Chimpanzees and bonobos exhibit divergent spatial memory development

Spatial cognition and memory are critical cognitive skills underlying foraging behaviors for all primates. While the emergence of these skills has been the focus of much research on human children, little is known about ontogenetic patterns shaping spatial cognition in other species. Comparative developmental studies of nonhuman apes can illuminate which aspects of human spatial development are shared with other primates, versus which aspects are unique to our lineage. Here we present three studies examining spatial memory development in our closest living relatives, chimpanzees (Pan troglodytes) and bonobos (P. paniscus). We first compared memory in a naturalistic foraging task where apes had to recall the location of resources hidden in a large outdoor enclosure with a variety of landmarks (Studies 1 and 2). We then compared older apes using a matched memory choice paradigm (Study 3). We found that chimpanzees exhibited more accurate spatial memory than bonobos across contexts, supporting predictions from these species’ different feeding ecologies. Furthermore, chimpanzees – but not bonobos – showed developmental improvements in spatial memory, indicating that bonobos exhibit cognitive paedomorphism (delays in developmental timing) in their spatial abilities relative to chimpanzees. Together, these results indicate that the development of spatial memory may differ even between closely related species. Moreover, changes in the spatial domain can emerge during nonhuman ape ontogeny, much like some changes seen in human children.     

Comparative cognitive development

This paper aims to compare cognitive development in humans and chimpanzees to illuminate the evolutionary origins of human cognition. Comparison of morphological data and life history strongly highlights the common features of all primate species, including humans. The human mother-infant relationship is characterized by the physical separation of mother and infant, and the stable supine posture of infants, that enables vocal exchange, face-to-face communication, and manual gestures. The cognitive development of chimpanzees was studied using the participation observation method. It revealed that humans and chimpanzees show similar development until 3 months of age. However, chimpanzees have a unique type of social learning that lacks the social reference observed in human children. Moreover, chimpanzees have unique immediate short-term memory capabilities. Taken together, this paper presents a plausible evolutionary scenario for the uniquely human characteristics of cognition.     

'Unwilling' versus 'unable': chimpanzees' understanding of human intentional action

Understanding the intentional actions of others is a fundamental part of human social cognition and behavior. An important question is therefore whether other animal species, especially our nearest relatives the chimpanzees, also understand the intentional actions of others. Here we show that chimpanzees spontaneously (without training) behave differently depending on whether a human is unwilling or unable to give them food Chimpanzees produced more behaviors and left the testing station earlier with an unwilling compared to an unable (but willing) experimenter These data together with other recent studies on chimpanzees' knowledge about others' visual perception show that chimpanzees know more about the intentional actions and perceptions of others than previously demonstrated     

Understanding the Point of Chimpanzee Pointing: Epigenesis and Ecological Validity

Abstract— Pointing has long been considered to be a uniquely human, universal, and biologically based gesture. However, pointing emerges spontaneously, without explicit training, in captive chimpanzees. Because pointing is commonplace in captive chimpanzees and virtually absent in wild chimpanzees, and because both captive and wild chimpanzees are sampled from the same gene pool, pointing by captive apes is attributable to environmental influences on communicative development. If pointing by captive chimpanzees is so variably expressed in different rearing environments, this suggests that pointing by humans may also be attributable to situational factors that make pointing effective in certain developmental contexts.     

Chimpanzee (<Emphasis Type="Italic">Pan troglodytes</Emphasis>) and orangutan (<Emphasis Type="Italic">Pongo abelii</Emphasis>) forethought: self-control and pre-experience in the face of future tool use

Planning for future needs has traditionally been considered to be restricted to human cognition. Although recent studies on great ape and corvid cognition challenge this belief, the phylogenesis of human planning remains largely unknown. The complex skill for future planning has not yet been satisfactorily established in any other extant primate species than our own. In humans, planning for future needs rely heavily on two overarching capacities, both of which lie at the heart of our cognition: self-control, often defined as the suppression of immediate drives in favor of delayed rewards, and mental time travel, which could be described as a detached mental experience of a past or future event. Future planning is linked to additional high complexity cognition such as metacognition and a consciousness usually not attributed to animals. In a series of four experiments based on tool use, we demonstrate that chimpanzees (Pan troglodytes) and orangutans (Pongo abelii) override immediate drives in favor of future needs, and they do not merely rely on associative learning or semantic prospection when confronted with a planning task. These results suggest that great apes engage in planning for the future by out competing current drives and mentally pre-experiencing an upcoming event. This suggests that the advanced mental capacities utilized in human future planning are shared by phylogenetically more ancient species than previously believed.     

