ADVANCES IN THE STUDY OF BEHAVIOR V 11, Volume 11 (v. 11)

Advances in THE STUDY OF BEHAVIOR VOLUME 11 Contributors to This Volume ABRAM AMSEL R. J. ANDREW AND& CORNET DAVID C...

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Advances in

THE STUDY OF BEHAVIOR VOLUME 11

Contributors to This Volume ABRAM AMSEL R. J. ANDREW AND& CORNET DAVID CREWS MICHAEL DOMJAN GUNTER EHRET PIERRE JOUVENTIN JOHN R. KREBS DONALD E. KROODSMA PIERRE LE NEINDRE PASCAL POINDRON MARK STANTON

Advances in

THE STUDY OF BEHAVIOR Edited by JAY S. ROSENBLATT Institute of Animal Behavior Rutgers University Newark, New Jersey

ROBERTA. HINDE Medical Research Council Unit on the Development and Integration of Behaviour University Sub-Department of Animal Behaviour Madingley, Cambridge, England COLINBEER Institute of Animal Behavior Rutgers University Newark, New Jersey MARIE-CLAIRE BUSNEL Laboratoire de Physiologie Acoustique Institut National de la Recherche Agronomique Jouy en Josas (78350),France

VOLUME 1 1

ACADEMIC PRESS A Subsidiary of Harcourt Brace Jovanovich, Publishers

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1980

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80 81 82 83

9 8 7 6 5 4 3 2 1

Contents

List of Conrributors . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Preface . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

ix xi

Interrelationships among Ecological. Behavioral. and Neuroendocrine Processes in the Reproductive Cycle of Anolis carolinensis and Other Reptiles DAVID CREWS

I . Introduction ............................................

I1 . Natural History of Anolis carolinensis . . . . . . . . . . . . . . . . . . . . . . 111. Behavioral Repertoire of Captive Anolis carolinensis . . . . . . . . . .

1 3 6

IV . Studies of the Biological Bases of Species-Typical Behavior Patterns . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . V . Studies of the Behavioral Ecology of Anolis . . . . . . . . . . . . . . . . . . VI . Extension to Other Reptilian Species . . . . . . . . . . . . . . . . . . . . . . . . VII . Concluding Remarks . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

44 51 65 66

10

Endocrine and Sensory Regulation of Maternal Behavior in the Ewe PASCAL POINDRON AND PIERRE LE NEINDRE I . Introduction ............................................ 76 I1. Influence of the Endocrine State of the Ewe on the Onset of Maternal Behavior ....................................... 77 111. Influence of the Newborn Lamb on the Development of Postpartum Maternal Behavior . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 88 IV . Mother-Young Relationships beyond the Postpartum Period . . . . . 99 V . Maternal Behavior in Inexperienced Ewes . . . . . . . . . . . . . . . . . . . . 108 VI . Conclusion and Future Prospects of Research . . . . . . . . . . . . . . . . . 113 References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 115

V

vi

CONTENTS

The Sociobiology of Pinnipeds PIERRE JOUVENTIN AND ANDRE CORNET I , Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . I1. Social Structures ........................................ 111. Adaptive Strategies among Phocidae and Oteriidae . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

121 123 133

139

Repertoires and Geographical Variation in Bird Song JOHN R . KREBS AND DONALD E . KROODSMA

I. I1. I11. IV .

Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Repertoires ............................................. Geographical Variation ................................... Conclusion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

143 144 159

170 170

Development of Sound Communication in Mammals GUNTER EHRET

I . Introduction ............................................ I1. Components of Sound Communication Systems: General Aspects of Development . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 111. Time Courses of the Development of Vocal Behavior and Hearing in Subhuman Mammals and Man ........................... IV . Characteristics and Common Tendencies of the Development of Vocal Behavior ......................................... V . Characteristics and Common Tendencies in the Development of Sound Communication . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . VI . Conclusions ............................................ VII . Summary .............................................. References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

179

181

183 198

208 216 216 218

Ontogeny and Phylogeny of Paradoxical Reward Effects ABRAM AMSEL AND MARK STANTON I . Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

I1. Paradoxical Effects of Reinforcement .......................

227 230

CONTENTS

vii

I11 . Frustration Theory as One Mechanism for the Paradoxical Effects 234 236 V . Toward an Ontogenetic Analysis of Paradoxical Effects . . . . . . . . 242 VI . Comments on the Neural Substrate of Paradoxical Effects . . . . . . . 257 VII . Concluding Considerations: Implications for Behavior and Behavior Theory . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 263 References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 267

IV . The Comparative Analysis of Learning ......................

Ingestional Aversion Learning: Unique and General Processes MICHAEL DOMJAN 1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 276 I1. The Associative-NonassociativeControversy . . . . . . . . . . . . . . . . . 278

111. Poison-Avoidance Learning and the Complexity of the Ingestive

Sequence . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . IV . The Selectivity of Associations in Ingestional Aversion Learning . V . Limitations on Ingestional Aversion Learning . . . . . . . . . . . . . . . . . VI . Conclusion: A Continuing Search for General and Unique Characteristics of Ingestional Aversion Learning . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

292 303 318 326 330

The Functional Organization of Phases of Memory Consolidation R . J . ANDREW

I . Phases of Memory in Higher Vertebrates: Evidence from Amnestic Agents . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . I1 . Human Memory . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 111. Models of Memory Formation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1v . Previous Studies of Memory. Using Pecking in the Chick . . . . . . . V . Hormones and Other Enhancing Agents in the Chick: Opposition to Arnnestic Agents . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . VI . Conclusion: General Implications ........................... References .............................................

Index . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Contents of Previous Volumes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

338 347 348 350 352 361 363

369 315

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List of Contributors Numbers in parentheses indicate the pages on which the authors’ contributions begin

ABRAM AMSEL, Department of Psychology, University of Texas at Austin, Austin, Texas 78712 (227) R. J . ANDREW, Ethology and Neurophysiology Group, School of Biological Sciences, Universit), of Sussex, Brighton, United Kingdom (337) ANDRE CORNET, Laboratoire d’Evolution des Vertebres, Universite des Sciences et Techniquesdu Languedoc, 34000 Montpellier-Cedex,France (12I ) DAVID CREWS, Departments of Biology, Psychology and Social Relations, and Museum of Comparative Zoology, Harvard University, Cambridge, Massachusetts 02/38 ( I ) MICHAEL DOMJAN, Department of Psychology, University of Texas at Austin, Austin, Texas 78712 (275) GUNTER EHRET, Fakultat Biologie, Universitat Konstanz, 0-7750 Konstanz, Federal Republic of Germany ( I 79) PIERRE JOUVENTIN, Laboratoire d’Evolution des Vertebres, Universite des Sciences et Techniques du Languedoc, 34000 Montpellier-Cedexx,France (12I J JOHN R. KREBS, Department of Zoology, Edward Grey Institute of Field Ornithology, South Parks Road, Oxford OX1 3PS, England (143) DONALD E. KROODSMA, Rockefeller University, Field Research Center, Millbrook, New York 12545 (143) PIERRE LE NEINDRE, Laboratoire de Production de Viande, I.N.R.A. de Theix, 63110 Beaumont, France (75) PASCAL POINDRON, Laboratoire de Comportement Animal, 1.N.R.A . de Nouzilly, 37380 Monnaie, France (75) MARK STANTON, Department of Psychology, University of Texas at Austin, Austin, Texas 78712 (227)


Preface With the publication of the eleventh volume of Advances in the Srudy of Behavior, we wish to restate in more contemporary terms the aims stated in the original preface, namely, to serve ". . . as a contribution to the development of cooperation and communication among scientists in our field. " Since that preface was written in 1965, an increasing number of scientists from disciplines as widely separated as behavioral ecology and the biochemistry of behavior have become engaged in the study of animal behavior, employing the specialized techniques and concepts of their disciplines. Even then, the boundaries of ethology and comparative psychology were no longer distinct: now they have been merged with broader syntheses of social and individual functioning and have together provided the bases for studies of the neural and biochemical mechanisms of behavior. New vigor has been given to traditional fields of animal behavior by their coalescence with closely related fields and by the closer relationship that now exists between those studying animal and human subjects. Scientists engaged in studying animal behavior now range from ecologists through evolutionary biologists, geneticists, endocrinologists, ethologists, and comparative and developmental psychologists, to neurophysiologists and neuropharmacologists. The task of developing cooperation and communication among scientists whose skills and concepts necessarily differ in accordance with the diversity of the phenomena they study has become more difficult than it was at the inception of this publication. Yet the need to do so has become even greater as it has become more difficult. The Editors and publisher of Advances in the Srudy of Behavior will continue to provide the means by publishing critical reviews of research in our field, by inviting extended presentations of significant research programs, by encouraging the writing of theoretical syntheses and reformulations of persistent problems, and by highlighting especially penetrating research that introduces important new concepts.

xi


ADVANCES LN THE STUDY OF BEHAVIOR

VOL. I I

Interrelationships among Ecological, Behavioral, and Neuroendocrine Processes in the Reproductive Cycle of Anolis carolinensis and Other Reptiles DAVIDCREWS DEPARTMENTS OF BIOLOGY, PSYCHOLOGY A N D SOCIAL RELATIONS, A N D MUSEUM OF COMPARATIVE ZOOLOGY

H A R V A R D UNIVERSITY CAMBRIDGE, MASSACHUSETTS

I. Introduction . . . . . . . . . . . . . . . . . . ......................... 11. Natural History of Anolis rrrrohe ..... ... ......... 111. Behavioral Repertoire of Captive Anolis carolinmsis . . . . . . . . . . . . . . . . . . . IV. Studies of the Biological Bases of Species-Typical Behavior Patterns . . . . . . A. Hormonal Control of Female Sexual Receptivity B. Stimulus Control of Male Mounting Behavior . . . . . . . . . . C. Sociosexual Control of Seasonal Gonadal Recru D. Hormonal Control of Male Aggressive and Sexual Behavior . . . . . . . . . . Secretion . . . . . . .

............................

1 3 6 10 10

17 25

33

37 44 45

................. C. Crocodilians . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . D . Parthenogenetic Lizards . . . . . . . . . . . . . . . . . . . . ......... VII. Concluding Remarks. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . References .......................... ........................

I.

48 51 51 57 59 61 65

66

INTRODUCTION

More than 1 5 years ago Niko Tinbergen ( 1963)argued that to understand fully a naturally occurring behavior pattern, it is necessary to study how the behavior adapts the organism to its environment, how the behavior evolved through his1

Copynphl @ 1980 by Academic Ress. lnc All nghts ofrepmduclim in any form reserved. ISBN 0-12-004511-7

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DAVID CREWS

toric time, how the behavior develops within the organism’s own lifetime, and, finally, the mechanisms underlying the behavior (see also Beach, 1950). Each of these “questions” are today represented in the fields of behavioral ecology, evolutionary biology, behavioral development, and behavioral physiology or physiological psychology. Although the boundaries of these areas are artificial and often times indistinct, it is not uncommon to find that behavioral ecologists know little of the development of the behavior they are investigating. Similarly, few physiological or developmental psychologists know the principles of evolutionary biology or appreciate the potential of an evolutionary investigation of behavior. In addition to the differences in training scientists receive within these different disciplines, the lack of communication between these areas of behavioral investigation can be traced to the ultimate questions being asked and the level of analysis that characterizes the area. Thus, behavioral ecologists and evolutionary biologists have traditionally been concerned with problems above the level of the behavior of the individual organism. Researchers interested in the immediate causation of behavior, on the other hand, have tended to concentrate at or more typically below the level of the behavior of organisms. Such division and specialization, however, was not the intention of Tinbergen. As exemplified by Tinbergen’s own research, the combination and integration of all levels of analysis, cellular, physiological, organismal, and evolutionary, into a single research program make this approach an extremely powerful method for achieving an understanding of the biological bases of behavior. For example, after the behavioral repertoire of the species has been described and quantified, the latest techniques in physiological analysis can be used to study the mechanisms underlying the behavior. Ideally, behavioral hypotheses arising from the laboratory should then be tested in the field to learn what role the behavior plays in the animal’s natural history as well as what constraints the environment places on individual behavior. Although there are relatively few examples of such comprehensive investigations, those that do exist have led to major advances in our understanding of the adaptive significance of behavior and of the forces controlling the behavior of organisms in nature (Dewsbury, 1975, 1978; Hinde, 1965; Hinde and Steele, 1978; Konishi, 1973; Leon, 1974, 1978; Murton and Westwood, 1977; Roeder, 1967, 1974). One reason why there are so few practitioners of this multileveled approach is the difficulty in obtaining an organism that lends itself to such a wide-ranging investigation. Indeed, I believe this problem of suitability is the major reason behind the long-standing differences between field-oriented versus laboratoryoriented behavioral biologists. That is, an animal that a behavioral ecologist might find interesting (e.g., a mountain gorilla) cannot conveniently be brought into a laboratory and expected to behave normally. Conversely, it is rare to find in nature animals as convenient (and genetically similar) as the inbred strains of small mammals commonly used by many laboratory behavioral physiologists.

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3

A candidate species for such a psychobiological approach to the study of behavior should satisfy at least six criteria. The species chosen must not be secretive in its natural habitat but should be obvious and preferably conspicuous. It should reproduce reliably and at frequent intervals in the laboratory and should grow rapidly. This is particularly important if one is interested in studying the developmental and genetic basis of behavior. The species should have an interesting and sufficiently complex social organization. Experimental manipulation of the animal in the field should be possible and, when transferred into seminatural laboratory conditions, the animal should continue to exhibit similar behavioral patterns and social organization to that observed in the field. The species should also belong to a taxon whose members occupy a variety of diverse habitats for it is likely that species that show different behavior patterns as a consequence of different environmental constraints are also likely to differ in the underlying physiological mechanisms. Finally, it would be preferable if there existed some knowledge of the evolution, ecology, behavior, and physiology of the species to be studied on the basis of which experiments can be designed. Many species of the lizard genus Anolis satisfy the aforementioned criteria.

11.

NATURAL HISTORYOF Anolis carolinensis

The genus Anolis consists of more than 200 species found throughout the West Indies and South and Central America. A considerable amount of information on the evolution and ecology of the different anoles has been gathered by Ernest Williams and his colleagues and students (Etheridge, 1960; Huey and Slatkin, 1976; Huey and Webster, 1975, 1976; Kiester e r a / . , 1975; Paul1 et a/.,1976; Rand, 1967; Roughgarden, 1974; Schoener, 1970, 1975; Trivers, 1976; Williams, 1969, 1972; and Yang et uf., 1974). The outstanding characteristic of Anolis is its diversity. Anoles are found in a very wide variety of habitats from montane cloud forest to lowland desert. The adaptive radiation within each life zone is equally remarkable (Fig. I ) with each species specialized to live in different parts of the habitat. Anoles are similar to birds; that is, in multispecies communities they are distributed vertically such that a single tree might contain several species. Typically, one very large "giant" species inhabits the crown and thick branches of the tree while slightly smaller species reside on the tree trunk. Even smaller species tend to be found at the periphery of tree branches, on twigs, in grassy areas, and in the underbrush surrounding the trees. This ecological and evolutionary diversity makes anoles excellent candidates for an investigation of not only ecological principles, but also of behavior and its controlling mechanisms. One species of Anolis, A . carolinensis, is particularIy well suited for study of the ecological aspects of behavioral endocrinology. This species is found throughout much of the southeastern United States and is especially abundant in

-

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DAVID CREWS

A N O L E RADIATION

.

(sunny area 1

.

(deep shade 1

FIG. I . Andis lizards have undergone an extensive adaptive radiation in Central and South American and in the West Indies. Species differ in (I) body size, with “giant” species of greater than 100 mm snout-vent length to “dwarf” or twig species of less than 50 mm snout-vent length; (11) diameter of preferred perch, with species inhabiting the tree crown to species living in bushes andor grass; and (111) microclimate, with species living in open, sunny areas to species living in deep shade. From Crews and Williams (1977) with permission of the American Society of Zoologists.

Louisiana, reaching densities of more than 1500 lizards per acre (Gordon, 1956); they are most numerous around clearings, forest edges, and in disturbed ecotones. Like most iguanid lizards, the males and females are sedentary, establishing and defending discrete areas against conspecifics. The size and shape of the territories vary depending upon the vegetation, but may average 20 ft in diameter and encompass 400-600 fig.Generation time is short and, if maintained in the laboratory under a constant stirnulatory environmental regimen, A . carolinensis will undergo three to four complete reproductive cycles within a year (Crews, unpublished). Eggs incubate for approximately 6-8 weeks before hatching in the field but in the laboratory a 30-day incubation is common. Young born in the laboratory grow rapidly and are reproductively mature in 6 months; in nature, males grow more rapidly than females and usually are mature before the

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Anolis carolinensis

5

winter of their birth (Gordon, 1956). Further, A . carolinensis is a hardy animal, living up to 3 years in captivity. Laboratory housed animals exhibit the same behavioral displays as in nature even if housed in small cages containing only a food dish, drinking tube, and a stick on which to perch (Crews, 1975b, 1977). Finally, more is known of the ecology, behavior, and physiology of this species than of any other reptile, making A . carolinensis the best candidate for a systematic investigation of the psychobiology of reptilian reproduction. Anolis carolinensis breeds in the spring and summer (Fig. 2) with the exact timing and length of the reproductive season varying with geographic locality (Gordon, 1956; King, 1966). In late summer decreasing daylength causes the gonads to regress (Licht, 1971), and the animals enter into a month long refractory period (Crews, 1975c, 1978b). During this time, they are insensitive to the high temperatures which in the spring and summer stimulate and maintain breeding activity (Crews and Licht, 1974; Licht, 1971). Following this refractory period, which in the female is maintained by a substance (probably progesterone) produced by the degenerating follicles (Crews and Licht, 1974), the male and female begin winter hibernation. During the winter, animals can be found singly or clustered in groups beneath the bark of dead trees and under fallen logs or rocks in areas of dense vegetation such as swamps and woods. Although there is some testicular growth at this time (Licht, 1971), ovarian activity is minimal (Crews, 1975c, 1978b). In early spring, the increase in temperature stimulates 0

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FIG. 2. Major physiological and behavioral events in the annual reproductive cycle of the green anole, Anofis carofinensis. See text for further details. From Crews ( 1 9 7 5 ~ ) with permission of the American Association for the Advancement of Science.

6

DAVID CREWS

both the emergence and the final phases of testicular activity in the males, who quickly establish breeding territories. Approximately 1 month later, the females emerge (Gordon, 1956) and establish home ranges within the males’ territories although they may move during the breeding season, establishing another home range. Typically, a single male’s territory will encompass a home range of two or three females and will also contain several subordinate males in the underbrush. During the breeding season which follows, the females show periods of sexual receptivity (Crews, 1973a; G. Gorman, personal communication; Greenberg and Noble, 1944; Stamps, 1975; Trivers, 1976). A considerable amount is known about the daily activity cycle and behavioral ecology of A . carolinensis (Crews, unpublished observations; Gordon, 1956; W. Haas, unpublished manuscript; King, 1966). In the summer, A . carolinensis become active approximately 30-60 min after sunrise, leave their sleeping sites (usually a twig or grass stem), and spend several hours basking. There is some evidence that females sleep in less exposed positions than males (Gordon, 1956). Social displays (see Section 111) are frequent during this period but then diminish and are rarely seen around midday (6-9 hr after dawn) at which time animals mostly feed on small, soft-bodied insects. In the late afternoon, animals again interact frequently and most copulations occur at this time, a fact also noted by Stamps (1975) for A . aeneus in Grenada. Copulations which occur during the morning activity period are usually brief, whereas those in the afternoon are usually of long duration; only after the long matings during the afternoon does the female show behavioral nonreceptivity (see Section IV,A). Lizards move from their territory or home ranges to sleeping perches about 1 hr before sunset.

III. BEHAVIORAL REPERTOIRE OF CAPTIVE Anolis carolinensis Anolis carolinensis exhibit a varied and easily identifiable behavioral repertoire in the laboratory that resembles closely that seen in nature. Assertion, challenge, and courtship displays all share an up-and-down bobbing movement but differ in both the cadence and the patterning of the bobbing as well as in other characteristics (Cooper, 1977; Crews, 1975b, 1979b; Greenberg, 1977; Greenberg and Noble, 1944) (Table I). Male aggressive behavior, which actually is a continuum of agonistic displays, is dramatic and unmistakable (Fig. 3). A sexually active male will patrol his territory, stopping at prominent perches to exhibit the Assertion display. This display is given while standing still and is characterized by a species-typical bobbing movement coordinated with the extension of a red throat fan called the dewlap. If a strange A. carolinensis enters the territory of a male, the resident will immediately challenge the intruder. The Challenge display is identified by an extreme lateral compression of the body and a highly stereotyped, species-typical bobbing movement. If the intruding animal

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7

TABLE I SOCIAL DISPLAYS I N LABORATORY POPULATIONS O F Anolis carolinensis AND THEIR IDENTIFYINGCHARACTERISTICP Display

Context

Orientation Posture Movement

Dewlap Approach

Assertion

Challenge

Courtship

Submission

Response often seen performed by dominant animal after an aggressive bout or when reaching favorite perch; occasionally seen when animal alone in cage None apparent

Response to strange lizard, subordinate, or toward any displaying conspecific

Response to the introduction of a female or toward any lizard giving submission display

Response to the approach, challenge display or courtship display by a dominant lizard

Oriented toward recipient Laterally compressed Bobbing with forepart of body Extended None, display stationary

Oriented toward recipient Relaxed Bobbing with forepart of body Extended Approaches other lizard, stopping to display

Variable

Relaxed Bobbing with forepart of body Extended None, display stationary

Relaxed Nodding of head only Absent None, display stationary

“From Crews (1975a), with permission.

does not immediately give the Submission display (a rapid nodding of the head) or if it reacts aggressively to the resident male’s challenge, the resident will approach the intruder and a fight will ensue. During a fight, the dewlap is not extended but the entire hyoid apparatus is lowered and the throat region is engorged in both contestants. As the fight progresses, a crest is erected along the back and neck, and a black spot forms immediately behind the eye (the eye spot). It is not uncommon for males to lock jaws while circling one another, each trying to throw the other off the perch. Fights may last several hours, after which the winning male (almost always the resident) will typically climb to a prominent perch and perform a series of Assertion displays. During courtship, the male advances toward the female, pausing to perform a series of bobbing-dewlap displays (Fig. 4). The number of bobbing movements during the Courtship display varies greatly between individual males and so may aid in individual recognition (Crews, 1975b). When approached by a courting male, female A . carolinensis will either flee immediately and hide or remain stationary. As the male nears, the female may begin to whip her tail (TailWhip), indicating nonreceptivity, or remain immobile until the male comes in contact. A

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DAVID CREWS

FIG.3 . Agonistic behavioral displays of the lizard, Anolis carolinensis. (A) A sexually active, temtorial male performs an assertion display. (B) A dominant male performs a challenge display. The extreme lateral compression and engorged throat are the identifying characteristics of the challenge display. See Table I and text for further details.

FIG.4. Mating sequence in Anolis carolinensis. (A) A sexually active male performs a courtship display toward a female. The relaxed body posture ana distinctive cadence of the bobbing movement are characteristic of courtship (see also Table I and text). (B) Female exhibits a neckbend as courting male approaches. This behavior is seen only if the female is sexually receptive. (C) After taking a neck grip, the male mounts the female and intromits one of his two hemipenes.

10

DAVID CREWS

receptive female will then arch her neck (Neckbend), pointing the snout down, as the male grasps her neck skin between his jaws; a highly receptive female will stand and neckbend in response to the courtship display of a male performed at a distance or she may even approach the male and solicit courtship by performing submissive headnods to attract the male’s attention. After taking the neckgrip, the male straddles the female’s back and usually within 1 min of mounting swings his tail to the right or left, trying to appose the cloaca1 regions (see Section IV,B). This is not always successful and the male may twist his body to the right and left several times before intromission is achieved. OF THE BIOLOGICAL BASESOF SPECIES-TYPICAL IV. STUDIES BEHAVIOR PATTERNS

A.

HORMONAL CONTROL OF FEMALE SEXUAL RECEPTIVITY

During the breeding season, the female periodically lays a single egg often in moist leaves or in a shallow hole (Tokarz and Jones, 1979). The interval between egg laying is usually 2 weeks but this may vary with the humidity (Brown and Sexton, 1973) and the species (King, 1966). In all anoline lizards, the ovaries alternate in the production of a single ovum (Smith et al., 1973)and,

FIG.5 . Urogenital system of a reproductively active female Anolis carolinensis. Stippled follicles in both ovaries are yolked (vitellogenic); other follicles are previtellogenic. Note the alternating hierarchial pattern of follicle maturation between the ovaries. See text for further details.

REPRODUCTION IN

Anolis carolinensis

11

within each ovary, the follicles mature in a hierarchical manner (Jones, 1975) (Fig. 5). Typically, a breeding female has one shelled oviducal egg about to be oviposited and, in the contralateral ovary, a large preovulatory follicle. In A . carolinensis, an egg is ovulated once every 10-14 days and, during the breeding season, a female may lay as many as 15 eggs (Crews, 1973a; Hamlett, 1952; Licht, 1973); Gordon (1956), however, estimates from field samples that the average reproductive potential for a single female is seven eggs per season. Coincident with this cycle of ovarian activity are predictable fluctuations in the female’s sexual behavior with estrus (receptivity) occurring prior to ovulation (Crews, 1973a) (Fig. 6). These cycles reflect corresponding fluctuations of circulating sex steroids, although the levels of circulating ovarian hormones during the estrous cycles of lizards are still being investigated. The pattern and sequence of circulating hormone levels during the follicular cycle of both recently captured, breeding females and gonadotropin-stimulated females have been determined. In A . carolinensis as in other oviparous reptiles (cf. Callard rral., 1978), plasmaestradiol levels increase during follicular development, reaching a peak immediately before the surge in progesterone around the time of ovulation (Fig. 7). As would be expected, removal of the ovaries abolishes sexual receptivity in female A , carolinensis (Valenstein and Crews, 1977), and estrogen replacement therapy reinstates this behavior in a dose-related manner (Crews, 1978b, 1979). For example, the threshold dose for the neckbending response, one of the components of female sexual receptivity, appears to be 0.6 pg of estradiol benzoate (EB) (McNicol and Crews, 1979).

I

7

14

21

28

DAYS

35

42

49

56

nonreceptiwe

0

receptive

FIG.6. Relationship between maturation and ovulation of the ovarian follicle and sexual receptivity in Anolis carolinensis. During the breeding season, female A . carolinrnsis undergo cycles of sexual receptivity which are correlated with the maturation and ovulation of a single follicle alternately between ovaries. The exact onset of estrus varies between females, occurring when the largest ovarian follicle is between 3.5 and 6 0 mm in diameter. Females are receptive to male courtship behavior until ovulation or until mating. From Crews (1977) with permission of Sigma Xi.

12

DAVID CREWS

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4 5 6 7 8 DIAMETER OF LARGEST OVARIAN FOLLICLE ( M M ) FIG.7. Correlation between diameters of the largest ovarian follicles and plasma levels of estrogen in the untreated- and follicle-stimulating hormone (FSH)-treated female lizard, Anolis carolinensis. Adult female lizards with seasonally inactive ovaries were obtained in February and housed in a laboratory animal colony room. After 1 week in the laboratory, a number of these animals were sacrificed (A). The remaining animals were treated with ovine FSH (10 pg/animal/day) for either 7 (0)or 14 (0) days prior to sacrifice to stimulate ovarian follicular growth. Following sacrifice, the diameter of the largest ovarian follicle in each animal was measured and the plasma estrogen level was determined by radioimmunoassay. Analysis of the data revealed a significant positive correlation between follicular diameters and plasma estrogen levels (r(46)= 0.59, p < 0.01). Sexually active females bled during the breeding season exhibit a similar correlation between follicular diameter and circulating estrogen levels. From Tokarz and Crews, unpublished. I

Females ovariectomized while reproductively inactive and long-term ovariectomized females are much less sensitive to exogenous estrogen; such females fail to show signs of sexual receptivity at the end of 48 hr following an injection of 1.4 pg of EB; pretreatment with low amounts of estrogen (0.2 pg) results in a much more rapid response to suprathreshold estrogen dosages (Fig. 8). It is possible that estrogen receptors in brain areas subserving female receptivity are diminished in these females (Hutchison, 1978; Lisk, 1978).

REPRODUCTION IN

Anolis carolinensis

13

As in many mammalian species (reviewed in Lisk, 1978), progesterone plays a major role in regulating female sexual receptivity. Also, as in some mammals, progesterone in A . carolinensis also appears to be involved in controlling estrous behavior. When administered done, progesterone (up to 160 pg) fails to induce female sexual receptivity (Crews, 1975c, 1978b) but when administered 24 hr after subthreshold estrogen priming (a single injection of 0.4 pg EB), progesterone (60 pg) will synergize with estrogen to facilitate sexual receptivity (McNicol and Crews, 1979) (Fig. 9). This pretreatment with estrogen is neces-

DAYS FIG. 8. Effect of estrogen pretreatment on the induction of female sexual receptivity in the lizard, Anolis carolinensis. Ovariectomized females were injected daily for 3 days with either 0.2 p g of estradiol benzoate (EB) or with steroid suspension vehicle (SSV). The following day (arrow), animals pretreated with EB received a single injection of 0.8 pg EB (circles); females pretreated with SSV received a single injection of 1.4 pg EB (triangles) at the same time. Daily behavioral testing for sexual receptivity began on day 1. Female receptivity was scored as follows: 0, unreceptive, female runs from courting male; I , low receptivity, female allows male to take a neckgrip but then struggles; 2, moderate receptivity, female passively allows male to take a neckgrip and mating is accomplished with little or no struggling; 3, high receptivity and proceptivity , female performs distinct neckbend as male approaches to take a neckgrip, female may also solicit male courtship. Sample sizes are shown in parentheses. From Tokarz and Crews (unpublished).

14

DAVID CREWS

FIG.9. Effects of varying amounts of progesterone on the sexual receptivity of estrogen-primed female Anolis carolinensis. Ovariectomized females were given a single injection of 0.4 pg estradiol benzoate (EB) and a second injection of steroid suspension vehicle (SSV) or progesterone 24 hr later. All females were tested 24 hr following the second injection. Sample sizes are shown in parentheses. From McNicol and Crews (1979) with permission of Academic Press.

sary for the induction of progesterone receptor in the hypothalamus (Crews, Tokarz, and McEwen, unpublished data). Studies of the time course of this facilitatory role of progesterone indicate that progesterone begins to exert its effect within 3 hr of its injection following estrogen priming (Fig. 10). Recent experiments have demonstrated that both luteinizing hormone-releasinghormone

FIG.10. Facilitatory effects of a single injection of 60 p g progesterone (P)or steroid suspension vehicle (SSV) on sexual receptivity in estrogen-primed ovariectomized Anolis carolinensis. All females were primed with a single subthreshold dose of 0.4 pg estradiol benzoate 24 hr prior to injection of progesterone. Sample sizes are shown in parentheses. From Crews (1979a) with permission of the Society for the Study of Reproduction.

REPRODUCTION I N

Anolis carolinensis

15

(LHRH) and thyrotropin-releasinghormone (TRH) rapidly induce sexual receptivity in ovariectomized, estrogen-primed female lizards (Alderete et al., 1980) (Fig. 11). The finding that TRH is capable of stimulating estrus is novel and suggests a major difference in the neuroendocrine regulation of receptivity in female lizards as compared to that of birds and mammals. Experiments with small mammals indicate that progesterone can also inhibit estrus, depending upon when it is administered in relation to estrogen (reviewed in Feder, 1977; Feder and Marrone, 1977; Morin, 1977). This may also be true in lizards. For example, by 72 hr following progesterone facilitation of estrogen-primed ovariectomized lizards, only a small percentage of females are still sexually receptive (see Fig. 10). This decline may indicate an active inhibition by progesterone, since females receiving a single injection of 0.8 p g of EB alone continue to be highly receptive for 1 4 4 hr (Crews, unpublished). Other experiments indicate that a single injection of 160 p g of progesterone 48 hr after 3.0W

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FIG. 1 1 Both luteinizing hormone-releasing hormone (LHRH) and thyrotropinreleasing hormone (TRH) induce sexual receptivity in ovariectomized, estrogen-primed female Anolis carolinensis. Deamido TRH under the same conditions fails to induce sexual receptivity. Females were pretreated with three daily injections of a subthreshold dose (0.2 pg) of estradiol benzoate (EB). Behavioral tests were conducted 48 hr following the last EB injection. Immediately following the pretest, each female received a single injection of 1000 ng of LHRH (filled circles), TRH (filled triangles), deamido TRH (open triangles), or a comparable volume of steroid suspension vehicle (open circles). Behavioral tests were conducted 2, 4,6, and 24 hr following injection. Sample sizes are shown in parentheses; mean and SEM are shown. See Fig. 8 for explanation of receptivity score. From Alderete er al. (1980) with permission of S. Karger. I

16

DAVID CREWS

a priming injection of 0.8 pg of EB will completely inhibit the effects of the estrogen (Crews, unpublished). Again, the effect of the progesterone is extremely rapid, and the majority of females are no longer receptive within 24 hr of progesterone administration. In many mammalian species, mating has at least two effects apart from sperm transfer and fertilization. First, copulation terminates or markedly reduces female sexual receptivity (Carter and Schein, 1971; Goldfoot and Goy, 1970; Hardy and DeBold, 1972). Second, vaginocervical stimulation arising from mating induces hormonal changes leading to the establishment of corpora lutea necessary for successful pregnancy (Adler, 1974, 1977). In A . carolinensis, intact females are no longer sexually receptive following mating (Crews, 1973b). This transition from receptivity to nonreceptivity (a) is extremely rapid, beginning immediately after the male dismounts, and ( h ) is maintained for several days until ovulation; ovulation in this species appears to be spontaneous. The presence of the ovary is critical for the maintenance of this matinginduced refractoriness (Valenstein and Crews, 1977): if ovariectomized, estrogenprimed females are allowed to mate, they will again be receptive to male courtship in about 6 hr following the mating (Table 11). Intact, reproductively active females, on the other hand, continue to be unreceptive to male courtship for several days if treated with estrogen. This suggests that the presence of the ovaries or some change in ovarian hormone production (progesterone?) is critical for long-term inhibition of female sexual receptivity. Intromission of the hemipenis by the male is a critical component underlying inhibition of female sexual receptivity. Intact, preovulatory females that are

INFLUENCE

TABLE I1 OVARIES ON POSTCOPULATORY SEXUAL RECEPTIVITY THE FEMALE L I Z A R D , Anolis carolinensis"

OF T H E IN

Treatment Sham-operated females A. 0.8 pg EB injection B . 6 mm EB implant Ovariectomized females C. 0.8 f i g EB injection C. 6 mm EB implant

Number initially receptive

Percentage receptive 24 hr after copulation

9 5

22% 20%

9

1 OO%b

15

93%'

From Valenstein and Crews ( I 977). with permission * p )gror~iana) Rufous-collared sparrow (Zonotrichia capensis)

Reference

Konishi (1965) Lemaire ( 1975) Bremond ( 1976) Becker (1977 a,b) Becker ( I 977a.b) Todt ( 1970)

Gompertz (1961); Hunter and Krebs (1979); McGregor ef al. (1980) Dixon ( 1969) Lemon

(

168)

Thielcke 1961. 1965, 1969) Thielcke 1961, 1969)

Grimes (1974); Payne (1978)

Kaiser ( 1965) Conrads ( 1976); Conrads and Conrads ( I97 I ) Tinbergen ( I 939); Chapman in Gatty (1 958) Martin ( 1977, 1979) Harris and Lemon ( 1972); Eberhardt and Baptista I 1977)

D.E. Kroodsma (unpublished data) Nottebohm (1969. 1975); King (1972)

164

JOHN R . KREBS A N D DONALD

E. KROODSMA

TABLE I1 (continued) Species White-crowned sparrow (Zonotrichia leucophrys) Darkeyed junco (Junco hyemalis) Savannah sparrow (Ammodramus sandwichensis beldingii) Vesper sparrow (Poeecetes gramineus) lndigo bunting (Passerina cyaneu) Lazuli bunting (Passerina amoena) Rufous-sided towhee (Pipilo erythrophthalmus) Cardinal (Cardinalis cardinalis) Pyrrhuloxia (Pyrrhuloxia ( =Cardinalis?) sinuata) Rose-breasted grosbeak (Pheucticus ludovicianus) Vireonidae Solitary vireo (Vireo solitarius) Yellow-throated vireo ( Vireojlavifrons) Icteridae Red-winged blackbird (Agelaius phoeniceus) Cacique (Cacicus cela) Bobolink (Dolichonyx oryzivorous) Fringillidae Chaffinch (Fringilla coelebs) Greenfinch (Chloris ( =Carduelis?) chloris) European siskin (Carduelis spinus) Pine siskin (Carduelis pinus) American goldfinch (Curduelis tristis) Twite (Carduelis (=Acanthis?)ji’avirostris) Cassin’s finch (Carpodacus cassinii)

Reference

Marler and Tamura (1962) Baptista (1975); many others Williams and MacRoberts (1977) Bradley ( 1977) Kroodsma ( 1 972) Thompson (1970); Emlen et al. (1975) E d e n et al. (1975) Kroodsma ( I97 1 ); Ewert ( 1978) Lemon (1966, 1975) Lemon and Herzog ( 1969) Lemon and Chatfield (I 973)

James (1973, 1976) James (1973, 1976)

E.S. Morton (personal communication) Feekes ( I 977) Avery and Oring (1977)

Marler ( 1 952); Metzmacher and Mairy (1974) Giittinger (1974, 1977) Mundinger ( 1970) Mundinger (1970) Mundinger ( 1970) Marler and Mundinger (1975) Samson ( 1978)

165

VARIATION IN BIRD SONG TABLE I1 (continued) Species House finch (Carpodacus mexicanus)

Pine grosbeak (Pinicola enuclearor) Bullfinch (Pyrrhula pyrrhula) Plocediae Village indigobird (Vidua chalybeata) Sturnidae Indian hill mynah (Cracula religiosa) Callaeidae Saddleback (Philesturnus ( =Creadion?) carunculatus) Corvidae Blue jay (Cyanocirta cristara) ____

Reference

Mundinger ( 1975); Bitterbaum and Baptism (1979) Adkisson (personal communication) Nicolai ( 1 959); Wilkinson and Howse ( 1 975)

Payne (1973b)

Bertram ( 1970)

Jenkins ( 1977)

Kramer and Thompson (1979)

~~

‘l In these species, songs of neighbors are more similar to one another than they are to the songs of more distant conspecifics.

