developmental cognitive neuroscience: looking ahead

Early Development and ParentingEarly Dev. Parent. 7: 163–169 (1998)

Developmental CognitiveNeuroscience: Looking Ahead

Mark H. Johnson*Department of Psychology, Birkbeck College, University of London,London WC1E 7HX, UK

THE COMMON GROUND

First, I wish to thank all of the reviewers fortheir constructive, and often insightful, com-ments on my book. They all appear to share mybelief that the time is ripe for bringing togetherevidence from brain development, cognitive de-velopment, and computational modelling, andthus that Developmental Cognitive Neuroscience(DCN from here on refers to the book) is atimely volume. Most go further with me in thebelief that we have to ‘walk the line betweennarrow nativism and empty empiricism’ (Aslin)and that ‘if one begins to consider the structureof the CNS and its relationship to behaviourwithin a developmental framework, a construc-tivist approach to both brain and behaviourbecomes an almost inescapable theoretical posi-tion’ (Colombo). A couple of the reviews, how-ever, did manage the escape from theinescapable and implied that my aim in DCNwas to ‘refute nativism’. Interestingly, these re-viewers (Johnson and Jusczyck, Marcus) aremainly experts in the domain of speech andlanguage acquisition, a field in which the olddichotomy seems particularly entrenched.

As I hope to clarify in what follows, my aimin the book was not to actively refute nativismor, indeed, empiricism, but rather to present apositive case for constructivist accounts of neu-rocognitive development. As discussed at somelength in Chapter 1 of DCN, constructivism

does not equate with empiricism and is as much‘anti-empiricist’ as it is ‘anti-nativist’. Specifi-cally, it is an orthogonal dimension of develop-mental theory in which the aim is not toidentify the source of pre-existing informationin the genome or in the environment, but ratherto unravel the mechanisms of interaction thatgenerate change from an existing structure to anewer one. In other words, constructivism isabout the process of change (see also Karmiloff-Smith, 1992; Siegler and Munakata, 1993). Thus,I agree with Stiles that ‘ . . . in specifying theprocess of interaction, the dualism of nature–nurture vanishes’.

ECHOES OF THE PAST

Aslin points out that while I share Piaget’smetatheory of constructivism, the viewpoint ex-pressed in DCN necessarily differs from Piagetdue to the incorporation of evidence from neu-robiology. Specifically, neurocognitive develop-ment is a non-linear and inexact process thatoccurs within a sea of noise; it is not logical, butbio-logical. Related to this is Stiles’s emphasison probabilistic epigenesis, the bi-directional in-terplay between levels, as an important founda-tion of DCN. As Stiles notes, this way ofthinking about development does not originatewith me, but has a long history including fig-ures such as Gottlieb and Waddington.

Colombo correctly identifies another strongroot of DCN as being in the comparative, phys-iological and ethological analyses that com-posed traditional developmental psychology,but which is now often referred to as develop-mental psychobiology. I agree that developmen-tal cognitive neuroscience is to some extent areturn to these more traditional brain and be-

* Correspondence to: Department of Psychology, BirkbeckCollege, University of London, Malet Street, London WC1E,UK. E-mail: [email protected]

Contract grant sponsor: UK Medical Research CouncilContract grant sponsor: EC Biomed IVContract grant sponsor: Human Frontiers Science Founda-tion

CCC 1057–3593/98/030163-07$17.50© 1998 John Wiley & Sons, Ltd.

Received 1 April 1998Accepted 1 April 1998

M.H. Johnson164

haviour approaches. However, a distinctive ad-ditional feature is the central importance ofcognition in the form of the emergence, expan-sion and manipulation of representations. Weshould no longer be content with identifyingneural correlates of behavioural change, butwhere possible should focus our developmentalanalysis on the intermediate neurocomputa-tional and cognitive levels.

AIMS AND SCOPE OF THE BOOK

Several reviewers point out that my book pre-sents just the ‘tip of the iceberg’ (Colombo) andis not a comprehensive review of the field. Ifully agree. While the contents of the book maynot entirely live up to its main title, I hope thatit lives up to its subtitle—An Introduction. Asstated in the Preface of DCN, the book wasdesigned to introduce the advanced student tothe new field, and to inspire them into joiningit. It was not intended to serve as a referencevolume for experts. Further, I suspect that afully comprehensive review of the field is bestdone in a format other than a single-authoredmonograph. For these reasons, I have chosennot to respond to reviewers who pointed outgreater depth and/or complexity to some of thetopics covered, on the grounds that I judgedsuch detailed accounts to be inappropriate for afirst introduction to the field. For example,while Richards correctly points out a number ofomissions and simplifications in two sections ofChapter 3 (on visual orienting and visual atten-tion), other reviewers intimated that some of thepage space used for these topics would havebeen better allocated to other domains, such asMemory. Every researcher reading the bookwill probably wish for more coverage of theirown topic, and every teacher will have theirown view as to the balance of the coverage.

