Naturwissenschaften 86, 101–111 (1999) Q Springer-Verlag 1999 101

The Development of AnimalBehavior: From Lorenz toNeural NetsJohan J. Bolhuis

Behavioral Biology, Institute of Evolutionaryand Ecological Sciences, University of Leiden,P.O. Box 9516, 2300 RA Leiden,The Netherlands

In the study of behavioral development both causaland functional approaches have been used, and theyoften overlap. The concept of ontogenetic adapta-tions suggests that each developmental phase in-volves unique adaptations to the environment of thedeveloping animal. The functional concept of opti-mal outbreeding has led to further experimental evi-dence and theoretical models concerning the role ofsexual imprinting in the evolutionary process of sex-ual selection. From a causal perspective it has beenproposed that behavioral ontogeny involves the de-velopment of various kinds of perceptual, motor,and central mechanisms and the formation of con-nections among them. This framework has beentested for a number of complex behavior systemssuch as hunger and dustbathing. Imprinting is oftenseen as a model system for behavioral developmentin general. Recent advances in imprinting researchhave been the result of an interdisciplinary effort in-volving ethology, neuroscience, and experimentalpsychology, with a continual interplay between theseapproaches. The imprinting results are consistentwith Lorenz’ early intuitive suggestions and are alsoreflected in the architecture of recent neural netmodels.

Introduction

In recent years there has been renewed interest inthe analysis of the development of animal behavior.For example, the field of developmental cognitiveneuroscience has emerged, in which cognitive devel-opment is related to development of the brain (e.g.,Johnson and Morton 1991; Johnson 1992, 1997).Furthermore, within ethology new syntheses of be-havioral development have appeared (Bateson 1991;Hogan and Bolhuis 1994; Bolhuis and Hogan 1999).This article does not give a historical account of de-velopmental research over the past half century but,rather, reviews some of the major recent trends inthe study of the development of animal behavior.The last section briefly discusses work that my col-leagues and I have carried out on the developmentof filial preferences in the chick. This specific re-search paradigm reflects some of the major direc-tions in the analysis of behavioral development ingeneral. Some of the questions asked in the earlydays of developmental research, such as the nature/nurture issue, are still with us, under a differentguise. However, the main thrust of contemporary re-search involves both functional and causal ap-proaches, and often integrates ethology, experimen-tal psychology, and neuroscience.

Nature/Nurture Revisited

The nature/nurture debate which plagued animalbehavior research in the 1950s and 1960s (Lehrman1953; Lorenz 1965) was in fact less about “nature”(genetic, or “innate” factors) versus “nurture” (ef-fect of learning and experience) determining behav-ior than about whether one can separate geneticfrom environmental effects in particular behavior

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patterns, as Lorenz had originally implied. Lehrman(1970) provided the definitive statement about thisissue, and more recently Oyama (1985) further de-veloped this view in her monograph. Lehrman(1970) noted that an important issue in the controv-ersy between him and Lorenz was that they were re-ally interested in two different problems. Lehrmanwas interested in studying the effects of all types ofexperience on all types of behavior at all stages ofdevelopment, whereas Lorenz was interested only instudying the effects of functional experience on be-havior mechanisms at the stage of development atwhich they begin to function as modes of adaptationto the environment (for discussion see Hogan 1988).As Hogan (1988) pointed out, this means that Lehr-man used a causal criterion to determine what wasinteresting to study, while Lorenz used a functionalcriterion. Hogan argued that these two criteria areequally legitimate, but that Lorenz’ functional crite-rion corresponds to the way in which most peoplethink about development. The latter is true, butmost contemporary researchers hold a view of onto-geny in which development is seen as a complex se-ries of interactions between the individual and its in-ternal and external environment; developmentalchange at any time is affected by the preceding de-velopmental stage, which in itself has been the prod-uct of a complex interaction between the individualat a certain time and its environment. That this viewis still not commonplace among all students of be-havior can be illustrated with two examples.The first comes from work on sexual imprinting, theprocess by which animals develop a preference for asexual partner from the morph or species with whichthey were reared (Immelman 1969, 1972; Kruijt1985; Bischof 1994). When young zebra finches(Taeniopygia guttata castanotis) are raised (cross-fostered) by adults of the related Bengalese finch(Lonchura striata), they show a sexual preferencefor a partner of the foster species over one of theirown species (e.g., Immelman 1969). However, Im-melmann (1972) and others also noted that the pre-ference for the foster species in cross-fostered zebrafinches is not as strong as that of normally rearedzebra finches for conspecifics. This led to the sugges-tion that in zebra finches there is an innate bias toprefer a member of their own species (Immelmann1972). Ten Cate (1982) confirmed the findings ofImmelmann (1972) and others and observed thatwhen zebra finch young are reared by a mixed pairof a zebra finch parent and a Bengalese finch parent,the young develop a sexual preference for a zebrafinch mate. However, ten Cate (1982) found thatwhen mixed pairs are used, the zebra finch parentsspend significantly more time with the zebra finch