Instead the young male had adopted a song component similar to that of neighboring males and abandoned the one learned from its father. Thus, indigo birds and saddlebacks may disperse as adults and modify their song repertoire to match the song types of other adults with which they interact. Juvenile Bewick’s wrens can probably imitate their father’s songs, but after dispersing to their permanent breeding territory, additional songs are acquired or the father’s songs are modified to conform to the local song neighborhood. The end result in all three species is that neighbors have similar songs. 3 . Microgeographical Variation and Genetic Isolation

It has been suggested by a number of authors (Marler and Tamura, 1962, 1964; Nottebohm, 1969) that microgeographicalpatterns of song variation might reflect genetic differentiation of local populations. The idea proposed by Nottebohm is that songs are learned close to the site of hatching, and that young birds do not disperse beyond the boundaries of the population in which their own song variation is prevalent. In consequence, pairs tend to form between birds from the same song population, and genetic differentiation of populations could arise as a result of learned song traditions (see also Section 11,B,4,d). The best data supporting this hypothesis have been collected by Baker (1974,

166

JOHN R . KREBS AND DONALD E. KROODSMA

1975; Baker and Mewaldt, 1978). Male white-crowned sparrows at Point Reyes, California, generally have only one song type in their repertoires and neighboring males have nearly identical songs, indicating, as had been amply demonstrated in the laboratory (Marler, 1970), that males learn their songs from one another. Very sharp boundaries exist where territorial males on opposite sides sing recognizably different song patterns (Baptista, 1975; Baker, 1974), and analyses of genetic differences (by measuring enzyme polymorphisms) and dispersal patterns among birds in the region of the song boundary suggested that birds of the two song traditions tend not to interbreed. However, these conclusions may not apply to all white-crowned sparrow populations. For example, in the Rocky Mountains of Colorado white-crowned sparrows show genetic differences within a song tradition, while in coastal California such changes in allozyme frequency occur across the boundary between two song traditions (Baker, 1975). In a detailed study of white-crowned sparrows in Berkeley, California, L. F. Baptista and L. Petrinovich (personal communication) have found that testosterone-injected females from the field may sing songs which are similar to the songs of a neighboring population. This is evidence against the idea that birds only disperse and mate within a song tradition, although there could still be some preference for mates from within a tradition. Baptista and Petrinovich also found that very few birds banded as nestlings survived within the song population. While many probably died, it also seems likely that some dispersed out of the area. Baker and Mewaldt (1978) banded birds as juveniles rather than as nestlings, and it is possible that a significant portion of the juveniles had already dispersed a considerable distance. Finally, even though white-crowned sparrows in the laboratory are capable of learning songs prior to the age when dispersal would normally occur in nature (Marler, 1970), actual patterns of vocal learning in nature have not been documented. Given the stimulation of adult singing males in nature rather than the monotonous repetition of a song pattern over a loudspeaker, a juvenile may be able to alter his song patterns much later in life (Kroodsma, 1978b). As we have already mentioned in Section 11, there are two published studies in which juveniles of known parentage have been followed during dispersal, and sonagrams of song patterns of fathers and sons have been compared (Kroodsma, 1974; Jenkins, 1977). [Nice (1943) compared songs of fathers and sons without spectrographic analysis.] In agreement with both of these studies, and with Payne’s evidence that parasitic indigo birds change their song types according to their breeding site, two unpublished studies on the great tit (McGregor et al., 1980) and Swamp Sparrow (Kroodsma and Pickert, 1980) have shown that young males do not preferentially learn their father’s songs (see Section II,B,3). Jenkins (1977) suggested that in the saddleback young males avoid settling near males with song types similar to their own fathers’ songs. This is in com-

VARIATION I N BIRD SONG

I67

plete contrast to the idea discussed earlier for white-crowned sparrows. Jenkins recognized four song groups in his island population of saddlebacks, and studied five father-son combinations. All five sons settled outside their father’s song group. This evidence may not be as convincing as appears at first sight, since it is likely that many young would settle outside the parental song group even if dispersal were random with respect to song type. If, for example, each young male had an equal chance of settling anywhere on the island, and if song groups were equal in size, three-quarters of the young males would breed outside the parental song group. Since three of the five males studied by Jenkins were born in the smallest song group, the chance of settling within the father’s song area is even smaller. Thus it is possible that Jenkin’s results do not differ significantly from chance, but more detailed calculations cannot be made without more information. 4 . Repertoire Size and Spatial Variation As repertoire size increases, thorough documentation of the spatial distribution of song components becomes extremely difficult. For example, obtaining the repertoire for an individual with 20 to 50 song types might take 1 to 2 days; at the extreme, adequately documenting the vocal repertoire of a male brown thrasher (Tamstoma rufurn) would require weeks and involve more than a million comparisons among thousands of spectrograms (Kroodsma and Parker, 1977). Studies of geographical variation require analyses of many individuals, and it is not surprising that some of our best data come from species in which males sing only one song type (e.g., Baptista, 1975; Bradley, 1977; Thielcke, 1969). Some insights into the relationship between song repertoires and the existence of sharp boundaries between song populations may be obtained by comparing three species: the white-crowned sparrow (subspecies nurtaffi) with one song type/individual (Baptista, 1975), the saddleback with an average of two songs/ individual (Jenkins, 1977), and the Bewick’s wren with an average of 16 song typeshdividual (Kroodsma, 1974). When comparable numbers of song components are examined for each species, the patterns of variation through space are strikingly similar. In all three species, studying a single song type (which is all a white-crowned sparrow has, but which is only a portion of the repertoire of the other two species) reveals the following. Some song types (or some aspect of them) may be restricted to males which share contiguous territories, and sharp boundaries with no discernible changes in habitat features may exist beyond which a given song type does not occur. Males near the boundaries may have hybrid songs, including in a single song type characteristics of songs which typically occur on opposite sides of the boundary or they may be “bilingual” (Baptista, 1975) and have enlarged song repertoires [Jenkins, 1977; see also Kaiser (1965), and Mundinger (1975) for similar data on the yellowhammer (Ernberiza citrinella) and house finch (Car-

168

JOHN R . KREBS A N D DONALD E . KROODSMA

poducus mexicanus), respectively.] Thus, identifying a local area in which virtually all males share a single song type or component can be relatively straightforward, given that song types can be classified (see Section 11,A). The larger song repertoires, on the other hand, complicate attempts to delineate areas with homogeneous vocal behaviors. Jenkins (1977), in studying saddlebacks with 1.4 to 1.9 songs per male, found that, by extensive culling of distribution patterns which seemed of lesser importance, he could define areas to which certain combinations of song patterns were restricted. The task becomes very difficult indeed when one considers the Bewick’s wren in Oregon, where males possess an average of about 16 song types each. Even though males share most of their songs with each immediate neighbor, different song types or song components may have very different yet well-defined spatial distributions; attempts to delineate geographical areas with a given set of unique vocal behaviors are doomed to failure. 5 . The Functions of Dialects We have so far avoided using the term dialect. Instead we have referred to cultural song traditions, song neighborhoods, microgeographical variations, and so on. Some authors would use the term dialect to refer to all of these local variations in song type which can be attributed to vocal learning, while others use the word dialect to refer only to contiguous populations with clearly differentiated vocal patterns. We prefer to use the term in its more general sense, rather than abandoning it altogether as some have advocated (Mulligan, 1975). The operational criterion for recognizing the occurrence of dialects is that neighboring birds have songs which are more similar to one another than to the songs of more distant birds. There may or may not be clearly delineated boundaries between dialects, and questions about how, when, and where young males learn song types are more likely to be fruitful than attempts to define dialect boundaries have been. As with repertoires which we discussed in Section 11, it is unlikely that any single explanation will account for the selective forces leading to dialect formation. However in attempting to assess various hypotheses it is useful to think of the question of the functions of dialects in two parts: the question of why birds learn to sing, and why learned songs vary from place to place. The relationshp between learning and dialects has been viewed in two ways in the past. On the one hand it has been argued that the formation of local dialects is one of the most important selective factors favoring learning (Nottebohm, 1972), while on the other hand some view dialects as mere epiphenomena of song learning which is favored in some other context, such as matched countersinging between neighbors (Section II,B,2,b). If songs are learned and dispersal after learning is restricted, dialects are very likely to arise. As we have discussed, the evidence from a number of studies does not support the view that learned dialects

VARIATION IN BIRD SONG

169

act as strong barriers to prevent dispersal and intermixing of neighboring populations. Even if one accepts that it is advantageous for individuals to mate with partners sharing similar adaptations to the local environment, there is no convincing evidence that dialects are used as a mechanism to promote assortative mating. There might still, however, be slight effects which are detectable only on a much longer time scale. M. C. Baker (personal communication) has found, by comparison of the number of subspecies per species in different avian groups, that speciation appears to be more rapid in species with vocal imitation than in other groups. Similarly, among red-winged blackbirds and rufous-sided towhees (Pipilo erythrophthalamus) males of the widespread and largely migratory eastern nominate subspecies share few songs with neighbors, while males in the more restricted, largely resident western subspecies share many songs with neighbors (Kroodsma, 1971; Ewert, 1978; E. Morton, personal communication; K. Yasukawa, personal communication). Among the two Cistothorus wrens, the marsh wren imitates song and has subspeciated considerably, while the sedge wren improvises songs and has not subspeciated. It could be argued from these data that sedentary habits and site fidelity are either a cause or a consequence of well-developed local dialects. Although sedentary habits may be essential for both rapid speciation and dialect formation, the evidence suggests that vocal learning itself is not a prerequisite for rapid formation of new species. The Tyrrannid flycatchers, for example, have undergone intense speciation to produce over 1000 species, but they are not known to have vocal learning (Nottebohrn, 1972). In some species with clearly defined dialects, the spatial distribution of songs may arise as a consequence of microgeographical separation of small populations of singing males. For example, Lemon (1975) speculates that dispersing cardinals may introduce new songs into a breeding area, and Baker (1975) discusses the possibility that the relatively discrete song dialect areas in Nuttall’s whitecrowned sparrow of coastal California are a consequence of recolonization of regenerating habitat in a fire climax community; the existence and location of boundaries between dialect areas are then a result of secondary contact between two formerly isolated populations. In summary, there is rather conflicting evidence relating to the idea that vocal learning plays a role in promoting or maintaining genetic isolation between neighboring populations. An alternative idea is that dialects arise either as a by-product of vocal imitation of neighbors by young males, andlor as a result of geographical separation of local groups of singing males. Vocal imitation of neighbors may be favored for the kinds of reason discussed in Section II,B,2: if young birds learn songs from their parents (this does not seem to be the case in the few species so far studied) kin recognition might be an important consequence of learning. Vocal imitation may simply be an economical way of acquiring a large repertoire, or it may result in song sharing between neighbors, which

170

JOHN R. KREBS AND DONALD E. KROODSMA

could be important if songs are used in matching duels (Section II,B,2). R. B. Payne (personal communication) suggests that by imitating the song of the most successful male in a display group, a subordinate individual can deceptively take over the successful site if its owner disappears. Thus although there is much descriptive evidence to show that dialects exist, much more detailed information will be needed to evaluate specific hypotheses about their significance.

IV. CONCLUSION We started out by considering repertoires and dialects as two separate questions, but our conclusion is that the same kinds of data are required to understand the functional significance of both phenomena. In order to understand why birds learn to sing, and why songs vary within an individual and between populations, it will be necessary to collect more information on the following points: where, when, and from whom young birds learn their songs; how and why differences in reproductive success between males are related to differences in vocal behavior; and how female choice of mates is related to male songs.

Acknowledgments We thank the Science Research Council (J.R.K.) and National Science Foundation (D.E.K.) for financial support. A number of people kindly allowed us to quote from their unpublished results: L. Baptista, P. K. McGregor, K. Yasukawa, L. Petrinovich, J. Baylis, M. Baker, C. Catchpole, G. Morton, P. Slater, and C. M. Perrins.

References Armstrong, E. A. 1973. “A Study of Bird Song.” Dover, New York. Avery, M., and Oring, L. W. 1977. Song dialects in the bobolink (Dolochonyxoryzivorus). Condor 79, 113-118. Baker, M. C . 1974. Genetic structure of two populations of white-crowned sparrows with different song dialects. Condor 76, 351-356. Baker, M. C. 1975. Song dialects and genetic differences in white-crowned sparrows (Zunorrichia leucophrys). Evolution 29, 226-241. Baker, M. C . , and Mewaldt, L. R. 1978. Song dialects as barriers to dispersal in white-crowned sparrows, Zonotrichia leucophrys nuttalli. Evolution 32, 712-722. Baker, R. R., and Parker, G. A. 1979. The evolution of birdcoloration. Proc. R . Soc. London, Ser. B 287, 63-130. Baptista, L. F. 1975. Song dialects and demes in sedentary populations of the white-crowned sparrow (Zonotrichia leucophrys nuttalli). Univ. Calq.. Berkeley, Publ. 2001.105, 1-52. Baptista, L. F., and King. J. R. 1980. Geographical variation in song and song dialects of montane white-crowned sparrows (Zonotrichia leucophrys oriantha). In preparation.


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ADVANCES IN THE STUDY OF BEHAVIOR VOL. I I

Development of Sound Communication in Mammals GUNTEREHRET FAKULTAT RIOLOGIE UNIVERSITAT KONSTANZ KONSTANZ, FEDERAL REPUBLIC OF GERMANY

1. Introduction ............................................ 11. Components of Sound Communication Systems: General Aspects Development . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . III. Time Courses of the Development of Vocal Behavior and Hearing in Subhuman Mammals and M a n . , . , . , . . . . . . . . . . . . . . . . . . . . . . , . . , , . , , . . A. Chiroptera . . . . . . . . . . . . . . . . . . . . . . . . . . . . . B. Carnivora . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . C. Rodents . . . . . . . . . ................................ D. Primates . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . IV. Characteristics and Co nt 0 Behavior . . . . . . . . . . . . .... Ut ............. A. Development of Phys 9 . Does the Development of Vocalizations Depend on Hearing? . . . . . . . . . C. Do External Stimuli and Behavioral Contexts Influence the Development of Vocalizations'? . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . D. Does Arousal Influence the Development of Vocalizations? . . . . V. Characteristics and C Communication . . . . . A . Can Infant Mamm B. Do Infant Mammals React to Sounds of the Adults? . . . . . . . . . . . . . . . . . C. Which Features of Infant Calls Do Adults Respond to? . . . D. Does Adult Responsiveness Paralle the Young? . . . . . . . . . . . . . . . . . . E. Nonacoustic Determinants of Adult Response Behavior . . . . . . . . . . . . . . VI. Conclusions .................................. VII. summary.. . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

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I. INTRODUCTION Adult mammals generally hear and they vocalize in quite a number of different behavioral contexts. The sound they produce may have communication effects in I79

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that it regularly alters the behavior of members of their own or of other species. This definition of sound communication will be used in this study and it is similar to a more general definition by Altmann (1967): “Social communication is a process by which the behavior of an individual affects the behavior of others. . . [by that] we mean that it changes the probability distribution of the behavior of others” (p. 326). We should be aware of pitfalls in using the term sound communication, which, strictly speaking, is justified only after we have established a consistent relation between the sound signal emitted by one animal and the alteration of behavior in another animal. Obviously investigating “sound communication” is always more difficult than recording “vocal behavior. In the latter one has to observe the behavior and the behavioral context of sound production in one animal, the sender, only, whereas in the former we deal with the behavior of two animals at least, which interact. Further, if the animals can see, feel, or smell each other in addition to hearing each other we face the problem of separating communication by sound from all the other possible modes. In this article an attempt is made to distinguish between vocal behavior and true sound communication. This may be helpful not only for organizing research but also and particularly for understanding ontogenetic and phylogenetic sequences of development of sound communication. It is different to ask whether an animal in a special motivational or emotional state vocalizes as an integrated part of its behavior or whether such vocalizations have signal characteristics capable of influencing the behavior of others. Our knowledge of vocal behavior in mammals exceeds what we know about sound communication by far. This is especially true with regard to the development of sound communication in young mammals. There are numerous questions on the interaction by sound between young and adults and among young during development. Many of these questions are relevant in understanding ( a ) the general organization of behavior in young and adults, ( b ) the interrelation between innate maturation patterns and influences of the social environment on the adult behavior, and ( c ) the significance of sound communication in mammals with different habitats and social organization. The purpose of this article will not and cannot be a comprehensive survey of the literature on this topic. The intention is to review the research on those mammals for which sufficient data exist and derive some common foundations and guidelines concerning the development of sound communication in mammals. Human data on the development of acoustic behavior are also included for comparative rather than for linguistic purposes. It need not be mentioned that one condition for sound communication is hearing, at least in the receiver. Thus we have to consider both the development of sound production and of hearing in order to understand who, physiologically, is able to communicate with whom. Many rodents, for example, are born in a very altricial state and do not hear during the first days of life. Therefore sound ”

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communication among the littermates is simply impossible although they can produce a variety of sounds from birth. We should also consider the analytical capacities of the auditory systems of mammals when we are interested in details of sound parameter detection and information extraction. In the development of echolocation in bats, for example, it is most important that the frequency bands of ultrasonic calls match with those of extremely good acoustic analysis. One could argue that the echolocation system in bats is one of “self-communication” rather than one of social importance. Although few data are available on sound communication in bats, there are many other mammals that produce very complex sound patterns and also ultrasound’ during infancy, so that the ability for complex sound analysis has general importance. As far as data are available, sound patterns and auditory acuity will be compared in order to approach questions of the development of “feature detection” in communication sounds.

II. COMPONENTS OF SOUND COMMUNICATION SYSTEMS: GENERAL ASPECTS OF DEVELOPMENT When we study the ontogeny of sound communication in a mammal we have to consider time courses of development of the components of the sound communication system. Why does a dog not bark in his first days of life (Rheingold, 1963; Cohen and Fox, 1976)? Is it because his vocal repertoire has not yet matured, or must he learn how to bark? Is it because an undeveloped vocal tract makes it physically impossible for him to bark? He may need external and/or internal stimuli, a special motivation, or a special behavioral context, which are not present in the nest. Or, is he not barking because he cannot hear? The answers to these questions all contribute to our understanding of the ontogeny of vocal behavior in the dog; however, they do not tell us whether or not a dog communicates by barking. In addition to the development within the sender and to changes of his environment we have to measure the behavior of a potential, usually conspecific, receiver. More precisely, we must determine the responses of another dog to the developing acoustic behavior of a puppy. These may range from no overt response to a call to a very strong and specific response. Again developmental changes are possible as, for example, an increase in accuracy and selectivity of sound pattern recognition or a decrease of the response threshold to a particular call. Figure 1 summarizes the main components of a sound communication system and shows examples of developmental changes that may occur. It also gives an ‘Calls with fundamental frequencies higher than 20 kHz will be referred to as ultrasound throughout this article. One reason is that ultrasonic communication has now been accepted as a general term for sound communication in the high frequency range (f > 20 kHz),especially in rodent communication.

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Frc. 1. Diagram of the main components of a sound communication system (inner circle) with developmental aspects of these components (outer circle). The diagram should be read from the sender side (circles) starting with the behavioral context and stimuli a sender is exposed to. Neural mechanisms representing the vocal repertoire within the brain will be activated to coordinate nervous patterns which will activate mechanisms of sound production, so that a sound signal is produced. A receiver (triangles) perceives the auditory input via the cochlea. Neural mechanisms will decode and filter the excitation pattern from the cochlea and transfer it to brain centers which can recognize signal-specific excitation patterns and will activate corresponding motor centers to produce behavior. The behavior of the receiver can feed back on the original behavioral context or on the stimuli which induced the sender to vocalize. By that, the communication system is closed. The rectangles of the diagram include some aspects and questions which have to be considered when investigating the development of the communication system.

idea of the diversity of starting points for research in the field of development of sound communication. So far points of major interests have been the behavioral contexts of sound production and the vocal repertoires of the developing young on the one hand and the development of hearing on the other. Descriptive data are accumulating but there are few detailed analyses of changes in behavioral contexts, stimuli, and motivation which could be the basis of developing vocal behavior. Thus we have a more or less incomplete knowledge of what happens during the ontogeny of the sender for a number of mammals, but we know almost nothing at all about why it happens. We have evidence that neonates and juveniles produce calls which are specific for their age and which do not occur in

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adults (compare Figs. 2-12). The mechanisms underlying these changes in vocal repertoire are not well understood. Areas ripe for study are the development of neural mechanisms of sound pattern recognition, the development of behavioral responsiveness to sound, and, most interesting for ethologists, the development of sound-mediated social interactions among littermates and between parents and their young. This brief outline of what has to be done rather than of what has been done will, I hope, set the stage for a critical and more holistic view of the data which will be presented and of the conclusions which will be drawn.

III. TIMECOURSES OF THE DEVELOPMENT OF VOCALBEHAVIOR AND

HEARINGIN SUBHUMAN MAMMALS A N D MAN

Many studies of the vocal behavior in mammals include data on the vocal repertoire of the young and the behavioral contexts in which they vocalize. Thus we have evidence for sound production by the young in most of the orders of the class Mammalia, such as Marsupialia (Eisenberg et al., 1975), Insectivora (Gould, 1969; Poduschka, 1977), Perissodactyla (Kiley, 1972; Klingel, 1977), Artiodactyla (Tembrock, 1968; Kiley, 1972), Hyracoidea (Fourie, 1977), Cetacea (Caldwell and Caldwell, 1977), and Lagomorpha (Eisenberg and Kleiman, 1977). More comprehensive investigations on the development of vocal behavior and hearing are available for species in the orders chiroptera, carnivora, and rodentia, and for primates. In the following we will be concerned with representatives of these orders. Diagrams of the development will be shown (Figs. 2-13) including days of eye opening, weaning, and sexual maturation and some other characteristic dates in the development of the young. It is important to note that the names used to characterize calls of the different species are mostly derived from situations in which the calls are produced or from the physical characteristics of the sound. They do not imply any function a call may have to influence the behavior of the other animals. Further, we cannot be sure whether the vocal repertoires described for the mammals shown in Figs. 2-12 are complete or not. Additional studies may find additional calls with different time courses of development. A.

CHIROPTERA

Bats are well known for emitting ultrasound for echolocating prey and for orienting in their environment. Since they extract information from the echoes of their own calls and change their behavior accordingly, one can speak of a highly specialized “self-communication system. The postnatal development of orientation sounds and other vocalizations was studied in the vespertilionid bats An”

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rrozous pullidus (Gould, 1975a,b; Brown, 1976), Eptesicus fuscus (Gould, 1971, 1975a,b), Myoris lucifugus (Gould, 1971, 1975a), and Myotis oxygnarhus (Konstantinov, 1973). Gould (1979) reports neonatal vocalizations in 10 species of Malaysian bats. Figure 2 shows data for Anrrozous. A very similar development was found in Eptesicus and Myotis. The young of the latter two species are born in a less altricial state and therefore progress in the development is made earlier than in Anrrozous (Gould, 1971, 1975a). Anrrozous starts hearing at the sixth or seventh day of life and adult sensitivity is reached by day 24 (P. E. Brown et al., 1978). The development of binaural hearing continues up to about day 28. Newborn Antrozous can produce only one call type, the isolation call. This call disappears from the vocal repertoire at about day 20. Another call characteristic for juveniles is the sound emitted just before take-off during the first month of self-reliant flight. The production of the other six calls starts at different times mostly after the onset of hearing, and adult patterns are reached around weaning at about day 50 at the latest. t

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isiol. Psychol. 94, 446-458. Stanton, M..Daily, W.,and Amsel, A. 1980. Patterned (single) alternation in 11- and 14-day-old rats under various reward conditions. J. Comp. Physiol. Psychol. 94, 459-471. Surridge, C. T., and Amsel. A . 1966. Acquisition and extinction under single alternation and random partial-reinforcement conditions with a 24-hour intertrial interval. J . Exp. Psvchol. 72, 361368. Sutherland. N. S., and Mackintosh, N. J . 1971. “Mechanisms of Animal Discrimination Learning.” Academic Press, New York. Thorndike. E. L. 191 I . “Animal Intelligence: Experimental Studies.” Macmillan, New York. Traupmann. K. L. 1972. Drive, reward, and training parameters, and the overlearning-extinction effect (OEE). Leurn. Morivcir. 3, 359-368. Tyler, D.W.,Wortz, E. C., and Bitterman, M. E. 1953. The effect of random and alternating partial reinforcement on resistance to extinction in the rat. A m . J. Psycho/. 66, 57-65. Vanderwolf, C. H., Kramis, R., Gillespie, L. A , , and Bland, B. H. 1975. Hippocampal rhythmic slow activity and neocortical low-voltage fast activity: Relations to behavior. In “The H i p pocanipus. Vol. 2: Neurophysiology and Behavior” (R. L. lsaacson and K. H. Pribram, eds.), pp. 101-128. Plenum, New York. Vorhea, H., Kleeman, C. R.,and Lehman, E. 1967. Oxytocin-induced stretch reaction in suckling mice and rats: A semiquantative bioassay for oxytocin. Endocrinology 81, 71 1-715. Wagner, A. R. 1961. Effects of amount and percentage of reinforcement and number of acquisition trials on conditioning and extinction. J. Exp. Psycho/. 62, 234-242. Wagner. A. R., Siegel, L.S., and Fein, G. G. 1967. Extinction of conditioned fear as a function of percentage of reinforcement. J . Comp. Physiol. Psycho/. 63, 160-164. Wakerley. J. B., and Lincoln, D. W. 1971, Intermittent release of oxytocin during suckling in the rat. Nature (London) 233, 180- I81. Walker, D. W., Messer, L. G . , Freund, G . , and Means, L. W. 1972. Effect of hippocampal lesions

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and intertrial interval on single-alternation performance in the rat. J . Comp. Physiol. Psychol. 80, 469-477.

Warburton, D. M. 1969. Effects of atropine sulfate on single alternation in hippocampectomized rats. Physiol. Behav. 4, 64-644. Warburton, D. M.1972. The cholinergic control of internal inhibition. I n “Inhibition and Learning” (R.Boakes and H. Halliday, eds.), pp. 431-460. Academic Press, New York. Wickelgren, W. A. 1979. Chunking and consolidation: A theoretical synthesis of semantic networks, configuring in conditioning, S-R versus cognitive learning, normal forgetting, the amnesic syndrome, and the hippocampal arousal system. Psychol. Rev. 86,44-60. Wolfe, J . W., Lubar, J. F., and Ison, J. R. 1966. Effects of medial cortical lesions on appetitive instrumental conditioning. Physiol. Behav. 2 , 239-244.

ADVANCES

~~

~~

M THE STUDY OF BEHAVIOR VOL.

II

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Ingestional Aversion Learning: Unique and General Processes' MICHAELDOMJAN DEPARTMENT OF PSYCHOLOGY UNIVERSITY OF TEXAS AT AUSTIN AUSTIN, TEXAS

I. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . ...... . .. . . . . . . . . .... A. Taste-Aversion Experiments and Expectations Based on Associative Interpretations . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . B. Aspects of Taste-Aversion Learning That Cannor Be Attributed to Sensitization Effects of Poisoning . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . C. The Role of Neophobia and Poison-Enhanced Neophobia in Ingestional Aversions . . , . . , , . . , . . . . . . . . . . , , . . . . . . . . . . . . . . . . , . , . . . . . . . . . . . 111. Poison-Avoidance Learning and the Complexity of the Ingestive Sequence . A . The Role of Ingestion in Taste-Aversion Learning. . . . . B. The Role of Ingestion in Odor-Aversion Learning . . . . . . . . . . . . . . . . . . . C. Learned Aversions to Nongustatory Orosensory Stimuli . . . . . . . . . . D. Ingestion as a Source of Stimuli That Mediate Conditioned Aversion Nongustatory Cues E. Ingestion as a Dete F. Ingestion and Poison-Avoidance Learning: Overvie .......... 11. The Associative-Nonassociative Controversy

276 278 219 282 284 292 292 296 300

C. Proximal Unconditioned Stimulus Reexposure .

300 302 303 303 303 308 317 318 319 320 324

Ingestional Aversion Learning , . . . . . . , , , . . . . . . . . . . . . . , . . . . . . . . . . . . . . .......... References . . . . . . . . . . .

326 330

B. Interpretations of the Selective Association Effect . . . . .

'Preparation of this manuscript was supported by Grant MH 30788-01 (from the U . S . Public Health Service) and BNS 77-01552 (from the U.S. National Science Foundation). 215

Copyright 0 1980 by Academic Ress. Lnc. All nghrr of reproduction in any fonn reserved. ISBN 0-12-004511-7

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I.

