ADVANCES IN CHILD DEVELOPMENT AND BEHAVIOR
VOLUME 15
Contributors to This Volume Jiiri All& Richard N. Aslin John M...
14 downloads
1139 Views
15MB Size
Report
This content was uploaded by our users and we assume good faith they have the permission to share this book. If you own the copyright to this book and it is wrongfully on our website, we offer a simple DMCA procedure to remove your content from our site. Start by pressing the button below!
Report copyright / DMCA form
ADVANCES IN CHILD DEVELOPMENT AND BEHAVIOR
VOLUME 15
Contributors to This Volume Jiiri All& Richard N. Aslin John M. Belmont Earl C. Butterfield Susan T. Dumais William Fowler Fred Rothbaum Dennis Siladi Jaan Valsiner
ADVANCES
IN CHILD DEVELOPMENT AND BEHAVIOR
edited by Hayne W. Reese
Lewis P. Lipsitt
Department of Psychology West Virginia University Morgantown, West Virginia
Department of Psychology Brown University Providence, Rhode Island
VOLUME 15
@
1980
ACADEMIC PRESS A Subsidiary of Harcourt Brace Jovanovich, Publishers
New York London Toronto Sydney San Francisco
COPYRIGHT @ 1980, BY ACADEMIC PRESS, INC. ALL RIGHTS RESERVED. NO PART OF THIS PUBLICATION MAY BE REPRODUCED OR TRANSMITTED IN ANY FORM OR BY ANY MEANS, ELECTRONIC OR MECHANICAL, INCLUDING PHOTOCOPY, RECORDING, OR ANY INFORMATION STORAGE AND RETRIEVAL SYSTEM, WITHOUT PERMISSION IN WRITINQ FROM THE PUBLISHER.
ACADEMIC PRESS,INC.
111 Fifth Avenue, New York, New York 10003
Uniied Kingdom Edition published by ACADEMIC PRESS, INC. ( L O N D O N ) LTD. 24/28 Oval Road, London N W l
LIBRARY OF
7DX
CONGRESS CATALOG CARD
NUMBER:63-23237
ISBN 0-12-009715-X PRINTED IN THE UNITED STATES OF AMERICA 80 81 82 83
9 8 7 6 5 4 3 2 1
Contents ..........................................................
vii
Preface.. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
ix
List of Contributors
visual Development in Ontogenesis: Some Reevaluations J-I ALLIK AND JAAN VALSINER .......... I. Introduction ................................... 11. A Conceptual Framework for Infant Visual Preferen Discrepancy Hypothesis . . ......... 111. Acuity and Spatial Modulation Transfer Function ............................ IV. Conceptualizationof the Relative Functions of Environmental and Organismic Influences .................................................. V. Perception of Flicker and Movement ...................................... VI. Binocular Vision . . . . . . . . . .... ................... VII. Conclusions .................................... ......... References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
2 4 7
23 25 28
39 42
Binocular vision in Infants: A Review and a Theoretical Framework RICHARD N. ASLIN AND SUSAN T. DUMAIS I. Introduction
..........................................................
II. Levels of Binocular Function ............................................ 111. IV. V. VI.
Developmental Constraints on Binocular Vision ............................. Empirical Findings on Infant Binocular Vision .............................. Early Experience and Binocular Function .................................. Concluding Remarks ................................................... References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
54 54 62 68 79
90 90
Validating Theories of Intelligence EARL C. BUTERFIELD, DENNIS SILADI, AND JOHN M. BELMONT I. Introduction
..........................................................
11. A Strategy for Studying Intellectual Development
...........................
111. Illustration of the Strategy for Studying Intellectual Development. .............. IV. A Strategy for Studying the Generality of Cognitive Processes ................. V. Illustration of the Research Strategy for Testing Process Generality . . . . . . . . . . . . . VI. Concluding Considerations .............................................. References ...........................................................
V
% % 102 124
131 153 159
vi
Contents
Cognitive Differentiation and Developmental Learning I. I1. 111. IV . V.
VI.
WILLIAM FOWLER Introduction .......................................................... Biases Limiting Scope of Developmental Theory ............................ Integrating the General and Individual in Developmental Theory . . . . . . . . . . . . . . . Mechanisms of Cognitive Change and Development ......................... Developmental Phases of Concept Learning ................................ Summary and Conclusions . . . . . . . . ................................. References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Children's Clinical Syndromes and Generalized Expectations of Control FRED ROTHBAUM I . Overview . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . I1. Factor Analytic Research on Syndromes in Children ......................... III . Support for the Helplessness-Reactance Model ..............................
IV . Toward a Helplessness-Reactance Explanation of Syndromes .................. V . Conclusion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . References ...........................................................
Author Index Subject Index
................................................................ ............................................................
Contents of Previous Volumes
..................................................
163 164 170 188 195 199 201
207 209 211 220 234 241 247 257 261
List of Contributors Numbers in parentheses indicate the pages on which the authors' contributions begin.
JURI ALLIK Department of Psychology, Tartu State University, Tiigi 78,202400 Tartu, Estonian SSR, USSR ( I )
RICHARD N. ASLIN Department of Psychology, Indiana University, Bloomington, Indiana 47405 (53) JOHN M. BELMONT Kansas Mental Retardation Research Center, University of Kansas Medical Center, Kansas City, Kansas 66103 (95) EARL C. BUTTERFIELD Kansas Mental Retardation Research Center, University of Kansas Medical Center, Kansas City, Kansas 66103 (95) SUSAN T. DUMAIS' Indiana University, Bloomington, Indiana 47405 (53)
WILLIAM FOWLER* Ontario Institute for Studies in Education, Toronto, Ontario M5S 1 V6, Canada (163) FRED ROTHBAUM Eliot-Pearson Department of Child Study, Tufts University, Medford, Massachusetts 02155 (207) DENNIS SILADI O&e of Research and Development, Stamford Public Schools, 195 Hillandale Avenue, Stamford, Connecticut 06902 (95) JAAN VALSINER Department of Psychology, Tartu State University, Tiigi 78,202400 Tartu, Estonian SSR, USSR (1)
'Present address: Bell Laboratories, Murray Hill, New Jersey 07974. Tresent address: Laboratory of Human Development, Graduate School of Education, Harvard University, Cambridge, Massachusetts 02138. vii
This Page Intentionally Left Blank
Preface The amount of research and theoretical discussion in the field of child development and behavior is so vast that researchers, instructors, and students are confronted with a formidable task in keeping abreast of new developments within their areas of specialization through the use of primary sources, as well as being knowledgeable in areas peripheral to their primary focus of interest. Moreover, there is often simply not enough journal space to permit publication of more speculative kinds of analyses which might spark expanded interest in a problem area or stimulate new modes of attack on the problem. The serial publication Advances in Child Development and Behavior is intended to ease the burden by providing scholarly technical articles serving as reference material and by providing a place for publication of scholarly speculation. In these documented critical reviews, recent advances in the field are summarized and integrated, complexities are exposed, and fresh viewpoints are offered. They should be useful not only to the expert in the area but also to the general reader. No attempt is made to organize each volume around a particular theme or topic, nor is the series intended to reflect the development of new fads. Manuscripts are solicited from investigators conducting programmatic work on problems of current and significant interest. The editors often encourage the preparation of critical syntheses dealing intensively with topics of relatively narrow scope but of considerable potential interest to the scientific community. Contributors are encouraged to criticize, integrate, and stimulate, but always within a framework of high scholarship. Although appearance in the volumes is ordinarily by invitation, unsolicited manuscripts will be accepted for review if submitted fmt in outline form to the editors. All papers-whether invited or submittedreceive careful editorial scrutiny. Invited papers are automatically accepted for publication in principle, but may require revision before fiial acceptance. Submitted papers receive the same treatment except that they are not automatically accepted for publication even in principle, and may be rejected. We wish to acknowledge with gratitude the aid of our home institutions, West Virginia University and Brown University, which generously provided time and facilities for the preparation of this volume, We benefited as well from the facilities of the Center for Advanced Study in the Behavioral Sciences at Stanford, where one of us (LPL) was located during the final editing of the volume. We also wish to thank Daniel Ashmead, Eve V. Clark,Barry Gholson,
ix
X
Preface
Martin J. Hofmann, Marion Perlmutter, Philip H. Salapatek, Martin E. P. Seligman, Robert S. Siegler, Irving E. Sigel, and Billy Wooten for their editorial assistance. Hayne W. Reese Lewis P. Lipsitt
ADVANCES IN CHILD DEVELOPMENT AND BEHAVIOR
VOLUME 15
This Page Intentionally Left Blank
VISUAL DEVELOPMENT IN ONTOGENESIS: SOME REEVALUATIONS'
Jiiri Allik and Jaan Valsiner DEPARTMENT OF PSYCHOLOGY TARTU STATE UNIVERSITY TARTU, USSR
I. INTRODUCTION ...................................................... 11. A CONCEPTUAL FRAMEWORK FOR INFANT VISUAL PREFERENCE AND THE DISCREPANCY HYPOTHESIS . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . .
. ..
In. ACUITY AND SPATIAL MODULATION TRANSFER FUNCTION . . . . . . . . . . . A. FACTORS AFFECTING VISUAL RESOLUTION . . . . . . . . . . . , , , , . . . . . . . B. PERCEPTION OF ONE-DIMENSIONAL PA"ERNS . . . . . . . . . . . . . . . . . . .. . . . . . . C. PERCEPTION OF TWO-DIMENSIONAL PATTERNS . . . . . . . D. DEFICIENCY OF VISUAL RESOLUTION.. . . . . . . . . . . . . . . . . . . . .. .. E. EXPERIMENTAL VISUAL DEPRIVATION .. . . . . .. . . . . . . . . . . . . . . . ... .
.
. . . .. . .. .
IV. CONCEPTUALIZATION OF THE RELATIVE FUNCTIONS OF ENVIRONMENTAL AND ORGANISMIC INFLUENCES . . . . . . . . . . . . . . . . . . . .
..
V. PERCEPTION OF FLICKER AND MOVEMENT . . . . . . . . . . . . . . . . . . . . . . . . . .... . . . A. INFANT RESPONSE TO FLICKER AND MOVEMENT . . . . . B. REARING IN STROBOSCOPICALLY ILLUMINATED AND UMDIRECI'IONALLY MOVING ENVIRONMENTS . . . . .. . . . . . . . . . . . . . .
. .. . .
VI. BINOCULAR VISION.. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . A. INFANT BINOCULAR VISION . . . . . . . , . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . B. DISPARITY . . . . . . . . . . . . . . . . . . . . . . . . , . . . . . . . . . . . . . . . . . , , , . . , . . . . . . C. ABNORMALITIES OF BINOCULAR VISION.. . . . . . . . . . . . . . . . . . . . . . . . . D. DEVELOPMENT OF BINOCULAR VISION IN ANIMALS.. . . . . . . . . . . . . . E. MONOCULAR DEPRIVATION . . . . . . . . . . . . . . . . ... . . . . . . . . . . . . . . .. . . .
2
4
1 7 9 11 14 18
23 25 25
26 28 28 30 31 34 35
'The authors are very grateful to Philip Salapatek for his critical comments on the manuscript, and to Michael Kuskowski, Martin J. Hofmann and Daniel Ashmead (all from the Institute of Child Development, University of Minnesota) for their very valuable editorial assistance. However, the authors reserve for themselves the responsibility for all the shortcomingsof the present article. James Wertsch's organizational help in preparing the manuscript is also gratefully acknowledged. 1 ADVANCES IN CHILD DEVELOPMENT AND BEHAVIOR, VOL. IS
Copyrighl@1980 by Academic Press, Inc. All rights of RpodUctirn in any form reserved. ISBN 0-12-0(m15-X
Juri Allik and Jaan Valsiner
2
VII. CONCLUSIONS. ...................................................... A. NEWBORNS’ VISUAL ABILITIES ................................... B. COURSE OF DEVELOPMENT ......................................
40
........................................................
42
REFERENCES
39 39
I. Introduction Probably everyone agrees that modem theories of visual perception tend to be far less metaphysical, less ideological, and more experiment-bound than in the past. There are, of course, theoretical differences within the field of perception, but they are more sophisticated and more devoted to specific issues than before (Dodwell, 1975). The same is entirely true concerning the subfield of infant visual perception. This area has progressed from sterile discussions regarding the relative importance of nature and nurture toward a field of serious science, with unique methodology, experimental skills, and research problems. Several overviews have given a fascinating and complete picture of that progress (see Bower, 1974; Cohen & Salapatek, 1975a,b; Haith & Campos, 1977). The aim of this article is to analyze the development of infant visual perception, trying to integrate the findings of that research field with those of the developmental neurophysiology of visual perception in animals. The logic of our presentation is based on the following data: 1. Comparisons between infant and normal adult vision. This comparative analysis is limited, largely because of the lack of data about infant visual perception. As a rule, some knowledge exists about general properties of infant vision-for example about spatial resolution and localization brightness, and color vision-but the fine structure, the exact operating routines of visual perception, has not yet been described. 2. Acquired abnormalities of visual perception. Acquired abnormalities are treated as an additional source of information about possible ways in which perceptual development might occur. We shall pay primary attention to the cases of total or partial monocular or binocular visual deprivation. The results of visual deprivation, which may be treated as an unfortunate natural experiment, show the weakening or failure of certain algorithms required for transformation of visual information. Such abnormalities, in some conditions, may reveal the mechanisms of perceptual development or the relationship between experience and the functioning of perceptual processes. 3. Animal studies. “Environmental surgery, “selective visual deprivation,’’ and other related expressions are terms coined for a very popular area in ”
Visual Development in Ontogenesis
3
recent neurophysiological research. Although environmental modification of central nervous system structures has been convincingly demonstrated for some time, intensive study of such malleability has begun only since it has been shown that the properties of single visual cells can be altered by early visual experience. Although the enthusiasm of the first reports has waned, many important findings about the fine structures involved in the development of visual functions have been collected and many new controversies have arisen. We are very far from believing in the face value of metaphors such as “what the cat’s eye tells the human brain,” but it may be fruitful to look at animal studies, mainly on cats and partly on monkeys, for a possible model of neuronal modification in the human visual system. It is astonishing to note that although a very great number of studies have been devoted to infant perception, they allow us to deal with only some areas in the rich field of infant vision and rarely shed direct light on specific models of neural modification. There seems to be a certain “encapsulation” among scientists who study these delicate and perspicuous phenomena. They generally use only one method of study-for example, the visual preference technique-and interpret their findings along conceptual lines that are not nested in the contemporary terminology of visual psychophysics. As we try to show in Section 11of our analysis, it may even be argued that their interpretations do not follow from their experimental data in an unambiguous manner, and, because of this, many of the research efforts on infant visual perception (as well as many tears produced by the infants dragged into laboratories) must be classified as rather barren from the viewpoint of understanding infant perception. Our goal in analyzing the data on visual perception stems from our belief that much could be achieved if studies on infant vision were directed along the lines in which contemporary psychophysics is moving. One of the most interesting developments in contemporary psychophysics is the tightening of its ties with neurophysiology; such a development might be of similar value for infant researchers. Along this line, we have decided to analyze a very broad spectrum of data and concepts in this article. It may be difficult for researchers in infant perception to maintain close and continuous contact with the burgeoning area of animal vision research, especially as the number of experiments devoted to early visual ontogenesis in different species of animals is ever-increasing. Ow reading of the research literature concerning human infant perception certainly indicates that cross-species comparisons are very rare. Therefore, much of the reasoning in this article is based on animal data, with the hope that our ideas will intrigue the reader and lead to experiments on human infants to prove or destroy our hypotheses. To some readers, our presentation might seem to be a simple renaming of concepts. Indeed, we use the terminology developed in psychophysics and related disciplines instead of the idiosyncratic terminology that is currently being
4
Juri Allik and Jaan Valsiner
used by infant vision researchers (especially in infant visual attention and memory studies), with the single aim that the reader will recollect t k old scientific truth that a conceptual framework is better if it gains breadth without sacrificing depth and clarity.
11. A Conceptual Framework for Infant Visual
Preference and the Discrepancy Hypothesis
Research that involves infant visual preference techniques modeled after the preliminary investigationsby Fantz (1956, 1961, 1963)is usually termed “infant attention research. ” As Kinney and Kagan (1976)noted, the studies concerning human infant attention are directed toward two different goals. The f i t is to study how physical stimulus parameters influence the infant’s attention and perception; this issue is treated at length in other parts of the present article. The second goal is to study the outcome of infant perception-an engram, or schema, or model of the stimulus. We shall examine the relationship between the perceptual outcome and infant attention here. Although it goes without saying .that different assumptions may be used as bases for alternative conceptual systems and that those assumptions are not to be studied within the framework of their own particular systems, it seems that very little attention has been given to developing alternative assumptions concerning the human infant’s visual attention. The overwhelming majority of studies are conducted within the framework of “schema development,” which in more operational terminology is deeply associated with the “discrepancy hypothesis” and, in experimental practice, with habituation paradigms. It is assumed that, in the course of development and visual experience, the infant acquires (or develops further on the basis of existing experience) a “schema” or model of some event. Piaget has had great influence on this type of thinking. He has tied “schema development” to the general principle of assimilation-accommodation as the process along which development works. It should be noted that Piaget suggests that any new developing schema will be based on already existing ones, which are modified in the process of assimilation (Piaget, 1970). Accommodation is the term coined by Piaget to denote any modification of an assimilatory schema by the elements it assimilates. Piaget stresses the necessity for studying assimilation and accommodation always together, viewing cognitive adaptation as an equilibrium of these two processes. It is certainly safe to speak about the development of schemata on such a high level of abstraction. However, if one begins to ask more particular questions about what the concrete schemata might be like in real infants, problems begin to emerge. How do we unambiguously tie the various measures of infant attention,
Visual Development in Ontogenesis
5
measured quite precisely in the laboratory, to the high-level, abstract concept, “schema”? Habituation of infant attentional responses provides one possibility, When the infant is repeatedly shown the same stimulus, his “attention,” as measured by some index (e.g., fmation duration or frequency, heart rate changes), seems to decline. Therefore, it seems reasonable to assume that the infant has “assimilated” the stimulus into the schema and that this is why the infant pays less attention to it. However, here we must deal with some implicit assumptions that have not been (and possibly cannot be) based on anything except adult common sense. These may be roughly described as follows: 1 . The indices of an infant’s visual attention are linearly related to schema development; if the schema develops, the infant’s attention declines; 2. The decline in infant attention toward the stimulus is paralleled by an inner comparison process within the infant. The infant monitors the schema being formed to the stimulus. If the schema has become more similar to the stimulus, the infant’s attention declines, and if not, it does not decline. Here too a kind of linear relationship between observable habituation measures and a hypothetical schema assimilation process is presumed.
The difficulty with these implicit assumptions is that they leave open questions as to whether they provide a fair basis for developing a conceptual system of infant visual attention. Even if attempted, the form of the relationships between an observable objective phenomenon and a hypothetical construction may be more than impossible. One important aspect of infant attention research is the “discrepancy hypothesis. Many different models of infant attention are based on this hypothesis (see Cohen & Gelber, 1975, for review). The general principle they share is the experimentally demonstrated fact that after familiarization with a stimulus and habituation to it, infants show an increase in attentional parameters when exposed to a different, discrepant stimulus (Figurin and Denisova used habituation and dishabituation as a research method as long ago as 1929; see Zaporozhets, Venger, Zintchenko, & Ruzskaja, 1967). Very often an inverted U-shaped relationship is found between discrepancy of the familiarized from the novel stimulus and infant attention measures (McCall, 1971). In other words, infants appear to pay most attention to those stimuli that are within an optimal range of discrepancy from the habituated stimulus. If the discrepancy is too great and the stimulus too novel, then the infants do not pay more attention to it than to the former stimulus. From the viewpoint of the conceptual system of schema development, the findings on optimal discrepancy preferences in infants are valuable in that they may show in the following way how assimilation occurs: If an optimally discrep”
6
Jiiri Allik and Jaan Valsiner
ant stimulus enters the infant’s visual field, he turns his attention toward it and assimilates it into his developing schemata. If the new stimulus is too discrepant to assimilate, no extra attention will be paid to it. The directing of attention on the basis of a discrepancy principle helps the infant organize his stimulus environment in the optimal way for a given developmental level. The conceptual problem with both schema development theory and the discrepancy hypothesis is the lack of specificity of the function of visual fixation in perceptual development. Specifically, visual preference for some environmental stimuli may be a necessary cause of “schema development,” may correlate only with schema development, or may be the motor result of some implicit schema development. It is not apparent that we can decide among these alternatives within the conceptual frameworks and methods currently used. Because of these multiple interpretations, the explanation of the infant’s visual system development as the progressive development of schemata of different kinds would not make a perspicuous explanatory paradigm for the data. A more exact specification of the role of different aspects of infant fixation in habituation has been provided by Cohen (1973), based on experimental data that show that the overall size and number of elements in a checkerboard have different effects on infant looking (Cohen, 1972). He found that the size of the checkerboard influenced the infant’s latencies of turning to the stimulus, but the number of checks had more influence on the duration of looking at the stimulus. Cohen (1973) has formulated a two-process model of infant visual attention in which the process of attention is divided into attention-getting and attentionholding processes, and he has attempted to demonstrate their independence. His success in discovering these two processes stemmed from his use of independent criteria of infant’s visual fixation-latency and fixation time. His success illustrates the point that much of our theorizing is very procedure-bound. Had he used only traditional measures of fixation, such as visual choice or total looking time, he could not have obtained data in support of the two-process model. The mechanisms Cohen has described can be considered mainly as means of regulating the visual input, that is, as mainly a way (overwhelmingly motor) by which an infant can regulate its visual experience. This mechanism is not, at least at the very beginning of life, intentionally controlled by the infant. It may be more of a specific evolutionary adaptation that allows the motorically very immature human infant to extract the kind of stimulation from the environment that is necessary for the functional development of the visual system at that particular developmentlevel. The tendency for the human infant (and other primate infants) to combine a precocial pattern of sensory development with an altricial pattern of motor development (Gottlieb, 1971) makes possible the presence of some adaptational mechanisms during this developmental asynchrony-and we propose that selective fixation and habituation are among them.
Visual Development in Ontogenesis
7
111. Acuity and Spatial Modulation Transfer Function A. FACTORS AFFECTING VISUAL RESOLUTION
Discussions regarding theoretical confusions among the various measures of visual acuity have been presented elsewhere (see Thomas, 1975; Westheimer, 1972). Here, we note that the resolving power of the visual system is determined by the optical system of the eyes, the spatial packing of the receptors, and the neural integration of the peripheral and central visual areas. Visual acuity may be defined by means of the spatial frequency variable, in a most general way, as the highest spatial frequency the visual system is capable of differentiating. In this section, we examine the various factors that are related to the functioning of the visual system as measured through the Modulation Transfer Function (MTF), which provides a measure of the sensitivity of the visual system to all spatial frequencies, hence being a more general measure of the spatial organization of vision than is acuity. 1. Optical Factors The quality of the retinal image is largely determined by appropriate accommodation. It is well established that infants younger than 1 month of age do not appropriately accommodate to the changes in the distance of a test object. Haynes, White, and Held (1965) found that the focus of the alert newborn is locked at one focal distance. The median distance for the group of newborns investigated in their study was 19 cm. During the second month of life, the accommodative system began to respond, to some extent, to the changes in target distance. By 3 or 4 months, the infants’ accuracy of accommodation was found to be comparable to that of emmetropic adults (White, 1971, Fig. 15). Therefore, the very young infant is myopic at almost all of the target distances. It has usually been found that visual acuity in infants at and below 2 months of age is 20/400or worse-that is, limited to spatial frequencies not higher than 2-3 cycles per degree (Banks & Salapatek, 1976). In those studies in which it was examined, acuity was found to be independent of the distances at which test gratings were presented. Therefore, for the young infant, the optical defocusing that accompanies changes in viewing distance does not appear to affect visual acuity (Salapatek, Bechtold, & Bushnell, 1976). The optical system of the infant differs remarkably from that of the adult. Since the infant’s cornea is more spherical, the radius of curvature is about 1 mm shorter than in the adult (Maurer, 1975). Further, the sagittal length of the eye is approximately 24 mm in the adult, and only 17-17.5 mm in the neonate (see Maurer, 1975; Slater & Findlay, 1975). These measures allow an approximate
8
Juri Allik and J M n Valsiner
calculation of the size of the retinal image corresponding to the size of a visible stimulus. Stimuli subtending equal visual angles will fall on a retinal area about 48 times smaller in the newborn than in the adult. Therefore, fewer receptors are involved in the analysis of the same stimulus in the infant’s vision (assuming that the receptor packing is the same as or less dense than in the adult), which may be one reason for the newborn’s poor acuity (Maurer, 1975). The MTF of the infant’s visual system is partly limited by the cut-off frequency of the infant’s optical system. The MTF of the human infant’s optical system has not been assessed with satisfactory measures such as the reflected fundus image (Westheimer, 1972) or interference fringes (Campbell & Green, 1965). These techniques allow a separate estimation of the spatial frequency attenuation resulting from the optics of the eye, and that resulting from the nervous system isolated from the optics. Salapatek et al. (1976) stated that considerable optical defocusing, up to about 5 diopters, does not seriously affect the infant’s visual acuity or cut-off frequency of the transfer function, since the infant is sensitive only to spatial frequencies lower than 3 cycles per degree. In addition, some theoretical methods for the computation of the effect of defocus on the optical transfer function are available (Hopkins, 1955). These equations were applied to the psychophysical contrast sensitivity function by Freeman and Thibos (1975a), who showed that the usual notion that defocusing attenuates only the high-frequency end of an optical transfer function continuum is incorrect. A careful examination of the defocusing effect shows that the middle and low ranges of spatial frequency are also significantly depressed (see Freeman & Thibos, 1975a, Fig. 8, for the theoretical effect of defocusing, computed for Gullstrand schematic eyes). Using a different approach, Krueger, Moser, and Zrenner (1973) experimentally determined the effect of defocusing on the optical transfer function of the frog eye. Because the transfer function of the frog eye is qualitatively similar to that of the human eye (Krueger & Moser, 1973), their results are valuable for the understanding of the human eye as well. Defocus affects the image formation process throughout the spatial frequency spectrum, and even for very low frequencies the attenuation is significant. 2 . Neural Factors Campbell and Green (1965) assessed the relative roles of optics and nervous system in the transmission of spatial frequency in the human adult. They found that over the range of 30-40 cycles per degree, optical attenuation increased by a factor of 1.25, while attenuation by the nervous system increased by a factor of 2.4. Therefore, high-frequency attenuation is mainly determined by some process in the nervous system of the human adult. In recent years, several studies have been performed to measure the infant’s responses to spatial frequency. Banks and Salapatek (1976) presented sine wave gratings to probe the infant’s
Visual Development in Ontogenesis
9
frequency response. In other studies, rectangular distributions of light-gratings consisting of black and white stripes-were used (e.g., Leehey, MoskowitzCook, Brill, & Held, 1975; Salapatek et a l . , 1976). In spite of the infinite number of “higher order harmonics” in a rectangular grating, the response of the visual system is determined mainly by the amplitude of the fundamental frequency. The method for determining whether a particular spatial frequency has been detected by infants is another serious problem. The most popular response measure is visual preference for the modulated over the unmodulated field with the same average luminance. The degree of preference is assumed to be equivalent to “amplitude attenuation” in linear system engineering. In other words, we might say that “infant looking preferences are determined by visibility, ” or “the infant looks at something that is more clearly visible to him. ” This, of course, is a model picture of the infant’s visual preferences, which cannot be turned into an explanatory principle for the interpretation of the preference data obtained in purely behavioral experiments. B. PERCEPTION OF ONE-DIMENSIONAL PATTERNS
From the studies by Atkinson, Braddick, and Braddick (1974), Banks and Salapatek (1976), and Salapatek et al. (1976), one might conclude that there are few, if any, qualitative differences between infant and adult modulation transfer functions. The main similarity is in the band pass character of the transfer functions: An optimal spatial frequency exists at which the modulation attenuation is minimal and below and above which modulation suppression increases progressively. The same idea expressed in spatial terms states that the human eye is relatively insensitive to very slow and very fast spatial changes in luminance. Though the modulation transfer functions appear to be qualitatively similar for the infant and .adult, very remarkable quantitative differences exist between the two: 1. The transfer function of the infant eye is displaced toward the lower spatial frequencies (the peak frequency is below 1 cycle per degree). The corresponding peak value for the human adult eye is somewhere between 4 and 8 cycles per degree, depending on the average illumination and other conditions (Kelly, 1975; Kelly & Savoie, 1973). 2. The exact location of the peak value of the infant function has not yet been clearly determined, since the modulation transfer is relatively flat in the region of peak sensitivity. A measure more appropriate than peak frequency is the cut-off frequency, defined as the frequency at which amplitude attenuation is increased by a factor of 2, or at which, for example, the amplitude drops to l/e’’*compared to the maximum. However, even the criterion of cut-off frequency has limited application because of the questionable measures of infant transfer function collected so far.
10
Juri Allik and Jaan Valsiner
3. The cut-off frequency of the 1-month-old infant transfer function may be roughly estimated as about 1-2 cycles per degree. The comparable value for the human adult is 10-20 cycles per degree, or higher by a factor of 10. One should remember that this is only a very approximate estimate that does not take into account any differences in adaptation level or decision criteria. In ophthalmological terminology, the newborn infant is 10 times more defocused than the adult. The young infant’s visual transfer function is quantitatively very similar to the cat’s. Various investigators, using very different methods (e.g., microelectrode recording-campbell, Cooper, & Enroth-Cugell, 1969; evoked potential recording-campbell, Maffei, & Piccolino, 1973; behavioral training techniques-Blake, Cool, & Crawford, 1974), have found that the point of maximal sensitivity of the cat’s modulation transfer function is near .5 cycle per degree, and the high-frequency cut-off is between 3 and 5 cycles per degree. These values are comparable to the corresponding values of the 1-month-old human infant’s MTF.One possible reason for the cat’s poor visual resolution is the low density of visual cells in the cat’s retina. The cat’s area centralis contains only about 350 ganglion cells per square degree of visual angle, while in the human, the corresponding number is 6500 (Stone, 1965). Anatomical factorsthe dimensions of the infant eye and the density of visual cells in the retina-are probably the most important factors determining the young infant’s spatial resolution. Results mentioned so far in this section have been based on the use of gratings that are periodic in one dimension and constant in the perpendicular dimension. Using one-dimensional patterns implies a belief that the visual system is isotropic, that is, that the detection of unidimensional gratings is invariant to the absolute orientation of the patterns. However, a good deal of evidence indicates that the human visual system is more sensitive to gratings in vertical or horizontal orientation than to patterns in an oblique orientation (for a review, see Apelle, 1972). In other words, the human visual system is orientationally anisotropic. The orientational asymmetry of the visual system is perhaps an inherent feature that appears even at birth. Kessen, Salapatek, and Haith (1972) reported newborn anisotropy in visual scanning patterns along horizontal and vertical orientations. Leehey et al. (1975) found that infants prefer to look at horizontal or vertical rather than oblique gratings. This last result suggests that acuity for oblique orientations is worse than that for horizontal and vertical lines or edges. Orientational anisotropy suggests that the contrast sensitivity function for a twodimensional sine wave distribution cannot be predicted simply from a onedimensional contrast sensitivity function that assumes the applicability of the principle of linear superposition. Rather, it is necessary to measure the contrast sensitivity function of one-dimensional gratings in many orientations. However, as Carlson, Cohen, and Gorog (1977) have indicated, the anisotropy in the visual
Visual Development in Ontogenesis
11
system is not large enough to invalidate the assumption of linear superposition. Nevertheless, it is evident that the operational transfer function of the human visual system is two-dimensional in principle. Hence, there has been an increased interest in determining the perception of two-dimensional patterns. The contrast threshold for many types of two-dimensional patterns is being studied: for circular targets (Kelly & Magnuski, 1975), for unstructured (noise) patterns (Mitchell, 1976; Mostafavi & Sarkison, 1976), for two-dimensional sine wave patterns (Carlson et al., 1977), and for checkerboards (Kelly, 1976). One of the most significant discoveries in child psychology is that infants prefer to fixate some visual stimuli longer than other ones (Berlyne, 1958; Fantz, 1958). However, the mechanisms that control these preferences are still unclear, in spite of much experimentation. The most popular explanation relates the total (or mean) looking time to the “complexity” of the stimulus pattern. However, the concept of “complexity” is ambiguous for the following reasons: (1) it is specifically related to the pattern used as the stimulus; there exists no universal scale of “complexity”; (2) although the units of “complexity” are often not defined, “complexity” is usually related to numerosity, density, or some other quantifiable measure. We should like to consider most of the recent pattern preference studies as empirical attempts to find a stimulus parameter that is coherently and monotonically related to fixation preferences. However, the concept of “complexity” has remained an abstract, “etic” entity (to use the “emic”-“etic” distinction introduced into social sciences by K. L. Pike), which has not been related to the infant visual system. Let us suppose that visual preferences in infancy are determined by the visual images formed in the perceptual system of the infant. The infant prefers visual features that match hidher own perceptual capacities. In the interpretations of the visual preference data, the other possible factors regulating the infant’s visual attention (e.g., general activation state) are usually a priori considered to be less efficient than the features of the stimulus-and are seldom controlled in the experimental paradigms themselves. Let us take an analogous case from the field of the matched filters theory (Rosenfeld, 1969). If one has some idea about the transfer function of a filter, then it is possible to discover the signal that optimally matches this filter. The peak response from such a filter occurs when the form of the stimulus matches the weighted function of this filter. Therefore, we may propose that the concept of stimulus “complexity” should be replaced by the concept of the stimulus that optimally matches the infant’s perception. C . PERCEPTION OF TWO-DIMENSIONAL PATTERNS
Karmel and Maisel (1975) have written an excellent review of studies of the infant’s perception of two-dimensional patterns. Karmel and his co-researchers expressed looking preference as a function of the amount of contour per square
12
Jiiri ANik and Jaan Valsiner
degree of visual angle. The empirical function has an inverted U-shaped form that is optimally fitted by quadratic or cubic equations (Karmel, 1969; Karmfl& Maisel, 1975). For any infant, there exists a most preferred contour density level. Looking times will drop for patterns with contour densities below and above that optimal contour density level (Kannel & Maisel, 1975, Table 2.2). It is important that there is a significant correlation between behavioral preferences and pattern-dependent evoked potentials (Harris, Atkinson, & Braddick, 1976; Karmel, Hoffmann, & Fegy, 1974). Using two-dimensional patterns, we can again see the inverted U-shaped curve appropriate to the band-pass characteristic of the transfer function. However, this comparison islimited, because the stimuli (e.g., checkerboards and random check patterns, also Julesz-patterns) do not correspond to the single spectral line of the basic function. The stimuli employed possess a complex energy distribution in the spectral domain. The regular checkerboard pattern has a two-dimensional Fourier spectrum. The spectmm of a normally oriented checkerboard with 10' squares has four fundamental frequency components, which are located on the diagonal meridians at 4.2 cycles per degree from the origin, while the other harmonics are widely distributed throughout the spatial frequency plane (compare this to the two fundamental frequencies found in the square-wave grating). The higher harmonics have a hyperbolically decreasing amplitude (Kelly, 1976, Fig. 5 and Appendix A). However, the thresholds for two-dimensional patterns, as with the thresholds for one-dimensional patterns, can be explained in terms of the maximum amplitude of the two-dimensional Fourier spectrum. In the case of the checkerboard, this is equivalent to the amplitude of the fundamental frequency (Kelly, 1976; Kelly & Magnuski, 1975). On the assumption that infant looking preference is governed by the fundamental frequency, the checkerboard results may be treated as a measure of the two-dimensional transfer function. A correspondence between one- and two-dimensional cases is obvious, though exact numerical comparison is difficult. Karmel(l969) used regular checkerboards and randomly scattered contour test Patterns in his studies. These two types of stimuli are related to each other by the amount of contour or by the length of the white-black luminance transitions in the pattern. However, in the Fourier frequency domain these patterns have very different energy distributions (spectra). The random patterns are produced by the Markov process 5' = +a, for a constant duration of the impulse 6.The autacorrelation function of this process is expressed by a2(1 - 17116). (1) It is not difficult, by applying the Fourier transforms, to reveal the spectral distribution of this stochastic process: The energy spectrum has the following form: g ( w ) = v ( a sin W V / W V ) ~ (2) +(7) =
Visual Development in Ontogenesis
13
Thus, the random patterns have continuous spectra without any distinct fundamental frequency. Those patterns are the results of the low-frequency broad-band visual noise process with a peak at zero frequency (Rytoff, 1976). Random patterns contain considerable noise, which is fdtered out by a differentiation process in the visual system so that the amplitude of the useful signal is relatively weak compared to the redundant patkm having energy concentration at the fundamental frequency. It can be assumed that the difference between a regular checkerboard and random patterns does not result from the contour density difference. It may be that the description in terms of Fourier analysis is the optimal language for expressing the functioning of the mechanisms responsible for the visual processing of two-dimensional patterns. It is obvious that this kind of explanation is more powerful than the one using contour density (or “complexity”) as the basic stimulus parameter. The latter has a limited range of application; only a narrow class of visual stimuli having two levels of luminance may be described by this concept. Moreover, Fourier analysis has greater theoretical generalizability. In Fourier analysis, an arbitrary stimulus can be described in terms of the transfer function. The present argument on the usage of matched filters leads us to ask the following general question of the infant vision data: “What does the infant detect in different visual scenes?” Karmel and Maisel (1975) speculated about the relation between hypothetical receptive field properties and contour density. They assumed that the visual system responds to the average contour density value by integrating contour over area. They proposed that the image is analyzed by a set of receptive fields. The output of this system is determined by the convolution of the stimulus with the weighted function of the receptive fields in the spatial domain or by the multiplication of the Fourier spectrum of the stimulus with the transfer function. The complete modulation transfer function must be known in order to make predictions about the behavior of the system. Karmel and Maisel postulated the existence of an operation involving the “integration of the contour over area,” without any references to the properties of the receptive fields that would be able to perform that transformation. The authors prefer a phenomenological and qualitative description to a more exact and quantitative one. Karmel and Maisel (1975) proposed that the peak location of the inverted U-shaped preference function on the contour density axis would depend on the field size of the neurons, that is, the field size of the hypothetical processing routine. However, Kelly (1975) has shown that frequency selectivity depends not on variations in the size of receptive fields but on the regularity of their spatial distribution. Using fixation measures, Slater and Sykes (1977) presented evidence that the “amount of contour, ” even in a binary-luminance pattern, is ,not the primary determinant of the infant’s looking behavior. Different patterns (checkerboards, square wave gratings, etc.) having similar amounts of contour elicited remarkable differences in infant looking preferences.
