Species comparative studies and cognitive development

Species comparative studies andcognitive developmentJuan-Carlos Gomez

Scottish Primate Research Group, School of Psychology, University of St Andrews, St Andrews, Fife KY15 9JU, UK

The comparative study of infant development and

animal cognition brings to cognitive science the promise

of insights into the nature and origins of cognitive skills.

In this article, I review a recent wave of comparative

studies conducted with similar methodologies and

similar theoretical frameworks on how two core com-

ponents of human cognition – object permanence and

gaze following – develop in different species. These

comparative findings call for an integration of current

competing accounts of developmental change. They

further suggest that evolution has produced develop-

mental devices capable at the same time of preserving

core adaptive components, and opening themselves up

to further adaptive change, not only in interaction with

the external environment, but also in interaction with

other co-developing cognitive systems.

Dog

Gorilla Human

Macaque

Invisibledisplacement

No A-B error

A-B Error

Introduction

The comparative study of infant development and animalcognition brings to cognitive science the promise ofinsights into the nature of cognitive skills by studyingtheir origins in different genetic time scales [1–3].

Development is a key mechanism of evolution – anarena for the interplay of phylogenetic and ontogeneticavenues of adaptation – and therefore the best way tofulfill this explanatory promise is to combine develop-mental and evolutionary approaches in comparativedevelopmental studies [1–6]. In this article I explore twodomains in which comparative studies of developmentwith comparable methodologies and theoretical frame-works have been conducted in the past few years: theability to track and locate objects in space and the abilityto find objects through the gaze of others. Both exemplifythe growing strength of combining developmental andevolutionary perspectives in understanding the corebuilding blocks of cognition.

TRENDS in Cognitive Sciences

4 8 12 16Age (months)

Figure 1. The last three steps in the development of the ability to retrieve objects

(Piagetian object permanence: Stage 4, retrieval with A-not-B error; Stage 5,

retrieval without A-not-B error but failure with invisible displacement; Stage 6,

invisible displacement passed). Different primate species follow exactly the same

developmental steps but at different developmental rates. Apes are slightly faster

than humans, and monkeys develop 3 to 4 times faster (but might never reach the

Understanding the invisible life of objects

Finding and keeping track of objects such as food,conspecifics or predators is a function shared acrossvirtually all animal species [7]. Developmental psycholo-gists found that object search skills – Piagetian ‘objectpermanence’ – emerge in human infants through a fixedseries of steps with characteristic transitional errors [8,9].Before the age of 7 or 8 months, infants fail to retrieve an

Corresponding author: Gomez, J.-C. ([email protected]).Available online 1 February 2005

www.sciencedirect.com 1364-6613/$ - see front matter Q 2005 Elsevier Ltd. All rights reserved

object completely hidden from their view (Stages 1–3).After 8 months, they retrieve hidden objects, but if anobject successfully retrieved from location A is then movedto location B, they search again in location A, despitehaving clearly seen that the object was now placed in B(Stage 4). This so-called ‘A-not-B error’ is overcome at11–12 months, when infants systematically search in thelast place they saw the object disappear (Stage 5). However,at this age infants have problems with ‘invisible displace-ments’. If the experimenter hides an object with his handclosed, then until 18 months of age (Stage 6), infantssearch only in the hand, without realizing that the objectwas left behind.

Object permanence in animals

Comparative research shows that many species developPiagetian object permanence skills in exactly the samesequence as human infants [1,2,10] but at different speeds(Figure 1). Apes are slightly faster than humans in allsteps. Monkey species develop about three to four timesfaster than humans [11,12], but might fail to masterinvisible displacements [1,2,10], although controversypersists over this point [13,14]. Non-primate speciesdevelop object permanence even faster [10]. Dogs andcats reach Stage-5 performance in only a couple of months,but interestingly, in contrast to all primate species studied

Review TRENDS in Cognitive Sciences Vol.9 No.3 March 2005

last step). Other mammals, like dogs and cats, develop even faster, but skip the

characteristic transitional error (A-not-B) of Stage 4 and do not reach invisible

displacements. (Based on data reviewed in [2]).

. doi:10.1016/j.tics.2005.01.004

http://www.sciencedirect.com


Standard task

Prepotent gravity location removed(b)

(a)

Figure 2. (a) When an object is visibly dropped into the tube, adult rhesus monkeys

and children under 3 years old search for the object in the location just under the

release point committing what is known as a ‘gravity error’. It has been

hypothesized that this error could be caused by the inability to inhibit a prepotent

tendency to search straight under the release point of falling objects (a ‘gravity

bias’), which could override correct knowledge about the location of the object.

(b) However, when the possibility of finding the object in the gravity location is

eliminated from the beginning, children and monkeys search at random,

suggesting a lack of understanding of how tubes work.

Review TRENDS in Cognitive Sciences Vol.9 No.3 March 2005 119

so far, they skip the phase of committing A-not-B errors.Contrary to initial reports [10], they also fail to reach theinvisible displacements phase. This developmental diver-gence suggests that the cognitive basis of their perform-ance in object retrieval tasks might be fundamentallydifferent to primates [2,15].