INTRODUCTION

Poisons play an important role in the organization of plant and animal life. Although nonliving matter can be poisonous, many of the poisons that are of ecological importance are “secondary substances” synthesized by plants to govem their relationship to other plants and animals (Whittaker and Feeny, 1971). Certain of the higher plants, for example, synthesize poisons which inhibit the germination and growth of seeds of other plants which would otherwise provide competition for space and mineral resources. Others produce substances toxic to animals. Since plants are the basic food source for the animal kingdom, the presence of poisons in plants has provided evolutionary pressure for the development of mechanisms that protect animals against toxins, Some animals have evolved mechanisms for detoxifying certain poisons. Others sequester the poisonous substances so as not to experience the toxic effects. Detoxification and sequestration mechanisms provide animals with access to poisonous food avoided by other animals. In certain cases, the presence of a specific poison has even come to act as an attractant which guides animals with detoxifying or sequestering mechanisms to the poisonous plant (Whittaker and Feeny, 1971). Although sequestering poisons achieves some of the same effects as the detoxifying mechanisms, sequestration has the additional advantage of making the animals unpalatable to their predators. For example, monarch butterflies readily feed on milkweed containing cardiac glycoside poisons that do not affect them but are toxic to blue jays that feed on the monarchs (Brower et al., 1967). In addition to detoxification and sequestration mechanisms that protect animals from the effects of poisons, many animals have evolved a learning mechanism whereby they come to avoid eating substances that have made them sick on previous occasions. This learning mechanism of poison avoidance is potentially the most versatile of the three poison-protection mechanisms because it can provide a defense against just about any substance that produces postingestional malaise (Gamzu, 1977). Therefore, this mechanism is very important for omnivorous species, which select their diet from a wide variety of substances whose availability is constantly changing. Of the various defenses against poisoning, psychologists are most interested in this learning mechanism of poison avoidance. Current psychological research on poison-avoidance learning developed from several applied research programs started as a result of problems encountered during World War 11. Two of these programs involved attempts to develop effective rodent control techniques in the United States and the United Kingdom. In the course of this work it soon became apparent that rats avoided poisoned bait if they had previously experienced aversive postingestional effects after eating such bait (Richter, 1953; Rzoska, 1953). Thus, successful rodent population

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control through the use of poisoned foods requires poisoned bait that kills rats the first time it is eaten. A third research program involved investigating the behavioral effects of exposure to ionizing radiation. The results of greatest interest to psychologists were obtained with irradiation used as an unconditioned stimulus in a learning paradigm. Rats learned aversions to the taste of a relatively novel saccharin solution, for example, when ingestion of the saccharin was followed by exposure to y-radiation (Garcia et a / . , 1955). The two rodent control programs did not stimulate much systematic scholarly research on poison-avoidance behavior, although they formed the basis of a rather interesting agricultural application in which poison-avoidance behavior in mice was shown to be of potential benefit to farmers of Douglas fir in northern California (Tevis, 1956). Once Douglas fir is logged in certain areas of northern California, the region becomes invaded by tan oak because conditions are not favorable for the growth of conifers. Attempts to seed denuded areas with Douglas fir often failed because forest mice consumed the seeds. Extermination of the mice is not effective because nonpoisoned mice from neighboring areas quickly invade the exterminated territory. The problem can be solved, however, by adding a nonlethal poison to the Douglas fir seeds so that mice learn to avoid eating Douglas fir seeds without being killed or leaving the area (Tevis, 1956). In contrast to the rodent control programs, early demonstrations that rats acquire taste aversions as a result of exposure to ionizing radiation after experiencing the taste have stimulated much further research. This work was at first pursued primarily by John Garcia and his colleagues and later attracted the attention of James Smith, Paul Rozin, Marvin Nachman, Sam Revusky, and others. Through the efforts of these investigators and their intellectual descendents, the taste-aversion learning paradigm has become one of the most popular procedures for the investigation of learning (Barker e t a / . , 1977; Milgram e t a / . , 1977). A recent bibliography of reports relevant to this area listed 632 titles (Riley and Clarke, 1977). The current interest in taste-aversion learning developed in response to two landmark discoveries published in 1966. One of these (Garcia et a / . , 1966) involved the observation that rats will learn an aversion to a taste experienced before an aversive drug treatment or radiation exposure even if the interval between the taste and the consequent malaise is more than an hour. This phenomenon has come to be called the long-delay learning effect. The second major discovery (Garcia and Koelling, 1966) was that for rats taste stimuli are much more readily associated with toxicosis than are audiovisual cues, whereas audiovisual cues are much more readily associated with peripheral pain produced by footshock than are taste cues. This variation of the conditionability of tastes and audiovisual cues as a function of the use of toxicosis and footshock could not be attributed to differences in the salience or intensity of the individual events. Therefore, the experiment demonstrated that the strength of conditioning is

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greatly influenced by the combination of conditioned and unconditioned stimuli used. This phenomenon has come to be called the selective association or cueconsequence specificity effect. The long-delay learning and the cue-consequence specificity effects attracted a great deal of attention to the taste-aversion learning paradigm because they were unlike any other phenomena previously observed in conditioning laboratories. The reaction of some investigators to the uniqueness of these phenomena was to challenge interpretations of them as instances of associative learning (e.g., Bitterman, 1976; McLaurin, 1964; McLaurin and Scarborough, 1963). This approach to the long-delay learning and cue-consequence specificity effects makes it unnecessary to try to incorporate these findings into theories of learning. Another approach to the uniqueness of taste-aversion learning phenomena has been to use these effects to argue that previously formulated laws of learning are not generally applicable and that the pursuit of general laws of learning is an ill-fated venture (e.g., Hinde and Stevenson-Hinde, 1973; Rozin and Kalat, 1971; Seligman, 1970; Seligman and Hager, 1972; Shettleworth, 1972a). This approach contends that each instance of learning is best understood as an evolutionary adaptation to a particular challenge to survival and that learning mechanisms that evolve to deal with one such challenge may not necessarily have much in common with mechanisms that evolve to cope with other situations. The thesis of the present article is that neither of the above reactions to the findings of taste-aversion experiments is justified. Taste-aversion learning is indeed an associative process, and many aspects of it fail to challenge the existence of general laws of learning. Since there have been numerous detailed reviews of these issues in recent yeas (e.g., Logue, 1979; Revusky, 1977b; Spiker, 1977; Testa and Ternes, 1977), the present article will not attempt to be comprehensive. Rather, it will focus on several aspects of the research that my colleagues and I have conducted in the past decade that are relevant to these questions. Most of the experiments to be described were performed with laboratory rats. There is some reason to believe that the food selection behavior of rats is similar to that of other omnivores such as man (Rozin, 1976). However, it is unlikely that ingestional aversion learning in rats is representative of aversion learning in the feeding system of disparate animals such as insects and cephalopods.

II. THEASSOCIATIVE-NONASSOCIATIVE CONTROVERSY One of the recurring controversies involving research on ingestional aversions has been whether or not the enduring aversion to a taste which results from postingestional malaise following taste exposure represents an association between the flavor and the aversive postingestional event. The argument against an associative interpretation of ingestional aversions has taken three different forms.


279

First, it was suggested that results of taste-aversion experiments do not conform to expectations based on an associative interpretation (McLaurin, 1964; McLaurin and Scarborough, 1963). Then, it was suggested that critical tasteaversion experiments failed to include important control groups to rule out nonassociative interpretations (Bitterman, 1975, 1976). Finally, it was suggested that certain nonassociative processes are activated by tastes and aversive interoceptive stimulation, and these processes may obscure evidence of the operation of associative mechanisms in the acquisition of ingestional aversions (Mitchell, 1978; Mitchell et al., 1977). I will discuss each of these criticisms in turn. A N D EXPECTATIONS BASEDON A. TASTE-AVERSION EXPERIMENTS ASSOCIATIVE INTERPRETATIONS

I . Early Experinierits Investigators of taste-aversion learning have been concerned from the beginning of this field of research with demonstrating the associative basis of ingestional aversion. In one of the early experiments, for example, Garcia and Kimeldorf (1957) investigated the importance for aversion learning of the temporal relationship between drinking saccharin and exposure to y-radiation. Four groups of rats were exposed to radiation for 4 hr, and a fifth group served as nonirradiated controls. The manipulation of interest was when a highly palatable saccharin solution was made available in relation to the radiation exposure. One group had the saccharin available for 2 hr just preceding the 4-hr exposure period. Other groups had the saccharin available during either the first or last 2 hr of irradiation, while the last irradiated group had saccharin available for 2 hr just after irradiation. These treatments are analogous to trace, simultaneous, and backward conditioning sequences often tested in classical conditioning (Kimble, 1961, pp. 47-48). Groups having the saccharin solution available during exposure to irradiation (simultaneous conditioning) learned stronger aversions to saccharin than subjects that had saccharin available just before irradiation (trace conditioning), although the trace conditioning group also learned an aversion to saccharin. In contrast, subjects having the saccharin solution available just after irradiation (backward conditioning) failed to learn a taste aversion. Garcia and Kimeldorf interpreted their results as demonstrating the role of associative mechanisms in aversion learning because the groups that received exposure to both saccharin and radiation did not all acquire equivalent aversions to saccharin. Rather, aversion learning required that the saccharin and radiation exposure occur in certain temporal arrangements. Simultaneous exposure to saccharin and radiation produced the strongest aversions, and no aversion was evident in subjects given saccharin to drink after radiation exposure. In contrast to Garcia and his colleagues, several other investigators expressed

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doubts about a learning interpretation of radiation-induced aversions. McLaurin and Scarborough (1963) pointed out that the trace conditioning procedures used by Garcia and his colleagues to condition taste aversions with ionizing radiation may have allowed delays between exposure to the taste and subsequent irradiation on the order of several minutes, delays which, on the basis of work in other learning preparations, would not be expected to support associative learning (Kimble, 1961, pp. 155-160). For example, in the Garcia and Kimeldorf (1957) experiment, subjects in the trace conditioning group received access to saccharin for 2 hr prior to irradiation. No data concerning temporal drinking patterns during the 2-hr period are presented. However, since subjects were water deprived, they probably drank to satiation long before the end of the 2-hr period, thus introducing a delay between taste and subsequent irradiation. Troubled by this possibility, McLaurin and Scarborough (1963) sought to determine the effects of various delays between exposure to a taste and subsequent irradiation. If taste aversions reflect an association between taste and radiation distress, then progressive delays between exposure to a taste and subsequent irradiation should result in progressive decrements in taste-aversion learning. McLaurin and Scarborough (1 963) assessed the saccharin aversion learning of rats exposed to X-irradiation 0, 25, or 50 min after a 10-min period of access to saccharin. Aversions were measured in saccharin-water preference tests conducted soon after conditioning. Contrary to predictions from a learning interpretation, progressive delays between exposure to saccharin and radiation did not weaken the taste aversions observed. Even the group exposed to radiation 50 min after drinking saccharin, an interval unprecedented for usual demonstrations of associative learning, acquired a strong aversion. McLaurin ( 1964) repeated the McLaurin-Scarborough experiment with groups of rats exposed to X-irradiation 3,60, 120, and 180 min after access to saccharin. The saccharin preference of subjects was tested immediately after irradiation. As in the previous experiment, all irradiated subjects acquired aversions to saccharin with no differences among the 60-, 120-, and 180-min delay groups. Introducing delays between the taste and X-irradiation again did not have the expected decremental effect on taste-aversion learning. Further evidence against a learning interpretation of the radiation-induced taste-aversion effect was obtained in a group that had not been given saccharin prior to X-irradiation but also evidenced an aversion to saccharin during the postirradiation test.

2.

Establishing the Delay Gradient

In contrast to the findings of McLaurin and Scarborough, numerous other investigators have found orderly decrements in taste-aversion learning as a function of the delay between access to a flavor and subsequent toxicosis. In the first such demonstration Garcia et a f . (1966) used apomorphine hydrochloride injections (7 mgkg, ip) as the US instead of X-irradiation and compared groups of

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28 1

rats injected with the toxin 30, 45, 75, 120, and 180 min after access to saccharin. Five conditioning trials were conducted, and subjects were tested for their response to saccharin 3 days after the last conditioning trial. Increasing the delay between access to saccharin and the apomorphine injections during conditioning attenuated the learning of saccharin aversions, and no aversions were learned in groups in which the apomorphine injections were delayed 120 or 180 min. The basic finding of Garcia et (11. (1966) that delays between taste and toxicosis result in orderly decrements in taste aversion learning have since been replicated by numerous other investigators (e.g., Kalat and Rozin, 1971; Nachman, 1970; Revusky, 1968; Smith and Roll, 1967; Wright er al., 1971). Furthermore, the difference in results between these experiments and the experiments of McLaurin and Scarborough cannot be explained in terms of the unconditioned stimulus used, since at least two of these studies also used X-irradiation (Revusky, 1968; Smith and Roll, 1967). The inconsistency between the experiments of McLaurin and Scarborough and the subsequent studies was resolved by a series of experiments that showed that rats can learn aversions to flavors experienced immediately after exposure to X-irradiation, presumably because the aversive effects of radiation last for a considerable time after radiation exposure (McLaurin et af., 1964; Morris and Smith, 1964; Scarborough et al., 1964; Smith et al., 1965; see also review by Smith, 1971). In the experiments of McLaurin and Scarborough all subjects were tested for saccharin aversions soon after exposure to X-irradiation. Thus, groups with various delays between taste and toxicosis, as well as subjects not given saccharin before irradiation, had equal opportunity to associate saccharin given during the postexposure test with the prolonged aversive aftereffects of irradiation. This aversion learning motivated by the aversive aftereffects of X rays was probably responsible for the lack of differences among groups. The other studies of the effects of delay between taste and toxicosis avoided this technical problem by testing for taste aversions at least 24 hr after toxicosis, by which time the aversive aftereffects of the irradiation or toxins used were probably no longer present. The finding that taste-aversion learning is a decreasing function of the interval between taste exposure and the aversive postingestional events is important evidence of the role of associative processes in ingestional aversion learning. Since all of the groups in a delay of reinforcement experiment have the same exposure to the CS flavor and the US malaise, the gradient of aversion learning observed cannot be attributed to the individual experience of these events. For example, in the first successful delay experiment (Garcia et al., 1966), the aversion learning observed in groups that had been injected with apomorphine 30, 45, or 7 0 min after taste exposure could not be attributed merely to previous exposure to saccharin and apomorphine because groups that were exposed to these two events separated by 120 and 180 min did not learn aversions. Rather, the pairing or opportunity to associate the flavor and malaise was necessary for aversion learn-

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ing. [A nonassociative interpretation of the delay gradient was recently proposed by Mitchell et a / . (1977). This possibility is discussed in Section II,C,3.]

3 . Other Similarities between Taste-Aversion and Other Types of Learning

McLaurin and Scarborough (1963) were concerned with just one characteristic of associative learning: that less learning is evident as the delay between the conditioned and unconditioned stimuli is increased. However, there are many other phenomena that are also commonly observed in cases of associative learning, and one might ask whether or not these relationships are likewise observed with taste-aversion learning. This evidence overwhelmingly favors an associative interpretation of aversion learning. The details of this argument have been presented elsewhere (Logue, 1979; Revusky, 1977b; Spiker, 1977; Testa and Temes, 1977). Briefly, the following phenomena observed in many instances of associative learning can be also observed in taste-aversion learning. Aversion learning is an increasing function of the intensity of the taste CS (e.g., Nowlis, 1974) and the drug or radiation US (e.g., Nachman and Ashe, 1973). The taste aversion is extinguished if subjects experience the flavor without aversive consequences after conditioning (Garcia et a l . , 1955). Repeated exposure to the flavor CS without aversive consequences before conditioning reduces the degree of aversion that is learned (e.g., Revusky and Bedarf, 1967), and preconditioning exposure to the unconditioned stimulus also interferes with subsequent aversion learning (see Randich and LoLordo, 1979, for a review). Aversions learned to one flavored solution generalize to other similar flavors (Nachman, 1963), and there is a gradient of generalization such that subjects conditioned to avoid one taste do not avoid all other novel flavors (Domjan, 1975; Nachman, 1963). Aversion learning to one taste is disrupted if during conditioning subjects are exposed to other stimuli that were previously conditioned with the aversive US (e.g., Gillan and Domjan, 1977; Willner, 1978), and aversion learning is also disrupted when the taste of interest is not the best predictor of malaise (Luongo, 1976). Phenomena such as conditioned inhibition and sensory preconditioning also do not differentiate taste-aversion learning from other types of learning (Best, 1975; Lavin, 1976; Taukulis and Revusky, 1975).

B. ASPECTSOF TASTE-AVERSION LEARNING THATCANNOT BE ATTRIBUTED TO SENSITIZATION EFFECTS OF POISONING The second type of criticism made against associative interpretations of ingestional aversion learning has been that many of the widely cited experiments in the field failed to include control groups to rule out sensitization effects of poisoning (Bitterman, 1975; Mitchell et a l . , 1977). According to this argument the taste aversions observed in these experiments may have reflected merely the fact that


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the subjects were previously poisoned and not the fact that the subjects associated the taste with the poisoning experience. There has been a great deal of discussion about whether or not certain experiments had proper control groups for sensitization effects (Bitterman, 1976; Garcia, 1978; Garcia et al., 1976; Mitchell, 1977; Revusky, 1977a, 1978; Smith, 1978). Regardless of what control groups were or were not included in these experiments, there are a number of aspects of ingestional aversion learning that are contrary to predictions of a sensitization interpretation. One widely accepted criterion for the identification of associative mechanisms is the demonstration of stimulus discrimination (Gormezano, 1966). In a discrimination procedure, one stimulus (the c s + ) is paired with the US on some trials, and another stimulus (the CS-) is presented without the US on other trials. Complete discrimination is said to exist if the conditioned response occurs in response to the CS+ but does not occur in response to the CS- . If taste aversions develop through nonassociative mechanisms, equal aversions would be expected in response to both the CS+ and CS- flavors. However, this is not what is observed. Discrimination procedures typically yield differential aversions in the taste-aversion paradigm (e.g., Gillan and Domjan, 1977; Rozin, 1969). Another finding contrary to a sensitization interpretation is that animals that have one flavored solution paired with toxicosis do not subsequently avoid all other novel flavors (e.g., Domjan, 1975; Nachman, 1963). If the taste aversions were only a response to prior toxicosis, the aversions would not be specific to the flavor that was paired with toxicosis. There is some evidence that animals that learn an aversion to one novel fluid may subsequently avoid other very different novel flavors ( e . g . , Best and Batson, 1977). However, these observations also appear to be mediated by associative mechanisms because the nonspecific avoidance of novel flavors is attenuated by extinction of the aversion to the drug-paired taste (Best and Batson, 1977). It appears that if animals learn an aversion to one novel flavor, this conditioned aversion may generalize to other flavors along the dimension of flavor novelty. If ingestional aversions were due to nonassociative effects of poisoning, then animals that are exposed only to the toxin US or to the US unpaired with a flavor CS should evidence as strong aversions to a novel flavor later as animals that are treated with the aversive US after drinking the flavored solution. Such control groups have been included in many experiments, and the outcome is never as predicted by sensitization. Poison injections unpaired with a novel taste rarely suppress the intake of novel solutions during tests conducted 1 day or more later (e.g., Domjan, 1975; Mitchell er al., 1977; Monroe and Barker, 1979). When such a suppression is observed, it is transitory and disappears as subjects recover their baseline water intake levels from the toxicosis (Best and Batson, 1977; Carroll et al., 1975). Another line of investigation that fails to substantiate claims that enduring

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flavor aversions result from mere exposure to the toxin US concerns the effects of repeated exposure to the toxin US prior to taste-aversion conditioning. If exposure to the toxin US alone produces an enduring suppression in the intake of novel solutions, then subjects that receive repeated exposure to the toxin US before conditioning should be suppressed in their intake of the CS flavor during the conditioning trial. However, such suppressions are typically not observed (e.g., Braveman, 1975a; Cannon etal., 1975; Goudie etal., 1975a; Revusky et a / . , 1976). A related set of evidence is provided by experiments in which subjects receive exposure to the toxin US shortly (within several hours) before the usual pairing of the flavor CS with a consequent toxin US. Such a proximal US preexposure treatment increases the total toxicosis subjects experience on the aversion conditioning day. Therefore, if ingestional aversions reflected the nonassociative effects of toxicosis, then proximal US preexposure would be expected to facilitate aversion performance. However, contrary to this prediction, proximal US preexposure has been found to disrupt taste-aversion conditioning (Best and Domjan, 1979; Domjan, 1978; Domjan and Best, 1977).

C. THEROLEOF NEOPHOBIA AND POISON-ENHANCED NEOPHOBIA IN INGESTIONAL AVERSIONS The third type of criticism against associative interpretations of ingestional aversion learning is that evidence of associative mechanisms has been obscured by the possible occurrence of taste neophobia and poison-enhanced neophobia in taste-aversion experiments (Mitchell et al., 1975, 1977). Animals typically ingest very little of novel substances, and under certain circumstances this flavor neophobia can be increased by a prior poisoning experience (see Corey, 1978; Domjan, 1977a, for reviews). Therefore, the avoidance of novel solutions after a taste-toxicosis conditioning trial may in part reflect nonassociative neophobia and enhanced neophobia processes. One possible approach to determining the role of flavor neophobia and enhanced neophobia in ingestional aversion learning is to test control groups that would permit evaluation of the contribution of these processes. However, given the unending disputes that exist concerning the adequacy of various control procedures (Bitterman, 1975, 1976; Garcia, 1978; Garcia et al., 1976; Mitchell, 1977, 1978; Revusky, 1977a, 1978; Smith, 19781, it is unlikely that any set of control procedures would satisfy all investigators. Another, perhaps more fruitful, approach to this problem is to investigate the circumstances in which flavor neophobia and enhanced neophobia phenomena are prominent. Once these situations have been identified, it becomes much easier to decide whether or not particular taste-aversion conditioning procedures are likely to permit the flavor neophobia and enhanced neophobia to occur.

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I . Flavor Neophobia The degree of aversion or neophobia nonpoisoned subjects display to a novel solution no doubt depends on its taste. Some tastes are simply more distinctive from the animal’s customary diet than other flavors and will therefore evoke a greater aversion when first presented. It is difficult to quantify or manipulate distinctiveness. However, the concentration of flavored solutions usually covaries with novelty. For animals raised on ordinary laboratory chow and tap water, increasing concentrations of a solution will be increasingly distinctive from their customary fluid and will therefore evoke greater neophobia. The relationship between taste concentration and neophobia is illustrated by one of our experiments with aqueous solutions of saccharin (Domjan and Gillan, 1976). Laboratory rats were first adapted to a daily 23.5-hr deprivation schedule. They then received access to a saccharin solution for 30 min each day. This saccharin drinking period was always followed by access to water for 30 min so that the animals could satisfy their daily fluid needs even if they chose to drink very little saccharin. Each group of rats was tested with a different concentration of saccharin. Figure 1 shows the amount of saccharin each group drank during the daily test sessions. Subjects initially showed strong aversions to the 0.5, 1.0, 2.0,and 3.0% saccharin solutions. In contrast, the animals drank substantial amounts of the 0.15% saccharin from the first day. The initial aversions that were evident with the concentrated saccharin solutions were no doubt in part a response to

-

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FIG. 1 . Amount ingested by independent groups of rats given access to 0.15,0.5, 1 .O, 2.0, and 3.0%saccharin for 30 min daily. The saccharin drinking period was always followed by access to water for 30 min. Water intakes are not shown. Redrawn from Domjan and Gillan (1976).

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their novelty; subjects increased their intakes as they were repeatedly tested and received exposure to the flavors. The smallest increase in consumption with repeated testing occurred with the 0.15% saccharin solution, indicating that this solution initially elicited very little neophobia. The intakes of 0.5 and 1.0% saccharin eventually matched the intake of 0.15% saccharin. However, the intakes of the 2.0 and 3.0% solutions never reached this level. The difference in the asymptotic levels of drinking achieved with these solutions may be interpreted as indicating that the response to the 2.0and 3.0% solutions was not completely determined by their novelty. Results such as those presented in Fig. 1 suggest that complications arising from flavor neophobia can be minimized in taste-aversion experiments by using weak taste solutions that elicit minimal neophobia (Smith, 1978). This has been the common practice. Probably more experiments have been performed with 0.1 and 0.15% saccharin than with any other solution (see Riley and Clarke, 1977, for a bibliography).

2 . Poison-Enhanced Neophobia Even more important than the role of neophobia in taste-aversion conditioning experiments is the possible contribution of poison-enhanced neophobia. That is, the aversion that subjects display after a taste-conditioning trial may not be due to the association of the taste with the toxicosis but may reflect a nonspecific increase in their aversion to novel tastes caused by the poisoning experience. Such an interpretation is not applicable to many taste-aversion experiments because of the reasons listed in Section II,A, 2. A detailed study of the circumstances that lead to poison-enhanced neophobia also makes this interpretation untenable for many experiments (see Domjan, 1977a, for a review). There is no doubt that animals poisoned after exposure to one novel taste subsequently avoid a variety of other novel flavors. This phenomenon has been well known to rodent control professionals for a long time and was one of the findings of early research on poison-avoidance learning (Richter, 1953; Rzoska, 1953).Recent research indicates that there are two mechanisms that contribute to this phenomenon. One of these does not involve an association between taste and poisoning (Domjan, 1977b) and the other mechanism requires the integrity of such associations (Best and Batson, 1977; Domjan, 1975). a. Nonassociative Mechanisms of Poison-EnhancedNeophobia. If subjects are tested before they have fully recovered from the effects of toxicosis, their flavor neophobia will be increased (Domjan, 1977b). In one of our experiments that illustrates this phenomenon, Sprague-Dawley rats were first adapted to a daily 23.5-hrwater deprivation schedule. Independent groups of subjects then received drinking tests with a 0.5% saccharin solution and water starting 30 min after the injection of 0-3.0 meqkg lithium chloride. The water and saccharin tests were conducted 6 days apart in a counterbalanced order.

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The amount of each solution subjects drank during the 60-min drinking tests is shown in Fig. 2. Generally, subjects consumed more water than saccharin, and increasing doses of lithium did not produce progressive decrements in water intake. However, a dose-related suppression in the intake of the saccharin solution occurred. We have found such a suppression in the intake of all novel solutions we tested (various concentrations of saccharin, 3% vinegar, and 5% casein hydrolyzate) whenever the drinking test was conducted shortly after the toxin injection. However, we did not find such a suppression of drinking with highly familiar solutions. Subjects reared with access to tap water, saccharin, or vinegar did not suppress their intake of these solutions in test sessions conducted shortly after the injection of less than 3.0 meq/kg lithium (Domjan, 3977b). It is quite likely that complete suppression of all ingestive behavior would occur with higher drug doses. The suppression of intake illustrated in Fig. 2 is not only specific to novelflavored solutions but is also limited to a relatively short period after drug treatment. In another of our experiments (Domjan, 1977b), independent groups of rats were given a 60-min drinking test with a novel 1 .O% solution of saccharin starting 10 to 120 min after the injection of 1.8 meq/kg lithium. The control group received injections of physiological saline. The amount of saccharin each group drank during these test sessions is displayed in Fig. 3. Progressively less suppression of drinking occurred with subjects whose drinking test was delayed longer after the drug injection. In fact, the intakes of subjects tested 90 and 120 min after drug treatment were not significantly less than the intakes of the control 2 5-

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FIG.2. Amount of water and 0.5% saccharin ingested during a 60-min test session started 30 min after the injection of various amounts of lithium chloride for independent groups of rats. From Domjan (1977b).

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group. Thus, the enhanced neophobia reaction was not an enduring response to the toxin drug treatment but dissipated quickly as the animals were allowed to recover from the toxicosis. Other investigators who used more severe deprivation schedules than what we typically employ observed enhanced neophobia reactions 24 and 48 hr after toxicosis treatment (Best and Batson, 1977; Carroll et al., 1975). However, even in these cases the enhanced neophobia response decayed if sufficient time passed to allow the baseline water intakes of the subjects to recover from the effects of the toxin. The transient nature of the enhanced neophobia effects that are observed as a direct result of toxicosis make it difficult to attribute enduring conditioned aversions to the same nonassociative mechanisms. Conditioned taste aversions are evident many days after the toxin administration. In one experiment, for example, conditioned aversions were observed in subjects tested 90 days after the taste-toxin pairing (Dragoin et af., 1973). b . Associative Mechanisms in Poison-Enhanced Neophobia. In certain circumstances, a poisoning experience can result in a lasting avoidance of novel flavored solutions that have not been paired with the toxicosis. In one of our experiments on this phenomenon, we found that animals that are first conditioned to avoid a weak saccharin solution subsequently also avoid a solution of casein hydrolyzate (Domjan, 1975). This is an example of enhanced neophobia because the generalized avoidance response occurs only if the casein solution is novel. However, the enhanced neophobia is not a direct effect of poisoning but is rather mediated by the aversion which subjects first learn to the saccharin solution. The casein aversion is evident only as long as subjects retain their conditioned aversion to saccharin. This important aspect of the phenomenon is illustrated in Fig. 4.

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All of the animals that provided data for Fig. 4 were first conditioned to avoid saccharin. However, before being tested for their intake of a novel casein solution, half of the subjects were given extensive access to saccharin in the absence of toxicosis. Figure 4 shows that this extinction procedure was effective in reducing the aversion that subjects had to the saccharin flavor. However, the extinction procedure for saccharin also substantially reduced the subjects' avoidance of the casein solution. Even though the extinction and control groups had the identical prior experience with toxicosis, only the control group evidenced enhanced neophobia for casein. This outcome, as well as the fact that an enhanced neophobia for casein is not observed if the prior toxicosis is not paired with exposure to saccharin, suggests that the enhanced neophobia effect is mediated by associative mechanisms. In our experiments on the associative poison-enhanced neophobia phenomenon, we did not find increased avoidance of all novel solutions following the pairing of a specific taste with toxicosis. For example, animals that had toxicosis paired with saccharin rarely if ever, showed increased avoidance of a novel vinegar solution. In a related series of experiments, Best and Batson (1977) found that animals that received access to a coffee solution paired with toxicosis subsequently showed enhanced neophobia to the taste of vinegar and the taste of casein. Based on these results, Best and Batson suggested that a conditioned aversion to one solution may generalize to other flavors along a dimension of novelty. However, their results are also an example of the associative poisonenhanced neophobia effect because the enhanced neophobia to vinegar and casein was not evident if the subjects' conditioned aversions to the coffee flavor were extinguished. The results of the experiments by Domjan (1975) and Best and Batson ( 1 977) are important because they indicate that associative mechanisms can be involved in enhanced neophobia effects. Therefore, one must not dismiss the possible SACCHARIN TEST

3

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FIG. 4. Saccharin and casein consumption of animals that initially had the taste of saccharin paired with lithium. Following the saccharin conditioning, the extinction group received extensive access to saccharin in the absence of toxicosis whereas the control group did not. From Domjan (1975).

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involvement of associative mechanisms merely because enhanced neophobia is observed after poisoning experiences. More sophisticated tests procedures are required before such a conclusion can be reached.

3 , Interruption of the Attenuation of Neophobia: A Nonassociative Explanation of the Delay Gradient in Taste-Aversion Learning Mitchell et al. (1977) recently suggested another nonassociative role of poisoning in taste-aversion experiments, the interruption of the attenuation of neophobia. The avoidance of novel flavored solutions is reduced as subjects have increasing exposure to the flavor (e.g., Domjan, 1976). However, the attenuation of flavor neophobia is also a function of the passage of time without aversive consequences following a taste exposure. Evidence of this is provided by experiments in which animals are exposed to a flavored solution on two occasions, with the interval between these two presentations systematically varied. Subjects drink more during the second exposure to the solution as a direct function of the interval between the two presentations (Nachman and Jones, 1974). This increased intake as a function of the passage of time is not attributable to increased thirst and is prominent only with novel-flavored solutions (Nachman and Jones, 1974). Therefore, the phenomenon appears to reflect the gradual loss of neophobia as a function of time after the first exposure to the taste solution. The attenuation of neophobia that occurs with the passage of time can be interrupted by the introduction of another novel taste (Green and Parker, 1975). Based on this observation, and related results from the study of other response systems, Mitchell et al. (1977) suggested that the administration of the toxin US in taste-aversion experiments may also interrupt the attenuation of neophobia that occurs after the taste presentation. In a delay of reinforcement experiment, this interruption would occur later in the process of the attenuation of neophobia for groups that receive longer delays between exposure to the taste and administration of the toxin. Mitchell et al. suggest that subjects that are conditioned with a long CS-US interval may drink more of the taste solution during later test sessions because the US was administered for them after they had already experienced a substantial loss of neophobia. Thus, this interruption by the US of the attenuation of neophobia which occurs with time predicts that a gradient of intake will be observed as a function of the CS-US interval during later tests with the flavor CS. The reinterpretation of the delay gradient offered by Mitchell et al. is rather interesting and creative. However, it would be difficult-perhaps impossible-to prove that an example of a flavor aversion was a result of the interruption by the US of the attenuation of neophobia. All of the results of such a mechanism could equally well be attributed to a weak association between the taste and the US. For example, the interruption hypothesis predicts a delay gradient as a function of the CS-US interval, which is exactly what is predicted by associative mechanisms.


29 1

The interruption mechanism also predicts that the aversion resulting from the interruption of neophobia loss will be specific to the flavor that was followed by the toxin US. An associative interpretation also makes this prediction. The interruption hypothesis predicts more of an aversion following a CS-US trial with stronger flavor CSs because such CSs elicit more neophobia. The same prediction is derived from associative accounts because stronger associations between CS and US are predicted with more intense CSs. The interruption hypothesis predicts stronger aversions with more intense USs because such USs can presumably better disrupt the attenuation of neophobia. Associative mechanisms can also explain this result because stronger associations occur with more intense uss. Although all of the predictions of the interruption hypothesis can also be explained by associative mechanisms, this does not mean that the two processes are indistinguishable. There are some predictions of associative mechanisms that cannot be explained by the interruption hypothesis. The most important and obvious of these is that the interruption hypothesis does not predict taste aversions that are stronger than the initial reaction of an animal to an edible substance. If the attenuation of neophobia is interrupted, then the subjects will respond to a flavored solution as they did on their first encounter. In contrast, the associative hypothesis predicts that as a result of the pairing of a flavor with a toxin it should be possible to produce stronger aversions than what are evident the first time an animal ingests the flavored solution. This is in fact the case in the preponderance of experiments on taste-aversion learning (e.g., Garcia et a l . , 1966) and is also observed in delay experiments in which the toxin US is administered 30 min or more after taste exposure (e.g., Garcia et nl., 1972; Nachman, 1970; Rozin, 1969; Wright et a l . , 1971). The interruption hypothesis also cannot explain cases in which subjects drink less of a flavored solution after the CS-US pairing than do animals that did not have previous exposure to the CS flavor (e.g., Carroll el al., 1975). 4 . Role of Nonassociative Mechaiiisms in Ingesrional Aversions: Overview

There is no doubt that omnivores suppress their intake of novel flavored substances and that this neophobia can be aggravated by poisoning experiences (Domjan, 1977a). However, these facts do not necessarily imply that ingestional aversions are governed by nonassociative mechanisms. The various arguments presented also do not prove that ingestional aversions are always the result of associations between novel flavors and toxicosis. Rather, ingestional aversions appear to be a joint function of both nonassociative and associative processes. In some situations one type of mechanism predominates, in other cases the other processes predominate, and in still other instances both types of mechanisms may contribute to the observed results. We now know enough about the mechanisms

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of neophobia and poison-enhanced neophobia to examine the circumstances in which a particular ingestional aversion is observed and make an educated judgment about the possible involvement of nonassociative processes. If a highly unfamiliar taste solution is used and the aversion is measured before the subjects have fully recovered from the toxicosis, then it is highly likely that the aversion will have a large nonassociative component. In contrast, if a low concentration palatable solution serves as the CS and subjects show a profound aversion long after they have recovered from toxicosis, it is unlikely that nonassociative processes will be involved. Obviously, appropriate control groups will also help in making these decisions.