14
Juri Allik and Jaan Valsiner
In summarizing the review of the studies conducted by Karmel and his associates, it is necessary to note their importance. Although the contour density measure of two-dimensional patterns has limited application and there are no processing routines specially tuned to this stimulus parameter, their formulation has helped to sharpen theoretical ideas in infant pattern perception. In terms of the spatial frequency approach, some conclusions can be drawn from the studies mentioned above: 1. The modulation transfer function of the newborn infant has a band-pass character and the entire transfer function passes frequencies about 10 times lower than those passed by the human adult visual system. Interestingly, there is great similarity between the quality of the visual systems of the human infant and of the cat in that both are myopic to a comparable degree. 2. With increasing chronological age, the modulation transfer function continuously shifts toward the higher end of the spatial frequency axis, approaching adult values by the middle of the first year of the infant’s life (see also Pirchio, Spinelli, Fiorentini, & Maffei, 1978). 3. There is fragmentary but quite impressive evidence that the infant’s transfer function behaves in a manner qualitatively similar to the adult modulation transfer function under conditions of light adaptation. With a decrease in luminance, the form of the transfer function becomes flatter and the peak shifts toward the lower spatial frequencies. These changes are usually interpreted as a weakening of inhibitory interactions in the visual system (see McCarvill & Karmel, 1970). 4. Karmel and Maisel (1975) advanced the very strong theoretical hypothesis that optimal stimuli, matching the properties of infant visual processing, elicit more active responses from the infant than do other stimuli. D. DEFICIENCY OF VISUAL RESOLUTION
Since the classic study by von Senden (1932), it has been widely accepted that restoration of sight following a cataract operation is not sufficient for efficient vision. However, early reports about postoperative visual functions were based mainly on phenomenological observation. Recently, some cases have been studied by means of experimental paradigms (e.g., Ackroyd, Humphrey, & Warrington, 1974; Gregory & Wallace, 1963; Umezu, Torii, & Uemura, 1975). How does early visual deprivation affect visual resolution ability? As a rule, the physical condition of the eye after surgery is sufficient to permit relatively good visual acuity. For example, Ackroyd et al. (1974) found that in the case of patient H. D., acuity was as good as 6/18 or 6/12. But the actual visual acuity was poorer than the acuity measure obtained from direct ophthalmological investigations of the eyes. More than 150 trials were required before H. D. was able to
Visual Development in Ontogenesis
15
state the presence or absence of a -5-cm square placed directly in front of her. In another study, Umezu et al. (1975) used Landolt rings as the acuity measure. The patient was able to find five out of six gap positions correctly if the Landolt ring for acuity of. 1 was placed at a distance of 25 cm. Therefore, acuity was .005 (.l X 25/50). This value is in the range of human newborn acuity. Ackroyd et al. (1974) noticed certain striking similarities between the case in which primary visual cortex was removed in the monkey and the phenomenology described in H. D. ’s case. After the removal of the primary cortex, however, the monkey’s spatial resolution was, in fact, better than H. D.’s. The qualitative picture that emerged was very much the same. This kind of similarity and the fact that human patients of that kind have had normal optics of the eyes restored by means of surgery, have been the basis for the discussions about “cortical blindness”: If a person has his eyes’ optics restored after functioning as blind for some time but still cannot see in a normal way, some changes must have taken place in the higher levels of the visual system. Additional support for the idea of “cortical blindness” of persons whose vision was restored after some time comes from the body of data on scotomata patients, whose visual fields are impaired after cortical damage. The rudimentary functions of the visual system of these patients are very similar in character to those described for recovered vision. Patients can see luminance transients in scotomata and make saccadic localizations of targets in the scotomata even though these targets are not consciously perceived (Perenin & Jeannerod, 1975; Poppel, Held, & Frost, 1973; Poppel, Von Cramon, & Backmund, 1975; Richards, 1973). In the context of our discussion, the most interesting studies are those of Bodis-Wollner (1972, 1976). He measured the contrast sensitivity function of patients with cerebral lesions. In several cases, it was parametrically demonstrated that the greatest loss in the contrast transfer function occurred at high spatial frequencies, even though attenuation also occurred in the midfrequency range. This implies that the cortical lesions more deeply affect the higher end of the axis of spatial frequency transfer functions. Routines that process finer aspects of the visual image may need more sophisticated metabolic processes to support their activity. Bodis-Wollner (1976) suggested that cortical cells tuned to higher spatial frequencies are especially vulnerable to metabolic deficit. This hypothesis may contribute to an understanding of the effect of lasting visual deprivation. Well-documented experiments suggest that spatial frequencies having different orientations are processed by separate mechanisms; in other words, separate routines of analysis are used for the processing of gratings having different orientations (e.g., Campbell & Kulikowski, 1966). If this is the case, it is possible that one orientational channel can be damaged independently of other channels. Astigmatism is a condition in which the eye’s refractive power differs in various meridians. An astigmatic lens produces a bIurred image along a certain
16
Juri Allik and Jaan Valsiner
visual meridian and a sharp image along the meridian perpendicular to the first one. When severe astigmatism is present shortly after birth and remains uncorrected throughout childhood, the conditions for partial visual deprivation in the human are satisfied. Freeman, Mitchell, and Millodot (1972) proposed that abnormal visual experience in the form of ocular astigmatism can cause permanent changes in the visual system. These orientational differences in visual resolution remain after complete optical correction because of the deficiency of visual resolution owing to the altered properties of the neural network. If the retinal image of a developing visual system suffers from astigmatism that brings with it an extensive blur along the horizontal axis, the visual cortex might adapt to the discordant input from the retina by “tuning” itself to the features clearly imaged along the vertical axis. Obviously, the development of neural connections is involved in resolution. Hence, resolution of horizontally imaged details would be Kduced (Freeman et al., 1972). This psychophysical finding was confirmed by electrophysiological experiments (Freeman & Thibos, 1973). Subjects who exhibit reduced resolution for a pattern of a particular orientation also show a decreased evoked potential response for the same pattern. Again, since an optical explanation of the effect can be ruled out, the results are consistent with the hypothesis that partial visual deprivation of higher spatial frequencies along a particular visual meridian can alter or stop development of that portion of the visual system sensitive to the particular visual axis. There can be no doubt that this effect has a neural origin, since some measurements were made by sinusoidal interference fringes formed directly on the retina (Mitchell, Freeman, Millodot, & Haegerstrom, 1973). There is a close relationship between the amount of astigmatism, as an optical defect, and meridional amblyopia, as a neural defect, with the axes of astigmatism and amblyopia coinciding. These relationships between astigmatism and amblyopia indicate a causal relation between image quality and the development of spatial resolution during childhood. The effect of partial visual deprivation can be shown by estimating the modulation transfer function of the human with astigmatic visual experience. Freeman and Thibos (1975a, 1975b) investigated contrast sensitivities of the meridional amblyope for sinusoidal gratings of diffenent spatial frequencies and orientations. Results showed that the contrast sensitivities for gratings of a given orientation in meridional amblyopes are reduced along the entire spatial frequency domain. The extent of meridional amblyopia may be expressed as the ratio of the contrast sensitivities corresponding to the astigmatic axis to those corresponding to the axis free from astigmatic influence. As was shown, this ratio is nearly constant for most spatial frequencies, including the frequencies of .5 and 1.0 cycles/ degree. Freeman and Thibos also established some other very important features of developmentally acquired meridional amblyopia. One subject had pronounced
Visual Development in Ontogenesis
17
oblique astigmatism and matching meridional amblyopia in one eye only. Another subject had very severe astigmatism in his left eye and required no refractive correction in his other eye. These two cases with monocular astigmatism suggest that visual experience can independently affect spatial resolution in each eye. Experience can selectively modify visual resolution along certain visual axes as well as visual resolution of monocular input. The simplest speculation is that cortical neurons tuned to a given orientation receive a normal monocular input from the normal eye, while at the same time the resolution in the astigmatic eye is highly abnormal. If we suppose that the meridional deficit is the result of defocusing, then it is possible to predict the amblyopic contrast sensitivity function by computing the attenuation factor for the appropriate defocused optics. In the case of the most severe sensitivity reduction, the experimental points are unlike any defocused curve, but, in moderate cases, the contrast reduction falls in the region of about .4 D defocus. Freeman and Thibos (1975a) concluded that the reduced contrast sensitivity functions can be equivalent to the theoretical effect of a small amount of defocus. This conclusion is very important in the context of our problem, since it allows us to connect the spectral content of the image on the retina with the perceptual capacities that are most likely predetermined by the spatial frequency spectrum available for the system. It was established that meridional amblyopia is not just a simple shift of the high-frequency cut-off. The modification of the contrast sensitivity function over the entire range of spatial frequencies suggests principal changes in the processing routines applied in the visual image analysis. It is possible to examine the properties of the transfer function in the spatial domain as one approach to the problem. By using the Fourier transform, one can convert data from the frequency domain into the spatial domain with the line-spread function (in the one-dimensional case) and point-spread function (in the twodimensional case). The resulting spatial weighting functions characterize the interaction of points of different spatial separation. As we mentioned above, the similarity between the forms of the neuropsychologically determined receptive field and the line- or point-spread functions have led to speculations about the functional similarity of the underlying phenomena. In the case of the amblyopic eye, it can be predicted that the weighting function in the spatial domain has broad character and lower values at the origin. This denotes decreased sensitivity in the case of merid-ional amblyopia compared with normal cases. The broadening of the weighting function or point-spread function can be considered to be a sign of increase in the integrative power in the neural network. In accordance with this suggestion, Beyerstein and Freeman (1976) found a drastic increase in summation distance, by a factor of two or three, along the amblyopic meridian. As the difference between the normal transfer function and the amblyopic one is diminished when the back-
18
Juri ANik and Jaan Valsiner
ground illumination is lowered, it seems that the differentiation operation (or lateral inhibition, which turns on at higher levels of illumination) has been lost. As a conclusion, it may be argued that the properties of the visual optics shape the form of perceptual functions. The young infant is highly myopic with fixed refraction. The growth of the visual optics increasingly improves the quality of the image formation process. A sharper, more finely detailed image is available to the infant as he grows older. If the growth of optical quality is stopped or limited early in life, the growth of visual capacities will also be limited. There can be no doubt that normal visual experience, without optical limitations, is a necessary requirement for the development of visual functioning. Specific visual deficit can cause corresponding deficits in perceptual functions. Both the visual optics and the visual environment affect perceptual development. The difference between horizontal-vertical and oblique grating resolution and contrast sensitivity is well documented for subjects living in a carpentered urban environment (Campbell, Kulikowski, & Levinson, 1966). The possibility that the visual environment associated with urban civilization can specifically shape the visual function is interesting. Annis and Frost (1973) provided some experimental evidence that orientational anisotropy, the oblique effect, depends upon a particular human visual environment. The oblique-horizontal difference is not as strong among Cree Indians as it is in the Euro-Canadian urban population. However, this evidence has some strong limitations in that no attention was paid to anisotropical effect not contributed by the environment, as Timney and Muir (1976) correctly pointed out. It is still risky to attempt a detaiIed formulation of how genetic preprogramming interacts with amounts and kinds of stimulation of the visual system in the system’s development. E. EXPERIMENTAL VISUAL DEPRIVATION
Although data on the human infant’s visual system development during the first months of life are scarce, evidence toward the understanding of this development can be obtained from the very wide and intense experimentation with animals, where fewer ethical considerations apply for scientific inquiry. Certainly, some problems emerge when we attempt to compare the ontogenetic development of the visual systems of different species, in the hope that some of these species can be comparable to the human infant as far as visual system development is concerned. However, in our overview, rather than concentrating on the problems of interspecies comparability, we try to utilize the different results of animal experimentation for the understanding of visual system development in general. Hubel and Wiesel(l962, 1965a) have shown that cats’ visual areas are highly organized for spatial orientation. The visual cortex consists of parallel slabs perpendicular to the surface of the cortex, within which cells have the same
Visual Development in Ontogenesis
19
preferred stimulus orientation. The preferred orientation of a cortical slab changes from one slab or column to another. The functional architecture of the monkey’s striate cortex is, in the orientational domain, very similar to that of the cat (Hubel & Wiesel, 1968). The cat (Albus, 1975b) and the monkey (Hubel & Wiesel, 1974a) have a systematic arrangement of orientational slabs or columns. In oblique or tangential microelectrode penetrations, the preferred orientation changes continuously with a lateral shift of the electrode’s tip relative to the surface of cortex. Hubel and Wiesel(1974b) and Albus (1975a) have shown that there are spatial subunits within the visual cortex, having diameters of 2-3 mm. This cortical block or cylinder contains the units that function as routines needed to analyze a region of the visual field. As the area of the visual field being analyzed increases in retinal eccentricity and the ganglion cell density in the retina is reciprocally decreased, there must be a constant relationship between number of retinal ganglion cells and cortical cells. Maffei and Fiorentini (1977) presented evidence that the visual cortex of the cat is spatially ordered in the spatial frequency domain. In penetration parallel to the surface (i.e., parallel to the slabs of constant orientation) cells of the same parallel layer represent a variety of preferred orientations (from 0 through 180” rotation), with maintenance of the same spatial frequency preference over the whole electrode track distance. The most provocative finding in the area of experimental visual deprivation research during the last decade is the impairment of certain orientations in the cat’s cortex as a result of early selective visual stimulation. Blakemore and Cooper ( 1 970) reared kittens in an environment consisting entirely of horizontal or vertical stripes. They reported that most of the responses of the cortical cells were like those in a normal animal, but the distribution of preferred orientation matched the orientation experienced by the animal during development. Similar results were reported by Hirsch and Spinelli (1970, 1971), who exposed a horizontal grating to one eye and a vertical grating to the other eye of the kitten. Cats reared under these conditions had visual cortexes with monocularly driven neurons preferentially responsive to the experienced orientation. Later, Blakemore and Mitchell (1973) reported that an extremely short exposure can modify the distribution of preferred orientations within the cortical cell population. Uniorientational experience for 1 hour at a peak time of sensitivity (twenty-eighth postnatal day) was sufficient for the development of a strong cortical bias in orientation toward the orientation experienced. This rapid modification is an extreme one; the functional plasticity of the cortical circuits remains for a longer time and exists even in the adult animal (e.g.. Creutzfeldt & Heggelund, 1975). Pettigrew and Freeman (1973) and Van Sluyters and Blakemore (1973) found environmentally induced neural properties in kittens’ cortex. For example, Pettigrew and Freeman reared kittens in a “planetarium” that had no straight contours and was composed of light spots. Compared with normal cats reared in a
20
Juri Allik and Jaan Valsiner
contour-rich environment, the “dot cats” had fewer cells with normal properties. Atypical receptive fields, called “spot detectors,” appeared in the cortexes of these kittens. These findings were treated as clear evidence of a causal role played by early visual input in the determination of the functional properties of the visual system. The original enthusiasm of the first studies was weakened by data showing limited changes in brain structures under environmental pressure or without any visual experience at all. Leventhal and Hirsch (1975) showed a remarkably weaker adaptation effect when the horizontal or vertical stripes were replaced by oblique ones. In this case, visual stimulation did not restrict the development of cells with the preferred horizontal or vertical orientation; these cells did not require a specific visual input for maintenance or for development. Selective visual stimulation also failed to modify rabbits’ visual cortexes (Mize & Murphy, 1973). The most serious argument against environmental modification in the cat was reported by Stryker and Sherk (1975). They had not been able to replicate the strong effects of Blakemore and Cooper (1970). Using a more quantitative technique of investigation, they failed to find a bias toward the orientation of the environment the animals under study had encountered. This discrepancy poses many questions and highlights the difficulties of the field, beginning with the exhausting procedure of surgery and ending in difficulties with maintaining cats in colonies that are notoriously liable to obliteration by epidemics (Barlow, 1975). However, although Stryker and Sherk failed to replicate the results of Blakemore and Cooper, they reported results similar to those of Leventhal and Hirsch ( 1975). Muir and Mitchell (1973,1975) and Mitchell, Giffin, and Timney (1977) have subjected cats to selective visual exposure for different periods of time in the f m t 4 months of life. The cats were trained on stimulus discriminations between gratings of various orientations and a blank field of the same mean luminance. The spatial frequency of the gratings was then systematically altered and the contrast sensitivity functions of the selectively stimulated and normal cats were determined. Selectively deprived cats performed the discrimination tests as well as normally reared ones, except for poorer acuity for the gratings oriented orthogonally to the one the animals had been exposed to. This orientational deficit appeared throughout the spatial frequency domain. There are striking similarities between this attenuation of sensitivity functions and those described in astigmatic humans (Freeman & Thibos, 1975a). d u i r and Mitchell expressed the cat’s visual acuity in terms of a crossing point between high-frequency asymptote and a line representing chance performance level. The deficits in acuity for a grating perpendicular to the experienced orientation varied between .26and .87 of an octave with a mean value of .48. Careful examination showed that the deficit was not the result of optical astigmatism or lowered motivation in deprived cats. It was also shown that the orientational amblyopia was long-lasting. Therefore, orientational acuity deficit seems to be caused by selective visual stimulation and
Visual Development in Ontogenesis
21
is located in the nervous system. Optical or other factors should be rejected as having no significance here. Hubel and Wiesel(1963), investigating receptive fields in very young kittens, reported that cortical cells in inexperienced kittens had all the specific properties of cells of the adult cat. This finding introduces new questions in visual development. First, do receptive field properties develop or does the kitten possess all the visual machinery of the adult cat just after eye-opening? Second, if some receptive field properties appear later during maturation, what is the role of visual experience in this progress? Contrary to the findings of Hubel and Wiesel, a lack of functional specificity in young kittens’ visual neurons was reported by Barlow and Pettigrew (1971). Supporting the view of Barlow and Pettigrew, several other studies failed to reveal orientational selectivity in the kitten’s visual cortex (Blakemore & Mitchell, 1973; Pettigrew, 1974). However, another study (Sherk & Stryker, 1976) provides support for the views of Hubel and Wiesel. Sherk and Stryker studied kittens that had not received visual experience because of a binocular lid suture performed before the age of natural eye-opening. They tested the kittens at 22-3 1 days of age, and found that most cortical cells preferred a bar stimulus over a moving spot. The data suggested that the cells closely approximated the selectivity found in the adult cat. Similar results were obtained in fur$er experiments by Wiesel and Hubel (1974) on visually naYve monkeys. Binocular lid suture was performed just after birth or at various ages after it, and the lids were kept closed for varying periods of time. Two visually inexperienced monkeys at the ages of 17 and 30 days showed the presence of a highly ordered sequence of orientation shifts that were in no obvious way different from those seen in adults. The main parameters were similar to adult values. It was concluded that the ordered columnar system was completely formed in early infancy and no visual experience was necessary for its development. The orientation tuning of the visual cells was also normal by adult standards, which indicates that the monkey’s visual cortex with respect to processing of orientational informationis innately determined and is not influenced by the lack of early visual experience. This conclusion is in agreement with anatomical observations showing that, compared to other species, the macaque is already well developed at birth-as far as the visual system is concerned. Experimental evidence suggests that the cat and rabbit are less mature at birth than the macaque. Many studies provide evidence for a gradual delayed appearance of specific properties in the visual neurons of the rabbit (e.g., Grobstein, Chow, Spear, & Mathers, 1973). The data suggest that the immature rabbit’s cortical neurons (Mathers, Chow, Spear, & Grobstein, 1974) and superior colliculus neurons (Makarova, 1974) are functionally different from those of the adult until at least 18 days after birth. It was found that simpler types of receptive fields were present near the time of eye-opening (10-1 1 days), while more complex functions, such as directionally selective and asymmetric receptive fields, did not
22
Jiiri Allik and Jaan Valsiner
appear until several days later (Makarova, 1974; Mathers et al., 1974). This picture of neural maturation is well correlated with the ability to form a conditioned reflex at different ages (Shilagina, 1974). Rapisardi, Chow, and Mathers (1975) detailed the maturation process in dorsal laterate geniculate neurons, suggesting that all parts of the rabbit visual system develop after eye-opening. Effects of prolonged visual deprivation have been the subject of many recent investigations. Imbert and Buisseret (1975) obtained results in agreement with those of Blakemore and Cooper (1970) that dark-reared 5- to 6-week-old kittens are totally nonspecific with respect to the functional properties of cortical cells. This is diametrically opposite to the finding of Stryker and Sherk (1975). A more multiple-sided picture was provided in a study by Singer and Tretter (1976). These authors found that the cells of 1-year-old dark-reared cats did not lack specific properties, but did lack the high selectivity for stimulus orientation characteristic of normal cells. The total number of orientation-specific cells was altered; the orientation selectivity loss in area 17 was about 39%, less than in area 18 (about 46%). One must certainly agree with Singer and Tretter that the main principles of cortical functional organization were not affected by deprivation. The structuresprobably became less specific than the normally reared cat’s cortical structure, but the basic outline was clearly stable. Light-deprivedcells lacked the sharp tuning for orientation and the sharp boundaries of the excitatory receptive field areas. Most of these changes can be accounted for by reduced efficiency in synaptic transmission. Intracortical inhibition is essential in the elaboration of the specific properties of cortical cells (Shevelyev, 1977). It appears that the absence of visual stimulation would freeze or impair the development of the intracortical specific connections. This would not be true if specific properties were already established at birth. In this case another explanation would seem to be more appropriate-that the specific properties of cortical cells become degraded without visual stimulation. In other words, lack of specificity results in degradation rather than in restriction of growth. Supporting this idea, Buisseret and Imbert (1 976) found that up to 3 weeks of age there were no significant differences in the proportion of the different types of cells in the dark-reared and normal kittens. Thereafter, in the dark-reared kittens, the specific cells tended to disappear while the nonspecific ones increased in number. Therefore, highly specialized neurons are present in the earliest stages of development, and specificity decreases gradually in the absence of visual experience. Garey and Pettigrew (1974) reported that visual deprivation causes a reduction in the density of synaptic vesicles in the axon terminals. Observable biochemical changes associated with light deprivation take place there (Pigareva, 1975; Uzbekov, 1976; Volokhov & Pigareva, 1975). Perhaps specific cells are vulnerable to deficits in metabolic processes. Conclusions It is difficult to draw definite conclusions from the studies analyzed above.
Visual Development in Ontogenesis
23
There are many difficulties and controversies within the field of visual experience and brain development. Many of the problems are presented in a comprehensive review article (Barlow, 1975), but we would like to emphasize a few of them here. First, behavioral effects, as a rule, are less dramatic than changes in the functional structure of the cortex following long-lasting visual deprivation. Light-deprived cats show remarkable or even complete recovery of visuomotor behavior (Ganz & Haffner, 1974; Van Hof-Van Duin, 1976a). In addition, Mitchell, Giffin, Muir,Blakemore, and Van Sluyters (1976) reported that a cat with a surgically rotated eye behaviorally compensated for this rotation, and was able to discriminate vertical-horizontal coordinates using only the rotated eye. Postdeprivationalrecovery has been shown on the receptive field level (Cynader, Bennan, & Hein, 1976). Second, diametrically different results were reported in experimental conditions that had no obvious setback differences (Blakemore & Cooper, 1970; Stryker & Sherk, 1975). In addition, Maffei and Fiorentini (1974) reported that selective exposure to a certain spatial frequency reduces sensitivity to gratings of the exposed frequency independent of orientation. Further studies are necessary to make the picture clearer. A large amount of data support the view that the principial structure of the visual cortex is already formed at the time of birth. The plan of this structure is determined by innate factors. We think that genetic factors shape routines executing analysis of spatial structures in the visual scene. These routines may be incomplete. However, anatomical findings suggest the appealing answer that complete refinement and maturation takes place during the early period of infancy. The experiments that showed unusual receptive field properties based on selective experience allow for the hypothesis that the process of development can be modulated by visual stimulation. While questions about the extent of the modulation remain open, the principial architecture seems fixed. Visual deprivation causes a noticeable impairment of the contrast sensitivity function. The results are in good agreement with human data on the astigmatic person’s contrast sensitivity. Amblyopia is well evidenced in the case of selective exposure as well as in the case of total visual deprivation. Therefore, we conclude that early visual stimulation is of importance at least for the building of a neural mechanism having high visual resolution abilities.
IV. Conceptualization of the Relative Functions of Environmental and Organismic Influences The relationship between nature and nurture, ever present as a problem in the empirical studies mentioned earlier, seems to pose difficulties more on the conceptual than on the empirical level. The experiments outlined in the previous
24
Jiiri ANik and Jaan Vabiner
sections showed how a new scientific finding can stimulate a number of studies and speculations that, especially in the latter case, go their own way with little concern for the objects under study. For example, Blakemore and Cooper (1970) and Hirsch and Spinelli (1970) thought that the simple idea of environmental modifiability of the visual cortex was the main strategy of vision development. Now, after certain controversies pertaining to the data have appeared, the enthusiasm for attributing the prime cause of visual development to the organism’s environment has greatly waned. Things that seem simple soon turn complicated-until simplicity is again assumed in some other way. Among scientists doing research on visual neurophysiology, Grobstein and Chow (1976) have tried to make some conceptual refinements to account for the discrepant findings. They use two distinct concepts to denote the different degrees of environmental influence on nervous system development. Experience sensitivity denotes the milder degree of influence; it means merely that the neuronal connectivity is affected by the organism’s individual experience, while the framework of connections in general is determined by internal factors. Experience dependency is said to be present when the functional appropriateness of neuronal connections depends on visual experience. Experience is necessary to maintain a connection pattern that is elaborated on the basis of genetic information; without the experience the function does not develop in its full form. The most elaborate system of concepts applied to elucidate the nature-nurture controversy has been provided by Gottlieb (1976a, 1976b). At the lowest level of environmental influence-that of maintenance-experience can preserve the already developed state or end point (with no regard to how that point has been reached). Maintenance can occur by means of suppression of those nerve connections that are functionally unrelated to a certain kind of experience. This concept is in accord with the theory of Marcus Jacobson (1974) stating that the initial number of neuronal connections is selectively reduced by means of experience. Facilitation refers to cases in which some neuronal connections would in general be able to develop without any experience, but experience is necessary to give them fine functional tuning. The findings mentioned above on the role of experience in visual ontogenesis show either facilitative or maintaining effects but no inductive effects at all (which effects might have been assumed at the beginning of the 1970s). Induction is the experiential influence on neuronal C O M ~ C ~ ~ O ~ S that leads to the appearance of some functional structure in the organism. Inductive influence is unambiguous; if the organism is exposed to some environmental parameter, the necessary connections to cope with it are formed. Without exposure, the connections would not develop (Gottlieb, 1976a). This conceptual system treats the function of the environment in more detail than was done previously, but the problem of how these effects work at the level of neuronal connections (e.g., by suppression of nonfunctional connections, by selective rapid growth of the functional ones, by simple degeneration of the nonfunctional ones) remains to be soIved.
Visual Development in Ontogenesis
V.
25
Perception of Flicker and Movement
A. INFANT RESPONSE TO FLICKER AND MOVEMENT
Our knowledge about infant responses to flicker is limited to the study by Karmel, Lester, McCarvill, Brown, and Hoffmann (1976). A parametric relationship was found between infant visual preferences and the occipital visual potential evoked by the temporal frequency of variation in test stimulus luminance. Both behavioral and electrophysiological response functions were best described by inverted U-shaped curves with a maximum response at 5-6 Hz. It is well documented that the temporal contrast sensitivity is determined solely by the amplitude of the fundamental frequency. Therefore, the quality (“sharpness”) of the subjective image regulates infant looking behavior. The infant’s response to flickering patterns depends on the flicker rate, just as with the adult’s response. We propose that the infant’s visual system processes the temporal modulation of luminance in a fashion qualitatively similar to that used by the adult visual system. Turning to movement, we must note that visual tracking occurs as early as several minutes after birth (Goren, Sarty, & Wu,1975). Clear movements measured by induced optokinetic nystagmus have been recorded on the fust day of postnatal life (Dayton, Jones, Aiu, Rawson, Steel, & Rose, 1964). Recordings of optokinetic nystagmus show that some newborns may possess a visual acuity of at least 20/150, which is remarkably better than static acuity. It was shown that newborn infants (from 8 hours to 10 days of age) were able to perform a visual task demanding the localization and maintenance of the image of a moving target on the general macular area (Dayton, Jones, Steele, & Rose, 1964). In the Russian literature, there are some early observations that the infant is able to localize peripheral moving stimuli (Figurin & Denisova, 1949), but this ability is considered to be not very accurate until 6-10 days after birth (Fonaryov, 1959, cited in Zaporozhets et al., 1967). The successful tracking of a moving object provides evidence of movement processing in the newborn infant’s visual system, but the optomotor effects are confounded with perceptual ones in this case. The studies cited above show that the newborn infant possesses routines for movement processing, but unfortunately they say nothing about the structure of these routines. Tauber and Koffler (1966) showed that optokinetic nystagmus is elicited in the infant not only by continuous moving stimulation but also by stroboscopic stimulation. Some attempts have been made to determine the threshold for visual motion detection in newborn infants. Ames and Silfen (1965) reported an increase in sensitivity to movement with age. If 75% looking time is taken as a criterion of movement threshold, then 7-week-old infants had a threshold of about 6.3 cm/ second and 20-week-olds, of about 2.8 cdsecond. Volkmann and Dobson (1976) investigated 1- to 3-month-old infants’ responses to a horizontal oscilla-
26
Jiiri Allik and Jaan Vahiner
tory motion. Consistent with the results of Ames and Silfen, an increase with age was found in the discrimination of the oscillating vs stationary patterns. The established function, relating looking behavior to rate of oscillation, resembles an inverted U-shape, with a peak at about 100 cycleslminute, independent of infant age. Therefore, infants show the highest sensitivity to movement with a midfrequency rate and/or moderate speed. Again, little can be said about the mechanisms of movement perception. The study by Harris, Cassel, and Bamborough (1974) can be regarded as evidence for the relative potency of relative movement (displacement of an object relative to a background) over absolute stimulus movement for infants as young as 8-28 weeks. A more complicated aspect of motion perception is reported by Bower, Broughton, and Moore (1970a), Ball and Tronick (197 1), and Ball and Vurpillot (1976). The defensive behavior of 1-week-old infants was evaluated in situations in which different objects were seen to approach by the infant. It was shown that the kinematic properties of a motion parallax field (see Koenderink & Van Doom, 1975) could be discriminated by the infant, and that defensive responses were appropriate for the direction of approach of objects. This selectivity obviously implies differential evaluation of the distribution of local movement over the visual field. Newborn infants certainly possess the processing routines for movement analysis, and these routines may even be rather complicated, as indicated by an appropriate evaluation of motion parallax. B. REARING IN STROBOSCOPICALLY ILLUMINATED AND UNIDIRECTIONALLY MOVING ENVIRONMENTS
Effective for the study of selective deprivation of movement information is a visual environment illuminated by a train of short flashes (say, with a duration of .01 second, and frequency of 2 Hz) visible as a sequence of static pictures. Such stroboscopic illumination “freezes” retinal displacements due to movement of either the visual environment or the perceiver. Cynader, Berman, and Hein (1973) reared cats in a stroboscopically illuminated environment (flash durations 10 psec, frequency .5 Hz).The number of both orientation and direction selective neurons observed was greatly reduced in the stroboscopically reared cats as compared to normal cats. A similar reduction of directionally selective neurons was observed in another study (Olson & Pettigrew, 1974). Flandrin, Kennedy, and Amblard (1976) demonstrated a more dramatic effect of stroboscopic rearing upon the cat’s superior colliculus;stroboscopicrearing significantly reduces directional preferences of the cortex, and it apparently almost completely eliminates directional preferences in the superior colliculus. Handrin et al. (1976) concluded that visual experience of motion constitutes an absolute criterion for the development of direction selectivity in the superior colliculus, while in the visual cortex it merely reduces the breadth of tuning. This conclusion
Visual Development in Ontogenesis
21
implies that total visual deprivation affects the cell properties of the superior colliculus in a way similar to selective movement deprivation. This last conclusion is supported by an experimental observation of dark-reared kittens (Flandrin & Jeannerod, 1975). Another method for selective deprivation of movement information is the rearing of kittens or infants of other species in a unidirectional environment. Daw and Wyatt (1974) tried to modify the directional sensitivity in the rabbit’s retina after selective visual exposure to a moving visual environment. The rabbit’s retinal cells were not modified under the environmental pressure. This negative result is contradictory to many other results that show modification of directional selectivity in the cat’s visual cortex and superior colliculus due to selective movement deprivation. Tretter, Cynader, and Singer (1975) exposed cats to unidirectionally moving black and white stripes for a few hours per day for 1-4 days at about 4 weeks of age. They found a strong bias in neuronal specificity toward movement direction experienced during this exposure. Similar results were reported by Cynader, Berman, and Hein (1975). Cats were reared in a visual environment in which irregular patches of luminescent paint moved constantly leftward. It was shown that most of the cortical cells, simple as well as complex, had leftward components in their directional preferences. However, the collicular neurons studied in these cats did not differ strongly from those of normal cats in the distribution of their preferred directions of movement. Daw and Wyatt (1976) and Berman and Daw (1977) introduced an important method for measurement of a critical period for movement perception. Kittens were placed inside a drum rotating leftward until a certain age, when the direction of rotation was changed. If movement-sensitiveneural networks have plastic properties, then selective exposure to a unidirectionally moving environment should shape this network. Daw and Wyatt (1976) showed that the critical period for developing directionally sensitive cortical mechanisms was about the fourth week of age. The “time window” of the critical period is relatively narrowapproximately 1 or 2 weeks wide. Before or after this critical period (outside the “window ”), exposure to selective visual environments does not significantly alter the responses of directionally tuned cortical units. It Seems extremely interesting that the critical period for movement terminates earlier than does the critical period for binocularity (Berman & Daw, 1977). Berman and Daw proposed that more “peripheral” synapses (the geniculocortical ones) retain their plasticity longer than more “central ’* (intracortical) ones, on the assumption that intracortical synapses are involved in direction-sensitive networks. The common belief that movement perception is not vulnerable to environmental modification by means of binocular enucleation or rearing in a unidirectional environment is seriously threatened by the nemphysiological studies cited. However, case studies of recovery from long-lasting blindness have not included parametric measures of movement perception abilities. It seems that we
Jiri Allik and Jaan Valsiner
28
have no information about the visual processing of temporal information after recovery from early blindness. The only thing we know from reported clinical observations is that patients are better able to answer “where” questions than “what” questions. However, this function is essentially different from the ability to process spatiotemporal luminance modulation, that is, two-dimensional timevaried visual patterns. Different kinds of spatiotemporal information are necessary to give satisfactory answers to the different questions. Therefore, the problem of processing movement information after prolonged deprivation is still open for future clarification.