young in a number of social behaviors than the Ben-galese finch foster parents. In a subsequent study(ten Cate 1984) the amount of social interaction be-tween young zebra finch males and the two mem-bers of a mixed pair of foster parents was manipu-lated. Decreasing the number of social interactionsbetween the zebra finch parent and the young led toa corresponding shift in sexual preference toward apreference for a Bengalese finch female. Thus theeventual sexual preference is likely to be affected bythe differential social interactions that the youngbirds experience during development (for furtherexamples see Kruijt 1985). It was not necessary toinvoke a role for “innate” species-specific predispo-sitions to explain the behavior. Below we will seeexamples of predispositions in filial preferences thatalso go beyond a simple innate/acquired dichoto-my.A more recent example stems from the emergingfield of developmental cognitive neuroscience,where the nature/nurture problem has survived in adifferent guise. Quartz and Sejnowski (1997) suggestthat, contrary to current popular views in cognitiveneuroscience and psychology, constructive neuralevents such as synapse formation and the strength-ening of synapses are more important for cognitivedevelopment than regressive neural events such as“synapse pruning,” where there is an elimination of“overproduced” connections. Below I discuss neuralevidence that supports a “constructivist” view. Theauthors argue that invoking regressive neural eventsleads to a “need for domain-specific prespecifica-tion” with a “heavy burden that nativism places ongenetic mechanisms.” They go on to say that(p. 539):

“The far-reaching interaction between environ-mental structure and neural growth mechanismssuggests that development has been in the grip ofa misleading dichotomy. On the one hand, empir-icists offer a general-purpose, computational ar-chitecture with generic learning procedures; onthe other hand, rationalists offer domain-specificknowledge implanted in cognitive structures. It isstriking how readily so much of the developmen-tal literature falls into these two extremes.”

Clearly the debate continues in this field. The term“innate” is still widely used in the developmentalcognitive literature.

Four Questions About Behavior

In any ethological investigation it is good to beginby considering Tinbergen’s (1963) four questions

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about behavior, namely causation, survival value (orfunction, as it is now called), evolution, and develop-ment. Tinbergen acknowledged that the first threeof these had already been proposed by Julian Hux-ley as the important problems in biology. Clearly,Tinbergen thought that development is importantenough in itself to be added to the list. Broadlyspeaking, causation and development are consid-ered causal approaches to the study of behavior,while function and evolution are functional ap-proaches. The present contribution illustrates howcausal and functional approaches can both be im-portant ways of discovering more about the devel-opment of behavior. In addition, some of the resultsof developmental research may have important con-sequences for evolutionary theory. Not only is it im-portant to consider both causal and functional as-pects of behavior when analyzing a particular prob-lem, but it is also essential to realize that one cannotsolve a functional problem with a causal analysisalone, just as one cannot discover the mechanisms ofbehavior by asking functional questions only. Theconsequences of behavior are not its causes (Hogan1994a). With this in mind, one often finds that bothcausal and functional approaches are employedwithin a single developmental paradigm.