III. POISON-AVOIDANCE LEARNING A N D THE COMPLEXITY OF THE INGESTIVE SEQUENCE Because animals that suffer some type of malaise after ingesting a novelflavored substance quickly learn a profound aversion specific to the flavor of what they ate, it is tempting to think about this phenomenon as involving only the taste stimulus and the aversive postingestional event. Such an analysis of the taste-aversion paradigm follows the model of Pavlovian conditioning and is analogous to the analysis of other simple conditioning situations such as Pavlovian salivary conditioning (Pavlov, 1927) and fear conditioning (Kamin, 1965). However, closer examination of the typical taste-aversion conditioning situation reveals that in addition to having toxicosis follow exposure to a taste, the subjects also approach and orient toward the source of the ingestible material, take the material in their mouths, manipulate it with the tongue, and swallow it. The tactile and orosensory stimulation involved in this consummatory sequence may also have an important role in ingestional-aversion learning. The ingestion also occurs in a specific location and in the presence of specific olfactory cues, and these stimuli may be likewise involved in the aversion that is learned. A. THEROLEOF INGESTION IN TASTE-AVERSION LEARNING In the typical taste-aversion conditioning procedure subjects receive exposure to the taste CS by ingesting a flavored solution or food. Investigation of the importance of ingestion in aversion conditioning requires exposing subjects to the flavor CS in ways that either do not require ingestive behaviors or that require modified modes of ingestion. We chose the first of these approaches and studied how rats learned aversions when they were exposed to the flavor CS during conditioning in a passive manner not involving ingestive behaviors. Learning under these circumstances was then compared to the aversion learning that results


293

from toxicosis following the ingestion of the flavored CS solution in the typical manner. In our first experiment (Domjan and Wilson, 1972a, Experiment 1) passive exposure to the flavor CS during conditioning was achieved by paralyzing the subjects with curare and rinsing the taste solution over the tongue before the injection of lithium chloride. The animals were then tested for their saccharin preference after complete recovery from both the paralysis and the lithium. We found that subjects conditioned under the influence of curare learned much weaker aversions to saccharin than animals that were allowed to drink the saccharin solution in the customary manner before toxicosis. Thus, the absence of ingestive behaviors during conditioning was accompanied by attenuation of taste-aversion learning. However, these results are somewhat difficult to interpret because curare paralysis is a multifaceted treatment. The results of our curare experiment were confirmed in a second study which involved less drastic procedures to achieve passive taste exposure than the curarization technique (Domjan and Wilson, 1972a, Experiment 2). In this experiment all of the subjects had a cheek cannula inserted which allowed infusion of the taste solution directly into the oral cavity. Instead of being paralyzed, the animals remained in the normal state and were held manually during the taste presentations. By varying the rate of infusion of the flavored solution and the state of thirst of the animals, we could manipulate the extent to which they swallowed the infused fluid. The taste presentation lasted for 2 min for all subjects. The amount animals swallowed, and the percentage of the 2-min taste presentation during which they were observed to make drinking jaw movements, are summarized in Fig. 5 for the various groups. The animals were first adapted to drinking their entire daily fluid requirements in a 25-min period of access to water each day. On the conditioning day, Group WF-Li was first allowed access to water for 25 min so that it would not be thirsty. To discourage Group WF-Li further from swallowing the saccharin solution during conditioning, the taste fluid was infused into the oral cavity at a very high rate (46m l h i n ) . Twenty-five minutes after the end of the taste presentation the subjects were injected with lithium. Figure 5 shows that the method of taste exposure for Group WF-Li was highly effective in minimizing ingestion of the saccharin CS. The subjects swallowed a negligible amount and were seldom observed making ingestive jaw movements. Group DF-Li received the same rapid oral infusion of saccharin during conditioning as Group WF-Li except that for these animals the saccharin exposure was conducted while they were water deprived. The higher level of thirst in this group resulted in their drinking considerably more of the saccharin solution than had Group WF-Li. Group DS-Li received a slow (3 ml/min) oral infusion of saccharin while water deprived, and Group FI was allowed to ingest the saccharin solution freely from a

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drinking tube for 2 min during the conditioning trial. These last two groups drank the greatest amount of the flavor CS. All of the water deprived groups (DF-Li, DS-Li, and n)were allowed to drink water for 25 min after the taste exposure so that their level of hydration would match that of Group WF-Li when the lithium was administered 25 min later. On the first and second days after the conditioning trial, each subject received a preference test in which the saccharin solution and tap water were simultaneously available for 30 min. The results of these test sessions are summarized in Fig. 6. All of the groups that had ingested considerable amounts of saccharin during the conditioning trial (Groups DF-Li, DS-Li, and Fl) subsequently showed strong aversions to the saccharin flavor. In contrast, subjects that had not swallowed the flavor CS during conditioning (Group WF-Li) had substantially higher preferences for the saccharin taste. In fact, the saccharin preferences of these subjects were very similar to the preferences of animals that had been conditioned while paralyzed with curare in the previous experiment. These results confirm that aversion learning is attenuated if subjects do not engage in the various mastication movements that are normally involved in ingestion.

FIG.5 . Amount of 0.2% saccharin ingested and percentage of time animals were observed drinking under various taste presentation procedures. Group WF-Li was not water deprived and received a fast oral infusion of saccharin. Groups DF-Li and DS-Li were water deprived and received a fast and a slow oral infusion of saccharin, respectively. Group FI was water deprived and was allowed to drink the saccharin from a drinking tube. From Domjan and Wilson (1972a).


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FIG. 6 . Saccharin preference of independent groups of rats injected with lithium chloride following the various taste presentation procedures depicted in Fig. 5. Group Na was not injected with the drug and indicates response to saccharin in the absence of aversion conditioning. From Domjan and Wilson (1972a).

The reduced taste aversion performance observed in animals that received passive exposure to the taste before toxicosis may reflect an attention decrement. Perhaps subjects that do not ingest a flavored solution pay less attention to its taste. The attenuated aversion performance can also be explained in terms of a stimulus generalization decrement from conditioning to testing. The test procedure for all subjects in the above experiments involved ingestion. Perhaps flavored solutions have different sensory properties when they are ingested as compared to when the solution is passed over the tongue in the absence of ingestive behaviors. Such a difference may have contributed to the weaker aversions of subjects that were conditioned in the absence of ingestion. This possibility could be evaluated by devising a test of taste-aversion learning which also does not involve having the subject drink the CS flavor. If stimulus generalization decrements occur between ingestion and no-ingestion situations, ingestionconditioned rats should evidence weaker aversions in tests that d o not involve eating and drinking than animals conditioned with passive taste exposure. Our subsequent experiments were motivated by these ideas. Although noningestion tests of flavor-aversion learning could be devised, our approach was to investigate these issues by conditioning aversions to olfactory stimuli with toxicosis. It seemed to us easier and more direct to devise odor-aversion test procedures that d o not involve ingestion.

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THEROLEOF INGESTION

IN

ODOR-AVERSION LEARNING

Animals that experience toxicosis after exposure to a novel odor can learn an aversion to the odor as a result (e.g., Garcia and Koelling, 1967; Lorden et al., 1970). We created an ingestion context for this odor-aversion learning by allowing animals to drink water in the presence of the CS odor (Domjan, 1973). However, we wanted to make sure that proximity to the drinking spout would not also bring the animals closer to the source of the odor. Therefore, odor exposure was accomplished during conditioning by placing the animals in plastic pails with tightly fitted lids, with the CS odor provided by spreading Mentholatum cream on the inside surface of the lids. The drinking spout was inserted about 5 cm above the floor of the pails when it was needed. The standard conditioning procedure involved placing the subjects in the odor-exposure chambers for 7 min, injecting them with lithium, and returning them to the home cage. This procedure resulted in the suppression of drinking in the presence of the CS odor during subsequent test sessions (Domjan, 1973). The drinking suppression was due to an association between the CS odor and the aversive effects of lithium because the aversion was not observed if subjects were tested in the absence of the odor or if they were injected with lithium in the absence of the odor and later tested with the odor present (Domjan, 1973). In some ways the effects of ingestion on odor-aversion learning (Domjan, 1973) were very similar to the effects of ingestion on taste-aversion learning described in the previous section. Animals that were allowed to drink water during the odor-conditioning trial evidenced much greater suppression of water intake during later test sessions in the presence of the CS odor than animals that were not given the opportunity to ingest anything during conditioning. Thus, ingestion facilitated odor-aversion learning, just as it facilitated taste-aversion learning in the earlier experiments. Because evidence of aversion learning was inferred from the suppression of water intake, one might be tempted to conclude that the enhanced aversions of animals that also drank water during conditioning reflected a learned aversion to water. However, there is no evidence for this possibility because animals that were allowed to drink water during odoraversion conditioning subsequently drank just as much water in the absence of the CS odor as subjects that received odor-aversion conditioning without ingestion (Domjan, 1973, Experiment 2). In an effort to specify better the test conditions in which the facilitative effects of ingestion on odor-aversion learning are evident, we constructed a special odor-testing chamber. A top view of this apparatus is provided in Fig. 7. Subjects were placed in area A and could explore compartments B and C when the guillotine doors D and E leading to these compartments were raised. Compartment B was odorized with Mentholatum. Using this test apparatus, we could assess the strength of an odor aversion in both ingestion and noningestion contexts. For ingestion tests, drinking spouts were inserted into compartments B and

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c=

A

I.

c!

FIG.7 . Top view of odor-choice test apparatus. Arrows indicate exhaust fans; see text for further details. From Domjan (1973). C at points F and G, and the response to the CS odor was inferred from how much animals drank from the fluid available in compartment B in comparison to the total fluid intake in both compartments. For noningestion tests, the two test compartments were both empty and the amount of time subjects spent exploring compartment B was measured as a percentage of the total time spent in exploration of both compartments. In one of our experiments using the special odor test apparatus, we compared the odor-aversion performance of three groups of subjects (Domjan, 1973, Experiment 4). During conditioning, Group Ingestion was allowed to drink water in the presence of the odor of Mentholatum before being injected with lithium chloride. Group No-Ingestion was exposed to the CS odor in the absence of fluids before the toxin injection, and subjects in Group Control received either ingestion or no-ingestion exposure to the CS odor followed by treatment with physiological saline. The aversion performance of these three groups was then assessed using three test procedures. In one of the tests, no fluids were available in the odor test apparatus, and the percentage of time subjects spent exploring the odorized compartment was measured. In another test session, a highly familiar 0.2% saccharin solution was available in both compartments of the test chamber and the percentage of intake in the odorized compartment was measured. In the third type of test session, access to tap water was made available in each test compartment.

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FIG. 8. Mean percentage preference for the conditioned stimulus odor for independent groups that during conditioning received exposure to the CS odor in the presence of access to tap water (ingestion) or without water (no-ingestion). Control subjects were not injected with lithium during conditioning. The animals were tested for their odor preference in the absence of edibles, and with access to saccharin (SACC) or water in the odor-choice apparatus. For the test without fluids, the numbers above the bars indicate mean total seconds spent exploring both test compartments. For the tests with saccharin and water, the numbers indicate mean total milliliters ingested in the test compartments. From Domjan (1973).

Preference for the Mentholaturn odor as measured by exploration, saccharin intake, and water intake is summarized in Fig. 8. During the exploration test without fluids, both the Ingestion and the No-Ingestion poisoned groups evidenced an aversion to the CS odor in comparison to the control subjects. However, the aversion performance in this test session was not facilitated by ingestion during conditioning. Similar results were obtained in the test session with saccharin available in the test compartments. Again both poisoned groups evidenced an aversion to the Mentholatum odor in comparison to controls, but there was no significant difference between the Ingestion and No-Ingestion groups. The facilitatory effect of ingestion during conditioningwas evident only when subjects


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were tested for their preference for drinking water in the presence of the CS odor. In this case Group Ingestion displayed significantly lower odor preferences than Group No-Ingestion. The results displayed in Fig. 8 confirm that ingestion during conditioning can facilitate odor aversion performance and help to specify the test conditions in which this effect is evident. The fact that enhanced aversions were not observed when subjects were tested for their preference to drink saccharin in the presence of the CS odor indicates that drinking measures of odor preference are not sufficient for observation of the phenomenon. Ingestion was necessary for the enhanced aversions to occur, since Groups Ingestion and No-Ingestion performed comparably in the exploration test. However, the nature of the ingested fluid was also important. More specifically, subjects had to be tested with the same drinking fluid that they drank during the conditioning exposure to the CS odor. As was noted above, the enhanced odor aversions of Group Ingestion could not be attributed to a learned aversion to the taste of water. Why is it, then, that the enhanced aversions were only evident in water-drinking measures of odor preference? An answer is suggested by analysis of the various stimuli that animals experienced when they drank water in the presence of the CS odor. The sensory experience of animals in Group Ingestion during conditioning can be conceptualized as consisting of three components: the CS odor, the taste of water, and a configural stimulus consisting of taste and odor. Our suggestion is that animals in Group Ingestion learned an aversion to both the odor component and the odor-taste configural stimulus (Domjan, 1973). Presumably the odortaste configuration becomes altered when subjects are tested with a taste that is different from what they experience during the conditioning trial. Therefore, the aversions manifest by Group Ingestion in the tests without fluids and with saccharin reflected only their conditioned aversions to the odor stimulus. In contrast, the aversions manifest in the water-drinking test also reflected a conditioned aversion to the odor-taste configural stimulus. This enhanced aversion was not evident with Group No-Ingestion because for these subjects the odor-water configuration had not been paired with poisoning during the conditioning trial. The present analysis of the effects of ingestion on odor-aversion learning in terms of the conditioning of configural stimuli that result from the ingestion context can be extended to the effects of ingestion on taste-aversion learning. Ingestion may also promote the perception of a configural stimulus in tasteaversion experiments. However, it is not entirely clear what the components of this configuration are. Nongustatory orosensory stimulation (the tactile sensations of the food in the mouth, for example) may constitute one of the components, and the taste of the ingested material may provide another component. Animals in the usual taste-aversion experiment may learn an aversion not only to the taste of what they ingest but also to the configuration created by taste and the

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orosensory stimulation involved in eating. Changing these orosensory stimuli would then result in weaker aversions. Such a mechanism could explain the attenuated aversions observed in animals tested for their preference for saccharin after they had passive exposure to this flavor paired with toxicosis (Domjan and Wilson, 1972a). C.

AVERSIONS TO NONGUSTATORY OROSENSORY LEARNED STIMULI

Experiments in which different methods of taste presentation are compared (e.g., Domjan and Wilson, 1972a) indicate that alteration of the orosensory stimuli normally involved in mastication and swallowing can modify tasteaversion performance. More direct evidence of the involvement of orosensory stimuli in ingestional aversion learning is provided by experiments in which different orosensory stimuli rather than different taste cues signal the presence or absenc.: of toxicosis. In one such experiment (Nachman, 1970), animals were adapted to drinking room temperature distilled water (27'C) for 10 min each day. During the conditioning trial, the distilled water was warmed to 43"C, and independent groups were injected with lithium chloride at various intervals after drinking the warm water. Subsequent drinking tests with the warm water indicated that the animals learned an aversion to this orosensory stimulus if the toxicosis was induced within 15 min after the first exposure to the warm water. Aversions have also been conditioned to the orosensory stimuli involved in drinking distilled water from a small-diameter drinking spout as compared to a large-diameter spout (Nachman et al., 1977). D.

INGESTION AS A SOURCE OF STIMULI THATMEDIATE CONDITIONED AVERSIONSTO NONGUSTATORY CUES

Animals typically experience a rich array of stimuli in the course of ingestion, including the taste, olfactory, and tactile properties of the edible, the orosensory stimuli involved in mastication and swallowing, and the visual, auditory, and spatial context in which the eating takes place. There is some evidence that in certain situations the taste stimuli encountered during ingestion may facilitate the association of nongustatory cues with toxicosis. In one of the first experiments of this type, Morrison and Collyer (1974) initially trained rats to press a response lever for water reward in a dark experimental chamber. On conditioning days the experimental chamber was illuminated by a 15-W light. One group of animals continued to receive water reward for pressing the lever, whereas for another group the reward was changed to a 0.1% saccharin solution. At the end of the 60-min bar-pressing session, each subject was injected with


30 1

lithium chloride. Three such conditioning sessions were conducted at 3-day intervals. Subjects were then tested for lever-pressing without either water or saccharin reward in the presence of the CS light and in darkness. Evidence of aversion learning to the illumination of the experimental chamber was provided by differential suppression of lever pressing during the extinction test. Subjects that received saccharin reward on conditioning days responded much less frequently during the extinction test than animals that had always been rewarded with water. Furthermore, the water-rewarded group did not appear to have learned an aversion to the light because its rate of responding was not different from that of a third group of subjects that had received the same procedures but had never been injected with lithium. Galef and Osborne (1978) recently also observed the conditioning of visual aversions mediated by taste using procedures that more closely approximate events outside the laboratory. They presented rats with gelatin capsules that were either 100% clear or 50% blue and 50% clear and were always filled with powdered laboratory chow. On the conditioning day, ingestion of the distinctive (50% blue) capsules was followed by treatment with lithium chloride. For some of the animals, the capsules were unflavored during conditioning, whereas for others the capsules were filled with powdered chow flavored with quinine or sucrose. All of the animals were then tested for their willingness to ingest the 50% blue capsules filled only with unadulterated chow. Subjects for which the distinctive capsules had been flavored with quinine or sucrose during conditioning subsequently evidenced stronger aversions to the 50% blue capsules than animals that had received unflavored capsules paired with lithium. Thus, the taste of quinine and sucrose facilitated the learning of an aversion to the visual features of the distinctive capsules. In related experiments with rats, Martin and Ellinwood (1974) found that access to 0.1% saccharin facilitates the conditioning of an aversion to the gray side of a black-gray shuttle box. More recently, Rusiniak et al. (1979) and Durlach and Rescorla (1980) observed that the presence of a distinctive taste facilitates the conditioning of an aversion to olfactory cues with lithium. Such potentiation effects have been also found in research with pigeons. Clarke et al. (1979) and Westbrook et al. (1980) reported that pigeons learn stronger aversions to visual aspects of a drinking solution if the drinking fluid also has a salient taste. The above examples of the facilitation of aversions to nongustatory cues by distinctive tastes are unexpected on the basis of research in other conditioning paradigms. Tastes are much more easily associated with toxicosis than are nongustatory cues (see Section IV). The presence of an easily conditioned stimulus usually reduces the association of other less salient stimuli with the US (Pavlov, 1927; Kamin, 1969). In fact, such overshadowing has also been observed with

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taste stimuli. Best er al. (1973) found weaker aversion conditioning of spatial cues with toxicosis when animals drank a novel-flavored solution in the distinctive environment. Similarly, Revusky and Parker (1976) found that animals form weaker aversions to a distinctive water cup if during conditioning they are allowed to drink a novel sucrose solution from the cup instead of familiar tap water. In a related experiment, Braveman (1975b) found that guinea pigs are less likely to learn an aversion to the color of their water if the water has an added novel flavor. It is not clear at the present time why in certain situations tastes facilitate the conditioning of aversions to nongustatory stimuli, whereas in other cases the opposite outcome is observed. The procedures involved in these widely disparate outcomes are very different and have yet to be analyzed. Whether one or the other effect is observed may depend on the relative rates of aversion conditioning of the taste and nongustatory stimuli and whether or not an association is established between the cues before each cue becomes associated with the toxicosis (cf. Durlach and Rescorla, 1980). OF SELECTIVE ASSOCIATIONS E. INGESTIONAS A DETERMINANT In the experiments described in Section I I I , D , tastes encountered during the course of ingestion facilitated aversion conditioning to nongustatory stimuli paired with toxicosis. In other situations, ingestion has been reported to facilitate aversion learning to nongustatory cues even in the absence of specific taste mediation (Shettleworth, 1972b). Furthermore, in these experiments the presence and absence of ingestion appeared to determine which of several stimuli were selected for association with the aversive US. These observations were made with baby chicks. The unconditioned stimulus was provided by shock to the feet or beak, and auditory and visual cues served as conditioned stimuli. In some cases the auditory and visual cues were encountered during the course of the ingestion of water. In other cases, the conditioning was carried out in the absence of ingestive responses. Whether or not ingestion was permitted in the situation turned out to be very important for the results observed. When water was available during conditioning and testing, the chicks evidenced stronger learned aversions to the visual cues than to the auditory stimuli. In contrast, when water was not available during conditioning and testing, the animals evidenced stronger aversions to the auditory cues paired with shock than to the visual stimuli. Thus, the presence or absence of ingestion determined which stimulus had predominant control over the aversion performance. This result probably reflected the conditioning of different associations in the ingestion and noingestion situations. However, it is also possible that the ingestion and noingestion tests were differentially sensitive to the conditioned aversiveness of the visual and auditory stimuli.


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F. INGESTION A N D POISON-AVOIDANCE LEARNING: OVERVIEW The ingestion of a novel food with toxic consequences is a very complex experience involving not only the taste of what is consumed but also its odor, its visual and tactile properties, and the orosensory stimuli involved in mastication and swallowing. The research reviewed above suggests that many aspects of this complex experience can be involved in the ingestional aversion that is learned. Animals may learn aversions not only to the taste of what they eat but also to the olfactory and visual features of the food, to the orosensory cues involved in the ingestion, and to the configuration of various combinations of these stimuli. In some situations the flavor of the ingested substance can also mediate the conditioning of aversions to nongustatory aspects of what is eaten, and in other cases the ingestive sequence can modulate which of the various stimuli in the situation will become associated with the aversive consequence. Thus, instances of ingestional aversion learning in laboratory and natural settings can reflect several associative components acting in concert to motivate the aversion performance. Rather than relying solely on the taste of edibles to guide their food selection, animals can make use of the full range of stimulation experienced during the course of eating.

Iv. A.

THESELECTIVITY OF ASSOCIATIONSIN INGESTIONAI, AVERSIONLEARNING

DEMONSTRATIONS OF SELECTIVE ASSOCIATIONS

The research reviewed in the previous section shows that many of the various stimuli that are encountered during the course of ingestion can become associated with toxic postingestional consequences. However, these findings should not be interpreted as indicating that animals can learn aversions equally well to all of the various stimuli that are paired with toxicosis. In fact, one of the most important aspects of ingestional aversion learning is that there is a selectivity in the associations. I . Dijfeerentiul Effectiveness of Various Coriditiorzed Stimuli

Early experiments on aversion conditioning with toxicosis, particularly toxicosis induced by radiation exposure, followed the Pavlovian tradition and attempted to demonstrate that all of the various stimuli animals can experience could be conditioned equally easily. In one of these experiments, for example, aversions to spatial cues were successfully conditioned with radiation exposure in rats (Garcia et n l . , 1957). However, it soon became evident in this line of research that the conditioning of aversions to spatial cues with radiation expo-

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sure requires more conditioning trials and higher radiation intensities than tasteaversion conditioning (Garcia et al., 1961). Consistent with this observation, Rozin (1969) found that the introduction of a 0.5-hrdelay between CS and US greatly interferes with the association of nongustatory cues with toxicosis but does not preclude taste aversion learning. In contrast to the successful demonstrations of spatial aversion learning motivated by toxicosis previously described, spatial aversions are typically not found in poison-avoidance learning experiments. Several investigators have found that while rats learn to avoid the taste of poisoned bait, they do not learn to avoid the location of the poisoned bait (Hargrave and Bolles, 1971; Rozin, 1967; Tevis, 1956). In these experiments it may be that the taste of the poisoned bait overshadowed (Kamin, 1969) the cues provided by location. However, attempts to condition aversions to auditory, spatial, and visual cues in the absence of concurrently available distinctive gustatory stimuli using toxicosis have also provided negative results (Domjan and Wilson, 1972b; Garcia and Koelling, 1967; Garcia er al., 1968). The fact that nongustatory cues are not as easily associated with toxicosis as novel taste stimuli is not necessarily inconsistent with traditional concepts of Pavlovian conditioning. Differences in the ease of conditioning of various potential CSs is expected if these stimuli differ in intensity, salience, or novelty. Furthermore, the fact that some stimuli are not as easily conditioned as another class of cues is not sufficient evidence for the existence of selective associations. Categories of stimuli that are not optimal in aversion conditioning with toxicosis may be equally ineffective in conditioning with other types of unconditioned stimuli. 2 . Cue-Consequence Specificity

Evidence for the selectivity of association in aversion conditioning is provided by experiments in which the conditionability of different categories of stimuli is found to depend on the type of unconditioned stimulus used (Schwartz, 1974; LoLordo, 1979). The first experiment of this type was the classic study reported by Garcia and Koelling (1966). Rats in this experiment were allowed to drink from a specially outfitted drinking tube that provided a flavored solution (sweet or salty) and an audiovisual stimulus (light from a 5-W bulb and sound from a clicking relay) each time the animal licked. Ingestion in this situation was paired with exposure to radiation, lithium toxicosis, or shock to the feet. Several conditioning trials were conducted, and the animals’ rates of drinking were then observed when licks produced either the taste stimulus alone or the audiovisual cue alone. Following conditioning with radiation exposure and lithium toxicosis, the rats were slower to lick in tests with the taste cue than in tests with the audiovisual stimulus, In contrast, following pairing of the audiovisual stimulus


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with footshock, the animals were slower to drink in tests with the audiovisual cue than in tests with the taste stimulus. Thus, the relative aversion subjects evidenced to the gustatory and audiovisual stimuli depended on the type of unconditioned stimulus they had been exposed to during the training trials. In the Garcia-Koelling experiment the distinctive taste and audiovisual stimuli were both present during the conditioning trials. Therefore, it is possible that the two types of conditioned stimuli did not become conditioned equally with each unconditioned stimulus because the presence of one of the CSs somehow interfered with strong conditioning of the other. Thus, the selective association effect observed by Garcia and Koelling may have been mediated by a stimulus competition process. The possibility of competition between CSs was ruled out by procedures used in a subsequent study (Garcia er nf., 1968). In this experiment taste and nongustatory conditioned stimuli were paired with radiation illness and footshock in independent groups so that none of the subjects experienced both types of conditioned stimuli at the same time. The gustatory stimulus was provided by coating food pellets with either powdered sugar or flour, and the nongustatory stimulus was provided by the size of the pellets. Subjects for which the unconditioned stimulus was paired with a distinctive flavor always received food pellets of the same size, and subjects for which the US was paired with a distinctive size (large or small) always received pellets of the same flavor. Tests conducted after the five conditioning trials revealed that stronger aversions were conditioned to size than to taste when the unconditioned stimulus was footshock. In contrast, stronger aversions were conditioned to the taste than to the size of the food pellets when the unconditioned stimulus was radiation exposure. Thus, this experiment yielded the same type of selectivity in aversion performance as a function of the unconditioned stimulus as had been observed by Garcia and Koelling (1966). These results show that subjects do not have to have both taste and nongustatory stimuli present on conditioning trials to show selectivity in aversion performance. The experiment by Garcia et al. (1968) ruled out the possibility of explaining the selectivity in aversion performance in terms of stimulus competition mechanisms. However, it introduced another problem in the comparison of the associability of taste and nongustatory cues. Taste stimuli were presented by allowing the animals to ingest food pellets. Thus, the subjects did not receive exposure to the flavor until they approached a food pellet, picked it up, and inserted it into the mouth. In contrast, the size conditioned stimulus did not require the same sequence of events. The subjects may have been able to either see or feel with their whiskers the size of the food pellets before they picked them up. Therefore, ingestion was not necessary in order for the rats to come in contact with this CS. This difference in the way in which the subjects experienced the

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taste and nongustatory stimuli may have introduced differences in the temporal relationship of each CS to the unconditioned stimuli used. Garcia and his colleagues were not unmindful of the confounding that is introduced by presenting taste and nongustatory conditioned stimuli to animals in different ways. That is why in their first experiment (Garcia and Koelling, 1966) both the taste and audiovisual CSs were presented contingent on licking a drinking tube. Differences in the method of CS presentation can also be minimized by presenting both taste and nongustatory cues without requiring licking or ingestive responses, the way that audiovisual stimuli are usually received. The presentation of audiovisual stimuli without requiring ingestion does not involve special problems. Taste stimuli can be presented without approach and drinking responses by infusing the fluid directly into the oral cavity of nondeprived rats through a fistula (Domjan and Wilson, 1972a). We used such an approach in two replications of the selective association design (Domjan and Wilson, 1972b). One of our experiments (Domjan and Wilson, 1972b, Experiment 2) was modeled after the study by Garcia et al. (1968) and investigated the selectivity of associations with taste and nongustatory CSs presented individually during conditioning. The rats first had an oral fistula implanted with one end secured to the inside surface of the cheek and the other end exiting at the back of the neck. The fistula permitted the presentation of taste solutions while the animals moved about freely. After recovery from the operation, access to water was restricted to 35 min each day. Once the animals were adapted to the deprivation schedule, three conditioning trials were conducted on successive days, each scheduled after the daily 35-min access to water. For three groups of subjects, the oral infusion of a 0.2% saccharin solution at 1 ml/sec served as the conditioned stimulus, and for the other three groups the CS was an irregularly pulsed buzzer which added 20 dB to the 50-dB (SPD) background noise. Each CS was presented for 35 sec. Immediately after the saccharin infusion, the subjects received a 10-ml oral infusion of tap water to help terminate the saccharin flavor. One taste CS group was then injected with lithium chloride, another received exposure to electric shock, and the third group served as a control and received only an injection of physiological saline. The buzzer CS groups were similarly conditioned with lithium, shock, or saline injection after the buzzer presentations. In addition to receiving one of the conditioned stimuli immediately before the unconditioned stimuli during the training trials, each subject was also exposed to the alternative conditioned stimulus (buzzer for the saccharin-conditioned rats and saccharin for the buzzer-conditioned rats) 1.5-2.5 hr after each conditioning trial. This aspect of the procedure allowed us to evaluate the nonassociative effects of the unconditioned stimuli used. After the conditioning trials, each subject was tested for its preference for the saccharin and buzzer stimuli. During the saccharin preference test, the animals had simultaneous access to two drinking tubes, one filled with saccharin and the other filled with tap water. During the


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FIG. 9. (A) Saccharin preference of rats exposed to saccharin in Conditioning with lithium, shock, or saline. (B) Buzzer-water preference of rats exposed to the buzzer in conditioning with lithium, shock, or saline. From Domjan and Wilson (3972b).

buzzer preference test, both drinking tubes were filled with tap water. However, drinking from one of the tubes always produced the sound of the buzzer. Preference for the stimulus (saccharin or buzzer) that served as the CS in conditioning with lithium treatment, shock, and saline injection is summarized in Fig. 9 for the six groups of animals. The results were very similar to what Garcia and his colleagues found. Lithium-conditioned subjects acquired significant aversions to the taste of saccharin whereas shock-conditioned animals did not show such aversions. In contrast, shock-conditioned animals learned strong aversions to the buzzer CS whereas lithium-injected rats did not. Preference for the stimulus (saccharin or buzzer) that did not serve as the CS for a particular subject but was presented after each conditioning trial is not shown in the figure. However, the three groups conditioned with the buzzer as the CS did not differ in their preference for saccharin, and the three groups conditioned with saccharin as the CS did not differ in their preference for the buzzer. This aspect of the findings, overlooked by some readers (e.g., Bitterman, 1976), shows that the aversions observed resulted from associative processes. If lithium had produced an aversion to saccharin in the absence of an association between these events, then animals that had the buzzer CS paired with lithium should have also shown an aversion to saccharin. Similarly, if shock had produced an aversion to the buzzer without an association, then animals that had the saccharin CS paired with shock should have also shown an aversion to the buzzer.

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MICHAEL DOMJAN

INTERPRETATIONS OF THE SELECTIVE ASSOC~ATION EFFECT

I . Anatomical Convergence of Sensory Pathways Garcia and his associates (Garcia and Ervin, 1968; Garcia et al., 1974) have suggested that the cue-consequence specificity observed in aversion learning reflects the anatomical organization of the sensory pathways conveying information about the conditioned and unconditioned stimuli. The clearest evidence cited in support of this hypothesis is provided by the organization of the somatic and visceral neuropils in the medulla oblongata of the tiger salamander (Herrick, 1948). The somatic neuropil receives input from both the auditory system and from the cutaneous receptors, and the visceral neuropil receives fibers from the gustatory system and visceral receptors. Such separation of the exteroceptive and interoceptive sensory systems is assumed to be the basis for selective associations involving stimuli in these systems. Unfortunately, selective associations have not been investigated in the tiger salamander. Furthermore, as others have pointed out (Nachman et al., 1977), it is not known how anatomical convergence leads to facilitation of' conditioning. Behavioral evidence for selective associations has been provided by experiments with mammals. In these species the neural projections of sensory systems which provide exteroceptive information are not as limited as in the salamander. However, both gustatory and visceral receptors in mammals send fibers to the nucleus of the fasciculus solitarius (e.g., Morest, 1967), and this convergence may be the basis for the selectivity of taste-toxicosis associations. If selective associationsresult from the convergence of sensory pathways relaying information about the conditioned and unconditioned stimuli, then certain lesions should selectively disrupt the learning of taste-toxicosis associations and other lesions should selectively disrupt the learning of audiovisual-shock association. This prediction has been only partially confirmed. Some lesions, such as in the lateral septum and the ventral hippocampus, have been found to disrupt the learning of noise-shock associations without disrupting taste-aversion learning. However, lesions have not been reported which interfere with taste-aversion learning but do not disrupt noise-shock association (Gaston, 1979; McGowan et al., 1972). 2 . Adaptive Specializations of Learning

Another interpretation of the selective association effect in aversion learning states that the mechanisms controlling the learning of taste-toxicosis and audiovisual-shock associations are the product of an evolutionary selection process which has made these two types of learning ideally suited to protect the animal from such challenges to survival as food poisoning and external sources of injury (Rozin and Kalat, 1971; Seligman, 1970; Seligman and Hager, 1972). This interpretation is rather unspecific because it does not detail what aspect of


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the conditioning process is altered by evolution to facilitate certain associations and hinder other types of learning. The selection process may act on attentional mechanisms, memory mechanisms, or various aspects of the association process to promote selective associations. In any event, one possible outcome of evolution is that selective associations reflect the operation of unique learning processes in the association of different classes of conditioned and unconditioned stimuli (Rozin and Kalat, 1971). Although this is a possibility, such a conclusion is not required by what we know about selective associations so far. Selective associations may result from mechanisms, described below, that are applicable to a variety of conditioning situations. 3 . The Development of Learning Sets

One approach to explaining instances of selective associations in terms of general principles of learning has stressed the possible involvement of learning sets (e.g., Testa and Ternes, 1977). During the lifetime of the organism, stimuli arising from ingestion are followed by postingestional consequences every time the animal eats. The postingestional events usually involve various digestive processes and thirst and hunger reduction rather than toxicosis. Nevertheless, this repeated pairing of orosensory stimulation with visceral events may lead to the development of a learning set which then facilitates the learning of associations between novel tastes and toxicosis. A comparable argument is made to explain the rapid learning of associations between exteroceptive (e.g., audiovisual) stimuli and cutaneous pain. Because exteroceptive stimuli are often followed by other exteroceptive cues in the normal life of the animal, a learning set is assumed to develop which facilitates the learning of an association between a novel exteroceptive stimulus and cutaneous pain. The learning set interpretation of selective association can be investigated by modifying the normal feeding history of the animal and seeing if this changes the selective association effect. In an application of this strategy, Lucy Sullivan (cited in Testa and Ternes, 1977) raised rats in an environment in which visual cues were made predictive of ingestive consequences and taste stimuli were irrelevant. This training facilitated the conditioning of aversions to visual cues with toxicosis. However, the animals were equally able to form associations between taste cues and toxicosis. Attempts such as that of Lucy Sullivan to establish an artificial learning set demonstrate that learning sets can be involved in selective associations. However, such demonstrations do not prove that learning sets contribute to the phenomenon under normal rearing conditions. Another approach to investigating the learning set interpretation involves exploration of the selective association effect in very young animals that have had limited feeding experiences. Using this approach, Gemberling et al. (1980) recently found what may be a selective association effect in 5-day-old rats. Six groups of pups were used. For three of

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the groups, the conditioned stimulus was provided by the infusion of a 0.5% solution of sodium saccharin through an oral fistula. For the remaining three groups a tactile conditioned stimulus was presented by placing the animals in a small enclosure lined with either terrycloth or smooth cardboard. Animals in each CS condition received one of three possible unconditioned stimuli: a 1% body weight injection of 0.30 M lithium chloride, a 1% body weight injection of 0.15 M sodium chloride, or cutaneous shock. The shock US consisted of a series of five shocks (1-sec, 1-mA, constant current) administered at 1-min intervals during the 5-min CS through two metal electrodes placed on either side of the body near the hind legs of the animals. Twelve hours after conditioning, the pups were tested for their aversion to their respective conditioned stimuli. For the animals that had saccharin infusion as the conditioned stimulus, the aversion test involved a 5-min oral infusion of the saccharin solution, and the amount ingested was calculated from the weightgain the animals showed following the infusion. For animals that had the tactile conditioned stimuli, the aversion test was conducted in a chamber identical to that used in conditioning except that half of the chamber was fully lined with terrycloth and the other half was lined with smooth cardboard. (For half of these animals, terrycloth served as the CS and for the remaining animals the cardboard served as the CS.)At the beginning of each preference test, the pup was placed so that the midline of its body coincided with the junction of the two textures at the center of the chamber. The amount of time spent on each texture during the 5-min test was measured for each animal. The results of the aversion tests are displayed in Fig. 10. The lithiumconditioned pups drank significantly less saccharin during the test session than the saline-injected controls. However, such an aversion was not observed for the shock-conditioned animals. In contrast, the shocked pups showed a significant aversion to the texture-conditioned stimulus in comparison to the saline-injected controls, but no such aversion was evident among the lithium-conditioned rats. This pattern of results is identical to what is observed with adult animals in experiments employing audiovisual instead of tactile stimuli as the exteroceptive conditioned stimulus. The fact that the same kinds of selective aversions observed in adults are evident as early as 5 days of age suggests that an extensive history of ingestion and experiences with exteroceptive cues is not necessary for the phenomenon. Thus, these results are contrary to the learning set interpretation of selective associations. In a subsequent experiment, Gail Gemberling investigated selective associations in 1-day-old rats in an effort to further reduce the possible contribution of a history of ingestive and exteroceptive experiences. The conditioning procedure was the same as what we had used with the 5-day-old rats except that the conditioned stimuli (0.5% saccharin for some rats and terrycloth or smooth cardboard for the remaining subjects) were presented for 10 min, and the shock


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FIG. 10. Saccharin intakes (corrected for body weight) of 5-day-old rats exposed to saccharin in conditioning with lithium (Li), shock, or saline (Na), and preference for the CS texture (cardboard for some and tenycloth for others) in 5-day-old rats exposed to this texture i n conditioning with lithium, shock, or saline. From Gemberling ri al. (1980).

unconditioned stimulus consisted of 10 1-sec shocks delivered at 1-min intervals during the 10-min CS. Following conditioning with lithium, control injection of physiological saline, or shock, the pups were returned to their mothers until they were 5 days old. Tests for aversion to the saccharin and tactile conditioned stimuli were conducted at 5 days of age in the same manner as in the previous experiment except that the test sessions lasted 10 instead of 5 min. Results of the postconditioning test sessions are presented in Fig. 1 1 . The lithium-conditioned pups drank significantly less saccharin than both the salineinjected controls and the shock-conditioned animals, which did not differ from one another. In contrast to the pups conditioned at 5 days of age in the preceding experiment, the rats conditioned at 1 day of age and tested at 5 days of age responded differently to the two textures (terrycloth and cardboard) used as the exteroceptive conditioned stimuli. Therefore, the data are presented separately for these textures. There were no significant differences among the three groups of pups that had been conditioned with terrycloth as the CS. In contrast, significant group differences were apparent among the groups for which the smooth cardboard served as the conditioned stimulus. Shock-conditioned animals showed a significantly lower preference for the cardboard CS than the salineinjected controls or the lithium-conditioned rats. Furthermore, these latter two groups did not differ from one another. The findings with saccharin and cardboard as conditioned stimuli in aversion learning in the 1-day-old rats are similar to what was observed with the 5-day-old animals and are similar to selective association effects observed in adult rats. It is

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FIG.11. Saccharin intakes (corrected for body weight) of rats exposed to saccharin in conditioning with lithium (Li), shock (Sh), or saline (Na), and preference for the CS texture (cardboard for some and terrycloth for others) in rats exposed to this texture in conditioning with lithium, shock, or saline. The animals received one conditioning trial when they were 1 day old and were tested when they reached 5 days of age. From Gemberling (unpublished). not clear at the present time why terrycloth was not an effective conditioned stimulus for the 1-day-olds. Perhaps terrycloth is not sufficiently different from the tactile sensations of the nest to allow 1-day-old rats to differentiate it from the nest cues. Alternatively, returning the pups to the nest for 4 days between conditioning and testing may have resuIted in extinction of the conditioned aversions to the terrycloth stimulus. In any event, given the young age of the animals at conditioning, it is very unlikely that the results observed were due to the development of learning sets based on extensive ingestive and other experiences. The experiments with 5- and 1-day-old rats are exciting because they minimize the contribution of extensive life experiences to the behavioral effects observed. However, it is important to point out that these investigations are only preliminary. We have performed experiments that show that the aversions in rats con-


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ditioned at 1 day of age i n fact reflect associative processes. However, we have yet to determine the contribution of other variables, discussed below, to the selective associations learned shortly after birth. 4.