One of my guiding principles for selectingmaterial to present was that it should specifi-cally illustrate an attempt to relate brain devel-opment to an aspect of cognitive development.This means that large swathes of the cognitivedevelopment literature on topics such as atten-tion (Richards), and language acquisition (John-son and Jusczyk) were omitted. In addition, dueto the relative youth of the field, some of thematerial included as being illustrative of waysto relate brain development to cognition is bothspeculative and controversial.

MISCONCEPTIONS ANDCLARIFICATIONS

Three of the reviews suggest that I deny theexistence of innate representations in the brain.I can only apologise for being insufficientlyclear on this point in my precis of DCN, but inthe book itself I hope it is clearer that I hypoth-esise a lack of innate representations within thecerebral neocortex, and not in the brain as awhole. Indeed, as many readers are aware, Ihave been at the forefront of demonstrating theexistence of such representations (mediated bysubcortical structures) in newborn infants andnewly hatched chicks (see Chapter 4 of DCN),and, indeed, have previously been accused ofbeing a ‘rampant nativist’ for doing so! To dealwith the specific point of whether there areinnate representations, I fully agree with John-son and Jusczyk that there are. In fact, I wouldgo further than them in stating that there isindeed strong evidence for innate visual repre-sentations. However, I suggest that these arecommonly mediated by subcortical rather thancortical systems. They lament my omission ofneonatal imitation (as supposedly a clear exam-ple of representational innateness), but to myknowledge the only speculation on the neuralbasis of this ability was Johnson and Morton(1991) observation that it has the same develop-mental time course as many newborn sensori-motor reflexes, and is thus likely to besubcortical—at least in its initial manifestationsover the first few days of life. In addition, asJohnson and Jusczyk are doubtless aware, thereis still great controversy about whether cogni-tive interpretations of imitation are required, orwhether simpler reflexive accounts will actuallysuffice.

A second strand to the Johnson and Jusczykcritique is that I failed to report evidence forlanguage-related innate representations whichmay arise after birth. I fully acknowledge thatmy coverage of the language literature washighly selective, partly due to my expressedaim of focusing on areas in which attempts hadbeen made to relate cognition to brain develop-ment. The specific omissions concerned evi-dence that infants and children go ‘beyond theinformation given’ during spoken and signedlanguage, and recent evidence about the speechsegmenting and processing capacities of infants8–9 months of age. Presumably, these lines of

© 1998 John Wiley & Sons, Ltd. Early Dev. Parent. 7: 163–169 (1998)

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evidence are taken by these commentators to besupportive of late emerging innate representa-tions. My own view is that this evidence is alsoentirely consistent with a constructivist (not em-piricist) view, the essence of which is that newlevels of organisation or representation are con-structed through the interaction between genesand environment. By this view it is not at allsurprising that infants are capable of going be-yond the (environmental) information given—itis, in fact, a feature common to all of biologicaldevelopment, and is in no way unique to lan-guage acquisition. For example, the same em-bryonic tissue that gives rise to beak formationin one context, can give rise to teeth in another(see p. 7 of DCN). Even in this simple case it ispointless to attribute the emergence of the newstructure to genes or environment—a properdevelopmental analysis has to include an ac-count of the interaction between them.

At this point, I should perhaps emphasisethat the conclusions about brain developmentpresented in DCN, while perhaps surprising tosome cognitive psychologists, are not as contro-versial as a couple of the reviews imply. Forexample, in a very recent review of brain devel-opment, Nelson and Bloom (1997) state ‘Anunfortunate misconception of developmentalneurobiology is that most aspects of brain de-velopment during the pre- and immediate post-natal periods reflect rigidly deterministic,genetic programs that are implemented at dif-ferent points in time . . . this view is inappropri-ate for even the very earliest stages of braindevelopment.’ (p. 979).