Functional Questions and EvolutionaryConsequences

Oppenheim (1981) suggested that stages in develop-ment are often not merely a kind of immature pre-paration for the adult state – although they certainlycan be – but that each developmental phase involvesunique adaptations to the environment of the devel-oping animal. Oppenheim called these “ontogeneticadaptations.” As a consequence, certain early be-havior patterns may disappear in the course of de-velopment, a phenomenon that Oppenheim termeda “retrogressive process.” Hall and Williams (1983)provide a good example of this, demonstrating thatin rat pups “suckling isn’t feeding.” Suckling behav-ior is qualitatively different from later feeding be-havior, and it is the sole means of food intake untilweaning, which, according to Oppenheim (1981),qualifies it as an ontogenetic adaptation.Figure 1 shows the two possible developmentalscenarios for suckling and feeding in rats. One possi-bility, illustrated in Fig. 1A, is that suckling mergesinto feeding at weaning, and the two behaviors shareinternal and external controls. Alternatively, asshown in Fig. 1B, the two behaviors are relatively

Fig. 1A,B. Two scenarios for the development of suckling and feedingin rats. A) Suckling can be seen either as continuous with later feed-ing, merging into the feeding system at the time of weaning; or B)suckling and feeding can be seen as relatively separate systems, shar-ing only some controls at weaning. (Reprinted with permission of Ac-ademic Press, Inc. from Hall and Williams 1983)

separate, and they share only some internal and ex-ternal controls. Hall and coworkers found that adultingestion is not a continuation of suckling, as it hasdifferent internal and external controls. Further-more, if pups are deprived of suckling by feedingthem with a cannula, later feeding behavior emergesnormally, suggesting that suckling is not a necessaryantecedent for adult feeding (Hall 1979). Oppen-heim (1981) also suggested that imprinting and birdsong learning, because they occur only early duringontogeny, may be other examples of “ontogeneticadaptations.” Below I consider examples of earlylearning processes during imprinting in domesticchicks (Gallus gallus domesticus) that have differentcharacteristics from learning in the adult animal. Allthese examples are essentially causal analyses thatconfirm hypotheses derived from functional consid-erations.An example of an initially causal investigation withimportant functional implications is Bateson’s(1982) findings concerning sexual imprinting andoptimal outbreeding. As becomes clear below, “op-timal outbreeding” is a functional concept. In oneexperiment (Bateson 1982) Japanese quail chicks(Coturnix coturnix japonica) were reared in small si-bling groups, and after a period of isolation their so-cial preferences were tested. Both males and fe-males spent most of the test period with an unfamil-iar individual, particularly a first cousin. Bateson ar-gued that by choosing stimulus birds that are slightlydifferent, but not too different, from the rearingstimuli, the animals strike an optimal balance be-tween the adverse effects of inbreeding and exces-sive outbreeding. He called this “optimal outbreed-ing.”

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This makes functional sense, but the phenomenonmay also have evolutionary consequences. This in-volves the possible role of sexual imprinting in sex-ual selection and the resulting evolution of conspicu-ous plumage. Ten Cate and Bateson (1988) reexam-ined the relationship between these two processesand concluded that the traditional view, with a rath-er limited role for sexual imprinting in evolution,may not be adequate. Sexual imprinting has tradi-tionally been considered a relatively rare phenome-non, limited to special situations such as rapidlyevolving groups, and to one sex only. Also, sexualimprinting was thought to be incompatible with pre-ferences for conspicuous features such as can beseen in sexual selection. Ten Cate and Vos (1999)learned from a review of the literature that sexualimprinting actually occurs in the majority of bird or-ders and in both sexes. The traditional view of sex-ual imprinting is that it leads to a sexual preferencefor an individual that closely resembles the individu-al with which the experimental animal was reared(Kruijt 1985). Such a process would have a stabiliz-ing effect on the evolution of plumage characteris-tics. Indeed, when the animals are given a prefer-ence test involving the rearing species or colormorph and a novel species or color morph, this is atypical result (Kruijt 1985; Bolhuis 1991; Bischof1994; ten Cate and Vos 1999). However, when theanimals are provided with a choice between variousindividuals of the rearing species or color morph, asin the case of Bateson’s quail experiment, they mayshow a preference for an individual that has a differ-ent appearance from that with which they werereared. If this preference is for individuals that areslightly more conspicuous, or that are “supernor-mal” – and there is evidence that this is the case – itis clear that, when there are mutations with differentplumage characteristics, individuals with a plumagethat is slightly more conspicuous than that of therearing type are preferred. This would lead to a shifttowards more conspicuous plumage (ten Cate andBateson 1988; Laland 1994).To test whether slight deviations from the familiardo indeed make a novel individual more attractive,ten Cate and Bateson (1989) reared quail chickswith an adult with a certain number of black dotsartificially applied to its white plumage. The ani-mals’ preferences were tested later with stimulusbirds having either the same number of dots, moredots, or fewer dots. Overall there was a significantpreference for the stimulus animals with a greaterrather than a smaller number of dots than on thefamiliar individual. In separate preference tests itwas found that the experimental animals preferredan individual of the white rearing morph to a wild-