Event Covariation

One of the most interesting beliavioral interpretations of selective associations is based on the suggestion that the rate of conditioning is directly related to how similar the conditioned and unconditioned stimuli are in terms of their spatial location and temporal-intensity characteristics (Testa, 1974). According to this hypothesis, tastes are easily associated with toxicosis because both tastes and malaise tend to be prolonged and are slow to begin and end. Correspondingly, brief audiovisual cues are presumably easily associated with discrete footshock because of the similarity of the durations and onset and termination characteristics of these stimuli. In contrast, tastes and footshock and audiovisual cues and toxicosis are not readily associated because these pairs of stimuli have very different intensity and time course characteristics. The selectivity of associations observed in aversion learning is compatible with the event covariation hypothesis but was not predicted by this idea. However, the hypothesis has been the impetus for several other findings. One of these involved a comparison of the effectiveness of various combinations of visual conditioned stimuli in association with different types of air blast as unconditioned stimuli in rats (Testa, 1975). The visual conditioned stimulus was either pulsed and emanated from the ceiling or was presented in a wave form emanating from the floor. The air blast unconditioned stimulus was also either pulsed and originated from the ceiling or was presented in a wave form and originated from the floor. Various groups received different combinations of these stimuli in conditioning. Stronger aversions to the visual CS resulted in cases in which the conditioned and unconditioned stimuli had a similar temporal distribution and originated from the same location as compared to cases in which the temporal distribution and location of the CS and US were different. These results are exactly as predicted by the event covariation hypothesis. However, as the author noted, it is unclear whether the results reflected associative changes or sensitization effects because the appropriate control groups were not included in the experiment. More convincing evidence for the event covariation hypothesis was provided by a series of second-order conditioning experiments by Rescorla and Furrow (1 977). Two of these experiments investigated the development of second-order associations between different combinations of visual and auditory stimuli in rats. These studies showed that an association develops more rapidly between stimuli of the same modality (both auditory or both visual stimuli) than it does between stimuli of different modalities (auditory-visual associations or visualauditory associations). The third experiment provided similar evidence of selec-

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tivity in the development of second-order associations in pigeons. All of the stimuli in this last experiment were visual. Two of them were color stimuli (blue and green), whereas the other two were orientation cues (horizontal and vertical lines). Associations developed more rapidly if both of the stimuli were of the same type (color or orientation) as compared to cases in which one of the stimuli was color and the other was orientation. Similar results were recently reported with the association of stimuli presented in the same or different locations (Rescoda and Cunningham, 1979). 5 . Differential Time Course of CS Traces

This explanation (Krane and Wagner, 1975) is similar to the event covariation hypothesis in that it emphasizes the importance of the temporal characteristics of the stimuli involved in selective association experiments. Another important factor in this explanation is the delay between exposure to the conditioned stimulus and the onset of unconditioned stimulus effects. It is assumed that the trace of taste stimuli is considerably longer than the trace of audiovisual cues. Therefore, when a taste is paired with an immediate brief electric shock, it is quite likely that the trace of the flavor persists after the unconditioned stimulus. This reduces the extent to which the taste serves as a signal for shock and therefore little conditioning occurs. Audiovisual-shock conditioning, in contrast, is robust because in this case the trace of the CS does not linger beyond the unconditioned stimulus to reduce the signaling relationship between CS and US. The poor associability of audiovisual cues with toxicosis is explained by the fact that toxicosis is usually delayed in its onset and therefore may not occur while the trace of the audiovisual CS still exists. The delayed onset of toxicosis does not similarly interfere with conditioning of taste stimuli because the trace of taste cues presumably persists long enough to overlap with the toxicosis. Evidence consistent with the differential CS trace hypothesis was provided by Krane and Wagner (1975) in an experiment that compared the effectiveness of brief footshock in conditioning aversions to an audiovisual stimulus and the taste of 0.7% saccharin. Independent groups were shocked 5 , 30, and 210 sec after exposure to these conditioned stimuli. Subsequent test sessions revealed that aversion learning to the audiovisual stimulus was best at the 5-sec CS-US delay, and learning progressively decreased with longer delay intervals. In contrast, the strongest saccharin aversion learning occurred when the shock US was delayed 210 sec, and no conditioning was evident with the 5-sec delay interval. The inverse relationship observed between conditioning of the audiovisual CS and the CS-US interval presumably occurred because with longer CS-US intervals the trace of the CS did not persist to coincide with the unconditioned stimulus. The direct relationship between conditioning of the taste CS and the CS-US interval presumably reflected the long trace of the flavor CS, which persisted beyond


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the US in groups conditioned with a short CS-US interval and lasted long enough to overlap with the US in groups conditioned with a long CS-US interval. Although the results presented by Krane and Wagner (1975) are good evidence for the differential time course of the trace of audiovisual and flavor conditioned stimuli, others (e.g., Hankins et al., 1976) have pointed out that these results may have limited applicability to the selective association effects reported with toxicosis and shock (e.g., Domjan and Wilson, 1972b; Garcia and Koelling, 1966). Krane and Wagner used a much more concentrated saccharin solution than had been used in the earlier selective association experiments, and therefore the aversions observed may have been in part controlled by the odor of the saccharin. It is also not clear to what extent the shock-conditioned aversions to saccharin were similar to saccharin aversions conditioned by toxicosis. The shock-conditioned aversions may have been weaker than typical toxicosisinduced aversions and may have been much more limited to the conditioning situation. Thus, it remains to be seen whether or not the original selective association effect observed in conditioning with shock and toxicosis can be eliminated by sufficiently delaying the shock unconditioned stimulus for the taste-conditioned groups. 6. Differeniiul Orientdon Produced by Unconditioned Stimuli

Another interesting behavioral interpretation of the selective association effect attributes the phenomenon to differential orientations caused by the different unconditioned stimuli (Rescorla and Holland, 1976). This interpretation assumes that footshock causes animals to attend especially to audiovisual stimuli, and toxicosis causes animals to attend especially to taste stimuli. This differential attention to one or the other type of conditioned stimulus is then assumed to be responsible for the rapid association of these stimuli. Differential orientations evoked by the unconditioned stimuli are most likely to determine which CS becomes conditioned on the next trial. Therefore, such a mechanism would appear to be of limited applicability to situations in which selective associations are observed following a single conditioning trial. Although the classic demonstrations of the selective association effect involved multiple trials (Domjan and Wilson, 1972b; Garcia and Koelling, 1966; Garcia et a / . , 1968), recent experiments on selective associations in infant rats were performed with a single conditioning trial (see Section IV,B,3). The differential orientations evoked by the unconditioned stimuli would also have to be long lasting to account for selective associations because such effects are usually demonstrated with intertrial intervals of 24 hr or more (Domjan and Wilson, 1972b; Garcia and Koelling, 1966; Garcia et a / . , 1968). Rescorla and Holland (1976) suggested an experimental design for precluding the operation of differential orientation mechanisms in selective association

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experiments. Basically, the strategy involves exposing subjects to both of the unconditioned stimuli. One unconditioned stimulus is to be paired with the conditioned stimuli, and the other unconditioned stimulus is to be presented during the intertrial interval. For example, one group of subjects might receive an auditory-taste compound CS paired with toxicosis and have the footshock unconditioned stimulus presented during the intertrial intervals. Another group might receive the auditory-taste CS paired with footshock and have toxicosis administered at some other time. Presumably because both of the unconditioned stimuli are presented to both groups, any differences in aversion performance between them could not be attributed to nonassociative orientation effects of the unconditioned stimuli. This experimental design has been used with success in demonstrationsof selective association effects in second-orderconditioning (Rescorla and Furrow, 1977; Rescorla and Cunningham, 1979). However, the experimental design remains to be tested in connection with the taste-toxicosis audiovisual-shock selective association effect.

7. Differential Sensitivity of Response Measures Another possibility that must be considered is that the differential aversions evident in conditioning with toxicosis and footshock reflect differential sensitivity of the response measures employed (e.g., LoLordo, 1979; Rescorla and Holland, 1976; Testa and Ternes, 1977). The tests used to measure taste-shock and audiovisual-toxicosis associations may not be as sensitive as the tests used to measure taste-toxicosis and audiovisual-shock associations. It is always possible that a particular failure to observe learning reflects insensitivity of the test procedure used rather than the absence of learning. The discovery of test procedures that show strong evidence of taste-shock and audiovisual-toxicosis learning would indicate that a selective association effect does not exist with these CSs and USs. However, such evidence would not completely dispose of the phenomenon originally identified by Garcia and Koelling. Garcia and Koelling (1966), Garcia et al. (1968), and Domjan and Wilson (1972b) all used the same response measures in assessing the conditioning of various CSs with footshock and toxicosis. In most cases this involved the suppression of ingestion. Even if the results obtained did not reflect selective association effects, it remains to be explained why the same response measure was more sensitive to taste-toxicosis and audiovisual-shock associations than it was to taste-shock and audiovisual-toxicosis associations. For a complete theory of behavior, it is just as important to explain such selective performance effects as it is to explain selective association effects.

8. Dixerential Innate Reactions to the Conditioned Stimuli Selective association effects are commonly interpreted as reflecting different rates of acquisition of different associations. However, the initial strength of the


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different indicant responses may not be equivalent. For example, it may be that the innate reaction to taste stimuli involves some of the same responses that are conditioned by toxicosis, and the innate response to audiovisual cues involves some of the same responses that are conditioned by footshock. Evidence of taste-toxicosis and audiovisual-shock associations may appear quickly because in these cases less learning is required to bring the conditioned response above threshold. This kind of reasoning, originally contemplated by Konorski (1948, 1967), was recently discussed in detail by LoLordo (1979). There is no evidence in toxicosis and shock conditioning to preclude such an interpretation.

c.

THEUNIQUENESS OF SELECTIVE ASSOCIATIONSIN THE FEEDING SYSTEM

The observation that ingestion-related stimuli are favored in associations with toxicosis and that audiovisual cues are favored in associations with peripheral pain is one of the important facts that have been used to argue that learning in the feeding system has certain unique properties. The experiment by Garcia and Koelling ( 1966) was the first striking demonstration of selective associations. Because much of the work of Garcia and his colleagues involved the feeding systems, it was tempting to conclude that the results represented special properties of conditioning in this system. This conclusion, however, was probably premature. First, the cue-consequence relationship Garcia and Koelling ( 1966) discovered involved both toxicosis conditioning and conditioning with shock, and the selective association effect was as true of fear conditioning with shock as it was of taste-aversion conditioning with toxicosis. That is, tastes were found to be much less effective in conditioning with footshock than were audiovisual cues. Thus, if the selective associations found with toxicosis are used to argue for the uniqueness of conditioning with toxicosis, a similar argument should be made for the uniqueness of fear conditioning with footshock. The cue-consequence specificity Garcia and Koelling (1966) first identified also cannot be used to argue for the uniqueness of learning in the feeding system because similar selective association effects have been observed since then in other situations. For example, Testa (1975) observed that if the unconditioned stimulus was an air blast from the ceiling, a visual stimulus from the ceiling became better conditioned than a visual stimulus from the floor. In contrast, if the unconditioned stimulus was an air blast from the floor, the visual stimulus from the floor became conditioned more readily. In other examples of selective association effects, Rescorla and Furrow (1977) observed that stimuli that were similar in modality or visual characteristics became more readily associated with one another in a variety of second-order conditioning procedures than stimuli that were less similar, and Rescorla and Cunningham (1979) found that stimuli presented in the same location became more readily associated than stimuli pre-

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sented in different locations. Finally, LoLordo and his associates (reviewed in LoLordo, 1979) have found that in pigeons auditory stimuli become more readily conditioned in shock-avoidance experiments than visual cues and visual stimuli are favored over auditory cues in conditioning with food reward. The various examples of cue-consequencerelationships that have been discovered since the original work of Garcia and Koelling (1966) suggest that the selective association effects observed in conditioning with toxicosis are not unique. Rather, it appears that selective associations and cue-consequence relationships are but another common characteristic of associative learning. As the mechanisms that contribute to such effects become better understood, other examples of selective associations will no doubt be discovered.

ON INGESTIONAL AVERSION LEARNING V. LIMITATIONS

Although the mechanisms of selective associations in aversion learning have not been fully characterized yet, there is no dispute that taste stimuli are favored in conditioning with toxicosis in omnivores such as the rat. There is also no dispute that taste aversions can be learned in one trial even if there is a long delay (more than an hour) between the taste exposure and the subsequent toxicosis. These characteristics of the phenomenon have encouraged the view that ingestional aversion learning is a primitive type of conditioning which occurs automatically when taste exposure is paired with postingestional malaise. The implication is that animals will learn aversions to tastes paired with toxicosis even if a causal inference between ingestion and toxicosis cannot be easily drawn. This view is perhaps best exemplified by the title of an article by Kalat and Rozin (1972), “You can lead a rat to poison but you can’t make him think.” Recent research suggests that it may be incorrect to view taste-aversion leaming as a primitive type of conditioning that is immune to the influence of informational variables. Stated in the language of Kalat and Rozin, it appears that rats can be made to think when they are led to poison. Several lines of investigation have shown that aversion learning is disrupted by experiences that reduce the extent to which a causal inference can be made between the target conditioned stimulus flavor and toxicosis. One type of evidence involves the effect of repeated exposure to the CS flavor in the absence of toxicosis before the conditioning trial. A food that is repeatedly ingested without aversive effects in nature is not likely to be the cause of malaise experienced later. As expected on the basis of this consideration, extensive exposure to the CS flavor in the absence of toxicosis before the conditioning trial severely disrupts taste-aversion learning. Similarly, extensive exposure to the toxin unconditioned stimulus alone before the conditioning trial also interferes with aversion learning. Preconditioning US exposures in the absence of taste also reduce the extent to which a causal in-


3 19

ference can be made between taste and toxicosis. Because these two phenomena have been discussed extensively elsewhere (e.g., Domjan 1977a; Randich and LoLordo, 1979), they will not be treated further here. The CS preexposure and US preexposure phenomena noted disrupt aversion learning because of special experiences several days or more before the actual taste-aversion conditioning trial. Other research has shown that events closer to conditioning can also disrupt aversion learning. These events similarly reduce the extent to which a causal inference can be made between the target conditioned stimulus flavor and toxicosis. One of these types of experiments has shown that the presentation of several novel flavors during the conditioning trial reduces aversion learning to the target flavor. The second type of experiment has shown that aversion learning is disrupted if stimuli are introduced during conditioning that are better predictors of toxicosis than the target conditioned stimulus flavor. Finally, conditioning is similarly disrupted if in addition to receiving toxicosis after taste exposure, the animals are also injected with the toxin within several hours before access to the flavor. These phenomena are discussed in greater detail below. IN TASTE-AVERSION LEARNING A. OVERSHADOWING

It is a common observation in conditioning experiments that learning is disrupted if in addition to the target conditioned stimulus the animals are also exposed to other novel stimuli during the conditioning trial (e.g., Kamin, 1969). Pavlov (1927) referred to this effect as overshadowing. Overshadowing is also characteristic of taste-aversion learning. In one demonstration of the effect, Revusky (1971) conditioned an aversion to 0.2% saccharin in several groups of rats by allowing the animals to drink 2 ml of saccharin 75 min before the injection of lithium chloride. Fifteen minutes after the saccharin exposure, independent groups of animals were allowed to drink 5 ml of a novel 0.5, 1.5, or 4.5% solution of vinegar. Tests of saccharin conditioning conducted later showed that aversion learning was disrupted by the presentation of the vinegar flavor during the conditioning trial, and the extent of this disruption was directly related to the concentration of the vinegar solution. This latter aspect of the results is probably related to the fact that the more concentrated vinegar solutions were more novel to the subjects (Kalat, 1974). Consistent with this view, Revusky, Lavin, and Pschirrer (reported in Revusky and Garcia, 1970) found that the overshadowing of one flavor by another in taste aversion conditioning is greater if the overshadowing flavor is more novel. The experiments conducted by Revusky and his colleagues involved presenting one overshadowing novel flavor during the conditioning trial in addition to the target conditioned stimulus flavor. In a related experiment, Kalat and Rozin (197 1) investigated the effects of presenting three flavored solutions in addition

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to the target flavor during conditioning. Although the animals learned an aversion to the target stimulus when they also tasted three other substances during conditioning, the aversion learning was attenuated by exposure to the nontarget flavors. This effect was especially evident in Experiments 2B and 2C. The authors analyzed their data in terms of the absolute amount of the target flavor ingested during the postconditioning test session. However, the test session consisted of a choice between the target flavor and plain water. Intakes of the CS flavor in the overshadowing groups of Experiments 2B and 2C were 21 and 51% of total intake during the test session. In contrast, the corresponding values for the subjects not exposed to overshadowing flavors during conditioning were 4 and 5%, respectively. B.

RELATIVEVALIDITYOF CONDITIONED STIMULI

Another common observation in conditioning experiments is that the conditioning of one stimulus is disrupted by the presence of other conditioned stimuli that are better predictors of the unconditioned stimulus (see reviews by Rescorla and Wagner, 1972; Wagner, 1969). This research shows that the relative validity of cues as predictors of the US influences the rate of their conditioning. One of the important paradigms used in these investigations involves the prior conditioning of the interfering stimuli; another important paradigm involves the concurrent conditioning of the interfering cues.

I.

Prior Conditioning of Interfering Stimuli: The Blocking Effect

In this procedure one conditioned stimulus is first paired with the unconditioned stimulus until learning is well established. This conditioned stimulus is then presented during the conditioning of a novel stimulus, and conditioning of the novel stimulus is thereby severely disrupted. This blocking of conditioning by the presentation of a previously conditioned stimulus has been observed in several situations, including fear conditioning (Kamin, 1969) and foodreinforced discrimination learning (Miles, 1970). Explanations of the blocking effect have invoked cognitive mechanisms such as attention (Mackintosh, 1971, 1975; Sutherland and Mackintosh, 1971), expectancy (Rescorla and Wagner, 1972), and processing in short-term memory (Kamin, 1969; Terry and Wagner, 1975; Wagner et al., 1973; Wagner and Terry, 1975). Because of this, demonstrations of the blocking effect in taste-aversion learning have been considered important evidence for the involvement of cognitive mechanisms in tastetoxicosis conditioning as well. Some of the early efforts to demonstrate the blocking effect in taste-aversion learning were unsuccessful, and this failure was used to argue that taste-aversion learning is not influenced by cognitive processes (Kalat and Rozin, 1972). However, the phenomenon has been repeatedly demonstrated in other research. In


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some of these experiments, exteroceptive cues served as the blocking stimuli (e.g., Batson and Best, 1979; Braveman, 1979; Rudy er a / . , 1977; Willner, 1978). During the first phase of these studies, the animals were injected with lithium after placement in a distinctive environment for several trials. After this exteroceptive conditioning, the animals had the taste of saccharin paired with lithium. Saccharin aversion learning was attenuated for subjects that were exposed to the drug-conditioned spatial cues during the saccharin conditioning trial. Blocking may be more difficult to demonstrate when a taste solution rather than spatial cues serves as the blocking stimulus. The animals have to be exposed to the initially conditioned taste for this flavor to block the conditioning of a novel taste solution. However, the subjects will learn an aversion to the blocking flavor in the first phase of the experiment, and this will limit their voluntary contacts with the blocking stimulus during conditioning of the novel taste solution. In the first successful demonstration of blocking with taste stimuli, Revusky (197 1) facilitated exposure to the blocking taste stimulus during conditioning of the novel flavor by conducting conditioning after 2 days of water deprivation. Another approach to the problem is to expose subjects to tastes during the conditioning trials by infusing the flavored solutions directly into the oral cavity through a chronic fistula. This is the method we used in our experiments on blocking in the taste-aversion system (Domjan and Gemberling, unpublished; Gillan and Domjan, 1977). Most of our blocking experiments consisted of two phases. During the first phase, all subjects received differential conditioning in which the oral infusion of flavor D (the drug-predictive taste) was repeatedly paired with the injection of lithium chloride, and the oral infusion of flavor ND (the non-drug-predictive taste) was repeatedly presented without toxicosis. Solutions of vinegar and sodium chloride served as taste stimuli during this phase of the experiment and were assigned as flavors D and ND in a counterbalanced fashion. Following the initial differential conditioning, all animals had the taste of 0.5% saccharin paired with lithium malaise. In one of our experiments, one group of animals received an oral infusion of flavor D immediately before the saccharin conditioning trial, and another group was exposed to flavor ND immediately before saccharin conditioning. Several days after the saccharin conditioning trial, subjects were tested for their intake of the saccharin solution in a one-bottle test. The results of this test session are displayed in Fig. 12. As is evident from the figure, animals exposed to the drug-predictive flavor immediately before saccharin conditioning (Group D) learned a much weaker aversion to the saccharin flavor than animals for which the lithium was not expected during saccharin conditioning (Group ND). Group D drank more than twice as much saccharin during the test session as Group ND. In other experiments (Gillan and Domjan, 1977), we have found that exposure to flavor ND does not influence taste-aversion learning. That is, Group ND

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MINUTES

FIG.12. Mean cumulative intake of saccharin following aversion conditioning. For Group D, the lithium injection during the saccharin conditioning trial was announced by exposure to a flavor that was previously paired with drug treatment on several occassions. For Group ND, the lithium injection during the saccharin conditioning trial was preceded by a stimulus that had never before been followed by drug treatment. From Gillan and Domjan ( 1977). acquires as strong an aversion to saccharin as animals that do not receive any flavor in addition. to saccharin during the saccharin conditioning trial. Furthermore, the blocking of conditioning, which is produced by exposure to the previously conditioned flavor D, is related to the drug-conditioned properties of flavor D because extinction of these properties also attenuates the extent to which flavor D blocks saccharin aversion learning. Finally, for the drug-predictive flavor D to block saccharin conditioning, it has to be presented within an hour of the saccharin conditioning trial. If saccharin conditioning is conducted more than an hour after subjects are exposed to the drug-predictive flavor D, an interference with aversion learning does not occur (Domjan and Gemberling, 1980).

2. Concurrent Conditioning of Interfering Stimuli In the standard blocking experiment, the blocking stimulus is conditioned first. Aversion learning to a novel conditioned stimulus is then disrupted by the presence of the blocking stimulus because the blocking stimulus is a better predictor


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of the unconditioned stimulus than is the novel cue. Another experimental design for investigating how conditioning is influenced by the relative validity of the conditioned stimuli in the situation was introduced by Wagner er al. (1968). Repeated conditioning trials were administered, and the target conditioned stimulus (A) was paired with the unconditioned stimulus on 50% of the trials. In one group, the animals were exposed to a second CS (B) in addition to stimulus A on all reinforced trials (AB+) and a third stimulus (C) was presented with stimulus A on all nonreinforced trials (AC-). Thus, this group received an equal number of AB+ and AC- trials. The comparison group also had stimulus A paired with the unconditioned stimulus on 50% of the trials. However, in this case stimuli B and C occurred equally often on reinforced and nonreinforced trials ( A B k / A C k ) . It is important to note that in procedure AB+-/AC*, stimulus A is as good a predictor of the unconditioned stimulus as are stimuli B and C because each of these cues is paired with the US 50% of the time. In contrast, in procedure AB+/AC- , stimulus A is a less effective predictor of the US than is stimulus B because stimulus A is reinforced only 50% of the time whereas the US is presented every time stimulus B occurs. If conditioning is influenced by the extent to which one CS is more or less predictive of the US than other CSs in the situation. then procedure AB +/AC- should produce less conditioning of stimulus A than procedure ABdACzk. This outcome was observed by Wagner er a / . (1968) in both instrumental and classical conditioning situations with auditory and visual cues serving as conditioned stimuli. Much less research has been done in taste-aversion learning with the concurrent conditioning of interfering stimuli than with the prior conditioning of interfering cues in the blocking design. However, it appears that results comparable to those of Wagner et al. (1968) can also be observed in taste-aversion learning. Luongo (1976) compared the conditioning of stimulus A in procedures AB+I AC- and AB+-/AC* with tastes serving as stimuli A, B , and C and toxicosis serving as the unconditioned stimulus. Stimulus A was the flavor of 0.16% saccharin, and the tastes of cinnamon and wintergreen extract dissolved in water were assigned as stimuli B and C in a counterbalanced fashion. The compound stimuli AB and AC were made by adding the cinnamon and wintergreen extracts to the saccharin solution so that the resultant fluids consisted of 1% extract. In Experiment 1 subjects received 11 trials paired with lithium toxicosis and 1 I nonreinforced trials; in Experiments 2 and 3, 16 reinforced and 16 nonreinforced trials were administered. Following this training with the flavor mixtures, subjects were tested for their intake of the saccharin solution unadulterated with cinnamon or wintergreen. Animals that received the conditioning procedure AB+/AC- learned significantly weaker aversions to the saccharin solution in each experiment than subjects that received procedure AB?/AC+. This outcome was observed even though the saccharin solution was paired with toxicosis an

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equal number of times for both groups. Thus it appears that as in the research of Wagner et a!. (1968), taste-aversion learning is influenced by the extent to which the flavor CS is a good predictor of toxicosis relative to other tastes in the situation. C, PROXIMAL UNCONDITIONED STIMULUS PREEXPOSURE Another procedure that reduces the extent to which a causal relationship between taste and toxicosis can be inferred involves injecting the subjects with the toxin not only shortly after the taste exposure but also shortly before the taste presentation. Such proximal unconditioned stimulus preexposure has been found to reduce eyelid conditioning in rabbits (Terry, 1976). Recent experiments by Michael Best and me indicate that a similar interference effect occurs in tasteaversion learning (Best and Domjan, 1979; Domjan, 1978; Domjan and Best, 1977). The proximal US preexposure effect is illustrated by one of our experiments that compared the saccharin aversion learning of seven groups of rats (Best and Domjan, 1979, Experiment I). During the saccharin conditioning trial, all animals were given access to a 0.15% saccharin solution for 20 min or until they drank 3 ml, whichever occurred first. Forty minutes after the beginning of the saccharin presentation, each subject received a conditioning injection of 1.8 meq/kg lithium chloride. This was the only drug injection given to subjects in Group TAC (Taste-Aversion Control). The other groups not only received the conditioning injection but were also injected with lithium 90 min, 360 min, or 1 day before the saccharin conditioning trial. For three of the groups, the preexposure drug injection dose was 1.8 meq/kg, whereas for the other three groups the preexposure dose was 3.0 meqkg. Several days after the conditioning trial, subjects were given a 20-min onebottle test with the saccharin solution. The mean saccharin intake of each group is summarized in Fig. 13. The nonpreexposed Group TAC learned the strongest aversion to saccharin. Lithium preexposure 1 day before the conditioning trial did not produce a significant attenuation in saccharin aversion learning with either the 1.8 or 3 .O meq preexposure dose. In contrast, significant attenuations in conditioning were observed in both of the groups that were preexposed to lithium 90 min before the conditioning trial and in animals that received a 3.0 meq lithium injection 360 min before conditioning. However, the lower preexposure drug dose did not produce a significant interference effect when administered 360 min before the conditioning trial. The results described above indicate that a single drug injection administered before conditioning interferes with aversion learning only if the US preexposure occurs within a relatively short period before the conditioning trial. Drug treatment 1 day or more before conditioning does not disrupt aversion learning. However, the time course of the interference effect is related to the drug dose: the


lo

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1

OJ,

i

90min

360rnin

1 Day

PREEXPOSURE INTERVAL

FIG. 13. Mean saccharin test intakes for independent groups of rats that received either a 1.8 or a 3.0 meq/kg lithium injection 90 min, 360 min, or 1 day before saccharin conditioning. The dashed horizontal line represents the mean intake of Group TAC which

received saccharin conditioning in the absence of lithium preexposure. From Best and Domjan (1979).

interference effects of a higher preexposure dose persist longer than the disruptive effects of low drug doses. Other experiments have identified many characteristics of the proximal US preexposure effect and have shown that the phenomenon occurs in a wide variety of situations. Proximal US preexposure disrupts aversion learning even if the preexposure US treatment is otherwise effective in producing a “backward” conditioned saccharin aversion (Domjan and Best, 1977). The phenomenon also occurs whether or not the conditioning drug treatment is administered before or after exposure to the CS flavor during the training trial (Domjan, 1978). The interference effect is also evident when subjects are tested for their conditioned taste aversions while they are under the influence of the drug US (Best and Domjan, 1979), and proximal US preexposure disrupts conditioning even if the preexposure drug injection is paired with a novel flavor (Best and Domjan, 1979). In all of our published research on the proximal US preexposure effect, both the preexposure drug injection and the conditioning drug injection administered later consisted of lithium chloride. However, one drug administered shortly before a taste-aversion conditioning trial can also interfere with aversion conditioning induced by other drugs or treatments. We have observed that proximal preexposure to lithium disrupts taste-aversion conditioning induced by rotational stimulation (Domjan, unpublished). Others have reported that proximal preexposure to atropine disrupts taste aversions conditioned by lithium and radiation

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exposure (Deutsch, 1978; Gould and Yatvin, 1972; 1973); preexposure to pimozine disrupts conditioning with amphetamine (Grupp, 1977); proximal preexposure to antihistamine disrupts conditioning with irradiation (Levy et al., 1974); preexposure to dexamethasone disrupts conditioning with lithium (Hennessy et al., 1976); and preexposure to a-methltyrosine disrupts amphetamine conditioning (Goudie et al., 1975b). These effects may be in part due to the fact that the preexposure drug treatments create some malaise which reduces the causal inference that can be made between the taste experience and the subsequent conditioning drug treatment. Consistent with this suggestion, Deutsch ( 1978) found that atropine interferes with taste-aversion learning produced by lithium if the atropine is injected shortly before the conditioning trial but does not disrupt learning if the atropine is given between the taste exposure and the lithium injection during conditioning. Similarly, Sessions (1975) reported that the interference effects of antihistamine on radiation-induced aversion conditioning reported by Levy er al. (1974) do not occur if the antihistamine is injected between the taste exposure and irradiation rather than before the taste exposure during conditioning.