Aslin also interpreted my argument in DCNas eschewing innate representations completely,and he thus reasonably concludes that I believethat subcortical structures cannot support‘proper’ representations. To clarify, my in-tended claim was that there was currently littleevidence for representational innateness withinthe cerebral cortex (see below for further discus-sion of this issue). By contrast, I believe thatthere is strong evidence (some of it collected inmy own lab) for representational innateness insubcortical structures. I would add that while Ido believe that subcortical structures can sup-port proper representations, I agree with othersthat the cerebral cortex has evolved primarily asa machine for the manipulation of representa-tions.

The third commentator who interpreted DCNas arguing for a complete lack of innate repre-sentations was Marcus. The essence of his argu-ment is that I have presented a straw man in thesense that no ‘serious nativist’ holds that thereare neural networks in the newborn’s brain inwhich ‘ . . . the patterns and strengths of linksbetween nodes (neurons) are innate . . . ’ and hequotes from Pinker (1997) to this effect. How-ever, as recently as Pinker (1994), we have adetailed description of the sense in which heenvisages that a (connectionist) neural networkwould be prepared for language within thenewborn brain. In this analysis, a particular andspecific pattern of connectivity between a num-ber of different groups of nodes (neurons)‘ . . . corresponds to the child innately ‘expect-ing’ there to be, say, suffixes for persons, num-bers, tenses, and aspects, as well as possibleirregular words for those combinations . . . ’(Pinker, 1994, p. 320). To his credit, Pinker ofcourse also allows for some fine tuning of thenetwork through experience to make it sensitiveto a particular language. However, the point isthat the original state of the network in terms ofits patterns of connectivity is specific to languageacquisition, and the same initial pattern of con-nectivity could not develop into one suitable forface processing or planning to make a cup oftea; the plasticity within the network is confinedto possible human languages. In contrast, inDCN I have suggested that at some point dur-ing development many of the areas of cerebralcortex that are involved in higher cognitivefunction share a very similar overall pattern ofintrinsic connectivity, and that it is onlythrough activity-dependent processes, in somecases driven by sensory and motor experience,in collaboration with extrinsic patterns of con-nectivity (to and from subcortical regions), thatdomain specific differences in intrinsic connec-tivity arise. Pinker’s analysis is, I would sug-gest, considerably more sophisticated thanthose from some other nativists and I concludethat representational nativism is not quite thestraw man that Marcus suggests.

REPRESENTATIONAL INNATENESSAND THE CORTEX

In DCN I suggested that there was currentlylittle evidence for innate representations within


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the cortex, but that representational specificitycommonly arises through a combination of sev-eral constraints, both intrinsic and extrinsic tothe cerebral cortex. Further amplification andmodification of this view is required in the lightof comments from the reviewers and recentevidence from developmental neurobiology.The three issues on which I will expand are (i)the recent evidence on cortical differentiationarising through spontaneous patterns of neuralactivity, (ii) the importance of extrinsic patternsof connectivity (to and from the cortex) in con-straining the type of representations thatemerge in a given region, and (iii) increasedemphasis on the graded nature of the transitionfrom pre- to postnatal activity-dependentresponses.

Marcus suggests that I neglected the recentwork of Shatz and colleagues demonstratingthat prenatal spontaneous activity could play animportant structuring role in cortical differentia-tion1. What are the implications of this recentline of evidence for the conclusions reached inDCN? In Chapter 2 I introduced a distinctionbetween the Protomap and Protocortex hy-potheses of the origins of cortical specialisation.Briefly, the former view hypothesised prespeci-fication of cortical areas through intrinsicmolecular markers or through prespecificationof the proliferative zone (which gives birth tocortical cells). By contrast, the Protocortex viewwas described as ‘The different areas of thecortex arise out of an undifferentiated protocor-tex that is divided up into specialized areas as aresult of input through projections from thethalamus . . . ’. Thus, the essence of the Proto-cortex view is that cortical differentiation arisesthrough activity-dependent processes. As notedby Marcus, recent evidence indicates that spon-taneous activity during prenatal developmentcan play a role in structuring neural circuits. Forexample, Shatz and colleagues have identifiedpatterns of spontaneous firing in retinal cellsthat project to the Lateral Geniculate Nucleus(LGN) (see Katz and Shatz, 1996). These wavesof spontaneous activity probably play an impor-tant role in the establishment and refinement ofretinotopic maps in the LGN, and possibly alsoeventually in the differentiation of occular dom-inance columns within visual cortex. Other as-pects of the structure of the primary visualcortex, however, such as orientation tuning andcolumns, may be dependent on waves of spon-