Object permanence is therefore a core universal ofprimate cognition not only in terms of the basic compe-tence achieved, but also in terms of its pattern ofemergence in ontogeny. Of special interest is the apparentuniversality of the A-not-B error phase and the elasticityof the developmental pattern across species.

Representations or executive skills?

The traditional interpretation was that object permanencereflects the progressive acquisition of the ability torepresent (i.e. mentally encode) the hidden objects [8,9].Contemporary research suggests, however, that complexknowledge about objects – including their existence whenthey are out of sight –is present in infants by 3–4 monthsof age before manual search skills develop [16]. Such earlyknowledge is revealed by infants’ increased attention toevents that violate principles of object permanence (e.g. anobject failing to re-appear where it was placed) [9].

This implies that human infants might have a develop-mental mismatch between object knowledge and its usein action. Object permanence might be an index not ofrepresentational change, but of the growth of an executiveability to use knowledge that already exists.

This idea could help to explain the enigmatic A-not-Berror and the developmental elasticity across species.Within their own developmental spans, rhesus monkeysand human infants go through the A-not-B error phase inidentical microgenetic detail [12]. A proposal is thatduring this phase both species develop stronger executiveskills (i.e. skills to organize goal-directed action effectively,such as working memory and inhibition) based on thematuration of the prefrontal cortex [11]. This maturationoccurs at different rates in each species, so that rhesusmonkeys would have executive access to their existingobject representations earlier than humans, therebyshowing earlier object permanence development.

The executive hypothesis, therefore, is consonant withthe looking-time findings with human babies and seemsable to account for interspecies similarities and differ-ences. However, a crucial piece of evidence for this view iswhether mismatches between looking and reachingmeasures of object knowledge can be found in non-humans.

Knowledge/action mismatches in non-humans

We do not know yet if infant monkeys, like human infants,show a developmental precedence in looking measure-ments of Piagetian object permanence or, having anearlier maturation of executive skills, whether theirperception and action performances unfold in synchrony.However, looking/reaching mismatches have beenreported in adult macaque monkeys in some advancedtasks of object permanence.

For example, both human children (aged just under3 years) and adult monkeys show a gravity bias in their

www.sciencedirect.com

understanding of invisible displacements involving fallingobjects [7,17,18]. They consistently tend to search for anobject on the ground just under the place where it fellwhen the falling trajectory is occluded by a screen. Thisgravity bias is so powerful that they search on the groundeven when there are unavoidable physical constraintsthat prevent the objects from falling straight down – forexample, when a solid board is blocking the verticaltrajectory of the object, or the object is dropped into anopaque tube that goes diagonally to a lateral location(Figure 2). They can repeat this error perseveratively, thatis, without learning from repeated negative experience.Human children eventually overcome this gravity bias(at 3 years) and take into account the physical constraints,but adult rhesus and Tamarin monkeys continue commit-ting the error [19].

A proposed explanation for the gravity bias, consonantwith the executive hypothesis of object permanence, isthat the error is induced by a failure to inhibit theprepotent expectation that objects fall straight down –which would be hardwired as a sort of ‘modular macro’ inprimate, and maybe other vertebrate brains [19,20].Indeed, in a similar task where the object is not dropped,but is rolled into tubes lying horizontally, the gravity biasdisappears (even if performance is not perfect) [19].Moreover, when tested with looking time paradigms,


Box 1. Developmental interplay between number systems

The interaction between cognitive systems can produce new

cognitive skills both in development and evolution. For example,

looking time and manual search provide converging evidence that

both adult monkeys and human infants share two systems of

number representation – one for approximate values of large sets,

another for exact values of small sets (up to 3 or 4) [3,69]. However,

children, but not monkeys, eventually develop their number systems

in the cognitive context of natural language acquisition. Using labels

for numbers and verbal counting routines could decisively change

how these phylogenetically old systems grow into what will

eventually become the higher-order system of natural numbers [3].

The presumed existence of these systems in chimpanzees could

explain the apparent success of attempts to teach them rudimentary

counting systems and labels for numerals [70].


adult monkeys [18] and young human children whocommit the gravity error show surprise when objectsappear in the gravity-congruent, impossible location.Their perceptual system is somehow aware that the objectshould not be there, whereas their action system isstubbornly convinced that it must be.

The executive hypothesis assumes that 3-year-oldchildren grow out of this contradiction [21], not becausethey acquire new knowledge about the physical con-straints affecting gravity, but because their brains developthe power to inhibit the inappropriate gravity response,thereby liberating their existing knowledge. By contrast,monkeys (who reveal a similar correct knowledge ofphysical constraints in some looking tasks) never acquirethe requisite inhibitory skills and are condemned byevolution to keep this cognitive dissociation [19,22].

A similar permanent dissociation in understandingobject support relations might exist in chimpanzees. Theyidentify impossible support relations in looking tasks [23],but fail to do so in active problem solving [24].