type individual, indicating that sexual imprintinghad occurred. Thus, there was a preference for thecolor morph with which the animals were rearedand at the same time a bias for plumage characteris-tics that deviated from those of the familiar individ-uals.There are still many questions to be answered, con-cerning both the functional aspects of this behaviorand the mechanisms involved. For instance: To whatextent is the bias a result of learning? Do the ani-mals habituate to the familiar stimulus? Neverthe-less, these results suggest that, rather than sexual im-printing limiting the direction of evolutionarychange, it might well be an important factor in sex-ual selection (Laland 1994; ten Cate and Bateson1988; ten Cate and Vos 1999).

Causation: Development of BehavioralStructure

In a number of papers Lorenz (e.g., 1935) proposedthe concept of “schema,” which is a kind of percep-tual mechanism that “recognizes” certain objects(Hogan 1988). In the development of a social bondbetween parents and young, Lorenz suggested thatin certain bird species (such as the curlew, Numeniusarquata) the newly hatched chicks come equippedwith a schema which is thought to be “innate,” whilein others (such as the greylag goose, Anser anser)the schema develops as a result of particular experi-ence.More on the motor side of behavior, important sug-gestions were made by Kruijt (1964) in his classicmonograph on the development of social behaviorin the jungle fowl (Gallus gallus spadiceus). Kruijtsuggested, among other things, that in the youngjungle fowl chick – and obviously, in other species aswell – many of the motor components of behaviorappear as independent units prior to any opportuni-ty for practice, and that only later, often after specif-ic experience, do these motor components becomeintegrated into more complex systems such as hun-ger, aggression, or sex. An example is aggressive be-havior in young male chicks, where behavioral com-ponents initially occur quite independently but laterbecome integrated into behavioral sequences seenduring agonistic encounters with other males.Hogan (1988) has generalized these early proposalsby Lorenz and especially Kruijt and suggested ageneral framework for the analysis of behavioral de-velopment using the concept of behavior system(see Fig. 2). A behavior system consists of variouselements: a central mechanism, perceptual mecha-

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Fig. 2. Hogan’s framework of behavior systems. Stimuli from the ex-ternal world are analyzed by perceptual mechanisms. Output from theperceptual mechanisms can be integrated by central mechanisms and/or channeled directly to motor mechanisms. The output of the motormechanisms results in behavior. In this diagram, central mechanism I,perceptual mechanisms 1–3, and motor mechanisms A–C form onebehavior system; central mechanism II, perceptual mechanisms 3–5,and motor mechanisms C–E form a second behavior system. 1-A, 2-B,etc. can also be considered less complete behavior systems. (Repro-duced with permission of Plenum Publishing Corp. from Hogan1988)

Fig. 3. A diagram of the hunger system of a young chick, based on results of Hogan and others. Solid lines, mechanisms and connectionsbetween them that develop prefunctionally; dashed lines, mechanisms and connections that develop as the result of specific functional experi-ence. Perceptual mechanisms include feature recognition mechanisms (of color, shape, movement, etc.), object recognition mechanisms [such asof grainlike objects (G), wormlike objects (Wo), and possibly others], and a function recognition mechanism (Food). Motor mechanisms includethose underlying specific behavior patterns such as pecking (P), ground scratching (S), walking (Wa), and possibly others. There is also a centralhunger mechanism (H). (Reproduced with permission of Plenum Publishing Corp. from Hogan 1988)