VI. Binocular Vision A.
INFANT BINOCULAR VISION
Coordinated binocular fixation is a basic requirement for binocular vision. What do we know about the newborn’s ability to fixate objects binocularly at different distances from the perceiver? In a pioneering study, Ling (1942) showed that the infant’s ability to fixate binocularly is relatively poor during the first weeks of life. She gathered filmed records of vergence eye movements in response to target approach and recession along the median plane. The records, which permitted only qualitative analysis, showed an absence of systematic vergence movements until 7 weeks of life. Wickelgren (1967) measured infant scanning of two-dimensional patterns. He used the corneal reflection method (Haith, 1969; Maurer, 1975) to measure the area of the pattern that was scanned by each eye. The areas scanned by each eye overlapped only partly; for a centrally presented flickering light, the overlap was only about 9%. Wickelgren concluded that the two eyes were actually directed at different parts of the visual field. The neonate’s eyes were more divergent than is required for appropriate binocular fixation. This conclusion is limited by the accuracy of the corneal reflection technique. Moreover, other artifacts may make the corneal reflection technique invalid. One of these is due to projective distortion during reflection (Slater & Findlay, 1975a). Another is due to the anatomy of newborn’s eye; there is a disparity of about 8.5” between the newborn’s visual axis and the axis of regard (Slater L Findlay, 1972, 1975a). During binocular fixation, disparity between the recorded centers of the pupils and the actual axis of regard has a magnitude of 17”. Hence, the newborn baby’s divergent “squint” might be a result of an erroneous measuring technique. Binocular fixation can be estimated by two different methods: (1) measuring the vergence eye movement to the response of approaching or receding visual targets or (2) measuring the ocular responses to the target movement on the same plane of depth. In the latter case, conjugate eye movements (pursuit or saccadic)
Visual Development in Ontogenesis
29
are required for the appropriate binocular fixation. Dayton et al. (1964) electrooculographicallystudied the fixation reflex in 45 newborn infants. They found that at least 17 subjects were able to perform a visual task demanding the placement and maintenance of the image of a moving target on the general macular area. A similar conclusion was reached by Hershenson (1964). Dayton et al. (1964) documented that the newborn's saccadic eye movements were closely conjugated, although relatively coarse and hypermetric compared with those of an adult. Other studies have confirmed these results in general ( A s h & Salapatek, 1975; Harris & MacFarlane, 1974). Aslin and Salapatek (1975) studied the ability of 1- to 2-month-old infants to localize saccadically targets presented parafoveally or peripherally. Contrary to the previous finding, the infants' saccadic movements were found to be highly hypometric, and corrective saccades occurred frequently. However, the main conclusion is the same: Conjugate eye movements are present at early stages of development, suggesting that very young infants possess binocular fmation ability. The presence of conjugate eye movements in young infants is accepted by the majority of investigators, but there is less agreement about vergence eye movements. Slater and Findlay (1975b) found clear differences in fixation of targets at distances of 25 and 50 cm in infants ranging from 10 hours to several hundred hours in age. The difference between convergence angles for the two distances was 2.6", close to the expected value (3.lo). Taking into account necessary correction of the recorded data, they concluded that the objects were fmated bifoveally . The bifoveal fixation and appropriate convergence angle were not found when the target distance was 12.5 cm. Slater and Findlay (1975b) proposed that the lack of appropriate convergence was caused by the absence of accommodation for near vision in the newborns. However, it is reasonable to assume that the newborn is well equipped to fixate binocularly, and will manifest this ability when a suitable stimulus is shown at a reasonable distance from the eye. It is possible that binocular fixation is infrequently observed simply because of crying and other infant behaviors that seem to be more important from the evolutionary point of view than training of the binocular system in the first hours of infant life. Slater and Findlay summarized their studies by concluding that there seems to be no reason why the newborn baby should not have binocular vision. The suggestion that the major characteristics of binocular vision are present at birth was presented in Slater's contribution to the International Congress of Psychology in Paris, July 1976. Aslin (1977) used a luminous target moving along a path on the infant's visual midline and measured the vergence eye movements of the infant from 1 to 6 months of age. The amplitude of the approaching and receding targets was 12 to 57 cm. The results indicated that the ability to converge and diverge the eyes in the appropriate direction is present as early as 1 month of age, but only for some infants. As the infant's age increases, the frequency of making correct vergence eye movements also increases. Although the direction of ver-
30
Juri Allik and Joan Valsiner
gence movement is appropriate, the amplitude of vergence or divergence is erroneous. The convergence angle that is needed to maintain appropriate binoculrrr fixation as the target is moved is significantly below the expected value. The 1-month-old infants did not show changes in convergence sufficient to maintain binocular ftxation, but the 2-month-olds did. A s h (1977) noted that responses to the faster target movements improved with age (the speeds used in the study were 12 and 22 cdsec). Working with adults, Zuber and Stark (1968) realized that the vergence eye movements are relatively “lazy” movements and it would be predicted that a newborn baby’s vergence system is even more “lazy” than that of the adult. Therefore, it is quite possible that the slow speed (12 c d s e c in A s h ’ s experiment) nevertheless exceeds the resolution power of the system. In this respect the infant’s vergence eye movements need a more careful examination before any conclusions can be drawn. B. DISPARITY
Bower, Broughton, and Moore (1970) used a stemswpic device to create virtual objects at different distances in space. They claimed that the infants at the age of 1 week reached and grasped for the virtual object. The fact that the “object” had no tactual properties produced frustration and crying (although there might have been many other reasons for distress). This work provides evidence for stereoscopic vision in infancy as early as the first weeks of life. However, the experimental setup of this study is open to serious criticism. Appel and Camps (1977) presented a stereoscopic image of a toy rabbit to 7- to 9-week-old infants. Different groups were habituated to the particular disparity value of the image and after a period of habituation, the reactions (heart-rate deceleration) to the disparity changes were recorded. A sophisticated procedure was reported by Gordon and Yonas (1976). The subjects of this study were infants aged 20 to 26 weeks whose reaching behavior toward the position of stereoscopically presented virtual objects was videotaped. Analysis of the infants’ behavior showed that they discriminated between the far and near positions of the virtual object. When the virtual object was positioned out of reach, the infants tended to lean farther forward and to reach less frequently than when the virtual object was positioned within reach. As disparity was the only feature varied in these experimental conditions, the conclusion seems rather clear-5-month-old infants are sensitive to binocular information for depth. Similar results for older infants (18-32 months) were reported by Von Hofsten (1977). The infant’s reach was always directed toward the virtual position definqd by the angle of convergence. Atkinson and Braddick (1976) performed a study in which random dot stereograms were presented to the infant as stimuli. The ability to make discriminations based on binocular disparity was investigated
Visual Development in Ontogenesis
31
in 2-month-old infants by two methods: (1) fixation preference between patterns differing in the disparity they contained and (2) recovery from habituation of high-amplitude sucking when there was a change in disparity of the visual reinforcer. The results obtained with both methods indicated that at least some infants at the age of 2 months were sensitive to binocular disparity. As individual variation and differences in the methods are not important to the aims of the present discussion, we can conclude that the disparity-extracting system is developed by the age of 2 months. This ability to discriminate binocular disparities does not necessarily imply the perception of stereoscopic depth. It is quite possible that infants can detect disparity at an early age, but do not interpret this information as signifying a difference in distance. The interpretation of depth might be learned later, as a consequence of the correlation of disparities with sensory and motor events, as proposed by Atkinson and Braddick (1976). C.
ABNORMALITIES OF BINOCULAR VISION
About 2 to 4% of humans are stereoblind (Julesz, 1971; Richards, 1970). People who lack stereopsis are unable to use retinal disparity as a cue for depth. Richards (1970) found that genetic factors play an important role in this defect. However, stereoscopic vision is vulnerable to developmental influences as well. Therefore, acquired visual stereodefects are also frequent in the human population. There may be several reasons for impairment of the stereoscopic system: (1) binocular deprivation (blindness), (2) monocular deprivation, or (3) impairment of synchronous eye movements due to squint. Many perceptual defects involve the transfer of monocularly acquired information from one eye to another. For example, the magnitude of interocular transfer in the tilt aftereffect for normal vision is 70%. Interocular transfer implies the existence of binocular interaction, which probably takes place in the visual cortex. There must be binocular neurons that receive information from both eyes simultaneously. In other words, successful interocular transfer shows that the images presented to the left eye and to the right eye stimulate the same population of cortical neurons. Movshon, Chambers, and Blakemore (1972) were the first to demonstrate that humans who lack stereopsis also have little or no interocular transfer of the tilt aftereffect. Three groups of humans acted as subjects in this experiment. The fist group were normal subjects who were sensitive to depth cues in random dot stereograms. The second group were completely insensitive to depth cues in the tests; they had no clinical history of uncorrected or corrected strabismus, nor did they show strabismus on simple observation. The final group of subjects lacked stereopsis completely and also had a clinical history of strabismus; in some cases, the squint had been surgically corrected but in no case was the correction made
32
Juri Allik and Jaan Valsiner
before the age of 2 years. The results for the three groups were as follows: The normal group showed 70% interocular transfer, the nonstrabismic group lacking stereoscopic vision had interocular transfer around 4 9 8 , and the strabismic group had only 12% interocular transfer. The reduction of interocular transfer for strabismic subjects compared with normal ones suggests that the cortical units were not sensitive to binocular influences. No integration of the information received from the left and the right eyes took place. The loss of binocularity in the case of strabismus is apparently caused by lack of conelation of ocular alignment and optical inequality in the two eyes. This point has an important implication for understanding the development of stereoscopic vision: Normal congruent visual input is a necessary condition for maintenance (or perhaps development) of stereoscopic vision. Mitchell and Ware (1974) confirmed and extended the previous results. They measured percentage of interocular transfer vs stereoacuity and found a strict linear relationship between these two measures: Persons who have a higher mean percentage of interocular transfer show better stereoacuity. Hohmann and Creutzfeldt (1975) studied the effect of the age at which the squint f m t appeared on interocular transfer of the tilt aftereffect. Twelve children ranging in age from 5 to 15 years served as subjects. Nine of them had suffered from strabismus in early life and had had corrective operations between the ages of 3 and 5 years. Results were quite impressive: The later a squint began in the child, the higher was his mean interocular transfer and the better his binocular vision. The authors hypothesized that about 2 to 2.5 years of age may be considered the end of the critical period for the development of binocular vision in humans. At the same time Banks, A s h , and Letson (1975) published a study of a larger population of isotropic persons whose ages at the onset of strabismic deviation were well established. The amount of interocular transfer of the tilt aftereffect was used as a measure of the normality of binocular vision. The age at which the greatest influence in determining the development of normal binocular functions was found was 1.7 years. Banks et af. (1975) concluded that the sensitive period for the development of binocularity begins several months after birth and reaches a peak between 1 and 3 years of age. The absence of normal binocular experience during some part of this critical period causes irreversible changes or occasionally total lack of binocular functions. It is well known from ophthalmological observations that squint significantly decreases visual acuity in the nondominant eye. Von Noorden (1973a) attempted to determine the critical period for the development of amblyopia ex anopsia. The effects of unilateral lid closure and artificial esotropia on the development of visual acuity were studied in visually immature rhesus monkeys. He found that irreversible amblyopia occurred in all animals whose lids were sutured between birth and 9 weeks of age. During this period, only a brief period of occlusion (2-4 weeks) was necessary to cause severe amblyopia. Results on experimental
Visual Development in Ontogenesis
33
amblyopia in monkeys were compared with some cases of amblyopia in humans. Observation of patients with early unilateral visual deprivation showed that amblyopia ex anopsia can occur in children as old as 52 months. Therefore, the critical period in the human is much longer than that in monkeys. It is interesting that the only area where histological anomalies were noticeable was the lateral geniculate nucleus (von Noorden, 1973b; von Noorden & Middleditch, 1975). Hence, unilateral lid closure or esotropia causes unequal resolution power in the two eyes and at the same time results in an impairment of stereoscopic vision. The suppression of acuity in the nondominant eye can be seen even in an apparently normal visual system without obvious squint or refractive errors. Coren and Duckman (1975) studied cases of strabismic amblyopia and found that 57% were left-eye amblyopic. It is established that about 65% of the general human population is right-eye dominant and they therefore concluded that strabismic amblyopia occurs more frequently in the subdominanteye. Hence, the nondominant eye is chosen for functional expression more frequently than the dominant eye. In this respect, it is important to mention that ocular dominance is already developed at the age of 44 weeks, by which time the percentage of right-eye dominance is similar to that of adults (Coren, 1974). However, the situation is unfortunately complicated by the recent finding that there are at least three different types of ocular dominance: sighting dominance, sensory dominance, and acuity dominance (Coren & Kaplan, 1973; Porac & Coren, 1976). The binocular system is an example of extraordinary coordination between the oculomotor and perceptual systems. These systems are mutually dependent, in that exact binocular fixation requires an estimation of disparity of egocentric localization in both eyes and relatively good visual acuity from one side. Conversely, precise binocular fixation is required for normal binocular and stereoscopic vision. Various kinds of visual stimuli might serve as cues for vergence eye movements (Westheimer & Mitchell, 1969). For every vergence angle, there is an approximately constant error of binocular fixation (phoria). Richards (1969) showed that the fixation disparity changes with a change of wave-length of fixation stimuli. This furation disparity change may be the result of the different resolution capacities of the chromatic mechanisms. Therefore, the size of the operating receptive field determines the precision of binocular furation. The refractive error may cause a loss of stereoscopic vision by means of unwanted fixation disparity, For example, ophthalmologists have noted a correlation between the frequency of squint and the growthof visual acuity in infancy (Kogan, 1971). A large fixation error leads to a suppression of input from one eye. This is a possible cause of the frequent cases of diplopia. Richards and Miller (1969) found that about one-third of the whole population is not able to use convergence angle as a cue for depth. Those people who are unable to use convergence for depth estimation show an abnormal curve of fixation disparity with a tendency toward a greater error.
34
Juri Allik and Jaan Valsiner
The binocular system is a complicated structure involving the coordination of the activities of many subsystems, A common activity of stereoscopic vision is the fusion of retinal images in the right and left eyes. This fusion is achieved by vergence eye movements that eliminate large fixation disparity. The releasing stimulus for vergence (fusional) eye movements is disparity in egocentric localization. Obviously, only mechanisms receiving information from both eyes simultaneously can perform thisjob. As we see from the study by Richards and Miller (1969), an impairment of the vergence system may have taken place when fusion breaks down. Jones (1977) reported similar findings showing that the total lack of stereopsis is not necessarily accompanied by apparent anomalies of vergence eye movements. Large fixation disparity causes a lack of fusion and diplopia of images. However, even crude diplopia does not prevent stereoscopic vision. The implication is that binocular fusion is not an absolute requirement for depth perception. However, diplopia has other consequences-for example, binocular rivalry. Images differing in relative egocentric space exhibit binocular competition and suppression of the input from one eye. This normal mechanism preventing image doubling operates effectively during development. As discussed previously , the nondominant eye becomes amblyopic more frequently than the dominant eye. Prolonged suppression of the nondominant images causes amblyopia ex anopsia in the suppressed eye. One mechanism that may be involved in the phenomenal suppression is a degradation of binocularity. Let us suppose that binocular units that received incongruent input from the two eyes resolve this confusing situation by disregarding one set of inputs. Herman, Tauber, and Roffwarg (1974) found that monocular deprivation for 24 hours remarkably impairs stereoscopic acuity, but binocular deprivation does not affect the stereoscopic capacities noticeably. Hence, the stereoscopic system is impaired not by the disuse of the mechanism, but by the absence of balanced stimulation from the two eyes. If that disequilibrium takes place at any time during the critical period for development of binocularity, then the consequences of that abnormal experience are irreversible. D. DEVELOPMENT OF BINOCULAR VISION IN ANIMALS
Hubel and Wiesel (1%2) established that the majority of cells in the visual cortex are binocularly driven. The cortical cells have receptive fields in both eyes. These fields are functionally very similar and have a relatively corresponding localization in the visual field. Although the majority of neurons are binocularly driven, they are not equally excited by both eyes. This inequality is called eye dominance, and Hubel and Wiesel proposed a system for classifying the different phenomena subsumed under that category. Cells were divided into seven groups. Groups 1 and 7 are monocular cells driven by contralateral and ipsilateral eyes, respectively; groups 2 to 6 show increasing shift of eye dominance from contralateral to ipsilateral dominance. It was found that mofe cells
Visual Development in Ontogenesis
35
fall into groups 1 to 3 than into 5 to 7; that is, the majority of neurons are dominated by their input from the contralateral eye. Binocular cells stimulated through both eyes simultaneously respond best to an egocentrically located stimulus in both eyes. However, there are systematic deviations from an exact binocular correspondence. One of them, relative localization or binocular disparity, has been carefully investigated. Results lead one to conclude that there is disparity specificity in binocularly driven cells in the visual cortex of the cat (Barlow, Blakemore, & Pettigrew, 1967; Bishop, 1973; Nikara, Bishop, & Pettigrew, 1968; Pettigrew, Nikara, & Bishop, 1968). Hubel and Wiesel(l963) reported that the binocular system is present in very young kittens without visual experience. In later work, Wiesel and Hubel (1974) showed a similar state of affairs in a normal 2-day-old monkey, whose visual cortex had almost the same ocular dominance distribution as that found in the adult cortex. Similar to the organizationof visual cortex in the orientation domain, an ordered distribution of the ocular dominance column exists. Therefore, visual experience is not necessary for the development of cortical inputs from both eyes to a single neuron. However, prolonged binocular deprivation causes a decrease in binocularity in the visual cortex. Binocular deprivation of a few weeks duration in the monkey will bias the normal binocular distribution histogram remarkably, and there will be some shift toward monocularity (groups 1 and 7 become more dominant than others). Hence, binocular deprivation in both the cat and monkey results in deterioration of innate connections subserving binocular convergence in the visual cortex (Hubel & Wiesel, 1974). This finding has been extended by m a sures of the development of binocular disparity (Pettigrew, 1974). Disparity selectivity improved from birth until 30 days, when binocular neurons were seen approaching adult-like specificities. In the second and third weeks, there were no marked differences in cell specificity between normal and binocularly deprived animals. However, after the fourth and fifth weeks, significant differences become apparent between the experienced and inexperienced animals. Visually inexperienced cats do not have sharp binocular disparity tuning curves. These animals are less selective to binocular disparity in that they tolerate relatively large variations in the egocentric localization in each eye. One of the most stimulating findings in the field was the discovery that monocular eye closure or artificial squint is a more effective disturbing factor for the normal development of binocular vision than is total binocular deprivation (Wiesel & Hubel, 1965). This neurophysiological finding is in accord with the psychophysical demonstration reported above (Herman et al., 1974). E. MONOCULAR DEPRIVATION
Hubel and Wiesel (1970) discovered that monocular deprivation leads to almost total loss of binocular neurons. In the visual cortex of monocularly deprived
36
Juri AlIik and Jaan Valsiner
kittens, most cells can be influenced through the opened eye. Behavioral examination confirms this neurophysiological finding; such an animal appears behaviorally blind when forced to use its deprived eye (Dews & Wiesel, 1970). However, some evidence suggests that behavioral defects after monocular deprivation result from deficiencies in the complicated visuomotor control rather than in pattern identification, that is, visual perception per se (Van Hof-Van Duin, 1976b). Hubel and Wiesel (1970) established the existence of a critical period during which the changes in cortical ocular dominance occurred. They found that changes in ocular dominance took place only if the deprivation occurred between about 3 and 15 weeks of age. A deprivation period as short as 3 days is sufficient to cause remarkable changes in the ocular dominance distribution. The same experiment showed that the reorganizationof the cortex persisted despite a period of full visual experience after the initial deprivation period. Olson and Freeman (1975) studied the time course of the reduction of binocular units after the monocular deprivation period. A severe reduction in the proportion of units responsive to the deprived eye occurred over the f i t few days of monocular vision. Functional abnormalities appeared in scattered cases after 1 day of deprivation, were marked after 3 days, and became complete after 10 days. Schechter and Murphy (1976) were able to show that even 3 hours of monocular deprivation are sufficient to cause a reduction in cortical binocularity. However, this period of deprivation is insufficient to cause a shift in ocular dominance favoring the experienced eye. Hence, this result may be an indication that there are two different processes underlying binocularity and ocular dominance. The principal findings of the previous authors seem to be confirmed in the studies performed by Colin Blakemore and his associates. Peck and Blakemore (1975) found that little visual experience was needed to cause changes in the visual cortex for binocularity. Twenty hours of monocular experience produced a distinct shift in ocular dominance toward the open eye, but this effect needed more time for consolidation. Recording immediately after the period of deprivation was less successful than recording 2 days later, when the deprivation effect was found. Blakemore, Van Sluyters, and Movshon (1976) reported experiments in which kittens were reared in normal conditions until the age of 32 days and then were monocularly deprived for 10 days. These monocularly deprived animals seemed to be very similar to those who had visual experience before the 10 days of deprivation. This result clearly shows that the “window” of sensitivity is restricted from both sides of the age axis. Monocular occlusion affects the functional architecture of ocular dominance columns in the cortex of monkeys. In the normal animal, ocular dominance columns occupy approximately equal areas in the visual cortex with the width of an individual column being about 400 pm. However, after monocular deprivation, the columns corresponding to the deprived eye decrease in width, and the
Visual Development in Ontogenesis
37
width of the healthy eye’s columns expands at the expense of the deprived eye’s columns (Hubel, Wiesel, & LeVay, 1976). Hubel et al. (1976) concluded that the ocular dominance architecture of the monkey’s cortex changes markedly after monocular deprivation. This change is in contrast to the stability of orientation columns, which may collapse in an orientadonal domain but do not expand at the expense of other orientations. The response to monocular deprivation in the cat’s visual cortex is similar to the response found in the monkey’s visual cortex. Blakemore er al. (1976) showed in monocularly deprived animals that during long oblique electrode penetration, the sequential alternation between cells strongly dominated by one eye was similar to that found in normal animals. However, the electrode track distances in which the deprived eye dominated were drastically reduced. Therefore, cells dominated by the nondeprived eye expanded into the territory of the deprived eye, which resulted in an alteration of the entire functional architecture of the visual cortex of the cat. The majority of investigators working in the field of monocular deprivation accept the concept of competitive interaction between the pathways that go from the two eyes to the cortex. The existence of competitive interaction was proposed in its most explicit form by Murray Sherman. Sherman, Hoffmann, and Stone (1972) demonstrated that monocular deprivation causes a collapse of a specific cell type in the lateral geniculate nucleus (Y cells, the largest of the geniculate cells). This electrophysiological finding correlates well with the morphological demonstration of a reduction in the mean cell size in the layers of the geniculate nucleus that are innervated by the deprived eye. However, this change occurs only in the segments of the visual pathways that receive input from the binocular parts of the visual field; it has not been found in the parts of the visual pathways that receive their inputs from the monocular crescents of the visual field. Behavioral tests show that monocularly deprived animals respond to objects that result in input from the monocular crescent of the visual field (Sherman, 1973). The difference in behavior between the monocular and binocular segments of the visual pathways suggests that competitive interaction occurs between pathways that reach the cortex from each eye. Guillery (1972) and Sherman, Guillery, Kaas, and Sanderson (1974) developed a method for testing this proposal. The method consists of placing a lesion within the binocular segments of the opened retina. The most important and critical finding for the proposed theory of competitive interaction was that the damaged area in the opened eye can, to some extent, prevent deleterious effects of monocular deprivation. The morphological ground of this competitive interaction is a translaminal growth of axons from layers that are stimulated by the opened eye to the layers receiving no visual information (Hickey, 1975). Hence, changes in the representation of the normal eye in the visual cortex are extended at the expense of the deprived eye. Binocular competition occurs during a limited period of time, the “sensitive
38
Jiiri AUik and Jaan Valsincr
period. ” An appropriate method to demonstrate simultaneously the effects of binocular competition and the sensitive period is the procedure of reverse suturing. The lid of one eye is sutured until a certain age. After the sutured eye is opened, the other eye is closed. Movshon and Blakemore (1974) and Blakemore and Van Sluyters (1974) demonstrated that reverse suturing at 3-5 weeks caused a complete switch in ocular dominance. Reverse suturing at 14 weeks had almost no further effect on ocular dominance, because most cells were driven dominantly by the eye opened before the reversal of monocular deprivation. Therefore, results with reverse suturing are in good agreement with those of monocular deprivation: There are critical periods of sensitivity during which binocular competition occurs. As one might expect, artificial squint in animals leads to changes in the binocularity of the visual cortex very similar to those that occur in the case of monocular deprivation. For example, Yinon (1976) showed that the normal eye could drive twice as many cortical cells as the deviating eye. The period of susceptibility to the effect of squint is limited to the first 3 postnatal months; this finding, again, is in agreement with data on monocular deprivation. However, some data show that altered ocular motility per se is sufficient to affect cortical binocularity. Maffei and Bisti (1976) raised artificially strabismic kittens in total binocular deprivation and found a loss of binocularity in these cats. Moreover, there was a significant shift in dominance toward the normally moving eye similar to the shift that was experienced in strabismic animals with opened eyes. It was shown that the influence of the artificial strabismus on the cat’s visual cortex is specific: Only simple cortical cells are vulnerable to the immobilization of one eye (Fiorentini & Maffei, 1974). A significant reduction of binocularity in the visual cortex appeared after surgical rotation of one eye in the cat (Blakemore, Van Sluyters, Peck, & Hein, 1975; Yinon, 1975). In general, one can conclude that normal binocularity is maintained in the condition of visual and/or motor equality of the two inputs. The reduction of activity in one of these inputs causes reduction of binocularity because of competitive interaction between the two input pathways. The previously mentioned reduction seems to persist even in the adult cat, probably to a lesser degree and in a more reversible form (Maffei & Fiorentini, 1976). Severe reduction of binocularly driven cells in the cortex of monocularly deprived cats is accompanied by misalignment of the two eyes. Blake, Crawford, and Hirsch (1974) found that alternating monocular deprivation causes marked esotropia in the cat. In these animals, binocular convergence seems to be impaired as well. These results lead to the assumption that the loss of binocularity by means of monocular deprivation is a consequence of strabismus. In any case, disparity in the binocular system is only one of many stimulus cues that control vergence eye movement and binocular fixation. It is evident that binocularity is at least a necessary condition of appropriate eye alignment.
Visual Development in Ontogenesis
39
Studies of albinos are closely relevant to the facts reported here. It is established that vertebrates with laterally placed eyes and panoramic vision have in the majority of cases complete decussation of optic fibers at the optic chiasma. However, in animal albinos, the number of decussated fibers is significantly reduced, leading to an abnormal visual mapping in the lateral geniculate body and visual cortex (Guillery & Casagrande, 1976; Guillery, Casagrande, & Oberdorfer, 1974; Shatz, 1977a, 1977b). The nondecussated optic system develops because of retinal hypopigmentation and apparently does not depend on species differences (Creel, Dustman, & Beck, 1973; Creel, Witrop, & King. 1974). The nondecussated visual system leads to serious problems in Siamese cats (albinos), because cortical representation of the visual field is ambiguous. The probable mechanism preventing ambiguous representation in the visual cortex is the suppresion of one monocular input, as in experimental strabismus. This possibility was confirmed and it is clear that Siamese cats solve this problem in the manner described for normally pigmented animals ’ responses to abnormal visual inputs. Balanced and approximately congruent stimulation of both eyes is a critical requirement for the normal development of the binocular system. Taking into consideration our knowledge about the Siamese cat’s visual system, the requirement can be reformulated in terms of the congruence of the two inputs at the level of the visual cortex: Visual mapping in the two eyes must be fairly equal. Hence, the degree of congruence or equality would be an important subject of investigation. Blakemore (1976, 1977) investigated this problem very carefully. He showed that contrast differences in the two eyes do not significantly change normal cortical binocularity.
VII.
Conclusions
A. NEWBORNS’ VISUAL ABILITIES
The situation in infant visual perception research is typical for a developing scientific area. primary interest is being directed toward disproving widespread “folk stories” that constitute the prescientific stage of knowledge. It seems indisputable that the field of infant visual perception is devoted mostly to demonstrating the existence of global visual abilities in the infant. Very little is known about the fine structure of the visual routines in infant vision. There is also a great shortage of data concerning quantitative comparisons between infant and adult. However, in spite of these difficulties, we can say that the long-lived myth about the functional “blindness” of the infant is dying out. The infant seems to acquire new visual abilities with each improvement in the ingenuity and methodology of the researchers.
40
Juri Allik and Jaan Valsiner
We feel that there are compelling reasons to believe that a complete set of global visual abilities exists in the infant at or closely following birth. Therefore, the newborn is far from being a “blind person” and can analyze the visual environment along the most important dimensions, such as pattern, movement, color, and depth. Moreover, the infant processes these aspects in a manner qualitatively similar to that of the adult. We can presume that there is a strict homology between newborn and adult visual routines for analysis of the following aspects of visual scenes: (1) the spatial distribution of light in the retinal image, (2) the spatial position of visual objects, (3) temporal changes in luminance contours, (4) the movement of visual objects, and ( 5 ) the binocular depth due to binocular disparity. This list is not complete with respect to either the exactness or the exhaustiveness of its categories. For example, nothing has been mentioned here regarding infant color vision. Color vision is one of the most advanced branches in the study of infant visual perception mainly because of Marc Bornstein’s studies, which have thrown considerable light on the underlying mechanisms for newborn color vision (Bornstein, 1976; Bornstein, Kessen, & Weiskopf, 1976a, 1976b). A recent review by him gives the most thorough and thoughtful account of the research in this somewhat more independent area of infant vision research (Bornstein, 1978). Adding these data on color vision to those reviewed in the present paper, we can conclude that the infant possesses very advanced structures for visual routines even at the moment of birth. However, since we have very poor knowledge about the exact properties of these routines, it seems preferable to assume that they are relatively immature. This immaturity, indeed, may be only quantitative rather than qualitative-the manner in which the newborn infant views his world is similar to that of the adult, although less differentiated. The infant’s subjective image of the external world is evidently more robust than that of the adult. The presence of certain routines at the very early stages of development leads us to hypothesize that the principal structure of the visual machinery is planned by genetic instructions and that visual experience plays a lesser role in the building of the general architecture of the perceptual system than was thought in the past. However, the exact degree to which the visual system, with its different functions, is modifiable by experience in the course of its ontogenesis remains to be settled (Mitchell, 1978). B. COURSE OF DEVELOPMENT
Experiments on the environmental modifiability of the visual system convincingly demonstrate that developing vision shows adaptive abilities to match the properties of the environment. The problem here is how to determine the degree of adaptive plasticity. It seems that deficiencies arising from some special kind of
Visual Developmew in Ontogenesis
41
environmental input to the visual system may be caused by a process of degradation from the normal course of development, rather than by construction of special cortical mechanisms to adapt to the abnormal input. This hypothesis seems to gain support from the studies on binocular competition presented earlier. However, as far as the development of human infant vision is concerned, it is only a speculation. Experimental studies to date are not sophisticated enough to allow the people who like to “talk” about infants’ development (rather than study it) to put forward stronger propositions based on relevant data. It must be stressed that, despite intense interest and some considerable breakthroughs in infant vision during recent years, very little is known about the development of specific visual routines in human infants. Nevertheless, because it can be argued that there are similarities in the courses of visual development among human infants, monkeys, and cats (Mitchell, 19781, the prospects for relevant research are by no means poor. In studies of the environmental modifiability of the visual systems of young organisms, a methodological problem emerges, which may become a source of confusion in both research data and interpretations:Visual deprivation may cause impairment not only in the visual routines the investigator is most interested in unveiling, but also in the behavioral ways the organism makes use of the impaired visual input. This is especially the case in human studies; because of some environmental agent, understanding or interpretation of the visual representation may be impaired together with or instead of the routines of visual information processing. Although it is even more difficult to solve this problem in the case of infants, because of the difficulties of extracting visual routines from general behaviors in experiments, we feel that this kind of methodological difficulty needs to be considered. In general, we may conclude that although the general structure for vision is formed on the basis of genetic instructions, visual experience is necessary for elaboration of the system. Within certain limits, visual routines may adapt to the properties of the visual environment. The degree of this modifiability, however, varies with different visual routines. For example, binocular depth perception is more influenced by abnormal environmental stimulation than are other routines. It is natural to hypothesize that the criticalhensitive periods, if they exist, are also differently distributed for different visual routines along the age continuum. It can be hypothesized that all the “hardware” of the visual routines (e.g., specific pathways in the nervous system, age schedules for sensitive periods of different functions, the extent of modifiability by environmental stimulation) is preprogrammed by genetic factors, while the “software” of the organism’s functioning in real environments depends upon the nurturant factors-how effectively these factors can program the organism to behave in one way or another. In any case, it must be stressed that the general range of modifiability may itself be genetically programmed.
42
Jiiri Allik and Jaan Yalsiner
REFERENCES Ackroyd, C.. Humphrey, N. K.,& Warrington. E. Lasting effects of early blindness: A case study. Quarterly Journal of Psychology, 1974, 26, 114-124. Albus, K.A quantitative study of the projection area of the central and the paracentral visual field in area 17 of the cat. I. The precision of the topography. Experimental Brain Research, 1975,24, 159-179. (a) Albw, K.A quantitative study of the projection area of the central and paracentral visual field in area 17 of the cat. II. The spatial organization of the orientation domain. Experimental Brain Research, 1975, 24, 181-202. (b) Ames, E. W., & Silfen, C. K. Methodological issues in the study of age differences in infants’ attention to stimuli varying in movement and complexity. Paper presented at the meeting of the Society for Research in Child Development, Minneapolis, March 1965. Annis, R. C., & Frost. B. Human visual ecology and orientation anisotropies in acuity. Science, 1973, 182,729-731. Appel, M. A., & Campos, J. J. Binocular disparity as a discriminable stimulus parameter for young infants. Journal of Experimental Child Psychology, 1977, 23,4746. Apelle, S. Perception and discrimination as a function of stimulus orientation: The “oblique effect” in man and animals. Psychological Bulletin, 1972, 78,266-278. A s h . R. N. Development of binocular fixation in human infants. Journal of Experimentul Child Psychology, 1977, 23, 133-150. Aslin, R., & Salapatek, P. Saccadic localization of visual targets by the very young human infant. Perception and Psychophysics, 1975, 17,293-302. Atkinson, J., & Braddick, 0. Stereoscopic discrimination in infants. Perception, 1976, 5 , 29-38. Atkinson. I., Braddick, O., & Braddick, F. Acuity and contrast sensitivity of infant vision. Nature (bndon). 1974, 247,403-404. Ball, W., & Tronick, E. Infant responses to impending collision: Optical and real. Science, 1971, 171, 818-820. Ball, W. A., & Vurpillot, E. La perception du mouvement en profondeur chez le nounisson. L‘AnnPe Psychologique. 1976, 76,383-400. Banks, M. S., A s h . R. N., & Letson, R. D. Sensitive period for the development of human binocular vision. Science, 1975, 190,675-677. Banks, M. S., & Salapatek, P. Contrast sensitivity function of the infant visual system. Vision Research, 1976, 16, 867-869. Barlow, H. B. Visual experience and corticaldevelopment. Nature (London), 1975,258,199-204. Barlow. H. B., Blakemore, C., & Pettigrew, J. D. The neural mechanism of binocular depth discrimination. Journal of Physiology, 1%7, 193,327-342. Barlow, H. B., & Pettigrew, J. D. Lack of specificity of neurones in the visual cortex of young kittens. Journal of Physiology, 1971, 218,98-100. Barten, S.,Bims, B., & Ronch, J. Individual differences in the visual pursuit behavior of neonates. Child Development, 1971, 42, 313-319. Berlyne. D. E.The influence of the albedo and complexity of stimuli on visual fmtion in the human infant. British Journal of Psychology, 1958, 56,315-318. Berman, N., & Daw, N. W. Comparison of the critical periods for monocular and directional deprivation in cats. Journal of Physiology, 1977, 265, 249-259. Beyerstein, B. L., & Freeman. R. D. Increment sensitivity in humans with abnormal visual experience. Journal of Physiology, 1976, 260,497-514. Bishop, P. 0. Neumphysiology of binocular single vision and stereopsis. In R. Jung (Ed.), Handbook of sensory physiology (Vol. 7, Part 3): Central processing of visual information. Berlin and New York Springer-Verlag, 1973.
Visual Development in Ontogenesis
43
Blake, R.,& Antoinetti, D. N.Abnormal visual resolution in the Siamese cat. Science, 1976, 194, 109-1 10.
Blake, R.,Cool, S. J., & Crawford, M. L. J. Visual resolution in the cat. Vision Research, 1974, 14, 1211-1217.