Prelinguistic Infants, but Not Chimpanzees, Communicate About Absent Entities

ABSTRACT— One of the defining features of human language is displacement , the ability to make reference to absent entities. Here we show that prelinguistic, 12-month-old infants already can use a nonverbal pointing gesture to make reference to absent entities. We also show that chimpanzees—who can point for things they want humans to give them—do not point to refer to absent entities in the same way. These results demonstrate that the ability to communicate about absent but mutually known entities depends not on language, but rather on deeper social-cognitive skills that make acts of linguistic reference possible in the first place. These nonlinguistic skills for displaced reference emerged apparently only after humans' divergence from great apes some 6 million years ago.     

Different early rearing experiences have long‐term effects on cortical organization in captive chimpanzees (Pan troglodytes)

Consequences of rearing history in chimpanzees (Pan troglodytes) have been explored in relation to behavioral abnormalities and cognition; however, little is known about the effects of rearing conditions on anatomical brain development. Human studies have revealed that experiences of maltreatment and neglect during infancy and childhood can have detrimental effects on brain development and cognition. In this study, we evaluated the effects of early rearing experience on brain morphology in 92 captive chimpanzees (ages 11–43) who were either reared by their mothers (n = 46) or in a nursery (n = 46) with age‐group peers. Magnetic resonance brain images were analyzed with a processing program (BrainVISA) that extracts cortical sulci. We obtained various measurements from 11 sulci located throughout the brain, as well as whole brain gyrification and white and grey matter volumes. We found that mother‐reared chimpanzees have greater global white‐to‐grey matter volume, more cortical folding and thinner grey matter within the cortical folds than nursery‐reared animals. The findings reported here are the first to demonstrate that differences in early rearing conditions have significant consequences on brain morphology in chimpanzees and suggests potential differences in the development of white matter expansion and myelination.     

Tool use as a way to assess cognition: how do captive chimpanzees handle the weight of the hammer when cracking a nut?

Tool use in apes has been considered a landmark in cognition. However, while most studies concentrate on mental operations, there are very few studies of apes’ cognition as expressed in manual skills. This paper proposes theoretical and methodological considerations on movement analysis as a way of assessing primate cognition. We argue that a privileged way of appraising the characteristics of the cognitive abilities involved in tool use lies at the functional level. This implies that we focus on how the action proceeds, and more precisely, on how the functional characteristics of the task are generated. To support our view, we present the results of an experiment with five captive chimpanzees investigating the way how chimpanzees adapt to hammers of various weights while cracking nuts. The movement performed in the hammering task is analyzed in terms of energy production. Results show that chimpanzees mobilise passive as well as active forces to perform the compliant movement, that is, they modulate the dynamics of the arm/tool system. A comparison between chimpanzees suggests that experience contributes to this skill. The results suggest that in tool use, movements are not key per se, but only in as much as they express underlying cognitive processes. Electronic supplementary material  The online version of this article (doi:) contains supplementary material, which is available to authorized users.

Great apes infer others’ goals based on context

In previous studies claiming to demonstrate that great apes understand the goals of others, the apes could potentially have been using subtle behavioral cues present during the test to succeed. In the current studies, we ruled out the use of such cues by making the behavior of the experimenter identical in the test phase of both the experimental and control conditions; the only difference was the preceding “context.” In the first study, apes interpreted a human’s ambiguous action as having the underlying goal of opening a box, or not, based on that human’s previous actions with similar boxes. In the second study, chimpanzees learned that when a human stood up she was going to go get food for them, but when a novel, unexpected event happened, they changed their expectation—presumably based on their understanding that this new event led the human to change her goal. These studies suggest that great apes do not need concurrent behavioral cues to infer others’ goals, but can do so from a variety of different types of cues—even cues displaced in time.     

A group-specific arbitrary tradition in chimpanzees (Pan troglodytes)

Social learning in chimpanzees has been studied extensively and it is now widely accepted that chimpanzees have the capacity to learn from conspecifics through a multitude of mechanisms. Very few studies, however, have documented the existence of spontaneously emerged traditions in chimpanzee communities. While the rigour of experimental studies is helpful to investigate social learning mechanisms, documentation of naturally occurring traditions is necessary to understand the relevance of social learning in the real lives of animals. In this study, we report on chimpanzees spontaneously copying a seemingly non-adaptive behaviour (“grass-in-ear behaviour”). The behaviour entailed chimpanzees selecting a stiff, straw-like blade of grass, inserting the grass into one of their own ears, adjusting the position, and then leaving it in their ear during subsequent activities. Using a daily focal follow procedure, over the course of 1 year, we observed 8 (out of 12) group members engaging in this peculiar behaviour. Importantly, in the three neighbouring groups of chimpanzees (n = 82), this behaviour was only observed once, indicating that ecological factors were not determiners of the prevalence of this behaviour. These observations show that chimpanzees have a tendency to copy each other’s behaviour, even when the adaptive value of the behaviour is presumably absent.     