nisms, and motor mechanisms. These mechanismshave corresponding structures in the central nervoussystem, and one could also call them cognitive struc-tures. The structural definition of a behavior systemis “any organization of perceptual, central and mo-tor mechanisms that acts as a unit in some situa-tions” (Hogan 1994a). According to Hogan (1988),behavioral development is essentially the develop-ment of these mechanisms and the changes in theconnections among them. Often these mechanismsand their connections develop only after functionalexperience, i.e., experience with the particular stim-uli involved or with the consequences of performingspecific motor patterns.An example of a developing behavior system is thehunger system in the jungle fowl chick (Hogan 1977,1988). The system involves perceptual mechanismsfor the recognition of features (color, shape, etc.)and, for instance, of food versus nonfood (seeFig. 3). There are also motor mechanisms underly-ing behavior patterns such as ground scratching andpecking, and there is a central hunger mechanism.Importantly, several of the connections between themechanisms (Fig. 3, dashed lines) develop as a resultof specific functional experience. For instance, onlyafter a substantial meal does the chick differentiatebetween food items and nonfood items to eat (Ho-gan-Warburg and Hogan 1981). On the motor sideof the system, young chicks’ pecking behavior doesnot depend on the level of food deprivation. A sim-ilar phenomenon occurs in the case of suckling in ratpups, as studied by Hall and Williams (1983). Suck-

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ling decreases as weaning approaches, but, impor-tantly, suckling behavior does not become depriva-tion dependent until about 2 weeks after birth. Wedo not know whether and what functional experi-ence is needed to connect the suckling motor mech-anism with the central hunger mechanism in the ratpup, but we do know what is needed in the chick. Inthe young chick, initially the feeding-related behav-ior (in this case pecking) does not depend on thelevel of food deprivation. Thus there the centralhunger mechanism and the pecking motor mecha-nism are not connected. Only after the experience ofpecking and swallowing (and not necessarily offood: pecking and swallowing sand are equally effec-tive) do the two mechanisms become connected, andonly then does the level of pecking depend on thelevel of food deprivation (Hogan 1977).The development of behavioral structure is not uni-form but may proceed along different pathways fordifferent behavior systems. An example of this is thedevelopment of dustbathing in jungle fowl chicks, asstudied by Vestergaard and coworkers (Vestergaard1982; Vestergaard and Hogan 1992; Vestergaard etal. 1990, 1993). Dustbathing is a behavior in whichadult birds of many species frequently engage. Itconsists of a sequence of coordinated movements ofthe wings, feet, head, and body that serve to spreaddust through the feathers. The function of this be-havior is to remove excess lipids from the feathersand to maintain good feather condition (van Liereand Bokma 1987). Unlike the development of feed-ing behavior in rats and chicks, dustbathing is depri-vation dependent as soon as it appears in the ani-mal’s behavioral repertoire (Hogan et al. 1991).Thus, in this case, chicks do not require functionalexperience to connect the motor mechanisms withthe central dustbathing mechanism. Dustbathing isalso affected by a circadian rhythm (Vestergaard1982). On the perceptual side, other experimentshave shown that the chick initially performs dust-bathing on virtually any kind of surface, includingwire mesh, suggesting that the perceptual mecha-nism and the central mechanism are not yet con-nected (Vestergaard et al. 1990). The perceptualmechanism itself develops more quickly with somesubstrates than others, which is similar to the devel-opment of perceptual mechanisms in song learning(Marler 1991) and filial predispositions (Bolhuis1991). Furthermore, it has been shown that prefer-ences for functionally unlikely surfaces (in this case,a skin of jungle fowl feathers) can be acquired as aresult of experience with them (Vestergaard andHogan 1992) – another example of the developmentof a perceptual mechanism and one that is not dis-similar to filial imprinting.

The finding by Vestergaard et al. (1990) that junglefowl raised on wire mesh with no opportunity forfunctional dustbathing show the same amount ofdustbathing as birds reared with dusty substrates isof great theoretical importance. Other results (re-viewed in Hogan 1994b, 1997) also suggest that ex-ternal factors, such as the availability of dust and theamount of parasites and lipids in the feathers, arenot an important cause of the regulation of dust-bathing. Rather, they suggest that, apart from a cir-cadian rhythm, there is another endogenous processthat governs the behavior: a build-up of motivationduring periods of deprivation, very much accordingto early proposals by Lorenz (1937a). Hogan (1997)has recently reviewed these and other results and ar-gues for a reconsideration of energy models of moti-vation.