In human infants, knowing/acting mismatches can beunderstood as a transitory developmental phenomenonthat occurs in the process of assembling a complexcognitive system. However, in adult primates, the senseof a permanent mismatch between knowledge and actionis not clear. Without being translated into action, how canknowledge exert an adaptive impact upon individuals andtherefore evolve by natural selection?


Obj permanence

Stick use

4 8 16 22 24Age in months

Macaque

Gorilla Human

?

28

Constructsdetour bridge

Not present

Uses existingdetour

Support/stringuse

12

Figure 3. The cognitive context in which object permanence develops differs among

primate species. For example, effective use of sticks as a hand extension for raking

objects occurs very early in human ontogeny (shortly after developing object

permanence for visible displacements), but much later in gorilla and chimpanzee

ontogeny, and rarely, if ever, even in adult macaque monkeys (unless specific

training is given). By contrast, use of objects like boxes or poles to prolong

locomotor reach occurs earlier in gorilla than in human ontogeny. (Based on data

reviewed in [2]).

Representational accounts of knowledge/action

mismatches

One possible explanation is that the knowledge revealedby looking-time methods is not the same knowledge usedfor successful action [25,26]. In an adaptation of thediagonal tubes task (Figure 2), when given the benefit ofseeing that the object cannot be directly under its releasepoint (because the space underneath is visibly empty),macaque monkeys and young children – unable now togive the gravity response – still fail to choose the correctlocation (Southgate and Gomez, unpublished). No hiddenknowledge for successful action is liberated by removingthe prepotent response, as executive accounts predict[19,22]. Adult monkeys and younger children do notunderstand well how tubes constrain object trajectories,whereas older children must have acquired a betterunderstanding of tubes as physical devices.

A recent developmental theory suggests that looking-time data reflect ‘weak’ object representations, whereassuccessful search requires ‘stronger’ representations [25].This implies a process of graded representational changeduring ontogeny. A similar notion could be applied tophylogenetic comparison. Some species might only attainweak representations in some domains (e.g. invisiblephysical constraints), which they fail to develop into full-blown, strong versions. Weak representations might be aby-product of other processes that do exert an adaptiveimpact on behavior. However, the question remains ofwhat is required to develop weak into strongrepresentations.


Global cognitive systems

Other developmental approaches emphasize changes inthe overall dynamics of behavioral systems, rather thanchanges in individual components, as being responsiblefor development [27]. What matters here is the globalinterplay among subsystems (see Box 1). If we take thisview to phylogeny, core cognitive components like objectpermanence can be seen as developing in differentcognitive contexts in different species.

For example, although gorillas and chimpanzeesdevelop object permanence following a similar scheduleto humans, they are slower at developing tool-use as anextension for grasping (e.g. raking with a stick) andfaster with tool use as an extension of locomotor reach(e.g. moving a box to use as a ladder) (Figure 3). Mostmonkey species never develop either type of tool use oronly do so as adults. This might put children on the trackof coordinating object search with understanding mech-anical interaction among objects, much earlier than apes.Such differences in timing (‘heterochronies’) in the



ontogeny of cognitive systems across different domainscould play a major role in explaining cognitive differencesamong primate species [1,28].

Integrating developmental accounts

Different comparative findings about the core cognitiveskill of object permanence appear to favor differenttheoretical accounts of developmental change. However,a global perspective suggests that the best option is anintegration of rival theories. The growth of executiveprocesses like inhibition and working memory mightenable the dynamic coordination of systems of perceptionand action. Such coordination could in turn be one of thefactors fostering the conversion of weak into strongrepresentations. Complex object cognition results fromdevelopmental interactions among a variety of behavioraland representational systems.

Finding objects with the eyes of others

We have discussed the ability to track objects individually,by processing information provided by the physicalenvironment. However, we can also find objects usingsocial cues – following the gaze of others.

Gaze following is part of a set of skills called ‘jointattention’ (Box 2). As recently as 8 years ago it was notknown whether gaze following was a uniquely humanskill. Now, several studies have firmly established thatmonkeys and apes will spontaneously look in the samedirection as a conspecific or a human [29,30], not only inresponse to live models, but also with the limitedinformation provided by a photograph [31–33]. Gazefollowing is a prevalent primate adaptation, but is notexclusive to primates: it has been reported in domesticdogs [34], domestic goats [35], captive corvids [36], andcaptive dolphins [37]. Gaze following responses are there-fore widespread among distantly related animal species.

Development of gaze following

Human infants start turning to look in the same directionas other people at around 6 months. At 12 months, theyconsistently look at the correct object, and at 18 monthsthey follow gaze even behind themselves [38]. The origins

Box 2. Joint attention

Joint attention is the ability to coordinate one’s attention to a target

with another person. It involves several different skills that can work

separately or in combination [38,71]. Following another’s gaze could

alert an individual to the presence of relevant targets in the

environment. Detecting gaze upon ourselves might alert us that we

are to become the target of an impending action. Combining both

skills – gaze following and eye contact – gives rise to intentional

referential communication; for example, I call your attention to me to

ensure that you follow my gaze to the predator I have detected [2].