Genes and the parsing of cognitive processes

Now that the human genome has been sequenced there exists the possibility of identifying specific genes that affect human cognition. In this article, recent studies that have found associations between common gene variants and specific cognitive processes are reviewed. Several principles for evaluating this new field are also discussed. The interpretation of results is far from simple because a single gene can affect multiple processes, multiple genes can impact on a single process, and multiple cognitive processes are intercorrelated. In general, functional neuroimaging has been a more sensitive assay of cognitive processing than behavioral measures used alone, although there are important caveats regarding its use. Replicated findings so far involve associations between a COMT polymorphism and prefrontally-based executive functions and neurophysiology, and a BDNF polymorphism and medial-temporal-cortex based declarative memory processes. Implicit in this review is a concern that many of the cognitive paradigms used evolved for purposes well outside those described here. As such it may be necessary to view cognition in novel ways, based on constraints imposed by genomics and neurobiology, in order to increase the effect size of genotypic influences on cognition.     

Preliminary Validation of a Multidimensional Model of Wittiness

ABSTRACT Past research on wittiness has found that ( a ) self-ratings and peer ratings of wittiness are highly correlated, but neither type of rating is appreciably correlated with measured humor production, and ( b ) sociability is correlated with both types of wittiness ratings but not with humor production. An interpretation of these findings was provided by a multidimensional model of wittiness that conceptualizes wittiness as a factorially complex dimension shaped by three component traits: humor motivation, humor cognition, and humor communication. We conducted three correlational studies to test the hypotheses, derived from the theory, that ( a ) wittiness ratings are influenced by humor motivation and humor communication, whereas humor production taps only humor cognition, and ( b ) sociability is positively correlated with humor motivation and humor communication but unrelated to humor cognition. Results were consistent across studies and generally confirmed the predictions.     

Goal attribution in chimpanzees

Does the chimpanzee attribute goals to others? Recent infant studies using the looking time measure have been interpreted as evidence that human infants attribute goals. An experiment modeled on these studies was carried out on chimpanzees, and the chimpanzees responded the way infants do. This indicates that chimpanzees also attribute goals and hence that this capacity is not distinctively human.     

Different social motives in the gestural communication of chimpanzees and human children

Both chimpanzees and human infants use the pointing gesture with human adults, but it is not clear if they are doing so for the same social motives. In two studies, we presented chimpanzees and human 25-month-olds with the opportunity to point for a hidden tool (in the presence of a non-functional distractor). In one condition it was clear that the tool would be used to retrieve a reward for the pointing subject (so the pointing was selfish or 'for-me'), whereas in the other condition it was clear that the tool would be used to retrieve the reward for the experimenter (so the pointing was helpful or 'for-you'). The chimpanzees pointed reliably only when they themselves benefited, whereas the human children pointed reliably no matter who benefited. These results are interpreted as evidence for the especially cooperative nature of human communication.     

Is cognition seasonal?

The idea that our mental life is more sluggish in winter is apparently seductive. This article reviews the evidence for the claim that there is a seasonal cycle in human cognition. Several methodologies have been used with participants such as over-wintering scientists in Antarctica, residents of polar regions, and patients with seasonal psychopathology and there is no clear tendency for cognition to be impaired in winter. Some large-scale public health studies report seasonality of cognition but are inconsistent regarding when in the year there is a peak and trough. Claims that human cognition has an annual cycle should be regarded as speculative and the burden of proof must be borne by anyone inclined to claim that such a cycle exists. An analysis of the influence of some key studies shows that their results are misleadingly cited and that there is resistance to the null conclusion.     

Multimodal communication by captive chimpanzees (Pan troglodytes)

Many studies have shown that apes and monkeys are adept at cross-modal matching tasks requiring the subject to identify objects in one modality when information regarding those objects has been presented in a different modality. However, much less is known about non-human primates’ production of multimodal signaling in communicative contexts. Here, we present evidence from a study of 110 chimpanzees demonstrating that they select the modality of communication in accordance with variations in the attentional focus of a human interactant, which is consistent with previous research. In each trial, we presented desirable food to one of two chimpanzees, turning mid-way through the trial from facing one chimpanzee to facing the other chimpanzee, and documented their communicative displays, as the experimenter turned towards or away from the subjects. These chimpanzees varied their signals within a context-appropriate modality, displaying a range of different visual signals when a human experimenter was facing them and a range of different auditory or tactile (attention-getting) signals when the human was facing away from them; this finding extends previous research on multimodal signaling in this species. Thus, in the impoverished circumstances characteristic of captivity, complex signaling tactics are nevertheless exhibited by chimpanzees, suggesting continuity in intersubjective psychological processes in humans and apes.     