Learning and Predispositions in theDevelopment of Filial Preferences

The remainder of this contribution describes our in-vestigation of the mechanisms underlying the devel-opment of filial preferences in the domestic chick.This developmental process has several characteris-tics that may be important in behavioral develop-ment in general. Our research involves a synthesis ofethology, neuroscience, and experimental psycholo-gy, and each of these are considered in turn.The development of filial preferences in the domes-tic chick is under the influence of at least two sepa-rate systems. One of these involves what Hogan(1988) called the prefunctional development of aperceptual mechanism; Horn (1985) coined thephrase “predisposition” to describe this system. Theexistence of predispositions in the chick was origi-nally derived from lesion studies involving two im-printing stimuli, a rotating red box, and a stuffedjungle fowl hen (Horn and McCabe 1984). Horn andMcCabe have reported that the effects of lesions toa forebrain region called the intermediate and me-dial hyperstriatum ventrale (IMHV; see below) de-pend on the stimulus used for imprinting training.IMHV lesions greatly impair filial preferences ofchicks trained with a red box but have a relativelysmall (but significant) effect on the preferences ofchicks trained by exposure to the stuffed fowl. Theseand other findings (Horn 1985) led to the suggestionthat chicks’ preferences are influenced not only bylearning but also by a predisposition to approachcertain stimuli such as the stuffed fowl.Figure 4 summarizes the results of one of our subse-quent behavioral experiments (Johnson et al. 1995).

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Fig. 4. Mean preference scores, expressed as a preference for the stuf-fed fowl, of chicks previously trained by exposure to a rotating stuffedjungle fowl, a rotating red box, or exposed to white light (black bars).Preference scores are defined as: activity when attempting to ap-proach the stuffed jungle fowl divided by total approach activity dur-ing the test. Preferences were measured in a simultaneous test either2 h (Test 1) or 24 h (Test 2) after the end of training. k1–k4, differencesbetween the preferences of the trained chicks and the controls; Dy,difference in preference between the control chicks at Test 2 and atTest 1. See text for further explanation. (By permission of the OxfordUniversity Press from Horn 1985, after Johnson et al. 1985)

We gave dark-reared chicks imprinting training byexposing them to either the red box or the stuffedjungle fowl for a certain period of time. We also hada control group that was exposed only to white over-head light for the same period. The chick’s approachpreferences were tested either 2 h or 24 h after theend of the training experience.Preferences are presented in Fig. 4 as relative ap-proach to the stuffed fowl; scores above 50% indi-cate a preference for the fowl over the box. Therewas an effect of training on preferences (indicatedhere as k1–k4) as well as an increase in preferencefor the fowl with time, irrespective of whether thebirds were trained or not (indicated here as Dy).Subsequent studies confirmed that the former re-flects a learning process (filial imprinting) and thelatter the effect of an emerging predisposition (e.g.,Johnson and Horn 1986; Bolhuis et al. 1989a). Thepredisposition can also develop in dark-rearedchicks, provided that they receive some kind of non-specific experience. If chicks are left in the dark, thepredisposition is not expressed during preferencetests with the box and the fowl. However, if thechicks are placed in running wheels (in darkness) orare handled only briefly, the predisposition emergesover the same time course as before (see Bolhuis1996 for a recent review).

Thus the development of this perceptual mechanismdoes not require specific functional experience, butit does require some kind of experience. Other ex-periments demonstrate that the nonspecific experi-ence needed for the induction (Gottlieb 1976) of thepredisposition in dark-reared chicks must occurwithin a sensitive period approximately 14–40 h aft-er hatching (Johnson et al. 1989). The predispositionis not species specific but for stimuli with a head andneck (Johnson and Horn 1988). The presence of aneye in the stimulus animal (i.e., the stuffed hen) isimportant for the expression of the predisposition,but not crucial (Bolhuis 1996).

Neural Mechanisms of Imprinting

Filial imprinting has become an important paradigmfor the study of the neural mechanisms of learningand memory (for reviews see Horn 1985, 1990,1998). As indicated above, the work on filial predis-positions comes from a series of forebrain lesionstudies. The crucial lesion was restricted to theIMHV. It is important to point out that the lesionexperiments were a relatively late addition to therange of techniques that Horn et al. applied; theywere control experiments to confirm suggestions de-rived from other studies. The IMHV had becomethe focus of attention after a series of biochemicalstudies demonstrated that it is crucially involved inthe learning process of imprinting. Early studies re-vealed a significant increase in incorporation of ra-dioactively labeled RNA precursers into the IMHVafter imprinting. RNA synthesis suggests that pro-tein synthesis takes place, which would be necessaryto achieve structural changes in neural connectivitythat were presumed to underlie learning. Most ofthe structural and biochemical changes related tolearning occurred particularly in the IMHV and onthe left side of the brain. For instance, there was anincrease in postsynaptic densities, which is essential-ly the contact zone between two neurons, an in-crease in the number of a particular kind of gluta-mate receptor, namely the NMDA receptor, and anincrease in phosphorylation of MARCKS protein, aprotein kinase C substrate, all in the left IMHV.These parameters are correlated significantly withthe chicks’ preference score, a measure of thestrength of learning (Horn 1985, 1992, 1998). Im-printing also leads to a learning-related increase inimmunoreactivity of the immediate early gene prod-uct Fos in the IMHV (McCabe and Horn 1994). Theexpression of immediate early genes is used as ameasure for the activation of cells, in this case neu-

