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Species comparative studies and cognitive development Juan-Carlos Go´mez 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 components 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 developmental 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.
Introduction The comparative study of infant development and animal cognition brings to cognitive science the promise of insights into the nature of cognitive skills by studying their origins in different genetic time scales [1–3]. Development is a key mechanism of evolution – an arena for the interplay of phylogenetic and ontogenetic avenues of adaptation – and therefore the best way to fulfill this explanatory promise is to combine developmental and evolutionary approaches in comparative developmental studies [1–6]. In this article I explore two domains in which comparative studies of development with comparable methodologies and theoretical frameworks have been conducted in the past few years: the ability to track and locate objects in space and the ability to find objects through the gaze of others. Both exemplify the growing strength of combining developmental and evolutionary perspectives in understanding the core building blocks of cognition. Understanding the invisible life of objects Finding and keeping track of objects such as food, conspecifics or predators is a function shared across virtually all animal species [7]. Developmental psychologists found that object search skills – Piagetian ‘object permanence’ – emerge in human infants through a fixed series of steps with characteristic transitional errors [8,9]. Before the age of 7 or 8 months, infants fail to retrieve an Corresponding author: Go´mez, J.-C. (
[email protected]). Available online 1 February 2005
object completely hidden from their view (Stages 1–3). After 8 months, they retrieve hidden objects, but if an object successfully retrieved from location A is then moved to location B, they search again in location A, despite having clearly seen that the object was now placed in B (Stage 4). This so-called ‘A-not-B error’ is overcome at 11–12 months, when infants systematically search in the last place they saw the object disappear (Stage 5). However, at this age infants have problems with ‘invisible displacements’. If the experimenter hides an object with his hand closed, then until 18 months of age (Stage 6), infants search only in the hand, without realizing that the object was left behind.
Object permanence in animals Comparative research shows that many species develop Piagetian object permanence skills in exactly the same sequence as human infants [1,2,10] but at different speeds (Figure 1). Apes are slightly faster than humans in all steps. Monkey species develop about three to four times faster than humans [11,12], but might fail to master invisible displacements [1,2,10], although controversy persists over this point [13,14]. Non-primate species develop object permanence even faster [10]. Dogs and cats reach Stage-5 performance in only a couple of months, but interestingly, in contrast to all primate species studied
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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 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]).
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so far, they skip the phase of committing A-not-B errors. Contrary to initial reports [10], they also fail to reach the invisible displacements phase. This developmental divergence suggests that the cognitive basis of their performance in object retrieval tasks might be fundamentally different to primates [2,15]. Object permanence is therefore a core universal of primate cognition not only in terms of the basic competence achieved, but also in terms of its pattern of emergence in ontogeny. Of special interest is the apparent universality of the A-not-B error phase and the elasticity of the developmental pattern across species. Representations or executive skills? The traditional interpretation was that object permanence reflects the progressive acquisition of the ability to represent (i.e. mentally encode) the hidden objects [8,9]. Contemporary research suggests, however, that complex knowledge about objects – including their existence when they are out of sight –is present in infants by 3–4 months of age before manual search skills develop [16]. Such early knowledge is revealed by infants’ increased attention to events that violate principles of object permanence (e.g. an object failing to re-appear where it was placed) [9]. This implies that human infants might have a developmental mismatch between object knowledge and its use in action. Object permanence might be an index not of representational change, but of the growth of an executive ability to use knowledge that already exists. This idea could help to explain the enigmatic A-not-B error and the developmental elasticity across species. Within their own developmental spans, rhesus monkeys and human infants go through the A-not-B error phase in identical microgenetic detail [12]. A proposal is that during this phase both species develop stronger executive skills (i.e. skills to organize goal-directed action effectively, such as working memory and inhibition) based on the maturation of the prefrontal cortex [11]. This maturation occurs at different rates in each species, so that rhesus monkeys would have executive access to their existing object representations earlier than humans, thereby showing earlier object permanence development. The executive hypothesis, therefore, is consonant with the looking-time findings with human babies and seems able to account for interspecies similarities and differences. However, a crucial piece of evidence for this view is whether mismatches between looking and reaching measures of object knowledge can be found in nonhumans. Knowledge/action mismatches in non-humans We do not know yet if infant monkeys, like human infants, show a developmental precedence in looking measurements of Piagetian object permanence or, having an earlier maturation of executive skills, whether their perception and action performances unfold in synchrony. However, looking/reaching mismatches have been reported in adult macaque monkeys in some advanced tasks of object permanence. For example, both human children (aged just under 3 years) and adult monkeys show a gravity bias in their www.sciencedirect.com
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understanding of invisible displacements involving falling objects [7,17,18]. They consistently tend to search for an object on the ground just under the place where it fell when the falling trajectory is occluded by a screen. This gravity bias is so powerful that they search on the ground even when there are unavoidable physical constraints that prevent the objects from falling straight down – for example, when a solid board is blocking the vertical trajectory of the object, or the object is dropped into an opaque tube that goes diagonally to a lateral location (Figure 2). They can repeat this error perseveratively, that is, 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 committing the error [19]. A proposed explanation for the gravity bias, consonant with the executive hypothesis of object permanence, is that the error is induced by a failure to inhibit the prepotent expectation that objects fall straight down – which would be hardwired as a sort of ‘modular macro’ in primate, 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 bias disappears (even if performance is not perfect) [19]. Moreover, when tested with looking time paradigms,
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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.
