 16

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Figure 8. Development of cross-orientation inhibition in one infant at three different ages. VEPs in response to contrast-reversal of a sinusoidal grating of low spatial frequency are plotted against the stimulus contrast (circles). The other symbols indicate VEPs in response to the same stimulus in the presence of a masking grating reversed in contrast at a different temporal frequency and either parallel (squares) or orthogonal (triangles) to the test grating. Note that at 4 months the parallel mask, but not the orthogonal mask, attenuates significantly the VEP, indicating orientation selectivity at that age. At 10 months, both the parallel and the orthogonal masks affect the VEP amplitudes, though in different ways, as occurs in the adult. Reprinted by permission from Nature, Vol. 321, p.235. Copyright (C) 1986 Macmillan Magazines Ltd. In human infants we have seen that some type of inhibitory phenomena are present at an early age. For instance, it is possible to suppress the response to a grating of a certain spatial frequency by


101

a mask of a different spatial frequency, but the masking effect is less strong than in the adult (Fiorentini et al., 1983; Banks et al., 1985). The CSF of young infants was reported to be low pass in shape, but probably this is an artifact due to not having used sumciently low spatial frequencies. Effects revealed by VEPs in response to complex visual stimuli, attributed in the adult to lateral inhibitory interactions, seem to be present in 8 week old infants (Sokol, Zemon and Moskowitz, personal communication). There is evidence, however that more subtle inhibitory effects, such as those that occur between orthogonal gratings at suprathreshold contrasts, do not emerge until six to eight months of age (Figure 8) (Morrone and Burr, 1986). This phenomenon, known a s "cross-orientation inhibition." is present in single cells of the cat visual cortex (Morrone et al.. 1982) and is believed to reflect GABA-mediated interactions among cells tuned to different orientations (Morrone. Burr and Speed, 1987). Also VEPs evoked by windmill-dartboard stimuli, that in the adult have been attributed to short-range lateral interactions (Zemon and Ratliff. 1982) do not appear earlier than 5 months from birth, and are still very immature at this age (Moskowitz and Sokol, 1989). The development of interactions between orthogonal stimuli and other types of complex stimulus interactions probably require the refinement and progressive selectivity of horizontal connections in the visual cortex, like those observed in visual cortical areas of the monkey (see Gilbert, 1985 for a review). These have been found to develop after birth (Burkhalter and Bernardo. 1989) and may rely upon the development of dendritic trees in the upper cortical layers (Becker at al. 1984) a s well a s in the progressive selectivity of intracortical synaptic connections, likely to start around the 8th month of age (Garey and de Courten. 1983).

Color vision The development of color vision in infants has been recently reviewed by Teller and Bornstein (1987). They conclude their overview of all the relevant literature with a few important established facts. First, photopic and scotopic spectral sensitivities are mature within the first or second postnatal month. Second, infants in the second month of life have trichromatic color vision, since they can do both Rayleigh discriminations (and therefore are neither protanopes nor deuteranopes) and tritan discriminations (and therefore must have a third type of cones, sensitive to short wavelengths). The three cone types with highest sensitivity in the long (L),medium (M) and short (S) range of wavelengths, respectively, are likely to have spectral absorption properties not dissimilar to adult photopigments. Third, infants 4 months old categorize wavelengths of the visible spectrum much in the same way as adults. Infant categorization is based on a habituation-dishabituation paradigm and grouping occurs for four ranges of wavelengths corresponding to the spectral regions that adults categorize a s blue, green, yellow and red, by hue naming (Bornstein et d., 1976: Boynton and Gordon, 1965). However, neonates and very young infants (3 weeks old) seem to have an immature S cone system Warner et al., 1985; Adams et al..

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1986). Moreover, 3-week-old infants fail to discriminate monochromatic lights (at mesopic luminances) that are discriminated by 7-week-olds (Clavadetscher et al.. 1988). Thus the ability to discriminate colors, a t least under mesopic conditions, emerges between 3 and 7 weeks from birth. Color vision seems therefore to develop early in infants and to have the main characteristics of trichromatic vision. This general statement is supported by further experimentation, that has also

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103

uncovered other important aspects of color vision. Brown and Teller (1989) report a n interesting experiment in which the spectral sensitivity of 3 month old infants was evaluated a t five different wavelengths in the range 540 - 650 nm. In the middle of this range the spectral sensitivity curve presents a notch, like in adults, that reflects the non-additivity of responses of L and M cones (Figure 9). These findings are consistent with a color-opponent model. Therefore they provide evidence that at 3 months from birth, color-opponent mechanisms can be functional (with the caveat that infant color opponency has not been proven identical to adult opponencyl. Heterochromatic flicker photometry, a means to evaluate photopic spectral sensitivity, is usually performed with uniform field illumination. Anstis and Cavanagh (1983) have devised a technique for matching the luminances of gratings of different colors. The gratings are presented temporally in such a way to produce apparent motion in one or the other direction, according to their relative luminances. In adults this method yields spectral sensitivity curves equivalent to those evaluated with flicker photometry. Its usefulness for infant testing comes from the fact that patterns that are not isoluminant produce optokinetic nystagmus in either direction, while a t isoluminance the pattern appears practically stationary, and no OKN is elicited. Thus isoluminance can be determined by observing the presence and direction of optokinetic eye movements of infants. Application of this method (Maurer et al., 1989) and a variant of it (Teller and Lindsey, 1989) have confirmed that relative spectral sensitivities of 1 to 3 months old infants are remarkably similar to those of adults. It is important to recall, however, that the conditions of the motion-nulling OKN technique are likely to reveal the properties of a photopic mechanism of the peripheral retina. Previous disagreement about a difference between infant and adult spectral sensitivity curves in the short wavelength region of the spectrum may derive from methodological differences. Another possible reason is the lower density of ocular media of infants compared with adults. Hansen and Fulton (1989) measured absolute sensitivity a t the short wavelength end of the spectrum (401 nm) as well as a t 561 nm, in 10 week old infants. Comparison of the sensitivities at the two wavelengths in infants and adults showed that infants are relatively more sensitive than adults at 401 nm. Since human rhodopsin absorbs these two wavelengths equally well, the difference between infants and adults has to be ascribed to a higher optical density of the adults' eye at 401 nm. Most of this difference is probably due to the lens and is likely to decrease progressively with age. In conclusion, there is convergent evidence that the photopic spectral sensitivity of young infants is very similar to that of the adult and that in the second month from birth three types of cones are active and some color discriminations are possible. This does not a t all mean that color vision is completely developed at this age. For instance, infant color discriminations require large color contrast and also stimuli of large size (Packer et al., 1984; Adams et al.. in press). This suggests that the spatial characteristics of the infant color system are different from those of the adult.

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Spatial and temporal characteristics of color contrast sensitivity Visual potentials evoked by chromatic stimuli have offered a means to investigate the development of color contrast sensitivity in infants, both in the spatial and temporal frequency domain (Morrone et al., 1989). The stimulus was a periodic pattern obtained by superimposing two sinusoidal gratings of the same spatial frequency at crossed orientations. It appeared as a plaid pattern with very blurred contours. Two such patterns were generated by the red and the green guns of a T V monitor, and either presented separately or superimposed with a 180 deg spatial phase shift, to form a red-green plaid. The relative luminances of the red and green components could be varied at will, from 100% red to 100% green, while keeping constant the total mean luminance and the equal contrasts of the two components. If the proportion of red to green is varied continuously, a value of this ratio has to be such that the red and green components are matched in brightness. This is the so-called isoluminant point.

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Figure 10. VEP amplitude as a function of the ratio of red-to-total mean luminance in the stimulus pattern. A: adult subject, 1 c/deg stimulus, mean luminance: 16 cd/m2, contrast: 30%. square-wave reversal: 7.5 Hz. B and C: infant PAB, at two ages. Stimulus spatial frequency: 0.1 c/deg. mean luminance: 16 cd/m2, contrast: 90%, square-wave reversal rate: 2 Hz (B),3 Hz (C). In adults, plaid patterns reversed in contrast (at a temporal frequency of say 5 - 6 Hz) evoke a second harmonic VEP response for any value of the ratio of the red luminance to the total luminance. At relatively low contrasts, the VEP amplitude has a minimum for the ratio corresponding to the isoluminant point, a s determined by flicker photometry (Figure 10. A). Similarly to what is done with the


105

pattern-reversal VEPs in response to luminance contrast, it is also possible to evaluate a contrast threshold by extrapolation of VEP amplitude against chromatic (isoluminant) contrast. This threshold coincides with the psychophysical contrast threshold. Not surprisingly, therefore, application of this method to adults yields contrast sensitivity curves for chromatic contrast that are very similar in shape to those obtained psychophysically (Mullen, 1985). This method has been applied recently to investigate the development of chromatic contrast sensitivity in infants (Morrone et al.. 1989). Chromatic VEP responses to patterns of very low spatial frequency (0.1 c/deg) reversed in contrast a t a low temporal frequency do not emerge prior to 5 to 7 weeks of age (Figure 10, B and C). Responses at higher spatial and temporal frequencies have a later onset. Chromatic contrast sensitivity increases progressively with age between 2 and 6 months and approaches adult values before contrast sensitivity to luminance modulated patterns of the same spatial and temporal low frequencies (Figure 11. top). The same is true for chromatic acuity, i.e. the highest spatial frequency a t which a chromatic (isoluminant) VEP can be obtained: with the emergence of chromatic responses it increases more rapidly than VEP acuity for isochromatic, luminance modulated gratings (Figure 11, bottom). Sensitivity for chromatic contrast with isoluminant patterns is relatively low because of the broad and largely overlapping action spectra of the photopigments. This fact together with the immaturity of photoreceptors in the infant retina has been considered to be the main factor responsible for the difference between contrast sensitivity for luminance- and color-contrast in young infants (Banks and Bennett, 1988). However, other factors must play a role in the development of infant chromatic contrast sensitivity, since the rate of increase in sensitivity with age is different for chromatic and luminance contrast. It is likely that mechanisms responsible for encoding and processing color information a t post receptoral levels, e.g. color opponent receptive fields, are immature a t birth and develop later, at least in part independently from developmental processes involved in the increase of luminance contrast sensitivity with age. A recent report seems to disagree with this conclusion, however. Using the VEP swept contrast technique (Norcia et al., 1985) for evaluating contrast sensitivity, Allen et al. (1990) report that the contrast sensitivity for isoluminant stimuli has the same ratio as the sensitivity for luminance contrast in young infants and adults, suggesting that the reduced infant sensitivity results entirely from preneural factors. Further investigation seems to be required to resolve this controversy.

Discussion Not all possible aspects of human visual development have been covered in this chapter. For instance, visual attention, recognition of complex shapes or other cognitive aspects of vision have not been considered. Still, the picture that emerges from the previous sections is rather complex. The reader will be easily convinced that, as anticipated in the introduction, there is usually little ground for ascribing this or that aspect of human visual development to the maturation of one or

CHAPTER 3

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Figure 11. Contrast sensitivity for a low spatial frequency (A)and acuity (B),evaluated from VEPs in response to red-green isoluminant gratings (open symbols) or to isochromatic (red-black or green-black) gratings (closed symbols) reversed in contrast at a low temporal frequency, plotted against age, for a group of infants 5 to 30 weeks old. Different symbols indicate different infants. Each point was obtained by extrapolation to zero amplitude of VEP amplitudes plotted against stimulus contrast (top) or spatial frequency (bottom). Points below the unit contrast sensitivity in the top graph indicate infants and ages at which no significant VEP could be obtained with isoluminant stimuli, although a t the same age VEPs in response to luminance-contrast reversals were clearly present.


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another neuronal population. I t is clear, however, that different visual capabilities may emerge at different times after birth and that different visual functions may show different developmental trends. And there is convergent evidence from morphological and behavioral findings that postnatal visual development in human infants proceeds both serially, at subsequent stages of the visual pathways, and in parallel, along dffferent neural streams. There have been recent proposals to differentiate an early phase of visual development, dominated by retino-tectal structures, from a later phase, when cortical functions become predominant and the visual activity mediated by the cortex starts to control the subcortical visuomotor functions (see Atkinson. 1984). This two-stage developmental process accounts for some facts, such as the separate emergence of the two opposite directions of OKN. but it comes u p against the fact that newborns can discriminate patterns of different orientations. This behavioral performance has to rely upon neural mechanisms that respond selectively to different orientations. Orientational selectivity is a property of cortical neurons that is not shared, at least in non-human primates, by tectal neurons. Thus it has to be recognized that the visual cortex is active to some degree even in the newborn, though possibly very immature. Before discussing the possible functional effects of maturation at a cortical level, let u s consider those aspects of vision that may be determined primarily by the development of structures peripheral to the visual cortex. This is the case, for instance, for visual acuity and spatial contrast sensitivity. There seems to be general consent that contrast sensitivity for temporally modulated patterns of low spatial frequency is mediated by the M retino-cortical pathway, while color contrast sensitivity is subserved by cells in the P pathway (Merigan. 1989: Kaplan et al., 1990; Schiller et al.. 1990: Mollon, 1990). Scotopic pattern detection may imply primarily the activity of the M stream (Kaplan et al.. 1990). Now, the contrast sensitivity for temporally modulated patterns of spatial frequency less than 1 c/deg develops early (Atkinson et al.. 1974: Harris et al.. 1976: Pirchio et al., 1978: Norcia et al., 1988, 1990) and at low luminances contrast sensitivity matches adult values earlier than at higher luminances (Fiorentini et al., 1980).This may be ascribed to a n early functional maturation of M cells. On the other hand, if we consider how the contrast sensitivities for luminance and color contrast increase with age (Figure 10) it is tempting to jump to the conclusion that the development of the P system is somewhat delayed, but more accelerated with respect to the M system. While the findings of Figure 10 are not inconsistent with this interpretation, other factors have to be taken into account. First, as mentioned in the previous section, the delayed onset of responses to color contrast compared with luminance contrast (Morrone et al., 1990) may be a consequence of the spectral properties of the photoreceptors: the largely overlapping action spectra of the L and M cones impose a limit to the maximum attainable color contrast. Thus, what might appear to be a delayed emergence of the neural system mediating color contrast sensitivity can largely be accounted for by preneural factors (Banks and Bennett, 1988). The different slopes of the two developmental curves of Figure 10. on the contrary, cannot be

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accounted for by preneural factors, because these should affect by the same amount the sensitivities for luminance and color contrast. Secondly, a word of caution h a s to be said about the interpretation of contrast reversal VEPs in terms of separate contributions from the P and M systems. The steady-state VEP responses to contrast reversal, either luminance contrast or color contrast, contain only the even harmonics of contrast modulation and therefore represent non-linear components of the response. Second harmonic non-linearities have been observed in the responses of monkey M ganglion cells to flickering red-green uniform lights matched in luminance and have been ascribed to non-linear interactions between the L- and M-cone inputs to the non-color opponent M cells (Lee et al.. 1989). Before more is known about the neural origin of contrast-reversal VEPs, it would be premature to ascribe the isoluminant contrast-reversal VEPs exclusively to the P system. Some promising results for the differentiation of pure color-contrast VEPs from responses to luminance-contrast are being obtained from patterns modulated in contrast in the on-off mode a t low temporal frequencies (Fiorentini et al., 1990). The preliminary findings of these experiments are consistent with those obtained with pattern-reversal isoluminant V E P s indicating a differential development of color- a n d luminance-contrast responses. As to contrast sensitivity a t medium and high spatial frequencies, there is no general agreement whether in the adult this is subserved mainly by the M or the P system. I t is in this range that the infant data obtained under different experimental conditions differ mostly (see for example Figs. 1 and 4). In particular, VEP contrast sensitivities obtained with the swept-contrast technique are much higher than those obtained in a number of different laboratories with the extrapolation method of Campbell and Maffei (1970).The latter are generally in good agreement with each other. Whether this is a peculiarity of the swept-contrast technique, or is due to the much higher luminance employed (see Figure 4) remains to be clarified. I t is noteworthy, however, that peak contrast sensitivity at low photopic luminance (around 10 a t 10 weeks, according to most published data) deviates from the square-root law, in contrast with the contrast sensitivities found at low mesopic and high photopic luminances, which stand approximately in the same ratio a s the square-root of the respective luminances. One may speculate that contrast sensitivity results from the combined activity of different neuronal populations with different sensitivities, and that different experiments may reveal preferentially the contribution of one or the other of these populations. In summary, the data on infant CSF suggest that the M system. considered to be responsible for contrast detection of temporally modulated patterns of low spatial frequency, develops early, possibly during the first few months of life. This may appear difficult to reconcile with the fact that in the monkey, cells of the magnocellular LGN layers have to undergo a greater increase in contrast sensitivity during development than the cells of the parvocellular layers (Blakemore and Hawken. 1985). On the other hand, anatomical data on the plasticity of segregation of monocular inputs to the monkey striate cortex indicate that the postnatal period in which plastic changes can be induced in layer IVC. by reversal of monocular deprivation, is shorter


109

for the magnocellular inputs to layer IVC-alpha t h a n for the parvocellular inputs to layer IVC-beta (LeVay et al., 1980). This is consistent with a shorter developmental period of the magnocellular, compared with the parvocellular pathway. Visual acuity takes much longer to develop fully than contrast sensitivity a t lower spatial frequencies and the major constraint to infant visual acuity is probably the immaturity of the retina, and in particular the fovea. Whether a t each age the resulting acuity reflects primarily the properties of the P system, as seems to be the case for the adult monkey, or whether the M system also contributes to spatial resolution in infancy requires further investigation. The visual functions considered so far define the lowest values of the luminance- and color-contrast, in the spatial and temporal frequency domain, below which no vision is possible. Probably these threshold characteristics result from constraints imposed already at the input to the visual cortex and/or a t the earliest stages of cortical processing. Further processing however is required for the perception of suprathreshold stimuli and for guiding visuomotor responses. Various visual functions reviewed in the previous sections imply cortical processing, e.g. orientation discrimination, motion perception, stereopsis and, possibly in part, vernier acuity. Orientation discrimination, at least in a crude form, is present at birth and rapidly becomes more selective. Discrimination of moving from stationary patterns, VEP responses to reversal of motion direction, and smooth oculomotor pursuit have a later onset. In the monkey, processing of motion information relevant both for the perception of moving objects and the control of smooth pursuit seems to proceed primarily along the cortical stream leading from V1 to MT (Newsome et al., 1985; Livingstone and Hubel, 1988; Newsome and Pare', 1988: Schiller et al., 1990). which receives its major input from the M pathway. Accordingly, one might interpret the onset of motion responses during the third and fourth month of life as a sign of the emergence of cortical activity along this route. Orientation and color information required for the perception of other stimulus attributes are likely to be processed primarily along the cortical stream from V1 through V2 and V4 to IT (Mishkin et al.. 1983; Livingstone and Hubel, 1988; Merigan, 1989; Schiller et al.. 1990). The early presence of orientation selectivity and of color discrimination in infants might indicate an early functionality of this route, but we do not know how long it will take for it to reach its full potential. There may be various developmental stages, a s suggested by the fact that the orientation and spatial frequency channels, that provide the basic machinery for a multiscale analysis of form, are present shortly after birth, while more complex stimulus interactions emerge later. Judging from the latest findings on stereo- and vernier-acuity in children, the development of some cortical processes may cover a period of several years. outlasting the maturation of more peripheral stages. In conclusion, there are indications that visual development proceeds at different rates and/or emerges a t different ages for visual functions that are likely to be mediated by different neural streams between the retina and the primary visual cortex. As to the functions that imply further cortical processing, we are just beginning to acquire some knowledge of their age of onset and duration of development.