Referential communication can be enhanced with pointing (typically

human, but some varieties of pointing also occur in chimpanzees

and other primates) [72]. Checking other’s attention might also

produce social referencing (learning about the emotional valence of

an object from the facial expression of someone who is looking at it)

or facilitate word-meaning learning [73]. Developmental and com-

parative researchers agree that joint attention skills might represent

the earliest manifestations of theory of mind both in ontogeny and

phylogeny [2,74].


of gaze following can be traced to newborns, whodistinguish between gaze directed at them and elsewhere,and preferentially attend to direct gaze [39]. By 4 months,humans orient their saccades in the same direction asaverted faces if their attention is first engaged with directgaze [40]. Gaze following might emerge out of aninteraction between an innate preference for direct gazeand more general mechanisms of attentional orientationto movement activated when the model’s eyes turnsideways [40–41].

Few developmental studies exist about gaze followingin non-humans. Laboratory-reared pigtailed macaquesfollow gaze in response to head and eye movements ofhumans well after infancy (2–4 years), and only adultsfollow eye movements alone [42]. However, rhesusmacaques housed in larger social groups follow humangaze by 6 months of age [43]. Similar to human babies,2-month-old chimpanzees and 1-month-old gibbons dis-criminate between direct and averted gaze, preferentiallyattending to faces that look directly at them [44–45].Although one report found gaze following in chimpanzeesonly at 3–4 years [43], one chimpanzee baby followed headmovements of humans towards objects at 10 months, eyemovements at 13 months [46], and looked behind himselfat 20 months [47], which closely resembles humandevelopment.

Although more comparative developmental studies areneeded, primate gaze following appears to be the result ofa developmental interplay between initial predispositionsto process gaze stimuli and experience. This basicdevelopmental mechanism is probably shared by apesand humans, but a core gaze-following skill is eitherphylogenetically older or independently selected in differ-ent species [48].

A functional dissociation

There are two main methods to test gaze following skills(Figure 4). One is to measure if animals spontaneouslylook in the same direction as a model; the second is toallow them to use gaze as a cue to a hidden object (e.g. foodin a box). Non-human primates consistently do the first,but find the second unexpectedly difficult [30,49]. In choicetasks, most primates fail to use human gaze or evenpointing gestures to select the container with hidden food.Children solve these problems only at around 3 years ofage [50], although they show spontaneous gaze followingmuch earlier.

A possible explanation of this paradox (to some extentreminiscent of the looking/reaching dissociations dis-cussed in the previous section) is that gaze following innon-humans is just a tendency to look in the samedirection as a model, but without the mentalistic repre-sentations that humans superimpose on gaze [51]; that is,without attributing intentions or knowledge. By contrast,in human children the gaze-following mechanisms sharedwith other primates would become developmentallyinterlocked with mechanisms of mentalistic attribution,widening their functions.

In contrast to primates, domestic dogs perform excel-lently in object-choice paradigms. They reliably andaccurately follow gaze and pointing cues to locate hidden



Do you look in the same direction as the model?

Under which box will you search for the hidden object?

(a)

(b)

Figure 4. There are two main methods of assessing gaze following in animals. The

first (a) consists of exposing animals to a model looking in a particular direction

(with or without a possible target object; in this example, the yellow bar) and

recording whether or not they spontaneously look in the same direction. A large

variety of animal species show gaze following with this method. (b) The second

method consists of assessing if an animal can use gaze or other social cues from the

model to locate an object that has been previously hidden in one of two (or more)

locations. Primates, including apes, find this second method more challenging. By

contrast, dogs show excellent performance.


objects [52–55]. Dogs’ superior performance might be dueto their rearing by humans. The minority of apes who dorelatively well in object-choice tasks typically had exten-sive human rearing [30]. However, when similarly rearedby humans, wolves (the closest evolutionary relatives ofdomestic dogs) fail to follow human social cues [56,57].Humans might have artificially selected dogs with geneticpredispositions to learn to respond to human cues [34].Privileged attention to faces might be one such predis-position (dogs, but not wolves, typically look back at theirowners’ faces in problem situations) [34,57]. But goodperformance in choice tests might require more than suchpredispositions.

Motives to follow gaze

Chimpanzee performance in object choice is facilitated byseveral factors, such as experience with humans andcombining sounds with gaze and pointing [30,49]. But themost effective facilitator is changing the motivationaldomain of the task. Chimpanzees choose correctly when ahuman competitor looks and reaches to the baited box as iftryingtogainthe reward, but fail whena cooperative humanpoints to show them the baited box [58]. This findingconverges with other evidence that in competitive situationschimpanzees use conspecifics’ cues of attention [59,60]. Onepossible explanation is that chimpanzees don’t understandthe communicative intention to show something [30],whereas they do understand the intention to reach a target.However, competitive contexts also increase performance insimple discriminative tasks involving no social cues, whichsuggests that competition might be a domain-generalperformance enhancer for chimpanzees [58].

Dogs and human infants might bring to the task oflearning to follow attentional cues, not only specific


attentional and processing biases, but also a distinctiveset of cooperative motives [58,34]. Chimpanzees mighthave predispositions to process social cues, but, withdifferent motives for social interaction, find it moredifficult to develop certain functions for their attention-following skills, independently of their degree of mental-istic understanding.