A CONTINUING SEARCH FOR GENERAL AND VI. CONCLUSION: U N I Q U E CHARACTERISTICS OF INGESTIONALAVERSION LEARNING

The taste-aversion learning paradigm has become a prominent field of investigation because some of the characteristics of this type of learning at first appeared to be unique, and this brought into question the advisability of trying to identify general laws of learning. The attack on the generality of the laws of learning had two aspects. One was the suggestion that different types of mechanisms may be involved in the various examples of learning that are exhibited by a given species. The other was the suggestion that the laws of learning discovered with one species may not be applicable to other types of animals. Because the research reviewed in the present chapter did not compare and contrast learning in different types of animals, the discussion does not permit reaching a conclusion about the generality of the laws of learning among various species. However, we can say something about the generality of learning mechanisms across various types of conditioning procedures for at least one type of animal, the omnivorous mammal as exemplified by the rat. For this type of organism, some of the characteristics of taste-aversion learning that were initially considered to be unique, such as the stimulus selectivity effect, have since been identified in other conditioning preparations. There are also few instances of conditioning phenomena observed in other conditioning preparations that have not been also observed in taste-aversion learning after sufficient exploration. These developments suggest that the pursuit of general theories of learning may not be as ill-fated a venture as some have suggested. Furthermore, the use of


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examples from taste-aversion learning to argue against the generality of the laws of learning is no longer very convincing. Although ingestional aversion learning appears to have many characteristics in common with other types of conditioning, it is probably an overstatement to suggest that this type of learning is entirely lacking in unique features. There are at least two aspects of ingestional aversion learning that may turn out to be unique. First, the conditioning situation involves having animals experience the conditioned stimuli during the course of ingestion, and this provides a complex array of covarying and interrelated stimuli including the visual, olfactory, taste, and tactile properties of the food as well as the orosensory stimuli involved in mastication and swallowing. These numerous sensations that accompany ingestion contrast with the simple auditory and visual conditioned stimuli used in other conditioning preparations and play an important role in ingestional aversion learning. The other characteristic of ingestional aversion learning that may turn out to be unique is that aversions are learned in one trial even if the toxicosis is not induced until several hours after ingestion of the target edible. Ingestional aversion learning may have some unique features because the stimuli involved in this type of conditioning have certain characteristics that are very different from the characteristics of stimuli involved in other types of learning. The unique characteristics of ingestional stimuli may lead to unique conditioning phenomena which are nevertheless governed by generally applicable laws of learning (cf. Krane and Wagner, 1974). Alternatively, the unique phenomena observed in ingestional aversion learning may result from the operation of unique learning processes (cf. Rozin and Kalat, 1971). Whether unique learning processes or unique stimulus features are responsible for the unusual aspects of ingestional aversion learning is central to theoretical evaluations of this type of learning. Research on the importance and role of the complex of ingestive sensations for aversion learning is still in its infancy. For example, very little is known about the mechanisms of the modulation of selective associations by ingestion-related events in the systems in which these effects were discovered. We also do not know if comparable phenomena exist in other situations. Therefore it is premature to speculate whether these effects reflect unique aspects of the stimuli involved or unique learning mechanisms. In contrast to the paucity of research on the importance of the complex of ingestive sensations, there has been a great deal of empirical work and theoretical speculation concerning the mechanisms of long-delay ingestional-aversion learning (see, for example, reviews by Best and Barker, 1977; Garcia and Ervin, 1968; Kalat, 1977; Revusky and Garcia, 1970; Revusky, 1977c; Rozin and Kalat, 1971). Furthermore, this research suggests that long-delay ingestionalaversion learning may be the result of a unique learning process and not the result of unique properties of ingestional stimuli. Two types of evidence support this conclusion. First, long-delay learning of the sort found in ingestional condition-

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ing with toxicosis is rarely found in other conditioning preparations. Second, long-delay ingestional aversion learning is not limited to taste cues encountered during ingestion. The most systematic attempt to discover long-delay learning effects in other learning preparations has been carried out by Revusky and his colleagues and has been motivated by the concurrent interference theory proposed by Revusky (for reviews, see Revusky, 1971, 1977~).The basic tenet of the concurrent interference theory is that long-delay learning will occur in situations in which there is minimal concurrent interference with the association of the events of interest, the conditioned and unconditioned stimuli in Pavlovian conditioning experiments. Concurrent interference is said to occur when either the CS or the US of interest becomes associated with other stimuli in the situation. In the typical long-delay taste-aversion learning experiment, subjects are exposed to only one novel flavor, followed by the toxin US several hours later. There is little opportunity for concurrent interference in such a procedure because there are no prominent stimuli other than the toxin with which the novel taste can become associated. Similarly, there are no prominent stimuli other than the novel taste that can become easily associated with the toxin US. (The various nongustatory stimuli animals are likely to encounter during the delay interval are not easily associated with toxicosis.) In contrast to conditioning with toxicosis, there are many opportunities for concurrent interference in conditioning with cutaneous shock. Most situations involve a continually changing array of audiovisual and tactile cues as the animal moves about, and all of these stimuli can be easily associated with shock to provide concurrent interference for the conditioning of an aversion to the conditioned stimulus of interest. The long-delay learning effect in taste-aversion conditioning is predicted by the concurrent interference theory from the fact that there is a limited number of stimuli that can be easily conditioned with toxicosis. Revusky (1971, 1977c) has referred to this selectivity of association as a relevance principle, and has suggested that long-delay learning should be evident in all situations that involve relevance principles. He further suggested that in addition to the taste-toxicosis relevance principle, there is also situational relevance. According to the situational relevance principle, events that occur in an experimental chamber are not very likely to become associated with events that occur outside the experimental chamber (such as in the home cage), and vice versa. The concurrent interference theory, together with the principle of situational relevance, predicts that animals will associate events that occur in the same experimental chamber with one another even if a long delay separates the events. What is required is that the animals be removed from the experimental chamber during the delay interval. Consistent with this prediction, several experiments have demonstrated learning with a long delay introduced between the discriminative stimulus and reinforcement and between the response and reinforcement in


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runway and T-maze situations when animals spend the delay interval outside the experimental chamber (see Revusky, 1977c, for a review). However, the delay interval was never as long in these experiments as the intervals that can support long-delay taste-aversion learning. For example, in one intertrial association experiment (Pschirrer, 1972), the delay interval was about 15 min, and in a delay of reinforcement experiment the longest delay interval tested was 60 min (Lett, 1975). Furthermore, a conditioning effect was often not evident in these studies until extensive training had been provided. Learning was not evident with a 60-min delay between response and reinforcement in the T-maze until the rats received more than 30 rewarded trials (Lett, 1975). In a black-white discrimination experiment with about a 4-min delay between discriminative stimulus and reinforcement (Revusky, 1974), learning was not evident until subjects received more than 300 trials. In contrast to the above efforts to obtain learning with long delays between a response or discriminative stimulus and reinforcement, one-trial long-delay learning of positive affective responses is possible if special procedures are employed. In one experiment (D’Amato and Buckiewicz, 1980), Cebus monkeys were first tested for their baseline side preference in a T-maze. During conditioning, they were confined to the nonpreferred arm for 1 min, than placed in a holding cage for the delay interval (30 min), and finally returned to the start area of the T-maze to receive the food reward. This procedure increased their preference for the arm of the T-maze that had been paired with food. One-trial spatial preference learning has been also obtained in rats with as long as a 2 hr CS-US interval when the CS exposure during conditioning was 40 min and the animals received the sucrose US in a novel waste basket instead of the T-maze or the home cage (D’Amato, 1980). These are intriguing findings. However, further empirical and theoretical analysis of these procedures is needed before a detailed comparison with long-delay taste-aversion learning can be made. The fact that long-delay associations are not easy to demonstrate in situations that do not involve poison avoidance is not conclusive evidence that unique learning processes are involved. In many demonstrations of long-delay learning distinctive tastes were used to signal toxicosis. Because taste stimuli have temporal-intensity patterns that are very different from the temporal-intensity characteristics of other types of stimuli, it is possible that long-delay tasteaversion learning reflects these unique stimulus features and not the operation of unique learning processes (cf. Krane and Wagner, 1974; Testa, 1974). However, long-delay ingestional aversion learning has also been observed in situations in which distinctive visual cues signal toxicosis (e.g., Braveman, 1977; Martin and Bellingham, 1979; Wilcoxon, 1977). The visual cues in these studies did not have the temporal-intensity pattern characteristic of tastes. Therefore, the unique stimulus features of taste cannot be used to explain long-delay visual aversion learning.

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Much has yet to be discovered concerning the mechanisms of long-delay visual-aversion learning. For example, we do not know whether all visual cues can become readily associated with toxicosis or only visual features of ingested foods. We also do not know whether the mechanisms of visual-aversion learning are the same as the mechanisms of taste-aversion learning. It will be exciting to witness the resolution of these issues in the coming years and to see whether long-delay poison-avoidance learning in fact turns out to be mediated by unique conditioning mechanisms. References Barker, L . M., Best, M. R., and Domjan, M. (eds.). 1977. “Learning Mechanisms in Food Selection.” Baylor Univ. Press, Waco, Texas. Batson, I . D.. and Best, P. J. 1979. Drug-preexposure effects in flavor-aversion learning: Associative interference by conditioned environmental stimuli. J . Exp. Psychol. Anim. Behav. Proc. 5 , 273-283. Best, M. R. 1975. Conditioned and latent inhibition in taste-aversion learning: Clarifying the role of learned safety. J. Exp. Psychol. Anim. Behav. Proc. 1 , 97-1 13. Best, M. R., and Barker, L. M. 1977. The nature of “learned safety” and its role in the delay of reinforcement gradient. In “Learning Mechanisms in Food Selection” (L. M. Barker, M. R. Best, and M. Domjan, eds.), pp. 295-317. Baylor Univ. Press, Waco, Texas. Best, M. R.,and Batson, J. D. 1977. Enhancing the expression of flavor neophobia: Some effects of the ingestion-illness contingency. J . Exp. Psychol. Anim. Behav. Proc. 3, 132-143. Best, M. R., and Domjan, M. 1979. Characteristics of the lithium-mediated proximal US pmxposure effect in flavor-aversion conditioning. Anim. Learn. Behav. 7 , 433-440. Best, P. J., Best, M. R., and Mickley, G. A. 1973. Conditioned aversion to distinct environmental stimuli resulting from gastrointestinal distress. J . Comp. Physiol. Psycho/. 85, 250-257. Bitteman, M. E. 1975. The comparative analysis of learning. Science 188, 699-709. Bitterman, M. E. 1976. Flavor aversion studies. Science 192, 266-267. Braveman, N. S. 1975a. Formation of taste aversions in rats following prior exposure to sickness. Learn. Motiv. 6 , 512-534. Braveman, N. S. 1975b. Relative salience of gustatory and visual cues in the formation of poisonbased food aversions by guinea pigs (Cavia porcellus). Behav. Bio. 14, 189-199. Braveman, N. S . 1977. Visually guided avoidance of poisonous foods in mammals. In “Learning Mechanisms in Food Selection” (L. M. Barker, M. R . Best, and M. Domjan, eds.), pp. 455-473. Baylor Univ. Press, Waco, Texas. Braveman, N. S. 1979. The role of blocking and compensatory conditioning in the treatment preexposure effect. Psychopharmacologia 61, 177- 189. Brower, L. P., Brower, J. V. Z., and Corvino, J. M. 1967. Plant poisons in a terrestrial food chain. Proc. Narl. Acad. Sci. U.S.A. 57, 893-898. Cannon, D. S., Berman, R. F., Baker, T.B., and Atkinson, C. A. 1975. Effects of preconditioning unconditioned stimulus experience on learned taste aversions. J. Exp. Psychol. h i m . B e h v . Proc. 1, 270-284. Carroll, M. E., Dinc, H. I., Levy, C. J., and Smith, J. C. 1975. Demonstrations of neophobia and enhanced neophobia in the albino rat. J . Comp. Physiol. Psyrhol. 89, 457-467. Clarke, J. C., Westbrook, R. F., and Irwin, J. 1979. Potentiation instead of overshadowing in the pigeon. Behav. Neural B i d . 25, 18-29. Corey, D. T. 1978. The determinants of exploration and neophobia. Neurosci. Biohehav. Rev. 2, 235-253.


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Mitchell, D. 1977. Reply to Revusky. Anim. Learn. Behav. 5 , 321-322. Mitchell, D. 1978. The psychological vs. the ethological rat: Two views of the poison avoidance behavior of the rat compared. h i m . Learn. Behav. 6, 121-124. Mitchell, D., Kirschbaum, E. H., and Perry, R. L. 1975. Effectsof neophobia and habituation on the poison-induced avoidance of exteroceptive stimuli in the rat. J. Exp. Psyrhol. Anim. Behav. Proc. 1, 47-55. Mitchell, D., Scott, D. W., and Mitchell, L. K. 1977. Attenuated and enhanced neophobia in the taste-aversion “delay of reinforcement” effect. h i m . Learn. Behav. 5, 99-102. Monroe, B., and Barker, L. M. 1979. A contingency analysis of taste aversion conditioning. Anim. Learn. Behav. 7 , 141-143. Morest, D. K. 1967. Experimental study of the projections of the tractus solitarius and the area postreme in the cat. J. Comp Neurol. 130, 277-293. Morris, D. D., and Smith, J. C. 1964. X-ray-conditioned saccharin aversion induced during the immediate postexposure period. Radiur. Res. 21, 513-519. Morrison, G. R., and Collyer, R. 1974. Taste-mediated conditioned aversion to an exteroceptive stimulus following LiCl poisoning. J. Comp. Physiol. Psyrhol. 86, 51-55. Nachman, M. 1963. Learned aversion to the taste of lithium chloride and generalization to other salts. J. Comp. Physiol. Psyrhol. 56, 343-349. Nachman, M. 1970. Learned taste and temperature aversions due to lithium chloride sickness after temporal delays. J. Comp. Physiol. Psychol. 73, 22-30. Nachman, M., and Ashe, .I.H. 1973. Learned taste aversions in rats as a function of dosage, concentration, and route of administration of LiCI. Physiol. Behav. 10, 73-78. Nachman, M., and Jones, D. R. 1974. Learned taste aversions over long delays in rats: The role of learned safety. J. Comp. Physiol. Psyrhol. 86, 949-956. Nachman, M., Rauschenberger, J., and Ashe, J. H. 1977. Studies of learned aversions using non-gustatory stimuli. In “Learning Mechanisms in Food Selection” (L. M. Barker, M. R. Best, and M. Domjan, eds.), pp. 395-417. Baylor Univ. Press, Waco, Texas. Nowlis, G. H. 1974. Conditioned stimulus intensity and acquired alimentary aversions in the rat. J. Comp. Physiol. Psychol. 86, 1173-1 184. Pavlov, I. P. 1927. “Conditioned Reflexes.” Oxford Univ. Press, London and New York. Pschirrer, M. E. 1972. Goal events as discriminative stimuli over extended intertrial intervals. 1. EXP. Psycho/. 96, 425-432. Randich, A., and LoLordo, V. M. 1979. Associative and nonassociative theories of the UCS preexposure phenomenon: Implications for Pavlovian conditioning. Psyrhol. Bull. 86, 523548.

Rescorla, R. A., and Cunningham, C. L. 1979. Spatial contiguity facilitates Pavlovian second-order conditioning. J. Exp. Psychol. Anim. Behav. Proc. 5, 152-161. Rescorla, R. A., and Furrow, D. R. 1977. Stimulus similarity as a determinant of Pavlovian conditioning. J. Exp. Psychol. h i m . Behav. Proc. 3, 203-215. Rescorla, R. A , , and Holland, P. C. 1976. Some behavioral approaches to the study of learning. In “Neural Mechanisms of Learning and Memory” (M. R. Rosenzweig and E. L. Bennett, eds.), pp. 165-192. MIT Press, Cambridge, Massachusetts. Rescorla, R. A., and Wagner, A. R. 1972. A theory of Pavlovian conditioning: Variations in the effectiveness of reinforcement and nonreinforcement. In “Classical Conditioning 11” (A. H. Black and W. F. Prokasy, eds.), pp. 64-99. Appleton, New York. Revusky, S. H. 1968. Aversion to sucrose produced by contingent x-irradiation: Temporal and dosage parameters. J . Comp. Physiol. Psychol. 65, 17-22. Revusky, S . 1971. The role of interference in association over a delay. In “Animal Memory” (W. K. Honig and P. H. R. James, eds.), pp. 155-213. Academic Press, New York. Revusky, S. H. 1974. Long-delay learning in rats: A black-white discrimination. Bull. Psychon. Sor. 4, 526-528.

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Revusky. S. 1977a. Correction of a paper by Mitchell, Scott, and Mitchell. Anim. Learn. Behrrv. 5 , 320. Revusky, S. 1977b. Learning as a general process with an emphasis on data from feeding experiments. I n “Food Aversion Learning” (N. W. Milgram. L. Krames, and T. M. Alloway, eds.), pp. 1-51. Plenum, New York. Revusky. S. 1 9 7 7 ~ .The concurrent interference approach to delay learning. I n -earning Mechanisms in Food Selection” (L. M. Baker, M. R. Best, and M. Domjan, eds.), pp. 319-366. Baylor Univ. Press, Waco, Texas. Revusky, S. 1978. Reply to Mitchell. Anim. Learn. Behnv. 6 , 119-120. Revusky, S. H., and Bedarf. E. W. 1967. Association of illness with ingestion of novel foods. Scienc~155, 2 19-220. Revusky, S. H.. and Garcia, J . 1970. Learned associations over long delays. I n “Psychology of Learning and Motivation” ( G . H.Bower and J . T. Spence, eds.), Vol. 4, pp. 1-84. Academic Press, New York. Revusky. S., and Parker, L. A. 1976. Aversions to unflavored water and drinking cup produced by delayed sickness. J. Exp. Psychol. Anim. Behav. Proc. 2, 342-353. Revusky, S., Parker. L., Coombes, J . , and Coombes, S. 1976. Rat data which suggest alcoholic beverages should be swallowed during chemical aversion therapy, not just tasted. Behuv. Res. Ther. 14, 189-194. Richter, C. P. 1953. Experimentally produced behavior reactions to food poisoning in wild and domesticated rats. Ann. N.Y. Acnd. Sci. 56, 225-239. Riley, A. L., and Clarke, C. M. 1977. Conditioned taste aversions: A bibliography. 111 “Leaming Mechanisms in Food Selection” (L. M. Barker, M. R. Best, and M. Domjan, eds.), pp, 593-616. Baylor Univ. Press, Waco, Texas. Rozin. P. 1967. Specific aversions as a component of specific hungers. J. Comp. Physiol. Psycho/. 64, 237-242. Rozin, P. 1969. Central or peripheral mediation of learning with long CS-US intervals in the feeding system J . Comp. Phjaiol. Psychol. 67, 421 -429. Rozin, P. 1976. The selection of foods by rats, humans, and other animals. In “Advances in the Study of Behavior” (J. S. Rosenblatt, R. A. Hinde, C. Beer, and M. Busnel, eds.), Vol. 6, pp. 21-76. Academic Press, New York. Rozin, P.. and Kalat, J. W. 1971. Specific hungers and poison avoidance as adaptive specializations of learning. Psychol. Rev. 78, 459-486. Rudy, J . W . , Iwens. J . , and Best, P. J . 1977. Pairing novel exteroceptive cues and illness reduces illness-induced taste aversions. J . Exp. Psycho/. Anint. Behav. Proc. 3, 14-25. Rusiniak, K. W., Hankins, W. G., Garcia, J., and Brett, L. P. 1979. Flavor-illness aversions: Potentiation of odor by taste in rats. Behav. Neurol. Biol. 25, 1-17. Rzoska, J. 1953. Bait shyness, a study in rat behaviour. Br. J . Anim. Behav. 1, 128-135. Scarhorough, B. B., Whaley, D. L..and Rogers, J . G. 1964. Saccharin avoidance behavior instigated by x-irradiation in backward conditioning paradigms. Psychol. Rep. 14, 475-481. Schwanz, 9 . 1974. On going back to nature: A review of Seligman and Hager’s “Biological Boundaries of Learning.” J . Exp. Anal. Behnv. 21, 183-198. Seligman, M. E. P. 1970. On the generality of the laws of learning. Psychol. Rev. 77, 406-418. Seligman, M. E. P., and Hager, J. L. 1972. “Biological Boundaries of Learning.” Appleton, New York. Sessions, G. R. 1975. Histamine and radiation-induced taste aversion conditioning. Science 190, 402-403. Shettleworth, S. J. 1972a. Constraints on learning. fn “Advances in the Study of Behavior” (D. S. Lehrman, R. S. Hinde, and E. Shaw, eds.), Vol. 4, pp. 1-68. Academic Press, New York. Shettleworth, S. J . 1972b. Stimulus relevance in the control of drinking and conditioned fear responses in domestic chicks (Gallus gallus). J . Comp. Physiol. Psvrhol. 80, 175-198.

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Smith, J. C. 1971. Radiation: Its detection and its effects on taste preference. In “Progress in Physiological Psychology” (E.Stellarand J. M. Sprague, eds.), Vol. 4, pp. 53-1 18. Academic Ress, New York. Smith, J . C. 1978. Comment on paper by Mitchell, Scott, and Mitchell. Anim. Learn. Behav. 6 , 117-118.

Smith, J. C., and Roll, D. L. 1967. Trace conditioning with x-rays as an aversive stimulus. Psychon. sci. 9, 11-12. Smith, J. C., Taylor, H. L., Morris, D. D., and Hendricks, J. 1965. Further studies of x-ray conditioned saccharin aversion during the postexposure period. Rudiur. Res. 24, 423-431. Spiker, V. A. 1977. Taste aversion: A procedural analysis and an alternative paradigmatic classification. Psychol. Rec. 27, 753-769. Sutherland, N. S., and Mackintosh, N. J. 1971. “Mechanisms of Animal Discrimination Learning.” Academic Press, New York. Taukulis, H . K., and Revusky, S. H. 1975. Odor as a conditioned inhibitor: Applicability of the Rescorla-Wagner model to feeding behavior. Learn. Motiv. 6, 11-27. Terry, W.S. 1976. Effects of priming unconditioned stimulus representation in short-term memory on Pavlovian conditioning. J. Exp. Psychol. Anim. Behav. Proc. 2, 354-369. Terry, W. S . , and Wagner, A. R. 1975. Short-term memory for “surprising” versus “expected” unconditioned stimuli in Pavlovian conditioning. J. Exp. Psychol. Anim. Behav. Proc. 1, 122-133.

Testa, T. J . 1974. Causal relationships and the acquisition of avoidance responses. Psychol. Rev. 81, 49 1-505.

Testa, T. J. 1975. Effects of similarity of location and temporal intensity pattern of conditioned and unconditioned stimuli on the acquisition of conditioned suppression in rats. J. Exp. Psycho/. Anim. Behuv. Proc. 1 , 114-121. Testa, T.I . , and Ternes, J. W. 1977. Specificity of conditioning mechanisms in the modification of food preferences. In “Learning Mechanisms in Food Selection” (L. M. Barker, M. R. Best, and M. Domjan, eds.) pp, 229-253. Baylor Univ. Press, Waco, Texas. Tevis. L. 1956. Behavior of a population of forest-mice when subjected to poison. J. Mammal. 37, 358-370.

Wagner, A. R. 1969. Stimulus validity and stimulus selection. In “Fundamental Issues in Associative Learning’’ (W. K. Honig and N. J. Mackintosh, eds.), pp. 90-122. Dalhousie Univ. Press, Halifax. Wagner, A. R.,and Terry, W. S. 1975. Backward conditioning to a CS following an expected versus a surprising UCS. Anim. Learn. Behuv. 3, 370-374. Wagner, A. R., Logan, F. A., Haberlandt, K.,and Rice, T. 1968. Stimulus selection in animal discrimination learning. J. Exp. Psychol. 76, 171-180. Wagner, A. R.,Rudy, J. W., and Whitlow, J . W. 1973. Rehearsal in animal conditioning. J . Exp. Psychol. 91,407-426. Westbrook, R. F., Clarke, J. C., and Provost, S. 1980. Long-delay learning in the pigeon: Flavor, color, and flavor-mediated color aversions. Behav. Neural Biol. 28, 393-407. Whittaker, R. H., and Feeny, P. P. 1971 Allelochemicals: Chemical interactions between species. Science 171, 757-770. Wilcoxon, H. C. 1977. Long-delay learning of ingestive aversions in quail. In “Learning Mechanisms in Food Selection” (L. M. Barker, M. R. Best, and M. Domjan, eds.), pp. 419-453. Baylor Univ. Press, Waco. Texas. Willner, J . A. 1978. Blocking of a taste aversion by prior pairings of exteroceptive stimuli with illness. Learn. Moriv. 9, 125-140. Wright, W. E., Foshee, D. P., and McCleary. G. E. 1971. Comparisonof taste aversion with various delays and cyclophosphamide dose levels. Psychon. Sci. 22, 55-56. I

ADVANCES IN THE STUDY OF BEHAVIOR VOL. I I

The Functional Organization of Phases of Memory Consolidation R . J . ANDREW ETHOLOGY AND NEUROPHYSIOLOGY GROUP SCHOOL OF BIOLOGICAL SCIENCES UNIVERSITY OF SUSSEX BRIGHTON, UNITED KINGDOM

I Phases of Memory in Higher Vertebrates: Evidence from Amnestic Agents A. One or More Phases of Memory Formation'?

I1 111 1V V

VI

,

...

B. Amnesia: Disruption of Consolidation or of Retri C. Sequential Dependence of Phases of Memory . . Human Memory . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Models of Memory Formation . . . Previous Studies of Memory, Using Pecking in the Chick ............... Hormones and Other Enhancing Agents in the Chick: Opposition to Amnestic Agents . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . A . The Enhancement of Normal Memory in the Chick.. . . . . . . . . . . . . . . . . B. Phases of Memory in the Chick. . . . . . . . . . . . . . . . .......... C. Testosterone and Retrieval Processes ............................. Conclusion: General Implications . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

338 339

344 345 341 348 350 352 354 357 359 36 1 363

There is little agreement as to the functional properties and interrelation of different phases of memory formation; their possible number, and even the existence of genuinely different phases, have been matters for dispute. A major difficulty in the interpretation of mammalian studies, as will be seen, is the considerable variation in estimates of even the most basic property of such hypothetical phases: their duration in time. Much of this variation is undoubtedly due to differences of species or strain, and to differences in task or in testing procedure, and it is clearly necessary to standardize all of these to a far greater extent than in the past, if separate studies are to be collated and interpreted fully. One instance in which this has to some extent been done is that of a task based on the inhibition of spontaneous pecking in the domestic chick. A comprehensive and well-supported model of memory formation already exists (Gibbs and Ng, 337

Copyright @ 1980 by Academic Ress. Inc. All rights of reprnduction in any form resewed ISBN 0-12-a)4511-7

338

R. J . ANDREW

1977), based on this task; it convincingly defines a series of phases in memory formation, which are sequentially dependent, so that the disruption of one causes subsequent phases to fail to establish. In this article, I examine some of the main issues raised by studies of memory formation in mammals in the light of evidence from the chick. Recent work in my laboratory has demonstrated brief sharply timed transitions between phases, which can be defined not only by time courses of susceptibility to, or survival under, amnestic agents, but also by changes in the vulnerability of the trace to interference from subsequently established traces. Earlier work on the effects of testosterone on attention had suggested that these might depend upon increased stability of information in a short-term memory store. Effects of the hormone on the different phases of consolidation were therefore sought: almost all (and not just the earliest) proved to be affected. However, the timings of most of the main transitions are unaffected; this, and the character of the changes themselves, suggests that the hormone is acting upon a mechanism external to the stores in which the consolidating trace is held; I argue that this mechanism may be important in retrieving and sustaining information. I.

PHASES OF MEMORY IN HIGHER VERTEBRATES: EVIDENCE FROM AMNESTIC AGENTS

The main measures with which I will deal here, and in the later sections devoted to work on memory in the chick, are the persistence in time, following a brief and precisely timed learning event, of ( a ) susceptibility to various agents or manipulations, and ( b ) forgetting subsequent to the application of the agent or manipulation, or in its continuing presence. Estimates of these time courses vary greatly, and are certainly affected by variables such as intensity of the agent, and sensitivity of the test, as well as varying between strain and species (McGaugh and Herz, 1972). Thus by increasing test sensitivity a considerable extension of the period of susceptibility to electroconvulsive shock (ECS)can be obtained (McGaugh and Dawson, 1971), while susceptibility to ECS can be extended from much less than 5 sec after training to more than 30 min by increasing the intensity of current and shifting its site of application on the cortex (Gold et al., 1973b). Indeed, some authors (e.g., McGaugh and Gold, 1974) have taken the robust view that variability is so great and of such a type (i.e., it is sensitive to intensity of agent or to effectiveness of reinforcer) that either no useful conclusion can be drawn from such evidence as to the duration of memory processes, or a single process of consolidation must underlie memory formation, with traces becoming progressively more resistant to disruption. It is certainly impossible to use such evidence to prove or disprove any of the models of memory formation considered later. However, there do seem to be

MEMORY CONSOLIDATION

339

typical values for both susceptibility and survival which differ between agents, and some at least of the markedly discrepant values can be given special explanations. My aim in this section will be to show what likely hypotheses are raised by the existing evidence, and then to turn, in later sections, to a large body of data from the chick in which time courses involving widely different types of manipulations, but all based on the same standard test, can be compared. It will be convenient to divide this section into three parts: ( a ) how many phases of memory formation are there likely to be; ( h )do the usual amnestic agents act by disturbing consolidation or by making subsequent retrieval impossible; and ( c ) are memory phases sequential, in the sense that information can reach a later phase only by passage through the immediately previous one? A.

O N E OR

MOREPHASES

OF

MEMORY FORMATION?

The amnestic agents commonly in use are often (and perhaps rightly) assumed to have obvious central consequences which ensure that their main central effects should be on distinct phases of memory formation. Electroconvulsive shock (ECS) is assumed to disrupt patterns of neuronal firing (e.g., Kesner, 1973); the induction (or reversal) of changes at synapses such as might normally provide the first basis of storage following neural activity has also been suggested (Flood et al., 1977). Anesthetics and similar agents should interfere with the processing of information, while protein synthesis inhibitors should block the final establishment of structural changes. In fact, as might be expected of such powerful agents, both ECS and protein synthesis inhibitors have other effects which could affect memory formation. Thus, for example, ECS depresses protein synthesis significantly, if only moderately (Dunn, 1971); inhibition of protein synthesis may inhibit tyrosine hydroxylase and thereby depress monoamine systems (Flexner ef al., 1973; Flexner and Goodman, 1975). It is perhaps not likely that the main effects of these agents are to be explained in these ways; thus inhibition of tyrosine hydroxylase alone does not produce amnesia (Squire et a/., 1974), while the production of amnesia correlates well with the attainment of high levels of inhibition of protein synthesis (McGaugh and Gold, 1974). However, it is clearly impossible to assume that each group of agents always acts by the most obvious route and only by that route. The duration of susceptibility to ECS is typically no more than 30 sec to 1 min after learning, and is often less (Table I). However, even without obvious special conditions (see following), times as long as 6 hr have been reported (Kopp et al., 1966), and McGaugh and Herz (1972) note that the more extended periods of susceptibility tend to be found in studies in which more sensitive test procedures were used. The classical position, that susceptibility to ECS defines an initial very short phase in which memory is sustained by neural activity alone, is thus

TABLE I DURATIONOF SUSCEPTIBILITY TO AND SURVIVAL OF AMNESIC AGENTS"~

Agent I . ECS At 8 sec At 20 sec

Animal Mouse

Rat

Reference

Still susceptible

No longer susceptible

17 19 19

0 min

11 15 12

30 min 6hr

30 min

5 sec

10 sec

10 sec

30 sec

15-30 sec

60 sec

Surviving

Lost

5 rnin

< I hr Ihr

6 hr

1-2 hr?

8 High punishment

LOW punishment 23 18 Test

Short Long Subconvulsive Convulsive 2. ECS

Chick

20 16

Several seconds Ihr 15 min 0-10 sec

30 sec

3 0 4 0 sec 50 sec

+ special conditions

Inhibition of protein synthesis Deprivation of REM sleep

Mouse

11

9 hr (duration of inhibition)

17

3hr 2 days

9

6 hr

3. Anesthetics

Ether

Mouse

14

I

Rat

2 21

5 min 24 min 24 hr 5 min

15 min 24 min

10 min

30 rnin

Halothane Sodium pentobarbital NO

co

2

Concussion

Chick

7 27 21

Rat Mouse Mouse Man

25 26

Chick

6

Mouse

4

5

0 20 min 10 min

0 30 min 30 min

1.5 hr 40 min 20 min 15 min 60 min

4. Convulsant ether

Flurothyl

5. Protein synthesis inhibitors Cycloheximide

Anisomycin Acetoxycycloheximide

Mouse

Chick Chick Mouse

24 23 Low punishment High punishment 3 13 13

3

4 min, 64 min, 24 hr. according to dose 6hr 3 hr

10-20 min 20 min

0

10

Puromycin Puromycin on cortex

3 10

11-60 days

30-45 min 30-45 min 30 min

6hr 1 min

6hr

24 hr

3hr

6hr

3hr 5h r 15 min 10-20 hr

6hr 5hr 3hr c 20hr

“The latest times at which there was susceptibility or survival are given, together with the fmt at which there was not. The studies considered here were chosen because they gave relatively clear timings of susceptibility or survival. They were: 1. Abt eral. (1961); 2. Alpem and Kimble (1967); 3. Barondes and Cohen (1968); 4. Bohdanecky eral. (1%8); 5. Bovet er al. (1966); 6. Cherkin (1969); 7. Cherkin and Lee-Teng (1965); 8. Choroverand Schiller (1965); 9. Fishbeinetal. (1971); 10. Flexnerera/. (1%7); 11.Floodetal. (1977); 12.GellerandJarvik(1968); 13.GibbsandNg(1977); 14. Herz(1969); 15.Kopp era/. (1966); 16. Lee-Teng(1970); 17. Linden etal. (1975); 18. McGaugh and Dawson(l971); 19. McGaugh and Landfield (1970); 20. Miller and Springer (1971); 21. Pearlman et al. (l%l); 22. Quartermain and McEwen (1970); 23. Quartermain eral. (1%5); 24. Squire and Barondes (1972); 25. Taber and Banuazizi (1966) 26. Weissman (1%7); 27. Zinkin er al. (1976). “High punishment” and “low punishment” refer to levels of footshock during training; it will be Seen that high footshock reduces the duration of susceptibility but extends that of survival. Flurothyl, as a convulsant ether, is considered separately from anesthetics. Fuller information on the chick is given in Table 111.