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adult monkeys [18] and young human children who commit the gravity error show surprise when objects appear in the gravity-congruent, impossible location. Their perceptual system is somehow aware that the object should not be there, whereas their action system is stubbornly convinced that it must be. The executive hypothesis assumes that 3-year-old children grow out of this contradiction [21], not because they acquire new knowledge about the physical constraints affecting gravity, but because their brains develop the power to inhibit the inappropriate gravity response, thereby liberating their existing knowledge. By contrast, monkeys (who reveal a similar correct knowledge of physical constraints in some looking tasks) never acquire the requisite inhibitory skills and are condemned by evolution to keep this cognitive dissociation [19,22]. A similar permanent dissociation in understanding object support relations might exist in chimpanzees. They identify impossible support relations in looking tasks [23], but fail to do so in active problem solving [24]. In human infants, knowing/acting mismatches can be understood as a transitory developmental phenomenon that occurs in the process of assembling a complex cognitive system. However, in adult primates, the sense of a permanent mismatch between knowledge and action is not clear. Without being translated into action, how can knowledge exert an adaptive impact upon individuals and therefore evolve by natural selection?
Representational accounts of knowledge/action mismatches One possible explanation is that the knowledge revealed by looking-time methods is not the same knowledge used for successful action [25,26]. In an adaptation of the diagonal tubes task (Figure 2), when given the benefit of seeing that the object cannot be directly under its release point (because the space underneath is visibly empty), macaque monkeys and young children – unable now to give the gravity response – still fail to choose the correct location (Southgate and Go´mez, unpublished). No hidden knowledge for successful action is liberated by removing the prepotent response, as executive accounts predict [19,22]. Adult monkeys and younger children do not understand well how tubes constrain object trajectories, whereas older children must have acquired a better understanding of tubes as physical devices. A recent developmental theory suggests that lookingtime data reflect ‘weak’ object representations, whereas successful search requires ‘stronger’ representations [25]. This implies a process of graded representational change during ontogeny. A similar notion could be applied to phylogenetic comparison. Some species might only attain weak representations in some domains (e.g. invisible physical constraints), which they fail to develop into fullblown, strong versions. Weak representations might be a by-product of other processes that do exert an adaptive impact on behavior. However, the question remains of what is required to develop weak into strong representations. www.sciencedirect.com
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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].
Global cognitive systems Other developmental approaches emphasize changes in the overall dynamics of behavioral systems, rather than changes in individual components, as being responsible for development [27]. What matters here is the global interplay among subsystems (see Box 1). If we take this view to phylogeny, core cognitive components like object permanence can be seen as developing in different cognitive contexts in different species. For example, although gorillas and chimpanzees develop object permanence following a similar schedule to humans, they are slower at developing tool-use as an extension for grasping (e.g. raking with a stick) and faster with tool use as an extension of locomotor reach (e.g. moving a box to use as a ladder) (Figure 3). Most monkey species never develop either type of tool use or only do so as adults. This might put children on the track of coordinating object search with understanding mechanical interaction among objects, much earlier than apes. Such differences in timing (‘heterochronies’) in the
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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]).