In summary, comparative evidence from human babies,apes, monkeys and canids suggests that gaze and socialcue following is the result of a complex ontogeneticinterplay between genetic predispositions for selectiveattention, appropriate experience, and distinctivemotives.

Representing attention

A central question is if similar gaze-following perform-ances in different species can be attributed to similarcognitive mechanisms. Do animals read gaze with mental-istic representations, that is, do they attribute theexperience of seeing and attending?

Gaze following could be a reflex or a mechanically-learned reaction [51]. When turning, animals might notrepresent the visual perspective of the looker, but just lookat the first interesting object found. Human babiesinitially do this, but between 12 and 18 months theybecome more sophisticated – they identify the right targetby precisely following the gaze line of others [38], and theydo not look at objects that, albeit in the geometric line ofgaze, cannot possibly be seen by the other [61].

Adult chimpanzees behave like older human infants. Ifa barrier is in the line of sight of the looker, chimpanzeesdo not follow her gaze to objects beyond the barrier [62].Moreover, chimps use this ability to outwit other chim-panzees in competitive situations [59]. We don’t know yethow dogs behave in a barrier test.

These findings suggest that gaze followers expectlooking to be directed towards a specific target, and thatthis must be in the uninterrupted line of vision of thelooker. Cognitively, one possible interpretation is thatadult chimps and 18-month-old infants do representlooking behavior mentalistically; that is, they attributeto the looker the internal experience of seeing or notseeing an object [61,63]. This interpretation remainscontested [64].

An alternative, reconciling interpretation is thatchimpanzees represent agents as externally attending tosomething without simultaneously representing the innerexperiences of seeing or attending. Adult humans repre-sent mental states as simultaneously private, unobserv-able, and intentional. Non-humans (and maybe humaninfants) might represent ‘aboutness’ (a defining feature ofthe mental, also known as ‘intentionality’ [65]) indepen-dently of the other dimensions [2].

Attention as an external mental state

Laboratory-reared rhesus monkeys follow the gaze ofphotos depicting lions, orangutans, and domestic cats –species they had never seen before [66] (Figure 5). Thisfinding suggests that gaze following is based upon theextraction of highly invariant features of faces acrossspecies. This is in sharp contrast to individual face


Figure 5. Rhesus monkeys are sensitive to the gaze direction of static photographs depicting animal species they have never seen before. This Figure shows the visual

scanning of a monkey confronted with the photograph of a lion looking sideways as recorded with an eye-tracking device [66]. Note that the monkey’s eye movements are

exclusively in the direction the lion is looking, and ignore the opposite side. This implies that gaze following is based upon an abstract schema of gaze that can be applied to

completely new types of faces. (Photo reproduced with permission of E. Lorinctz, J.-C. Gomez, and D. Perrett).


recognition, where specific experience is required forbuilding the relevant representations [67]. One possibilityis that rhesus abstract the eyes and their alignment as thekey invariant across species. However, in the rhesusbrain, neurons specialized in detecting attention directedat specific locations (e.g. attention down), fire in responsenot only to eye gaze, but also to models with eyes and headcovered but whose body is oriented down [68]. The monkeybrain might represent attention as an intentional (in the

Box 3. Avian cognition: widening the comparative scope

An important trend in recent years has been the expansion of

comparative studies of complex cognition to avian species. Many

species of birds reach Stage-5 object permanence, and one – the

grey parrot – might understand invisible displacements (Stage 6).

Interestingly, like primates, some bird species go through an A-not-B

error phase, whereas other species skip this (as dogs do) [75]. This

offers a unique opportunity for a double comparative approach to

understanding how the two types of developmental pattern have

evolved independently in mammals and birds.

Natural tool-using behaviors of birds such as finches or corvids

were traditionally dismissed as ‘instinctive’ [48,76]. However, current

research suggests that some birds attain highly flexible tool use.

Wild ravens routinely modify twigs to render them useful for food

foraging [76]. In experimental settings crows select tools of adequate

length from a ‘tool-box’ [77], and can even modify pieces of wire by

bending them into a shape appropriate for hooking a reward [78].

Hand-reared ravens follow the gaze of humans and pass a barrier

test like chimpanzees from as early as 6 months of age [36]. Corvids

sometimes refrain from caching food while other corvids are

present, and scrub-jays recache food in a different location if other

birds witnessed the initial caching [79].

We know very little about the ontogeny of these behaviors in birds,

but given the different organization of the avian brain [48], they could

provide an insightful source of information about the interaction

between ontogenetic and neural mechanisms in the development of

complex behavior.


sense of ‘aboutness’) property of agents beyond theparticular physical configurations displayed. This couldbe a core mentalistic primitive that does not entail theattribution of internal mental states [2].

In summary, using the eyes of others to find objectsappears to be a widespread function among animals.Like object permanence, gaze following develops ininteraction with other cognitive and motivational systems,which might vary among different species (see alsoBoxes 3 and 4). These different cognitive contexts ofdevelopment might substantially affect the range offunctions subserved by the core skill of gaze following indifferent species.