Blake, R.,Crawford, M.L.J., & Hirsch, H.V. B. Consequencesof alternating monocular deprivation on eye alignment and convergence in cats. Investigative Ophthalmology. 1974, 13, 121126.
Blake, R., & Hirsch, H. V. B. Deficits in binocular depth perception in cats after alternating monocular deprivation. Science, 1975, 190, 1114-1116. Blakemore, C. The conditions required for the maintenance of binocularity in the kitten’s visual cortex. Journal of Physiology, 1976, 261, 423-444. Blakemre. C. Genetic instructions and developmental plasticity in the kitten’s visual cortex. Philosophical Transactions of the Royal Society of London, Series B. 1977, 278, 425-434. Blakemore, C., & Cooper, G. F. Development of the brain depends on the visual environment. Nature (London), 1970, 228,477-478. Blakemre. C., & Mitchell, D. E. Environmental modification of the visual cortex and the neural basis of leaming and memory. Nature (London), 1973, 241, 467-468. Blakemore, C., & Van Sluyters, R. C. Reversal of the physiological effects of monocular deprivation in kittens: Further evidence for a sensitive period. Journal OfPhysiology, 1974,237, 195-216. Blakemore, C., Van Sluyters, R. C., & Movshon, J. A. Synaptic competition in the kitten’s visual cortex. Cold Spring Harbor Symposia on Quantitative Biology, 1976, 40, 601-609. Blakemore, C., Van Sluyters, R. C., Peck, C. K., & Hein, A. Development of cat visual cortex following rotation of one eye. Nature (London), 1975, 257, 584-586. Bodis-Wollner, I. Visual acuity and contrast sensitivity in patients with cerebral lesions. Science, 1972, 178, 769-771.
BodisWollner, I. Vuherabiliq of spatial frequency channels in cerebral lesions. Nature (London), 1976, 261, 309-31 1.
Bornstein, M. H. Infants are trichromats. Journal of Experimental Child Psychology. 1976, 21, 425-445.
Bornstein, M. H. Chromatic vision in infancy. In H.W.Reese & L. P.Lipsitt (Eds.), Advances in child development and behavior (Vol. 12). New York Academic Press, 1978. Pp. 117-183. Bornstein, M. H., Kessen, W., & Weiskopf, S. The categories of hue in infancy. Science, 1976, 191,201-202. (a)
Bornstein, M. H., Kessen, W., & Weiskopf, S. Color vision and hue categorization in young human infants. Journal of Experimental Psychology: Human Perception and Performance, 1976, 2, 115-129. (b)
Bough, E. Stereoscopic vision in the macaque monkey: A behavioral demonstration. Narure (London), 1970, 2 2 5 , 4 2 4 . Bower, T. G. R. Developmem in igancy. San Francisco: Freeman, 1974. Bower, T. G . R., Broughton, J. M., & Moore, M. K. Infant responses to approaching objects: An indicator of response to distal variables. Perception and Psychophysics, 1970,9,193-196. (a) Bower, T. G. R., Broughton, J. M. & Moore, M. K. Demonstration of intention in the reaching behavior of neonate humans. Nature (London), 1970, 228,679- 681. (b) Buisswt, P.,& lmbert, M. Visual cortical cells: Their developmental properties in normal and dark reared kittens. .lournu! of Physidogy, 1976, 255,511-525. Campbell, S. W., Cooper,T. S., & Enroth-Cugell, C. The spacial selectivity of the visual cells of the cat. Journal of Physiology, 1%9, u)3, 223-235. Campbell, F. W., & Green,D. G. Optical and retinal factors affecting visual resolution. Journal of Physiology, 1965, 181, 576-593. Campbell, F. W.,& Kulikowski, J. J. Orientational selectivity of the human visual system. Journal of Physiology, 1966, 187, 437-455.
44
Juri ANik and Jaan Valsiner
Campbell, F. W., Kulikowski, J. J., & Levinson, J. The effect of orientation on the visual resolution of gratings. Journal of Physiology, 1966, 187, 427-436. Campbell, F. W., Maffei, L., & Piccolino, M. The contrast sensitivity of the cat. Journal of Physiology, 1973, 229,719-731. Carlson, V. R., Cohen, R. W., & Gorog, I. Visual processing of simple two-dimensional sine-wave luminance gratings. Vision Research, 1977, 17, 351-358. Cohen, L. B. Attention-getting and attention-holding processes of infant visual preferences. Child Development, 1972, 43,869-879. Cohen, L. B. A two process model of infant visual attention. Merrill-Palmer Quarterly, 1973, 19, 157- 180. Cohen, L. B., & Gelber, E. Infant visual memory. In L. B. Cohen & P. Salapatek (Eds.), Infant perception: From sensation to cognition (Vol. 1): Basic visualprocesses. New Y& Academic Press, 1975. Pp. 347-403. Cohen, L. B . , & Salapatek, P. (Eds.). Infantperception: From sensation to cognition (Vol. 1): Basic visual processes. New York: Academic Press, 1975. (a) Cohen, L. B., & Salapatek, P. (Eds.). lnfmt perception: From sensation to cognition (Vol. 2): Perception of space, speech, and sound. New York: Academic Press, 1975. @I) Coren, S . Development of ocular dominance. Developmental Psychology, 1974, 10, 304. Coren, S., & Duckman, R. H. Ocular dominance and amblyopia. American Journal of Optometry and Physiological Optics, 1975, 52,47-50. Coren, S., & Kaplan, C. P. Patterns of ocular dominance. American Journal of Optometry and Archives of American Academy of Optometry. 1973, 50,282-292. Creel. D. J.. Dustman, R. E., & Beck, E. C. Visually evoked responses in the rat, guinea pig, cat, monkey, and man. Experimental Neurology, 1973, 40,351-366. Creel, D., Witrop, C. J., & King, R. A. Asymmetric visually evoked potentials in human albinos: Evidence for visual system anomalies. Investigative Ophthalmology, 1974, 13, 430-440. Creutzfeldt, 0.D., & Heggelund, P. Neural plasticity in visual cortex of adult cats after exposure to visual patterns. Science, 1975, 188, 1025-1027. Cynader, M., Berman, N., & Hein, A. Cats reared in stroboscopic illumination: Effects on receptive fields in visual cortex. Proceedings of the National Academy of Sciences of the U.S.A., 1973, 70, 1353-1354. Cynader, M.,Berman, N., & Hein, A. Cats raised in a one-directional world: Effects on receptive fields in visual cortex and superior colliculus. Experimental Brain Research, 1975, 22, 267280. Cynader, M..Berman, N., & Hein, A. Recovery of function in cat visual cortex following prolonged deprivation. Experimental Brain Research, 1976, 25, 139-156. Daw, N. W., & Wyatt, H. J. Raising rabbits in a moving visual environment: An attempt to modify directional sensitivity in the retina. Journal of Physiology, 1974, 240, 309-330. Daw, N. W., & Wyatt, H.J. Kittens reared in a unidrectional environment: Evidence for a critical period. Journal of Physiology, 1976, 257, 155-170. Dayton, G. O., Jones, M. H., Aiu, P., Rawson, R., Steele, B.. & Rose, M. Developmental study of coordinated eye movements in the human infant. I. Visual acuity in the newborn human. Archives of Ophthalmology, 1964, 71, 865-870. (a) Jones, M. H., Steele, B., & Rose, M. Developmental study of coordinated eye Dayton, G. 0.. movements in the human infant. II. An electro-oculographic study of the fixation reflex in the newborn. Archives of Ophthalmology, 1964, 71, 871-875. (b) Dews, P. B.,&Wiesel, T. N. Consequences of monocular deprivation on visual behavior in kittens. JOUrMl of Physiology, 1970, 206, 437-455. Dodwell, P. C. Contemporary theoretical problems in seeing. In E. C. Carterette & M. P. Friedman
Visual Developmenr in Ontogenesis
45
(Eds.), Handbook of perception (Vol. 5): Seeing. New York Academic Press, 1975. Fantz, R. L. A method for studying early visual development. Perceptual and moror skills, 1956, 6, 13-15. Fantz, R. L. Pattern vision in young infants. Psychological Record, 1958. 8,43-47. Fantz, R. L. The origins of form perception. Scienrifc American, 1961,204, 66-72. Fantz, R. L. Pattern vision in the newborn infant. Scienrifc American, 1963,140, 296-297. Figurin, N. L.,& Denisova. M. P. Srages in the development of children of agesfrom birth to 1 year. Moscow: Medgiz, 1949. (In Russian; orig. publ. 1929) Fiorentini, A., & Maffei, L. Change of binocular properties of the simple cells of the cortex in adult cats following immobilization of one eye. Vision Research, 1974, 14, 217-218. Flandrin, J. M., & Jeannerod, M. Superior colliculus: Environmental influences on the development of directional responses in the kitten. Brain Research. 1975, 89, 348-352. Flandrin, J . M., Kennedy, H.,& Amblard, 8 . Effects of stroboscopic rearing on the binocularity and directionality of cat superior colliculus neurons. Brain Research, 1976,101, 576-581. Fox. R., & Blake, R. Stereoscopic vision in the cat. Nature (London), 1971,233, 55-56. Freeman, R. D. Asymmetries in human accommodation and visual experience. Vision Research, 1975,is, 483-492. Freeman, R. D., Mitchell, D. E., & Millodot, M. A neural effect of partial visual deprivation in humans. Science, 1972, 175, 1384-1386. Freeman, R. D.,& Thibos, L. N. Electrophysiological evidence that abnormal early visual experience can modify the human brain. Science, 1973, 180,876-878. Freeman, R. D.,& Thibos, L. N. Contrast sensitivity in humans with abnormal visual experience. Journal of Physiology, 1975,247, 687-710.(a) Freeman, R. D., & Thibos, L. N. Visual evoked responses in humans with abnormal visual experience. Journal of Physiology, 1975, 247,711-724. (b) Ganz, L.,& Haffner, M. E. Permanent perceptual and neurophysiological effects of visual deprivation in the cat. Experimental Brain Research, 1974, 20, 67-87. Garey, L. J., & Pettigrew, J. D. Ultrastructural changes in kitten visual cortex after environmental modification. Brain Research, 1974, 66, 165-172. Gordon, F. R., & Yonas, A. Sensitivity to binocular depth information in infants. Journal of Experimental Child Psychology. 1976,22,413-422. Goren, C. Form perception, innate form preferences, and visually-mediared head-turning in the human neonate. Paper presented at the meeting of the Society for Research in Child Development, Denver, Col., April 1975. Goren, C. C., Sarty, M . , & Wu, P. Y. K. Visual following and pattern discrimination of face-like stimuli by newborn infants. Pediatrics, 1975.56, 544-549. Gottlieb. G.Ontogenesisof sensory function in birds and mammals. In E. Tobach, L. R. Arenson, & E. Show (Eds.), The biopsychology of development. New York: Academic Press, 1971. Pp. 67-128. Gottlieb, G. The roles of experience in the development of behavior and the nervous system. In G. Gottlieb (Ed.), Studies on the development of behavior and the nervous sysiem (Vol. 3): Neural and behavioral specificity. New Yo& Academic Press, 1976. Pp. 25-54. (a) Gottlieb, G. Conceptions of prenatal development Behavior embryology. Psychological Review, 1976, 83, 315-334.(b) Gregory, R. L., & Wallace, J. G. Recovery from early blindness: A case study. Experimental PsychorogY Society Monograph, No. 2, 1%3. 46 p. Grobstein, P., & Chow, K. L. Receptive field organization in the mammalian cortex: The role of individual experience in development. In G. Gottlieb (Ed.). Studies on the development of behavior and the nervous system (Vol. 3): Neural and behavioral specificiiy. New York Acedemic Ress, 1976,4. 155-193.
46
Jiri Allik and Jaan Valsiner
Grobstein, P.,Chow, K. L., Spear,P. D.,& Mathers, L. H. Development of rabbit visual cortex: Late appearance of a claas of receptive fields. Science, 1973, 180, 1185-1 187. Guillery, R. W. Binocular competition in the control of geniculate cell growth. Journal of Comparative Neurology. 1972, 144, 117-127. Guillery, R. W., & Casagrande, V. A. Adaptive synaptic connections formed in the visual pathways in response to congenitally aberrant inputs. Cold Spring Harbor Symposia on Qwntitative Biology, 1976, 40,611617. Guillery, R. W., Casagrande, V. A., & Oberdorfer, M. D. Congenitally abnormal vision in Siamese cats. Nature (London). 1974, 252, 195-199. Haith, M. M.Infrared television recording and measurement of ocular behavior in the human infant. American Psychologist, 1969, 24, 279-283. Haith. M. M., & Campos. J. J. Human infancy. AnnuulReview OfPsychology, 1977,28,251-293. Harding, T. H., & Yates, J. T. Monkey contrast threshold for aperiodic patterns. Journal of the Optical Society of America, 1976, 66, 131-138. Harris. L., Atkinson, J.. & Braddick, 0. Visual coneast sensitivity of a 6-month-old infant measured by the evoked potential. Nature (London), 1976, 264,570-571. Harris, P., & MacFarlane, A. The growth of the effective visual field from birth to seven weeks. Journal of Experimental Child Psychology, 1974, 18, 340-348. Harris, P. L., Cassel, T. L., & Bamborough, P. Tracking by young infants. British Journal of Psychology, 1974, 65, 345-349. Haynes. H., White, B.L.. & Held, R. Visual accommodationin human infants. Science, 1965, 148, 528-530. Held, R., & Hein, A. Movement produced stimulation in the development of visually-guided behavior. Jownol of Comparative and Physiological Psychology, 1%3, 56,872-876. Herman, J. H.,Tauber, E. S., & Roffwarg, H. P.Monoculsr occlusion impairs stereoscopic acuity, but total visual deprivation does not. Perception and Psychophysics, 1974, 16, 225-228. Hemhenson. M. Visual dwrimination in the human newborn. Journal of Comparative and Physiological Psychology, 1964, 58, 270-276. Hickey, T. L. Translamina1growth of axons in the kitten dorsal lateral geniculate nucleus following removal of one eye. Journal of Comparative Neurology, 1975. 161,359-382. Hirsch, H. V. B., & Spinelli, D. N. Visual experience modifies distribution of horizontally and vertically oriented receptive fields in cats. Science, 1970, 168,869-871. Hirsch, H. V. B., & Spinelli, D. N. Modification of the distributionof receptive fiild orientation in cats by selective visual exposure during development. Experimental Brain Research, 1971, 13, 509-527. Hohmann, A., & Creutzfeldt,'O. D. Squint and the development of binocularity in humans. Nature (London), 1975, 254,613-614. Hopkins, H. H. The frequency response of a &focused optical system. Proceedings of the Royal Society of London. Series A , 1955, 231,91-103. Hubel, D. H., & Wiesel, T. N. Receptive fields, binocular interaction and functional architecture- in the cat's visual cortex. Journal of Physiology, 1962, 160, 106-154. Hubel, D. H., & Wiesel, T. N. Receptive fiilds of cells in striate cortex of very young, visually inexperienced kittens. Journal of Neurophysiology, 1963, 26, 994- 1002. Hubel, D. H.. & Wiesel. T. N. Receptive fiilds and functional architeehue in two nonstriate visual areas (18 and 19) of the cat. Journal of Neurophysiology, 1965, 28,229-289. (a) Hubel, D. H., & Wiesel, T. N. Binocular interaction in striate cortex of kittens reared with artifical squint. Journal of Neurophysiology, 1%5,28, 1041-1059. (b) Hubel, D. H., & Wiesel, T.'N. Receptive fields and functional architecture of monkey striate cortex. Journal of Physiology, 1968, 195,215-243. Hubel. D. H., & Wiesel. T. N. The period of susceptibility to the physiological effects of unilateral eye closure in kittens. Journal of Physiology, 1970, 206, 419-436.
Visual Developmenf in Onfogenesis
47
Hubel, D. H., & Wiesel, T. N. Sequence regularity and geometry of orientation columns in the monkey striate cortex. Journal OfComparafiveNeurolo(py. 1974, 158,267-294. (a) Hubel, D. H., 8c Wiesel, T. N. Uniformity of monkey striate cortex: A parallel relationship between field size, scatter and magnification factor. Journal of Comparafive Neurology, 1974, 158, 295-306. (b) Hubel, D. H., Wiesel, T. N., & LeVay, S. Functional architecture of area 17 in normal and monocularly deprived macaque monkeys. Cold Spring Harbor Symposia on Quantitative Biology, 1976, 40, 571-579. Humphrey, N. K. What the frog’s eye tells the monkey’s brain. Brain, Behuviour and Evolution, 1970, 3,324-327. Imbert,M.,& Buisseret, P. Receptive fiild characteristics and plastic properties of visual cortical cells in kittens reared with or without visual experience. Experimenfal Brain Research, 1975, 22325-36. Jacobson, M.A plentitude of neurons. In G. Gottlieb (Ed.), Sfudies on the development of behavior and the nervous system (Vol. 2): Aspecfs of neurogenesis. New York: Academic Press, 1974. 4. 151-168. Jannerod, M. Wficit visuel persistant chez les aveugles nCs opMs donnbs cliniques et exp6rimentales. L’Annde Psychologique, 1975, 75, 169-196. Jones, R. Anomaliesof disparity detection in the human visual system. Journal of Physiology, 1977. 264, 621-640. Julesz, B. Foundations of cyclopean perception. Chicago: University of Chicago Press, 1971, Karlson, J. L. Evidence for recessive inheritance of myopia. Clinical Generics, 1975. 7 , 197-202. Karmel, B. Z. The effect of age, complexity, and amount of contour on pattern preferences in human infants. Journal of Experimental Child Psychology, 1969, 7, 339-354. Karmel, B. Z., Hoffmann, R.F.,& Fegy. M.I. Processing of contour information by human infants evidenced by pattern-dependent evoked potential. Child Development, 1974, 45, 39-48. Karrnel, B. Z., Lester, M. L., McCarvill, S. L., Brown, P., & Hoffmann, M. J. Correlation of infants’ brain and behavior response to temporal changes in visual stimulation. PsychophysidOgy, 1977, 14, 134-142. Karrnel, B. Z., & Maisel, E. B. A neuronal activity model for infant visual attention. In L. B. Cohen & P. Salapatek Ws.),Infant perception: From sensation to cognifion (Vol. 1): Basic visual processes. New York: Academic Press, 1975. Kelly, D. H. Frequency doubling in visual responses. Journal of rhe Optical Society of America, 1966.56, 1628-1633. Kelly, D. H. Spatial frequency selectivity in the retina. Vision Research, 1975, 15, 665-672. Kelly, D.H.Pattern detection and the two-dimensional Fourier transform: Flickering checkerboards and chromatic mechanisms. Vision Research, 1976, 16, 277-287. Kelly, D. H. Flicker. In D. Jameson & L. N. Hurvich (Eds.), Handbook of Sensory Physiology (Vol. 7, Part 4): Visual Psychophysics. Berlin and New York: Springer-Verlag, 1972. Kelly, D. H., & Magnuski, H. S. Pattern detection and the two-dimensional Fourier transform: Circular targets. Vision Research, 1975, 15, 911-915. Kelly, D. H., & Savoie, R. E. A study of sine-wave contrast sensitivity by two psychophysical methods. Perception and Psychophysics, 1973, 14, 313-318. Kessen, W., Salapatek, P., & Haith, M. The visual response of the human newborn to linear contour. Journal of Experimenfal Child Psychology. 1972, 13,9-20. Kinney, D. K., & Kagan, J. Infant attention to auditory discrepancy. Child Developmenf, 1976,47, 155- 164. Koenderink. J. J., & Van Doom, A. J. Invariant properks of the motion parallax field due to the movement of rigid bodies relative to an observer. Opfica Acfa. 1975, 22,773-791. Kogan, A. I. The binocular system and 3-dimension space perception. In Handbook ofphysiology (Vol. 4): I . Sensory system physiology. Leningrad: Nauka, 1971. (In Russian)
48
Juri Allik and Jaan Vakiwr
Krueger, H.,& Moser, E. A. On the approximation of the optical modulation transfer function (MTF) by analytical functions. Vision Research, 1973, 13, 493-494. Krueger, H.,Moser, E. A., & Zrenner, E.Influence of defocusing on retinal images of test patterns calculated with the modulation transfer function. Ophthalmological Research, 1973, 5 , 33 1341. Leehey, S.C., Moskowitz-Cook, A., Brill, S.,& Held, R. Orientational anisotropy in infant vision. Science, 1975, 190,900-902. Legkndy, C. R. Can the data of Campbell and Robson be explained without assuming Fourier analysis? Biological Cybernetics, 1975, 17, 157-163. Leventhal, A. G., & Hirsch, H.V. B. Cortical effects of early selective exposure to diagonal lines. Science, 1975, 190, 902-904. Ling, B. C. A genetic study of sustained visual fixation and associated behavior in the human infant from birth to six months. Journal of Generic Psychology, 1942, 61, 221-277. Macle~d,I. D. G., & Rosenfeld, A. The visibility of gratings: Spatial frequency channels or bar-detecting units? Vision Research, 1974. 14, 909-915. Maffei, L., & Bisti. S. Binocular interaction in strabismic kittens deprived of vision. Science, 1976, 191, 579-580. Maffei, L., & Fiorentini, A. Geniculate neural plasticity in kittens after exposure to periodic gratings. Science, 1974, 186,447-449. Maffei, L., & Fiorentini, A. Asymmetry of motility of the eyes and change of binocular properties of Cortical cells in adult cats. Brain Research, 1976, 105,73-78. Maffei, L., & Fiorentini, A. Spatial frequency rows in the striate visual cortex. Vision Research, 1977, 17,257-264. Makarova, 0 . N. Activity of neurons of Colliculi superiores of the kitten in early ontogenesis. Pavlov Journal of Higher Nervous Activity, 1974, 24,378-385. (In Russian) Mansfield, R. J . W. Neural basis of orientation perception in primate vision. Science, 1974, 186, 1133-1 135. Marzi, C. A., Simoni, A., & Di Stefano, M. Lack of binocularly driven neurones in the Siamese cat’s visual cortex does not prevent successful interocular transfer of visual form discrimination. Brain Research, 1976, 105,353-357. Mathers, L. H., Chow, K. L., Spear, P. D., & Grobstein. P. Ontogenesis of receptive fields in the rabbit striate cortex. Experimental Brain Research, 1974, 19,20-35. Maurer, D.Infant visual perception: Methods of study. In L. B. Cohen & P. Salapatek (Eds.), Infant perception: From sensation to cognition (Vol. 1): Basic visual processes. New York: Academic Press, 1975. McCall, R. B. Attention in the infant: Avenue to the study of cognitive development. In D. Walcher & D. Peters (Eds.), The development of self-regulatory mechanisms. New York Academic Press, 1971. Pp. 109-141. McCarvill, S. L., 8r Kannel, B. Z. A neural activity interpretation of luminance effects on infant pattern preferences. Journal of Experimental Child Psychology, 1970, 22, 363-374. Mitchell, D. E. Effect of early visual experience on the development of certain perceptual abilities in animals and man. In R. D. Walk & H. L. Pick (Eds.), Perception and experience, New York Plenum, 1978. Pp. 37-75. Mitchell, D. E., Freeman, R. D., Millodot, M., & Haegerstrom, G. Meridional amblyopia: Evidence for modification of the human visual system by early visual experience. VisionResearch, 1973, 13, 535-558. Mitchell, D. E., Giffin, F., Muir, D., Blakemore, C., & Van Sluyters, R. C. Behavioral compensation of cats after early rotation of one eye. Experimental Brain Research, 1976,25,109-113. Mitchell, D. E., Giffin, F., & Timney, B. A behavioural technique for the rapid assessment of the visual capabilities of kittens. Perception, 1977, 6 , 181-193.
Visual Development in Ontogenesis
49
Mitchell, D. E., & Ware, C. Interocular transfer of a visual after-effect in normal and stereoblind humans. Journal of Physiology, 1974, 236, 707-721. Mitchell, 0. R. Effect of spatial frequency on the visibility of unstructured patterns. Journal of the Optical Society of America. 1976, 66, 327-332. Mize, R. R., & Murphy, E. H. Selective visual experience fails to modify receptive field properties of rabbit striate cortex neurons. Science, 1973, 180, 320-323. Mostafavi, H., & Sarkison, D. J . Structure and properties of a single channel in the human visual system. Vision Research, 1976. 13, 957-968. Movshon, J. A., & Blakemore, C. Functional reinnervation in kitten visual cortex. Nature (London), 1974, 251, 504-505. Movshon, J. A., Chambers, B. E. I., & Blakemore, C. Interocular transfer in normal humans, and those who lack stereopsis. Perception, 1972, 1,483-490. Muir, D. W., & Mitchell, D. E. Visual resolution and experience: Acuity deficits in cats following early selective visual deprivation. Science, 1973, 180, 420-422. Muir, D. W.,& Mitchell, D. E. Behavioral deficit in cats following early selected visual exposure to contours of a single orientation. Brain Research, 1975, 85,459-477. Nikara, T., Bishop, P. 0.. & Pettigrew, J. D. Analysis of retinal correspondenceby studying single units in cat striate cortex. Experimental Brain Research, 1968, 6, 353-372. Olson, C . R., & Freeman, R. D. Progressive changes in kitten striate cortex during monocular vision. Journal of Neurophysiology, 1975, 38,26-32. Olson, C. R., & Pettigrew, J. D. Single units in visual cortex of kittens reared in stroboscopic illumination. Brain Research, 1974, 70, 109-204. Packwood, J., & Gordon, B. Stereopsis in normal domestic cat, Siamese cat, and cat raised with alternating monocular occlusion. Journal of Neurophysiology. 1975, 38, 1485- 1499. Peck, C. K.,& Blakemore, C. Modification of single neurons in the kitten's visual cortex after brief periods of monocular visual experience. Experimental Brain Research, 1975, 22,57-68. Perenin, M. T., & Jeannerod, M. Residual vision in cortically blind hemifields. Neuropsychologia, 1975, 13, 1-7. Pettigrew, J. D.The effect of visual experience on the development of stimulus specificity by kitten cortical neurones. Journal of Physiology, 1974, 237, 49-74. Pettigrew, J. D., & Freeman, R. D. Visual experience without lines: Effect on developing cortical neurons. Science, 1973, 182, 599-601. Pettigrew, J. D., Nikara, T.,& Bishop, P. 0. Binocular interaction on single units in cat striate cortex: Simultaneous stimulation by single moving slit with receptive fields in correspondence. Experimental Brain Research. 1968, 6 , 391-410. Piaget, I. Piaget's theory. In P. H. Mussen (Ed.), Carmichael's manual of childpsychology. New York: Wiley, 1970. Pp. 703-732. Pigareva, 2.D. The role of specific impulses in the developmental chemistry of the microstructureof visual system in animals. Uspekhi Sovremennoi Biologii, 1975, 79, 48-63. (In Russian) Pirchio, M.. Spinelli, D., Fiorentini, A.. & Maffei, L. Infant contrast sensitivity evaluated by evoked potentials. Brain Research, 1978, 141, 179-184. Porac, C., & Coren, S. The dominant eye. Psychological Bulletin, 1976, 83, 880-897. Poppel, E., Held, R., & Frost, D. Residual visual function after brain wounds involving the central visual pathways in man. Nature (London), 1973, 243, 295-296. Poppel, E.,Von Cramon, D., & Backmund, H.Eccentricity-specificdissociation of visual functions in patients with lesions of the central visual pathways. Nature (London),1975, 256,489-490. Rapisardi, S. C., Chow, K.L.. & Mathers, L. H. Ontogenesis of receptive field characteristicsin the dorsal lateral geniculate nucleus of the rabbit. Experimental Brain Research, 1975, 22, 295305. Richards, W. The i@uence of oculomotor systems on visual perception. Final report (Contract F44620-67-C-0085). Massachusetts Institute of Technology, Cambridge, July 1969.
50
Juri Allik and Jaan Valsiner
Richards, W. Stereopsis.and s6reoblindness. Experimental Brain Research, 1970, 10,380-388. Richards, W. Visual processing in scotomata. Experimental Brain Research, 1973, 17, 333-347. Richards, W.. & Miller, J. F. Convergence as a cue to depth. Perception and Psychophysics, 1969, 5, 317-320, Rodieck. R. W. Quantitative analysis of cat retinal ganglion cell response to visual stimuli. Vision Research, 1965, 5, 583-601. Rose, L.. Yinon, U., & Belkin, M. Myopia induced in cats deprived of distance vision during development. Vision Research, 1974, 14, 1029-1032. Rosenfeld, A. Picture processing by computer. New York Academic Press, 1969. (Superceded by Rosenfeld, A.. & Kak. A. C. Digitaipictureprocessing. New York: Academic Ress, 1976.) Rytoff, S . M. An introduction to statistical radiophysics (Part I): Random processes; Moscow: Nauka, 1976. (In Russian) Salapatek, P., Bechtold, A. G., & Bushnell, E. W. Infant visual acuity as a function of viewing distance. Child Development, 1976, 41, 860-863. Schechter, P.B.,& Murphy, E. H.Brief monocular visual experience and kitten cortical binocularity. Brain Research, 1976, 109, 165-168. Sekuler. R. Spatial vision. Annual Review of Psychology, 1974, 24, 195-232. Shatz, C. A comparison of visual pathways in Boston and Midwestern Siamese cats. Journal of Comparative Neurology, 1977, 171,205-228. (a) Shatz, C. Abnormal interhemispheric connections in the visual system of Boston Siamese cats: A physiological study. Journal of Comparative Neurology, 1977, 171, 229-245. (b) Sherk, H., & Stryker, M.P. Quantitative study of cortical orientation selectivity in visually inexperienced kitten. Journal of Neurophysiology, 1976, 39,63-70. Sherman, S. M. Visual fEld defects in monocularly and binocularly deprived cats. Brain Research. 1973, 49,25-45. Sherman, S. M.,Guillery, R. W., Kaas,I. H.,& Sanderson. K. I. Behavioral, electrophysiological and morphological studies of binocular competition in the development of the geniculo-cortical pathways of cats. J o u r d of Comparative Neurology, 1974, 158, 1-18. Sherman, S. M.,Hoffmann. K. P., & Stone, J. Loss of a specific cell type from the dorsal lateral geniculate nucleus in visually deprived cats. Journal of Neurophysiology, 1972,35,532-541. Shevelyev. I. A. The plasticity of specialii detector properties in the neurons of visual cortex. In Sensory systems. Leningrad: Nauka, 1977. (In Russian) Shilagina, N. N.The formation of aversive conditioned reflex after visual deprivation in different age periods. Pavlov Journal of Higher Nervous Activity, 1974, 24, 728-734. (In Russian) Singer, W..& Tretter. F. Receptive-field properties and neuronal connectivity in striate and parastriate cortex of contour-deprived cats. Journal of Neurophysiology, 1976, 39,613-630. Slater, A. The development of binocular vision. Contribution to Symposium9: Perception in Infancy; International Congress of Psychology, Paris, 1976. Slater, A. M., & Findlay, J. M. The measurement of fixation position in the newborn baby. Journal of Experimenral Child Psychology. 1972, 14,349-364. Slater, A. M., & Findlay, J. M. The corneal-reflection technique and the visual preference method: Soulres of error. Journal of Experimental Child Psychology, 1975, 20,240-247. (a) Slater, A. M., & Findlay, J. M.Binocular fixation in the newborn baby. Journal of Experimental Child Psychology, 1975, 20, 248-273. (b) Slater, A., & Sykes, M.Newborn infant’s visual responses to square wave gratings. Child Development, 1977. 48, 545-554. Stone., J. A quantitative analysis of the distribution of ganglion cells in the cat’s retina. Journal of Comparative Neurology, 1965, 124, 333-352, Stryker. M. P.. & Sherk, H. Modification of cortical orientation selectivity in the cat by restricted visual experience: A reexamination. Science, 1975, 190, 904-905.
Visual Development in Ontogenesis
51
Tauber, E. S.,& Koffler, S. Optomotor response in human infant to apparent motion: Evidence of innateness. Science, 1966, 152, 382-383. Thomas, 1. P. Spatial resolution and spatial interaction. In E.C. Carterette & M. P.Friedman (Eds.), Handbook of perception (Vol. 5 ) : Seeing. New York: Academic Ress, 1975. Thorson, J., Lange, G. D., & Bilderman-Thorson, M. Objective measure of the dynamics of a visual movement illusion. Science, 1969, 164. 1087-1088. Timney, B. N., & Muir, D. W. Orientation anisotropy: Incidence and magnitude in Caucasian and Chinese subject. Science, 1976, 193, 699-701. Tretter, F.,Cynader, M., & Singer, W.Modification of direction selectivity of neurons in the visual cortex of kittens. Brain Research, 1975, 84, 143-149. Umezu, H.,Toni, S.,& Uemura, Y.Postoperative formation of visual perception in the early blind. Psychologia, 1975, 18, 171-186. Uzbekov, M. G. On the role of visual stimulation in the development of receptor properties of synoptosomes. Pavlov Journal of Higher Neurons Activity, 1976,26,1291-1295.(In Russian) Van Hof-Van Duin, J. Development of visuomotor behavior in normal and darkreared cats. Brain Research, 1976, 104,233-241. (a) Van Hof-Van Duin, J. Early and permanent effects of monocular deprivation on pattern discrimination and visuomotor behavior in cats. Brain Research, 1976, 111, 261-276. (b) Van Meeteren, A., & Vos, I. I. Applicabiliry of Fourier transfonnation upon contrast sensitivity functions. (RVO-TNO. Report No. 12F-1%8-20). Institute for Perception. Soesterberg, 1968. Van Sluyters, R. C., & Blakemore, C. Experimental creation of unusual neural properties in the visual cortex of kittens. Nature (London), 1973,246, 506-508. Vital-Durand, F., & Jeannerod, M. Role of visual experience in the development of optokinetic response in kittens. Experimental Brain Research, 1974, u),297-302. Volkmann, F. C.,& Dobson, M. V. Infant responses of ocular fixation to moving visual stimuli. Journal of Experimental Child Psychology, 1976,22, 86-99. Volokhov, A. A., & Pigareva, Z. D. Neurophysical and biochemical aspects of the development of visual system of rabbit in case of light deprivation. Pavlov Journal of Higher Nervous Activity, 1975,25, 799-807.(In Russian) von Hofsten, C. Binocular convergence as a determinant of reaching behavior in infancy. Perception, 1977, 6, 139-144. von Noorden, G. K. Experimental amblyopia in monkeys: Further behavioral observations and clinical correlations. Investigative Ophthalmology, 1973, 12, 721-726. (a) von Noorden, G. K. Histological studies of the visual system in monkeys with experimental amblyopia. Investigative Ophthalmology, 1973,12,727-738.(b) von Noorden, G. K., & Middleditch, P. R. Histology of monkey lateral geniculate nucleus after unilateral lid closure and experimental strabismus: Further observation. Invesrigative Ophthalmology, 1975, 14,674-683. Von Senden, M. R a m - und Gestaltauffassung bei operierren Blindgeborenen vor und nach der Operation. Leipzig: Barth, 1932. Westheimer, G. Visual acuity and spatial modulation thresholds. In D. Jameson & L. M. Hurvich (Eds.), Handbook of sensoryphysiology (Vol. 7,Part 4): Visualpsychophysics. Berlin and New York: Springer-Verlag, 1972. Westheimer, G. Fourier analysis of vision. Investigative Ophthalmology, 1973, 12, 86-87. Westheimer, G., & Mitchell, D. E. The sensory stimulus for disjunctive eye movement. Vision Research. 1969, 9, 749-755. White, B. L. Human infants: Experience and psychological development. New York Rentice-Hall, 1971. Wickelgren, L. W.Convergence in the human newborn. Journal of Experimental Child Psychology, 1967,5, 74-85.
52
Jiiri All& and Juan Valsiner
Wiesel, T. N.,& Hubel, D. H.Single-cell responses in striate cortex of kittens deprived of vision in one eye. Journal of Neurophysiology, 1963, 26, 1003-1017. Wiesel, T. N., & Hubel,D. H. Comparison of the effects of unilateral and bilateral eye closure on cortical unit responses in kittens. Journal of Neurophysiology, 1965, 28, 1029-1040. Wiesel, T.N., & Hubel,D. H. Ordered arrangement of orientation columns in monkeys lacking visual experience. Journal of Comparative Neurology, 1974. 158,307-318. Yinon, U. Eye rotation in developing kittens: The effect of ocular dominance and receptive field organization of cortical cells. Experimental Brain Research, 1975, 24, 215-218. Yinon, U. Age dependence of the effect of squint on cells in kitten’s visual cortex. Experimental Brain Research, 1976, 26, 151-157. Zaporozhets, A. V.. Venger, V. P.,Zintchenko, V. P.,& Ruzskaja, A. G . Perception and acrion. Moscow: hsveshtshenie, 1967. Zubek, J. P., & Bross, M. Depression and later enhancement of the critical flicker frequency during prolonged monocular deprivation. Science, 1972, 176, 1045-1047. Zuber, B. L., & Stark, L. Dynamic characteristicsof the fusional vergence eye-movement system. IEEE Transactions. System Science and Cybernetics, 1968, SSC-4, 72-79.