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ontogeny of cognitive systems across different domains could play a major role in explaining cognitive differences among primate species [1,28]. Integrating developmental accounts Different comparative findings about the core cognitive skill of object permanence appear to favor different theoretical accounts of developmental change. However, a global perspective suggests that the best option is an integration of rival theories. The growth of executive processes like inhibition and working memory might enable the dynamic coordination of systems of perception and action. Such coordination could in turn be one of the factors fostering the conversion of weak into strong representations. Complex object cognition results from developmental interactions among a variety of behavioral and representational systems. Finding objects with the eyes of others We have discussed the ability to track objects individually, by processing information provided by the physical environment. However, we can also find objects using social cues – following the gaze of others. Gaze following is part of a set of skills called ‘joint attention’ (Box 2). As recently as 8 years ago it was not known whether gaze following was a uniquely human skill. Now, several studies have firmly established that monkeys and apes will spontaneously look in the same direction as a conspecific or a human [29,30], not only in response to live models, but also with the limited information provided by a photograph [31–33]. Gaze following is a prevalent primate adaptation, but is not exclusive to primates: it has been reported in domestic dogs [34], domestic goats [35], captive corvids [36], and captive dolphins [37]. Gaze following responses are therefore widespread among distantly related animal species. Development of gaze following Human infants start turning to look in the same direction as other people at around 6 months. At 12 months, they consistently look at the correct object, and at 18 months they 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 comparative researchers agree that joint attention skills might represent the earliest manifestations of theory of mind both in ontogeny and phylogeny [2,74]. www.sciencedirect.com
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of gaze following can be traced to newborns, who distinguish 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 as averted faces if their attention is first engaged with direct gaze [40]. Gaze following might emerge out of an interaction between an innate preference for direct gaze and more general mechanisms of attentional orientation to movement activated when the model’s eyes turn sideways [40–41]. Few developmental studies exist about gaze following in non-humans. Laboratory-reared pigtailed macaques follow gaze in response to head and eye movements of humans well after infancy (2–4 years), and only adults follow eye movements alone [42]. However, rhesus macaques housed in larger social groups follow human gaze by 6 months of age [43]. Similar to human babies, 2-month-old chimpanzees and 1-month-old gibbons discriminate between direct and averted gaze, preferentially attending to faces that look directly at them [44–45]. Although one report found gaze following in chimpanzees only at 3–4 years [43], one chimpanzee baby followed head movements of humans towards objects at 10 months, eye movements at 13 months [46], and looked behind himself at 20 months [47], which closely resembles human development. Although more comparative developmental studies are needed, primate gaze following appears to be the result of a developmental interplay between initial predispositions to process gaze stimuli and experience. This basic developmental mechanism is probably shared by apes and humans, but a core gaze-following skill is either phylogenetically older or independently selected in different species [48]. A functional dissociation There are two main methods to test gaze following skills (Figure 4). One is to measure if animals spontaneously look in the same direction as a model; the second is to allow them to use gaze as a cue to a hidden object (e.g. food in a box). Non-human primates consistently do the first, but find the second unexpectedly difficult [30,49]. In choice tasks, most primates fail to use human gaze or even pointing gestures to select the container with hidden food. Children solve these problems only at around 3 years of age [50], although they show spontaneous gaze following much earlier. A possible explanation of this paradox (to some extent reminiscent of the looking/reaching dissociations discussed in the previous section) is that gaze following in non-humans is just a tendency to look in the same direction as a model, but without the mentalistic representations that humans superimpose on gaze [51]; that is, without attributing intentions or knowledge. By contrast, in human children the gaze-following mechanisms shared with other primates would become developmentally interlocked with mechanisms of mentalistic attribution, widening their functions. In contrast to primates, domestic dogs perform excellently in object-choice paradigms. They reliably and accurately follow gaze and pointing cues to locate hidden
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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 due to their rearing by humans. The minority of apes who do relatively well in object-choice tasks typically had extensive human rearing [30]. However, when similarly reared by humans, wolves (the closest evolutionary relatives of domestic dogs) fail to follow human social cues [56,57]. Humans might have artificially selected dogs with genetic predispositions to learn to respond to human cues [34]. Privileged attention to faces might be one such predisposition (dogs, but not wolves, typically look back at their owners’ faces in problem situations) [34,57]. But good performance in choice tests might require more than such predispositions. Motives to follow gaze Chimpanzee performance in object choice is facilitated by several factors, such as experience with humans and combining sounds with gaze and pointing [30,49]. But the most effective facilitator is changing the motivational domain of the task. Chimpanzees choose correctly when a human competitor looks and reaches to the baited box as if trying to gain the reward, but fail when a cooperative human points to show them the baited box [58]. This finding converges with other evidence that in competitive situations chimpanzees use conspecifics’ cues of attention [59,60]. One possible explanation is that chimpanzees don’t understand the communicative intention to show something [30], whereas they do understand the intention to reach a target. However, competitive contexts also increase performance in simple discriminative tasks involving no social cues, which suggests that competition might be a domain-general performance enhancer for chimpanzees [58]. Dogs and human infants might bring to the task of learning to follow attentional cues, not only specific www.sciencedirect.com