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Although there are indications that these may differ for different visual capacities, an interpretation in terms of different intracortical pathways must await future research.

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lications of Parallel Processing in Vision J.T r m a n (Editor) Q 1992 Elsevier Science Publishers B.V. All rights reserved A

119

Changes in Temporal Visual Processing in Normal Aging JULIE R. BRA"AN

Introduction Many aspects of visual processing change in association with normal aging. Acuity, spatial contrast sensitivity, color vision, dark adaptation, oculomotor function, binocular vision, and visual fields are often affected (see Owsley and Sloane. 1990, for a recent review), but perhaps the most pervasive change involves temporal sensitivity. Over a wide variety of tasks, older subjects generally find it difficult to detect rapid changes in a visual stimulus. This chapter will describe recent reports regarding temporal processing changes in older adults. The controversies over whether these changes are primarily due to optical or neural factors, and whether aging primarily affects one of two parallel systems, will also be discussed. Some of the earliest research on the effects of aging on temporal processing involved measurements of critical flicker fusion (CFF). the threshold temporal frequency where a flickering light no longer appears to be flickering. Several reports reveal that older adults consistently have lower CFFs than younger adults (Misiak. 1947; Coppinger, 1955; McFarland, Warren, and Karis, 1958; Huntington and Simonsen, 1965). suggesting that temporal resolution decreases with age. Some of this reduction can be attributed to yellowing of the lens and reduction in pupillary diameter with age (Kline and Schieber. 1982). but neural changes may also contribute to the decline in CFF sensitivity (Elliott, Whitaker, and MacVeigh, 1990). Another common change in the aging visual system, closely related to CFF threshold, is that older adults require more time between stimuli to detect their temporal order (McFarland. Warren, and Karis. 1958: Eriksen. Hamlin, and Breitmeyer. 1970; Kline and Orme-Rogers, 1978: Nine and Schieber. 1980). It has been suggested that age-related changes in temporal processing are due to an increase in stimulus persistence (Axelrod, Thompson, and Cohen.1963; for a review, see Kline and Schieber, 1982). Under this hypothesis, an overall slowing of the aging nervous system results in more time being necessary for recovery from a visual stimulus. If sufficient time is not provided, the first stimulus blurs, or persists, into the second. The results of many experiments support

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such a hypothesis. For example, Eriksen et al. (1970) required observers to detect the location of the gap in a Landolt-C. In spite of lower light sensitivity, if given sufficient time older adults' discrimination was equivalent to that of younger adults. This suggests that older adults may have compensated for lower overall sensitivity with longer integration (persistence) of the stimulus. While the stimulus persistence hypothesis may provide a convenient descriptive framework for temporal changes with age, it does not speculate on the cause of these changes. In the next section, a complementary hypothesis will be discussed which does suggest neural processes, specifically changes in one visual pathway, underlying agerelated decrements in temporal processing.

The "transient deficit" hypothesis There is considerable evidence that we process many aspects of visual information in parallel, along two separate pathways (see Weisstein, Ozog, and Szog, 1975; Breitmeyer and Ganz. 1976: Breitmeyer. this volume). Perhaps related to neuroanatomical dichotomies seen in ganglion cells of the cat (Enroth-Cugell and Robson, 1966) and cellular layers of the lateral geniculate nucleus in the monkey (Livingstone and Hubel, 1987; for a review see Shapley. this volume), this functional division of labor observed psychophysically in humans has been called the "transient/sustained" dichotomy. Under this heuristic division, the transient aspect of visual processing responds to stimuli with abrupt on- and off-sets, is optimally sensitive to low spatial and high temporal frequencies, contrasts near threshold, and produces a quick, rapidly decaying response. Because of these unique processing characteristics, the transient system might be best suited for holistic, global processing, the perception of motion, and the localization of objects in space. Conversely, the sustained aspect of visual processing responds in a more prolonged manner to stationary or slowly moving stimuli, higher spatial and lower temporal frequencies, and moderate to high contrasts. Its response characteristics make it optimally suited for analytic, featural processing, involving the perception of pattern information and fine detail. In general, stimuli presented in the fovea tend to activate the sustained system, with the transient system becoming more active a s stimuli move into peripheral vision. Kline and Schieber (1981) proposed that differential aging of the transient and sustained systems might account for changes in visual perception with age. Specifically, they suggested that a selective transient loss is consistent with the loss of temporal resolution with age, This idea has been followed up by many researchers (e.g.,Sturr, Kelly, Kobus. and Taub. 1982; Sturr, Church, and Taub, 1985; Sturr, Church, Nuding, Van Orden, and Taub, 1986; Kline. 1987; Sturr. Van Orden. and Taub, 1987; Sturr. Church, and Taub, 1988; Elliott et al.. 1990). with various conclusions. For a selective transient loss hypothesis to be correct, older adults should show consistent losses in sensitivity at high temporal and low spatial frequencies. As discussed previously. in general older adults do lose temporal resolution with age (although the use of certain paradigms result in little or no loss of temporal sensitivity with age,

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e.g.. Sturr et al., 1988). This temporal decline could be consistent with a "transient deficit" hypothesis. On the other hand, although there is one report of age-related contrast sensitivity losses at low and medium spatial frequencies (Sekuler. Hutman, and Owsley, 1980). most researchers have found losses a t higher spatial frequencies (e.g., Owsley, Sekuler. and Siemsen. 1983; Morrison and MacGrath, 1985; Owsley, Gardiner, Sekuler, and Lieberman. 1985; Elliott, 1987; Crassini, Brown, and Bowman, 1988; Elliott et al., 1990) or a generalized loss at all spatial frequencies (Ross, Clarke, and Bron. 1985; Sloane, Owsley, and Alvarez, 1988). It is difficult to relate spatial processing changes with age specifically to a neural "transient" loss as suggested originally by Kline and Schieber (1981). Some reports attribute spatial and/or temporal losses with age to changes in the optics of the eye such as senile miosis and increased lenticular light scatter (Owsley et al., 1983; Sturr et al., 19881, but others have reduced or compensated for these optical changes and suggest neural factors play a primary role (Morrison and MacGrath, 1985; Owsley et al.. 1985; Elliott, 1987; Brannan et al., 1988a. 1988b; Sloane. Owsley, and Jackson, 1988; Elliott, Whitaker. and Thompson, 1989; Elliott et al.. 1990). Elliott et al. (1990)has even suggested that aging may involve a selective sustained channel loss, based on Weale's (1975) theory of random cell death. Under this hypothesis, all cell types die randomly, but those types representing a one-to-one relationship between the retina and visual cortex (presumably those in the sustained system) would produce more disruption to visual perception than those with a many-to-one (transient) relationship. Although there is some consensus on the nature of temporal changes in aging vision, s o far there is no acceptable theoretical framework to account for these changes.

Recent experimental findings and a quantitative model of temporal processing changes with age To address many of the lingering questions regarding temporal processing changes with age, we (Brannan, Sekuler, Phillips, and Chan, 1988a; Brannan, Sekuler. and Phillips, 198813) designed experiments to provide a quantitative framework for describing age-related changes in visual temporal processing. The temporal properties of the visual system can be investigated by threshold contrast sensitivity measured for two or more temporal pulses separated by varying intervals (Ikeda. 1965; Rashbass, 1970). Using a variant of this approach, Bergen and Wilson (1985)demonstrated that the detectability of a trio of pulses can be accounted for by a model comprising linear filters together with nonlinear temporal probability summation. As the spatial properties of their pulsed stimuli varied, Bergen and Wilson found a covariation in the temporal impulse response function. For example, a biphasic impulse response function was needed to account for results with pulses of low spatial frequency, but a monophasic function was adequate for high spatial frequency pulses. This well-established procedure seemed promising a s a n instrument for probing age-related changes in vision. For any linear system, the impulse response function provides a complete characterization. Thus, if one could successfully describe the impulse

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response function, one could predict the system's response to any other temporal probe. Although the human visual system is inherently non-linear, it is possible to minimize non-linear effects by using a threshold detection paradigm (reducing contrast non-linearities) and stimuli of very short duration (lessening the contribution of temporal probability summation). It seems reasonable, a prtort, that the temporal impulse response function that underlies detection of a trio of near-threshold pulses should also control t h e perception of suprathreshold pulses, as manifest, for example, in studies of stimulus persistence. We decided to assess age-related changes in temporal processing in two different procedures: measuring near-threshold behavior by means of a three-pulse paradigm: and measuring suprathreshold responses in terms of persistence. Additionally, we wished to see whether age-related changes in these two measures could be accounted for by the Bergen and Wilson model. In the first experiment (Brannan et al., 1988b). the contrast sensitivities for three temporal pulses were obtained for a group of younger and older adults. Four older (three females, one male: mean age 74.1 years) and four younger (three females, one male: mean age 24.7) adults participated as subjects. Older adults had been screened for ocular disease during a thorough ophthalmological exam, and had normal or correct-to-normal visual acuity (mean 20/25, range 20/20 to 20/30).Acuity for all younger adults was 20/25 or better. All subjects were naive to the purpose of this experiment, although they had all previously participated in visual perception experiments unrelated to this one. Stimuli were spatial patterns whose one-dimensional luminance profiles were defined by the difference of Gaussians (hereafter, DOG): DOG(x,a) = 3 exp (-x2/02)- 2 exp (-x2/2.2502), where x is position along the horizontal, and Q is the DOG'S space constant. The advantage in using localized aperiodic spatial patterns such a s DOGS is that they are simultaneously well-localized in the space domain and band limited in the spatial-frequency domain. For all conditions, contrast sensitivities were measured for two sizes of DOGS, the narrower one having a peak spatial frequency of 12 c/deg and the broader one, 4 c/deg. The DOG patterns were temporally modulated by three, equally-spaced rectangular pulses, each 16.7 msec in duration. The amplitude (contrast) of the first and last pulses of the trio were 0.375 that of the middle pulse. Contrast was defined by Contrast = ( b e a k -

Lean

1/

Lean-

Threshold measurements were made a s a function of the delay between the pulses (the interstimulus interval: hereafter, ISI). Patterns were generated on the monochrome display of a Macintosh I1 computer. The mean luminance of the display was 22.1 cd/m2.

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Subjects sat 65 cm from the computer's monitor (17 cm x 25 cm) in a darkened room. A chin rest provided a comfortable rest for their heads, keeping the subjects' eyes even with the center of the display. Subjects viewed the display binocularly. Contrast thresholds were measured using a single interval forced choice procedure with a computer-controlled version of a randomized single staircase. 60

I

0

,

,

20

,

,

40

,

,

60

,

I

10

100 0

20

40

60

80

100

Interstimulus Interval (milliseconds)

Figure 1. Mean contrast sensitivity as a function of ISI. The left panel shows results for young subjects and the right panel shows results for old observers. Within each panel, filled symbols represent sensitivities for 4 c/deg, while open symbols are for 12 c/deg data. Arrows denote sensitivities to single pulses of 4 c/deg (filled arrow heads) or 12 c/deg (open arrow heads). Solid lines show the fits of the model to the data (see text for details). Within a single block of trials only one spatial frequency of DOG was used. For each trial, the computer chose at random one of seven ISIs, ranging from 0 to 100.4 msec in 16.7 msec increments. The subject initiated each trial with a key press. The DOG pattern was then presented at this IS1 at a preassigned contrast. The initial contrast of the middle DOG in all patterns was 80%. Following the presentation the subject was asked to press a key to indicate whether the pattern was "seen" or "not seen." If the response was "seen" the contrast was reduced by 1 dB for subsequent presentations at this ISI, otherwise it was increased by the same factor. Within a single block of trials each IS1 was presented 40 times. For each ISI. we computed the mean of the contrasts recorded for the last ten reversals of response (from "seen" to "not seen" or vice versa). The reciprocal of this mean contrast defined the contrast sensitivity. In addition, we measured the contrast sensitivity for each DOG modulated by just a single pulse of 16.7msec duration. Figure 1 shows the average contrast sensitivities for younger and older subjects. In each panel, sensitivity is plotted against ISI. The dark squares represent sensitivities for 4 c/deg, while the open squares are for 12 c/deg data. The solid straight llnes denote the single pulse sensitivity for the two spatial frequencies of DOGS. With 4 c/deg, younger subjects are more sensitive than older subjects a t all ISIs measured. Relative to the sensitivity of the single pulse data (solid line). both young and old subjects show facilitation at short ISIs followed

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by inhibition at ISIs beginning a t about 30 msec. The magnitude of the deviation from the single pulse sensitivity is more pronounced for the younger subjects. For the 12 c/deg DOG, younger subjects are again more sensitive than older subjects at all ISIs. At this spatial frequency only facilitation relative to the single pulse sensitivity is apparent. Contrast sensitivity as a function of IS1 is then monophasic for smaller DOG stimuli. To fit the data we used a form of temporal impulse response function proposed by Bergen and Wilson (1985): H(t) = A (t/d" exp(-t/r) [l/n! - B ( t / ~ ) ~ / ( n + k ) ! ] where A is the overall gain (amplitude), B is the area of the negative lobe (inhibition), l / z is the width of the positive lobe (facilitation), n is the steepness at onset and near the zero crossing, and k defines the shape of the negative lobe. The effects of temporal probability summation are taken into account by the Quick (1974) formulation: S=

(II

R(t') I'dt')

j/p

where R(t) =

L(t').H(t-t')d t '

and L(t') is the stimulus. The model fits to young and older subjects are shown as dashed lines in Figure la and lb. Parameters were chosen in order for the model curves to be within one standard deviation of the each data point. The parameters for each curve are tabulated in Table 1.

The data demonstrate that there are age-related changes in the sensitivity to three temporal pulses. It is possible to explain these changes in terms of the impulse response function proposed by Bergen and Wilson (1985). For the broad DOG (peak frequency, 4 c/deg), the parameters used to fit the young data are the same as those found in Bergen and Wilson (1985). except for the amplitude, A. To account for the changes in sensitivity with age, it was necessary to decrease the overall amplitude, A, by a factor of 1/410. However, simple attenuation of the impulse response was not sufficient to account for the changes. It was also necessary to decrease B. the area of the inhibitory lobe, by a factor of 1.6. This suggests that there is a differential loss of inhibition as well a s the overall decrease in temporal sensitivity with age. The contrast sensitivity data for the narrow DOG (12 c/deg) is monophasic and can be fit without a n inhibitory component (B=Oin the temporal impulse response function). For the young data, parameters were the same as those found by Bergen (1981).except for amplitude, A. To model the older adults' data, the amplitude, A, was decreased by a factor of 2. To maintain the temporal extent of the facilitory effect in the face of this decrease in amplitude it was necessary to decrease T, by a factor of 2. This suggests that temporal facilitation decreases with age, but its duration does not.


125

In a second experiment (Brannan et al., 1988a), we measured the stimulus persistence of two suprathreshold pulses in younger and older observers. For various temporal separations between the pulses, we determined whether the observers perceived the two pulse presentation to be a single continuous pulse or two distinct pulses.