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rons. Thus it is a means of visualizing the neuronsthat are active when learning takes place. Bilaterallesions to the chick IMHV impair both acquisitionand retention of filial preferences (Horn 1985).The results from the imprinting work support a“constructivist” interpretation (Quartz and Sejnows-ki 1997), where information storage in the brain isaccompanied by increased neuronal connectivity.Such neural changes had earlier been proposed byHebb (1949) in his famous statement (p. 62):

“When an axon of cell a is near enough to excitea cell B and repeatedly or persistently takes partin firing it, some growth process or metabolicchange takes place in one or both cells such thatA’s efficiency, as one of the cells firing B, is in-creased.”

In contemporary terms this means that changes inneuronal connectivity can come about as a result ofsimultaneous pre- and postsynaptic activity. As seenbelow, Hebb’s principle is also important in theanalysis of learning processes during imprinting.Apart from the intrinsic importance of the neuro-biological research (Horn 1985, 1998), it also givesus an opportunity to further analyze the behavioralphenomena (see also Bolhuis 1994). For instance,bilateral lesions to the IMHV impair imprinting butare without effect on the developing predisposition(Johnson and Horn 1986). Thus it is likely that theneural substrate for the predisposition is somewhereoutside the IMHV. Another example is reminiscentof sexual preferences for slightly novel stimuli. Thedomestic chicken also shows such preferences. Ani-mals reared with a group of other individuals prefera novel individual to either a familiar one or an indi-vidual of another strain. Early bilateral lesions tothe IMHV abolish this preference (Bolhuis et al.1989b).

Imprinting and Associative Learning

Lorenz (1935, 1937b) stated that imprinting differssubstantially from other forms of learning. However,it appears that when Lorenz spoke of imprinting(“Prägung” in his original 1935 paper) he was in factreferring to that which we now call sexual imprinting(for a detailed discussion see Bolhuis 1996). Whentalking about the formation of filial preferences inhis 1937 paper he actually said that it is “true asso-ciative learning which unites the different sets of rel-easing stimuli emanating from an individual com-panion” (Lorenz 1937b, p. 262).Lorenz’ intuitions are borne out by some of our re-cent findings concerning the mechanisms of learning

during imprinting. In the spirit of Lorenz’ quote, wetook into account that the mother hen not only has aparticular visual appearance but also makes certainsounds, and we wanted to study the interaction be-tween auditory and visual learning. A basic findingwas that when we trained domestic chicks by expos-ing them to a compound stimulus of a moving visualstimulus and a taped maternal call, and later testedpreferences without the call but with the trainingvisual stimulus and a novel visual stimulus, the pre-ference for the visual stimulus was enhanced as a re-sult of compound training (Van Kampen and Bol-huis 1993; Bolhuis and Honey 1994). This potentia-tion of learning has similarities with potentiation ef-fects in conventional psychological paradigms, forexample, when rats learn about tastes and odors(Durlach and Rescorla 1980), and we suggested thatthe underlying mechanisms are also similar. This didin fact prove to be the case. For instance, when weexposed the chicks to an element of the compoundstimulus (in this case the maternal call) either beforeor after exposure to the compound, the potentiationeffect was virtually abolished (Bolhuis and Honey1994).This result is very similar to findings in taste/odorlearning in rats, such as investigated by Rescorla andDurlach (1981), and can be interpreted as a case ofwithin-event learning, where links are formed be-tween the representations of the elements of thecompound stimulus, which can be weakened if thereis separate exposure to one of the elements. In a fur-ther study we found that when chicks are given aseries of brief presentations of the visual and the au-ditory elements, simultaneous presentation of thetwo elements is superior to sequential presentation,where presentation of the visual stimulus is followedby that of the auditory stimulus (Honey and Bolhuis1997). This finding is not consistent with a Pavlovianconditioning interpretation but supports a within-event learning explanation. In fact, both Rescorlaand Durlach’s and our results are consistent withHebb’s (1949) suggestion that constructing a respre-sentation of an stimulus involves the formation ofassociative links among those elements of the stimu-lus that reliably co-occur (see also Bolhuis and Hon-ey 1998).