taneous firing within the cortex (probably prop-agated via gap junctions, and not synapses). Forexample, Weliky and Katz (1997) used artificialstimulation to modify the spontaneous firinginput to primary visual cortex in ferret kitsbefore the formation of orientation selectivemaps. They found that although orientation se-lectivity in these stimulated animals was signifi-cantly weaker than normal, the overallorganisation of orientation across the visual cor-tex was not altered. While there are severalalternative explanations of this result, the mostplausible is that the intrinsic basic architectureof cortex, with waves of gap-junction mediatedfiring, ensure that certain spatial clustering pat-terns will emerge in cortex even after significantalterations to the normal patterns of electricalinputs.

While patterns of spontaneous firing proba-bly contribute to some degree of prenatal struc-turing of primary visual cortex, sensoryexperience-driven patterns of neuronal activityare also required. For example, Crair et al. (1998)observed that while cortical maps for orienta-tion and occular dominance columns in catsinitially develop in the absence of experience,these naive maps are powerfully dominated bythe contralateral eye. Visual experience is re-quired for the normal patterns of equal domi-nance. Further, without such experience,responses deteriorate and neurons cease to beselective at all after a period.

Two other considerations suggest that weshould be cautious about the generality of thesefindings, and that we need to wait for furtherevidence before strong conclusions can bedrawn. The first of these concerns the fact thatmost of the experiments so far are centred onthe primary visual cortex. As noted in DCN (p.47) the primary visual cortex, along with en-torhinal cortex, is an area in which there is clearevidence for prenatal differentiation in pri-mates. In addition, in the visual domain there isclear differentiation between spontaneous activ-ity that precedes eye opening, and experiencewhich occurs after the eyes open. This differ-ence is unlikely to be so clear in the auditorydomain, where it is known that human infantsprocess sounds from outside the womb (e.g.Moon et al., 1993).

The second consideration concerns speciesdifferences. While some mammals open theireyes with an already partially structured visual


Looking Ahead 167

cortex, it is less clear that this is the case inhuman infants who have a far more prolongedcourse of postnatal brain development. Indeed,as described in Chapter 3 of DCN, behaviouralevidence from human infants indicates that as-pects of binocular vision develop around theend of the fourth month, providing ample op-portunity for visual experience to contribute.Further, neuroanatomical evidence from post-mortem tissue indicates that the projectionsfrom the LGN may be only just entering thecortex at the time of birth (Conel, 1939–1967;Johnson, 1990), and have probably not yetreached their adult termination sites in layer 4.If these neuroanatomical observations are con-firmed, it suggests the possibility that humanvisual cortex may be developmentally delayedto favour postnatal experience.

Finally, it should be noted that the rodentexperiments of Sur and colleagues (see Sur,1993, and Section 2.5 of DCN), indicate thateven if visual cortex is replaced by corticaltissue from another region early in develop-ment, many of the same structures will arisethrough activity-dependent processes. In otherwords, the intrinsic and extrinsic spontaneousactivity that contributes to the prenatal structur-ing of visual cortex, could have similar effectson cortical tissue with different developmentalorigins. To the extent that these transplant find-ings can be extended to humans it suggests thatany piece of neocortex has the tendency toproduce certain types of structure, such as clus-tered and topographic representations, giveneven coarsely structured noise as input. Thiscorresponds to findings from computationalneurobiology studies (e.g. Oliver et al., 1996).

To summarise, activity-dependent differentia-tion within some regions of cortex is probablyinitially due to spontaneous activity, but latterlymay be due to experience. If these effects occurin domains other than vision, the transition islikely to be graded, with similar mechanisms ofplasticity operating at the cortical level. Due tothe exceptionally prolonged period of postnatalcortical development in human infants, corticaldifferentiation in our species is probably moresensitive to experience than in most other mam-mals. Thus, while there may be some degree ofcortical differentiation at birth, at least forhigher cognitive functions such specialisation ofintrinsic circuitry is often likely to occur ininteraction with the postnatal environment.

It is important to note that the role of neuralactivity in cortical differentiation and specialisa-tion significantly weakens and complexifies therelation between genes and adult brain struc-ture. Marcus states ‘all that is required forsomething to be innate is that it does not de-pend on information from the senses’. This defi-nition superficially corresponds to thatprovided in DCN (p. 8). However, it is impor-tant to stress that the DCN definition of innaterefers to the level of the interaction betweengenes and environment (cellular interactionswithin the organism), and not to the source ofthe information. In other words, this definitionof innate in no way equates with a geneticblueprint of any kind. While this difference inemphasis may appear subtle, I believe that ithas two related consequences.