Table 1. 4 c/deg

12 c/deg

YOUNG

OLD

YOUNG

OLD

A

100

67

25

12

B

0.8

0.5

0

0

T

9.5

9.5

12.5

6.7

n

4.0

4.0

4.0

4.0

k

1 .o

1 .o

0

0

Sixteen older (10females, 6 males; mean age 73.2years) and 16 younger adults ( 1 1 females, 5 males: mean age 22.7)participated as subjects. All eight subjects from Experiment One were included in Experiment Two. Older adults had been screened for ocular disease, and had normal or corrected-to-normal visual acuity (mean 20/27. range 20/20 to 20/30).Acuity for all younger observers was 20/25 or better. Subjects were naive to the purpose of this experiment, although 10 of the older and 7 of the younger subjects had previously participated in other, unrelated visual perception experiments. Again. stimuli were spatially localized DOG patterns. Four different DOG stimuli were used. The peak spatial frequencies for the different sizes were 1. 4,8. and 12 c/deg. The DOGS were temporally modulated by a pair of 16.7 msec rectangular pulses, separated by intervals (ISI) of 0 to 100.4 msec. Both pulses were of equal amplitude (contrast) and were presented well above threshold, a t 0.2 contrast. At each ISI, we measured the proportion of trials in which the two pulses would be perceived as a single continuous flash as well as the proportion where they were seen as two distinct flashes. Data were collected using the method of constant stimuli. For every subject, four blocks of trials were run, one for each of the peak spatial frequencies: 1. 4. 8, and 12 c/deg. For every spatial frequency, each IS1 was presented randomly 20 times. Seven ISIs were used, ranging from 0 to 100.4 msec in 16.7 msec increments. For an IS1 of 0. the stimulus consisted of a single, uninterrupted pulse of 33.4 msec duration (two times 16.7 msec). After every presentation, observers reported whether the two-pulse presentation appeared continuous or not. To assess the effect of retinal illuminance, all younger subjects were also run wearing 0.7 neutral density filters. This reduction in

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126

retinal illuminance is equivalent to the most severe estimates of loss due to senile miosis (Said and Weale, 1959). Subjects viewed the display binocularly. YOUNGER SUBJECTS: 1 cldeg

YOUNGER SUBJECTS: 4 cldeg

htanllmulua Interval (maec)

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Mean percent “continuous“ judgments a s a function of interstimulus interval for younger adults. Panels show data for 1. 4. 8, and 12 c/deg. Data for stimulus persistence of two pulses for younger and older observers are shown in Figures 2 and 3. For each spatial frequency, the proportion of two-pulse presentations that were reported as continuous is plotted against ISI. For younger observers (Figure 2). spatial frequency had little effect on the psychometric functions measured. However, for older observers (Figure 31, increasing the spatial frequency shifted the psychometric functions to the right, particularly at 12 c/deg. The rightward shift indicates that a s the spatial frequency increases, older observers require longer I S I s to detect the gap separating the two pulses. Figure 4 summarizes the persistence results. A threshold IS1 (in msec) for two-pulse persistence is plotted against the peak spatial


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frequency of the DOG stimuli used. To estimate the threshold for each spatial frequency, a least squares regression was fit to each set of data in Figures 2 and 3. The threshold value was defined as the IS1 a t which subjects had reported the two pulses as continuous 75% of the time. The psychometric functions measured for younger adults wearing 0.7 neutral density filters were also fit. It is evident that the decrease in retinal illumination produced by these filters had no significant effect on the two-pulse stimulus persistence for younger observers. These data capture the main findings of this experiment: 1) older subjects require longer ISIs than do young subjects before seeing the pair of pulses as not continuous: 2) this difference is largest at 12 c/deg: and 3) reducing retinal illuminance does not noticeably change younger subjects' persistence thresholds. OLDER SUBJECTS: 1 C/&g

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Figure 3. Mean percent "continuous" judgments as a function of interstimulus interval for older adults. Panels show data for 1, 4,8. and 12 c/deg. Differences in the psychometric functions for older and younger observers can not be ascribed to differences in criterion used by the two

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groups. Compare responses for an IS1 of 0 msec. where the stimulus should be continuous and a n IS1 of 100.2 msec. where the two stimuli should be distinct. In response to the continuous pulse (IS1= 0). all observers reported continuous virtually all the time. At an IS1 of 100.2 msec. two pulses were consistently reported by all observers. regardless of age.

Spatial Frequency (c/deg)

Figure 4. Threshold IS1 (msec) as a function of target center spatial frequency. Data are shown for old and younger observers, and for younger observers studied while viewing the display through neutral density filters. We wanted to see how well the data of this experiment could be accounted for using the same model that we had used for Brannan et al. (1988b). To do so, though, we had to give the model a n explicit criterion for distinguishing between a single pulse and two pulses. As before, the temporal response of the model is given by R(t). I t seems reasonable to assume that to detect two pulses rather than a single long combined pulse, there must be some criterion decrement, A, in the response R(t) over a sufficient time interval between the responses to the first and second pulses. We have chosen to assume that this criterion decrement follows a Weber law behavior

where


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is the maximum response to the first pulse pooled over some time

interval T and

is the minimum response which occurs between the two pulses pooled over some time interval (T). Weber law behavior was used as a first approximation because of the abundant evidence of its presence in a variety of discrimination tasks in visual processing. To complete the model, it is necessary to relate values of A to the percentages of "continuous" responses in the stimulus persistence task. This was done using the psychometric function, A: @(A) = 2

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The steps for the complete model are schematized in Figure 5. Temporal Impulse Function

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Figure 5. A schematic of the steps taken to derive the model of temporal processing in aging vision.

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Figure 6 shows the fit of the model to the averaged persistence data of younger and older subjects at 4 and 12 c/deg. The data has been averaged only across subjects who also participated in Brannan et al. (1988b). The parameters of the temporal impulse response function used for these fits were determined from the threshold temporal three-pulse data. The fit shown in Figure 6 are for a temporal pooling interval. T=30 msec, and q=4. However, the fit does not critically depend on either of these parameters. Reasonable fits to the results can be obtained with T ranging from 20 to 50 msec and q ranging from 2 to 6. Parameters 6=.91 and k=3.8 were determined by a least-mean-square fit of the model to the data. The cross-correlation of the fit is .94. So, the changes in the temporal impulse response function determined by the three-pulse data can account for the suprathreshold stimulus persistence data.

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Conclusions The nature of temporal deficits in normal visual aging has been debated for over three decades. Recently Sturr et al. (1988) have reported that older adults do not differ from younger adults in temporal summation. Sturr et al. suggested that previous reports of large temporal losses could be due in part to four factors: 1) the use of suprathreshold measures: 2) cognitive effort required by the tasks used; 3) less than rigorous screening for ocular disease in the elderly; or 4) differences in retinal illuminance between young and old due to senile miosis. However, recent reports (Sloane et al.. 1988a. 1988b; Mayer et al.. 1988) suggest that optical effects due to senile miosis cannot explain age-related differences in spatio-temporal processing. Moreover, Tulanay-Keesey et al. (1988) have suggested that there is neural decline in spatial and temporal processing channels with age, but that the substrate for spatio-temporal interaction remains relatively intact with increasing age. Tulanay-Keesey et al. further propose that age-related changes in visual processing only occur at threshold, not at suprathreshold. Recently Schieber, Hiris. White, Williams, and Brannan (1990) have compared oscillatory motion detection thresholds for a small dot displaced vertically at 8 Hz and thresholds for the detection of correlated motion in a random dot cinematogram. Interestingly, all older adults had higher thresholds than younger adults for the oscillating dot stimulus, but only older females had significantly higher thresholds to the cinematogram. When younger adults were run on the same tasks with optical blur of up to 2 diopters introduced, their performance did not decline. This provides converging evidence that optical factors cannot completely explain age-related changes in temporal processing. The results of our investigation support the idea that there is a consistent slowing of temporal processing in normal visual aging. We found that older adults were less sensitive to both threshold three-pulse and suprathreshold two-pulse temporal stimuli. This was true despite using a task presumed to require little cognitive effort (Brannan et al.. 1988b) and a suprathreshold measure (Brannan et al., 1988a). In addition, when retinal illuminance in the younger subjects was reduced to approximate that due to senile miosis. persistence threshold was not increased. Therefore, even when the four factors suggested by Sturr et al. (1988) are taken into account, there is still evidence for a significant decrement in temporal processing ability with age. These age-related changes in threshold and suprathreshold temporal tasks can be accounted for quantitatively. The threshold task determined contrast sensitivity to three temporal pulses. The sensitivity changes with age can be explained by a change in the temporal impulse response function. The suprathreshold task measured temporal persistence. Age-related changes in the temporal impulse response function determined by the threshold measurements of Brannan et al. (1988b) could account for these suprathreshold temporal processing changes with age. Our results suggest that the decrease in temporal response with age is due not only to an overall sensitivity loss, but also to a selective

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loss of inhibition. To detect a change between two stimuli, the visual system must register excitation from the first stimulus. This must then be followed by a decrease in excitation before any additional excitation can be processed from the second stimulus. If older adults do have less inhibition in temporal visual processing, they would find it more difficult to register a second stimulus. More time would be needed between stimuli before an older person would have enough fading of the initial excitation to detect additional excitation brought on by another stimulus. This need for additional time between stimuli is exactly what numerous studies have reported over the years (McFarland. Warren, and Karis, 1958: Eriksen. Hamlin, and Breitmeyer, 1970: Kline and Orme-Rogers, 1978) and what we have found. Thus, our model suggests a quantitative explanation for increased stimulus persistence with age. Interaction between inhibitory and excitatory lobes of our model suggest a role for cooperative parallel processing in age-related changes in temporal resolution. Currently however, a theory based on selective loss of one neurophysiological parallel channel over another appears to be too simplistic to account for the complicated processes underlying visual aging.

References Axelrod, S., Thompson, L.W., and Cohen. L.D. (1968). Effects of senescence on the temporal resolution of somesthetic stimuli presented to one hand or both. Journal of Gerontology. 23, 191-195. Bergen, J.R. (1981). A quantitative model of human spatiotemporal vision at threshold. Unpublished doctoral dissertation, The University of Chicago. Bergen, J.R.. and Wilson, H.R. (1985). Prediction of flicker sensitivities from temporal three-pulse data. Vision Research, 25. 577-582. Brannan. J.R.. Phillips, G., Chan. C.. and Sekuler, R. (1988a). Stimulus persistence in young and older adults: The effects of reduced retinal illumination. Inuestigatiue Ophthalmology and Visual Science, 2 9 (suppl.), 432. Brannan. J.R.. Phillips, G., and Sekuler, R. (198813). Temporal processing in young &d older observers. Presentation a t the annual meeting of the Psychonomic Society. Chicago, Illinois: November. Breitmeyer, B.G. (1991). Parallel processing in human vision: History, critique, and review. In J.R. Brannan (Ed.), Applications of parallel processing in vision Amsterdam: Elsevier. Breitmeyer. B.G.,and Ganz. L. (1976). Implications of sustained and transient channels for theories of visual pattern masking, saccadic suppression, and information processing. Psychological Review. 83. 136. Coppinger. N.W. (1955). The relationship between critical flicker frequency and chronological age for varying levels of stimulus brightness. Journal of Gerontology, 10, 48-52. Crassini. B., Brown, B., and Bowman, K. (1988). Age-related changes in contrast sensitivity in central and peripheral retina. Perception, 17, 315-332. Elliott, D. (1987). Contrast sensitivity decline with ageing: a neural or optical phenomenon? Ophthalmic and Physiological Optics.7. 415419.

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Elliott, D.. Whitaker, D., and MacVeigh, D. (1990).Neural contribution to spatiotemporal contrast sensitivity decline in healthy ageing eyes. Vision Researck30. 541-547. Elliott, D., Whitaker, D., and Thompson, P. (1989). Use of displacement threshold hyperacuity to isolate the neural component of senile vision loss. Applied Optics, 28. 1914-1918. Enroth-Cugell, C.. and Robson. J.C. (1966). The contrast sensitivity of retinal ganglion cells of the cat. Journal of Physiology, 187.517-552. Eriksen, C.W.. Hamlin. R.M. and Breitmeyer. R.G. (1970).Temporal factors in visual perception related to aging. Perception and PSyChophySicS, 7,354-356. Huntington, J.M.. and Simonsen, E. (1965). Critical flicker fusion frequency as a function of exposure time in two different age groups. Journal of Gerontology, 20. 527-529. Ikeda. M. (1965).Temporal summation of positive and negative flashes in the visual system. Journal of the Optical Society of America. 55 , 1527-1534. Kline, D.W. (1987). Ageing and the spatiotemporal discrimination performance of the visual system. Eye, 1. 323-329. Kline. D.W., and Orme-Rogers, C. (1978).Examination of stimulus persistence as a basis for superior visual identification performance among older adults. Journal of Gerontology, 33. 76-81. Kline, D.W., and Schieber. F. (1981). Visual aging: A transient/sustained shift? Perception and Psychophysics, 29. 181 182. Kline, D.W.. and Schieber. F.J. (1982).Visual persistence and temporal processing. In R. Sekuler. D. Kline, and K. Dismukes (Eds.). Aging and Human Visual Function. New York: Alan R. Liss. Inc. Livingstone, M.S., and Hubel, D.H. (1987). Psychophysical evidence for separate channels for the perception of form, color, movement, and depth. Journal of Neurophysblogy, 7.3416-3468. Mayer. M. J.. Kim, C. B. Y., Svingos, A.. and Glucs. A. (1988).Foveal flicker sensitivity in healthy aging eyes. I. Compensating for pupil variation. Journal of the Optical Society of America A, 5, 2201-2209. McFarland, R.A.. Warren, A.B.. and Karis, C. (1958).Alterations in critical flicker frequency a s a function of age and 1ight:dark ratio. Journal of Experimental Psychology, 56. 529-538. Misiak. H. (1947).Age and sex differences in critical flicker frequency. Journal of Experimental Psychology, 37. 318-332. Morrison, J.D., and MacGrath. C. (1985). Assessment of the optical contributions to the age-related loss of contrast sensitivity. Quarterly Journal of Experimental Physiology, 70.249-269. Owsley, C., Gardner. T., Sekuler. R., and Lieberman, H.(1985).Role of the crystalline lens in the spatial vision loss of the elderly. Inuestgatiue Ophthalmology and Visual Science, 26. 1165-1170. Owsley. C.. Sekuler, R., and Siemsen, D. (1983). Contrast sensitivity throughout adulthood. Vision Research, 23,689-699. Owsley. C.. and Sloane. M. (1990).Vision and aging. In F. Boller and J. Grafman (eds.), Handbook of Neuropsychology (Vol. 4). Amsterdam: Elsevier Science Publishers. Quick, R.F. (1974).A vector magnitude model of contrast detection. Kybernetik, 15, 65-67. Rashbass. C. (1970).The visibility of transient changes in luminance. Journal of Physiology, 210, 165-186.

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Ross, J.E.. Clarke, D.D.. and Bron. A.J. (1985).Effect of age on contrast sensitivity function: uniocular and binocular findings. British Journal of Ophthalmology, 69,51-56. Said, F.S., and Weale, R.A. (1959). The variation with age of the spectral sensitivity of the living crystalline lens. Gerontologia, 3, 213231. Schieber, F., Hiris. E.. White, J.. Williams, M.. and Brannan. J. (1990). Assessing age-differences in motion perception using simple oscillatory displacement versus random dot cinematography. Investigative Ophthalmology and Visual Science (suppl.), 355. Sekuler. R.. Hutman, L.P., and Owsley, C. (1980). Human aging and spatial vision. Science, 209. 1255-1256. Shapley, R. (1991).Parallel retinocortical channels: X and Y and P and M. In J.R. Brannan (Ed.). Applications of Parallel Processing in Vision. Amsterdam: Elsevier Science Publishers. Sloane. M. E.. Owsley, C.. and Alvarez, S. (1988a). Aging, senile miosis, and spatial contrast sensitivity at low luminance. Vision Research, 2 8, 1235-1246. Sloane, M. E., Owsley, C.. and Alvarez, S. (1988b).Aging, and luminance-adaptation effects on spatial contrast sensitivity. Journal of the Optical Society of America A, 6 , 2181-2190. Sloane. M.E.. Owsley. C.. and Jackson, C.A. (1988). Aging and luminance-adaptation effects of spatial contrast sensitivity. Journal of the Optical Society of America A, 5. 2181-2190. Sturr. J.F.. Church, K.L.. Nuding, S.C., Van Orden. K., and Taub, H.A. (1986). Older observers have attenuated increment thresholds upon transient backgrounds. Journal of Gerontology, 41, 743-747. Sturr, J.F.. Church, K.L.. and Taub, H.A. (1985).Early light adaptation in young, middle-aged, and older observers. Perception and PSyChophySicS, 37. 455-458. Sturr, J.F., Church, K.L.. and Taub, H.A. (1988).Temporal summation functions for detection of sine-wave gratings in young and older adults. Vision Research, 28, 1247-1253. Sturr, J.F.. Kelly, S.A., Kobus, D.A.. and Taub. H.A. (1982). Agedependent magnitude and time course of early light adaptation. Perception and Psychophysics, 31, 402-404. Sturr, J.F., Van Orden, K., and Taub, H.A. (1987).Selective attenuation in brightness for brief stimuli and at low intensities supports agerelated transient channel loss. ExperfmentalAging Research 13. 145149., Tulanay-Keesey. V., Ver Hoeve. J. N.. and Terkla-McCrane. C. (1988). Threshold and suprathreshold spatiotemporal response throughout adulthood. Journal of the Optical Society of America A, 5. 2191-2200. Weale, R.A. (1975).Senile changes in visual acuity. Transactions of the Ophthalmological Society. U.K.. 95. 36-38. Weisstein, N.. Ozog, G., and Szog. R. (1975). A comparison and evaluation of two models of metacontrast. Psychological Review, 82, 325-343.