BINOCULAR VISION IN INFANTS: A REVIEW AND A THEORETICAL FRAMEWORK'
Richard N . Aslin and Susan T . Dumais? INDIANA UNIVERSITY
I . INTRODUCTION ......................................................
54
11. LEVELS OF BINOCULAR FUNCTION ................................... A . BIFOVEAL FIXATION ............................................. B. RTSION . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . c. STEREOPSIS ..................................................... D . SUMMARY . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
54 55 55
58 60
I11. DEVELOPMENTAL CONSTRAINTS ON BINOCULAR VISION . . . . . . . . . . . . . A. ACUITY AND CONTRAST SENSITIVITY ............................ B. ACCOMMODATION ............................................... C . FACIAL DIMENSIONS ............................................. D . SUMMARY .......................................................
63
IV . EMPIRICAL FINDINGS ON INFANT BINOCULAR VISION . . . . . . . . . . . . . . . . . A . MULTIPLE-CUE DEPTH DISCRIMINATION STUDIES . . . . . . . . . . . . . . . . . B . BIFOVEAL FIXATION STUDIES .................................... C. FUSION STUDIES ................................................. D . STEREOPSIS STUDIES ............................................
68 69 70 72 73
V . EARLY EXPERIENCE AND BINOCULAR FUNCTION ..................... A. THE ROLES OF EARLY EXPERIENCE ............................... B. BINOCULAR NEURAL MECHANISMS IN THE CAT .................. C . SENSITIVE PERIOD FOR HUMAN BINOCULAR FUNCHON ........... D . A MODEL OF HUMAN BINOCULAR DEVELOPMENT . . . . . . . . . . . . . . . .
79 79
VI . CONCLUDING REMARKS . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . REFERENCES
....................................................
62 62 66 67
81
83 84
90 90
'Preparation of this article was partially supported by grants from NSF (BNS-77-04580) and NICHD (HD-00309) to RNA . We gratefully acknowledge the helpful comments and criticisms provided by Martin Banks. Robert Fox. Conrad Mueller. Clark Presson. Sandra Shea. Linda Smith. and Davida Teller. *Present address: Bell Laboratories. Murmy Hill. New Jersey 07974.
53
.
ADVANCES IN CHILD DEVELOPMENT AND BEHAVIOR VOL . 15
Cqyight 01980 by Academic F'ress. Inc. All rights of reproduction in m y form rcsrved.
ISBN 012-009715-X
54
Richard N. Aslin and Susan T.Dumais
I. Introduction The study of how adults perceive the three-dimensional nature of the visual world has captured the interest of philosophers and psychologists for centuries (Boring, 1942; Pastore, 1971). Investigators studying the classic subject of adult spatial perception understand quite clearly that several types of visual information can specify the perception of object distance and depth, and that only a small proportion of that information is uniquely binocular (see Hochberg, 1971, and Kaufman, 1974, for general reviews). Surprisingly little study, however, has been made of the development of spatial perception, and even fewer attempts have been made to study binocular depth perception in young infants. Recently, several methodological and technical advances have enabled researchers to investigate systematically the visual capabilities of young infants, including binocular function. Despite these recent advances, empirical findings on the development of human binocular vision have been rare, and, as a result, theories concerning binocular development have been virtually nonexistent. The purpose of the present article is to provide a framework within which the empirical findings on binocular development can be organized. Moreover, we shall attempt to describe a rudimentary model to account for these data with the goal of suggesting directions for future empirical investigations.
11. Levels of Binocular Function In the past decade several researchers have attempted to study binocular depth perception in very young infants. In general, these studies have yielded inconclusive empirical findings. Moreover, the interpretation of these findings has often been made without a consistent guiding theoretical orientation. Much of the confusion and resulting controversy surrounding these studies of infant binocular vision centers on two factors: (1) the difficulty of operationalizing binocular abilities in nonverbal subjects, and (2) a basic misunderstanding of the different levels of binocular function. This misunderstanding has led several developmentalists to make inappropriate assumptions and inferences about infants’ binocular vision. A conceptual framework for the major levels of binocular function will now be discussed with the aim of clarifying the goals and conclusions that can be drawn on the basis of past and future empirical research. The levels of binocular function that appear to offer a simple yet complete categorization of binocularity were set forth by Worth (1915) in his clinical text on strabismus. Worth classified binocular function into three hierarchically related levels: (1) bifoveal fixation, (2) fusion, and (3) stereopsis. For example, Worth believed that in normal adults the presence of bifoveal fixation is a necessary prerequisite for fusion and stereopsis. However, Worth was well aware
Binocular Vision in Infants
55
of the fact that bifoveal fixation is not a suficient condition for functional fusion or stereopsis abilities. Moreover, Worth's proposal that these three levels are hierarchically organized is strictly true only for normal adults. As we shall see later, this necessary but not sufficient hierarchy may be violated in the develop ing visual system. Nevertheless, tests of these three levels of binocular function are useful in characterizing both the developmental and the pathological state of the binocular visual system. We shall now consider each of these three levels of binocular function in some detail in an effort to describe the mechanisms underlying their development. A. BIFOVEAL FIXATION
The retinal locus of highest spatial resolving power (best acuity) is the fovea, a region of approximately 1-2", which in adults is coincident with the line of sight. Normal adults who fail to align the two foveas so that they are simultaneously directed toward a single object of regard typically perceive double images. Moreover, inaccurate bifoveal fixation results in a degradation in stereopsis (see Ogle, 1962, for a general review). Thus, it is of some importance to determine whether infants typically exhibit bifoveal fixation when presented with a visual target. Clearly, if one documented the presence of bifoveal fixation in infants, then only one of the criteria necessary for adult-like binocular vision would have been satisfied. If, however, one documented the absence of bifoveal fixation in infants, then, according to a hierarchical model of binocular function, fusion and stereopsis could not occur. Alternatively, it is possible that in the infant visual system, precise bifoveal fixation is not required for fusion and stereopsis. As we shall see, even this lowest level of binocular function, bifoveal fixation, has not as yet been satisfactorily described. B. FUSION
The second level of binocular function is fusion, or the combining of two retinal images into a single phenomenal percept. When viewing a single small object in space (see Fig. I ) , each eye receives stimulation on a particular retinal locus. If one considers only a single eye, the object of regard lies along a particular direction line (F,F in Fig. 1 for the left eye). If the object is moved to any other point along that direction line (i-e., at a different distance from the eye), the object's perceived direction remains invariant with respect to the single viewing eye. Since the two eyes are separated by approximately 6 cm, the direction line for an object is quite different for the opposite eye (F,F in Fig. 1 for the right eye). Under binocular viewing conditions, the conflict between the two direction lines is eliminated in the visual system of adults by a compromise directional judgment (e.g., CF in Fig. 1). This compromise judgment of the two
56
Richard N . Aslin and Susan T . Dwnais F
Fig. I . Illustration of the two direction lines, FLF and FRF , for the two eyes, and an example of the combination of direction lines, CF,occurring during jksion.
retinal direction lines is accompanied by the subjective experience of a single object located at a particular position in three-dimensional space (Sheedy & Fry, 1979). Thus, the stimulation of two retinal loci can resuIt in a single or fused percept of an object in space, a percept which is in fact veridical. One potential explanation of the fusion mechanism is to propose the existence of retinal loci in the two eyes that are paired at some level of the visual system (Hering, 1868A977). In other words, stimulation of either or both members of the pair results in the registration of a single rather than a dual direction line. The theory that particular loci on the two retinal surfaces are paired is called the theory of corresponding retinal points. Perhaps the strongest evidence for the existence of corresponding retinal points is the phenomenon of peripheral fusion and the specification of the horopter (see Shipley & Rawlings, 1970, for an historical review). Fusion is not limited to those objects viewed by the two foveas. If an observer maintains bifoveal fixation on a target, fusion can occur also for objects presented in the peripheral visual field. However, peripheral fusion is limited to objects located at a particular distance from an observer. These locations constitute a surface called the horoptel3 that passes through the point of bifoveal fixation (see Fig. 2). Any object located in front of or behind the horopter does T h e concept of a horopter is considerably more complex than what we have described. There are at least three types of psychophysicalcriteria for empirically determining the location of the horopter (1) judging equivalent visual directions (nonius), (2) judging equivalent visual distances (apparent frontoparallel plane), and (3) judging the midpoint of the region of fusion. Although each of these three criteria results in a slightly different form of the horopter, all three assume a common underlying mechanism based on the theory of corresponding retinal points. Since the fusion criterion is the one most directly relevant to our presentation, we chose to bypass a more detailed discussion of the other two criteria for determining the horopkr.
Binocular Vision in Infants
57
not stimulate corresponding retinal points and is therefore not fused. Stimulation of noncorresponding retinal points results in the perception of double images (diplopia). Although the foregoing description implies that the horopter is a very thin surface, there is in fact quite a large region surrounding the hypothetical horopter within which diplopia is not present. Figure 2 shows this region of single vision surrounding the horopter, a region called Panum’s fusion area. The functional significance of Panum’s fusion area becomes clear when one considers that the limit of spatial resolution (vernier acuity) is approximately 2-10 seconds of arc (Riggs, 1965) while the microsaccade and drift eye movements present in experienced adult observers who are fixating a very small target are typically in the 10-30 minutes of arc range (Nachmias, 1959). Thus, if the horopter itself defined the locus of fusion, then fusion would be very intermittent and of extremely short duration, given the comparatively large eye movements present during “steady” fixation. The extent of Panum’s fusion area (10-15 minutes of arc in central vision) maintains the phenomenal identity of objects in space despite the continual fluctuations in the position of the two retinas during binocular fmation. In addition, as shown in Fig. 2, the extent of Panum’s fusion area increases with increasing retinal eccentricity (more peripheral to the foveas). Although this broadening is at least partially the result of the decline in acuity with increasing eccentricity, it is also partially the result of a peripheral deficit in disparity resolution. However, regardless of its underlying mechanisms, the fact remains that fusion prevents the confusion (and diplopia) that would result if dual direction lines were not combined at some level of the visual system.
Fig. 2 . Representation of the horopter, the locus of corresponding retinal points, and Panum’s fusion area (the region of single vision surrounding the horopter). The subject isfmting point F with both foveas. Point P projects onto noncorresponding retinal points, creating retinal disparity. Retinal disparity, the angular measure of noncorrespondence. equals 6 , minus 8,.
58
Richard N . Aslin and Susan T . Dumais
c.
STEREOPSIS
The final level of binocular function is stereopsis-the ability to a p p i a t e depth (or relative object distance) based on retinal disparity. Retinal disparity refers to the magnitude of mismatch between corresponding retinal points stimulated by an object located off the horopter. The discovery that slight differences in the input to the two eyes could result in the perception of depth was made by Wheatstone (1838). A very simple case of stereoscopic depth is shown in Fig. 3. Both eyes view an identical surrounding figure (the rectangle) to maintain a constant fixation distance and, in addition, each eye separately views a vertical bar. In this dichoptic viewing situation the angular distance separating the two vertical bars is a measure of retinal disparity. If the dichoptic targets stimulate the two temporal retinas, the retinal disparity is referred to as crossed and the target is perceived in front of the horopter. If the dichoptic targets stimulate the two nasal retinas, then the disparity is uncrossed and the target is perceived behind the horopter. The presence of retinal disparity for an object within Panum’s fusion area will result in a depth percept accompanied by fusion, a situation referred to as patent stereopsis. If the amount of retinal disparity exceeds the extent of Panum’s fusion area, however, a depth judgment can still be made, but diplopia is present and patent stereopsis is absent (Blakemore, 1970). These
\
1111
Object Array L
Polaroid Filters
Right
Retinal Array
-m
Rawltant Percept
m
-
Fig. 3. Stimulus arrangement which presents slighily different information to the two eyes (dichopric viewing) and results in the perception of relative depth.
Binocular Vision in Infants
59
I
Region of Diplopia
Region of Potent Stereopsis
L
1’
I \
\
\
11
Region of Diplopio
Fig. 4 . Representation of an observerjkating a point in space and the resulting specifEation of the horopter, Panwn’sfusion area, the region of patent stereopsis. and the region of diplopia.
relationships between fusion, patent stereopsis, and gross (or diplopic) stereopsis are depicted in Fig. 4.4 Displays such as the one depicted in Fig. 3 are used to test for local stereopsis, i.e., stereopsis created by extended contours. Despite the simplicity and reliability of these stereoscopic displays, they suffer from one major drawback. An observer viewing such a display can detect the presence of retinal disparity by rapidly alternating fixation between the two eyes. When this alternation is performed, the observer will notice a shift in the location of the vertical bar relative to the fixed rectangular surround. Since this shift does not require simultaneous binocular fxation, it provides an obvious monocular cue to depth. Fortunately, most observers (unless trained) cannot correctly differentiate between crossed and uncrossed disparity using this monocular cue. However, in many *A simplification in the relationship between h u m ’ s fusion area and the region of patent stereop sis has been made in Fig. 4. Although under most conditions these two regions are coincident, one CM extend the region of patent stereopsisslightly beyond Panum’sfusion area if the amount of retinal dispnrity in the stereoscopic display is gradually increased (see Ogle, 1962). The mechanism that allows the normal adult visual system to fuse stereoscopic displays that contain relatively large amounts of retinal disparity is unknown and, fortunately, not germane to the basic relationships depicted in Fig. 4.
60
Richard N . Aslin and Susan T . Dwnais
psychophysical tasks designed to measure an observer’s disparity detection threshold (stereoacuity), the observer is required to indicate only whether the target is in the plane of the surrounding figure. Similarly, in clinical assessments of stereoacuity, the patient is typically required to pick from an array of targets the “one that looks different.” Obviously, displays that utilize a lateral displacement of the dichoptic target are subject to the criticism that monocular information mediated the observer’s “depth” judgments. A more complex stereoscopic display that does not contain monocular cues to depth is the random-element stereogram (Julesz, 1971). As shown in Fig. 5 , a random-element stereogram consists of an array of several hundred small, square-shaped elements that are viewed dichoptically so that each eye receives a separate random-element array. Both random-element arrays are identical except for a small region of one array that is offset with respect to the other array, thereby creating retinal disparity. This display differs from other stereograms in that no single element of the display creates or is sufficient to create retinal disparity. Rather, retinal disparity is defined by the region of elements that is displaced, and the resultant perception of stereoscopic depth is based on global disparity processing. Although the random-element stereogram provides an unambiguous measure of the presence of stereopsis, it has had limited application in the assessment of stereoacuity. For normal adults tested with displays containing contours (e.g., Fig. 3), stereoacuity values are typically in the range of 2-10 seconds of arc, a value comparable to that of vernier acuity (Berry, 1948). Stereoacuity values for random-element stereograms have not as yet been obtained because small random-element offsets are difficult to produce. Although several researchers have suggested that global stereoacuity is much poorer than local stereoacuity, this suggestion awaits a systematic empirical test. D. SUMMARY
The three levels of binocular function proposed by Worth provide a useful categorization scheme for assessing the development of binocular depth perception. The most important levels of binocular function, at least in terms of perceptual experience of the visual world, are fusion and stereopsis. Clearly, the absence of either level would result in a visual world for the infant quite different from that of the normal adult. Unfortunately, the study of fusion and stereopsis has been fraught with extremely difficult methodological problems. As a result, the level of bifoveal fixation has been addressed most often in empirical studies of binocular function in infants. It should be emphasized again, however, that the presence of bifoveal fixation in infants does not guarantee that fusion and stereopsis are present. Finally, it must be pointed out that the absence of bifoveal fixation in infants does not necessarily eliminate the possibility of fusion or stereopsis. For exam-
Binocular Vision in Infants
61
Fig. 5. Schematic of the techniquefor generating stereopsis in a random-element display. The top panel illustrates rhe appearance of the display when viewed monocularly. The middle panels depict the horizontal displacement of a region in the two dichoptic displays which creates retinal dispariry. The bottom punel represents the appearance of the stereoscopic display to a normal adult observer. Note that the middle and bottom panels do not show all the random elements contained in the actual display, since these background elements would prevent a clear illustration of retinal disparity and depth.
ple, if Panum’s fusion area were very large during infancy, the accuracy of bifoveal fixation would be less critical than it is for normal adults. Similarly, stereopsis can occur under certain circumstances without the presence of fusion. Therefore, each level of binocular function must be investigated separately, yet in the context of the three interrelated levels, in order to understand the mechanisms underlying binocular depth perception during infancy. Although it is
Richard N. Aslin and Susan T.Dmais
62
possible that the three levels of binocular function are hierarchically related and unfold developmentally in an invariant sequence, the possibility also exists that the three functions develop in parallel within a system of mutual constraints rather than a simple causal hierarchy.
111. Developmental Constraints on Binocular Vision A consideration of the mechanisms underlying the development of binocular function should not be attempted without considering the concurrent develop ment of other visual mechanisms that may influence the quality of binocular function. Few of these constraints have been systematically investigated in relation to binocular development, but they cannot be overlooked in explaining the status of a particular binocular function. The major constraints on binocular function are (1) acuity and contrast sensitivity, (2) accommodation, and (3) facial dimensions. Each of these will now be discussed with the goal of preventing unwarranted or premature theories of binocular development-theories that ignore the interrelationships among the complex subsystems involved in normal adult binocular vision. A.
ACUITY AND CONTRAST SENSITIVITY
The most obvious constraint placed upon the processing of binocular information is the availability of two monocular images of sufficient quality (size and contrast) to allow binocular information to be extracted. If the visual targets were too small (below acuity threshold) or of insufficient contrast (below contrast sensitivity threshold), then any observed binocular deficit would not necessarily imply the absence of some binocular function. Most researchers have been aware of the acuity constraint, but few have considered the possibility of degradations in image quality resulting from low target contrast (ratio of target luminance to background luminance). In normal adults, low target contrast results in poorer spatial resolution, which in turn (1) reduces the information available for accurate bifoveal fixation, (2) diminishes the stimulus for disparity, and (3) increases the area within which fusion is operative. Recent studies of acuity and contrast sensitivity in infants (Atkinson, Braddick, & Moar, 1977; Banks & Salapatek, 1978; Marg, Freeman, Peltzman, & Goldstein, 1976; see Dobson & Teller, 1978, for a general review) indicate that at maximal contrast (9096or greater), acuity thresholds improve from approximately 25 to 5 minutes of arc (20/500 to 20/100) during the first 6 months of life. Moreover, maximum contrast sensitivity shows a twofold increase between 1 and 3 months of age. Consequently, close attention must be directed to the monocular image quality of targets used in testing binocular vision in infants to ensure that acuity and contrast sensitivity thresholds are exceeded. A second issue related to monocular image quality is the balance of acuity in
Binocular Vision in Infants
63
the two eyes. For at least two reasons, there may be differences in the quality of information processed from the two retinas. First, differential refractive error (anisometropia) leads to differences in image sharpness. This differential error can be eliminated by placement of appropriate lenses before one or both eyes. Unfortunately, this is not typically done in studies of infant binocular vision. Second, differential acuity of a nonoptical origin (amblyopia) can also produce a binocular imbalance. Amblyopia is a common result of periods of constant eye misalignment or anisometropia (Duke-Elder & Wybar, 1973). Amblyopia by definition cannot be overcome by a simple optical correction and is also not typically assessed in studies of infant binocular vision (see Thomas, Mohindra, & Held, 1979, for a recent exception). The presence of differential acuity reduces stereoacuity in adults (Matsubayashi, 1938) and therefore is of serious concern for the accurate assessment of infant binocular function. Although norms on the incidence of anisometropia or amblyopia have not yet been obtained for young infants, the rapid development of the visual system in the early postnatal months suggests that such anomalies are likely to occur. Both anomalies could mask the presence of good binocular function in young infants. A final issue relevant to monocular image quality is the anatomical development of the fovea during the early postnatal period. Mann (1964) has shown that the configuration of retinal layers characteristic of the adult fovea is not typically present until 4 months postnatally. Recent evidence from infant monkeys (Hendrickson & Kupfer, 1976) also documents a significant development in foveal anatomy during the early postnatal period. The implication of these anatomical findings is that any functional advantage gained by retinal receptors in the foveal area as a result of diminished image interference from other retinal cell layers may be absent in very young infants. Whether these anatomical developments per se improve acuity is not known at the present time. However, it seems likely that the developing anatomy of the retinal cell layers acts to constrain the quality of the retinal image and in turn may degrade the control of bifoveal fixation. B. ACCOMMODATION
1 . Accommodation and Acuity The second major constraint placed upon the integrity of binocular function is ocular accommodation, or the ability of the lens in each eye to change curvature so as to optimize the focus of the retinal image. In adults, failure to accommodate appropriately to targets presented at various distances results in a loss of acuity and contrast sensitivity (Green & Campbell, 1965). Hence, it is possible that while the potential for good acuity is present in the infant visual system, a motor control deficiency (inability to accommodate) prevents the retina from receiving an optimal retinal image. Inaccurate accommodation, because it degrades acuity, may result in the same types of degradation in binocular function discussed in Section II1,A.
64
Richard N . A s h and Susan T.Dumais
Until recently the only systematic study of accommodation in young infants was that of Haynes, White, and Held (1965). They employed dynamic retinoscopy to measure the infant’s far point (plane of fixation) as a target was presented at various distances. Their results indicated that infants do not begin to accommodate differentially to variations in target distance until 2 months of age and that adult-like accommodation, in which target focus is nearly optimized for all target distances, does not occur until approximately 4 months of age. A potential confounding factor in the study of Haynes et al. (1965) concerns the target stimulus used to elicit changes in accommodation. In the study of Haynes et al. (1965) a 3-in.-diameter bulls-eye pattern was attached to the retinoscope for use in attracting the infant’s fixation. Although this target may have been sufficient in size and contrast to engage the accommodative system at near distances, the target’s overall retinal size decreased as the target was moved away from the infant and the concentric target rings may have dropped below the younger infant’s acuity threshold. Therefore, the finding that young infants show little change in accommodation and a relatively fixed focal plane at a near distance may have been an artifact of the small size of the stimulus. Banks (1980) replicated and extended the study of Haynes et al. (1965) using a large (30”) checkerboard pattern that was altered to maintain a constant retinal size at all target viewing distances. He found that 1-month-olds show evidence of partial accommodation and 2-month-olds show a nearly adult-like accommodation response. Braddick, Atkinson, French, and Howland (1979), using a different measurement procedure, have reported quite similar results. Consequently, although the general conclusion reached by Haynes et al. (1965) was correct, they somewhat overestimated the age at which the accommodation system becomes operative. These studies of infant accommodation demonstrate that until at least 2 months of age, infants do not consistently receive a clear retinal image of targets presented at various distances. For normal adults, this failure of accommodation would create a retinal image that was nearly always out of focus (except at the fixed focal plane of 15-25 cm), and a resultant degradation in acuity and contrast sensitivity. Although this pattern of results is applicable to the normal adult visual system, it does not appear to hold for the visual system of young infants. Green and Campbell (1965) have shown that in adults the proportional loss in spatial sensitivity resulting from defocus is not equivalent at different spatial freq~encies.~ In other words, if the visual system is capable of resolving very small elements (as in adults), then slight errors in image focus lead to significant losses in spatial resolution. But if the visual system is capable of resolving only %patial frequency refers to the number of repetitive light-dark stripes per unit of visual angle. For example, a pattern containing 30 black and 30 white bars in an area one visual degree wide has a spatial frequency of 30 cycleddegree. The highest spatial frequency stimulus which can be reliably detected by an observer is an estimate of acuity.
Binocular Vision in Infants
65
larger elements (as in infants), then image focus is less critical and results in little or no loss in spatial resolution. Salapatek, Bechtold, and Bushnell (1976), who assumed that little or no accommodation occurs in 1- and 2-month-old infants, showed that infants in this age range do not exhibit different acuity thresholds at different target viewing distances. This finding is consistent with the argument of Banks ( 1 980) that image focus is relatively unimportant to the spatial resolution of targets by infants under 2 months of age. The general conclusion to be reached from these studies is that measures of binocular function should employ targets that are well above the acuity and contrast sensitivity thresholds of infants, and that further losses of acuity and contrast sensitivity may occur in infants older than 2 months if the accommodative constraints on these abilities are not taken into account.
2. Accommodation and Convergence Another accommodative constraint on binocular function is the interaction between the accommodation and convergence systems. In normal adults, a synergistic link exists between changes in accommodation and changes in convergence (Muller, 1826/1943). As a target approaches a subject, the lens in each eye alters shape to maintain optimal image focus, and the angle formed by the two lines of sight (convergence angle) increases to maintain bifoveal fixation (see Morgan, 1968, for a general review). This link between accommodation and convergence is most impressively demonstrated under monocular viewing conditions. If a target approaches while one eye is occluded, then the binocular information for convergence (the extrafoveal location of the target’s image in the occluded eye) is absent. Yet adults consistently converge the occluded eye under these monocular viewing conditions, indicating that the accommodative change in the unoccluded eye is sufficient to activate an appropriate change in convergence. Anomalies in the accommodation-convergence relationship can lead to difficulties in maintaining bifoveal fixation under binocular viewing conditions (Duke-Elder & Wybar, 1973). If a young child is grossly hyperopic (farsighted), then the accommodation system is engaged even when the target is located at far distances. As the target approaches, the accommodation system saturates before the target reaches a near distance. Further approach by the target requires a further change in convergence to maintain bifoveal fixation, even though the target’s image begins to blur because accommodation is at a maximum. For some children, however, the strong link between accommodation and convergence induces a further change in convergence as more accommodative effort is exerted in an attempt to focus on the near target. As a result of this overacting accommodative-convergence, there is a breakdown of bifoveal fixation and a loss of fusion. Although the foregoing situation (accommodativeesotropia) is not common, there will be an imbalance between the accommodation-convergence link whenever an optical (refractive) error remains uncorrected. Since infants are
66
Richard N. Aslin and Susan T.Dumais
rarely corrected for refractive errors prior to binocular testing, the accommodation-convergenceimbalance may create some difficulty in maintaining consistent bifoveal fixation and therefore bias the assessment of binocular function toward obtaining negative findings. One final issue relevant to the accommodation-convergence relationship is whether the synergistic link is present at birth, is acquired maturationally according to a genetic program, or is acquired as the result of early visual experience. To date, the only study that has provided data on the development of the accommodation-convergence link is the report by Adin and Jackson (1979). They demonstrated that accommodative-convergence, as measured under monocular viewing conditions, is present in infants as young as 2 months of age. However, the quantitative aspects of the accommodation-convergence link, in the absence of a dynamic recording technique, could not be determined. Obviously, the link must not be totally determined by early experience; if it were, any relationship between the two systems would be adapted to and conflicts would not occur. On the other hand, however, the link may not be totally determined by genetic factors since only gross refractive errors appear to lead to easily observable difficulties in converging appropriately. Clearly, the development of the accommodation-convergence relationship demands careful study in the near future. C. FACIAL DIMENSIONS
The last constraint to be considered is the configuration of the two orbits and related musculature. Although facial dimensions have not been discussed in the past as a possible reason for failures of binocular vision, two facial dimensionsare quite relevant to bifoveal fixation and stereopsis: orbital position and interocular separation. The position of the two orbits changes drastically during prenatal and early postnatal development. Zimmerman, Armstrong, and Scammon (1929) have shown that the orbits shift from a lateral to a frontal skull position during embryonic development. This shift is greatest during the prenatal period, but a significant postnatal shift also occurs (see Fig. 6). Therefore, a greater amount of rotation from a central orbital position is required for bifoveal fixation to occur in infants than in adults, and this additional requirement may prevent (or constrain) the convergence system from maintaining accurate bifoveal fixation to targets at all viewing distances during the early postnatal months. Zimmerman et al. (1929) also documented the large increase in interocular separation that occurs during fetal development. More recently, Krieg (1978) extended those findings by taking analogous measurements in infants between birth and 4 months of age. These two studies, plus additional normative data from adults, provide consistent evidence for a rapid increase in interocular sep-
Binocular Vision in Infants
\
Tha optlc ox-
3
4
5
6
7
67
ot vorious periods d dewelopmml
8
9
10 BIRTH I
2
3
AGE (MONTHS) Fig. 6. Normative anatomical data on the angular separationof the optic axes during the prenatal
and early postnatal periods. Adaptedfrom Zimmerman, Armstrong, & Scammon. The Anatomical Record, 1929, 59, 119.
aration during prenatal development followed by an additional 50% increase between birth and adulthood. The importance of interocular separation for binocular function centers on the magnitude of retinal disparity. As shown in Fig. 7,the retinal disparity present in a display is inversely related to target distance and directly related to interocular separation. The 50% increase in interocular separation during postnatal development accounts for a 50% increase in disparity for an identical stereoscopic display, which means that a stereoscopic display containing retinal disparity that is just detectable by adults may be below an infant’s disparity detection threshold. Therefore, consideration of differences in interocular separation is crucial for the accurate assessment of infant stereopsis. D. SUMMARY
To conclude this section on developmental constraints, it should be clear that the size, contrast, viewing distance, and disparity of stimuli used to assess
binocular function must be taken into account when comparing the infant and adult visual systems. In addition, failures to demonstrate any given level of binocular function must be evaluated in light of other constraints, particularly those involving motor systems, to avoid possible underestimation of an infant’s
68
Richard N. A s h and Susan T.Dumais F
6 cm
L
I
Fig. 7. Illustration of the differences between a newborn (dashed) and an adult (solid)frxating point F with the foveas. Point P is an object that projects onto noncorresponding retinal points, thus creating retinal disparity. A measure of retinal disparity is the change in convergence angle needed to bring the two foveas onto point P.Retinal disparity in this figure equals a? minus atfor the adult and p1 minus PI for the newborn. The general formula for calculating retinal disparity is: 2 [arctan (IOSl2)lD minus arctan (IOSI2)lD D '1, where IOS = interocular separation.
+
binocular capability. In the literature review to follow, we shall see that conclusions reached in the past have rarely considered the constraints discussed in Section III.
IV. Empirical Findings on Infant Binocular Vision The study of depth perception in infants has involved four general lines of research. Three of these lines of research are closely related to the three levels of binocular function discussed in Section II. While the fourth line of research is not directly related to the specifically binocular aspects of depth perception, it represents the most extensive set of empirical findings on depth perception, and therefore deserves some attention in the following review. Our coverage of the literature on infant binocular function will begin with a very brief discussion of this fourth line of research, which we have called multiple-cue studies6 of infant Wur use. of the term multiple-cue refers to the fact that in many studies both mnwular cues to depth (shading, perspective, texture gradient, motion parallax, etc.) and binocular cues to depth (convergence, diplopia, disparity, etc.) are potentially available in the stimuli used to assess infant depth perception. Thus, it is often unclear which particular cue served either as the essential or sufficient condition for depth discrimination.
Binocular Vision in Infants
69
depth perception. We shall then focus on the three less frequently studied levels of binocular function during infancy. A. MULTIPLE-CUE DEPTH DISCRIMINATION STUDIES
The first studies of depth perception in infants utilized stimulus displays that contained many types of depth cues. For example, the early studies of differential reaching to objects presented at different distances (Cruikshank, 1941) and the early visual cliff studies (Walk & Gibson, 1961) did not present infants with purely binocular depth information. Monocular cues such as linear perspective, texture gradients, and motion parallax were confounded with binocular disparity information. In all fairness, however, these early studies were not designed to assess only binocular depth perception in infants, since at the time any evidence for early depth perception was considered quite remarkable. Partly as a result of the difficulty encountered by these pioneering researchers, more recent studies of depth perception in infants have also failed to separate monocular and binocular cues to depth. These studies have employed a variety of stimulus displays and dependent measures, including locomotor, manual, and affective indications of visual cliff avoidance (Scarr & Salapatek, 1970; Walters & Walk, 1974; Campos, Langer, & Krowitz, 1970); postural and affective indicators of avoidance to impending collision (Ball & Tmnick, 1971; Bower, Broughton, & Moore, 1971; Yonas, Bechtold, Frankel, Gordon, McRoberts, Norcia, & Sternfels, 1977); discriminative conditioning and habituation measures of size and shape constancy (Bower, 1964, 1965, 1966a, 1966b; Caron, Caron, & Carlson, 1978); and visual fixation and reaching preferences for three-dimensional compared to two-dimensional objects (Fantz, 1961, 1966; Bower, 1972; Dodwell, Muir, & DiFranco, 1976). With regard to the binocular aspects of depth perception, however, no consistent conclusions from these studies can be drawn. All of the results described in the studies listed can be accounted for by the infant’s processing of monocular cues to depth and/or other methodological artifacts. Furthermore, even the clear and consistent demonstration of a difference between the infant’s behavior under monocular versus binocular viewing conditions would not indicate which particular binocular cue was responsible for this differential performance. Information about the relative depth of objects can be specified by one or more of the following binocular cues: convergence angle, diplopia (double images), and retinal disparity. In line with our classification of binocular vision into three levels of binocular function, it is perhaps more instructive to examine in detail the development of each of these potential binocular functions than to discuss further the more global, multiplecue approach used most frequently in the past.