Neural Nets

Neural network models are being used increasinglyto model learning and development. In particular,our results can be interpreted within a neural netmodel of imprinting and object recognition memory

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Fig. 5. Flow diagram of the simplest version of the neural net modelby Bateson and Horn (1994). The network consists of three systems(Analysis, Recognition, Execution), which contain modules. For sim-plicity only two analysis modules and two recognition modules areshown. All modules in the analysis system are linked to all modules inthe recognition system which, in turn, are linked to all modules in theexecutive system. All modules in the analysis system are also linkeddirectly to the module in the executive system that controls filial ap-proach behavior. The strength of the links connecting the modules isreflected in the thickness of the lines. (Reprinted from Animal Behav-iour, 48, Bateson and Horn, Imprinting and recognition memory: aneural net model, p. 695–715, 1994, by permission of the publisherAcademic Press.)

put forward by Bateson and Horn (1994). A similarmodel was proposed by O’Reilly and Johnson(1994). Figure 5 is a simple diagram of the basicscheme of Bateson and Horn’s model. The networkhas three layers, as do many of the current paralleldistributed processing models (Rumelhart andMcClelland 1986). In this case the respective layersare called analysis, recognition, and executive sys-tems, and they consist of various modules that areall interconnected. The analysis system receives in-put from stimuli, while the executive system is re-sponsible for the behavioral output. There are somesuperficial similarities between this model and thebasic structure of Hogan’s (1988) framework I dis-cussed above. The first principle governing the net-work is that excitability of the various modules caninitially fluctuate randomly. Second, there are twobasic rules for changing the strength of the connec-tions between two modules. The first is basically aHebbian rule, such as we have seen above. That is, aconnection is strengthened whenever the two mod-ules are active simultaneously. In addition, connec-tions are weakened when there is activity in a recog-nition module but no activity in the correspondinganalysis module, a rule that was first formulated byStent (1973).What happens when we expose the animal, and inthis case the network, to a compound stimulus con-sisting of an auditory and a visual element? If weassume that recognition module R1 is active, bothA1-R1 and A2-R1 are strengthened according toHebb’s rule. As there is activity in both of these con-

nections, there is increased scope for strengtheningof the connections, which is an indication of the po-tentiation effect. If we then present the animal/net-work with the auditory stimulus only, as we havedone in our experiments, A2 is active, as is R1, butA1 does not become activated, as the visual stimulusis absent. As a result, A1-R1 is weakened, while A2-R1 is further strengthened. This is also what wefound in our experiments: on subsequent testing thechicks showed a much weaker preference for the vis-ual training stimulus than the control group. Also,further exposure to the auditory stimulus led to agreater preference for that stimulus over a novel call(Bolhuis and Honey 1994).

Conclusions

This review shows that all of Huxley/Tinbergen’squestions have a role to play in the investigation ofbehavioral development. In the study of the mecha-nisms of development, concepts and methods fromethology, experimental psychology, and neuros-cience are all important to achieve an overall con-cept of what is going on. Finally, it is gratifying tosee that Lorenz’ early intuitions about behavioraldevelopment are compatible with contemporaryanalyses of early learning, including interpretationsusing neural nets.

Acknowledgements. This review is based on a plenary lecture givenat the 25th International Ethological Conference in Vienna, August1997. I am grateful to Dr. Michael Taborsky and the organizing com-mittee for inviting me, and to Dr. Dieter Czeschlik for inviting me towrite this review. I also thank Jerry Hogan and Carel ten Cate fortheir comments on the manuscript. My own research discussed herewas supported by a Postdoctoral Research Fellowship from the Bio-technology and Biological Sciences Research Council (UK), held atthe Sub-Department of Animal Behaviour, University of Cam-bridge.

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