First, while ‘serious nativists’ such as Marcusacknowledge that there are very complex cellu-lar interactions (including the effects of noisyand non-linear spontaneous activity) that con-tribute to the end state they wish to call innate,unfortunately others who read their work stillcommonly lapse into the ‘straw man’ version ofnativism, i.e. the assumption that ‘innate’equates with ‘genetic’ (be it a ‘blueprint’ or a‘recipe’). One example of this is the search forgenes that ‘code for’ aspects of grammar, suchas the widely publicised claims of a set of genesfor the past tense (Gopnik and Crago, 1991;Pinker, 1991; Van der Lely, 1994; Elman et al.,1996).

The other problem with adopting a ‘seriousnativist’ approach to development is that ittends to change the emphasis for empirical re-search. Attempting to discover whether or not acomponent of cognition is innate is often thegoal of a nativist research program. As is evi-dent to readers of DCN, there are many inter-estingly different ways for a component ofcognition to emerge even within the categoryinnate (as defined in DCN). I believe that thestudy of development should include empiricaland theoretical investigation of these differentdevelopmental pathways. This difference in em-phasis may also turn out to be a differencebetween cognitive science and linguistics on theone hand, and developmental cognitive neuro-science on the other.

I am entirely in agreement with de Schonen’selegant descriptions of mechanisms that couldunderlie and limit recovery of function after


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early cortical damage. Her suggestion thatsome instances of an apparent increasing local-isation of function can be accounted for interms of more interaction between structuresbeing required during the acquisition of a taskis well taken. She rightly points out that differ-ent domains of cognition appear to have differ-ent developmental timetables of specialisation,and therefore may show differential capacityfor recovery of function following early braindamage. It is also worth reiterating her viewsthat the extrinsic connections of areas of cor-tex—such as inputs from sensory systems andoutputs to other areas such as the hippocam-pus—also constrain the range of areas that cansupport a function. For example, regions thatbecome recruited for face processing probablyhave to be located somewhere on the ‘what’(ventral) pathway of visual processing, simplyby virtue of the structures on the pathway hav-ing interaction with both visual processing andthe hippocampus.

LOOKING AHEAD: TESTING SPECIFICINTERACTIONIST THEORIES

While several of the reviewers have taken issuewith particular statements or hypotheses inDCN, I believe that one of its main values liesin helping to provide a framework withinwhich specific hypotheses can be advancedand tested. In this regard neural network mod-elling will be important. Everyone agrees withMarcus that current connectionist models aresimplistic and first generation. However, theyare already providing a useful frameworkwithin which more sophisticated debates aboutdevelopmental processes are taking place. In-deed, it is interesting to note that several ‘seri-ous nativists’ have begun to use such modelsto formalise their own hypotheses about devel-opment, or the lack of it, in neurocognitivesystems (e.g. Pinker, 1994; Marcus, 1997).

An excellent example of how neural networkmodelling could be used to crystallise the dif-ferences between plausible theories of corticalspecificity is provided in Mareschal’s reviewwhere he compares two models of the devel-opment of object permanence abilities. One ofthese models (Mareschal et al., 1995) starts withsome structured connection pathways (the‘what’ and ‘where’ pathways) while the other

does not (Munakata et al., 1997). Close com-parison between the extent to which the mod-els can account for a range of behaviouralphenomenon should allow us to refine and/orreject particular models. In the future it is to behoped that evidence from brain developmentand neuroimaging could also be used to differ-entiate such models. There are exciting timesahead.

ACKNOWLEDGEMENTS

I thank John Morton and Annette Karmiloff-Smith for comments on an earlier version ofthis reply, and the UK Medical Research Coun-cil, the EC, and the Human Frontiers ScienceFoundation for financial support.

Notes

1. To deal with the suggestion that I deliber-ately neglected this work, this line of researchis very new and some key papers had yet toappear when DCN was completed in early1996. In reviews that I have written since thepublication of the key paper by Katz andShatz (1996) I have included extensive discus-sion of this work (Johnson, 1997, 1998a,b,c).Contrary to Marcus’s perception of myviews, I find this new line of research to bean exciting empirical advance entirely consis-tent with a contructivist view of neuro-development.

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developmental cognitive neuroscience: looking ahead

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