70
Richard N. Aslin and Susan T.Dumais B. BIFOVEAL FIXATION STUDIES
Our earlier discussion pointed out that in normal adults bifoveal fixation is a necessary but not sufficient condition for good binocular vision. Several investigators, operating under the assumption that bifoveal fixation is also important for infants' binocular vision, have attempted to measure the accuracy of binocular eye alignment in young infants. These studies of binocular eye alignment have employed corneal photography (see Haith, 1969, or Maurer, 1975b, for general reviews). The corneal photographic technique estimates the direction of gaze by a detailed measurement of the relationship between the pupil center and reflections on the cornea of fixed (and invisible to the infant) reference lights. Several studies (Wickelgren, 1967, 1969;Maurer, 1975a)have recorded the position of the two pupil centers in newborns and older infants who were presented with single visual targets. Both investigators reported that the pupil centers of young infants are generally divergent and typically straddle the location of the visual target. In add,ition,Maurer (1975a) reported that the degree of divergence of the pupil centers decreases during the first 2 to 3 months of life. Initially, these findings were taken as evidence that young infants do not have bifoveal fixation until some time after birth. There are, however, several problems with the corneal photographic technique that have cast serious doubt upon the conclusion of these original studies. Slater and Findlay (1972) pointed out that a line extending outward from the center of the pupil (optic axis) is not coincident with the line of sight, refmed to as the visual axis (line from target to fovea). They documented this optic axis-visual axis discrepancy (or angle alpha) in both adults and newborns and concluded that the angle alpha is greater in newborns than in adults (8-10" vs 4-5"). Therefore, the finding of divergence in newborns may be the simple result of an estimation error attributed to the corneal photographic technique. The corneal photographic technique is further complicated by the fact that there are wide individual differences in the angle alpha and potential differences between the two eyes within an individual. Therefore, the combination of a constant measurement error and a variable angle alpha error makes any statement about bifoveal fmation using targets presented at a single viewing distance quite ambiguous. For example, Slater and Findley (1975a) reported that after an average correction factor for the angle alpha was applied, newborns fixated within 2 1.5 in. of a vertical row of lights during 90% of the time period sampled. However, at the 10 in. viewing distance used in their study, 1.5 in. converts to 8 3 , a value several orders of magnitude greater than the accuracy needed to conclude that bifoveal fixation is or is not present. In fact there is no objective technique currently available that can measure binocular fixation with sufficient accuracy to conclude that bifoveal fixation is present. While these problems rule out the accurate assessment of bifoveal fixation by
Binocular Vision in Infants
71
attempting to specify the absolute location of the two visual axes, several measurement techniques (including corneal photography) have sufficient resolution to measure the relative position of the eyes when viewing a target at different distances from the observer. Following this rationale, Slater and Findlay (1975b) presented visual targets to newborns at three viewing distances (5,10, and 20 in.) and recorded relative changes in eye alignment using corneal photography. They found that all newborns tested changed the relative position of the eyes (pupil centers) when the 10 and 20 in. distances were compared but not when the 5 in. distance was compared to the other two distances. Although this study provides evidence that newborns change their lines of sight appropriately as a target is presented at different distances, it is not clear which area of the retina is used as the line of sight, nor is it clear why the nearest target distance was not fixated appropriately. Another approach to the study of changes in binocular eye alignment is actually to move the distance of the target and record changes in eye alignment (convergent and divergent eye movements). An initial study of vergence in infants was conducted by Ling (1942), who tested infants from birth to 6 months of age. She moved a 2-in.-diameter black disk through a distance of 3 to 36 in. from the infant at a rate of 2 inhecond. On the basis of film records (not corneal photography), she concluded that binocular fixation (i.e., appropriate vergence) does not appear until 7 to 8 weeks of age. In a more recent study, A s h (1977) used corneal photography to measure changes in binocular eye alignment in 1-, 2-, and 3-month-dds as a luminous crosshair target moved along the midline from 57 to 15 cm at either 12 or 22 cdsecond. Results indicated that even the 1-month-olds converged and diverged appropriately, but only the 2- and 3-month-olds converged and diverged an amount indicative of bifoveal fixation. In general, both the amount of vergence and the speed with which these movements are executed appear to increase dramatically in the f i t 3 months of life. However, it is important to exercise caution in interpreting the presence of appropriate convergent eye movements as evidence of bifoveal fixation. Infants may consistently use a particular extrafoveal retinal locus in each eye to define the line of sight. Several researchers (Bronson, 1974; Lewis, Maurer, & Kay, 1978) have seriously considered this alternative of a nonfoveal newborn, and unfortunately it cannot be ruled out at the present time. In summary, the data on bifoveal fixation indicate that rudimentary binocular fixation (i-e., a consistent line of sight in the two eyes) may be present at birth. With increasing age, the infant is better able to maintain consistent binocular fixation, particularly to rapidly moving stimuli, and to change convergence over a larger range of target distances. It seems clear, however, that much of the young infant’s early visual experience is composed of misaligned images. Whether the images are ever in exact register bifoveally is also unclear, since no
72
Richard N. Aslin and Susan T.Dumais
measurement technique used to date can unequivocally demonstrate bifoveal fixation. Nevertheless, it seems reasonable to conclude that by 3 months of age, infants are fixating targets with some area of the retina very close to the fovea and that together the two foveal areas are in fairly close alignment. C. FUSION STUDIES
The study of fusion is perhaps the most problematic of the three levels of binocular function because it involves a perceptual experience that is difficult to operationalize in preverbal infants. One technique that has been useful to the study of fusion in adults involves wedge prisms (Jampolsky, 1964; von Noorden & Maunamee, 1967). When an adult views a target with both foveas, introduction of a prism in front of one eye shifts the image of the target in that eye and creates diplopia. In normal adults, an eye movement is initiated to realign the two images and reattain fusion. The typical adult response during this prism test consists of a biphasic eye rotation including a saccadic and a convergent component. Usually, only the saccadic component is measured during the prism test. In some adults, however, the affected eye is being suppressed, so that no disparity is created by the prism and no realigning eye movement is present. To date, the only study that has collected data concerning the development of fusion in infancy is that reported by A s h (1977). In that study, binocular eye alignment was altered by placing a wedge prism in front of one eye in 3-, 4%-, and 6-month-olds. Three different wedge prisms were used: 0, 2.5, and 5". The 0" condition was used as a control for the presence of an eye movement associated with placement of any object in front of the eye. Each prism was introduced while the infant fmated the experimenter's face. Three-month-olds showed the saccadic refixation response only once among 120 trials. Four-andone-half-month-olds showed the refixation response on 2% of the 2.5" trials and 13% of the 5" trials. Six-month-olds refixated on 45 and 72% of 2.5 and 5" trials, respectively. These results indicate a marked improvement in performance on the prism test between 444 and 6 months of age. There are several reasons for infants not consistently showing refiation responses to the prism test until nearly 6 months of age. First, the stimulus for eliciting a refixation response on the prism test, i.e., diplopia, may be absent if the size of Panum's fusion area is large in early infancy. Hence, if the size of Panum's fusion area decreased during development, then the amount of prism displacement required to create diplopia would decline as the infant became older. This explanation is plausible but it demands further investigation. Second, young infants who do not respond appropriatelyon the prism test may experience diplopia but may fail to program an eye movement to re-fuse the target images. Third, infants may in fact realign their eyes by means of slow convergent eye movements, but, since the experimenter was scoring only the more easily ob-
Binocular Vision in Infants
13
servable saccadic refixation movements, the slow convergent movements may have been missed. Clearly, more detailed measurements are needed to ensure that undetected refixation eye movements did not occur in the younger infants. Finally, poor monocular acuity may limit the young infant’s ability to detect the misalignment of the contours in the fixation target, making refixation eye movements unnecessary for the elimination of diplopia. As monocular acuity improved in subsequent months, the tendency to refixate would increase correspondingly. Variations in the characteristics of the fixation target used during the prism test are clearly called for in future research since certain types of targets may create more salient diplopic stimuli than others. In summary, there are no conclusive data on the presence of fusion in infants. Although the prism test results could be interpreted as evidence in support of fusion, they may also be accounted for by explanations involving measurement error, oculomotor immaturity, or deficits in spatial resolution. The study of fusion in infants awaits the development of an objective technique for the unambiguous measurement of the perception of single and double images. D. STEREOPSIS STUDIES
Although studies of the development of bifoveal fixation and fusion are of great interest, the classic question in binocular visual development is whether infants are capable of stereoscopic depth perception (and, if so, what mechanisms control its development). However, stereopsis, like fusion, has been difficult to study. In fact, only in the last 5 years has the presence of stereopsis been conclusively demonstrated in 2- to 4-year-olds (Reinecke & Simons, 1974; Romano, Romano, & Puklin, 1975; Walraven, 1975). Stereopsis, as defined previously, refers to the appreciation of the relative distance of objects based solely on retinal disparity. Since the percept of depth is a subjective experience and does not unequivocally result from the preseiice of an object in depth, it has been difficult to find an appropriate dependent measure of stereopsis in infants. For example, even though infants may be able to detect disparity (or other binocular cues), the perception of an object in depth may be absent. Nevertheless, the demonstration that infants can detect differences in retinal disparity is important, since disparity detection is a necessary prerequisite for stereoscopic depth perception. Our review of the infant stereopsis literature considers two major approaches to the study of stereopsis: (1) the development of spatially appropriate behaviors and (2) the development of disparity detection. 1 . Spatially Appropriate Behaviors
One approach to the study of the development of binocular depth perception in infants is to record the presence of spatially specific responses such as reaching or avoidance. Typically, studies of this type have employed a stereoscopic
14
Richard N. Aslin and Susan T . Dwnais
shadow-casting device to present disparate stimuli to the two eyes. The shadowcasting technique uses two horizontally separated point sources of light to cast the double shadow of an object onto a rear projection screen. By placing different chromatic or Polaroid filters in front of the two point sources and corresponding filters in front of the subject’s two eyes, it is possible to isolate each of the two double images of the stimulus and create a dichoptic viewing situation. The apparent distance of the fused images (for adult viewers) is proportional to the lateral separation of the stimulus images on the screen. If the left eye views the right image and the right eye the left image, then the stimulus object appears to be located in front of the screen. Conversely, if the left eye views the left image and the right eye views the right image, then the object appears in back of the plane of the screen. Thus, creation of a “virtual” object is based upon the extraction of binocular information for relative depth. Bower (1971, 1972) and Bower, Broughton, and Moore (1970) have reported that infants as young as 7 days of age reach appropriately to the location of a virtual object and become upset by the absence of tactual feedback from their intended reaching behavior. Unfortunately, both Dodwell, Muir,and DiFranco (1976) and Ruff and Hulton (1977) have failed to find evidence of either h s t r a tion or directed reaching in neonates under experimental conditions very similar to those reported by Bower and his colleagues (see also Bower, Dunkeld, & Wishart, 1979, and Dodwell, Muir, & DiFranco, 1979). In fact, the previously accepted norms on the development of reaching in infants (Gesell, Thompson, & Amatruda, 1934; White, Castle, & Held, 1964) report no directed (intentional) reaching toward real objects until 4 months of age. Furthermore, Gordon and Yonas (1976) have correctly noted that both binocular rivalry, which may result if the two stimulus images cannot be fused, and the conflict between accommodation and convergence, resulting from the large image separations used in the Bower studies, could account for the infant’s agitated behavior. Therefore, evidence from the reaching behavior of neonates that stereoscopic depth perception is present at birth must be seriously questioned. While the reaching behavior of neonates may be of questionable validity, the reaching behavior of older infants may provide evidence of appropriate target localization (cf. Bechtoldt & Hutz, 1979 and Gordon & Yonas, 1976). Gordon and Yonas (1976), however, found that 5- and 6-month-olds’ reaches were directed to approximately the same location in space regardless of the separation of the two stimulus images on the screen (and thus the presumed distance of the virtual object). This finding is difficult to interpret since even in their real object condition, reaches were often inaccurate and contact with the real object was often fortuitous. Three other measures (position of the infant’s head, number of reaches, and number of prehensile behaviors) did, however, vary with the apparent location of the virtual object. A follow-up study by Yonas, Oberg, and Norcia (1978) employed a virtual object display in which the separation of the two stimulus images increased rapidly during a trial, thus simulating the ap-
Binocular Vision in Infants
75
proach of the object on a collision course with the infant's face. Twenty-weekolds showed more attentive furation, more reaching, more head withdrawal, and more blinking on these virtual object looming trials than on trials in which dichoptic viewing conditions were eliminated (by removing the filters from in front of the light sources). These results suggest that some aspect of the display that is present only under binocular viewing conditions mediates these behaviors. However, the specific type of binocular information mediating these behaviors remains unclear. For example, all studies that have used the shadow-casting technique appear to assume that binocular parallax (disparity) is responsible for depth-related behaviors in infants. However, one must recall that disparity is defined as the stimulation of noncorresponding retinal points by the same object (or part of an object). In the shadow-casting technique used in past studies, there are no contours on the display screen (except the outline of the screen's frame) to lock convergence onto the plane of the screen. Consequently, infants may simply maintain bifoveal fiation on the two stimulus images rather than bifoveally fiiating the screen plane. Although this cross convergence situation (left fovea fixating right image and right fovea fixating left image) maintains fusion, it does not result in retinal disparity. Therefore, infants may be relying on convergence angle as a cue to depth in studies employing the shadow-casting device. von Hofsten (1977)has provided some evidence that convergence angle may mediate distance-appropriate reaching in infants. He placed wedge prisms in front of both eyes, thereby altering the angle of convergence for infants viewing an object. Infants from 18 to 32 weeks of age provided some evidence of reaching for the virtual location of the object. Therefore, convergence, as well as other nonstereoscopic cues (binocular rivalry, alternation of fixation between the two eyes, diplopia) may be responsible for the differential behavior of infants presented with virtual objects. In summary, the studies that have employed spatially appropriate behaviors as an index of binocular depth perception suffer from three major difficulties. First, the frequency of reaching in neonates is low, suggesting that reaching is not a reliable measure of depth perception. Second, although reaching and avoidance behaviors are reliably present in older infants, the specific forms of these responses lack a consistent relationship to object distance. Third, the shadowcasting technique used to present binocular displays to infants provides cues other than retinal disparity. Thus, responses other than reaching and avoidance and displays other than the shadow-caster are needed to assess infant stereopsis more accurately. 2 . Detection of Disparity Another approach to the study of binocular depth perception in young infants is to determine whether differences in disparity can be detected. One method for assessing disparity detection is the habituation-dishabituation procedure. Bower
16
Richard N. Adin and Susan T . Dumais
(1968), in a very sparsely documented report, suggests that infants show a decline in fixation duration (habituation) over repeated trials of a stereoscopic display and recovery of fixation (dishabituation) upon a subsequent change to a nonstereoscopic display. Without further details on his procedures, however, Bower’s results are only suggestions. A more systematic study of disparity detection using the habituationdishabituation procedure has been reported by Appel and Campos (1977). They measured habituation of three indexes (heart rate, skin potential, and sucking rate) and subsequent dishabituation when a stereoscopic display was shifted to a nonstereoscopic display (or vice versa). A two-dimensional form (rabbit) composed of two images, each viewed separately by the two eyes (with polaroid goggles), was presented to 8-week-olds. The shift from the nonstereoscopic to the stereoscopic display was reliably discriminated, but the shift from stereoscopic to nonstereoscopic was not. Appel and Campos (1977) argued that a shift from a depth to a planar display must have been less salient than a shift from a planar to a depth display. Although these results suggest that young infants can detect some changes in disparity, the use of pictorial forms in their stereoscopic display is subject to a criticism similar to that raised in the case of the shadowcasting studies: that infants may detect a monocular cue (the relative position of the two stimulus images, an effect easily seen if one alternates fixation between the two eyes) or a binocular cue (rivalry, diplopia) not indicative of a depth percept. Consequently, use of the stimulus display employed in the Appel and Campos (1977) study leaves unclear whether infants actually detected differences in disparity. A stimulus display perfected by Julesz (1960, 1971) offers a more unambiguous method for the assessment of disparity detection in young infants. This stimulus display, a random-element stereogram (see Fig. 5 ) , is composed of hundreds of small square-shaped elements randomly arranged across a wide stimulus field. Under monocular viewing conditions, the random-element display appears to be devoid of any coherent contours. However, it is possible to displace a region of the display under dichoptic viewing conditions and thereby create retinal disparity. The primary advantage of the random-element display is that it effectively eliminates any monocular cue present in displays that have extended contours. The disparity present in a random-element display is defined with respect to a region of elements rather than with respect to a simple contour displacement. Of course, one could argue that any demonstration of detection of disparity in random-element displays by infants provides evidence only of the processing of a proximal cue to depth and does not provide conclusive evidence for the presence of a depth percept. However, strong evidence for infants’ detection of disparity would provide useful information concerning whether stereopsis is possible in young infants. To date there are only three studies that have employed random-dot stereo-
Binocular Vision in Infants
77
grams to assess binocular function in young infants. Bower (1968),again in a very poorly detailed report, stated that when presented with a random-element display containing no form “the infant will frantically scan over the field” (p. 197). However, he stated that if the display contained a stereoscopic form, a majority of infants “will orient to the form with no rapid jumping at all” (p. 197). Very little detail was provided as to the infants’ ages or the method used to measure eye position, thus making this report very difficult to evaluate critically. Atkinson and Braddick (1976) have used both fixation preference and a habituation-dishabitation measure (high-amplitude sucking) to study disparity detection in four 2-month-olds. In the fixation preference procedure, a pair of random-dot displays (22” square) was presented side by side, separated by 11”. Pairings consisted of one stereoscopicdisplay (disparity = 26 minutes of arc) and one nonstereoscopic display. Only two of the four subjects showed differential fixation behavior to this paired comparison situation. In the habituationdishabituation procedure, each of the four subjects was habituated to a randomdot display containing either horizontal disparity (stereoscopic), vertical disparity (proximal cue without stereopsis), or no disparity (planar). After reaching a criterion of habituation, each subject received either a shift in disparity (horizontal to vertical, vertical to horizontal, planar to horizontal, or horizontal to planar) or a no-shift control. Two infants (only one of whom showed positive evidence of disparity discrimination on the fixation preference measure) showed reliable dishabituation to the disparity-shift condition compared to the no-shift control. The other two infants showed dishabituation to only one direction of disparity change (planar to horizontal and vertical to horizontal, but not the reverse). While these results suggest that some 2-month-old infants can detect changes in disparity, the fact that only four infants were tested, and only two showed positive evidence of disparity detection, leads one to question the reliability of disparity detection as measured in their two tasks. Fox, Aslin, Shea, and Dumais (1980) have recently reported the fiist compelling evidence for the existence of disparity detection in young infants. A key feature of their method was a system for generating random-element stereograms on-line by means of a rear projection color television display (Shetty, Brodersen, & Fox, 1979). The system presented red and green elements randomly arranged across the screen and in constant motion (Fox, Lehmkuhle, & Bush, 1977). Displacement of a small square-shaped region of red elements relative to the green elements created retinal disparity. Adults viewing this display while wearing a red filter over one eye and a green filter over the other report that the square-shaped region of elements appears to lie in front of the plane of the rear projection screen. The unique feature of the display system was its capability for moving the stereoscopic form within the entire field of random elements. Movement of the stereoscopic form capitalized upon the infant’s natural tendency to visually track moving stimuli. This dynamic random-element display (like static
I8
Richard N . Adin and Susan T . Dumais
random-element displays) eliminated all monocular cues to detection of the stereoscopic form, and the continual motion of the elements eliminated all monocular cues to the movement of the stereoscopic form. Thus, the presence of visual tracking behavior that correlated with the lateral displacement of the stereoscopic form would provide strong evidence for the existence of disparity detection. Forty infants between 2 and 5 months of age were tested while wearing a pair of spectacle frames containing one red and one green filter. A variant of the forced-choice preferential looking technique (Teller, Morse, Borton, & Regal, 1974; see Teller, 1979, for a general description) was used to assess the presence of visual tracking of the stereoscopic form. On each trial the form was moved either to the right or left of screen center and an observer, blind as to the direction of stimulus movement, made a forced-choice judgment of the direction of stimulus movement based on the infant’s eye movements. Results indicated that the infants’ performance improved significantly with age and that infants over 3 months of age performed at a level significantly greater than chance. The negative finding for infants under 3 months of age was not the result of a simple attentional deficit since all infants were required to pass a 75% criterion on trials containing a real form (physical contour) before stereopsis testing began. In addition, the element size in the display (45 minutes of arc) was well above the acuity threshold typical of infants across all of the ages tested. Hence, it would appear that some other factor(s) accounted for the younger infants’ poor performance-for example, poor bifoveal fixation, inaccurate convergence, or a deficit in the central neural mechanism subserving disparity processing. The results for the infants older than 3 months of age demonstrated that the capability for disparity detection was present. Although this demonstration is important for an understanding of the development of binocular depth perception, disparity detection is only a necessary and not a sufficient condition for stereopsis. It is possible that in the study of Fox et al. (1980) the infants detected the presence of disparity (a proximal cue) without the perception of the stereoscopic form lying in front of the screen (the distal depth percept). To test this alternative, an additional group of 3- to 5-month-olds was tested on trials in which disparity was manipulated. For adults, very large values of disparity result in the loss of patent stereopsis even though disparity information is still present and can be reliably discriminated. Results from this second experiment indicated that the infants’ performance exceeded chance levels only at moderate disparity values-values that adults judge as easily fusable and resulting in the percept of depth. The results of the study of Fox et al. (1980) provide the first convincing evidence that stereopsis is present in young infants. However, many questions remain, including the accuracy of stereopsis (stereoacuity) at different ages and whether variations in early experience contribute to individual differences in
Binocular Vision in Infants
79
stereoacuity. Moreover, it is clear that all of the constraints on stereopsis are sufficiently reduced by the fourth postnatal month to allow rudimentary stereopsis to occur. In Section V, we turn to the mechanisms responsible for the development of binocular function by considering how maturational and experiential factors interact to produce an adult level of binocular vision.
V. Early Experience and Binocular Function The preceding review of empirical research on infant binocular vision provides an up-to-date description of the three levels of binocular function-bifoveal fixation, fusion, and stereopsiAuring the first 6 months of life. However, those descriptions do not explain the mechanisms underlying developmental change in each of the three levels of binocular function. Although one cannot begin to understand how development is controlled until the basic abilities present at different ages are described, we feel that enough is now known about these basic binocular abilities to allow us to.propose a model of those factors influencing binocular development. Our goal in this final section, therefore, is to offer a model of binocular development that not only organizes the currently available descriptions of infant binocular abilities but also generates testable hypotheses to guide empirical research. A. THE ROLES OF EARLY EXPERIENCE
Perhaps the most basic question one can ask about the mechanism@) controlling binocular development concerns the relative influences of genetic and experiential factors during the early postnatal period. In the past, two dichotomous opinions have been raised regarding the basis of binocular development. In its most extreme form, the nativist position was that the mechanisms underlying binocular function are present at birth, although difficulties in measuring these abilities may prevent their accurate assessment. At the other extreme, the pure empiricist position was that the neural connections subserving binocular function and the sensory-motor coordination present in adults’ binocular vision are acquired solely as a result of postnatal experience. The preceding review of recent research on human infants strongly suggests that the three levels of binocular function undergo considerable postnatal improvement. In addition, these findings, along with related findings on the neural mechanisms underlying binocular function in nonhuman infants (see Grobstein & Chow, 1976, for a general review), suggest that the binocular visual system is significantly constrained by genetic factors. Therefore the simplistic (and extreme) forms of nativism and empiricism appear to be untenable as models of human binocular development.
80
Richard N . Aslin and Susan T . Dwnais
A more reasonable reformulation of the simple nativism-empiricism dichotomy is to ask (1) how severely do genetic factors constrain the plasticity of binocular functions, (2) what environmental manipulations influence binocular functions, and (3) when during development does the environment exert its greatest influence on binocular functions. A convenient method for addressing each of these questions is to consider the possible courses that binocular development can take as a result of the gene-environment interaction. A general scheme for illustrating these possible developmental outcomes has been proposed by A s h and Pisoni (1980). Although the scheme was originally applied to the developmental data on infant speech perception, it is based largely on the research and theorizing of Gottlieb (1976), a behavioral embryologist, and is generally applicable to a broad range of topics in sensory and perceptual development. The general scheme for describing the possible courses of infant binocular development is illustrated in Fig. 8. Although there are an unlimited number of developmental curves describing the possible progression of binocular develop ment, we have shown only three major alternatives that correspond to three degrees of genetic specification reached prior to birth. The first alternative describes a prenatal period during which the level of binocular function reaches the full adult status. The influence of postnatal experience is to maintain this mature binocular function. Failure to receive maintaining experience results in a loss of binocular function if that maintaining experience is absent during the particular postnatal period when the integrity of binocular function is susceptible to environmental influences (the sensitive period).
PRENATAL
POSTNATAL
A G E 4
Fig. 8 . Illustration of several possible roles that early visual experience might play in the development of binocular function.
Binocular Vision in Infanis
81
The second alternative developmental curve describes the partial specification of binocular development during the prenatal period. After birth, the level of binocular function either improves, declines, or remains the same as a result of the quality of binocular input received during the sensitive period. Binocular experience may facilitate, maintain, or decrease the partially specified (nearly adult-like) status of binocular function present at birth. The third alternative curve describes the absence of binocular function at birth. Postnatal improvement in binocular function is the result of an induction by environmental input received during the sensitive period. Both the qualitative and the quantitative aspects of binocular function are determined by early binocular experience. Finally, a postnatal improvement in binocular function might be determined by genetic constraints that are independent of any postnatal experience; that is, neural maturation may occur postnatally as well as prenatally, and this maturation may not depend upon any specific type of postnatal environmental input. In general, therefore, we can consider four major roles that postnatal experience might play in the development of binocular function. In the case of maintenance, the binocular ability is present at birth but must be consolidated during the sensitive period by visual experience that closely matches the genetically specified mechanism underlying a particular binocular function. For facilitation. the binocular ability is partially specified at birth but awaits postnatal experience to attune or align the mechanism underlying a particular binocular function to the specifics of the environment. For induction, the binocular ability is absent at birth and the path of postnatal development is primarily determined by the specific qualities of environmental experience. Finally, in the case of maturution, the binocular ability is either absent or only partially specified at birth and any postnatal improvement is determined primarily by genetic factors and not by the specifics of environmental input. One might infer that if postnatal improvement occurred, it would be impossible to choose among the three cases of facilitation, induction, and maturation. However, that inference is not correct provided that one can (1) vary the quality of visual experience during the early postnatal period and (2) measure accurately the integrity of binocular function at many postnatal ages. Although these two requirements are difficult to meet in the study of human binocular function, they have been met in the study of several nonhuman species. We shall now briefly consider two examples from the animal literature to highlight the importance of early experience in the development of binocular function. B. BINOCULAR NEURAL MECHANISMS IN THE CAT
Several experiments, including the pioneering reports of Hubel and Wiesel (1%5, 1970) and more recent replications (Blakemore & Van Sluyters, 1974, 1975; Movshon, 1976; Blakemore, 1976; Olson & Freeman, 1978), have
82
Richard N. A s h and Susan T.Dumais
documented four major aspects of neural functioning in the cat visual cortex. First, approximately 80% of single neurons in the visual cortex of the adult cat are responsive to visual input delivered to either or both retinas. Second, the newborn kitten has an adult-like distribution of binocular neurons. Third, these binocular neurons are absent in adult cats that have been deprived of normal binocular experience (e.g., having monocular occlusion). And fourth, a loss of binocular neurons occurs only if anomalous binocular input is received during a sensitive period extending from approximately 4 to 14 weeks postnatally. Therefore, the property of cortical neuron binocularity appears to be best described by a maintenance role for early experience. Adult-like binocularity is present at birth but is lost if abnormal binocular input is received during the cat's sensitive period. The property of cortical binocularity, however, does not provide a complete account of the cat's sensitivity to relative object distance, since binocularity indicates only that a neuron is responsive to input from both retinas. A further aspect of cortical responsiveness is the F i n g pattern of binocular neurons to the precise alignment of specific retinal loci. Barlow, Blakemore, and Pettigrew (1967) have shown that binocular neurons in the adult cat visual cortex are each optimally responsive to a particular value of retinal disparity. If the optimal disparity value is O", then that particular neuron represents a spatial location on the horopter. If the optimal disparity value is greater or less than O", then that particular neuron represents a location in front of or behind the horopter. Thus, the entire population of binocular neurons in the visual cortex of the cat can provide information on the relative depth of objects located in three-dimensional space. The property of cortical disparity specificity, unlike binocularity, does not appear to be present in an adult-like form in newborn kittens. Pettigrew (1974) has shown that at birth, individual binocular neurons are responsive to a broad range of disparity values. During early postnatal development, the range of disparities over which a particular binocular neuron will respond decreases, resulting in a population of binocular neurons each finely tuned to a particular disparity value. Obviously, if the kitten is binocularly deprived during the sensitive period, cortical binocularity will be lost, as will the property of cortical disparity specificity. More subtle manipulations of early visual experience may alter cortical disparity specificity. Shlaer (1971) found that the mean disparity value to which a particular neuron will become tuned is dependent upon the disparity values presented during the sensitive period and is not simply the result of innate or maturational factors. This plasticity in disparity tuning is apparently not unlimited, however, since large shifts in disparity (such as those resulting from gross eye misalignment) do not result in a shift in disparity tuning but rather in a loss of binocularity. Hence, the property of cortical disparity specificity appears to be best described by a facilitation role for early experience. The
Binocular Vision in Infants
83
disparity responsiveness of individual neurons is partially constrained by genetic factors, but the fine tuning of these neurons is determined by the specifics of postnatal experience during the sensitive period. The behavioral implications of these findings on binocular neural development have been clearly demonstrated by Blake and Hirsch (1975) and Packwood and Gordon (1975), who showed that the accuracy of disparity detection in a local stereopsis task is greatly diminished if cats have been binocularly deprived during the sensitive period. These behavioral results strongly suggest that cortical binocularity is a necessary prerequisite for stereopsis. However, the specific correspondence between cortical disparity values and the quality of stereopsis remains unclear. Moreover, an understanding of the development of stereopsis in cats awaits the development of a behavioral technique that effectively measures stereoacuity in very young kittens.' C. SENSITIVE PERIOD FOR HUMAN BINOCULAR FUNCTION
The general principles discussed in the foregoing summary of the binocular neural mechanism in cats led two groups of investigators (Banks, Aslin, & Letson, 1975; Hohmann & Creutzfeldt, 1975) to search for analogous effects of early binocular experience in humans. Both studies employed a psychophysical technique (interocular transfer of the tilt-aftereffect)8to assess binocular function in children and adults who had received nonconcordant binocular input during some period of their early lives. This nonconcordant input resulted from a particular type of strabismus, esotropia, that consists of a constant cross-eyed condition. Each subject had been deprived during a different developmental period prior to receiving corrective surgery. Although all subjects had correctly aligned eyes after surgery, those who had been deprived during the first 3 years of life had a permanent deficit in binocular function. Figure 9.shows the estimated sensitivity of the human visual system to binocular deprivation at different ages. These results provide strong evidence that binocular function in humans is dependent upon the quality of binocular experience received during a sensitive period. The results from these two studies, despite their importance in delineating the characteristic form and timing of a sensitive period in humans, do not clarify the exact role that early experience plays in human binocular development. One knows from these studies only that a simple maturational model is untenable 'The fmt studies of stereopsis in cats were performed with a local stereopsis display. Subsequently, Lehmkuhle, Fox, and Bush (1977) have demonstrated stereopsis in cats using a randomelement display. A global stereopsistask, such as the one employed by Fox er al. (1980) with human infants, may provide a useful technique for assessing the presence of stereopsisin the developing cat. 8Mitchell and Ware (1974) and Movshon, Chambers, and Blakemore (1972) have shown that interocular transfer of the tilt-aftereffxt is highly correlated with stereoacuity values in adults.
Richard N . Adin and Susan T . Dumais
a4
1.0
I
>-
t
L
0.8
z 2 Ia
0.4
k
1
a a w
D
0.2
0
I
2
3
4
5
6
7
8
9
AGE (yrs)
Fig. 9. An estimate of the relative importance of binocular deprivation to human binocular function during the first 10 years of life. (Adaptedfrom Banks, Adin. & Letson. Science, 1975, 190, 675477. Copyright 1975 by the American Association for the Advancement of Science.)
since binocular experience exerts some influence during the postnatal period. The only way of differentiating among the three remaining roles of experience-maintenance, facilitation, and induction-is to measure stereopsis in young infants to determine whether disparity responsiveness is completely specified at birth, partially specified, or not specified at all. The results of the study of Fox et al. (1980) suggest that experience is unlikely to play a maintenance role since infants did not show evidence of stereopsis until the fourth postnatal month. However, the negative findings from these younger infants must be interpreted with caution, since their poor performance may reflect deficits in one or more visual functions that limit disparity detection. Nevertheless, on the basis of currently available data, it appears that either a facilitation or an induction model offers the best description of the manner in which experience operates during the sensitive period for human binocular function. Based upon this conclusion and the previously reviewed findings on infant binocular function, we shall now propose a tentative model of human binocular development. D. A MODEL OF HUMAN BINOCULAR DEVELOPMENT
The model of binocular development we propose postulates that at birth, several factors constrain the integrity of binocular function. In the early postnatal period, the quality of visual experience tunes up those aspects of binocular
Binocular Vision in Infants
85
function that are already partially specified by genetics. In general, therefore, we believe that the facilitation role for early experience best describes the mechanism underlying binocular development. In the discussion to follow, we shall consider each of the three levels of binocular function by describing the capacity of each level at birth, how that capacity changes postnatally, and the manner in which early experience modifies binocular capabilities.
I . Bifoveal Fixation Although the empirical findings on bifoveal fixation are not conclusive, it is quite clear that bifoveal fixation is at best intermittent at birth. Newborns may fixate bifoveally for targets located at certain distances, but the range of bifoveal fixation is limited and the speed with which changes in eye alignment occur to maintain bifoveal fixation is restricted. Two nonbinocular factors appear to offer the most significant detriments to consistent bifoveal fixation in newborns. First, monocular acuity and contrast sensitivity are quite poor at birth, degrading spatial resolution. As a result, a small high-contrast target is effectively increased in spatial extent and degraded in salience. Although measures of peripheral acuity have not been obtained in infants, their poor foveal acuity suggests that the gradient of acuity from fovea to periphery may be less steep in newborns than in adults. Consequently, the need for small eye movements to maintain optimum spatial resolution by keeping the target on the fovea@) is likely r e d ~ c e d .In~ addition, this shallower acuity gradient indicates a decreased likelihood of detecting a small shift in the target’s image on the retina. A second factor that degrades bifoveal fixation is the immaturity of the oculomotor control system. Much of this oculomotor control inefficiency is undoubtedly the result of deficits in image processing (acuity). In addition, however, the rapid development of the neuromuscular system, as evidenced by changes in motor reflexes (Peiper, 1963), suggests that the oculomotor system may be poorly organized at birth. In sum, currently available evidence strongly suggests that bifoveal fixation is not consistently present in early infancy. There is now convincing evidence that during the first 6 months after birth, there is a marked improvement in acuity (Dobson & Teller, 1978) and oculomotor control (Aslin, 1977, 1980; A s h & Salapatek, 1975; Dayton & Jones, 1964; Ling, 1942). These advances strongly suggest that bifoveal fixation also becomes more accurate and more consistent during this age period. The 9Weassume here that current infant acuity estimates (see Dobson &Teller, 1978) reflect the spatial resolving power of the most sensitive portion of the retina. However, one could argue that infants’ relatively poor acuity is in part the result of employing extrafoveal retinal areas that possess poor spntial resolving powers. If so, the apparent flatness of the infant acuity threshold across the entire retinal surface would be an artifact of the inefficient use of the fovea. Nevertheless, small eye movements would still fail to enhance spatial resolution since the fovea would not be consistently used as the line of sight.
86
Richard N.Aslin and Susan T.Dumais
exact mechanism underlying improvements in the two subsystems of acuity and oculomotor control, however, is unclear. It would appear that unless a gross refractive error (myopia, hyperopia, anisometropia) is present, infants will show a nearly 10-fold improvement in acuity during the first 6 months of life. Although early deprivation degrades acuity in monkeys (von Noorden, 1973), it remains to be seen whether particular types of visual input are needed to facilitate acuity development in humans or whether acuity development occurs independently of early visual experience (i.e., according to a genetically specified maturational sequence). Similarly, the increase in oculomotor control might result from specific eye movement experience or general newomuscular maturation. However, regardless of the mechanism underlying development in these two subsystems, such development appears to be essential for accurate and consistent bifoveal fixation. In addition, it would appear that by 6 months of age, the major constraints of acuity and oculomotor control on bifoveal fixation are largely eliminated, since stereopsis is present. Any deficits in bifoveal fixation after this age can have long-term, often permanent effects on binocular function (Banks et al., 1975; Burian & von Noorden, 1974; Duke-Elder & Wybar, 1973; Hohmann & Creutzfeldt, 1975; Taylor, 1973). Finally, there are four other factors relevant to the question of bifoveal fixation that deserve brief mention. First, the absence of accommodation in newborns may create a conflict with the control of convergent eye movements and thereby prevent bifoveal fixation for targets presented at certain distances. Unfortunately, there are no data on the accommodation-convergence relationship in infants under 2 months of age. However, it appears that after 2 months of age, both systems are operating very well (Aslin & Jackson, 1979) although not necessarily as precisely as in adults. Second, the orbits are more divergent in newborns than in adults, hence demanding a greater degree of eye rotation to converge on fixation targets. This additional constraint on bifoveal fixation, however, is diminished by the third and fourth factors relevant to bifoveal development. The third factor is the increased optic axis-visual axis discrepancy in newborns compared to adults. The effect of this larger angle alpha is to demand less convergent eye rotation to near targets by newborns, since the visual axis in each eye is directed nasaliy from the optic axis. The fourth factor, interocular separation, also places less demand on convergent eye rotation. These last two factors raise an interesting point regarding the demand on the convergence system. In a newborn with a 40-mm interocular separation and an 8" angle alpha, the two optic axes (pupil centers) can be oriented in parallel (as if viewing an object at infinity), and the visual axes will-intersect at a point only 14.2 cm from the infant. In contrast, for an adult with a 60-mm interocular separation, a 4" angle alpha, and the two optic axes oriented in parallel, the point of visual axis intersection would be 42.9 cm away, thus requiring an additional 7.9" of convergent rotation for each eye in order to bring the visual axes to the
Binocular Vision in Infants
87
14.2 cm viewing distance of the infant. In light of these facts, it is perhaps not surprising that very young infants often appear walleyed, especially if they are attempting to fixate an object beyond 14.2 cm. Consequently, the newborn’s visual system is apparently biased toward nearobject fixation by three factors: (1) the anatomical and geometrical factors involved in eye alignment, (2) the degraded image processing powers that make any distant object (unless very large) below acuity threshold, and (3) the absence of accommodation that biases image focus to near distances and may conflict with the control of convergence.10Although the period of early postnatal development may consist of intermittent bifoveal fixation, there appears to be a functionally advantageous bias for this intermittent bifoveal fixation to operate primarily during near-object viewing. In short, if early visual experience influences neural development during the first months of life, the resultant neural modification is biased toward receiving input from near, large, and in-focus objects.