Parallel Processing in Higher-Order Perception


lications of Parallel Processing in Vision ~.Trman (Editor) @ 1592 Elsevier Science Publishers B.V. All rights resewed A

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M and P Pathways and the Perception of Figure and Ground NAOMI WEISSTEIN. WILLIAM MAGUIRE, and JULIE R. BRANNAN

Introduction A compelling idea in perceptual psychology is that figure and ground are processed in functionally different ways by the visual system (Rubin, 1922; Koffka, 1935; Calis and Leeuwenberg. 1981: Breitmeyer and Ganz. 1976; Julesz. 1978; Weisstein and Wong. 1986. 1987). Figure 1 shows a circle divided into a series of pie shaped sectors. Every other sector contains a fine grained texture. The sectors are easily grouped into one of two ambiguous configurations: a Maltese cross consisting of the fine grained textured sectors on a textureless background, or alternatively a Maltese cross consisting of the textureless sectors on a fine grained background. The two organizations can alternate. As they alternate, one can observe that the texture disappears when the textured sectors become ground, and the other cross is seen. Such simple demonstrations inspire the idea that figure and ground perception involve two different kinds of visual coding. We have researched figure/ground phenemona for the past decade particularly focusing our efforts on how the spatial and temporal frequency composition of a n image region contributes to the segmentation of that region into figure or ground, a s well a s how the segmentation of a region into figure or ground influences its spatial and temporal frequency sensitivity. This work indicates that the high spatial and low temporal frequency domain of visual information is strongly associated with figural perception, while the low spatial and high temporal frequency domain is strongly associated with ground perception. Exploring the spatial and temporal frequency basis of this dichotomy, we have found that a sine wave grating that is of a higher spatial or lower temporal frequency than an adjacent grating will appear to float in front of the adjacent grating. Recently we have also established that sine wave gratings that are colored red will float in front of gratings of the same or similar spatial frequency, a result which we describe in this paper and relate to current theories of magnocellular (M)and parvocellular (P) processing streams. We present a model where figurelground relations emerge from antagonistic interactions of M and P pathways responsive to luminance

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contrast over overlapping portions of the spatiotemporal frequency continuum. Much recent interest in early visual processing has centered around the magnocellular (M) and parvocellular (P) pathways which remain distinct and relatively independent going through LGN, V1, and visual associative cortex. These independent sets of neurons have been characterized a s having different sensitivities to visual information (Livingstone and Hubel. 1987. 1988). In particular, the magnocellular pathway has been regarded as relatively "color blind," although there is partial suppression of magnocellular response by diffuse red light (Dreher. Fukada. and Rodieck, 1976; Livingstone and Hubel. 1984). while there are great numbers of color opponent cells in the parvocellular pathways. The two pathways also differ in spatial and temporal frequency sensitivity, with parvocellular neurons generally responding to higher spatial and lower temporal frequencies than magnocellular neurons (Derrington and Lennie, 1984; Tootell et al., 1988a).

Figure 1. Maltese cross pattern consisting of black and fine grating sectors. When the black sectors are organized into figure, the background texture becomes indistinct. A number of theorists have pointed out that figure and ground regions have different appearances with the figure characterized by distinct form and fine detail (Koffka, 1935: Julesz. 1978: and see below). Most intriguing for theories of figure and ground perception is reported correlations between the M pathway and perceptions of motion, depth, and clear figure/ground segmentation (Livingstone and Hubel, 1987. 1988; Cavanagh. Tyler, and Favreau. 1984) while the smaller receptive field sizes and color opponency in the P pathway suggest a role in the analysis of form, fine detail, and color (but see Cavanagh, 1989, and Logothetis et al.. 1990. for the role of the parvocellular pathway in depth analysis). In this paper we pursue the idea that these functional distinctions establish a relationship between

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ground perception and M pathways and figure perception and P pathways. A consideration of previous work, and of new work discussed in the next section leads to a model of figure and ground perception. We suggest that both M and P pathways are sensitive to luminance contrast throughout most of the temporal and spatial frequency range overlapping considerably in the stimuli to which they respond, but each pathway is most sensitive to a different part of the spatio-temporal frequency spectrum. The M pathway is most responsive to low spatial and high temporal frequencies, while the P pathway is most sensitive to low temporal frequencies throughout the spatial range. The basic tenet of the model is that the magnocellular pathway produces a ground biased signal and the activity in the parvocellular pathway biases perception of a region towards figure. Where both M and P pathways respond to a stimulus, the perception is the result of a subtraction, parvocellular response minus magnocellular response with more positive responses associated more strongly with figural perception. This means that figure/ground coding is relative in these pathways, so that when the figure/ground relations between two regions are computed, the relatively more positive regional response will bias a perception of figure whatever the sign or absolute size of the regional figure and ground responses. We briefly review the notion of different types of processing associated with figure and ground perception below, and present a summary of empirical work that leads us to the model described above.

Early work The Gestalt theorists recognized the fundamental importance of figure-ground perception in human vision and pioneered the early phenomenological studies of figure and ground. They pointed out that figure and ground regions have different perceptual properties. Figural regions are "richer and more differentiated" than ground regions, and have a "thing-like" character while ground regions appear to "extend behind the figure" (Kofka, 1935. Rubin. 1922). The Gestalt theorists also postulated that figure and ground perception involved functionally different neural processes. Many of the ideas of the Gestalt psychologists have been abandoned in modem perceptual psychology, particularly their theories of brain function (see Hochberg, 1972). but the idea of two distinct processes underlying figure and ground perception continues to influence modern theory. Julesz (1978) proposed that figure and ground perception involves two different types of image analysis. Ground analysis involves the rapid detection and organization of the scene at the resolution of "blobs" while figure analysis takes place more slowly and involves the analysis of fine detail. This concept of two systems differing in sensitivity and function both involved in the initial analysis of the pattern, has also been central to the thinking of a number of others (Weisstein, 1968, 1972; Weisstein. Ozog, and Szoc. 1975; Kulikowski and Tolhurst, 1973; Breitmeyer and Ganz, 1976; Alwitt, 1981). Central to many of these models is the idea that the analysis of figural regions often involves scrutiny of details and attention, while the perception of background involves the detection of global shape (see also Henning, Hertz, and Broadbent. 1975).

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The .direct spatial frequency connection High spatial frequencies appear to play a dominant role in edge perception and the resolution of details in a n image (Carpenter and Ganz, 1972: Broadbent, 1977: Julesz. 1978: Ginsburg. 1982: Norman and Ehrlich, 1987: Shulman and Wilson, 1987: b u t see also Westheimer and McKee. 1980, for evidence that low spatial frequencies must be present for good stereoacuity). On the other hand, low spatial frequency information may be sufficient in a n initial rough scan of a scene when details are not required (Henning, Hertz, and Broadbent, 1975: Breitmeyer and Ganz. 1976: Broadbent, 1977: Marr and Poggio. 1979; Ginsburg, 1982: Shulman and Wilson. 1987).

Figure 2. Rubin faces/vases reversible figures where regions defined by high and low spatial frequencies.

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There appears then to be a link between high spatial frequency analysis and figural perception and blob or low spatial frequency analysis and ground perception. About ten years ago, Wong and Weisstein set out to see whether a more direct link could be established between low and high spatial frequencies and blob-ground. edge-figure perception. We have used ambiguous displays such as Rubin's familiar faces/vase drawing (see Figure 2) to explore the effects of a region being figure or ground on spatial sensitivity independent of the context's stimulus characteristics. Our findings are that sharp targets (with high spatial frequencies present) are detected better in the region of the ambiguous pictures seen as figure regardless of which physical region that is. Conversely blurred targets (with energy primarily in lower spatial frequencies) are detected better in the region perceived as background (Wong and Weisstein, 1983). More recently, we have obtained contrast sensitivity functions for Gaussian modulated sine-wave patches in figure and ground regions in a related design. The observer adjusted the contrast of a patch located in the center of the Rubin figure until it was just visible. The spatial frequency of the target ranged from 1 c/deg to 16 c/deg. In one block of trials, the observer made the adjustment only when the central region was perceived a s figure: in another block of trials, the adjustment was made only when the central region was perceived a s ground. The contrast sensitivity for gratings in the figure region was shifted toward relatively greater sensitivity at the higher spatial frequencies while that for gratings when the region was perceived a s ground was shifted toward lower spatial frequencies (see Figure 2). These findings are seem consistent with the general theoretical overview of blob type ground and edge type figure processing. Seeking a more specific formalization of this theoretical overview we turn to models of the distribution of channels in spatio-temporal frequency space based on the huge amount of detection data for flickering and stationary luminance contrast sine wave gratings gathered over the last twenty years (Graham, 1989). As Grossberg (1987a.b) and others have pointed out, the perception of such gratings involves multiple computations on the image and cannot be assumed to be isomorphic with the response of spatial and temporal frequency channels in early visual processing. Nonetheless these channels must be the building blocks for such perceptions and the evidence from these detection experiments seems a good place to start. In the following pages we present three models of figure/ground processing. These models are based upon putative sets of channels in the visual system that have been explored using threshold detection and discrimination methods (Watson, 1986; Graham, 19891. We start by asking whether our data and other data which we shall present later can be explained by looking at what we call the spatial channels of the visual system. These are the channels that are narrowly tuned to spatial frequencies and quite broadly tuned to temporal frequencies, with lower spatial frequency channels tuned to slightly higher temporal frequencies. These channels are also known a s sustained channels in previous literature and are closely associated with the P pathway. The spatial model of figure and ground processing will be seen to fail when the effects of temporal frequency and directional motion on figure and ground perception are considered. We will then consider a model where channels tuned to

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temporal frequencies and sensitive to direction of motion are the sole mechanism of figure and ground perception. We shall call these temporal channels. They have also been known as transient channels in earlier literature, and we believe they are closely related to the M pathway. These temporal channels are also inadequate alone to explain all data. We finally consider a model where input from both the spatial and temporal channels is antagonistically combined. This model does a good job of explaining our data. The putative spatial and temporal channels have characteristics that naturally lead to a n interpretation in terms of the parvocellular (P)and magnocellular (M) pathways of the primate visual system. We finally consider this interpretation and consider some new predictions and data generated by it. Before turning to these models however we wish to define some terms.

Some definitions In this paper we will frequently describe analyzers, channels and pathways. By analyzers we mean psychophysically identified mechanisms which are sensitive to a limited range of values on a specific stimulus dimension, and respond to a stimulus in a local region of the retinal image. Physiologically, the equivalent level of analysis is at the level of individual neurons and their receptive fields. Channel refers to a set of otherwise identical analyzers that differ in their responses along one or more dimensions. The variant dimension might typically be spatial position, in which case the channel would be a spatial distribution of identical analyzers. One might also speak of a channel responsive to vertical orientation which contained analyzers with identical orientation tuning, but different size and/or spatial position tuning. A pathway is a group of channels which share response characteristics on a limited set of dimensions. Thus we might speak of a motion pathway, consisting of channels sensitive to different speeds and directions of motion, which in turn are composed of spatially distributed sets of analyzers, tuned to particular speeds and directions. The term pathway is used as well to refer to the physiological structures underlying the psychophysically defined pathway. We can speak of a n analyzer or channel as being labeled (Graham, 1989; Watson, 1986: Treisman. 1986). With a labeled analyzer, mechanisms above in the processing hierarchy have information about their input sufficient such that even at the analyzer's threshold of responding, stimuli may be identified and discriminated from other patterns. An example of labelling is spatial position. A light flashed a t one location, is discriminable from an identical light flashed a t another spatial location at threshold. Thus the analyzers responsive at threshold are labeled for spatial position. For a labeled analyzer or channel, we would also like to know the aspects of the response profile that are most important in information terms. A channel response might be best characterized by the peak responding analyzer, or by the difference between the peak responding and lowest (trough) responding analyzer, the peak to trough response, or some other pattern (Graham, 1989). We will consider our channels in terms of peak or peak-to-trough response.

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A spatial model of figure and ground perception A schematic explanation of how two channels, one tuned to lower spatial frequencies and somewhat higher temporal frequencies than the other, would respond to a flickering sinewave grating patch, gaussian modulated in both space and time, is given in Figure 3.

P m

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c 0 n L m

time

Figure 3. (1) (Top) spatial luminance distribution and (bottom) temporal luminance distribution a t point x of a contrast reversal flickering sine wave grating. (2) Hypothetical spatial impulse response of two spatial channels. (3)Hypothetical temporal impulse response of these channels. (4) Time averaged respnse of these channels to the stimulus in panel 1.

The top row of panel 1 shows the luminance profile of a gaussian modulated sinewave grating patch, while in the bottom row, the temporal luminance profile of the spot marked x on the patch is given.

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In panel 2 the spatial sensitivity profiles of the analyzers tuned to lower spatial frequencies (top row) and higher ones (bottom row) are shown. The analyzers are centered at a retinal location corresponding to x on the patch. For this contrast and luminance the stimulus does not produce maximal response in either analyzer, since it is a little too small for the receptive field of the lower spatial frequency analyzer and a little too big for the receptive field of the higher one. An equal but opposite response occurs for the analyzers whose retinal location corresponds to the spot marked y on the patch. The integrated spatial peak-to-trough response from each channel is hence about the same. This is illustrated in panel 3 by the height of the vertical arrows as a percentage of the maximum peak-to-trough response in each channel for that contrast and luminance. But now consider the different temporal response of the two analyzers to the integrated spatial response. The top row in panel 4 shows the fast biphasic response of the low spatial frequency analyzer. The bottom row of panel 4 shows the slower monophasic temporal impulse response of the high spatial frequency one. Superimposed on each temporal impulse response is a temporal luminance profile of the flickering grating patch shown in the bottom row of panel 1. I t is a little harder to figure out what the temporal response of these two analyzers is because the answer requires a convolution of the impulse response with the stimulus rather than a simple correlation as in the spatial case, but the results are straightforward enough. The fast biphasic response follows the stimulus rising and falling as the stimulus does while the slower monophasic response barely gets started by the time the stimulus has fallen below its mean luminance level. The results of the convolution are shown in panel 5 and the peak of each function is shown by the height of the arrows in panel 6 as a function of maximum peak-to-trough difference of each channel for that contrast and luminance. Clearly the channel with the lower spatial frequency response and the higher temporal frequency response has the larger amplitude. If these were the only two channels in the visual system, a rule which chose the largest peak-to-trough amplitude among channels would choose the lower spatial frequency one. In general where a set of spatial analyzers differ in their temporal responses such that analyzers tuned to lower spatial frequencies are tuned to higher temporal frequencies, this type of response shift should occur. The number of spatial channels that are found psychophysically to be independent near threshold is about five or six when sensitivity to stationary gratings is measured along the spatial frequency axis. It is important to note that psychophysical methods define a minimum number of channels, however. Specifically they do not exclude the possibility of a near continuum of channels corresponding to the near continuous distribution of receptive field sizes, orientations, temporal response characteristics, etc. Consistent with the above analysis of spatiotemporal channels. We can build a spatial model of figure and ground perception based upon a set of analyzers narrowly tuned to spatial frequency and broadly tuned to temporal frequency. Such a model is shown in Figure 4 (see Graham. 1989). Each ellipse represents a different channel. The outline of the ellipse represents iso-response at half the peak sensitivity. Peak sensitivity at the center of the ellipse forms a series of

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points of decreasing temporal frequency with increasing spatial frequency. This is the configuration of a set of spatial channels maximally sensitive a t very low to low temporal frequencies specialized for the analysis of spatial structure.

"

c

P

d

log spatial frequency Figure 4 . A set of spatial channels derived from empirical studies of threshold detection and identification of sine wave stimuli. (After Graham, 1989.)

Assume that the spatial analyzers are arranged as shown in the above figure. Assume further that they are labeled not only with respect to spatial frequency but also with respect to "figureness." The channels tuned to the lowest spatial frequencies signal that the region from which the response originates is ground. The channels tuned to the highest spatial frequencies signal that the region of origin is figure. The channels in between generate increasingly weaker ground responses as their most sensitive spatial frequency is near the middle then

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increasingly stronger figure responses as we move towards high spatial frequency tuning. In two adjacent locations that stimulate the same analyzer, the region which elicits the greater response will be seen as figure, if the peak responding analyzer is tuned to high spatial frequencies, and ground if the peak responding analyzer is tuned to low spatial frequencies. Where different regions stimulate different analyzers, we will assume that the region's figure/ground response is determined by the most vigorously responding channel. The overall appearance of the display will be determined by the relative figure/ground labels of the regions modulated by the relative response strength of the channels being compared. With these assumptions we might explain our spatial frequency, contrast sensitivity, ground shift results in the following way, Since fluctuations in the ambiguous figure are not consequent to changes in the stimulus configuration which is unchanging, these changes in figure/ground organization are understood to be due to time varying activity in the spatially separated regions. When fluctuating activity in the lower spatial frequency analyzers is relatively great, the region will be seen as ground, and spatial sensitivity will be momentarily enhanced for lower spatial frequencies. When the activity in the high spatial frequency analyzers is greater, the region will be seen as figure, and spatial sensitivity will shift to higher spatial frequencies. An assumption in this model and in the models to follow, is that perceptual relationships like figure and ground, three dimensional structure, occlusion, and transparency are not only computed from the initial output of channels in early visual processing. These relations are represented by sustained ongoing changes in the activity and sensitivity of the channels for the duration of the percept. The representation of stable higher order perceptual relations by units that appear as elementary analyzers in most psychophysical contexts has been a theme of work that we have done for many years. We have found spatial frequency specific adaptation in a retinal area corresponding to an untextured portion of the visual field, if that portion is perceived to be part of a three dimensional object which occludes the grating (Weisstein, 1970: Weisstein. 1973; Weisstein and Maguire. 1978). We have found that a line is detected better if it is part of a two dimensional representation of a three dimensional object, than if it is presented alone or in a flatter less coherent context Weisstein and Harris, 1974: Williams and Weisstein, 1978). Extensive discussion of related findings by ourselves and others (n.b. Nakayama et aL.1989. Shimojo et aL.1988; Shimojo and Nakayama. 1990) is found in Maguire et al. (1990). A model of the representation of perceptual relations by early visual processing is elaborated in Maguire and Weisstein (199 1). We consider below a number of the experiments that we have performed in the past few years, and consider the application of the spatial model described above to that data. We believe that while explaining a number of our results, the spatial model is not adequate to explain the full range of figure and ground effects, nor is the alternative temporal channels model which follows it. Finally we consider a model which we do feel is adequate which combines information from spatial and temporal channels.