342

R . J . ANDREW

under challenge, and can be maintained, with some danger of circularity of argument, only by assuming that unusually long susceptibility times either represent secondary effects of ECS or have some other special explanation. There is in fact good evidence that considerable extension of susceptibility can result from manipulations such as deprivation of paradoxical sleep or sustained inhibition of protein synthesis (Table I), and that susceptibility is sustained only until a little after the end of the resulting special state (Fishbein et al., 1971; Flood et al., 1977); however, whatever the nature of this state, it seems unlikely that a trace could be sustained continuously for many hours or even days by neural activity alone. One explanation which avoids this problem is that of “reminder” or “reactivation” effects, which are discussed later: briefly, by presenting stimuli associated with training, the trace set up at training can be made once again vulnerable to amnestic agents, which would otherwise be quite ineffective. Since procedures such as handling are very likely to occur both at training and at any subsequent manipulation (such as administration of ECS) any aberrantly long period of susceptibility might be argued to be explicable in this way. Two remaining groups of amnestic agents, anesthetics and protein synthesis inhibitors, have been held to define two further phases of memory formation (Booth, 1970). A variety of anesthetics have yielded rather similar values for duration of susceptibility, between 10 and 30 min, although here too there are exceptional much larger values (Table I). It seems very likely that there is a real difference between these agents and ECS. It is less certain that any difference has as yet been established between anesthetics and protein synthesis inhibitors. The very extended periods of susceptibility to puromycin applied to the cortex (to 60 days: Flexner et a l . , 1967) are probably best considered entirely separately. Puromycin is known to cause potent central changes such as the release of abnormal peptides, in addition to inhibition of protein synthesis (review, Cohen, 1970). Deutsch (1971), using cholinergic agonists and antagonists, has demonstrated systematic changes in susceptibility (and retention) over weeks after learning, so that much longer term changes than those considered in this article may well be important; how far puromycin effects are of this type, rather than depending on reminder or similar effects, remains to be seen. Duration of survival offers another means of distinguishing different groups of amnestic agents (Table I); for obvious reasons, there is little or no such information for anesthetics. Memory often survives ECS for up to l hr. Protein synthesis inhibitors, on the other hand, rather typically allow survival for 3-5 hr; puromycin on the cortex is again aberrant (Table I). It is worth noting that the hypothesis that all amnestic agents act on the same process of consolidation, which becomes more resistant to disruption as it proceeds, would predict that the most potent agents would have the longest periods of susceptibility and the shortest periods of survival. In fact, both seem to be longer in the case of inhibitors of protein synthesis than in that of ECS (Table I). The value of comparison is reduced here

343


by the wide variety of conditions under which the data were obtained; however, a similar relationship will be shown later to hold in the chick for a variety of agents applied under identical conditions. Estimates of duration of susceptibility after learning to agents that enhance learning suggest that this is typically possible for 15-30 min (Table 11). This agrees well with similar estimates for susceptibility to anesthetics and to protein synthesis inhibitors, and supports the hypothesis that a phase of lability of the trace is replaced by a more permanent state, perhaps half an hour after learning. Estimates of susceptibility to enhancing agents suggest a rather similar course of events after reminder (Table 11). The same agents oppose amnesia due to ECS and to protein synthesis inhibitors: here susceptibility tends to be for longer periods (e.g., 1-3 hr, Table 11). If genuine, this difference may be compared to the extension of susceptibility to ECS during the period of action of anisomycin which has already been noted; unlike the latter, it cannot be due to synergism between two agents with basically TABLE I1 OF SUSCEPTIEII.ITY .TO ENHANCING AGENTS"~' DURATION

Agent

Animal

Reference

Mouse

6 2 13 3 12 9, 1 1

Measure of enhancement

Not Susceptible susceptible

I . After learning

Strychnine Amphetamine Vasopressin Strychnine

Flurothyl Pentylentetrazol Physostigmine Corticosteroids ACTH. norepinephrine Brain stimulation 2. After reminder Brain stimulation Strychnine

7 8

2 hr Opposition to ECS Opposition to CXM 3 hr Opposition to ECS I hr Increased use of redundant cues 0 I hr Improved learning 30 min Improved learning 4-16 min Improved learning 15 min Improved learning 15-25 min Improved learning Improved learning 150 min 0 improved learning

Rat

5

Improved learning

30min

60min

Rat Rat

5 9

Improved learning Improved learning

30min 15 min

60min 30min

Rat Mouse Rat Chick Mouse Mouse Mouse Rat

4

10 1

3 hr

6 hr

2 hr

30 min 210 min 2 hr

"The latest times at which there was susceptibility to enhancement are given, together with the first at which there was not. The studies considered here were chosen because they gave relatively clear timings. They were: 1 . Alpern and Mariott (1973); 2. Barondes and Cohen (1968); 3. Brennan and Gordon (1977); 4. Cherkin er al. (1975); 5 . Devietti ef a/. (1977); 6. Duncan and Hunt (1972); 7. Flood et al. (1978); 8. Gold and van Buskirk (1976);9. Gordon(1977); 10. KrivanekandMcGaugh(1968); 1 I . McGaugh(l966); 12. McGaughandKrivanek ( 1970); 13. Pfeifer and Bookin ( 1978). 'Brain stimulation was in the midbrain reticular formation.

344

R . J . ANDREW

similar effects. It suggests instead an unusual persistence of a labile phase from which transition to a more permanent state remains possible. The chick data, which will be presented later, also indicate a transition to a more permanent state (which in this case can be accurately timed) at about 30 min, with another important transition, this time gradual, over 40-90 min. Indeed, it could be argued that in this respect at least, consistency between studies done in different species and under different conditions is at least as obvious as the variability, which is undoubtedly also present. DISRUPTION OF CONSOLIDATION OR OF RETRIEVAL? B. AMNESIA: There has been some confusion of terms in this controversy, which remains an active one. Interference with retrieval has sometimes been taken to mean disturbance of mechanisms responsible for retrieval, and sometimes interference with the establishment of stored information allowing the retrieval of a particular trace (see Spear, 1973, who distinguishes ‘‘retrieval processes” and the “effectiveness of retrieval”). Here we will be concerned only with the second (which might very well be a consequence of the first, induced at an appropriate time during memory formation). It should be noted that where clear gradients of susceptibility subsequent to learning have been demonstrated, amnesia cannot be due to a disturbance of retrieval mechanisms, which clearly continue to be effective at test despite the administration of the agent. Consolidation is sometimes held to have occurred once the transition from the (hypothetical) initial phase based on neural activity has occurred (e.g., Lewis et al., 1969). Alternatively, it may be used of all phases up to the final transition to “permanent” memory (e.g., Cherkin, 1969, 1972). I have used the term in this second sense. The main lines of evidence whose interpretation is in dispute are recovery from amnesia, and the reappearance of susceptibilityto amnestic agents after ‘‘reminder” of training. Recovery suggests that a trace may be unavailable without being lost. A subsidiary dispute centers around the significance of failure to demonstrate recovery, since it is always possible to argue that another approach might have produced evidence of some retention despite amnesia. Gold (Gold and King, 1974; Gold et af., 1973a) has argued that the demonstration of recovery and of reminder commonly requires the provision of further information in a form that amounts to retraining. This is certainly often tme of reminder procedures, while even spontaneous recovery commonly is demonstrated after repeated testing. Gold and other theorists (e.g., Cherkin, 1969; Mah and Albert, 1973), who argue that amnestic agents interfere with consolidation, explain evidence of some survival of memory after apparently complete amnesia as due to “weak” or “subthreshold ’ ’ traces. Miller and Springer (1974) rightly emphasize that the strength of a trace is only


345

apparently a simple concept: it might involve more information, greater redundancy of the same information, or increased availability of information. It seems likely that, when pressed to a conclusion, the distinction between effects on consolidation and retrieval has meaning only if a memory trace depends on information held in two different types of store: one representing the main body of information, and the other holding information necessary for the retrieval of the main trace. Such a distinction cannot be justified by the available animal evidence, although Weiskrantz ( 1966) has argued strongly for defects of retrieval information in human amnesia; it does provide a framework within which the processing and retrieval of information can be discussed more clearly. Lewis (1976) has emphasized the probable importance of an early phase of memory in which such processing occurs, and has argued (Lewis er ul., 1969) that the reason why familiarization with the training apparatus markedly attenuates the effectiveness of ECS given just after training is that such familiarization greatly abbreviates the processing needed before an organized trace can be stored. Another phenomenon, which is commonly taken to show that amnestic agents can act on availability for retrieval (i.e., on the storage of information for use in retrieval) is that of “reminder” or “reactivation.” Many studies have shown that the presentation of the reinforcer used in training (e.g., footshock, Springer and Miller, 1972), or conditioned stimuli (e.g., tone, Misanin ef ul., 1968) or specific features of the training apparatus or problem (Bregman et d.,1976; Meyer, 1972) may render a memory once again susceptible to amnestic agents (ECS in the examples previously given), even many hours or days after learning. Reminder may also allow enhancement (preceding and Table 11). Amnesia following reactivation, coupled with the application of an amnestic agent, is commonly interpreted as due to a disruption of subsequent retrieval. It does seem most likely that it is retrieval information that is affected, but vulnerability of the main trace cannot be excluded, until the phenomenon is much better understood.

c.

SEQUENTIAL

DEPENDENCE OF PHASES

OF

MEMORY

If, as seems probable, consolidation is divisible into two or more phases, dependent on differing neuronal states (and so sensitive to different amnestic agents), then the simplest way in which they might be related is that of strict sequential dependence. This would mean that each phase was dependent on the previous one for its formation, and could not be set up from any other source. Such phases could well be successive states of the same populations of neurons, with each state providing conditions necessary for the initiation of the next; they need not (although they could) represent functionally different stores, as far as their role in the handling and accessibility of information.

346

R . J . ANDREW

If the whole of a phase were sensitive to a particular amnestic agent, then survival in the presence of that agent would be likely to be shorter than susceptibility to it (Fig. 1A and B). On the whole (Table I) reported survival times are longer than reported duration of susceptibility; this is also true for the chick over a wider range of agents (see following). This can be accommodated without giving up serial dependency, either by extending the overlap between phases until the first phase ends after the end of the second phase (Fig. lC), or by confining sensitivity to the beginning of each phase (Gibbs and Ng, 1977; Fig. 1D).The latter alternative is the only one adequately to explain the data for the chick; it also agrees with the data already presented. However, it remains perfectly possible to argue that memory formation may involve functionally different stores which operate in parallel. Kesner (1973) has argued for a specific model of which this is true. An initial store, which depends

FIG.1. A number of ways are shown in which duration of susceptibility to a particular agent might be greater than (A and B), less than (C and D), or equal and coupled to (El and &) the duration of survival in the presence of the agent. The period for which the trace is sensitive to the agent is shown by hatching; in A-C, it is assumed that the whole of one phase is sensitive, as might be the case if the agent affected the process by which the trace was held, while in D and E, only a period of formation is sensitive. The duration of susceptibility is shown as slightly shorter than the true period of sensitivity, in order to allow for a delay between administration of the agent and the beginning of effective central action. In general, where the whole of each stage is sensitive (A-C), survival times should be longer than susceptibility times. This is not true of the arrangement shown in C, which is, however, an unlikely one. When only the initial part of each phase is sensitive (D) it is more likely that susceptibilitytimes will be longer. The special case shown in E is suggested when susceptibility and survival times are the same, and respond similarly to manipulation.


347

upon neural activity, establishes traces separately in short-term, and in long-term memory. Such establishment is believed to be very rapid, particularly in the case of short-term memory, so that ECS (which is assumed to affect only neural activity) will not prevent short-term memory from establishing, unless it is given as training ends. If short-term memory establishes but not long-term, then survival will be observed up to a point at which traces are normally lost from short-term memory. This argument depends on the assumption that ECS does not produce effects which persist for some time, and so might block some process necessary for subsequent passage from one phase of memory to the next. However, there is other evidence consistent with parallel processing: Kesner and Conner ( 1974) found that stimulation of the hippocampus immediately after training resulted in memory which appeared to decay over 3-4 min, whereas stimulation of the midbrain reticular formation produced immediate apparent amnesia, with evidence of memory appearing after a few minutes. They argue that in the first case long-term, and in the second short-term memory is disrupted, and that (if so) the two are clearly capable of independent establishment.

II. HUMANMEMORY One of the few safe comparisons that can be made between human and animal studies of memory is the susceptibility gradient of amnesia for events preceding concussion in man. Retrograde amnesia can extend up to 30 min before concussion (Weissman, 1967) which, perhaps by coincidence, agrees well with animal estimates for agents like anesthetics. There is little evidence from studies of verbal memory and little current support from theorists in this area for decay over time as a process of fundamental importance in normal human forgetting (e.g., Crowder, 1976). This is perhaps to be expected, since if reminder effects in animals d o represent a reactivation of a memory trace, almost all human verbal memory tasks are likely to involve repeated reactivation (and so interruption of any decay processes), as material is manipulated in memory. Equally important is the fact that so much closely comparable verbal material is held in human memory that ability accurately to retrieve is likely to be of crucial importance. Therefore, it is worth mentioning one phenomenon in verbal memory which does seem to have a predictable time course, which is measured in minutes, even if it cannot as yet be easily explained. When retention scores for verbal items are compared in paired-associate tests for items that produced a marked, or little or no galvanic skin response, scores are initially poor for the first and then improve, whereas the reverse is true for the latter (Walker, 1958; Kleinsmith and Kaplan,

348

R . J . ANDREW

1963). The crossover is at about 15 to 20 min after learning, and a stable state is reached by about 45 min. A variety of types of explanation have been suggested, of which perhaps the most interesting is that a marked GSR indicates high degree of processing (Kahneman, 1973); it is probable that correlation between serial position in the list and GSR is not important (Kleinsmith and Kaplan, 1974). For our purposes the chief point of importance is the suggestion of a shift from dominance of one type of store or process to another somewhere between 15 and 45 min after learning the list. There is good evidence for decay in initial very short-term stores: thus loss seems to be very marked over 1 sec or less for both visual stimuli (iconic store: Sperling, 1960, 1967) and auditory stimuli (echoic store: Darwin el al., 1972; Howell and Darwin, 1977). These times are perhaps comparable with susceptibility to ECS in animals that are very familiar with the apparatus in which learning has just occurred (see previously). If all visual information passes through a store or stores with such rapid decay, then it must be possible to establish a very complex trace very rapidly, since human memory for complex scenes is remarkably capacious and retentive (e.g., Standing et al., 1970) even in normal subjects who lack eidetic imagery (e.g., Haber and Haber, 1964). An alternative might be parallel processing of the sort suggested by Kesner on animal evidence (see previously). The next store or system following the very short-term stores that have just been considered seems to have limited capacity. Baddeley (Baddeley and Hitch, 1974; Baddeley er al., 1975) has suggested that this system may function as a working memory with a “central processor” of limited capacity, and associated buffer stores (e.g., for verbal material) which may have only brief retention in time. One way of combining such a system, for which there is much evidence, with the possibility of entry to permanent memory of a very detailed description of a briefly perceived but complex visual stimulus would clearly be parallel entry to working memory and to a long-term store. Working memory could then have the establishment of means of retrieval as one role.

III. MODELSOF MEMORY FORMATION It may be helpful at this point to summarize the main types of model that are serious contenders at present. A single trace with progressively increasing resistance to disruption does not seem usefully to cope with the evidence already reviewed. On the whole, there is little theoretical interest in such a model. One current model (that of Gold and McGaugh, 1975) has been termed “single-trace”; it is nevertheless a two-phase model. It assumes that after a trace is set up, it will decay and be lost, unless “nonspecific” (i.e,. not holding specific information about learning) modulating


349

processes cause its storage. Effectively, this amounts to a labile phase and a permanent phase of meory. The nonspecific modulating processes that, on this model, determine whether storage occurs themselves would often arise at the time of learning: thus they would be initiated by appropriate reinforcement at learning. The way is clearly open to postulate increased information content in these processes (e.g., how far was reinforcement contingent on a stimulus or response involved in learning), and thereby bring the model nearer to models involving parallel stores. However, as formulated, central agents such as hormones (see following), concomitants of increased arousal, and aftereffects of reinforcement are argued to be critical in modulation of storage. Models with two or more phases which are sequentially dependent have the advantage that they are reasonably straightforward (in theory) to test, as long as relatively precise timings can be assigned to each phase. In the next section, the model of this sort developed by Gibbs and Ng (1977) for the chick will be examined in more detail. Parallel stores have been postulated in order to account for temporary survival of memory after, or in the presence of, an amnestic agent (see preceding). It may well prove to be the case that a store whose contents do not automatically consolidate, and which operates in parallel to the stores leading to permanent memory, is responsible for holding information required only in the short term; however, once such a parallel store is postulated testable predictions about the duration of survival and susceptibility become extremely hard to frame. It is necessary to make a variety of firm assumptions (e.g., which store will provide information at retrieval, when will information pass from the parallel store to the stores leading to permanent memory, which store is affected at a particular time by a particular amnestic agent), none of which can be justified by experimental evidence. Better justification for considering a parallel store of some sort comes from human evidence for a working memory with limited capacity. If information used in retrieval is really established separately from the trace proper in animals, then this too would argue for a parallel memory system of some sort. The best strategy seems to be to push a strictly sequential multiphase model to its limits, giving as precise temporal and physiological properties as possible to each successive phase. Only if a real inadequacy can be demonstrated in such a model is it sensible to assume in addition a parallel store. Information processing is clearly important in the establishment of a trace: Lewis (1976) has argued that the duration of the early phase susceptible to ECS may be dependent on the extent to which this is required. It is therefore crucial to be able to define stages of memory formation from evidence based on the handling of information, and to compare this with evidence from amnestic agents. A beginning to such work has been made in the chick work to be reviewed later.

350

R. I . ANDREW

Iv.

PREVIOUS STUDIES OF

MEMORY, USING PECKING CHICK

IN THE

Cherkin and Lee-Teng (1 965) introduced inhibition of spontaneous pecking in the young domestic chick as a result of an,unpleasant taste associated with the pecking target, as a simple standard passive avoidance task. It has the advantage that it requires no preliminary training, so that there is no ambiguity as to the point in time at which relevant learning occurred. Cherkin ( 1 969) replaced the original ill-tasting substance (n-propanol) by a new one, methyl anthranilate, which then became standard. Gibbs (Gibbs and Barnett, 1976; review, Gibbs and Ng, 1977) changed the target from a microminiature lamp to a metal or colored bead, so that at retention test discrimination between a bead of the color used in avoidance training (“aversive”) and a bead of another color (“neutral”) could be tested. She also housed her chicks in pairs (Mark and Watts, 1971; Watts and Mark, 1971), a change which proved to have a marked effect on some time courses (Gibbs and Ng, 1977), and gave a pretraining session using metal beads (two trials with a small bead and one with a large one), so as to reduce the proportion of birds, whose training is disturbed by fear of the bead. The timing and character of pretraining sometimes has important effects on memory formation, and will be considered further in later sections. Cherkin (1970) has argued that amnesia for this task, when induced by flurothyl (a convulsant ether, given as the vapor), probably involves disruption of consolidation, on the grounds that there is no recovery of memory even after 9 days (and good retention in control trained animals). Flurothyl amnesia was also resistant to “reminder” by presentation of a target coated with a dilute solution of methyl anthranilate in water (Cherkin, 1972), which was not in itself capable of producing permanent inhibition of pecking. It is worth noting that this evidence of permanent and complete amnesia was obtained with chicks whose training was not preceded by any pretraining with similar targets. Different results might be obtained in chicks allowed “familarization ” (see previously) before training. Much shorter, and more clearly defined susceptibility after training was obtained for enhancement (Cherkin er a [ . , 1975). The effectiveness of training was reduced by using dilute methyl anthranilate; the enhancing agent, flurothyl, this time in very low concentration, was effective only to 16 min. Gibbs and Ng (1977) define three sequentially dependent phases of memory (“short-term memory,” “labile memory,” and “long-term memory”), on the basis of work by Gibbs and her colleagues (see Mark and Watts, 1971 ;Watts and Mark, 197 l), using three groups of amnestic agents, administered systematically or by freehand injection bilaterally into the forebrain. Although the present article will not consider the sort of physiological mechanisms that may be involved in such phases, it may be helpful to note that the first group (glutamate, 1

35 1


or 2 m M KCl) is argued to interfere with hyperpolarization, the second group (ouabain, ethacrynic acid) is sodium pump inhibitors, and the third group [anisomycin, cycloheximide (CXM), and a-arninoisobutyrate (AIB)] interferes with protein synthesis or with the uptake of amino acids necessary for synthesis. All of the agents were applied over a wide range of times relative to training, so as to establish a time course of susceptibility from a point sufficiently far before training as to render the agent ineffective, to a corresponding point after training. Since all agents were effective at some time after as well as before learning, direct effects on learning can be excluded as important in subsequent performance; since all agents ceased to be effective at relatively clearly defined times in relation to training, but well before retention tests, direct effects at test are also unlikely to be important. Duration of both susceptibility and survival is relatively standard for each group of agents (Table 111). This is particularly clear for inhibitors of protein synthesis (Group 111), where both anisomycin and cyclohexirnide gave similar TABLE Ill THREEGROUPS OF AMNESTIC AGENTSI N Agent I

I1

Ill

llla

Task'

LiCl Ouabain

B B B

Ouabain (high dose) Ouabain Ouabain Ethacrynic acid CXM CXM Anisomycin AIB

B AW PF B B PF B B

KCI

THE

CHICK""'

Susceptibility (-10)

(-10) (-30)

- 5 to +2.5 ( + 5 ) - 5 to ?+2.5 (+5) - 1 5 to + 5 ( + l o )

+

(+ 10) further loss

?

+ 10

to +30 ( + 30)

-5 (I - 10"

(-15) (-45) (-45) (-10)

Survival

- 5 t 0 +5(+10) -30 to +20 (+30, ?45) - 10'' -30 to +20 (+30,?45) - 5 to +2.5/5 ( + l o )

O? +5 10/15,

+ 10" + 10" + 10 +30

+60" +30 +30

(+5)

(+ 15) (

+60190)

( + 120)

(+60) ( + 60/90)

"The data are taken from Gibbs and Ng (1977). and are for chicks of mixed sex. housed in pairs (and so not in an altered physiological state due to isolation stress), and untreated with hormones. The doses for which data are shown are 20 pl 2 mM KCI, 20 p1 154 mM LiCI, 0.4 pg ouabain, 0.6 p g ouabain (high dose), 1 .O pg ethacrynic acid, 20 pg cycloheximide (CXM), 20 p g anisomycin, 20 pl 250 m M a-aminoisobutyrate (AIB). All were given bilaterally intracranially. "Times before training are shown as negative. Limiting times at which the agent was no longer effective, or loss was complete are shown in parentheses. "B, Standard bead with methyl anthranilate task (test); AW, aversive wheat task learn to avoid aversive tasting red wheat in 30 sec exposure; PF, pebble floor: learn to discriminate food grain from stuck down pebbles in C 5 min exposure. Measured from beginning of task. 'Measured from end of task.

'

352

R.

J . ANDREW

values, which in the case of cycloheximide varied little over a wide range of doses (20-300 pg: Watts and Marks, 1971; Gibbs and Ng, 1977). Further, AIB (Gibbs and Ng, 1977) and L-proline (Gibbs et al., 1977), which are believed to interfere with specific protein synthesis by a different route, namely, by competing for transport with amino acids normally used in synthesis, also yield similar survival times. Their periods of susceptibility are the same as those of Group I (glutamate, KCl), which Gibbs and Ng (1977) explain by postulating that amino acids needed for subsequent synthesis are taken up during the phase of formation defined by Group 1 agents. The two Group I1 agents, ouabain and ethacrynic acid, also yield almost coincident estimates of susceptibility and survival, although here there is some hint that survival times are somewhat sensitive to concentration of ouabain (Table 111). However, there is no suggestion of overlap with Group I11 times. Group I shows rather more variation in survival time, since 2 mM KCl yields either no survival or survival over 1 or 2 min, while LiCl allows some survival for at least 5 min. Times for Group I and Group I1 are sufficiently close (particularly considering that the resolution interval is in general itself 5 min) to suggest that the two groups might perhaps be acting on the same phase of memory but by slightly different routes. However, the most obvious possibility, namely, that Group I has a longer latency, can be excluded since, as Gibbs and Ng (1977) point out, they have a very brief duration of action as estimated from the time course of susceptibility before training. It thus seems very probable that the two groups of agents act on different phases of memory. A striking feature of the data is that for each group of agents (with the possible exception of Group I) duration of survival consistently exceeds that of susceptibility. This can be explained, as already noted (Fig. ID), with sequentially dependent phases, if amnestic agents act only at the beginning of each phase, presumably during its formation (Gibbs and Ng, 1977; Fig. 3A). However, this hypothesis leaves open the physiological basis for that part of each phase that is not sensitive, and thereby weakens the argument that the trace itself is represented, at least at the beginning of each phase, by a neuronal state sensitive to one of the three groups of amnestic agents. Instead, it could be that mechanisms involved in the establishment of each phase (e.g., in transfer of information from one store to another) are sensitive. The sequential dependence of successive phases would remain the same in both cases. V.

HORMONES A N D OTHER ENHANCING AGENTS IN OPPoSITION TO AMNESTIC AGENTS

THE

CHICK:

For some time (Murphy and Miller, 1955; De Wied, 1964) hormones such as ACTH have been known to affect the acquisition and extinction of avoidance tasks. Later work showed that the effects are not specific to avoidance training: they can be obtained with either food or access to a sexual partner as reward


353

(Bohus er al., 1977). Recent, not necessarily contradictory interpretations of the effects of MSH, and ACTH or ACTH analogs have included “improvement of selective attention” (Sandman and Kastin, 1977) and improvement of retrieval andlor consolidation processes (van Wimersma Greidanus and de Wied, 1976; van Wimersma Greidanus er al., 1978). Gold and Van Buskirk (1976) showed that epinephrine and ACTH apparently could promote consolidation when given immediately after learning. In the case of steroid hormones, Flood ef af. (1978) have demonstrated enhancement of retention by corticosteroids given after training in poorly trained mice, and Gold and McGaugh (1 975) suggested more generally that hormones such as ACTH, vasopressin, and epinephrine might promote storage. Comparable effects in the chick are suggested by the marked extension of time courses of survival of amnestic agents when chicks were stressed by isolation, rather than being housed in pairs (Gibbs and Ng, 1977, and following). Here, I will be concerned chiefly with effects of testosterone on memory formation, although it should be noted that this is only one (albeit the most effective, except for estradiol, see Section V , A) of the steroid hormones that are effective in this way. Enhancement of memory formation can be demonstrated in the chick both by opposition to amnestic agents and by effects on normal memory formation; in this section, I will consider only the first type of effect. Testosterone (given as the free steroid, in dimethylacetamide, typically 10 pg/40 gm male chick) extends both susceptibility to and survival under ouabain. In our hands (Andrew and Stephenson, 1981) the two times are the same, both in control and in testosterone-treated chicks: in the first the times are greater than 5 and less than 10 min, and in the second greater than 15 and less than 20 min. There is some discrepancy with the times already noted for controls in another laboratory (Gibbs and Ng, 1977), of 5-10 min for susceptibility and greater than 10 min for survival, and the reason for this is not yet known.’ However, it is clear that survival and susceptibility are coupled in their response to testosterone, even if this coupling may be relaxed under other circumstances. If ouabain is acting directly on the trace, then such coupling of the durations of susceptibility and survival suggests that the ouabain-sensitive period is very brief, and is postponed by testosterone (Fig. 1E). An alternative possibility, which would be consistent with the data, is that it is not the trace itself, but a mechanism responsible for transfer of the trace from one store to another, which is sensitive to ouabain. Testosterone also extends survival in the presence of CXM (Gibbs er al., 1981). The survival time is determined by the time, not from training, but from injection; testosterone remains effective for between 4.5 and 5.5 hr according to ‘Slight differences in overall timing are not unexpected in a measure sensitive to hormonal state. It may be that survival is slightly longer than susceptibility in all three cases: it would be expected to be longer by the time required for ouabain to begin to act (Fig. l ) , for example. Given a resolution interval of 5 min a slight difference might be revealed only when a test fell at a crucial point.

354

R . J . ANDREW

dose. A similar estimate of duration of effectiveness is obtained from tests using enhancement of normal learning, such as are described in Section V,A. The processes underlying the loss of effectiveness are discussed elsewhere (Gibbs et al., 1981); here, it is important only because it allows the demonstration of an unusual state, in which the trace surviving the inhibition of protein synthesis can be sustained or held available for many hours, and yet is not permanently stored. Thus, a second injection of testosterone prolongs the lifetime of the trace, as long as it is given before the end of effectiveness of the first. A.

THEENHANCEMENT OF NORMAL MEMORY IN THE CHICK

Messent (1973) observed that, when first exposure to, and pecks at a target (a colored bead mounted on a wire) occurred after the administration of testosterone, such pretraining interfered with avoidance training, using a similar target coated with methyl anthranilate and given immediately afterward; without pretraining testosterone had no effect on behavior. Control animals never showed any interference with avoidance training. Andrew et al. (1981) confirmed the effect, and showed that interference occurred only when a bead identical in appearance with that used at training, was also used in pretraining. Testosterone was found to be effective only if given within a certain minimum time of pretraining. Its timing in relation to training, on the other hand, was not important: if it was not given in time to affect the consolidation of pretraining, then its presence at training (or testing) did not change behavior. Although I will deal here only with testosterone, it should be noted that it has been possible using this test to construct dosage curves for a wide range of of steroids (Rainey, unpublished): the two most effective proved to be testosterone and estradiol (threshold dosages la0 and 10 nglchick, respectively). The marked specifity of the interference between traces of training and pretraining suggested that this test might offer a way of studying the course of consolidation under conditions more normal than in the presence of amnestic agents, It also promised to allow the study of transfer of information, rather than changes in the physiological state of a trace. The basic procedure was to vary systematically the interval between pretraining and training. A somewhat similar approach has been taken by Spear and his colleagues (Spear et al., 1972; Spear, 1973), using interference between initial passive avoidance training and subsequent active avoidance training. If the two training trials are separated only by 1 min, interference with the second task is marked; with a longer interval ( 1 hr) interference is only slight. However, even with such longer intervals, there may be an effect on the long-term survival or availability of learning based on the second trial. With 1 hr between the training trials, active avoidance is remembered well at a test 1 hr subsequently, but shows considerable interference from passive avoidance 24 hr later (Gordon and Spear, 1973). In the chick experiments (Clifton et al., 1981) testosterone was given before


355

pretraining, since it was essential that it should have begun to act at the time of pretraining, if short intervals between pretraining and training were to be studied. Birds with differing intervals between pretraining and training fell into three groupings. Over the time range 10 sec to 2 min, pretraining dominated, in that birds (when tested 3 hr after training) tended to peck aversive type beads as much as neutral beads. From 3 to 25 min, training dominated at test and the aversive bead was not pecked, while at times of 30 min or greater, pretraining again dominated. Control groups withheld pecks in consequence of training whatever the interval between pretraining and training. The range of 10 sec to 2 min is of particular interest, since it suggests that once testosterone has begun to act, it affects the ability of the pretraining trace in the first few seconds of its life to compete with the establishment of subsequent training trace. The reasons why there should be three periods in the formation of a trace under enhancement by testosterone in which its competitive ability should differ so much are still a matter for speculation. The most reasonable working hypothesis seems to be the following. The outcome of the interaction, which the data indicate must occur between traces relating to the same stimulus, is assumed to depend upon the relative stability of the two traces. The first phase would be explained if information initially were to be held in a very short-term store, in which it decays very rapidly (as in the case of the human iconic or echoic stores), and from which it enters a store, within which traces are given increased stability by testosterone. As a result, the training trace, with only a brief time in which to enter, would be at a double disadvantage. Clearly, if this is so, loss of the training trace should be immediate with no period of survival: this is confirmed by the absence of any measurable inhibition of pecking 2 rnin after training (which is as close as testing can reasonably be taken without being greatly affected by direct aftereffects of training such as lingering taste in the mouth). The transition at between 2 and 3 rnin corresponds roughly but not perfectly with the end of susceptibility to Group I amnestic agents (between 2.5 and 5 min); it may be that these agents act on the store that has just been postulated (store 2 in Fig. 2B). The training trace may be given advantage during the second period in the life of the pretraining trace, because transfer from store 1 to the next store is a one-way traffic. As a result, the entering trace is likely to be at an advantage, since its basis remains secure during interaction. The third transition may indicate the point at which the pretraining trace changes state and becomes permanent, in the sense of becoming capable of resisting subsequent interaction with the training trace. This is not true of control birds, and it must therefore be assumed that the effects of testosterone during consolidation in some way give continuing advantage to the pretraining trace, once it passes into a permanent state. There are at least two points in time at which such a change in state might

356

R. J . ANDREW I

I

I

I

I

I

60

30rnin STM

A

I11 ,;'/L,

=- _J _L

- -/.;'*/:;'

r..

IIt

LM

,,

:'- -- -

I

I

I

I

10

20

30

40

,

50

LTM

60

FIG. 2. The sequentially dependent stages of consolidation postulated by Gibbs-Ng model. ES, Stage sensitive to ECS; STM,short-term memory; LM, labile memory; LTM, long-term memory. The periods of establishment of each phase, when the trace is sensitive to a particular group of amnestic agents, are indicated by hatching. The agents effective in each case are shown by Roman numerals: I, Group I (agents such as 2 mM KCI);11, Group 11 (ouabain and ethacrynic acid); 111, Group I11 (protein synthesis inhibitors). (B) Part B incorporates the sharply defined transition suggested by evidence from trace interaction experiments at 2/3 and 25/30 min. Points of sensitivity to amnestic agents are shown in the same way as in A. Since in the case of the transition between established short-term memory (3) and the next stage, it is possible that it is the transfer mechanism that is sensitive to ouabain; this is indicated by hatching in the m o w . The same convention is used for the transfer to long-term memory, which is shown as sensitive to sotalol (S). The stages of memory are numbered in order to provide a simple means of reference, without any undesired implications; they are equivalent to the following stages of A: 1, ES; 2, formation of STM, here an entirely separate stage; 3, established STM; 4, formation of LM, if this is present as a sensitive period;5 , established LM; 6, LTM. LTM is not shown as divided, although processes of structural change presumably continue through this time, and there is probably a shift of retrieval to LTM as stage 5 ends. A period of preparation for stage 6 is tentatively indicated as the place of action of protein synthesis inhibitors (111). The main sites of action of testosterone are indicated by T. They include the stabilization of traces in stage 2, the postponement in time of the transition from stage 3 to the next stage, the prolongation of stage 5 (when stage 6 is blocked), and late effects on the consolidation of the trace in stage 6. This last effect (measurable as increased effectiveness of the permanent trace in competition with subsequently established traces) can be obtained after the transition at 25/30 min. It may be due to an effect on stage 5 , if the contents of stage 5 continue to transfer to, or interact with, stage 6; alternatively, it may represent a direct effect on stage 6.