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attentional and processing biases, but also a distinctive set of cooperative motives [58,34]. Chimpanzees might have predispositions to process social cues, but, with different motives for social interaction, find it more difficult to develop certain functions for their attentionfollowing skills, independently of their degree of mentalistic understanding. In summary, comparative evidence from human babies, apes, monkeys and canids suggests that gaze and social cue following is the result of a complex ontogenetic interplay between genetic predispositions for selective attention, appropriate experience, and distinctive motives. Representing attention A central question is if similar gaze-following performances in different species can be attributed to similar cognitive mechanisms. Do animals read gaze with mentalistic representations, that is, do they attribute the experience of seeing and attending? Gaze following could be a reflex or a mechanicallylearned reaction [51]. When turning, animals might not represent the visual perspective of the looker, but just look at the first interesting object found. Human babies initially do this, but between 12 and 18 months they become more sophisticated – they identify the right target by precisely following the gaze line of others [38], and they do not look at objects that, albeit in the geometric line of gaze, cannot possibly be seen by the other [61]. Adult chimpanzees behave like older human infants. If a barrier is in the line of sight of the looker, chimpanzees do not follow her gaze to objects beyond the barrier [62]. Moreover, chimps use this ability to outwit other chimpanzees in competitive situations [59]. We don’t know yet how dogs behave in a barrier test. These findings suggest that gaze followers expect looking to be directed towards a specific target, and that this must be in the uninterrupted line of vision of the looker. Cognitively, one possible interpretation is that adult chimps and 18-month-old infants do represent looking behavior mentalistically; that is, they attribute to the looker the internal experience of seeing or not seeing an object [61,63]. This interpretation remains contested [64]. An alternative, reconciling interpretation is that chimpanzees represent agents as externally attending to something without simultaneously representing the inner experiences of seeing or attending. Adult humans represent mental states as simultaneously private, unobservable, and intentional. Non-humans (and maybe human infants) might represent ‘aboutness’ (a defining feature of the mental, also known as ‘intentionality’ [65]) independently of the other dimensions [2]. Attention as an external mental state Laboratory-reared rhesus monkeys follow the gaze of photos depicting lions, orangutans, and domestic cats – species they had never seen before [66] (Figure 5). This finding suggests that gaze following is based upon the extraction of highly invariant features of faces across species. This is in sharp contrast to individual face
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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. Go´mez, and D. Perrett).
recognition, where specific experience is required for building the relevant representations [67]. One possibility is that rhesus abstract the eyes and their alignment as the key invariant across species. However, in the rhesus brain, neurons specialized in detecting attention directed at specific locations (e.g. attention down), fire in response not only to eye gaze, but also to models with eyes and head covered but whose body is oriented down [68]. The monkey brain 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. www.sciencedirect.com
sense of ‘aboutness’) property of agents beyond the particular physical configurations displayed. This could be a core mentalistic primitive that does not entail the attribution of internal mental states [2]. In summary, using the eyes of others to find objects appears to be a widespread function among animals. Like object permanence, gaze following develops in interaction with other cognitive and motivational systems, which might vary among different species (see also Boxes 3 and 4). These different cognitive contexts of development might substantially affect the range of functions subserved by the core skill of gaze following in different species. Conclusions Although two core building blocks of human cognition – object permanence and gaze following – are adaptations with old phylogenetic roots, they are not hard-wired abilities. Rather, they rest upon developmental mechanisms partially shared with other species. Developmental devices like these have evolved because they are capable of preserving 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?
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time are open to further adaptive change, not only in interaction with the external environment, but also, crucially, in interaction with other cognitive systems in the developing organism. Cognitive development is an evolutionary tool that integrates cognitive bits and behavioral pieces into higher-order adaptive systems. To understand cognition we need to explain not only the structure and history of the individual parts, but also how they are articulated into higher-order systems in different ontogenies [2]. Cognitive development has evolved as a solution to the nature–nurture problem.
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