Conclusions

Although two core building blocks of human cognition –object permanence and gaze following – are adaptationswith old phylogenetic roots, they are not hard-wiredabilities. Rather, they rest upon developmental mechan-isms partially shared with other species. Developmentaldevices like these have evolved because they are capable ofpreserving core adaptive components, but at the same

Box 4. Questions for future research

† Can infant monkeys and apes pass looking-time tests of object

permanence before manual search tests, and, if so, is their

looking/reaching lag similar to humans or reduced?

† Can artificial symbolic training and human-rearing (‘enculturation’)

affect developmental outcomes in such a way that new cognitive

skills are created?

† Does the emergence of gaze-following unfold along similar critical

steps across primate species, like the emergence of object

permanence?

† Is the lack or presence of A-not-B errors diagnostic of different

cognitive underpinnings both in mammals and birds?



time are open to further adaptive change, not only ininteraction with the external environment, but also,crucially, in interaction with other cognitive systems inthe developing organism. Cognitive development is anevolutionary tool that integrates cognitive bits andbehavioral pieces into higher-order adaptive systems. Tounderstand cognition we need to explain not only thestructure and history of the individual parts, but also howthey are articulated into higher-order systems in differentontogenies [2]. Cognitive development has evolved as asolution to the nature–nurture problem.

References

1 Parker, S.T. and McKinney, M.L. (1999) Origins of Intelligence, JohnsHopkins

2 Gomez, J.C. (2004) Apes, Monkeys, Children and the Growth of Mind,Harvard University Press

3 Hauser, M. and Spelke, E. Evolutionary and developmental foun-dations of human knowledge: a case study of mathematics. In TheCognitive Neurosciences III (Gazzaniga, M.S., ed.), MIT Press (inpress)

4 Heyes, C.M. (2003) Four routes of cognitive evolution. Psychol. Rev.110, 713–727

5 Bjorklund, D.F. and Pellegrini, A.D. (2002) The Origins of HumanNature: Evolutionary Developmental Psychology, American Psycho-logical Association

6 Hernandez-Blasi, C. and Bjorklund, D.F. (2003) Evolutionary develop-mental psychology. Special Issue. Infancia y Aprendizaje 26, 261–349

7 Hauser, M.D. (1998) Expectations about object motion and destina-tion: experiments with a nonhuman primate. Dev. Sci. 1, 31–38

8 Piaget, J. (1937) La Construction du Reel Chez l’Enfant, Delachaux etNiestle

9 Bremner, J.G. (2001) Cognitive development: Knowledge of thephysical world. In Infant Development (Bremner, G. and Fogel, A.,eds), pp. 99–138, Blackwell

10 Dore, F.Y. and Goulet, S. (1998) The comparative analysis of objectknowledge. In Piaget, Evolution, and Development (Langer, J. andKillen, M., eds), pp. 55–72, Erlbaum

11 Diamond, A. (1991) Neuropsychological insights into the meaning ofobject concept development. In The Epigenesis of Mind. Essays onBiology and Cognition (Carey, S. and Gelman, R., eds), pp. 67–110,Erlbaum

12 Diamond, A. (1990) Developmental time course in human infants andinfant monkeys, and the neural bases, of inhibitory control inreaching. In The Development and Neural Bases of Higher CognitiveFunctions (Diamond, A., ed.), pp. 637–676, New York Academy ofSciences

13 Filion, C.M. et al. (1996) Can monkeys (Macaca mulatta) representinvisible displacement? J. Comp. Psychol. 110, 386–395

14 Mendes, N. and Huber, L. (2004) Object permanence in commonmarmosets (Callithrix jacchus). J. Comp. Psychol. 118, 103–112

15 Watson, J. et al. (2001) Distinguishing logic from association in thesolution of an invisible displacement task by children (Homo sapiens)and dogs (Canis familiaris): Using negation of disjunction. J. Comp.Psychol. 115, 219–226

16 Baillargeon, R. (1995) Physical reasoning in infancy. In The CognitiveNeurosciences (Gazzaniga, M.S., ed.), pp. 181–204, MIT Press

17 Hood, B.M. et al. (1999) Gravity biases in a non-human primate? Dev.Sci. 2, 35–41

18 Santos, L. and Hauser, M.D. (2002) A nonhuman primate’s under-standing of solidity: Dissociations between seeing and acting. Dev. Sci.5, F1–F7

19 Hauser, M.D. (2003) Knowing about knowing. Dissociations betweenperception and action systems over evolution and during develop-ment. Ann. New York Acad. Sci. 1001, 79–103

20 Osthaus, B. et al. (2003) Can dogs defy gravity? A comparison with thehuman infant and a non-human primate. Dev. Sci. 6, 489–497

21 Hood, B.M. (1995) Gravity rules for 2- to 4-year olds? Cogn. Dev. 10,577–598

22 Hood, B.M. (1997) Gravity does rule for falling objects?Dev. Sci. 1, 59–64


23 Cacchione, T. and Krist, H. (2004) Recognizing impossible objectrelations: Intuitions about support in chimpanzees (Pan troglodytes).J. Comp. Psychol. 118, 140–148

24 Povinelli, D.J. (2000) Folk Physics for Apes, Oxford University Press25 Munakata, Y. (2001) Graded representations in behavioral dis-

sociations. Trends Cogn. Sci. 5, 309–31526 Bogartz, R.S. et al. (2000) Object permanence in five-and-a-half-

month-old infants? Infancy 1, 403–42827 Smith, L.B. and E., T. (2003) Development as a dynamic system.