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occur. The most obvious is a little less than 30 min after the setting up of the pretraining trace. This corresponds closely with a very sharp end of susceptibility to sotalol (a P-adrenergic antagonist) which has its maximum effect in the chick 25 min after avoidance training, falling to little or no effect at 30 min (Stephenson and Andrew, in preparation). However, it is also possible that the crucial change in state occurs at a later gradual transition to permanent memory. It is necessary to assume in addition that, as long as they do not interact in the earliest phases of consolidation of the pretraining trace, the two traces consolidate independently until the training trace reaches this final transition, and that the training trace (presumably because associated with reinforcement) consolidates more effectively. It might then be that when 30 or more min separate pretraining and training the training trace has already become more stable than the pretraining trace when interaction begins (P. Clifton, personal communication). It is not at present possible to resolve this question; on balance the first explanation seems the more likely, since it is not clear that the second would be expected to yield the same crossover point in competitive advantage in all of a large group of chicks as would be needed to generate the sharp transition observed. The independent evidence of a sharp transition between 25 and 30 rnin also favors the first alternative. The technique of opposing two traces has provided further evidence about the handling of information in the successive phases of memory formation. Store 1 proves to have unusual properties (Andrew et al., 1981). If a blue bead is used in pretraining, in chicks that have been treated with testosterone, then it normally does not have any effect on subsequent avoidance training using a red bead. However, when the interval between pretraining and training is 1 or 2 min, there is full interference despite the difference in color; the transition to the normal lack of interference is sharp, occurring as the interval between pretraining and training is lengthened to 2-3 min (Clifton, unpublished). This result agrees well with the hypothesis that when the pretraining trace is still in store 1, the training trace is not allowed to establish at all. It also suggests that information handling in this phase of memory has a limited processing capacity, much as in human working memory.

B. PHASESOF MEMORYI N

THE

CHICK

It is now possible to pull together the various lines of evidence that help to define phases of memory in the chick. The main features of the Gibbs-Ng model (Fig. 2A) are confirmed by the new evidence which has been reviewed here. It will be easiest to consider the changes and extensions of the model that have been postulated here by taking each stage in turn (Fig. 2B). Little is known of the first stage, which is included because of evidence

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(Lee-Teng and Sherman, 1966; Lee-Teng, 1970) that susceptibility to ECS extends in the chick to about 30 sec. Gibbs and Ng (1977) also found it necessary to postulate a stage prior to that sensitive to Group I amnestic age-nts in order to explain temporary survival of such agents (e.g., Benowitz and Speny, 1973). On the Gibbs-Ng model stage 2 is the period of formation of short-term memory (sensitive to Group I agents). Its end coincides quite well with that of the period in which the resident pretraining trace' is able, when stabilized by testosterone, to exclude the training trace; it seems best therefore to distinguish it as a period spent in a store with special functional properties. Stage 3 (established short-term memory on the Gibbs-Ng model) ends with a probably brief period of transfer or change of state (here indicated as 4); either a mechanism necessary for transfer or the trace itself as it establishes in the next phase is sensitive to Group LI agents during this period. Testosterone postpones the transfer or change of state. Stage 5 (established labile memory), it is here argued, is divided into two periods by a sharply timed transfer that introduces the trace into long-term memory (stage 6), but does not terminate stage 5. This transfer probably occurs a little less than 30 min after learning: it can be detected both as the point at which the trace becomes more resistant to displacement or change, and as the time immediately after which sensitivity to the &antagonist sotalol suddenly ceases. Like the transition between stages 2 and 3, its timing is not affected by testosterone. The end of stage 5 is probably revealed by the progressive loss of the pace, which can be observed when the establishment of long-term memory is blocked. In chicks unaffected by testosterone or other hormones, all agents bringing about such blockage (CXM,anisomycin, AIB, Gibbs and Ng, 1977; sotalol, Stephenson, unpublished) yield roughly similar survival times, with progressive loss between 30 and 60 to 90 min. The timing of the end of stage 5 is affected by testosterone little, if at all, under one set of circumstances: when establishment of the training trace in long-term memory is prevented by the prior establishment there of the pretraining trace, rendered more effective by testosterone, the training trace once again shows progressive loss between 30 and 60 to 90 min (Clifton et al., 1981). One special feature of this last case deserves emphasis. It will be remembered that it requires that pretraining (in the presence of testosterone) and training be separated by 30 min or more. Training results in a trace reaching and entering state 5 ; with an appropriate interval between pretraining and training the pretraining trace is then still present in that stage (as well as in long-term memory, stage 6), and is presumably displaced or reshaped by the training trace. From then until the end of the life of the training trace in stage 5 , it is evidently retrieved at test in preference to the pretraining trace, which is simultaneouslyresident in long-term


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memory. The simultaneous presence of two contradictory traces in different stages of memory is of particular interest in that it shows that parallel storage without final permanent consolidation is possible, albeit so far demonstrated only under rather special circumstances. The timing of the end of stage 5 is affected by testosterone under one set of conditions, namely, when the establishment of long-term memory is blocked by Group I11 agents. In the presence of such a blockage, testosterone extends survival of the trace, presumably in stage 5 , for as long as it (testosterone) remains effective. Why this might be is considered in Section V,C.

C. TESTOSTERONE A N D RETRIEVALPROCESSES Testosterone has been shown to affect almost every stage of memory formation; it is not obvious what sort of direct action on the neuronal basis of the trace could explain this, and it seems worthwhile to examine alternative explanations. The effects of testosterone are broadly comparable in each stage that is affected: stabilization of the trace against interference in stage 2, extension of its life in stage 3, and under some circumstances at least in stage 5 also, and finally increased effectiveness in competition after permanent storage in long-term memory. Despite these extensive changes the times of establishment of stage 3 from stage 2, and of stage 6 from stage 5 , remain unchanged. This is consistent with an action of testosterone not directly on the trace itself, but indirectly through a mechanism that can intervene in each successive stage of consolidation. The effects of testosterone upon attention, as shown in search tests and tests of distractibility (Andrew and Rogers, 1972; Andrew, 1972, 1976), also have some basic features in common with the effects just discussed. Chicks treated with testosterone are much more likely to sustain attention on a particular type of stimulus during search, and are more likely to return to a previous point of attention after distraction. Both types of effect can most readily be explained by increased stability of information held in a short-term store. The increased stability of the consolidating trace in stage 2 is a comparable effect, operating over a similar time scale. The most important difference is that in search and distraction tests, the chick is commonly responding to familiar stimuli (e.g., familiar types of food, position and appearance of the food dish in a familiar runway). If in these tests also, testosterone acts by stabilizing a memory trace, then this trace is likely usually to be one retrieved from permanent memory. This difference, however, may not be a crucial one. The reminiscence experiments, which were discussed earlier, provide strong evidence that once retrieved, traces (or the information used in the retrieval of traces) are subject to the same enhancing (and disrupting) agents as during consolidation. It is not unreasonable

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therefore to suppose that testosterone might sustain retrieved traces, as well as ones consolidating for the first time; how this might occur in either instance is of course the basic issue to be resolved. The only mechanisms that are known to have access to all (or almost all2) phases of consolidation are those concerned with retrieval. Too little is known of the processes of retrieval to allow any unambiguous prediction as to the consequences of such access: it might not affect the character or stability of the trace at all, or it might weaken it rather than stabilize it. The hypothesis set out below begins with the premise that retrieval mechanisms can hold a consolidating trace stable. Its main attraction is that it provides a theoretical framework within which a variety of different effects can be explained, and from which a wide range of testable predictions about the nature of both consolidation and retrieval can be made. It must initially be assumed that when a trace is retrieved, so that its information content is held directly and readily accessible, this involves sustained access to the store in which the trace is then held; this would be long-term memory, except in the case of a consolidating trace. The alternative, here assumed not to be true, is that access is brief, and results in all of the information being duplicated in another bulk store, in which it remains while it is held accessible; in the meantime the trace proper persists in its original state. Testosterone is assumed to increase the time for which a trace is held available, once retrieved. An effect of this sort on traces retrieved from long-term memory provides the most satisfactory explanation for the changes produced by testosterone in search tests and tests of distractibility (see preceding). In the case of a trace based on a salient experience, such as the experiences with beads dealt with here, it seems reasonable to suppose that for some time after the experience, the consolidating trace would be held readily available. It is here assumed that this involves the same mechanisms as are responsible for retrieval from longterm memory, and that testosterone has the same effect of prolonging the time for which the trace is sustained in an available state. Those events that can be precisely timed during consolidation fall into two categories: those whose timing is changed by testosterone, and those that are unaffected by testosterone. The latter (the transitions at 2/3, and at 25/30 min) show that the overall timing of consolidation is unaffected by changes in the mechanism on which testosterone acts. The challenge for the present hypothesis is thus to explain why two other timings should be markedly changed by testosterone. It is important to remember *In both chick (Cherkin, 1971) and mouse (Irwin el al., 1968) there may be brief periods during consolidation, when a trace appears to be difficult to retrieve. Further study of the timing of such periods may shed light on the way in which retrieval mechanisms establish contact with consolidating traces.


36 1

that the evidence for survival in a particular phase of consolidation is usually really evidence that retrieval takes place from that phase. This is particularly clear for survival in stage 5 , where it has been shown that retrieval continues for some time to be from stage 5 , even though a comparable trace has been already established in stage 6. Here, then, it seems reasonable to suppose that “the end of stage 5” actually represents the time at which retrieval mechanisms shift from stage 5 to 6. Indefinite extension of stage 5 (or retrieval from stage 5 ) due to testosterone occurs only if the establishment of long-term memory is blocked: this suggests that the shift does not occur if no trace is available to the retrieval mechanism in the next stage. This is perhaps not unexpected, but if it can be confirmed, it is the first direct evidence that bears on the way in which retrieval mechanisms may determine in which store to search. The retrieval mechanisms then must be assumed to sustain the trace in stage 5 for as long as testosterone continues to affect them; in the absence of testosterone or a similar agent, access to the trace by the retrieval mechanisms is apparently no longer stable enough, so long after learning, to allow the trace to be sustained. The extension of stage 3 by testosterone is more difficult to explain on the present hypothesis. It suggests some special intervention of retrieval mechanisms in a particular early stage of consolidation. The only obvious reason for this is the selection of those features of the trace that are subsequently to serve in its retrieval. Recently we have found that the duration of stage 3 does indeed coincide with the time for which reclassification of the properties of a stimulus, as coded in a trace, can occur (Clifton and Andrew, unpublished). Further study of the effects of testosterone on stage 3 should therefore provide one means of testing the present hypothesis. The final effect that must be considered here is the increased effectiveness of the fully consolidated pretraining trace in competition with subsequent training, which results when consolidation is affected by testosterone. Too little is known of the causes of this increase in effectiveness to say whether it can be explained by the present hypothesis (or some other one). Two main types of explanation are possible: changes in the stability of the trace, and changes in the way it is classified for retrieval, such that interaction with a subsequent trace relating to the same stimulus is made more likely. Further work should show which is correct, and it may then be possible to decide whether this effect too could be caused by a change in the role played by retrieval mechanisms during consolidation.

VI. CONCLUSION: GENERAL IMPLICATIONS The answers to some of the questions posed in the first section of this article are now somewhat clearer, at least for the chick. All of the new evidence is in

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agreement with the most important feature of the Gibbs-Ng model, namely, the sequential dependence of successive stages of consolidation. It now seems likely that at least one of the transitions (that between stages 2 and 3) involves a shift of the trace between stores that differ in their capacity to handle information. The way is now open to characterize other stages in the same way, and to begin comparison with work on human memory (e.g., comparison of stage 2 and human working memory). Some of the transitions are surprisingly sharply timed, suggesting that there may be points during consolidation when the relative timing of two or more events is crucial. The properties of transitions such as that at stage 4 suggest points of manipulation by mechanisms external to the stores in which the trace is held. Some features of a parallel store may also be present: thus stage 5 may hold information which is different from that held at the same time in stage 6, and which is not finally consolidated. The main value of the work on chicks lies in the detail and the preciseness of the temporal structure, which has been established for consolidation. It seems unlikely that consolidation in the chick (or birds in general) differs radically from consolidation in other vertebrates, and in particular in mammals. It is impossible at present to tell how much of the variability in times of survival of, and susceptibility to particular amnestic agents would disappear, if a systematic body of data were available for a particular strain of mouse or rat, studied in a standard physiological state. Certainly even the data reviewed earlier are at least compatible with consolidation processes organized as in the chick, but with timings varying between strains and with variables such as levels of circulating hormones. One feature that may be to some extent peculiar to the chick experiments is the lack of experience of the chicks: nothing in their brief past experience is likely to be closely comparable with any aspect of the bead presentations. It may be that this makes the process of organization and consolidation of the trace much clearer, and perhaps more protracted, since they are starting from scratch. The most fundamental questions raised by the chick data are those of the possible relations between memory and attention. The effects of testosterone on consolidation and on attention suggest, as a hypothesis that deserves further pursuit, the possibility that this and perhaps other hormones act on mechanisms that select, manipulate, and sustain information in short-term stores. Such a hypothesis is not entirely novel: current explanations of the effects of hormones on retention include effects on “selective attention” (Sandman and Kastin, 1977), and the promotion of retrieval, or retrieval and consolidation (Gold and McGaugh, 1975). These different approaches could be reconciled by effects on retrieval mechanisms such as have been suggested here for testosterone. This hypothesis depends on the assumption that the same mechanisms, which select and maintain information within stores, are crucial not only in retrieval but in


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consolidation and in attention. If this is true, then studies of the kind discussed here may eventually turn into studies of thinking in animals.

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McGaugh, J. L., and Gold, P. E. 1974. Conceptual and neurobiological issues in studies of treatments affecting memory storage. Psychol. Learn. Moriw. 8, 233-264. McGaugh, J. L., and Herz, M. J. 1972. “Memory Consolidation.” Albion, San Francisco. McGaugh, J. L., and Krivanek, J. 1970. Strychnine effects on discrimination learning in mice: Effects of dose and time of administration. Physiol. Behav. 5 , 1437-1442. McGaugh, J . L., and Landfield, P. W. 1970. Delayed development of amnesia following electroconvulsive shock. Physiol. Behav. 5 , 1109-1 113. Mah, C. J . , and Albert. D. J . 1973. Electroconvulsive shock-induced retrograde amnesia: An analysis of the variation in the length of the amnesia gradient. Behav. Biol. 9, 517-540. Mark, R. F., and Watts, M. E. 1971. Drug inhibition of memory formation in chickens. I. Long-term memory. Pror. R. Sor. London E 178, 439-454. Messent, P. R. 1973. Distractibility and persistence in chicks. Ph.D. Thesis, University of Sussex. Meyer, D. R . 1972. Access to engrams. Am. Psycho/. 27, 124-133. Miller, R. R., and Springer, A. D. 1971. Temporal course of amnesia in rats after electroconvulsive shock. Physiol. B e h v . 6, 229-233. Miller, R . R., and Springer, A. D. 1974. Implications of recovery from experimental amnesia. Psycho/. Rev. 81, 470-473. Misanin, J. R., Miller, R. R., and Lewis, D. J. 1968. Retrograde amnesia produced by electroconvulsive shock after reactivation of a consolidated memory trace. Sciend 160, 554-555. Murphy, J . V., and Miller, R. E. 1955. The effect of adrenocorticotrophic hormone (ACTH) on avoidance conditioning in the rat. J . Comp. Physiol. Psychol. 48, 47-49. Pearlman, C. A., Sharpless, S. K.,and Jarvik, M. E. 1961. Retrograde amnesia produced by anesthetic and convulsant agents. J . Comp. Phvsiol. Psyrhol. 54, 109-1 12. Pfeifer, W. D., and Bookin, H. B. 1978. Vasopressin antagonizes retrograde amnesia in rats following electroconvulsive shock. Pharmacol. Biochem. Behav. 9, 261-263. Quartermain, D., and McEwen, B. S. 1970. Temporal characteristics of amnesia induced by protein synthesis inhibitors: Determination by shock level. Nature (London) 228, 677-678. Quartermain, D., Paolino, R. M., and Miller, N. E. 1965. A brief temporal gradient of retrograde amnesia independent of situational change. Science 149, 11 16-1 118. Sandman, C. A., and Kastin, A. J. 1977. Pituitary peptide influences on attention and memory. In “Neurobiology of Sleep and Memory” (R.R. Drucker-Colin and J. L. McGaugh, eds.), pp. 347-360. Academic Press, New York. Spear, N. E. 1973. Retrieval of memory in animals. Psychol. Rev. 80, 163-194. Spear, N. E., Gordon, W. C., and Chiszar, D. A. 1972. Interaction between memories in the rat: Effect of degree of prior conflicting learning on forgetting after short intervals. J . Comp. Physiol. Psychol. 78, 47 1-477, Sperling, G . 1960. The information available in brief visual presentations. Psychol. Monogr. 74. Sperling, G . 1967. Successive approximations to a model for short-term memory. Acra Psychol. 27, 285-292. Springer, A. D., and Miller, R. R. 1972. Retrieval failure induced by electroconvulsive shock: Reversal with dissimilar training and recovery agents. Science 177, 628-630. Squire, L. R., and Barondes, S. H. 1972. Variable decay of memory and its recovery in cycloheximide-treated mice. Proc. Narl. Acad. Sci. U.S.A. 69, 1416-1470, Squire, L. R . , Kuczenski, R., and Barondes, S. H. 1974. Tyrosine hydroxylase inhibition by cycloheximide and anisomycin is not responsible for their amnesic effect. Brain Res. 82, 241-248. Standing, L., Conezio, J., and Haber, R. N. 1970. Perception and memory for pictures: Single-trial learning of 2560 visual stimuli. Psychol. Sci. 19, 73-74. Stephenson, R. M., and Andrew, R. I. 1981. Amnesia induced by specific fi-antagonists in the chick (in preparation).


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Index

A Adaptation among Phocidae and Oteriidae convergent evolution of social structures, 136-138 divergence in geographical distribution, 135-I36 divergence in rearing methods, 133-135 divergences in ways of life, 133 to predation, among Pinnipeds. 128-129 selective association effect and, 308-309 Aggressive behavior, male. hormonal control of, 33-37 Amnesia, memory phases and, 344-345 Anolis carolinensis

behavioral ecology of, 44-45 character displacement in, 48-51 dewlap as species-isolating mechanism, 45-48 behavioral repertoire of, 6-10 biological bases of species-typical behavior patterns in hormonal control of female sexual receptivity, 10-17 hormonal control of male aggressive and sexual behavior, 33-37 neuroendocrine control of male reproductive behavior and gonadotropin secretion, 37-44 sociosexual control of seasonal gonadal recrudescence, 25-33 stimulus control of male mounting behavior, 17-25 natural history of, 3-6 Anolis sagrei, character displacement in, 48-51 Anosmia, effect on suckling, 100-105 Appetitive behavior, ontogeny of, paradoxical reward effects and, 263-265

369

Arousal, development of vocalizations and, 205-208 Associations, selectivity of demonstrations of, 303-307 ingestion as determinant of, 302 interpretations of, 308-317 uniqueness of, 317-318 Aversion learning, see Ingestional aversion learning

B Behavioral context, development of vocalizations and, 202-205 Bird song, 143-144 geographical variation in, 159-160 microgeographical, 160-170 repertoires, 144-145 contribution to survival and reproduction, 146-159 Blocking effect, in ingestional aversion learning, 320-322

C Carnivora, development of vocal behavior and hearing in, 185-189 Cat, development of vocal behavior and hearing in, 185-187 Character displacement, in Anolis carolinensis and Anolis sagrei, 48-51 Chick, memory in normal, 354-357 phases of, 357-359 previous studies of, 350-352 testosterone and, 359-361 Chimpanzee, development of vocal behavior and hearing in, 195-196 Chiroptera, development of vocal behavior and hearing in, 183-185

370

INDEX

Common seal, social plasticity in, 125 Communication, see Bird song; Sound communication Competition, between males, bird song and, 148-154 Crocodilians, reproductive cycle of, 59-6 I

D Dewlap, as species-isolating mechanism, 45-48 Dialects, in bird songs, functions of, 168-170 Discrimination maternal, in ewes, 97 of sound, by infant mammals, 208-209 Dog. development of vocal behavior and hearing in, 187-189

E Elephant seal, social plasticity in, 125 Event covariation, selective association effect and, 313-314 Ewe, maternal behavior in, see Maternal behavior Extinction effects, paradoxical reward effect and magnitude of reward and, 243-249 overtraining and, 255-257 partial reinforcement and, 243-249

Hearing development of vocalizations and, 200-202 of infant mammals, 208-209 time courses of development of, 183 in Carnivora, 185-189 in Chiroptera, 183-185 in primates, 194-198 in rodents, 189-194 Hormonal control of maternal behavior, in primiparous ewes, 111-112 of postparturient maternal responsiveness, 84-87 of species-typical behavior female sexual receptivity, 10-17 male aggressive and sexual behavior, 33-37 Hormones induction of maternal behavior with, 79-80 in nulliparous ewes, I 1 1-1 12 manipulations of, effect on maternal behavior in ewe, 105-106 retrieval processes and, 352-354, 359-361 House mouse, development of vocal behavior and hearing in, 192-194 Human, development of vocal behavior and hearing in, 196-198

F

Felidae, development of vocal behavior and hearing in, 185-187 Frustration theory, as mechanism for paradoxical reward effects, 234-236

G Genetic isolation, microgeographic variation in bird songs and, 165-167 Geographical distribution, divergences among Phocidae- and Oteriidae in, 135-136 Gonadal recrudescence, sociosexual control of, 25-33 Gonadotropin secretion, neuroendocrine control of, 37-44 a e y seal, social plasticity in, 124-125 Guinea pig, development of vocal behavior and hearing in, 189-190

H Habitat, sex ratio and, among Pinnipeds, 123 Habituation, bird song repertoires and, 152-154

I Imitation, of bird songs extent and accuracy of, 160-161 site of, 161-165 Ingestional aversion learning, 276-278 associative-nonassociativecontroversy and, 278-279 aspects which cannot be attributed to sensitization effects of poisoning and, 282284 expectations based on associative interpretations, 279-282 role of neophobia and poison-enhanced neophobia in aversions, 284-292 complexity of ingestive sequence in, 292,303 conditioned aversions to nongustatory cues and, 300-302 nongustatory orosensory stimuli and, 300 odor-aversion learning and, 296-300 selective associations and, 302 taste-aversion learning and, 292-295 future directions in, 326-330

37 I

INDEX limitations on, 318-319 overshadowing, 3 19-320 proximal unconditioned stimulus preexposure, 324-326 relative validity of conditioned stimuli, 320-324 selectivity of associations in demonstrations of, 303-307 interpretations of, 308-317 uniqueness of, 317-318

L Learning aversive, ingestional, see Ingestional aversion learning paradoxical reward effects and, 236-237 behavioral process and, 237-238 species differences and, 239-242 systematic variation and, 238 Learning sets, selective association effect and, 309-313 Lizards, parthenogenetic, reproductive cycle of, 61-65

suckling behavior, 100-106 research prospects in, 113-1 15 Memory, 337-338 hormones and other enhancing agents and, 352-354 normal memory and, 354-357 phases of memory and, 357-359 testosterone and retrieval processes and, 359-361 human, 347-348 models of formation of, 348-349 phases in higher vertebrates, 338-339 amnesia and, 344-345 number of, 339-344 sequential dependence of, 345-347 previous studies of, 350-352 Mimicry, in bird songs, 155-158 Monogamy, among Rnnipeds, I3 I - 133 Mortality, sex ratio and, among Pinnipeds, 129-130 Mounting behavior, male, stimulus control of, 17-25 Mouse, development of vocal behavior and hearing in, 192-194

N M Magnitude of reward extinction effect, paradoxical reward effect and, 243-249 Mammals, sound communication in, see Sound communication Maternal behavior, 76-77 in inexperienced ewes, 108, 112-1 13 in parturition in primiparous and multiparous ewes, 108-1 1 1 role of hormones in primiparous ewes, 111-112 influence of endocrine state of ewe on, 77-79, 87-88 fading of postpartum maternal responsiveness in absence of neonate and, 83-87 induction of maternal behavior in nonpregnant ewes, 79-82 influence of newborn lamb on development of, 88-89, 98-99 characteristics of neonate and, 89-93 information provided by neonate and maintenance of maternal behavior, 93-97 mother-young relationships beyond postpartum period in sheep, 99, 107-108 recognition of young, 106-107

Neonate absence of, fading of postpartum maternal responsiveness in, 83-87 influence on development of maternal behavior in ewes, 88-89, 98-99 characteristics of neonate and, 89-93 information provided by neonate and maintenance of, 93-97 Neophobia, role in ingestional aversions, 284292 Neuroendocrine control, of species-typical behavior, male reproductive behavior and gonadotropin secretion, 37-44

0

Odor-aversion learning, role of ingestion in, 2%-300 Orientation, differential, selective association effect and, 315-316 Overshadowing, in taste-aversion learning, 3 19-320 Overtraining extinction effect, paradoxical reward effect and, 255-257

372

INDEX

P Paradoxical reward effects, 227-234 comparative analysis of learning and, 236-

Primates, development of vocal behavior and hearing in. 194-198

R

237

behavioral process and, 237-238 species differences and, 239-242 systemic variation and, 238 frustration theory as mechanism for, 234-236 implications for behavior and behavior theory ontogeny of appetitive behavior and, 263265

ontogeny of reward leaming and, 265-266 neural substrate of, 257-263 ontogenetic analysis of, 242-243 overtraining extinction effect and, 255-257 partial reinforcement extinction effect and magnitude of reward extinction effect and, 243-249 successive negative contrast and patterned alternation and, 249-255 Partial reinforcement extinction effect, paradoxical reward effect and, 243-249 Patterned alternation, paradoxical reward effect and, 249-255 Physiological state, maternal behavior and, 80-82

Pinnipeds adaptive strategies among convergent evolution of social structures, 136- 138

divergence in geographical distribution, 135-136

divergence in rearing methods, 133-135 divergences in ways of life, 133 social structures of adaptation to Arctic predation, 128- 129 convergent evolution of, 136-138 ecological determinism of, 125-128 effect of sex ratio on sexual dimorphism, 130-131

effect of sex ratio on sexual maturity and mortality, 129- 130 monogamy and polygyny, 131-133 sex ratio and habitat, 123 social plasticity, 123-125 Poison-avoidancelearning, see lngestional aversion leaming Polygyny, among Pinnipeds. 131-133 Predation, adaptation to, among Rnnipeds, 128- 129

Rat, development of vocal behavior and hearing in, 190-191 Rearing methods, divergences among Phocidae and Oteriidae in, 133-135 Recognition of neighbors and kin, bird song and, 154-155 of young, 106-107 Reinforcement, see Paradoxical reward effects Reproduction bird song and, 146-159 male behavior, neuroendocrine control of, 37-44

Reproductive cycle of Anolis carolinensis, see Anolis carolinensis of crocodilians, 59-61 of parthenogenetic lizards, 61-65 of snakes, 5 1-57 of turtles, 57-59 Reproductive isolation, bird song mimicry and, 157- 158

Reward, see Paradoxical reward effects Rodents, development of vocal behavior and hearing in, 189-194

S Sensory pathways, anatomical convergence of, selective association effect and, 308 Sex ratio, among Pinnipeds habitat and, 123 sexual dimorphism and, 130-131 sexual maturity and mortality and, 129-130 Sexual behavior choice, bird song and, 146-148 female receptivity, hormonal control of, 10-17

male, hormonal control of, 33-37 Sexual dimorphism, sex ratio and, among Pinnipeds, 130-131 Sexual maturity, sex ratio and, among Pinnipeds, 129-130 Snakes, reproductive cycle of, 5 1-57 Social structures, of Rnnipeds adaptation to Arctic predation, 128- 129 convergent evolution of, 136-138 ecological determinism of, 125-128

373

INDEX effect of sex ratio on sexual dimorphism, 130-13 1 effect of sex ratio on sexual maturity and mortality, 129-130 monogamy and polygyny, 13 1- 133 sex ratio and habitat, 123 social plasticity, 123-125 Sociosexual control, of species-typical behavior, seasonal gonadal recrudescence, 25-33 Sound communication, 179- 18 1, see also Bird song characteristics and tendencies of development of, 208 adult responsiveness to infant calls, 210213 adult responsiveness and vocal behavior of young, 213-214 infant hearing and discrimination, 208-209 infant responsiveness to adults, 209-2 10 nonacoustic determinants of adult response, 214-216 components of systems, 181-183 development of vocal behavior, 198-199 arousal and, 205-208 external stimuli and behavioral contexts and, 202-205 hearing and, 200-202 physical characteristics of vocal output and, 199-200 time courses of development of, 183 in Carnivora, 185-189 in Chiroptera, 183-185 in primates, 194-198 in rodents, 189-194 Species differences. in paradoxical reward effects, 239-242 Species isolation, dewlap as mechanism for, 45-48 Species-typical behavior hormonal control of female sexual receptivity, 10-17

male aggressive and sexual behavior, 33-37 neuroendocrine control of, male reproductive behavior and gonadotropin secretion, 37-44 sociosexual control of, seasonal gonadal recrudesence, 25-33 stimulus control of, male mounting behavior, 17-25 Stimulus(i) external, development of vocalizations and, 202-205 interfering, in ingestional aversion learning, 320- 324 Stimulus control, of species-typical behavior, male mounting behavior, 17-25 Stumptail macaque, development of vocal behavior and hearing in, 194-195 Successive negative contrast, paradoxical reward effect and, 249-255 Suckling behavior, 100-106 Survival, bird song and, 146-159 Systematic variation, in paradoxical reward effects. 238

T Taste aversion, see Ingestional aversion learning Territoriality, bird song mimicry and, 156 Testosterone, retrieval processes and, 359-36 I Turtles, reproductive cycle of, 57-59

V Vocalization, see Bird song; Sound communication

W Weddell seal, social plasticity in, 123-124


Contents of Previous Volumes

Volume 1

Volume 3

Aspects of Stimulation and Organization in ApproacWWithdrawal Processes Underlying Vertebrate Behavioral Development T. C. SCHNEIRLA

Behavioral Aspects of Homeostasis D. J . McFARLAND Individual Recognition of Voice in the Social Behavior of Birds C. G. BEER

Problems of Behavioral Studies in the Newborn Infant H. F. R. PRECHTL

Ontogenetic and Phylogenetic Functions of the Parent-Offspring Relationship in Mammals LAWRENCE V . HARPER

The Study of Visual Depth and Distance Perception in Animals RICHARD D. WALK

The Relationships between Mammalian Young and Conspecifics Other Than Mothers and Peers: A Review Y . SPENCER-BOOTH

Physiological and Psychological Aspects of Selective Perception GABRIEL HORN

Tool-Using in Primates and Other Vertebrates JANE VAN LAWICK-GOODALL

Current Problems in Bird Orientation KLAUS SCHMIDT-KOENIG

Author IndexSubject Index

Habitat Selection in Birds P. H. KLOPFER and J . P. HAILMAN

Volume 4

Author IndexSubject Index

Volume 2

Constraints on Learning SARA J . SHETTLEWORTH

Psychobiology of Sexual Behavior in the Guinea Pig WILLIAM C. YOUNG

Female Reproduction Cycles and Social Behavior in Primates T. E. ROWELL

Breeding Behavior of the Blowfly V. G. DETHIER

The Onset of Maternal Behavior in Rats, Hamsters, and Mice: A Selective Review ELAINE NOIROT

Sequences of Behavior R. A. HINDE and J . G. STEVENSON

Sexual and Other Long-Term Aspects of Imprinting in Birds and Other Species KLAUS IMMELMANN

The Neurobehavioral Analysis of Limbic Forebrain Mechanisms: Revision and Progress Report KARL H. PRIBRAM Age-Mate or Peer Affectional System HARRY F. HARLOW

Recognition Processes and Behavior, with Special Reference to Effects of Testosterone on Persistence R. J . ANDREW

Author 1ndexJubjec.r Index

Author IndexSubjert Index

315

316

CONTENTS OF PREVIOUS VOLUMES

Volume 5

Volume 7

Some Neuronal Mechanisms of Simple Behavior KENNETH D. ROEDER

Maturation of the Mammalian Nervous System and the Ontogeny of Behavior PATRICIA S . GOLDMAN

The Orientational and Navigational Basis of Homing in Birds WILLIAM T. KEETON The Ontogeny of Behavior in the Chick Embryo RONALD W. OPPENHEIM Processes Governing Behavioral States of Readiness WALTER HEILIGENBERG Time-sharing as a Behavioral Phenomenon D. J . McFARLAND

Functional Analysis of Masculine Copulatory Behavior in the Rat BENJAMIN D. SACHS and RONALD J . BARFIELD Sexual Receptivity and Attractiveness in the Female Rhesus Monkey ERIC B. KEVERNE Prenatal Parent-Young Interactions in Birds and Their Long-Term Effects MONICA IMPEKOVEN

Male-Female Interactions and the Organization of Mammalian Mating Patterns CAROL DIAKOW

Life History of Male Japanese Monkeys YUKIMARU SUGIYAMA

Auihor Index-Subjeci Index

H.PHILIP ZEIGLER

Volume 6 Specificity and the Origins of Behavior P. P. G. BATESON The Selection of Foods by Rats, Humans, and Other Animals PAUL ROZIN

Feeding Behavior of the Pigeon Subject Index

Volume 8 Comparative Approaches to Social Behavior in Closely Related Species of Birds FRANK McKINNEY

Social Transmission of Acquired Behavior: A Discussion of Tradition and Social Learning in Vertebrates BENNETT G. GALEF. JR.

The Influence of Daylength and Male Vocalizations on the Estrogen-Dependent Behavior of Female Canaries and Budgerigars, with Discussion of Data from Other Species ROBERT A. HINDE and ELIZABETH STEEL

Care and Exploitation of Nonhuman Primate Infants by Conspecifics Other Than the Mother SARAH BLAFFER HRDY

Ethological Aspects of Chemical Communication in Ants BERT HOLLDOBLER

Hypothalamic Mechanisms of Sexual Behavior, with Special Reference to Birds J. B. HUTCHISON

Filial Responsiveness to Olfactory Cues in the Laboratory Rat MICHAEL LEON

Sex Hormones, Regulatory Behaviors, and Body Weight GEORGE N. WADE

A Comparison of the Properties of Different Reinforcers JERRY A. HOGAN and T. J. ROPER

Subject index

Subject index

CONTENTS OF PREVIOUS VOLUMES

377

Volume 9

Volume 10

Attachment as Related to Mother-Infant Interaction MARY D. SALTER AINSWORTH

Learning, Change, and Evolution: An Enquiry into the Teleonomy of Learning H. C. PLOTKIN and F. 1. ODLING-SMEE

Feeding: An Ecological Approach F. REED HAINSWORTH and LARRY L WOLF

Social Behavior, Group Structure, and the Control of Sex Reversal in Hermaphroditic Fish DOUGLAS Y. SHAPIRO

Progress and Prospects in Ring Dove Research: A Personal View MEI-FANG CHENG Sexual Selection and Its Component Parts, Somatic and Genital Selection, as lllustrated by Man and the Great Apes R. V. SHORT Socioecology of Five Sympatric Monkey Species in the Kibale Forest, Uganda THOMAS T. STRUHSAKER and LYSA LELAND Ontogenesis and Phylogenesis: Mutual Constraints GASTON RICHARD Subjecr Index

Mammalian Social Odors: A Critical Review RlCHARD E. BROWN The Development of Friendly Approach Behavior in the Cat: A Study of Kitten-Mother Relations and the Cognitive Development of the Kitten from Birth to Eight Weeks MILDRED MOELK Progress in the Study of Maternal Behavior in the Rat: Hormonal, Nonhormonal, Sensory. and Developmental Aspects JAY S. ROSENBLATT, HAROLD I. SIEGEL, and ANNE D. MAYER Subjec,! Index


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