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Spatial determinants of figure-ground perception We have in numerous experiments found that the spatial frequency composition of a region contributes to the perception of that region as figure or ground. Using a variety of configurations that produce figure/ground ambiguity (the Rubin faces/vase picture as in Figure 2, interposed Maltese crosses in a circular pattern as in Figure 1. a bipartite field. a center-surround configuration, and a diagonal/triangles ambiguous figure) sinewave gratings of different spatial frequencies are used to fill the regions with texture. In this way differences in spatial frequency define the regions (see Figure 2). Figure-ground stability as a function of spatial frequency difference is measured by the percentage of time one of the regions is perceived as figure. We found that the region filled with the lower spatial frequency was perceived predominantly a s background, for all these configurations (Klymenko and Weisstein, 1986; Brown and Weisstein. 1988; Wong and Weisstein, 1989). As the octave separation between the regions increased, the percentage of time the higher spatial frequency region was seen as figure increased.

Temporal determinants of figure-ground perception Several lines of evidence suggest that flickering regions of an ambiguous region are predominantly perceived as background, while adjacent nonflickering regions are perceived as figures (Wong and Weisstein, 1984. 1985. 1987; Meyer and Doherty, 1987). This is true whether the regions are outlined by contours or merely defined by temporal changes. Using on/off flicker (where the spatial pattern is replaced by a spatially uniform field of the same space averaged luminance on each half cycle, this "flicker-induced ground" effect was optimal when the flickering frequencies were between 6 and 8 Hz. Maximum perceived depth segregation between the flicker and nonflickering regions also occurred at these rates of flicker. At lower (1.4 Hz) and higher (12.5 Hz) rates of flicker, regions maintained their segregation, but the dominance of a region as figure or ground and the depth segregation between the flickering and nonflickering regions diminished. Klymenko et al. (1989) and Klymenko and Weisstein (1989) explored whether flicker induced orderly figure/ground perception throughout the spatial frequency domain. The display was spatially uniform consisting of a single spatial frequency. Regions were defined by differences in temporal frequency. In different conditions the spatially uniform texture was of different spatial frequencies. An ambiguous pattern consisting of a rightward and leftward leaning maltese cross (see Figure 1) positioned so that they perfectly filled a circular area was defined by the temporal frequency differences. There were four flicker rates (0, 3.75. 7.5. and 15 Hz). of which all combinations were tested, and four spatial frequencies (0.5. 1. 4. and 8 c/degl. In the two experiments, the waveform of the flicker differed, as did the ambiguous pattern (square wave on-off, Maltese cross, Klymenko et al., 1989; contrast reversal, bipartite field. Klymenko and Weisstein, 1989). The general result was that the cross with the higher temporal frequency was perceived primarily as background, regardless

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of the spatial frequency of the whole circular area. The effect of temporal frequency difference was greater for high spatial frequency patterns than for low for the square-wave contrast reversal flicker. In a final experiment, Klymenko et al. (19891 tested displays where low spatial, low temporal frequency patterns. and high spatial, high temporal frequency patterns were compared neither type of pattern dominated the figure response.

The role of depth in figure-ground perception In our figure/ground studies, a concomitant depth effect is also observed. Figure regions are always perceptually localized in front of ground regions. In fact, spatial frequency induced depth between the figure and ground regions can be perceived despite the presence of contradictory stereoscopic depth cues. If the magnitude of the contradictory binocular disparity cue is increased however, a point is reached a t which spatial frequency induced depth is cancelled (Brown and Weisstein, 1988; Wong and Weisstein, 1989). Brown and Weisstein (1988) assessed the amount of depth induced by spatial frequency differences in this way. Crossed disparity was added to one or both regions of a pattern containing sinewave gratings differing in spatial frequency. The display consisted of rectangular areas filled with sinewave gratings. The regions of higher spatial frequency were perceptually localized in front of the lower spatial frequency regions (see also Schorr and Howarth. 1986: Frisby and Mayhew, 1978). Again, the effect was dependent on the relative spatial frequency difference between the regions. When the spatial frequency difference between regions was greater than 1.32 octaves, the higher spatial frequency region tended to be seen as foreground regardless of the disparity imposed on the regions: i.e.. spatial frequency difference dominated binocular disparity as a cue to depth. Using the same configuration, we then instructed observers to cancel the depth induced by spatial frequency differences between the regions by adjusting the disparity of the image so that all regions within the display lay on the same depth plane. Observers consistently placed the regions fill with lower spatial frequency closer in stereo depth than the relatively higher spatial frequency areas. Similar trends were observed when the gratings were placed out of phase. As a control, the procedure was repeated using square wave gratings (which contain many very high spatial frequency components in addition to their fundamental frequency). Although depth was occasionally observed, neither region was reliably placed in front of the other. When stereo depth is supplied to cancel spatial frequency induced depth, the display becomes bistable with frequent figureground reversals. If regions of equal spatial frequency are induced into a particular figure ground interpretation by manipulation of binocular disparity, the stability of this configuration, its resistance to reversal, is determined by the magnitude of the relative disparity differences between the regions. We examined the joint roles of flicker and perceived depth on the perception of figure and ground by stereoscopically cancelling the depth induced by the flickering region (Wong and Weisstein. 1987b).

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The figure-ground context was an ambiguous figure that could either be seen as a diagonal stripe or a pair of triangles. There were no contours to define these regions which were simply composed of random dots. The regions were defined by homogeneous flicker rates and/or binocular disparities. The percentage of time a flickering region was perceived as ground was measured for four temporal frequencies (1.4. 6.3,8.3,and 12.5 Hz) and compared when disparity differences were absent and perceived depth present, or when depth differences were stereoscopically cancelled. Results indicated that temporal frequency induced depth differences between the two regions could be cancelled stereoscopically analogous to spatial frequency effects. Together these data show that spatial and temporal frequency effects on figure and ground organization, function much like binocular disparity differences. The resulting percept with simultaneous appearance of a particular figure ground organization, with particular depth relationships, with texture elements of particular sizes, is the result of a global computation that integrates spatial frequency, temporal frequency and binocular disparity information.

The effects of unidirectional motion on figure-ground organization The analysis of image motion and velocity fields can yield valuable information about how the visual system processes change. Image motion can be a powerful segmentation cue (Johansson. 1976). Wong and Weisstein (1987)investigated how the velocity of moving fields affected figure/ground perception. We used a display consisting of a center and surround region filled with 1 c/deg sinewave gratings. One region of the display was always stationary while the other region moved. The observer was instructed to monitor figure-ground perception in the way described in our previous experiments. We found that as the velocity increased, the moving grating was seen as ground more often than the stationary one. The effect increased with velocity up 8 degrees per second and remained high at the highest velocities tested (32 degrees per second). Since at high velocities observers reported blur or streaking in the images and at very high velocities the stimulus would be indiscriminable from a stationary field of uniform luminance, motion response in figure-ground perception must have a high velocity limit which we did not test. Wong and Weisstein (1989)compared absolute and relative motion between a center-surround display of moving gratings as predictors of relative figure ground segregation. They discovered that the fastest moving grating was generally perceived as ground, but the magnitude of this effect was influenced by whether the center or surround moved in same or opposite directions. This sensitivity to relative motion, implies that the mechanisms computing figure and ground in these experiments are direction selective.

Problems with the spatial model and a consideration of the temporal model A number of the results discussed above would appear to be difficult to explain using the spatial model. At all spatial frequencies

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there was a monotonic effect of temporal frequency on figure segmentation. The effect was more pronounced a t high spatial frequencies than low. I t would appear that the spatial model would predict different effects of temporal frequency a t high and low spatial frequencies. At high spatial frequencies, the effect of raising temporal frequency would be to reduce responding, reducing the figure response and thus producing the monotonic effects we have noted. If all the spatial channels are tuned to relatively low temporal frequencies, then a t low spatial frequencies, a fall-off in channel response with increased temporal frequency should produce a reduced ground response, and an effect opposite to what we observed. If the low spatial frequency channels, respond vigorously a t higher temporal frequencies, the model implies a single set of spatio-temporal frequency analyzers. Even characterizing the spatial channels in this way is problematic for the following reason. The effects of temporal frequency at the middle spatial frequencies where channels neither signal figure or ground very strongly should be less than at high and low spatial frequencies. We also have more recent research that is relevant to the model. Recent research indicates that as the contrast of low frequency gratings is raised, they are more likely to be perceived as figure, but if the low spatial frequency channel carries a ground signal, and responds monotonically to stimulus contrast, the opposite would be expected. Additionally as mentioned, figure/ground relations with moving gratings shows sensitivity to stimulus direction. This implies the channels underlying figure/ground segmentation are directionally selective. Such directional selectivity is generally associated with the temporal channels. We consider a temporal channel model briefly below. Figure 5 presents the outline of a set of directionally selective temporal channels, that appear to be the underlying mechanisms uncovered by experiments that examine subthreshold summation of flickering patterns and discrimination of pattern temporal frequency (see Graham, 1989: Mandler and Makous. 1984). This set of channels can be considered as a pathway particularly sensitive to information about stimulus motion. Individual channels appear to be labeled for the direction of stimulus motion (see Watson, 1986: Graham, 1989). The M pathway is considered to be rich in directionally selective analyzers, and particularly sensitive to stimulus motion (Livingstone and Hubel, 1987) It exhibits relative sensitivity to higher temporal and lower spatial frequency information. (The description of the M pathway also roughly corresponds to the descriptions of transient channels in previous research: see Breitmeyer. this volume: Kulikowski and Tolhurst. 1973.) This pathway has been characterized as playing a critical role in depth, and motion perception. Relative depth and motion are powerful segmentation cues, and our own research has established a strong relationship between binocular disparity and spatial and temporal frequency in determining figure/ground organization. I t has been suggested that the M pathway and not the P pathway is most critical in the segmentation of regions into figure and ground (Livingstone and Hubel. 1987, 1988). We consider a straightforward model of figure/ground organization in which temporal channels play an exclusive role. The model assumes all information from all temporal channels is summed.

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When a region stimulates the temporal pathway strongly that region is more likely than adjacent regions not as strongly stimulated to take on the characteristics of ground. Thus where two regions are ambiguous in their figure/ground relationships the region with the greatest ground response will form the ground. In this view the quick responding temporal channels accomplish the initial segmentation of the image. This in turn permits attention to be directed to regions defined as figure where detailed analysis of figural qualities can be accomplished by the slower responding spatial channels.

log spatial frequency Figure 5 . A set of temporal channels derived from empirical studies of threshold detection and identification of moving and flickering sine wave stimuli. (After Graham, 1989.) The model permits us to make a straightforward prediction. When we measure the spatio-temporal tuning of figure-ground perception, should simply arrive at a surface that represents the

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envelope of the temporal channels illustrated in Figure 5. One proviso should be made to this claim. Figure 5 is based upon threshold measurements of sensitivity. The stimuli used in figure/ground experiments are generally well above threshold contrast. Therefore we expect the actual surface generated to cover larger areas of the spatio-temporal plane than the figure suggests. The spatial frequency dependence of figure and ground is consistent with the model presented above. Since the envelope of the spatial frequency sensitivity of the temporal frequency sensitive channels is low pass one might expect the effects of spatial frequency to be roughly monotonic as we have found. It is worth noting however, that we have found good figure ground segregation between gratings 0.5 and 1 cycle per degree (Klymenko and Weisstein. 1986) in the region where the temporal envelope is relatively flat. If we consider the data reviewed above, the effects of spatial and temporal frequency are generally what one might expect, but there are certain details that appear troublesome for a model that relies exclusively on temporal channels. Klymenko e t al. (1989) and Klymenko and Weisstein (1989) found that there were differences in figure/ground segmentation between square wave on/off and contrast reversal flicker. As the temporal frequency difference Between two regions increased, the magnitude of the effect increased with contrast reversal flicker. Temporal frequency differences with on-off flicker showed leveling of the effect a t the lower spatial frequencies, at the highest flicker rate (15 hz.). Wong and Weisstein (1984) using random dot fields and on-off flicker found peak figure/ground effects a t around 7.5 hz. These differences have been also demonstrated with stereoscopic cancellation as well. With on/off flicker, maximal depth separation between regions (measured by disparity needed to cancel depth effect) is achieved when the background flickers at 7.5 hz. With contrast reversal, maximal effects are achieved a t 15 hz., the highest temporal frequency tested (Klymenko, Weisstein, and Maguire. 1990). The asymptotic behavior of the on-off flicker a t around 7.5 hz might be what a model of the temporal channels would predict given that this value represents peak sensitivity to sine wave flicker. This difference in asymptote for contrast reversal and on/off flicker has important implications for the mechanism of figure/ground segmentation. Kulikowski and Tolhurst (1973) found that threshold flicker sensitivity for the two types of flicker did not diverge a t high temporal frequencies, but that pattern sensitivity threshold did with much greater sensitivity to spatial structure for on/off flicker a t high temporal frequencies. This can be readily understood if we conceptualize on/off flicker as a stimulus composed of a stationary spatial frequency to which a contrast reversing grating of the same spatial frequency has been added. This in turn implies that the channels most responsive to spatial structure may play a role in figure/ground perception, specifically. stimulation of pattern sensitive pathways in a region may mitigate the ground response produced by stimulation of the temporal channels. In other experiments, Klymenko and Weisstein held temporal frequency constant within conditions while spatial frequency was varied. In one condition, the two crosses were filled with sinewave gratings of 1 and 4 c/deg; in the other condition, they were filled with

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gratings of 1 and 8 c/deg. For each of these two spatial frequency conditions, there were four temporal frequencies at which the entire pattern flickered (0,3.75, 7.5. and 15 Hz). Once again, the type of flicker and type of pattern differed between the two experiments. Results indicated that when flicker was absent, the low spatial frequency region was seen predominately as background, consistent with Klymenko and Weisstein (1986)and Wong and Weisstein (1989a).

log spatial frequency Figure 6 . Spatial and temporal channels combined in a single figure. (After Graham, 1989.) In general, with the addition of flicker to the display, the appearance was unchanged or declined slightly with the low spatial frequency less likely to be perceived as background. A dramatic decline in the spatial frequency effect was produced when the display with 1 and 8 cpd underwent contrast reversal flicker at 15 hz. In this case, the standard spatial frequency effect was actually reversed. The general effect of

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flicker then is to obliterate spatial frequency based figure/ground effects and perhaps when high and low spatial frequencies are compared to reverse them (Klymenko et al.. 1989; Klymenko and Weisstein. 1989b). If we assume that differences in temporal channel response to spatial frequency differences are more pronounced a t low temporal frequencies than at high temporal frequencies, one might expect a reduction in spatial frequency produced figure/ground effects, but Kulikowski and Tolhurst found the ratio of flicker thresholds between low and high spatial frequency patterns to be approximately equal a t low and high temporal frequencies (see Kulikowski and Tolhurst, 1973, Figures 7 and 8). They did however find that pattern thresholds for various spatial frequencies converged at high temporal frequencies, which might tend to flatten out figure/ground differences at high spatial frequencies if spatial channels play a role in figure/ground perception. To summarize, we have found that models that rely on spatial or temporal channels alone to explain figure and ground segmentation cannot explain all important aspects of the data we have gathered. The data lead u s rather to consider a model where the perception of figure and ground results from interaction between spatial and temporal channels in the human visual system.

A model of figure-ground perception based on the interaction between spatial frequency channels and temporal frequency channels If we assume both spatial and temporal channels are active and interacting in the perception of figure and ground then our data are explained quite well. Figure 6 shows the most likely distribution and shape of spatial analyzers in log frequency space. Again. the ellipses represent isosensitivity curves where the channel's sensitivity is half its peak sensitivity. Notice that the high spatial frequency spatial channels are more sensitive a t very low temporal frequencies than are the low spatial frequency channels. The extent of individual channels in the figure has been determined by threshold experiments and we assume t h a t they appear wider and overlap more extensively when suprathreshold stimuli of the type we use are processed. This overlap above threshold implies that both figure and ground pathways are activated over most of the spatial and temporal frequency range with the possible exception of the most extreme stimuli (extremely low spatial frequencies flickering a t high temporal frequencies, and stationary extremely high spatial frequency stimuli). The model assumes that spatial analyzers responding to a region bias the percept of that region towards figure, while temporal analyzers responding in a region bias the percept of that region towards ground. For any region, relative figureness is a monotonic function of the pooled spatial analyzer contrast response minus the pooled temporal analyzer contrast response. This can be described somewhat more formally as:

Figureness = F ( C S I rc(a.7) - CTI rc(a.r) )

(11

where S I rc(a.T) is the pooled spatiotemporal luminance contrast response of the spatial frequency tuned channels and TI rc(a,d is the pooled spatiotemporal luminance contrast response of the temporal

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frequency tuned channels for retinal region a in the interval T. Figure however is a relation relative to ground, so a more general formulation would be Figureness = M a x 1 F ( C S I rc(a,z) - CTI rc(a,z) 1 , F ( CSI rc(b,z) - CTI rc(b,z) 1 I

(2)

where the two regions a and b are potential figures. The spatial and temporal responses are time varying functions showing random fluctuations even during fixed input with corresponding perceptual effects such as reversal of figure/ground organization. There is another monotonic function which predicts the strength of a region's figureness measured as the percentage of time during which region a is perceived to be figure. Vividness = V 1 ( CS I rc(a,o) - CTI rc(a,z) )

It may turn out that a ratio between spatial and temporal responses or a ratio between different regions in Equation 3 fits the experimental data most closely. Similarly it is necessary to specify the channel response to stimulus contrast in order to accurately predict the effects of that important variable. A notable feature of the model is that it does not assign the calculation of figure/ground segmentation exclusively to either the spatial or temporal channels, Activity in both normally underlies figure/ground perception, and activity in either is sufficient for figure/ground segmentation. The absence of input from either spatial or temporal channels reduces Equation 3 to Strength= V ( CS I rc(a,z) - C S I rc(b.7) )

(4)

Strength = V ( CTIrc(a,z) - CTIrc(b,z) 1.

(51

or

This relationship will become important later when we reject the idea that either an M or P stream (e.g. Livingstone and Hubel. 1987 vs. Ingling and Rigby. 1990) exclusively codes for depth (see also Cavanagh, 1989).