2. Fusion The mechanism underlying this second level of binocular function is unfortunately not well understood. Moreover, little is known about the presence or absence of fusion in infants. However, it seems clear that the acuity deficit in newborns that degrades spatial resolution also reduces the need for accurate alignment of corresponding retinal points to guarantee fusion. That is, if fine spatial resolution is absent, then detection of spatial misalignment should be reduced. Nevertheless, it is impossible to state conclusively that fusion is present in young infants. They may very rapidly alternate viewing from one eye to the other and thereby exhibit few symptoms of the absence of fusion. In addition, they may have peripheral fusion without foveal (central) fusion, a fact that may not be functionally disadvantageous since in most normal viewing situations targets are quite large and scanning eye movements occur continuously. Although at present there are no conclusive data on infant fusion, our working hypothesis, based on the data from Aslin (1977) using the prism test and Fox et al. (1980) using random-element stereograms, is that infants have fusion by 4 to 6 months of age. We further hypothesize that the extent of Panum’s fusion area diminishes with age, and that this decrease is due both to an improvement in acuity and to an improvement in disparity resolution. Good monocular acuity is a necessary requirement for good disparity resolution, SO that disparity resolution must be built upon spatial resolution (Stigmar, 1970). However, good spatial resolution is not a guarantee of good disparity resolution, a fact borne out by the ‘ORecent estimates of the depth of focus in the infant eye (Banks, 1980; Green, Powers, & Banks, 1980) suggest that clarity of retinal image focus may not be critical for optimal acuity because the smaller infant eye, with a larger depth of focus, does not suffer a significant loss of acuity as the target becomes blurred.
88
Richard N. Aslin and Susan T.Dumais
large number of stereoblind adults who have good acuity in both eyes. As disparity resolution improves during early life, the requirements of binocular eye alignment increase so as to maintain fusion. Clearly there are limits to the degree of inaccuracy this eye alignment can have without creating diplopia. Presumably, these limits are specified genetically such that slight deviations in eye alignment during the first few months of life do not permanently degrade fusion. However, as disparity resolution improves, the accuracy of binocular eye alignment must conform to these genetically specified limits. Failure to conform results in a permanent loss of the fusion mechanism, an effect clearly documented in the clinical literature on strabismus (Burian & von Noorden, 1974; Duke-Elder & Wybar, 1973). We conclude from these findings that either the induction or the facilitation roles for early experience best describes the development of fusion. That persons with crossed eyes from birth do not have fusion (unless surgically corrected early in life) suggests that maturation cannot account for its develop ment . 3 , Stereopsis The final level of binocular function, stereopsis, develops quite similarly to fusion. The only significant difference between our understanding of fusion and that of stereopsis is that we have evidence for the existence of stereopsis in very young infants (Fox er al., 1980). The evidence that suggests the absence of stereopsis in infants under 3 months of age may reflect the poor spatial resolution and lack of consistent bifoveal fixation in young infants. Although infants show good convergence by 3 months of age (both in range and speed), they may have difficulty maintaining consistent bifoveal fixation, thereby creating a difficulty in extracting from the display the corresponding and disparate points that provide the essential information for stereopsis. Apart from these constraints, however, the disparity resolution mechanism appears to undergo significant improvement postnatally, provided that bifoveal fixation is within genetically specified limits. Based upon the typical minimum eye misalignment that receives surgical correction and the accuracy with which surgical corrections are performed, this genetic limit in eye alignment is most likely 5-8". If bifoveal fixation is beyond this limit, then correspondingpoints cannot link up in the higher visual areas and both fusion and disparity detection break down. Consequently, early experience operates as a facilitator in that visual input during the sensitive period tunes up the disparity resolving mechanism, provided that early visual input conforms to the limits specified by genetics. Finally, the data on a sensitive period in human binocular development suggest that stereopsis is not significantly influenced by early experience during the first 4 months of life (see Fig. 9). Although we realize the following point is speculative, we would suggest that the visual system delays the period of experiential
Binocular Vision in Infants
89
influence until the subsystems needed for all three levels of binocular function are at least minimally functional. This hypothesis, in concert with our previous discussion of the three levels of binocular function, suggests that the course of binocular development is characterized by a complex interaction between genetically constrained subsystems and early experiential effects. These genetic constraints place limits within which early experience must fall. Further development of binocular capabilities is directly dependent upon the quality of early experience. If that early experience conforms to the genetic constraints, then development proceeds normally. If the genetic limits are exceeded (i.e., producing binocular deprivation), then binocular abilities either fail to develop or show a permanent loss of function. 4. Summary
The general model of binocular development we have presented proposes that the basic mechanisms underlying bifoveal fixation, fusion, and stereopsis are present in rudimentary form at birth, but that they are constrained by various sensory and motor subsystems. These Constraints must be overcome for adult-like binocular functions to develop. During the first 4 to 6 months of life, as these constraints diminish, the three binocular functions become manifest. In addition, the postnatal period beginning at approximately 4 months after birth and extending at least into the second year of life is characterized by a heightened susceptibility to anomalous visual input. If the visual input during this sensitive period does not conform to the range of genetically specified limits for binocular functions, then the mechanism(s) underlying binocular functions fail to show further development and, in extreme cases of anomalous input, may become degraded or permanently impaired. The task for future research is to specify the precise relationship between the quality of early visual experience and the quantitative aspects of binocular function. This task will entail correlational studies linking the sensory (acuity) and motor (accommodative, oculomotor) subsystems with the integrity of binocular functions (Panum’s fusion area, stereoacuity). In addition to these correlational studies, attempts should be made to find naturally occurring variations in early visual input (crossed eyes, cataract, anisometropia) to determine the exact magnitude and timing of experiential influence on binocular function. Finally, the increasing study of genetic anomalies that affect visual functioning (e.g., albinism) may provide a useful insight into the limits placed by genetic factors upon experiential influence. The combined study of normal and clinical populations, as well as nonhuman primates, both during infancy and into adulthood, will eventually clarify the essential mechanisms and their time course in the development of binocular function.
90
Richard N . Aslin and Susan T . Dumais
VI. Concluding Remarks In this article we have attempted to summarize the empirical findings on infant binocular vision within a coherent theoretical framework. This framework includes (1) a consideration of the multileveled nature of binocular function, (2) the constraints placed upon binocular function by other aspects of visual development, and (3) the role that early visual experience may play in binocular development. The goal of future empirical research, therefore, should be to provide (1) a more accurate description of the integrity of binocular functions at different postnatal ages, (2) an interpretation of those developmental descriptions that takes into account the several constraints on binocular functions, and (3) a search for new methods and clinical populations that will provide insight into the magnitude and timing of experiential influence in binocular development, REFERENCES Appel, M. A., & Campos, J. J. Binocular disparity as a discriminable stimulus parameter for young infants. Journal of Experimental Child Psychology. 1977, 23,47-56. A s h , R. N. Development of binocular fiiation in human infants. Journal of Experimental Child Psychology, 1977, 23, 133-150. Aslin, R. N. Development of smooth pursuit in human infants. Paper presented at The Last Whole Earth Eye Movement Conference. St. Petemburg, Florida, February 1980. Aslin, R. N., & Jackson, R. W.Accommodative-convergence in young infants: Development of a synergistic sensory-motor system. Canadian Journal of Psychology, 1979,33, 222-231. Aslin, R. N., & Pisoni, D. B. Some developmental processes in speech perception. In G. H. Yeni-Komshian, J. Kavanagh, & C. A. Ferguson (Eds.), Child phonology: Perception and production. New Yo& Academic Press, 1980. A s h , R. N., & Salapatek, P. Saccadic localization ofxisual targets by the very young human infant. Perception & Psychophysics, 1975, 17, 293-302. Atkinson, J., & Braddick, 0. Stereoscopic discrimination in infants. Perception, 1976, 5, 29-38. Atkinson, J., Braddick, O., & Moar, K. Development of contrast sensitivity over the first 3 months of life in the human infant. Vision Research, 1977, 17, 1037-1044. Ball, W..& Tronick, E. Infant responses to impending collision: Optical and real. Science, 1971, 171, 818-820. Banks, M. The development of visual accommodation during early infancy. Child Development, 1980, in press. Banks, M. S . , A s h , R. N., & Letson, R. D. Sensitive period for the development of human binocular vision. Science, 1975, 190,675-677. Banks, M. S., & Salapatek, P. Acuity and contrast sensitivity in 1, 2, and 3-month-old human infants. Investigative Ophthalmology, 1978, 17, 361-365. Barlow, H. B., Blakemore, C., & Pettigrew, J. D. The neural mech@sms of binocular depth discrimination. Journal of Physiology (London), 1967, 193, 327-342. Bechtoldt, H. P., & Hutz, C. S. Stereopsis in young infants and stereopsis in an infant with congenital eaotropia. Journal of Pediatric Ophthalmology, 1979, 16,49-54. Berry, R. N. Quantitative relations among vernier, real depth, and stereoscopic depth acuities. Journal of Experimental Psychology, 1948, 38, 708-721,
Binocular Vision in Infants
91
Blake, R., & Hirsch, H. V. B. Deficits in binocular depth perception in cats after alternating monocular deprivation. Science. 1975, 190, 1114-1 116. Blakemore, C. The range and scope of binocular depth discrimination in man. Journal of Physiology (London), 1970, 211, 599-622. Blakemore, C . The conditions required for the maintenance of binocularity in the kitten’s visual cortex. Journal of Physiology (London), 1976, 261,423-444. Blakemore, C., & Van Sluyters, R. C. Reversal of the physiological effects of monocular deprivation in kittens: further evidence for a sensitive period.-J&naiof Physiology (London),1974, 237, 195-2 16. Blakemore, C., & Van Sluyters, R. C. Innate and environmental factors in the development of the kitten’s visual cortex. Journal of Physiology (London), 1975, 248, 663-716. Boring, E. G. Sensation and perception in the history of experimental psychology. New York: Appleton, 1942. Bower, T. G. R. Discrimination of depth in premotor infants. Psychonornic Science, 1964,1,368. Bower, T. G. R. Stimulus variables determining space perception in infants. Science, 1965, 149, 88-89. Bower, T. G. R.Slant perception and shape constancy in infants. Science, 1966, 151,832-834. (a) Bower, T. G. R. The visual world of infants. Scientific American, 1966, 215; 80-92. (b) Bower, T. G. R.Morphogenetic problems in space perception. In D. Hamburg & K.Ribram (Eds.), Proceedings of the Association for Research in Nervous and Mental Diseases. Stanford, Calif.: Stanford University Ress, 1968. Bower, T. G. R. The object in the world of the infant. Scientijic American. 1971, 225, 30-38. Bower, T. G . R. Object perception in infants. Perception, 1972, 1, 15-30. Bower, T. G . R., Broughton, J. M., & Moore, M. K. Demonstration of intention in the reaching behavior of neonate humans. Nature (London), 1970, 228,679-680. Bower, T. G . R., Broughton, J. M., & Moore, M. K.Infant’s responses to approaching objects: An indicator of response to distal variables. Perception & Psychophysics, 1971, 9, 193-196. Bower, T. G. R., Dunkeld, J., & Wishart, J. G. Infant perception of visually presented objects. Science, 1979, 203, 1137-1138. Braddick, O., Atkinson, J., French, J., & Howland, H. C. A photorefractive study of infant accommodation. Vision Research, 1979, 19, 1319-1330. Bronson, G. The postnatal growth of visual capacity. Child Development, 1974, 45, 873-890. Burian, H. M., & von Noorden, G . K. Binocular vision and ocular motility, St. Louis: Mosby, 1974. Campos,J. I . , Langer, A,, & Krowitz, A. Cardiac response on the visual cliff in prelocomotor human infants. Science, 1970, 170, 196-197. Caron, A. J., Caron, R. F., & Carlson, V. R. Do infants see objects or retinal images? Shape constancy revisited. Infant Behavior and Development, 1978, 1, 229-243. Cruikshank, R. M.The development of visual size constancy in early infancy. Journal of Genetic Psychology, 1941, 58, 327-351. Dayton, G . O . , & Jones, M.H. Analysis of characteristics of fixation reflexes in infants by use of direct current electtooculography. Neurology. 1964, 14, 1152-1 156. Dobson, V., &Teller, D. Y.Visual acuity in human infants: A review and comparison of behavioral and electrophysiological studies. Vision Research, 1978, 18, 1469-1483. Dodwell, P. C., Muir, D., & DiFranco, D. Responses of infants to visually presented objects. Science, 1976, 194,209-21 1. Dodwell, P. C., Muir, D. W., & DiFranco, D. Infant perception of visually presented objects. Science, 1979, 203, 1138-1139. Duke-Elder, S., & Wybar, K. System of ophthalmology (Vol. 6 ) . St. Louis: Mosby, 1973. Pp. 591-597.
Richard N . Aslin and Susan T . Dumais
92
Fantz, R. L.A method for studying depth perception in infants under six months of age. Psychological Record, 1961, 11,27-32. Fantz, R. L.Pattern discrimination and selective attention as determinantsof perceptual development from birth. In A. H. Kidd and J. L. Rivoire (Eds.), Perceptual development in children. New York International Universities Press, 1966. Fox, R.,Aslin, R. N., Shea, S. L.,& Dumais, S.T.Stereopsis in human infants. Science. 1980,
207,323-324. Fox, R.,Lehmkuhle, S. W., & Bush, R. C. Stereopsis in the falcon, Science, 1977, 197,79-81. Gesell, A., Thompson, H., & Amatruda, C. S . Infant behavior: Its genesis and growth. New York: McGraw-Hill, 1934. Gordon, F. R., & Yonas, A. Sensitivity to binocular depth information in infants. Journal of Experimental Child Psychology, 1976,22,413-422. Gottlieb, G. The roles of experience in the development of behavior and the nervous system. In G.Gottlieb (Ed.), Studies on the development of behavior and the nervous system (Vol. 3). New York Academic Press, 1976. Green, D. G., & Campbell, F. W.Effect of focus on the visual response to a sinusoidally modulated spatial stimulus. Journal of the Optical Society of America, 1965, 55, 1154-1157. Green,D.G.,Powers, M. K., & Banks, M. S. Depth of focus, eye size and visual acuity, Vision Research, 1980. in press. Gmktein. P.. & Chow, K. L.Receptive field organization in the mammalian visual cortex: The role of individual experience in development. In G. Gottlieb (Ed.), Neural and behavioral specificity. New York: Academic Press. 1976. Haith, M. M a r e d television recording and measurement of ocular behavior in the human infant. American Psychologist, 1969,24, 279-283. Haynes, H., White, B. L.,& Held. R. Visual accommodation in human infants. Science. 1965,148,
528-530. Hendrickson, A., & Kupfer, C. Histogenesis of fovea in macaque monkey. Investigative Ophrhalntology, 1976, 15, 146-752. Hering. E. [The theory of binocular vision] (B. Bridgeman and L. Stark, Eds. and trans.). New York Plenum, 1977. (Originally published, 1868.) Hochberg, J. Perception II. Space and movement. In J. W. Kling Br L. A. Riggs (Eds.), Woodworth and Schlosberg’s experimental psychology (3rd Ed.). New York Holt, 1971. Hohmann, A., & Creutzfeldt, 0. D. Squint and the development of binocularity in humans. Nature (London) 1975, 254, 613-614. Hubel, D. H., & Wiesel, T.N. Binocular interaction in striate cortex of kittens reared with artificial squint. Journal of Neurophysiology, 1965. 28, 1041-1059. Hubel, D. H.,& Wiesel, T. N. The period of susceptibility to the physiological effects of unilateral eye closure in kittens. Journal of Physiology (London), 1970,206,419-436. Jampolsky, A. The prism test for strabismus screening. Journal of Pediatric Ophthalmology, 1964,
1, 30-34. JuIesz, B. Binocular depth perception of computer-generatedpatterns. Bell System Technical Journal, 1960,39, 1125-1162. Julesz, B. Foundawns of qclopean perception. Chicago: University of Chicago Press, 1971. Kaufman, L . Sight and mind. London and New York: Oxford University Press, 1974. Krieg, K. Tonic convergence andfacial growrh in early infancy. Unpublished senior Honors Thesis, Indiana University, 1978. Lehmkuhle, S. W.,Fox, R.,& Bush, R. C. Global stereopsis in the cat. Paper presented at the annual meeting of the Association for Research in Vision and Ophthalmology. Sarasota, Florida, 1977. Lewis, T. L.,Maurer, D., & Kay, D. Newborns’ central vision: Whole or hole? Journul of Experimental Child psycho lo^, 1978,26, 193-203.
Binocular Vision in Infants
93
Ling, B. C. A genetic study of sustained fixation and associated behavior in the human infant from birth to six months. Journal of Genetic Psychology, 1942, 61, 227-277. Mann, I. The development of the human eye. New Yo& Grune & Stratton, 1964. Marg, E., Freeman, D. N.. Peltunan. P., & Goldstein, P. J. Visual acuity development in human infants: Evoked potential measurements. Investigurive Ophthalmology, 1976, 15, 150-152. Matsubayashi, A. Forschung iiber die Tiefenwiihmehmung.IX.Nippon G a n h GakkaiZasshi, 1938, 42, 1920-1929. (German abstract, Nippon Ganka GakkaiZasshi, 133; and Berichre ueber die Gesamte Physiologie und Experimentelle Pharmakologie. 1939, 112, 290-291 .). Maurer, D. The development of binocular convergence in infants. (Doctoral dissertation, University of Minnesota, 1974). Dissertation Abstracts Interncuional, 1975, 35, 6136-B. (University Microfilms No. 75-12. 121). (a) Maurer, D. Infant's visual perception: Methods of study. In L. Cohen & P. Salapatek (Eds.), Infant perception: From sensation to cognition (Vol. 1). New York: Academic Press, 1975. (b) Mitchell. D. E., & Ware, C. Intemular transfer of a visual aftereffect in normal and stereoblind humans. Journal of Physiology (London), 1974, 236,707-721. Morgan, M. W. Accommodation and vergence. American Journal of optometry and Archives of rhe American Academy of Optometry, 1%8,45,417-454. Movshon, J. A. Reversal of the physiological effects of monocular deprivation in the.kitten's visual cortex. Journal of Physiology (London), 1976, 261, 125-174. Movshon, J. A., Chambers,B.E. I., & Blakemore, C. Interocular transfer in normal humans and those who lack stereopis. Perception, 1972, I, 483-490. Muller, J. [Elements of Physiology] ( W . Baly trans.). Philadelphia: Lea and Blanchard, 1943. (Originally published, 1826.) Nachmias, J. Two-dimensional motion of the ntinalimage during monocular fixation. Journal of the Optical Society of America, 1959, 49, 901-908. Ogle, K. N. The optical space sense. In H. Davson (Ed.), The eye (Vol. 4). New York: Academic Press, 1%2. Pp.211-432. Olson, C. R.. & Freeman. R. D. Monocular deprivation and recovery during sensitive period in kittens. Journal of Neurophysiology, 1978, 41, 65-74. Packwood, J., & Gordon, B. Stereopsis in normal domestic cat, Siamese cat, and cat raised with alternating monocular occlusion. Journal of Neurophysiology, 1975, 38, 1485-1499. Pastore, N. Selective history of theories of visual perception: 1650-1950. London and New Yo& Oxford University Press, 1971. Peiper, A. Cerebralfunction in infancy and childhood. New York Consultants Bureau, 1963. Pettigrew, J. D. The effect of visual experience on the development of stimulus specificity by kitten cortical neurons. Jourml of Physiology (London). 1974, 237,49-75. Reinecke, R. D., & Simons, K.A new stereoscopic test for amblyopia screening. American Journal of Ophthalmology, 1974, 78,714-721. Riggs, L.A. Visual acuity. In C.H. Graham (Ed.), Vision and visualperception. New Yo& Wiley, 1965. Pp. 321-349. Romano, P. E., Romano, J. A., & Puklin, J. E. Stereoacuity development in children with normal binocular single vision. American Journal of Ophthalmology, 1975, 79,966-971. Ruff, H.A., & Hulton, A. Is there directed reaching in the human neonate? Developmental Psychology, 1977, 14,425-426. Salapatek, P., Bechtold, A. G.,& Bushnell, E. W. Infant visual acuity as a function of viewing distance. Child Development, 1976, 47, 860-863. Scarr, S., & Salapatek, P. Pattern of fear development during infancy. Mewill-Palmer Quarterly, 1970, 16,53-90. Sheedy, J. E . , & Fry, G. A. The perceived direction of the binocular image. VisionResearch, 1979, 19,201-212.
94
Richard N . A s h and Susan T . Dumais
Shetty, S. S., Brodersen, A. J., & Fox, R. System for generating dynamic random-element s t e w grams. Behavioral Research Methods and Instrumentation. 1979, 11, 485-490. Shipley, T., & Rawlings, S. C. The nonius horopter. I. History and theory. Vision Research, 1970, 10, 1225-1262. Shlaer, R. Shift in binocular disparity causes compensatory changes in the cortical structure of kittens. Science, 1971, 173,638-641. Slater, A. M., & Findlay, I. M. The measurement of fmation position in the newborn baby. Journal of Experimental Child Psychology, 1972, 14,349-372. Slater, A. M., & Findlay, I. M. The corneal reflection technique and the visual preference method: Sources of m.Journal of Experimenral Child Psychology, 1975, M, 240-247. (a) Slater, A. M., & Findlay, J. M. Binocular fixation in the newborn baby. Journal of Experimental Child Psychology, 1975, 20,248-273. (b) Stigmar, G. Observations on vernier and stereo acuity with special reference to their relationship. Acta Ophthalmologica, 1970, 48, 979-998. Taylor, D. M. Congenital esotropia: Management and prognosis. North Miami: Symposium Specialists, 1973. Teller, D. Y. A forced-choice preferential looking procedure: A psychophysical technique for use with human infants. Infant Behavior and Development, 1979, 2, 135-153. Teller, D. Y.,Morse, R., Borton, R., & Regal, D. Visual acuity for vertical and diagonal gratings in human infants. Vision Research, 1974, 14, 1433-1439. Thomas, J., Mohindra, I., & Held, R. Strabismic amblyopia in infants. American Journal of Optomeny and Physiological Optics, 1979, 56, 197-201. von Hofsten, C. Binocular convergence as a determinant of reaching behavior in infancy. Perception, 1977, 6 , 139-144. von Noorden, G . K. Experimental amblyopia in monkeys. Further behavioral observations and clinical correlations. Investigative Ophthalmology, 1973, 12, 721-726. von Noorden, G. K., & Maunamee., A. E. Atlas of Strabismus. St. Louis: Mosby, 1967. Walk, R. D., & Gibson, E. J. A comparative and analytical study of visual depth perception. Psychological Monographs, 1961, 75(15 Whole No. 519). Walters, C., & Walk, R. Visual placing by human infants. Journal ofExperimenta1 Child Psychology, 1974, 18,34-40. Walraven, J. Amblyopia screening with random-dot stereograms. American Journal ofOphrhalmo100,1975, 80, 893-899. Wheatstone, C . On some remarkable, and hitherto unobserved, phenomena of binocular vision. Philosophical Tmnsactions of the Royal Society of London, 1838, 128,371-394. White, B. L., Castle, R., & Held, R. Observationson the development of visually-directed reaching. Child Development, 1964, 35,349-365. Wickelgren, L. Convergence in the human newborn. Journal of Experimental Child Psychology, 1%7, 574-85. Wickelgren, L. The ocular response of human newborns to intermittent visual movement. Journal of Experimental Child Psychology, 1969, 8,469-482. Worth, C. Squint: Its causes, pathology, and treatment. Philadelphia: Blakiston, 1915. Yonas, A., Bechtold, A. G.,Frankel, D.,Gordon, F. R., McRoberts, G.,Norcia, A., & Stemfels, S. Development of sensitivity to information for impending collision. Perception & Psychophysics, 1977, 21, 97-104. Yonas, A., Oberg, C., & Norcia, A. Development of sensitivity to binocular information for the approach of an object. Developmental Psychology, 1978, 14, 147-152. Zimmennan, A. A., Armstrong, E. L., & Scammon, R. E. The change in position of the eyeballs during fetal life. The Anatomical Record, 1929, 59, 109-134.
VALIDATING THEORIES OF INTELLIGENCE'
Earl C . Butterjield. Dennis Siladi. and John M . Belmont KANSAS MENTAL RETARDATION RESEARCH CENTER
I . INTRODUCTION ......................................................
96
I1. A STRATEGY FOR STUDYING INTELLECTUAL DEVELOPMENT .......... A . ANALYZE PROCESSES WITHIN AGE GROUPS ...................... B. CORRELATE PROCESS MEASURES WITH AGE ...................... C. ELIMINATE AGE DIFFERENCES WITH PROCESS INSTRUCTION . . . . . .
96 97 99 100
111. ILLUSTRATION OF THE STRATEGY FOR STUDYING INTELLECTUAL
DEVELOPMENT . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . A. SELECTION OF AN INVESTIGATIVE DOMAIN ...................... B . PROBLEM SELECTION . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . C . CORRELATE PERFORMANCE WITH AGE ........................... D . ANALYZE PROCESSES WITHIN AGES . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . E . RELATE PROCESSES TO AGE ..................................... F . TEACH CHILDREN TO PROCESS AS ADULTS ....................... G . TEACH ADULTS TO PROCESS AS CHILDREN .......................
102 103 103 105 106 120 123 123
IV . A STRATEGY FOR STUDYING THE GENERALITY OF COGNITIVE PROCESSES .......................................................... A . IS THE PROCESS SUBORDINATE OR SUPERORDINATE? . . . . . . . . . . . . . B . DETERMINING THE GENERALITY OF SUBORDINATEPROCESSES ... C. DETERMINING THE GENERALITY OF SUPERORDINATE PROCESSES .
124 125 127 129
V . ILLUSTRATION OF THE RESEARCH STRATEGY FOR TESTING PROCESS GENERALITY ........................................................ A . DECIDE WHETHER PROCESS IS SUBORDINATE OR SUPERORDINATE B. TESTING THE GENERALITY OF SUBORDINATE PROCESSES . . . . . . . . . C . TESTING THE GENERALITY OF SUPERORDINATEPROCESSES ....... VI . CONCLUDING CONSIDERATIONS ..................................... A . THE SEVERAL ROLES OF PROCESS ANALYSIS ..................... B . NONMETRIC COMPLETENESS CHECKS ............................
131 131 140
147 153 153 155
'The preparation of this paper and the research on which its ideas are based were supported by USPHS grants HD.00026. HD.00870. HD.08911. and HD.13029 .
95 ADVANCES IN CHILD DEVELOPMENT AND BEHAVIOR. VOL. 15
.
Copyrighf @I980 by Academic Ress Inc. All rights of reproduction In any form reserved . ISBN 0-12-W971S.X
Earl C. Burterfild et at.
%
C. INSTRUCIPJG AWAY AGE-RELATED DIFFERENCES IN PERFORMANCE .................................................. D. ECOLQGICAL VALIDITY ..........................................
156
........................................................
159
REFERENCES
158
I. Introduction In this chapter we will describe and illustrate a research strategy for validating theories of intelligence. The strategy is dauntingly complex, but it is required by the wide acceptance of two simple ideas. The first is that intelligence develops: Behavior becomes increasingly complex and abstractly organized with age. The second idea is that individual differences in intelligence are general: People who perform relatively intelligently in one situation are likely to perform relatively intelligently in other situations. Even though some people use specialized forms of knowledge and specialized ways of thinking, a person must behave effectively in general to be termed intelligent. The idea that intelligence develops is accepted by process and structural theorists alike; it is accepted by continuity and noncontinuity theorists, by those who do and those who do not subscribe to stage theories, as well as by those who accept the atheoretical view that intelligence is only what IQ tests measure. The idea that intellectual differences are general can be seen in the functionalist argument that intelligence is adaptability, because adaptability amounts to performing well in diverse situations. It can be seen in the Piagetian argument that an instructional experiment has not influenced intelligence unless it has changed a wide range of uninstructed behaviors as well as the instructed ones. The idea can be seen in any standardized test of intelligence, since even the most factorially pure tests yield composite IQ or mental age scores. The wide acceptance of these two ideas makes their complex research implications fall on all who would test theories of intelligence, which is to say, on all who would test cognitive theory.
11. A Strategy for Studying Intellectual Development In cognitive theory, behavior is distinguished from processes that underlie it. The scientific goal is to explain behavior by reference to processes and (others would say) by reference to mental structures. By process, we mean any aspect of cognition that changes with age or can be changed by experience. This meaning includes most explanatory concepts invoked by cognitive theorists, including
Validating Theories of Intelligence
97
“structural” concepts. Since the goal is to explain performance by reference to processes, validating cognitive theory requires that one show relationships between performance and process, and this requires research designs and dependent measures that allow separate inferences about process and performance. It also requires process manipulations that influence performance. The belief that intelligence develops is based on the observation that as children age, their behavior becomes more complex and abstractly organized. The generic hypothesis of developmental cognitive theory is that at least some of the processes that underlie performance also become more complex and abstractly organized with age. The research strategy required to determine whether changes in underlying processes explain intellectual development must allow for the possibility that only some processes develop, and it must make provision for determining which processes do and which do not change with age. The fact of cognitive development and acceptance of the process/performance distinction require the use of the entire strategy outlined in Table I to validate a theory of intelligence. The strategy begins with three preliminary steps, the first two of which are judgmental. Step 1 is to choose an important intellective domain of investigation. As in all judgmental matters, importance lies in the mind of the investigator, but there are consensual constraints. Since Galton’s time, for example, few have supposed that sensory thresholds or simple reaction times reveal much about intelligence. Matters having to do with language, world knowledge, reasoning, or memory are now far more likely to be agreed upon as centrally important to intelligence. Having selected a domain of investigation, one must settle on some criterion problem(s). Most investigators settle on one, though the trend is toward the use of multiple performance problems. In part, this trend reflects an increased recognition that one should establish the generality of cognitive analyses (as will be discussed in the second half of this article). The third step is to establish that performance on one’s criterion problem(s) is correlated with age. Following these preliminaries, the research strategy begins in earnest at Step 4 (Table I) with a process analysis of criterion performance within narrowly restricted age groups. It continues, in Step 5 , with demonstrations that the processes identified in Step 4 change with age. In Steps 6 and 7, it moves to instructional experimentationdesigned to make the process theory meet the logical requirements of manipulative experimentation. A.
ANALYZE PROCESSES WITHIN AGE GROUPS
Even though one goal of cognitive theories must be to explain intellectual development, Step 4 calls for analyses performed within narrowly defined age groups. The purpose is to validate, independently of age, each process that accounts for any performance variability. Without such validity, no clear conclusions can be drawn from establishing procesdage relations, which is called for in
Earl C. ButterfEld et al.
98
TABLE I How to Validate a Process Explanation of Cognitive Development Step 1.
Choose an important cognitive domain.
Step 2.
Select criterion problem(s) that fairly represent performance in the chosen domain.
Show that performance on the criterion problem@)correlates with age. Step 3. So far, the work will have been judgmental (Steps 1 and 2) and descriptive (Step 3). Steps 4 through 7 are efforts after explanation. Step 4.
Step 5 .
Perform a process analysis of performance on criterion problem(s), within ages. A. Make process measurements that correlate with performance. B. Show correlations between independent measures of each process. C. Manipulate each process. D. Show that each process manipulation changes performance. E. Determine by multiple correlation whether the validated processes combine to account for all variance in criterion performance. If they do not, more process analysis will be needed (Steps 4A through 4D). Show that processes underlying performance change with age. Demonstrate correlations between age and each process measure. B. Using performance measures, demonstrate interactions between age and process manipulations. Collect concurrent process measurements. C. Determine by partial correlation whether the processes that correlate with age reduce the agelperformance correlation to zero. If they do not, more process analysis will be needed (Step 4).
A.
Step 6.
Teach children to process as adults, thereby raising their performance to the level of similarly instructed adults. If instructed children’s performance falls short of instructed adults’, check concurrently collected process measurements to see that instructions actually induced children to process as adults. A. If instructions failed to induce adult processing, revise them and try again. B. If instructions did induce adult processing, return to Steps 4 and 5 for further process analysis. C. If children’s and adults’ instructed performances are equal, but the instructions raised adult performance too, examine process measures to see that adults who contributed to the increase were using childish processing prior to instruction.
Step I.
Teach adults to process as children, thereby lowering their performance to the level of similarly instructed children. If the instructed adults’ performance lies above instructed children’s, use concurrently collected process measurementsto see that instructions actually induced adults to process childishly. A. If instructions failed to induce childish processing, revise them and try again. B. If instructions did induce childish processing, return to Steps 4 and 5 for further process analysis. C. If children’s and adults’ performance are equal. and the instructionslowered children’s performance, examine process measures to see that children who contributed to the lowering were using relatively mature. processing prior to instruction.
Validating Theories of Intelligence
99
Step 5 . Since age cannot be accelerated, reversed, or otherwise manipulated, ways must be provided to determine whether any process correlate of age arises from an unidentified confound of age. Step 4 calls for two such provisions: One is to establish the validity of each process within narrowly defined age groups; another is to produce and validate a process theory that accounts for all of the within-age variance in performance on the criterion problems used to study intellectual development. Having such a complete account allows, during Step 5 , determinations of which processes are directly correlated with age and which are correlated only because of their confounding with other processes. Such a complete account is also necessary to allow determination of which processes do not develop. A complete theory of intelligence will include concepts that are not developmental as well as those that are. Moreover, until a theory can account for all of the variance in its target performance measure(s), any other incomplete account can be claimed to be the basic account. Someone will always accept such counterclaims (Newell, 1973), although as long as any appreciable variance remains unaccounted, questions about which theory is basic or more general, elegant, or parsimonious can be given no disciplined answers. Only an exhaustive account of variance is immune to capricious challenge. An exhaustive account of variance is a basic account. Given two or more exhaustive accounts, disciplined considerations of elegance, generality, and parsimony become relevant. A complete accounting of performance variance within ages is necessary for full validation of a process theory, but it is not necessary to fulfill Step 4 before moving to Step 5 of the validation strategy. If it were a prerequisite, developmental studies could not yet be performed. Step 4 is included to emphasize that strong interpretations of developmental studies are possible only when all within-age variance has been explained. B. CORRELATE PROCESS MEASURES WITH AGE
The purpose of Step 5 is to determine whether a process changes with age. It also provides a test of the developmental completeness of a process theory. If the analysis upon which a theory builds is developmentally complete, then it will be possible to reduce performance/age correlations to zero by partialling out indices of processes that develop. Step 5 also provides information necessary to respond effectively to a question that inevitably arises in response to studies of the sort outlined in Steps 6 and 7. Such instructional studies have generally been done by investigators with a behavioral rather than a cognitive orientation. Usually, such studies have not been preceded by developmental process studies of the sort outlined in Step 5 . Rather, behavioral analysts take raising or lowering criterion performance as their goal, and they modify their instructional approach by intuition until the goal
100
Earl C . Butterfield et al.
is reached. Regardless of the utility of the goal, cognitivists may ask whether the behavior analysts’ instructional routines mimic or can be taken as a model of the normal course of development. Thoughtful behaviorists will say that the instructions stand only as a model of how development might normally proceed, but they will not assert that it is a model of how development does proceed. Then, it will often happen that the behaviorists’ work will be dismissed by cognitivists as developmentally irrelevant, particularly if the cognitive critics can think of some developmental fact to suggest that the behaviorists’ instruction might not exemplify a good model of normal development. Step 5 provides data to justtfy the assertion that the processes described in Steps 6 and 7 do in fact change in the normal course of development. Thus, if behaviorists who have used instruction in generalized imitation as a prerequisite to teaching language to severely retarded children had also shown that generalized imitation precedes language development, and that it accounts for normal children’s language acquisition, their work could be less readily dismissed by cognitivists as irrelevant to normal development. It might still be dismissed on the ground that normal development cannot be mimicked, but that would amount to a rejection of the possibility of studying development experimentally. Step 5 is stated in terms of chronological age (CA), but mental age (MA) can be a more appropriate index of developmental level. The strategy allows the use of MA as well as CA. In fact, the strategy in Table I is applicable to any sort of comparative research: cultural differences, personality differences, and sex differences. Thus, the study of sex differences would begin, in Step 4, with analyses performed separately for males and females, and it would proceed, in Step 5 , to comparisons between males and females. A more general expression of the strategy can be found in Butterfield (1978). C. ELIMINATE AGE DIFFERENCES WITH PROCESS INSTRUCTION
Cognitive theory in general is vulnerable to the criticism that its empirical bases are weak. It can fairly be said that the ties between the concepts of basic cognitive science and its data are tenuous (Anderson, 1976; Chi, 1976; Schank, 1976; Townsend, 1972, 1974). Developmental cognitive theory is only slightly less immune to this criticism than basic cognitive theory (Butterfield, 1978; Butterfield & Dickerson, 1976). Some argue that it is impossible with empirical methods alone to affirm any theory satisfactorily (Lachman, Lachman, & Butterfield, 1979; Reese & Overton, 1970; Weizenbaum, 1976). Nevertheless, the premise of Steps 6 and 7 is that applying the logic of manipulative experimentation to process explanations will greatly strengthen the ties between cognitive theory and data. In the f m t place, process instruction that affects performance shows most directly that the process is plausible. Perhaps more importantly, applying the full instructional logic provides the strongest possible basis for claims about the normal course of cognitive development.