Rhesus macaques (Macaca mulatta) as living fossils of hominoid personality and subjective well-being

Personality dimensions capturing individual differences in behavior, cognition, and affect have been described in several species, including humans, chimpanzees, and orangutans. However, comparisons between species are limited by the use of different questionnaires. We asked raters to assess free-ranging rhesus macaques at two time points on personality and subjective well-being questionnaires used earlier to rate chimpanzees and orangutans. Principal-components analysis yielded domains we labeled Confidence, Friendliness, Dominance, Anxiety, Openness, and Activity. The presence of Openness in rhesus macaques suggests it is an ancestral characteristic. The absence of Conscientiousness suggests it is a derived characteristic in African apes. Higher Confidence and Friendliness, and lower Anxiety were prospectively related to subjective well-being, indicating that the connection between personality and subjective well-being in humans, chimpanzees, and orangutans is ancestral in catarrhine primates. As demonstrated here, each additional species studied adds another fold to the rich, historical story of primate personality evolution.     

Aristotle's Cognitive Science: Belief,Affect and Rationality

I offer a novel interpretation of Aristotle's psychology and notion of rationality, which draws the line between animal and specifically human cognition. Aristotle distinguishes belief (doxa), a form of rational cognition, from imagining (phantasia), which is shared with non‐rational animals. We are, he says, “immediately affected” by beliefs, but respond to imagining “as if we were looking at a picture.” Aristotle's argument has been misunderstood; my interpretation explains and motivates it. Rationality includes a filter that interrupts the pathways between cognition and behavior. This prevents the subject from responding to certain representations. Stress and damage compromise the filter, making the subject respond indiscriminately, as non‐rational animals do. Beliefs are representations that have made it past the filter, which is why they can “affect [us] immediately.” Aristotle's claims express ceteris paribus generalizations, subject to exceptions. No list of provisos could turn them into non‐vacuous universal claims, but this does not rob them of their explanatory power. Aristotle's cognitive science resolves a tension we grapple with today: it accounts for the specialness of human action and thinking within a strictly naturalistic framework. The theory is striking in its insight and explanatory power, instructive in its methodological shortcomings.     

Human ostensive signals do not enhance gaze following in chimpanzees,but do enhance object-oriented attention

The previous studies have shown that human infants and domestic dogs follow the gaze of a human agent only when the agent has addressed them ostensively—e.g., by making eye contact, or calling their name. This evidence is interpreted as showing that they expect ostensive signals to precede referential information. The present study tested chimpanzees, one of the closest relatives to humans, in a series of eye-tracking experiments using an experimental design adapted from these previous studies. In the ostension conditions, a human actor made eye contact, called the participant’s name, and then looked at one of two objects. In the control conditions, a salient cue, which differed in each experiment (a colorful object, the actor’s nodding, or an eating action), attracted participants’ attention to the actor’s face, and then the actor looked at the object. Overall, chimpanzees followed the actor’s gaze to the cued object in both ostension and control conditions, and the ostensive signals did not enhance gaze following more than the control attention-getters. However, the ostensive signals enhanced subsequent attention to both target and distractor objects (but not to the actor’s face) more strongly than the control attention-getters—especially in the chimpanzees who had a close relationship with human caregivers. We interpret this as showing that chimpanzees have a simple form of communicative expectations on the basis of ostensive signals, but unlike human infants and dogs, they do not subsequently use the experimenter’s gaze to infer the intended referent. These results may reflect a limitation of non-domesticated species for interpreting humans’ ostensive signals in inter-species communication.     

Chimpanzee (Pan troglodytes) intentional communication is not contingent upon food

Studies of great apes have revealed that they use manual gestures and other signals to communicate about distal objects. There is also evidence that chimpanzees modify the types of communicative signals they use depending on the attentional state of a human communicative partner. The majority of previous studies have involved chimpanzees requesting food items from a human experimenter. Here, these same communicative behaviors are reported in chimpanzees requesting a tool from a human observer. In this study, captive chimpanzees were found to gesture, vocalize, and display more often when the experimenter had a tool than when she did not. It was also found that chimpanzees responded differentially based on the attentional state of a human experimenter, and when given the wrong tool persisted in their communicative efforts. Implications for the referential and intentional nature of chimpanzee communicative signaling are discussed.