The model is sufficient to explain key aspects of our data. With low spatial, low temporal frequency sine waves, a region that contains the higher spatial frequency sine wave will be perceived to be figure. This is because the spatial channel response increases with increasing spatial frequency in this range. In addition at lower temporal frequencies and throughout the spatial frequency range the contribution from the temporal channels will diminish continuously a s spatial frequency increases further increasing the figureness signal associated with the higher spatial frequency. The following data are explained. Over the spatial frequency range that we have tested, the higher spatial frequency is more likely to be seen a s figure. Over the temporal

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frequency range that we have tested, the higher temporal frequency is more likely to be seen as background. When the whole pattern flickers at high temporal frequencies, the differences between spatial frequencies will be diminished because the gradient is shallower above the 1 degree/second line. For the same reason, when two temporal frequencies are compared at the same spatial frequency with contrast reversal, the effect is greater for higher spatial frequencies. The inhibitory interactions between the pathways find some support in the fact that specification of a region a s figure or ground affects the spatial and temporal sensitivity to patterns in that region regardless of other stimulus characteristics. We also believe that changes in the appearance of a region associated with the shift from a ground to a figure percept, can be explained by a shift in the composition of analyzers most responsive to the pattern. These changes include the following: texture elements appear larger when an ambiguous region is perceived as figure than when it is perceived as background (Maguire and Weisstein. 199 1). [See also perceptual shrinkage associated with amodal contours, Kanisza and Gerbino (19821.1 Depth cues enhance the probability that a region will be seen as in front, even as a region appearing to be a figure brings it closer in depth. All these changes reflect a perceptual coupling of such stimulus dimensions as binocular disparity, size/ spatial frequency, and motion/ temporal frequency. We believe these perceptual effects are best explained by a shift in activity in the transition from figure to ground to a dominance of one pathway or another different in sensitivity to all of the above stimulus dimensions (see Maguire and Weisstein. 1991, for a discussion). Such a transition in turn may be accomplished by an inhibitory coupling of temporal and spatial signals a t some level of the visual system.

Fundamental implications of the combined model The model has two major implications regarding figure and ground. The first is that the perception of figure and ground is completely relative. The comparator of Equation 3 does not require information about where the signals come from, spatial channels alone, temporal channels alone or a combination of spatial and temporal channels. It merely assigns figure to the larger of the summed signals. This implies for instance, that any manipulation that increases the activity of spatial channels in one location rather than a n adjacent location will increase the perception of figureness in that location. The second implication is that the input from spatial and temporal channels to the figure mechanism in a region is antagonistic. Any manipulation that increases spatial channel activity over temporal channel activity increases figureness. Any stimulus manipulation that increases temporal channel activity over spatial channel activity decreases figureness. These principles allow u s to make a number of predictions about figure/ground organization as a function of varying stimulus parameters. We consider some predictions based upon varying the contrast of test regions. We have found that in the contrast region well above threshold, a stationary grating that appears as ground will reverse to figure as its contrast is raised provided its contrast becomes sufficiently greater

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than its neighbor. The effect of increasing contrast in general is to increase channel response broadly. Temporal channels however show high contrast gain and response saturation a t relatively low contrast (Pantle and Sekuler, 1969; Pantle. Lehmkuhle, and Caudill, 1978). This means that when one varies the contrast of stimuli well above contrast threshold, the effects are limited to the spatial channels since the temporal channels are saturated. Weisstein and Wong (1990) used a disc and annulus configuration filled with differing spatial frequencies and observed figure/ground organization. In one condition the spatial frequencies of the disc and annulus were the same: a shift in phase defining the regions. They presented the disc for one minute and measured the percentage of time during which the disc was perceived a s figure. They found that a n increase in contrast in either region increased its figureness. The region of lower contrast would start as ground, and with increasing contrast it finally would be seen as figure. In earlier experiments with random dot fields we looked a t temporal modulation depth of the flickering fields Wong and Weisstein. 1984). We found that 100% modulation of a region, flickering in the range of 6- 12 hz.,produced the greatest depth separation and ground response to that region relative to a stationary field of dots (Wong and Weisstein, 1984). These 100% modulation fields are essentially on/off flickering stimuli. Modulations of the random dot fields less than 100% created substantial stationary components in the pattern. A modulation of O?! would simply have been a stationary field of random dots. So it is consistent with the above theory that removing stationary components from the display would decrease spatial channel activity and increase the ground response of the field. The use of random dot stimuli makes contrast predictions which are based upon the contrast response to grating patterns somewhat difficult since the random dot fields are broadband stimuli and may stimulate many channels. We intend low contrast experiments with contrast reversing sine wave patterns in the future to determine whether raising contrast will increase ground response in the contrast range where the temporal channels are monotonically increasing in activity.

A model of figure-ground perception based on antagonistic P pathway and M pathway interactions in the visual system The temporal and spatial channels we have described closely resemble the transient and sustained channels of earlier work (Kulikowski and Tolhurst, 1973: Breitmeyer, 1975; Breitmeyer and Ganz, 1976; Weisstein et al., 1975. Meyer and Maguire, 1977). With Breitmeyer (this volume) we feel a case can be made that these psychophysically defined channels correspond closely to the anatomically defined parvocellular, P pathway and magnocellular. M pathway in the primate. By this reasoning the P pathway corresponds to the spatial (sustained) channels, while the M pathway corresponds to the temporal (transient) channels. We can make the link explicit by rewriting Equations 1-3 substituting P I rc(a.T) (parvo response), and M I rc(a.7) (magno response) for the spatial and temporal frequency tuned channels, respectively.

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Figureness = Max ( F ( CPI rc(a,z) - CM I rc(a.7) ) ,

where two regions a and b are potential figures. Strength = v 1 ( CP I rc(a,.c) - CM I rc(a.7)

Since figure/ground segregation inevitably leads to perceptions of relative depth between figure and ground regions, a two pathway model of figure/ground segregation would appear to contradict the view that depth perception is largely accomplished by the M pathway (Livingstone and Hubel, 1987). There appears now to be ample evidence that depth perception is not simply accomplished by M pathways. The argument for a n exclusive magnocellular mechanism is principally supported by demonstrations of difficulty in depth perception with isoluminant figures. The assumption that isoluminance leaves parvocellular function intact while eliminating magnocellular function however, has been strongly challenged recently (Cavanagh. 1989: Ingling and Grigsby, 1990; Logothetis et al., 1990; Breitmeyer, this volume). Isoluminance does not appear to be a n effective way of segregating magnocellular from parvocellular function. At the same time other evidence does suggest a role for P pathways in depth perception. This includes the loss of fine stereoscopic discrimination in rhesus monkeys after parvocellular but not magnocellular lesions (Schiller et al., 1990) and the finding that monocular depth perception is normal with stabilized images, stimuli which should effectively isolate the P pathway (Ingling and Grigsby, 1990). The loss in depth perception and clarity of figure/ground reported with isoluminant stimuli while not complete is striking, but current research indicates that this may stem from loss of activity in both P and M systems (Logothetis et al., 1990). Reduction of activity in P and M pathways would lead to a loss of depth and figure/ground stability in our model. This is can be seen by considering a n extreme example. Where one region strongly stimulates the M pathway, and another strongly stimulates the P pathway. A large figure-ground difference is computed for these two regions. As magnocellular and parvocellular activity is reduced. this difference gets smaller and smaller, reducing apparent depth and stability of perception. The correspondence of P pathway and spatial channels should be discussed. The P pathway has been described a s a system specialized for color information (see Shapley. this volume). Color channels have been found to have extremely poor spatial resolution (Poirsson and Wandel. 1990) making them very poor candidates for the spatial channels. We have been looking however a t luminance not color contrast and there are data around to suggest that high spatial frequency sustained information is carried by the P pathway. Kelly (1981) found that the peak of the contrast sensitivity function was

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shifted to higher spatial frequencies for stabilized grating images. There is also considerable research in the macaque to suggest a relationship between the P pathway and the processing of high spatial frequency information. Parvocellular neurons generally have smaller receptive fields and show tuning to higher spatial frequencies [Derrington and Lennie. 1984). There is 2-DG uptake in parvocellular sites with high spatial frequency luminance grating stimuli (Tootell et al.. 1988). Chemically induced lesions in the parvocellular layers reduce contrast sensitivity across the full range of spatial frequencies including high spatial frequencies (Merigan, 1989: Logothetis et al.. 1990).

Suppression of M pathway response by diffuse red light and figure-ground perception The explicit linkage of our spatial and temporal channels to P and M pathways respectively allows us to make some psychophysical predictions based upon what is known about the physiological properties of magnocellular and parvocellular pathways. Diffuse red light is unique in that it is an effective suppressor of magnocellular activity (Livingstone and Hubel. 1984. 1987: Derrington e t al.. 1984). Breitmeyer and Williams (1990) found a psychophysical analog showing that diffuse red light could be used to suppress transient masking responses in a metacontrast paradigm. In a new set of experiments Weisstein and Brannan. 1991) we have examined the effects of diffuse red light on figure/ground perception. We used a bipartite field comprised of horizontal gratings divided in the middle. On one side of the bipartite field was a 1 c/deg sinewave grating, on the other a 1.4 c/deg sinewave grating. Using achromatic gratings, the 1.4 c/deg grating consistently appeared "in front of' the 1 c/deg grating. However, when one side of the field was diffusely illuminated by red light, and the other by diffuse green light matched in luminance, the red grating consistently appeared "in front of' the green grating. This was true regardless of which spatial frequency was illuminated by the red light. In fact the result is the same when both regions have the same spatial frequency. The red side also displayed an interesting appearance: the red and black stripes appeared to be somewhat three-dimensional and wavy, as if the red was "in front of' the black, and the black "in front of' the green grating. We also tested very high spatial frequencies (15 and 21 c/deg). As achromatic gratings, neither appeared significantly in front of the other. When exposed to diffuse red and green light, no change in figure/ground appearance or depth occurred. Finally, we looked at red and green gratings presented alone, to determine if the effect is absolute or relative. Although there was minimal waviness to the red 1 c/deg grating presented alone, the strong effect seen with the bipartite field was not present. These findings provide strong support for the model. If magnocellular activity in a region is reduced, by whatever means, be it by the spatial and temporal composition of the area or its spectral characteristics, the region is more likely to be perceived as a figure and in front of adjacent regions. The chromatic effect is not evident with high spatial frequencies, because the spatial patterns elicit minimal activity from the magnocellular pathway, hence there is little

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or no activity to suppress. Taken together with the wealth of evidence relating to spatial and temporal effects on figure-ground perception, this preliminary chromatic data supports the hypothesis that the M pathway codes for background, while the P pathway codes for foreground. The actual appearance of a pattern is determined by comparison of M and P outputs.

Further implications of the model As originally proposed by Livingstone and Hubel (1987,1988) the organization of the primate visual system represented a true parceling of function into different processing streams with most form related functions handled exclusively by the M system. The model of figure/ground processing that we propose assumes that M and P systems overlap greatly in their response characteristics with differences in sensitivity generally being differences of degree. The more general question is whether it is necessary or desirable for different analyzers, channels or pathways to code exclusively for one feature or "primitive" or another. This has certainly been a popular idea among vision scientists (Livingstone and Hubel. 1987; Treisman and Gormican, 1988; Zeki, 1978). We are often disappointed to find that still another promising class of detectors, fails to code dimensions separably or shows broad responding across numerous dimensions. Empirically it appears that there is extensive overlap in response characteristics between the different analyzers, channels, and pathways. We do not believe that the extensive overlap in responding of "primitive" analyzers precludes their being labeled. We expect that analyzers carry labeled information, and this information has sensory effects, but is also crucial in producing perceptual properties. We perhaps fail to understand the labeling because perhaps these labels are terms in various heterarchical computations (e.g. Grossberg, 1987a.b). We seriously doubt that labels associated with analyzers reach thresholds as perceptual primitives of any sort. (In this connection, it is noteworthy that visual search paradigms where "primitive" features are supposed to "pop out" are heavily dependent on image context such as direction or lighting and structure of distractors.) We believe that the response components of early visual processing overlap because perceptual relationships are coded by broad arrays often carrying redundant information. The current model of figure/ground segmentation will serve to illustrate the point. Figure and ground relationships are coded broadly by analyzers in both P and M streams. Only when that information has been integrated do the current figure/ground relationships emerge. These same analyzers simultaneously are labeled to carry information about size, direction of motion, etc. of the images in the visual field. Because all this information passes through the same sets of analyzers we note empirical correlations between image size, direction of motion etc. and figure/ground organization. Nor do we feel that such a model of necessity implies a "higher" level a t which M and P input forms the basis for figure/ground computations. It appears t h a t these computations take place in some sense a t the same level a s conceptually more fundamental feature extraction operations.

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To state this another way, our model rests on the assumption that fundamental perceptual processing is part of what early visual components do. We have held to this idea for a long time (Weisstein. 1968. 1969, 1970, 1973; Weisstein and Maguire, 1978) but it is only recently with the renewed interest in M and P streams that the idea has received widespread acceptance. The most primitive sensory properties such as local brightness, chroma, edge orientation, etc.. are influenced by complex perceptual relationships and so we might expect that the analyzers whose responses appear to be most correlated with these elementary sensory experiences will show complex responses to a broad array of stimulus dimensions (Weisstein, 1973; Weisstein and Maguire, 1978; Maguire et al., 1990). Figure/ground relationships increase our confidence in this view. In a sense they illustrate the converse of what we found in early research. Earlier we found that complex perceptual relationships would affect simple sensory judgements. In our figure/ground experiments, simple sensory differences between regions affect fundamentally the way they are perceived, affecting in turn apparent form and depth. We need to expand our understanding of the visual system by building models that incorporate these traits in there fundamental organization.

Summary and conclusions We have found, in a number of studies, correlations between the spatial and temporal frequency composition of regions of ambiguous displays and the determination of which regions of the image appear predominantly as figure. In a search for a mechanism, we have found that models that are restricted to spatial or temporal channels alone cannot explain all the data associated with this effect. A model which assumes antagonistic interactions between a set of temporal channels coding regions for ground and a set of spatial channels coding regions for figure appears to provide a fair explanation for our results. We associate these sets of channels with the magnocellular and parvocellular pathways in the primate visual system. New data on effects of diffuse red light on figure/ground perception, and the effects of stimulus contrast on figure/ground perception support the model overall. We conclude that M and P pathways can be identified with neural signals for ground and figure processing respectively. The appearance of the segmented visual image will be determined in part by the relative strength of activity in the two pathways. Relative activity in the two pathways may also determine apparent size, depth, brightness and flicker frequency of the regions. We are currently pursuing experiments to explore these possibilities. Acknowledpments - We would like to thank Davida Teller, Norma Graham, Pat Phillips, Nancy Jerome, Jesse Lemisch. and Andrea Hodelin.

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Ap licalions of Parallel Processing in Vision J. (mitor) Q 1992 Elsevier Science Publishers B.V. All righfs reserved

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Cooperative Parallel Processing in Depth, Motion and Texture Perception DOUGLAS WILLIAMS

Introduction There are two distinct geniculostriate pathways in the visual system; one variously called the parvocellular, P. or color-opponent system, and the other the magnocellular. M. or broad-band system. As discussed in more detail in earlier chapters of this book, these have different physiological properties and possibly subserve different visual functions (Zeki. 1978: Lennie, 1980: Van Essen and Maunsell, 1983: DeYoe and Van Essen. 1988). The broad-band pathway is assumed to mediate motion and depth perception, while the color-opponent system is involved in texture perception (Livingstone. 1988). Recent physiological results have cast doubt on a strict segregation of these tasks exclusively to one or the other of these pathways (Logothetis. Schiller. Charles, and Hurlbert. 1990). There are however many aspects of stereo, motion, and texture perception which do depend on parallel processing but are not related to the chromatic/broad-band pathway controversy. It is to these aspects of parallel processing to which this chapter is devoted. The parallel nature of visual processing results because visual information is carried by independent spatially localized mechanisms or filters (Campbell and Robson. 1968; Blakemore and Campbell, 1969; Graham and Nachmias. 1971: Sachs, Nachmias and Robson. 1971). The visual scene is in effect fragmented into local entities. Perception requires the integration of these local responses into a global construct. A major challenge confronting psychology is that of understanding how the billions of neurons within the human brain interact to process sensory information and generate behaviorally appropriate responses. What is known is that these myriad neurons are interconnected in networks whose complexity almost defies description. The potential computational power represented by this rich interconnectivity has motivated the development of network models for brain function that are based upon parallel distributed processing (Rumelhart and McClelland. 1986). The informational unit in a parallel distributed network is represented not by the activity of an isolated processor but

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rather by the parallel activity in a distributed, interconnected set of such processors. Parallel distributed processing is essentially a variant on a form of interaction that has been known for some time from the study of non-linear systems - cooperativity. If the local elements of a parallel network are extensively interconnected and are permitted to interact, then global behavior can be generated that would not occur if the mechanisms were isolated from each other. Such behavior is termed "cooperative." According to the Gestalt school of thought, the act of perception involves more than a simple assimilation of individual sensations. Cooperativity in fact complements well the Gestalt expression that the whole is greater than the sum of its parts.