Trends Cogn. Sci. 7, 343–34828 Langer, J. (2000) The heterochronic evolution of primate cognitive

development. In Biology, Brains, and Behavior: The Evolution ofHuman Development (Parker, S.T. et al., eds), pp. 215–235, School ofAmerican Research Press

29 Tomasello, M. et al. (1998) Five primate species follow the visual gazeof conspecifics. Anim. Behav. 55, 1063–1069

30 Call, J. and Tomasello, M. (2004) Social cognition. In PrimatePsychology (Maestripieri, D., ed.), pp. 234–253, Harvard UniversityPress

31 Lorincz, E. et al. (1999) Visual cues for attention following in monkeys.Cahiers de Psychologie Cognitive 18, 973–1003

32 Emery, N.J. et al. (1997) Gaze following and joint attention in rhesusmonkeys (Macaca mulatta). J. Comp. Psychol. 111, 286–293

33 Scerif, G. et al. (2004) What do Diana monkeys know about the focus ofattention of a conspecific? Anim. Behav. 68, 1239–1247

34 Miklosi, A. et al. (2004) Comparative social cognition: what can dogsteach us? Anim. Behav. 67, 995–1004

35 Kaminski, J. et al. (2005) Domestic goats (Capra hircus) follow gazedirection and use social cues in an object choice task. Animal Behav.69, 11–18

36 Bugnyar, T. et al. (2004) Ravens, Corvus corax, follow gazedirection of humans around obstacles. Proc. R. Soc. Lond. B. Biol.Sci. 271, 1331–1336

37 Pack, A.A. and Herman, L.M. (2004) Bottlenosed dolphins (Tursiptruncatus) comprehend the referent of both static and dynamic humangazing and pointing in an object-choice task. J. Comp. Psychol. 118,160–171

38 Butterworth, G. (2001) Joint visual attention in infancy. In InfantDevelopment (Bremner, G. and Fogel, A., eds), pp. 213–240, Blackwell

39 Farroni, T. et al. (2002) Eye contact detection in humans from birth.Proc. Natl. Acad. Sci. U. S. A. 99, 9602–9605

40 Farroni, T. et al. (2003) Infants perceiving and acting on the eyes:Tests of an evolutionary hypothesis. J. Exp. Child Psychol. 85,199–212

41 Johnson, M.H. and Farroni. T. (2003) Perceiving and acting on eyegaze. In Face Processing in Infancy and Early Childhood (Vol. 99)(Pascalis, O. and Slate, A., eds), pp. 9602–9605, NOVA SciencePublishers

42 Ferrari, P.F. et al. (2000) The ability to follow eye gaze and itsemergence during development in macaque monkeys. Proc. Natl.Acad. Sci. U. S. A. 97, 13997–14002

43 Tomasello, M. et al. (2001) The ontogeny of gaze following inchimpanzees, Pan troglodytes, and rhesus macaques, Macacamulatta. Anim. Behav. 61, 335–343

44 Myowa-Yamakoshi, M. and Tomonaga, M. (2001) Perceiving eye gazein an infant gibbon (Hylobates agilis). Psychologia 44, 24–30

45 Myowa-Yamakoshi, M. et al. (2003) Preference for human direct gazein infant chimpanzees (Pan troglodytes). Cognition 89, B53–B64

46 Okamoto, S. et al. (2002) An infant chimpanzee (Pan troglodytes)follows human gaze. Anim. Cogn. 5, 107–114

47 Okamoto, S. et al. (2004) Looking back: The ‘representationalmechanism’ of joint attention in an infant chimpanzee (Pantroglodytes). Jpn. Psychol. Res. 46, 236–245

48 Emery, N.J. and Clayton, N.S. (in press) Comparing the complexcognition of birds and primates. In Comparative Vertebrate Cognition(Rogers, L.J. and Kaplan, G.T., eds), pp. 3–55, Kluwer Academic Press

49 Call, J. et al. (2000) Cues that chimpanzees do and do not use to findhidden objects. Anim. Cogn. 3, 23–34

50 Itakura, S. and Tanaka, M. (1998) Use of experimenter-given cuesduring object-choice tasks by chimpanzees, an orangutan and humaninfants. J. Comp. Psychol. 112, 119–126

51 Povinelli, D.J. and Eddy, T.J. (1996) What young chimpanzees knowabout seeing. Monogr. Soc. Res. Child Dev. 61, 1–152



52 Miklosi, A. et al. (1998) Use of experimenter-given cues in dogs. Anim.Cogn. 1, 113–121

53 Soproni, K. et al. (2001) Comprehension of human communicativesigns in pet dogs. J. Comp. Psychol. 115, 122–126

54 Soproni, K. et al. (2001) Dogs’ (Canis familiaris) responsiveness tohuman pointing gestures. J. Comp. Psychol. 116, 27–34