Validating Theories of Intelligence
i
101
The logic of Steps 6 and 7 is that instructed processes can be invoked as explanations of age or other group differences only if identical instructions are applied to various (age) groups, and then only if the instructions leave the groups performing at identical levels. The effect of the instructions can be to raise the performance of the younger group (Step 6) or to lower the performance of the older group (Step 7). However, if after instruction reliable differences remain between the age groups, then the processes affected by the instructions may not be responsible for differences between the ages under uninstructed conditions. In Step 6, where instructions are intended to improve poor performance, the notion is that older groups who naturally perform better are already using the instructed processes, but the younger groups who perform poorly are not. Therefore, the more accurate group should benefit little or not at all from the instructions, but the less accurate group should benefit greatly. Conversely, in Step 7, where the instructions are intended to eliminate the processing thought to account for adults’ accurate performance, the inaccurate children should be impaired relatively little, since they are presumably not using the target processes anyway. When the goal is to account for young children’s inaccurate performance, the instructional approach requires that older people be instructed along with the younger ones. In its most definitive form, which is not yet attainable, the instructional experiment leaves the performance of either the oldest (Step 6) or youngest (Step 7) group unchanged, and the performance of all groups identical. Implementing such an experiment would require a complete process understanding of the development of some intellectual performance, as well as accurate age norms specifying when the relevant processes have developed as completely as they will without special tuition. Given that there is no process analysis that completely accounts for any cognitive performance, producing identical group performance is improbable: Older groups will likely perform better than younger ones even after instruction, unless ceiling or floor effects are encountered. Moreover, there is ample evidence that fully mature individuals do not process optimally, so that older groups will almost always benefit from process instructions that are not carefully constrained by a knowledge of how far development carries people toward optimal processing. As long as the oldest group benefits, the process account of development is incomplete, even if the process analysis of within-age performance is complete. For these reasons, there must be a constant interplay and recursiveness between the various steps in the research strategy, and rules to guide this interplay are given in connection with Steps 6 and 7 (see Table I). Instructional experiments cannot be interpreted clearly unless unobtrusive measures are taken of the instructed processes. The goal of such experiments is to change performance by manipulating processes; especially when process analyses are incomplete, instruction can influence process without influencing performance. In order to determine whether a failure to change performance results from a failure to change the target process, unobtrusive process measures
102
Earl C . Butterfield et al.
should be taken during instruction. Also, when instructions designed to improve the performance of younger people also improve the performance of older people, unobtrusive process measures taken prior to instruction are needed to determine whether the older people who benefited did so because they were processing relatively youthfully before instruction. Whenever the effects of instructions are assessed with a posttest, process measures must be taken then, to assure that the subjects continued to use the instructed processes following the termination of instruction. Few intellective problems allow any, let alone unobtrusive, measurement of the processes required for their accurate performance. Cognitive scientists have invested heavily in inferential procedures and lightly in developing more direct measures of cognitive processes (Belmont & Butterfield, 1977). Until this lamentable trend (Newell, 1973) is reversed, satisfactorily complete instructional tests of developmental cognitive theory will be few indeed. Moreover, the few tests will be performed with criterion procedures that have been around for a long time, because only for well-studied problems have underlying processes been identified and the necessary range of unobtrusive measures been developed. Cognitive theorists now study criterion performances that are markedly different from what they used to be, so that any investigator who tries seriously to follow the strategy outlined in Table I may be criticized as old-fashioned and outdated with respect to his performance measures. Our best advice is to turn the other cheek and persist, because we see no way other than the strategy in Table I to produce valid developmental cognitive theory.
111. Illustration of the Strategy for Studying Intellectual Development We will use our own research to illustrate the strategy outlined in Table I. No other work seems as suitable for this purpose, although the programmatic studies of memory by Ann Brown (1975, 1978; Brown & Barclay, 1976; Brown & Campione, 1978; Campione & Brown, 1977), those of imagery by William Rohwer (1973), James Tumure (Taylor & Turnure, 1979; Turnure, Buium, & Thurlow, 1976), and John Borkowski (Kendall, Borkowski, & Cavanaugh, 1980; Kestner & Borkowski, 1980), and those of the balance beam problem by Siegler (1976; Klahr & Siegler, 1978) could be used to illustrate many of the substeps enumerated in Table I. The entire strategy outlined in Table I seems to have been satisfactorily approximated only by programmatic efforts of closely associated investigators. Having searched the literature extensively (Belmont & Butterfield, 1977), we find that no amount of research in a particular cognitive domain, when spread across many laboratories, has managed to approach a satisfactory representation of the strategy in Table 1. Two of us (Belmont and Butterfield) began to plan the research that we will
Validating Theories of Intelligence
103
use here for illustrative purposes in 1967, several years before we had fully formulated all aspects of the strategy outlined in Table I. Steps 1 through 3 occurred to us immediately, as we suppose they must to any investigator who contemplates a new investigative effort intended to clarify intellectual development. Table II shows that the first report of research from this program (Belmont & Butterfield, 1969) satisfied the requirements of Steps I through 3 and included instances of the sort of work called for by Steps 4A, 4B, 4C, 5A, and 6A. The next fourreports (Butterfield, Belmont, & Peltzman, 1971; Butterfield, Peltzman, & Belmont, 1971; Buttefiield & Belmont, 1971; Kellas & Butterfield, 1971) concentrated on within-age process analysis (Steps 4C and 4D).Then came six reports (see Table 11) that combined instructionalwork of the sorts called for in Steps 6 and 7 with further within-age analysis (Step 4) and correlation of age with process (Step 5 ) . Shortly before the last of these reports (Butterfield& Belmont, 1977), we finished formulating the strategy outlined in Table I. The most recent report in this series (Butterfield, 1978) described our first efforts to assess the completeness of our process account of performance in our domain of investigation (Step 4E) and of our account of performance development (Step 5C). The chronology depicted in Table I1 suggests that implementing the strategy is a back-and-forth affair, characterized by moving recursively among the strategy’s steps. The last column of Table I1 lists the pages in this article where descriptions are given of work that illustrates each step of the strategy. Some of the illustrations are drawn from the published reports listed in Table 11; others are from previously unpublished research. A. SELECI’ION OF AN INVESTIGATIVE DOMAIN
In 1967, Belmont and Butterfield began their program of research into the information-processing aspects of intelligence. They satisfied Step 1 of the strategy outlined in Table I by judging that the laboratory study of children’s memory functions would reveal intellectively important strategies for processing information. In part, memory seemed a suitable investigative domain because the science of mnemonics offered solid background data about normal adults and a wide range of methods that could be elaborated to expose the developmental character of information processing. Reviews of comparative and developmental research on both long-term memory (Belmont, 1966) and short-term memory (Belmont & Butterfield, 1969) showed that forgetting rate does not vary appreciably with either age or intelligence, so the research was focused on the relatively directly measurable processes involved in information input and retrieval. B. PROBLEM SELECTION
In order to provide separate measures of input and retrieval processes and to make input measures operationally independent of performance measures, Bel-
TABLE II. Steps of a Research Strategy to Validate an Explanation of Cognitive Development That Are Illustrated (X)by Experiments by Belmont, Buttefield, and colleagues
step I
103
step 2
103
sap3 X
X
10s 106
step 4
4A
X
X
Lo7
48
4c
X
X X
X
X
I11
X
X
X
X
X
X
X
X
114
X
X
116
4D 4E
X
117 120
steps
5A
X
X
X
X
x
120
X
x
121
x
122
5B
X
X
X
X
X
X
x step 6
6c
X
X
6A 6B
X
X
X
X
X X
X
X
X
X
X
stcp7
7A
m 7c
X
X
123
Validating Theories of Intelligence
I05
mont and Butterfield selected variants of subject-paced list recall procedures, reported first by Ellis and Dugas (1968), as the memory problems to be analyzed. As a person paces his or her way through a list of words, letters, or pictures, the time following each successive item is recorded. When a subject presses a push-to-see button, the first stimulus in a list appears for .5 seconds. When this stimulus disappears, a timer is started, and it runs until the next time the subject pushes-to-see. This second button-push records the time since the offset of the first stimulus, presents the second stimulus for .5 seconds, resets the timer, and starts again. This process is repeated until all stimulus items have been presented, and all interstimulus pauses are recorded. We used the subject-created pause times to make inferences about input processes. We sometimes supplemented these temporal data with overt rehearsals and introspective reports. We used several recall requirements with the subject-paced input procedure, including probes for the location of particular items, free recall, serial recall, and “circular” recall (described below). With each of these requirements, we have used response latencies or interresponse times to assess retrieval processes, and we have supplemented these data with examinations of the distribution of errors across serial positions. The procedures are thus rich with process measures, all of which can be taken on every trial of an experiment, and most of which can be taken unobtrusively. C. CORRELATE PERFORMANCE WITH AGE
It took little research to satisfy Step 3 (Table I). Even in 1967, a huge number of research articles reported age differences in various memory performances. The only thing we could not determine from the literature was whether performance measures derived from subject-paced memory procedures correlate with age. We have since shown that they do, for each of the several recall requirements we have studied. For example, it can be seen in Fig. 1 that subject-paced free recall increases with age. These data were derived from the performance of four groups of 40 children, ages 8, 10, 12, and 14. Individual children paced themselves through 15 different 9-word lists, which they then recalled in whatever order they chose. Figure 1 shows that each 2-year increment in age is associated with an increment in recall, especially across the first five serial positions. Circular recall also increases with age. By circular recall, we mean recollection of the last few items from a list before recollection of the rest. For example, in 3/5 circular recall of lists eight words long, words 6 , 7 , and 8 are to be recalled in order before words 1,2,3,4, and 5, which are also to be recalled in order. We recently administered subject-paced 3/5 circular recall to 80 people who ranged in age from 10 to 20 years. The correlation between age and number of words recalled correctly was .57 ( p < .01). Correlations of this magnitude are entirely typical of studies of age and memory performance. While the age/performance
106
Earl C . Butterfiehi et al. 100r
‘
I , . , , , , , , , 1 2 3 4 5 6 7 8 9 POSITION
Fig. 1 . Mean percentage correct recall at each of nine serial positions across 15 trials offree recall by 8- (open triangles), 10- (open circles), 12- (closed triangles). and 14-year-old (closed circles) children. (Afer Butterjield & Belmont, 1977, Fig. 7.4.)
relations are almost always statistically significant, they also leave enough unexplained variance in memory performance to allow within-age studies of the relations between process and performance. D. ANALYZE PROCESSES WITHIN AGES
None of the five sorts of studies listed under Step 4 (see Table I) produces by itself a process analysis of problem performance, but together they provide ample bases for inferring processes that underlie problem performance and for judging the completeness of the inferential analysis. Being comlational, Substep 4A provides no evidence for inferring that variations in a process cause variations in performance, but it can provide ample bases for causal hypotheses and for manipulative research that might justify causal inferences. Substep 4B embodies the cognitive science criterion of converging validation (Garner, Hake, & Erikson, 1956). Since no underlying process can be measured directly, process inferences must be validated by converging measurements. Substep 4C calls for experimental manipulations of identified processes. Substep 4D requires that such manipulations be shown to influence performance. Especially in the early stages of the analysis of a performance requiring the coordinated use of several processes, some of which have not yet been isolated, one can manipulate a process without influencing performance. In such early stages, successful manipulation of the process, even without consequent performance changes, is enough to justify retaining the process in one’s model. Eventually, however, it must be shown, as specified in Substep 4D, that performance changes result from manipulation of every process in one’s model. Substep 4E calls for a multiple regression analysis of the amount of performance variance explained by measured processes. It is one of the strategy’s several checks on the completeness of an ongoing analysis. Completeness checks are included in each step because it is
Validating Theories of Intelligence
107
unreasonable to require a complete process analysis (Step 4) before undertaking correlational (Step 5 ) and manipulative (Steps 6 and 7) developmental research, and the results of developmental research can provide important clues to guide further analysis within ages (Butterfield & Belmont, 1977; Butterfield, Wambold, & Belmont, 1973). 1 . Correlate Process with Performance To illustrate Step 4A, we will present data to show that three process measures predict short-term recall performance within narrowly constrained age groups. The process measures were derived from temporal features of input and output activity, and the performance measure was percent correct recall. Belmont and Butterfield (1969) used a position probe recall problem to establish a relation between process and performance measures. Having paced herself or himself through a list of consonant letters, the subject’s job was to expose a probe item (selected randomly from the list’s consonants) and to indicate its position by pressing one of the transparent windows covering each of the positions at which the letters were presented during list input. Ten 20-year-old college students studied 27 lists constructed by selecting nine consonants at random from a pool of 16 consonants. Ten 1 1-year-old sixth-graders studied 21 similarly constructed lists of seven consonants. On the hypothesis that the subjects’ pauses during self-paced input would reflect rehearsal, Belmont and Butterfield selected the five subjects from each age group who paused the most (High) and the five who paused the least (Low) during input. The two leftmost panels of Fig. 2 show the mean pause times following each consonant for these High and Low groups. The middle panels show the percentage correct recall at each position, and the right panels show the latency from probe onset until response, for correct responses only. The High subjects were selected because their total pause times were long, but Fig. 2 shows that pauses following the middle items in the list contributed much more to the total pause times than did pauses following the beginning and end items. From this pattern of pausing for the High subjects, Belmont and Butterfield inferred that even those people who rehearsed most do not rehearse for the final items in a list for which they will be tested by position probe. Therefore, the percent correct functions for the High and Low subjects should differ primarily at the middle and beginning positions, which is what the middle panels of Fig. 2 show. Within both age groups, pause time, which is a measure of the rehearsal process, predicts recall accuracy at the middle and early positions. Mean correct response latency (right panels of Fig. 2) also varies systematically across serial positions, in much the same way that input time does, suggesting a relation between input and output processes. The data show a relation between process and performance within both age groups, but they also indicate that the patterning of pauses as well as total pause time might reflect interesting processing.
Earl C. Butfefleld et al.
108
(COLLEGE STUDENTS) PERCENT
loor CORFECT RESPONSES
20
-
5r
CORRECT RESPONSE UTENCY
L
0
0
(SIXTH GRADE 1
'OF 8
6l
?
80
4
*tiEGGL
O
1
3
5
7
9
O
1
3
5
7
9
POSITION
Fig. 2 . Mean pause time, percentage correct responses, and correct response latenciesfor college students and sixth graders who showed long (open circles) and short (closed circles) total pause times. (After Belmont & Butterfield, 1969, Fig. 10.)
Results like the foregoing led us to distinguish two aspects of input processing: effort, which we index with total pause time, and strategy, which we index with the form of pause pattern across serial positions. Since patterns with longer total times have greater variability across positions, we study pattern form only after standardizing the pause times from each trial. For each trial of every subject, we use the observed mean and standard deviation to calculated standardized pause times with mean = 4.0 and standard deviation = 1.0. To compare the shapes of these standardized pause patterns, we use an omega square statistic (Dodd & Schultz, 1973).Omega square (a2) is derived from an analysis of variance calculated on a matrix of standardized pause times. The columns of the matrix are serial positions and the rows are the standardized patterns to be compared. From an analysis of variance of such matrices, 0 2
=
SS,, SS T
+ (dfapx MS error) + (n x MS error)
where sp symbolizes serial positions, T symbolizes total, and n is the number of patterns being compared. The limits of o approach 1.OO, when the compared patterns are identical, and - 1.OO, when the patterns are thorougw; dissimilar.
+
Validating Theories of Intelligence
109
We used standardized pause patterns and o * in a recent and previously unreported study to correlate accuracy with strategy. We required 48 college students to recall lists of nine words in two ways designed to produce different pause patterns. For the first 14 and last 7 of 35 lists studied, the subjects were to recall the words in the order 9 5678 1234 (called 1-4-4). This recall requirement led them to pause longer following the fourth and eighth words than following any of the other words. For trials 15 through 28, the subjects were required to recall in the order 789 456 123 (called 3-3-3). This led them to pause longest following the third and sixth words. We divided the 48 subjects randomly into two groups of 24, so that we could use replication by independent groups to assess the reliability of any observed relations between strategy and recall. We then selected the eight most and eight least accurate subjects from each replication group, by averaging the number of words recalled correctly across all 35 trials. The eight High accuracy subjects from Group 1 and Group 2 recalled a mean of 5.83 words (65%) and 6.31 words (70%) per trial, respectively. The two Low groups had means of 3.23 (36%) and 3.60 (40%). Thus, the High subgroups were nearly twice as accurate as the Low subgroups. For each of the four subgroups, we averaged pause patterns from Trials 26 through 28 (last 3-3-3 trials) and 33 through 36 (last 1-4-4 trials). The mean pause times thus obtained for each output order are shown in Fig. 3. The pause patterns for both High accuracy subgroups have higher peaks at the expected points than do the pause patterns of the Low accuracy subgroups. Since the total pause times of the High accuracy subjects were greater than those of the Low accuracy subjects, we used standardized pause times to study the relation of input strategy to accuracy. Since the High group's raw pause patterns (Fig. 3) fit ow expectations for appropriate 9r
1-4-4
1-44
-6
-4
-2
Fig. 3 . Mean pause times from two recall requirements ( I - 4 - 4 and 3-3-3) for high- (solid lines) and low- (dashed lines) accuracy subjecrsfiom two independent groups ( I and 2 ) .
Earl C . Butterfield et al.
110
processing on our two recall requirements, we used their standardizedpatterns as standards of appropriate processing. To keep the standards independent of the data to which they were compared, the standardized patterns from all subjects in Group 1 were fitted individually to the averaged data from Group 2 High subjects, and vice versa. Thus, every standardized pause pattern for every subject in Group 1 was fitted to the mean standardized pattern of Group 2 High subjects on Trials 33 to 35 (our 1-4-4 standard) and on Trials 26 to 28 (our 1-3-3 standard). The High and Low subjects’ o2statistics were averaged separately. If the High subjects fit the appropriate pattern more closely than the Low subjects, then their mean o2should be higher for trials on which the standard matched the recall requirement (1-4-4for Trials 1 to 14 and 29 to 35 versus 3-3-3 for Trials 15 to 28). Both Highs and Lows should have had low o2when the standards did not match the requirements. Figure 4 shows that the High subjects from both Groups 1 and 2 had greater w 2 than both Low groups when standard and requirement match. The nonmatching data were comparably low for both groups. We conclude that the process measure of strategy (standardized pause pattern) predicts performance (recall accuracy). In another previously unreported study, we examined the correlation between output processes and recall accuracy by administering 10 trials of 3/5 circular recall during which subjects were required to recall words in the order 678 12345. Total number of words recalled on Trials 6-10 served as the performance measure. We taperecorded the subjects’ recall, and selected the first two trials for which a subject recalled nothing but words from the list and recalled at least two of the last three words before recalling at least two of the first five words. These recordings were used to derive a measure for each subject of retrieval time for 1-4-4 ,3-3-3 , - -n
I 1-4-4
N
2 6n
-
a
az A 2:
P -
i
O-
q
I
1-7
I
I
1
I
1
8-14 15-21 22-28 29-35
TRIALS Fig. 4 . Mean similarity to standard pause time parierns for high- and low-accuracy subjects from two independent groups ( I and 2 ) . See text for explanatwn of recall requirements (1 - 4 - 4 and 3 -3 -3) and of matching and nonmatching.
Validating Theories of Intelligence
111
rehearsed material: the time from end of last word recalled from positions 6-8 to the beginning of second word recalled from positions 1-5. Four groups of 20 subjects were studied: CA 10, 11, 12, and 20. Correlational analyses within the age groups showed negative relations between overall accuracy and retrieval time for rehearsed words. For CA 10, 11, 12, and 20, the correlations were - .29, -.57, -.20, and -.30, respectively. We infer that speed of retrieval of rehearsed information predicts recall accuracy within ages.
Summary. Step 4A of our research strategy calls for the correlation of process with performance measures. To illustrate the implementation of Step 4A, we described three experiments. The first experiment, by Belmont and Butterfield (1969), showed that greater effort, as indexed by longer total pause time, is associated with greater recall. The second, previously unreported experiment showed that rehearsal strategy, as indexed by the standardized form of pause patterns, also predicts accuracy. The third experiment, also previously unreported, showed that faster retrieval of rehearsed information is associated with greater recall. These three process measures-ffort, strategy, and retrieval speed-will figure prominently in our subsequent illustrations of the implementation of the strategy required to show that a cognitive process develops. 2. Correlate Independent Measures of Processes Step 4B calls for the calculation of correlations between independent measures of each process. Part of the logic of Step 4B is the same as the logic of convergent validation: Unless a process can be shown to be measurable in two or more ways, an investigator cannot claim confidently that the process inheres in people instead of in a single measurement procedure. However, the logic of converging operations does not require that the various measurements be taken from the same people and that they be correlated. The logic for this requirement has been developed by Underwood (1975) and illustrated with experiments by Butterfield and Dickerson (1976). By Underwood’s logic, Step 4B is an individual differences test of process validity. Individual differences tests require that one measure of a process share appreciable variance with another measure of the process. Unless differences between individuals correlate across measures, the logic asserts that no important psychological process has been demonstrated. Our illustration of how to implement Step 4B is a previously unreported study of the correlation between two independent measures of input strategy. The two measures are pause time patterns and overt verbalizations. Fifteen 11-year-olds were required to study 30 lists for free recall. Each list was nine words long, and no word was repeated. The children were instructed for free recall, and for the first 20 trials they performed their study covertly, while we measured pause time. Immediately following the twentieth list, each child was asked how he or she had gone about learning it. The child was then instructed to show how he or she had
Earl C.Rutterfield et al.
112
studied the twentieth list by working through it again, exactly as during the first time, but saying aloud what had only been thought before. This verbalization procedure was used on each of the remaining 10 trials. A child first studied a list silently, and then worked through it again, trying to say exactly what he or she had thought the f i s t time through. In this way, each child produced two pause time curves for each of the last 11 lists (20 through 30); one with overt verbalization and one without. Since there were 15 subjects, there were a total of 165 lists for which verbalizations were taperecorded. To assess the effects on pause time of having to verbalize each list during a second time through, each child's mean pause time at each position was calculated for the last five trials (16 to 20) prior to introduction of the verbalization and for the first five trials (21 to 25) thereafter. For Trials 21 to 25, two average pause time curves were obtained, one for the covert and one for the overt productions. The three group average curves are shown in Fig. 5 . The pause time functions prior to introduction of the overt procedure (trials 16 to 20) do not differ qpreciably from pause times on the covert trials after introduction of the overt procedure (trials 21 to 25). The pause times taken while verbalizing Trials 2 1 to 25 are longer, but fall very much in the same pattern. We conclude that introducing the overt procedure did not importantly influence what the children did on subsequent covert trials, even though pause times were longer during verbalization. The taperecorded verbalizations were used to divide the 165 trials into six mutually exclusive categories of input strategy: Labeling, in which the child said each word as it appeared, but never said it again; Building, in which each word was said as it appeared, and again after all subsequent words (one; one-two; one-two-three; etc.); Building with Terminal Labeling, in which the child built from the beginning of the list, but only labeled the last word or two; Grouping, in which the child used building rehearsal for two or more isolated groups of words (one; one-two; one-two-three; four; four-five; four-five-six); Grouping with
z
'.i 1.o
I
I
1
2
1
3
1
I
I
I
I
J
4
5
6
7
8
9
POSITION Fig. 5. Mean pause times for coven study on Trials 16-20 (triangles),for overt stUrty on Trials 21-25 (squares), andfor overt study on Trials 21-25 (circles) of afree recall experiment.
113
Validating Theories of Intelligence
4
WITH TERMINAL LABELING
3
-
2
Vr 0
BUILDING WITH TERMINAL LABELING
F2 W
v,
q,
4
2
2
3
1
3
5
7
9
1
3
5
7
9
POSITION
Fig. 6. Mean covert pause times on trials classified on the basis of overt demonsrrarion of recollected study method.
Terminal Labeling; and Other, in which some or all of the words were said more than once, and again following the presentation of other words, but the verbalization pattern fit none of the preceding categories. Two judges independently categorized the recordings. They agreed on 94% of their categorizations. To examine the relationship between input strategy and pausing, we averaged the pauses taken during the covert (first) trial of each list in each category. That is, the categorizations were based on verbalizations during the second NII through each list, and the averaged times came from the first run through. The mean pause time curves for each category are shown in Fig. 6, where it can be seen that Labeling resulted in a low flat function, as it should have. The pause pattern for Building increased systematically from the first to the last word, again confirming expectations from the overt verbalizations. The verbalizations of most subjects who used Grouping indicated that each rehearsed group included three items. A minority of subjects grouped by twos or fours, but the majority pattern dictated the average seen in Fig. 6. Most subjects who used Terminal Labeling with Grouping grouped by threes. A minority grouped by twos, and the average pause pattern shown in Fig. 6 is consistent with this distribution of strategies. Most subjects who used Terminal Labeling with Building built either seven or eight items and labeled two or one. A minority built six or seven and labeled three or two. The mean pause pattern in Fig. 6 for Building with Terminal Labeling is consistent with this distribution of verbalizations. The Other category was a diverse mix of active rehearsal and labeling, which is reflected in
114
Earl C. Butterjkki et al.
the irregularity of the longer pauses in the Other category of Fig. 6. We conclude that the pause patterns and overt verbalizations are well-correlated independent measures of rehearsal activity. 3. Manipulate Processes According to the strategy outlined in Table I, the plausibility of a process is only incompletely established by correlating independent measures of it. The strongest evidence for the plausibility of a process comes from manipulating it, as called for by Step 4C (Table I). Depending upon how completely an investigator has analyzed the processes underlying performance on a criterion problem, these manipulations may be crude, producing gross effects, or they may be precise, producing subtle effects. The experiments used here for illustrative purposes were conducted after our understanding of the processes underlying probe recall was relatively complete. The experiments concern retrieval processes. The flow chart in Fig. 7 is a process model of probe recall as it was understood by Butterfield and Belmont (197 1). Among other things, the flow chart expresses the hypothesis that effective information processors conclude their study of a list (at Box 3, Fig. 7) with information about items from the early portion of the list in a longterm memory store and information about the terminal items of the list in an input buffer or short-term store. With information in these two stores, a probe is presented (ExperimentalEvent 2, Fig. 7). In response to this probe, the subject first transfers a representation of the terminal items to an output buffer (Box 4) and represents the probe item in the input buffer (Box 5 ) . The subject compares the contents of the input and output buffers (Box 6) and responds if there is a match between the two (Box 8). If no match occurs, the subject transfers the representation of the earlier items of the list to the output buffer (Box 7) and compares them to the probe representation in the input buffer (Box 6), responding when a match is made (Box 8). One implication of this analysis of output processes is that it should take longer to respond correctly to items retrieved from the long-term store than to those remaining in the input buffer at the end of acquisition. Thus, people who have input eight items by rehearsing the first four and merely labeling to the last four should take longer to respond to a probe from the first four than from the last four. Figure 8 shows the correct response latencies obtained from seven college students who used such a 4-4 strategy for lists of eight consonants. Every subject took longer to respond to the first four than to the last four items. Moreover, the group average of the seven subjects shows that there is a systematic increase in latency for the first four items, but not for the second four (see Fig. 8). Butterfield and Belmont ( 1971) reported six experiments that explained the pattern of response latencies in Fig. 8 by manipulating all of the output processes included in Fig. 7. For example, Box 6 implies that the number of items in the
Validating Theories of Intelligence
115
Experimental Event 1: A list is presented for input. The Subject:
first items to be stored
By Labeling, represents terminal items in input
Experimental Event 2: Presentation of t h e probe item whose position is t o be recalled. The Subject:
By Attention, represents probe item in input buffer
Transfers representation of terminal items from input buffer t o output
1 contents
Serially compares contents of input and output buffers
match
Transfers ordered representation of remainder of list from LTS
in output buffer to
Fig. 7 . A process model of probe recall when one group of items is rehearsed. (See Fig. 16 for model when more than one group of items is rehearsed.)
input buffer when study is completed controls the time before beginning the search for items transferred to the long-term store. Butterfield and Belmont tested this implication by having college students rehearse four consonants, and then label but not rehearse zero, one, or two additional consonants. Thus, there should always have been representations of four consonants in long-term memory, but the number represented in the input buffer at the conclusion of input processing
Earl C. Butterfield et al.
116
.[P
3
3
-
l2
9% , , ,
1
,d%{
1
1 4 2 d
-
1
GROUP MEANS I3
‘I.”& ‘
2
4
i. ....-..1 4
s
e
1
3
8
7
POSITION
Fig. 8. Median correct response laiencyfor seven people who used a 4-4 input strategyfor probe recall, and the group (N = 7 ) mean median latency. The differences between the open circles and closed circles are mi signifcant, and m a y be disregarded. (Afer Butterjeld & Belmnr. 1971. Fig. 2 . o 1971 by the American Psychological Association. Reprinted b y permission. )
should have varied between zero and two. Figure 9 shows a systematic elevation in the level of correct response latency across the four rehearsed items as the number of labeled items increased from zero (4-0) to one (4-1) to two (4-2), thereby verifying one of the implications of the model in Fig. 7. 4 . Change Peflormance by Manipulating Process Step 4D is a safeguard against retaining in one’s model processes that make no difference for performance. While epiphenomena may not abound in cognitive theory (Butterfield, 1978), one must guard against the possibility that modeled processes are functionless concomitants rather than causes of performance. Step 4D is intended to insure that an investigator’s analyses have identified processes that cause performance variability.
Validating Theories of Intelligence
117
A 4-4 2.5 v)
a
4- 2
z
4-1 v)
1.5
4-0
tr
1.0 1
2
3
4
5
6
POSITION Fig. 9. Mean correct position probe response latency for four rehearsed items followed by zero (4-0). one(4-I). or hvo (4-2) nonrehearsed items.(Afer Butterfield & Belmont, 1971, Fig. 6 . ) The points designated 4 - 4 are group means from Fig. 8.oAmerican Psychological Association.
In the early stages of an analysis, process manipulations might not change performance, because the effectiveness of any one (or group of) process(es) can depend upon the use of other processes. The following example of how to implement Step 4D illustrates this possibility, thereby arguing for continuing an analysis until it is reasonably complete. Butterfield et al. (1973)reported process manipulations based on the model of probe recall presented in Fig. 7.Mildly retarded adolescents were given a pretest prior to instruction about how to perform a six-item probe recall problem. They recalled inaccurately from both primacy (positions 1-3) and recency (positions 4-6) portions of the pretest lists (see Fig. lo). Following the pretest, some of the retarded adolescents were instructed in input processing alone (Boxes 1-3, Fig. 7),while others were instructed in input and output (Boxes 1-8, Fig. 7). Following instruction, both groups recalled more accurately than during pretest, and the recall gains were greater for the group that received instruction in all of the processes (see Fig. 10). We conclude that both input and output processes influence performance and that more complete process analysis allows greater instructional control of performance. 5 . Multiply Correlate Processes with Pevormance
Step 4E is a check on the completeness of a process analysis. It calls for calculating a multiple correlation between every process measure and performance. The demanding aspect of this step is that it requires measures of each process. It is not enough to implement manipulations that allow process inferences; one must measure process use. To date, our analyses have identified three processes that predict recall accuracy when taken singly. Input processes are reflected by the form of the strategy
Earl C.Butterfield et al.
118
INPUT INPUT
+
OUTPLlT
,Kx)
laor 80
.
m0
t
PRIMACY
I-
--I:
RECENCY PRlMlvn
RECENCY
Fig. 10. Pretest (open circles) and posnest (closed circles) mean percentage correct for primacy and recency by retarded people instructed about input or about both input and output. (After Butterfield et al., 1973, Figs. 3 and 4 . )
and the amount of effort invested in it. Output processes are reflected by retrieval time for items from the long-term store. To obtain multiple correlations of these three processes’ indices with recall accuracy, we administered 10 trials of 3/5 circular recall of lists of eight unrelated words to 20 18-year-old high school students. To index Effort, we used mean pause time per word on Trials 6-10. To secure a standard with which to index Strategy form, we instructed an independent group of 10 18-year-olds to rehearse the first five words cumulatively and to say simply the last three words once each. Following 25 trials of practice using this building-with-terminal labeling strategy, in preparation for 3/5 circular recall, we collected input pause times for one trial. These times were standardized separately for each subject, and mean standardized time pattern was calculated for the group. This pattern was fitted, using 0.3, to each of the uninstructed subject’s standardized pause patterns on Trials 6 through 10, and the mean of resulting five o2scores was taken as the index of each subject’s approximation to the appropriate input strategy for 3/5 circular recall. To measure Output, we taperecorded subjects’ recall. We selected recordings of the second trial from Trials 3 through 10 for which the subject said nothing but words from the list being recalled, and for which the subject recalled at least two of the last three words before recalling at least two of the first five words. For this trial, we measured the time from the end of the subject’s verbalization of the last word recalled from the lists’ last three words to the beginning of the verbalization of the second word of the first five from the list. This Output Time is an index of the time to retrieve words that should have been rehearsed and stored in long-term memory. Our performance measure was the number of words recalled on trials
Validating Theories of Intelligence
119
6-10, which could have been as great as 40. The mean number of words recalled by the 20 subjects was 32.0. We entered the three process variables (Effort, Strategy, and Output) as predictors in a stepwise multiple regression. F tests showed that each process measure added significantly (p€.O5) to the prediction of accuracy, and together the three accounted for 56% of the variance in recall accuracy ( r = .75). We conclude that our process analysis has moved a fair way toward completion, but we still need to improve our measures of identified processes or to identify other processes. We wish we knew of comparable analyses for other criterion problems, so that we could assess the completeness of this particular analysis relative to others. Our impression, untestable though it is, is that the analysis is relatively complete. 6 . Summary and Conclusions None of the five approaches listed in Step 4 is sufficient by itself to validate a within-age process analysis, but taken together they provide reasonable assurance of the validity of any process. Thus, we are reasonably confident of the validity of the three processes identified in connection with our several variations of self-paced short-term memory procedures. Besides the evidence cited above, other data validate the total time measure of Effort, the standardized pause time measure of Strategy, and the interresponse time measure of Output: Effort correlates with accuracy (as required by Step 4A) and with amount of rehearsal as determined by quantification of overt verbalizations during input (4B); it is manipulable with incentives and by direct instruction (4C); lessening effort with instruction lowers performance and raising effort increases performance (4D); and the total time index of effort contributes significantly to multiple prediction of performance by process measures (4E). Strategy indices correlate with recall accuracy (4A) and with quantification of overt verbalizations during input (4B); manipulating strategy so as to match recall requirements improves accuracy, whde manipulating it to mismatch recall requirements decreases accuracy (4C and 4D); and the standardized pattern measure enters significantly into multiple predictions of performance by process measures (4E). Output measures correlate with accuracy (4A); they are manipulable in ways that affect performance (4C and 4D); and the interresponse time measure enters significantly into the multiple prediction of recall accuracy (4E).
We conclude that each of these processes can be correlated with age with little risk that any resulting correlations will be due solely to some confound with age. The purpose of within-age analyses is to validate processes fully enough to counter the possible claim that any processlage correlation results from some
120
Earl C. Butterfield et al.
unidentified variable that is also correlated with age. Within-age analyses do this by showing that the process predicts performance independent of age. However, it should be recalled that until within-age analysis has accounted for all of the variance in performance, even processes that have gained validity in all five of the ways specified in Step 4 might appear valid only because of their correlation with some unidentified process. Our research on memory processes indicates that we can proceed to developmental studies with some cushion of validity, since each of our process measures has substantial and diverse evidence of validity within ages. Nevertheless, our process measures do not account for all variability in performance, so we must remain alert to the possibility that an entirely different set of processes provide a more valid account of short-term memory as we have measured it. E. RELATE PROCESSES TO AGE
Armed with evidence from Step 4 for the validity of one or more processes, an investigator following our strategy would ask whether the process(es) change with age. Step 3 will have shown that performance changes with age, but not all processes identified within ages need develop. Step 5 is designed to determine which processes account for the development of performance shown in Step 3. 1 . Correlate Age with Process Measures
In order to correlate our process measures with age, as called for in Step 5A, we tested 20 children of CA 10,20 of CA 11, and 20 of CA 12 using the procedures described above for 18-year-olds (see Section III,D,5). Nine of the 60 younger subjects did not recall accurately enough to meet our criteria for calculating Output Time (Section III,D,5), so we were left with 51 younger subjects, whose data we pooled with that of the 18-year-olds, giving a total of 71 people for whom we could correlate each process measure with age. For these 71 people, age accounted for 27% of the variance in recall accuracy ( r = .51, p