Depth The first evidence of cooperative neural parallel processing was in visual depth perception. Although we live in a three-dimensional world, its image on our retina is only two-dimensional. Each eye, however, views the world from a slightly different angle. By using this disparity between the two eyes, it is possible to recover the third dimension of information - depth. In order to do this, it is first necessary to be able to determine which retinal projections in the left and right eyes correspond to the same object in the visual field. This is not a trivial problem. For example, consider the case for which the object is an array of four identical dots equally spaced in a horizontal row. There is no apriori information available to determine which dot retinal images in one eye correspond to which in the other eye. In fact with four dots, there are 24 different depth combinations for the four dots which will produce the same two retinal projections. Each combination will be distinguished by which dot retinal projection in one eye corresponds to which dot projection in the other eye. The human visual system must determine which of the 24 potential combinations is the correct one. The combinatorial difficulties can become horrendous for random dot stereograms which consist of thousands of identical dots (Julesz. 1966). The problem is said to be under-constrained, in that there is not enough inherent information in the two retinal images to determine an unambiguous solution. In spite of this difficulty, the human visual system can reliably and quickly solve the correspondence problem. There is evidence that cooperative processes play a critical role in solving this problem. Extensively interconnected parallel networks which are cooperative are capable of exhibiting three properties: multistable states, order-disorder transitions, and "hysteresis." Hysteresis is a form of memory in which a system, having reached a stable state, shows resistance to further change. A consequence of such behavior is that the system's response depends on the history of stimulation. Hysteresis has been demonstrated for binocular stereopsis (Fender and Julesz. 1967). Fender and Julesz found that it was necessary for the left and right images for a stereo pair of random dot patterns to be moved within 6 minutes of visual angle before they fused into a single stereoscopic percept. Once fused, however, the disparity between the two halves could be slowly increased to 2 degrees before the single

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fused percept split into two. Once fusion was lost, the stereo pair had to be returned to a disparity of 6 minutes before refusion was reestablished. The amount of disparity required to fuse or split apart the two stereograms thus depended on the initial perceptual condition and direction of the disparity change. The response of the system is dependent on the history of stimulation. The lag in the change of state of the system (i.e.,from fused to split and vice versa) with stimulation is indicative of hysteresis. In their experiments, Fender and Julesz used stabilized retinal images. As such the hysteresis could not be attributed to the oculomotor system, but rather reflects neural parallel cooperative processing. As discussed above, given the ambiguities inherent in the correspondence process, the computational task represented in binocular stereopsis is said to be under-determined. Marr and Poggio (1979) proposed two constraints which must be applied to the sensory information for the brain to resolve this computational difficulty. The first stipulates that each point in the retinal images be assigned one and only one disparity value. This requirement is based on the principle that every point in physical space has a unique position. The second constraint posits that disparity values vary smoothly almost everywhere a s a consequence of the continuity of physical matter. Cooperative algorithms that implement these constraints have proven successful in resolving the matching problem and extracting disparity information (Sperling, 1970; Dev. 1975: Nelson,1975; Marr and Poggio, 1976). The constraints are incorporated in these models by means of the type and configuration of interactions. In the most general terms, the cooperative interactions which are common to all the models are nonlinear excitation between units of similar disparity tuning and nonlinear inhibition between units tuned to different disparities. These interactions are sufficient to provide an unambiguous solution to the correspondence problem and also exhibit hysteresis. Before considering other aspects of parallel processing, it is worth considering the function of binocular cooperativity. In normal vision random, small-amplitude eye movements occur. As a result, binocular images are constantly going in and out of registry. Since a cooperative system contains a lag between input and output (hysteresis). it will reduce such noise. Therefore, even though we constantly have oculomotor noise, because of our parallel cooperative system perceptually we have stable binocular stereopsis.

Motion

The motion correspondence problem The correspondence problem is not unique to stereopsis. An analogous paradox arises in motion perception. Within the framework of motion, correspondence is defined a s the process that identifies elements in different views as representing the same object a t different times. This maintains a perceptual identity of objects in motion. The difficulty of the motion correspondence problem can be illustrated using a pattern consisting of random dots. If a set of dots is displaced, there is no inherent information to determine which dot in the initial position matches which dot after the displacement. Intuitively it might

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be expected that a dot is matched or is perceived to move to the nearest displaced dot. However, this simple rule does not always hold (Ullman. 1979). There is evidence t h a t the solution to this correspondence problem requires parallel cooperative interactions. The evidence comes in the form of a phenomenon called "pulling." If the elements in a parallel network are isolated, then the action of a few elements could not influence the others. On the other hand, if cooperative interactions are permitted, the effect of a few elements could propagate throughout the network and change its overall state. Such pulling has been demonstrated in motion perception by Chang and Julesz (1984)using random dot stimuli. The stimuli are constructed such that the motion for every dot is ambiguous. That is. each dot has a potential matching dot after displacement to the left and to the right. Dots are thus likely to be perceived as moving left or right with equal probability. Chang and Julesz demonstrated that if only 4% of the dots are biased to move unambiguously in one direction, then all dots are perceived to be moving in that direction. That is, just 4% is sufficient to pull the entire system to one perceptual state. This phenomenon requires interactions between mechanisms. J u s t as in the case of binocular stereopsis, such a cooperative property in the visual system would maintain a stable motion percept in the presence of noise.

Global coherent motion In the preceding example we have seen a global percept determined by the activity of only a few local elements. There are several demonstrations in which a collection of localized motion vectors, each moving in a different direction, can produce the perception of global coherent motion moving in only a single direction (Adelson and Movshon. 1982;Williams and Sekuler, 1984). An example of this phenomenon is a stochastic random dot cinematogram for which each dot takes an independent, two-dimensional random walk of constant step size (Williams and Sekuler. 1984). Specifically, all dots move the same distance from frame to frame. However, each individual dot's direction of displacement from one frame to the next is chosen at random from a uniform distribution of directions. The resulting perception is dependent on the range of the uniform distribution (Williams and Sekuler. 1984). If the range of the uniform distribution of motion directions extends over a full 360 degrees only the local random motion of the individual dots is evident. This appears very similar to the noise of a detuned television set. However, if the range of the uniform distribution is 180 degrees or less, a percept of global coherent motion is generated and the pattern appears to flow enmasse in the direction of the mean of the distribution. This is true even though the individual perturbations of the dots are still evident. This looks like individual snowflakes that, although each perturbed individually by wind currents, together appear to drift together in one direction. Control experiments demonstrated that the direction of motion of the global coherent motion percept does not simply represent the average of the directions of motion of the local motion vectors (Williams and Sekuler, 1984). If the perception of global coherent motion is a result of cooperative processing, it would be reasonable to expect the percept to

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exhibit hysteresis. That is, one could measure the transition points marking the change from global coherent motion to local random motion and vice versa by gradually changing the directional content of the stimulus between the two extremes of a unique distribution with a range of 180 degrees or less and a uniform distribution with a range of 360 degrees. If the directional content of the stimulus for which these transitions occur depends on whether the perceptual change is from local to global motion or from global to local motion, then the results are indicative of hysteresis. The experimental results (Williams, Phillips, and Sekuler. 1986; Williams and Phillips, 1987a) confirm the existence of hysteresis for the global coherent motion percept. In addition, we were able to account for this hysteresis by cooperative, nonlinear excitatory and inhibitory interactions among direction-selective mechanisms for motion. The stimuli were dynamic random dot cinematograms, comprising 512 dots, generated by computer. Each dot took an independent, two-dimensional walk of constant step size (0.9 degrees]. The direction in which any individual dot moved was independent of its own previous displacement as well as the displacements of the other dots Williams and Sekuler. 1984). The direction of motion for each dot was chosen from either 1) one of two uniform distributions, or 2) a mixture of these two distributions. When all the dots drew their movements from a uniform distribution extending 360 degrees, only the local random motion of individual dots was evident. However, when all the dots drew their position from a uniform distribution of 180 degrees or less, the dots appeared to flow together in the direction of the distribution mean, although individual perturbations were still evident. In all experiments the mean of the signal distribution was chosen to be upward. The 180 degree and 360 degree distributions are referred to as the signal and noise distributions, respectively. When dots drew their movements from a combination of these distributions, each dot's displacement came randomly from either distribution. The resulting perception depended on the relative proportion of noise versus signal. Two types of trials were run in random order. In one type, the direction of motion for each dot was chosen initially from the signal distribution. This produced a percept of upward flow. After a random interval lasting u p to 12 seconds, the proportion of dots drawing directions from the signal distribution was progressively decreased and simultaneously the proportion choosing from the noise distribution increased. This continued until the observer responded that the cinematogram changed its appearance from upward flow to local random motion. After such a response, the proportion of signal continued to decrease for a random interval of up to 6 seconds. Then the process was reversed, with the proportion of signal increasing until the subject responded that the upward flow had reappeared. This response terminated the trial. For the second type of trial, the stimulus sequence was reversed. We started with all dots choosing directions of motion from the noise distribution which generated an initial percept of local random motion. The points of transition to a perception of upward flow and back again to local random motion were then measured. These two different trial structures, signal first versus noise first, were designed to produce different histories of directional

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exposure. This should reveal any perceptual biases dependent upon the history of stimulation. For both trial types, the signal to noise ratio was changed slowly, with the proportion of dots sampling from each distribution changing by only two dots per frame. At 10 Hz (the frame rate of our display), it took a minimum of 25 seconds for the display to shift from complete distribution on one distribution to complete dependence on the other. Observers viewed monocularly the center of a circular display subtending 16 degrees in diameter. The dots were presented a t two

"Upward"

"Upward"

"Locat'

"Local"

Dbserver TKD Sgnal rrnge.1 00

,

c

n

a

2

II

Upward"

Signd ro

"Upword"

a"

HH

c

=90a

HH

0 .c

"LocaI"

"~ocal" Signal range = 10

n-+

"Upward"

Y o c a 1''

-f

Signal range = 1.

"Upward"

"Local" 1

C

1

I

I

I

l

I

I

I

1

0.2 0.4 0.6 0.8 1 Proportion of Signal

I

C

Proportion of Signal

Figure 1. PerceDtual transitions measured under two different histories of stimuius exposure for three signal distributions. The results, for both observers J.F. and T.K.D., were obtained for signal distributions whose ranges were: 180 degrees, top: 90 degrees, middle; 1 degree, bottom. Measurements were collected using a step size of 0.9 degree. Data points show proportion of "signal" dots required for perceptual transition from local random motion to global upward flow ( 0 ) and for perceptual transition from global upward flow to local random motion ( 0 ) .Error bars indicate one standard deviation (100 measurements). In each panel the separation between transition points measured with the different exposure histories is and index of hysteresis. Note the narrowing and the leftward shift of the profiles with decreasing signal range.


173

times threshold luminance against a dim background. One hundred measurements were made over five sessions for each of three naive observers. This experiment was also repeated using two narrower ranges of signal distribution: 90 degrees and 1 degree. Each of the three signal distributions generated a different history of exposure. It is to be expected that as the distribution narrows the signal would become more effective in stimulating directionally selective visual elements that are tuned to upward motion. As a result, the occurrence of a transition between perceived states might require fewer dots. The results from two observers are shown in Figure 1. Similar results were obtained for the other observer. For each observer each panel illustrates data for a different range of signal. Notice that the transitions differ for the three signal ranges: 180 degrees, 90 degrees and 1 degree. More significantly, the transition from local random motion to upward flow requires a larger number of dots sampled from the signal distribution than does the transition from upward flow to local random motion. The two types of transition occur at significantly different ratios of signal to noise for all three signal distributions (P < 0.005). We considered and rejected a number of alternate explanations before attributing our results solely to neural hysteresis. For example, the results were unaffected by the use of a fixation point, suggesting that eye movements played little or no role in the results. Also, the motion after-effect, or waterfall illusion, cannot be responsible for our results since this after-effect would have facilitated rather than retarded the transition from upward motion to noise. Finally, given the slow time course for changing the signal proportion, reaction time could be dismissed as a possible explanation. We needed a more complete account of how spatial parameters might affect hysteresis before we could develop a simple network to describe our results. We used a 180 degree signal distribution and made measurements under four additional conditions: 1) with a fourfold decrease in the spatial density of the cinematogram's dots, 2 ) with a four-fold decrease in the area of the display, 3) with a nine-fold decrease in step size, and 4) with the display shifted horizontally into the periphery of the visual field so that the nearest dot was 4 degrees from fixation. The results for all four conditions did not differ significantly from the original measurements (Williams and Phillips, 1987a). It is probable that extreme changes in the variables would affect the hysteresis characteristics. However, due to these data and to previous results suggesting that spatial variables have little effect on the dot interactions responsible for motion in cinematograms (Baker and Braddick. 1982: Williams and Sekuler, 1984). we chose not to treat space explicitly in the development of a model network to account for our results. Our model comprises a set of direction-selective mechanisms which cover all 360 degrees of motion direction, with each mechanism having a gaussian profile for directional sensitivity. Based on previous results (Williams, Tweten, and Sekuler, 1984). the half-amplitude halfbandwidth of each mechanism's gaussian sensitivity profile was set to 30 degrees. The model, whose mathematical formulation is a modification of the cooperative neural network previously proposed by Wilson and

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Cowan (1973).assumes nonlinear excitatory interactions among mechanisms sensitive to similar directions of motion and nonlinear inhibition among mechanisms sensitive to different directions. The dynamic response of this cooperative system can be represented by a pair of coupled differential equations. For the excitatory activity, El. in direction channel i:

where S is a nonlinear function of sigmoidal shape, Pi is the external input to channel i, and alJ and by are the excitatory and inhibitory weights, respectively, of channel j with respect to channel i. A similar equation gives the inhibitory activity 11. in channel i:

where S is again the nonlinear function of sigmoidal shape, and cIJand dg are the excitatory and inhibitory weights, respectively. of channel j with respect to channel i. The functional form of the nonlinear sigmoidal function S is given by:

In general terms, interactions such as those in Equations 1 and 2 promote the formulation of stable coalitions between similarly tuned elements within the network (Feldman and Ballard, 1983). These neural coalitions can in turn produce various cooperative properties, including hysteresis. We constrained the parameters of the model so that the model behaved in what is defined (Wilson and Cowan, 1973) as the active transient mode. In this mode, the system shows hysteresis, switching back and forth between different states of activity. The perception of local random motion is represented in the model by a steady state of uniform activity across all mechanisms. Conversely, global upward flow is represented by a steady state in which all the activity is localized about the mechanism selective for upward movement. A transition point can be defined by the proportion of signal at which the network switches between these two states of activity. The results from this model are shown in Figure 2. Dashed lines represent the transition points calculated from the model using a single parameter set. I t is clear that the model captures both the leftward shift and the narrowing of the hysteresis profile with decreasing signal range. The model's behavior can be easily explained. As signal range decreases, more activity is concentrated in fewer motion selective elements arrayed about the upward direction. As a consequence, a smaller proportion of signal dots is sufficient to indicate upward motion. Additionally, fewer active elements reduces the opportunity for cooperative interactions in the network. This translates into a narrowing of the hysteresis profile. Accepting the concept that the perception of motion direction is dependent on a cooperative network, there may be circumstances outside the laboratory in which network's cooperativity might be especially useful. Observers must extract a mean direction vector from


175

a scene containing a large number of different local vectors in many naturally occurring situations. For example, we can determine the average direction in which the ocean's surf moves despite the fact that individual waves moves along somewhat different paths. We can also judge the average direction that the wind is blowing the leaves on a tree despite the random variations in that movement from one leaf to the next, or in any one leaf from one time toanother. Faced with such "Upward"

I'Lacal'' "Upward"

l lo cot" "Upward"

"Local" 1

0.0 0.2 0.4 0.6 0.6

Proportion of Signal

Figure 2. Hysteresis profiles as

4.0

1

1

1

1

1

1

1

1

0.0 0.2 0.4 0.6 0.6 1.0 Proportion of Signal

in Figure 1 but with additional data for the 0.1 degree step size. For a step size of 0.9 degree, data points denoted by the symbol, ( 0 ) .show the proportion of signal dots required for perceptual transition from local random motion to global upward flow; and data points denoted by (0) represent perceptual transitions from global upward flow to local random motion. For a step size of 0.1 degree, perceptual transition from local random motion to global upward flow are represented by (m): while transitions from global upward flow to local random motion are represented by ( 0 ) . The dashed lines mark the transition points calculated from a cooperative model incorporating cooperative interactions among directions-selective motion elements (see the text). The same parameter set for the model was used to fit the data in all panels. Note that for both step sizes, the model captures both the leftward shift and the narrowing of the hysteresis profile with decreasing signal range.

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multivectoral stimuli, a cooperative network like the one described by our model would enhance the signal to noise ratio, thereby facilitating the perception of the mean direction of motion.