55 Agnetta, B. et al. (2000) Cues to food location that domestic dogs(Canis familiaris) of different ages do and do not use. Anim. Cogn. 3,107–112

56 Hare, B. et al. (2002) The domestication of social cognition in dogs.Science 298, 1634–1636

57 Miklosi, A. et al. (2003) A simple reason for a big difference: wolves donot look back at humans but dogs do. Curr. Biol. 13, 763–767

58 Hare, B. and Tomasello, M. Chimpanzees are more skillful in com-petitive than in cooperative cognitive tasks. Anim. Behav. (in press)

59 Hare, B. et al. (2000) Chimpanzees know what conspecifics do and donot see. Anim. Behav. 59, 771–785

60 Hare, B. et al. (2001) Do chimpanzees know what conspecifics know?Anim. Behav. 61, 139–151

61 Moll, H. and Tomasello, M. (2004) 12- and 18-month-old infants followgaze to spaces behind barriers. Dev. Sci. 7, F1–F9

62 Tomasello, M. et al. (1999) Chimpanzees follow gaze directiongeometrically. Anim. Behav. 58, 769–777

63 Tomasello, M. et al. (2003) Chimpanzees understand psychologicalstates – the question is which ones and to what extent. Trends Cogn.Sci. 7, 153–156

64 Povinelli, D.J. and Vonk, J. (2003) Chimpanzee minds: suspiciouslyhuman? Trends Cogn. Sci. 7, 157–160

65 Dennett, D.C. and Haugeland, J.C. (1987) Intentionality. In TheOxford Companion to the Mind (Gregory, R.L., ed.), pp. 383–386,Oxford University Press

66 Lorinctz, E. et al. (in press) Do monkeys understand actions and mindsof others? Studies of single cell and eye movements. In From MonkeyBrain to Human Brain (Dehaene, S., ed.), Oxford University Press

AGORA initiative provides free agricult

The Health Internetwork Access to Research Initiative (HINARI) of the

and Agriculture O

As part of this enterprise, Elsevier has given 185 journals to Access to

institutions are now registered for the scheme, which aims to provid

ultimately help increase crop yields and e

According to the Africa University in Zimbabwe, AGORA has been w

information to our fingertips’ says Vimbai Hungwe. ‘The information

and research activities within the University. Given the economic hard

For more inform

http://www.healthin


67 de Haan, M. et al. (2002) Specialization of neural mechanismsunderlying face recognition in human infants. J. Cogn. Neurosci. 14,199–209

68 Perrett, D. (1999) A cellular basis for reading minds from faces andactions. In The Design of Animal Communication (Hauser, M. andKonishi, M., eds), pp. 159–185, MIT Press

69 Hauser, M.D. et al. Evolutionary foundations of number: spontaneousrepresentation of numerical magnitudes by cotton-top tamarins.Cogn. Dev. (in press)

70 Biro, D. and Matsuzawa, T. (2001) Chimpanzee numerical compe-tence: cardinal and ordinal skills. In Primate Origins of Human

Cognition and Behavior (Matsuzawa, T., ed.), pp. 199–225, Springer71 Moore, C. and Dunham, P.J. eds (1995) Joint Attention: Its Origins

and Role in Development, Erlbaum72 Leavens, D. and Hopkins, W. (1999) The whole hand point: The

structure and function of pointing from a comparative perspective.J. Comp. Psychol. 113, 417–425

73 Baldwin, D.A. (1995) Understanding the link between joint attentionand language. In Joint Attention: Its Origins and Role in Development

(Moore, C. and Dunham, P.J., eds), pp. 131–158, Erlbaum74 Tomasello, M. (1999) The Cultural Origins of Human Cognition,

Harvard University Press75 Pollok, B. et al. (2000) Development of object permanence in food-

storing magpies (Pica pica). J. Comp. Psychol. 114, 148–15776 Lefebvre, L. et al. (2002) Tools and brains in birds. Behavior 139,

939–97377 Chappell, J. and Kacelnik, A. (2002)Tool selectivity ina non-primate, the

New Caledonian crow (Corvus moneduloides). Anim. Cogn. 5, 71–7878 Weir, A.A. et al. (2002) Shaping of hooks in New Caledonian crows.

Science 297, 98179 Emery, N.J. and Clayton, N.S. (2001) Effects of experience and social

context on prospective caching strategies by scrub jays. Nature 414,443–446

ure journals to developing countries

WHO has launched a new community scheme with the UN Food

rganization.

Global Online Research in Agriculture (AGORA). More than 100

e developing countries with free access to vital research that will

ncourage agricultural self-sufficiency.

elcomed by both students and staff. ‘It has brought a wealth of

made available goes a long way in helping the learning, teaching

ships we are going through, it couldn’t have come at a better time.’

ation visit:

ternetwork.net


Species comparative studies and cognitive development

Documents

Transcript of Species comparative studies and cognitive development