Recovery of 3-D Structure from 2-D Motion 3-0 perceptfrom stochastic 2-0 motion In the preceding experiment, if the signal range is 180 degrees then it requires approximately a 0.8 signal to noise ratio before there is a transition from local random motion to global upward flow (see Figure 1). With a range of 90 degrees this ratio falls to 0.5. For this range and for ranges less than 90 degrees an interesting percept is produced for higher proportions of signal to noise. A global three-dimensional percept results (Williams and Phillips, 1986). This percept resembled a side-view of a rigidly rotating cylindrical volume with dots appearing on the surface of the cylinder as well as embedded inside. This volume appeared both to rotate about, and to translate along the upward direction (the mean of the distribution). Perceived direction of rotation, either right-handed or left-handed, varied from observer to observer. Unlike binocular stereopsis which uses the disparity between the two eyes to recover depth, this depth percept can be perceived monocularly. The sole cue to depth is the relative motion of the twodimensional retinal image. The basis for the recovery of an unambiguous three-dimensional percept under such circumstances is unclear since infinitely many combinations of three-dimensional structure and motion can project to the same two-dimensional retinal image. As in the case of the correspondence problems of binocular stereopsis and motion, recovexy is an under-determined task. We sought to determine if a cooperative algorithm might also underlie the recovery of three-dimensional structure in our display (Williams and Phillips, 1986). Using similar methods to those used to demonstrate hysteresis for the global coherent motion percept, we looked for hysteresis in the occurrence a n d loss of our three-dimensional percept. Display dots were permitted to randomly chose their directions of motion from two uniform distributions while the proportion of dots choosing from each distribution was slowly changed. One of the distributions had a directional range of 90 degrees (mean direction, upward) and was used to generate the percept of an upwardly moving, rotating three-dimensional volume. The other distribution had a directional range of 360 degrees, which generated a percept of two-dimensional local, random motion. We again refer to the first distribution as the signal, and to the second as noise, after the percept associated with each. Two types of trials were presented in random order. In one, all dots initially chose directions of motion from the signal distribution, generating an initial percept of a three-dimensional volume. After a random amount of time, the proportion of dots choosing from the signal distribution decreased slowly (under computer control) while the proportion of dots choosing from the noise distribution increased slowly. This continued until the subject responded that the three-dimensional percept had given way to a flat, two-dimensional percept. Following this response, the proportion of signal continued to


177

decrease for a random time. The procedure was then reversed and the proportion of dots choosing from signal increased until the observer responded that the three-dimensional percept had been restored. The latter response terminated the trial. In the other trial type, the procedure was reversed, with all dots initially choosing their directions of motion from the noise distribution. In this type, perceptual transitions were from two-dimensional to three-dimensional and back again. I t should be noted that for both types of trials, as the display shifted from complete dependence on one distribution to complete dependence on the other, a third percept was evident. Between the three-dimensional percept of a moving cylinder and the twodimensional motion percept of local random motion there is the intermediate two-dimensional motion percept of global upward flow described earlier. Subjects were instructed to ignore the difference between the two-dimensional motion percepts of local random motion and global upward flow and only respond to a transition between twodimensional and three-dimensional structure. Transition measurements were therefore actually obtained for the perceptual transition between the three-dimensional percept of a moving cylinder and the twodimensional percept of global upward flow. The two types of trials produce different histories for the directional content of the display, and thus should expose perceptual effects dependent upon history of stimulation. One hundred measurements were made of the signal content in the display for each perceptual transition (i.e.. two-dimensional to three-dimensional and vice versa ). Further data were obtained for two narrower signal ranges, 40 and 10 degrees. The results from two observers at all three signal distributions are shown in Figure 3. with each signal range represented in a different panel. For all three signal distributions, the two types of transition occur at significantly different ratios of signal to noise (P

(10)

where is the scalar product of the vectors F a n d 1,. Therefore, the functional can be characterized by one vector. The characteristic vector expressed in the basis 1400. . . .. 1700 is the spectral sensitivity of the mechanism, with each cF,I,> equal to the response to a unit amount of monochromatic light of wavelength I In the continuous case, the scalar product is equal to IF[&l(A) dil. The response of each mechanism is a scalar product, so no information about the constituents of the incident light is present in the response, consistent with the Principle of Univariance. A continuous linear functional satisfies both of Brindley's postulates: If the receptor has a non-zero response to both A and B, unidimensionality is satisfied if n is taken equal to /: substitutability is a direct consequence of Equation 8. Consequently, these mechanisms will also satisfy Von Kries' assumption. Three linearly independent continuous linear functionals F1. Fz. and F3 generate a three-dimensional linear vector space. A set of linear functionals is linearly independent if Ft are linearly independent vectors. Addition and scalar multiplication of linear functionals is defined as follows:

(cFJ(1) =

@tU)

(12)

The null functional is the functional SfZ) = 0 for all 1 in S. i.e. Ft = (0 , . . ..O). Every light 1 in S can be represented as a three dimensional point IFl(1). F2(1), F3Il)) in this vector space. I t is straightforward to prove that three functional mechanisms are consistent with the tri-variance and linearity of color matches. A corollary is the proof of Konig and Dieterici's (1886)assumption that, in trichromatic vision, the spectral sensitivities of the three channels determining trichromacy must be linear functions of the tri-stimulus values, with coefficients independent of test wavelength. The proof begins by assuming that given a system consisting of three independent linear functionals Fl, Fz. and F3. the number of primaries required for a color match is n. A color match for test wavelength A and primaries 11 , . . ., In, is defined as before:

By Von Kries' assumption, the response of each color mechanism should be equal for the two sides of the match. Therefore for each mechanism Ft:

Because the three mechanisms are linear, responses to a mixture can be separated into responses to each primary:

HUlVLAN COLOR MECHANISMS

Therefore, if I, matches 1, and Iy matches I, then ( I , + I=).

235

+ Iy) will match

(Ix

Figure 4. Tristimulus values for spectral lights. The values x. y. and z are the amounts of the three CE (1931)primaries required to color match a unit amount of energy having the indicated wavelength. To see that trichromacy can be derived from the proposed scheme, consider solving the three simultaneous linear equations (Equation 15)for unknowns a%as a function of the different numbers of primaries in the match. If for a wavelength A only one primary 11 is needed for a color match, then either two of the mechanisms have zero response for A and 11, or &(A)/FI(I,) is equal for all three mechanisms.

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If for a test wavelength A only two primaries are needed, then either one of the mechanisms has zero response for A. 11, and 12, or the response of one mechanism is the same linear combination of the responses of the other two for A, 11. and 12. If three primaries are used in the match, the set of equations will have a unique solution expressing the QJ a s linear combinations of F$A). If four or more primaries are used, there will be a n infinite number of solutions with all the extra primaries expressed as linear combinations of three primaries. Therefore, this set of mechanisms form a sufficient substrate for trichromatic matches. Furthermore, given a three primary match, for any wavelength A , the spectral sensitivities of each of the three mechanisms &(A) are expressed in Equation 15 as linear combinations of the tri-stimulus values ua, with coefficients Fi(1~)independent of wavelength A.

Figure 5. CIE (1931)chromaticity diagram showing the curved locus of spectral colors. The straight line joining 400 to 700 nm is the line of purples. All additive mixtures of the colors R and G lie on the line RG. Similarly, all real colors, i.e. all mixtures of the spectral colors, lie within the solid boundary.

Derivation of photopigment spectral sensitivities Light absorption by photopigments has linear properties similar to those attributed to the three color mechanisms above, and there is evidence from microspectrophotometry and electrophysiology that

H U M A N COLOR MECHANISMS

237

there are three classes of cone photopigment in the human fovea (Dartnall et al., 1983; Schnapf et al., 1987). Therefore, it is generally assumed that trichromacy is determined by the quantum catch of three cone photopigments S,M and L (short, middle and long wavelength sensitive). The derivation of the spectral sensitivities of these photopigments a s unique linear combinations of color matching functions, requires additional information to pick from among the infinite number of possible combinations. A number of derivations have been based on Konig's hypothesis that congenital dichromats have reduced forms of trichromatic vision, i.e. dichromats accept all color matches made by normal trichromats but not vice versa (e.g. Konig and Dieterici, 1893; Thomson and Wright, 1953: Vos and Walraven. 1971; Smith and Pokorny, 1975: Vos et al., 1990). In a three-dimensional representation of trichromatic vision, due to the linearity of dichromatic color matches (Nagy. 19841, color confusions of dichromats form a simple picture and the derivation of cone spectra is easy to intuit. Since almost all published derivations represent colors in a two-dimensional projection plane (Vos and Walraven. 1971; Wyszecki and Stiles, 1982). a simpler three-dimensional derivation based on Maxwell's suggestions is presented in this section. For notational convenience, the three mechanisms determining trichromacy are assumed to be L, M. and S cones. The characteristic vector, or spectral sensitivity of each of the cone types is given by:

M = ( m m , ..., m7d

s = (s400,

+

-

(18)

(19)

s700)

Each element in a vector represents the relative proportion of quanta absorbed by a class of cones from light of the subscripted wavelength. For example: D

1520

(20)

= 4.1520>

Because of the linearity of the mechanisms, the quanta absorbed by a class of cones from a heterochromatic light I is simply the sum of the quanta absorbed from each of the monochromatic constituents of I, i.e. 11

(21)

=

It would be easy to measure the spectral sensitivity of each cone type if three lights P, D,and T could be found such that each of them excited one type of cone only. If: sp =

0:

(22)

I D = 1. m D = 0 . S D =

0:

(23)

lp=

1. m p = O .

I T = 1, m T = O . s T = o :

(24)

then all three spectral sensitivities could be measured directly by an

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experiment in which a normal trichromat matched a unit amount of monochromatic light of each wavelength to a mixture of the three primaries P. D and T.Each match would yield an equation: Id

= PAP + dr.D + taT

(25)

From Equations 20 and 22-24. it is obvious that lr. = pa. ma = dr.,and sr. = Q, therefore Equation 25 can be rewritten so that the coefficients in the match are the cone spectral sensitivities for A:

However, this trio of real lights P, D and T does not exist, therefore the derivation will resort to a method suggested by Maxwell(l860) and revived by Nuberg and Yustova (1955) and Judd (1964). For a trio of arbitrary real primaries R . C. and B . if the color match for any monochromatic light Ir. can be written as: In = raR + gAG + br.B (27) Then the complete set of color matching functions can be depicted as:

B = (b400,

. - -, b700)

(30)

Maxwell's method requires assuming that spectral distributions (but not necessarily real lights) P. D and T exist, and can be matched to the three real primaries R. G and B,such that: P = rpR

+ gpG + bpB

Substituting Equations 31, 32. and 33 into 26: Id

= larpR

+ lkgpC + labpB

+ mArDR + mNgDG + mabDB + SarTR + S @ T G + s a b B Equating the amounts of R. G and B in Equations 27 and 34:

(34)

HUMAN COLOR MECHANISMS

239

This triplet of simultaneous linear equations can be solved for l ~ , SA by any of the traditional methods. A particularly convenient

rnn, and

method is to represent Equations 35-37in matrix notation:

The solution requires pre-multiplying both sides by the inverse of the matrix of coefficients:

Therefore, the spectral sensitivities of the three cone types In, ma, and sk can be derived for any wavelength h, from a color match of 1 ~ with . any three real lights R, C and B , if the nine coefficients of the matrix can be determined. These coefficients can be obtained from color matches made by congenital dichromats using the same primaries R. Gand B. Congenital dichromats accept the matches made by trichromats. but also match some pairs of colors that are distinct to a trichromat. therefore, their color vision is a reduced form of trichromatic vision. It is assumed that protanopes lack L cones, deuteranopes M and tritanopes S . For example, a protanope may match two lights J and K that are distinct to a trichromat. i.e.. J = K for a protanope but J z K for a trichromat. This can only be true if m ~ mK = and S J = s~ but 1J # ~ K .According to Maxwell's method, if P = J - K . then P will satisfy the requirements of Equation 22. Notice that even though J and K are real lights, P may be a spectral distribution with negative entries and hence not a physically realizable light. P is important only as a mathematical entity. Because cone absorptions are linear operations, the M cone absorption from P is equal to the M cone absorption from J minus the M cone absorption from K, i.e. zero:

mp = < M , P >= <M,(J - K)> = <M,J> - <M,K> = rnt - mk = 0

(40)

Similarly s p = 0 but lp+0, i.e. P excites only L cones. Since P is just the difference between two colors, the three coefficients of the matrix that correspond to P in Equation 39 can be derived from the tri-stimulus values for J and K. If for normal trichromats the color matches for J and K are represented by Equations 41 and 42: J = rjR + gjG

+ bJB

( 4 1)

K = TkR + g k c

+ bkB

(42)

then, because of the linearity of dichromatic color matches, the

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coefficients for P in Equation 31 are simply the difference between the coeMcients for the pair of confusion colors J and K

- TK)

(43)

gP = ( g J - g K 1

(44)

TP =

I rJ

It is worth noting that the difference between all pairs of protanopic confusion colors will give an estimate of the same n P where n is some constant. Similarly the coefficients corresponding to D and T can be derived by finding pairs of confusion colors for congenital deuteranopes and tritanopes. Then the spectral sensitivities L. M and S (Equations 17-19)for the three cone types can be derived from empirical color matching functions R , C. and B (Equations 28-30).by rewriting Equation 39 so that each row of variables is an array instead of a single wavelength:

This Ldebraic derivation can also be pictureL geometrically. Each I can be represented as a vector in the three-dimensional space formed by R. G, and B as axes. The three vectors P, D, and T are the vector differences of pairs of colors confused by congenital protanopes, deuteranopes and tritanopes respectively. Another way to visualize the confusion vectors is as follows: For any color E and any scalar n, let F = E + nP. Then using Equation 22 to add cone excitations from nP to excitations from E , mE = mF and SE = SF.but 1~ z IF. i.e. E and Fcan be distinguished by a trichromat but not by a protanope. So for any color vector in RGB space, adding a vector parallel to P results in a confusion pair for protanopes. Similarly, adding a vgctor parallel to D or T results in con fusion pairs for deuteranopes and tritanopes respectively. Reciprocally, the difference vectors between pairs of confusion colors for an individual dichromat are all parallel. If the space is transformed to P. D. and T as axes, then each I will be represented in a cone-excitation space. Because color spaces are affine. the relative heights of the cone sensitivities cannot be ascertained from color matching data. In practice there are a number of problems with the derivation of Konig fundamentals. The first problem is a logistic one. Generally, dichromatic color confusions were measured in chromaticity co-ordinates (Pitt. 1935: Wright, 1952) because colorimetric procedures were more accurate than available radiometric instruments. Since accurate instruments to measure tri-stimulus values are now available, it would be preferable to measure difference vectors, since in tri-stimulus values, every pair of confusion colors for a dichromat would provide a n independent estimate of the same confusion vector and lead to greater numerical precision. In a chromaticity diagram, P, D, and T

H U M A N COLOR MECHANISMS

0.9 0.8

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-

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0.1 02 03 0.4 0.5 0.6 0.7 08

X

Figure 6. Dichromatic color confusions converging to single points in the CIE chromaticity diagram for (a) (top panel, preceding page) protanope, (b) (bottom, preceding page) deuteranope. and (c) tritanope. each project to a single point called the convergence point for that class of dichromat (Figure 61,unless the plane of projection is parallel to one of the confusion vectors. The three pairs of dichromatic convergence coordinates only provide six of the coefficients needed in Equation 46, so auxiliary assumptions and data are needed for the remaining three. A usual strategy is to assume particular weights for the contributions of the three cone types to the luminosity function (Vos and Walraven, 1971: Smith and Pokorny. 1975; Vos et al., 1990). The second problem is that even if observers possess photopigments of identical spectral sensitivity, their color matching functions will be different due to differences in the amount of lens and macular pigments and in the optical density of the photopigments. A set of average color matching functions for a particular class of observer then depends on the characteristics of the sample of observers measured (Zaidi et al.. 1989). More importantly, it is not possible to test Konig’s reduction hypothesis by direct confrontation of trichromatic and dichromatic matches (Alpern and Pugh. 1977: Pokorny and Smith, 1977). A reduction system can be tested for an individual dichromat by testing that the differences between pairs of confusion colors are all parallel in RGB space, or equivalently, that in a chromaticity space the lines joining confusion colors converge to a single point. This problem has been dealt with by either using WDW normalization (Wright, 1928-1929) or using published estimates to correct to a n average observer (Smith and Pokorny. 1975). A third problem is the potential of relying too heavily

HUMAN COLOR MECHANISMS

243

on the precision of measurement of the dichromatic convergence points (Nimeroff. 1970: Walraven. 1974). Historically, the empirical estimates of convergence points have been adjusted iteratively so that the derived cone sensitivities are consistent with pigment nomograms and can predict not only color mixture data, but also a variety of types of other measurements on dichromats and monochromats. including spectral sensitivity and luminosity (Smith and Pokorny, 1972. 1975).A fourth problem is that whereas protanopes and deuteranopes have been shown to lack one of the normal pigments In the long wave part of the spectrum (Rushton, 19721.tritanopes with complete absence of S cone pigment may not exist (Pokorny, Smith and Went, 1981). Despite all these problems, estimates of cone sensitivities, derived from color mixture and other methods, converge to a set very close to that shown in Figure 7 (Stockman. 1989).This set (Smith and Pokorny, 1975) is based on the following transformation from Judd's (195la) modification of the CE (1931)color matching functions: .15514 .54312-.03286 .45684 ,03286 0 .01608

(47)

Recently, additional support for the theory explicated above has come from electrophysiological recordings from single cones of the human retina (Schnapf et al.. 1987). Four facts about the electrophysiological measurements are particularly germane. First, the response of a cone is the same for equal quanta caught from lights of different wavelengths, consistent with the Principle of Univariance. Second, the measured spectral sensitivities cluster into three discrete classes with minimal variability within each class. Third, the measured sensitivities provide a good fit to human color matching functions on the assumption that for a color match the quantal catch for each class of cone is identical for both sides of the match, and with adjustments for optical density of photo pigments and pre-retinal absorption. Fourth, within the freedom provided by these adjustments, the action spectra of the cones, that is the reciprocal of the amount of light of each wavelength required to produce a constant response, closely resemble the Smith-Pokorny fundamentals.

Cone interactions and opponent mechanisms Because the output of cones of different classes are combined very early in the retina, it is difficult to find other psychophysical tasks besides color matching where each class of cones functions independently. One notable exception is dark adaptation after intense bleaches, where sensitivity as measured by a method of revived afterimages seems to be regulated within each cone class independently (Williams and MacLeod, 1979).Another possible case is the detection of small, brief pulses of light (Krauskopf and Srebro. 1965).In most color experiments, the results indicate some degree of interaction between different classes of cones. For example, Stiles' (1939,1959) two color increment threshold technique identified seven foveal n-mechanisms, some of which are now thought to involve post-receptoral interactions

244

CHAPTER 7

(e.g. Pugh and Mollon, 1979). Wright (1946) examined the possibility of parallel independent adaptation processes in the three cone systems by testing the assumption of superposition (additivity) for binocular color matches. With the two eyes in different states of adaptation, an observer matched stimulus s1 in one eye by the mixture (rl, 91. b l ) in the other eye and stimulus sz by (rz, gz. bz). However, s3 equal to q + s 2 . was matched by (r3. g3. b3) some of whose components were considerably less than the sum predicted by the assumption of additivity, e.g., r3

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