Primate Cognition Test Battery Research Articles

Interaction-Mediated Tool Use Differently Enhances Physical and Social Cognition in Macaques (Macaca fascicularis)

In primates, learning to use a tool modulates cognitive functions related to the physical properties of objects. However, the impact of tool-use learning on social aspects of cognition has not been explored. We addressed this question via a training paradigm by using six, adult, long-tailed macaques (Macaca fascicularis), who were born in captivity and housed in the animal facility of the Department of Neuroscience and Rehabilitation of the University of Ferrara, Italy. We tested the effects of interaction-mediated tool use on overall cognitive performance in an experimental group (n = 2 males and n = 1 females). To evaluate changes in cognitive performance, we applied the Primate Cognition Test Battery at different stages of the training procedure that involved an interaction between the animal and an experimenter and the macaque using a rake to retrieve food items. As a control, we evaluated the performance of an age- and sex-matched group performing an interactive, manual grasping task. Several parameters related to the recognition of the position and noise of specific objects (i.e., space and causality in physical cognition), and those related to image-object association and object pointing to draw the attention of experimenter (i.e., communication aspects of social cognition) showed a significant improvement in the interaction-mediated tool-use group after the training period. The effects were transient, but the enhancement related to the noise and object pointing persisted for 35 days without further training. The control group showed no changes in cognitive performance. Our results show that interaction-mediated tool use enhances cognitive performance in both physical and social cognition domains.

Age, adrenal steroids, and cognitive functioning in captive chimpanzees (Pan troglodytes).

Dehydroepiandrosterone-sulfate is the most abundant circulating androgen in humans and other catarrhines. It is involved in several biological functions, such as testosterone production, glucocorticoid antagonist actions, neurogenesis and neuroplasticty. Although the role of dehydroepiandrosterone-sulfate (DHEAS) in cognition remains elusive, the DHEAS/cortisol ratio has been positively associated with a slower cognitive age-decline and improved mood in humans. Whether this relationship is found in nonhuman primates remains unknown. We measured DHEAS and cortisol levels in serum of 107 adult chimpanzees to investigate the relationship between DHEAS levels and age. A subset of 21 chimpanzees was used to test the potential associations between DHEAS, cortisol, and DHEAS/cortisol ratio in cognitive function, taking into account age, sex, and their interactions. We tested for cognitive function using the primate cognitive test battery (PCTB) and principal component analyses to categorize cognition into three components: spatial relationship tasks, tool use and social communication tasks, and auditory-visual sensory perception tasks. DHEAS levels, but not the DHEAS/cortisol ratio, declined with age in chimpanzees. Our analyses for spatial relationships tasks revealed a significant, positive correlation with the DHEAS/cortisol ratio. Tool use and social communication had a negative relationship with age. Our data show that the DHEAS/cortisol ratio, but not DHEAS individually, is a promising predictor of spatial cognition in chimpanzees.

Ravens parallel great apes in physical and social cognitive skills

Human children show unique cognitive skills for dealing with the social world but their cognitive performance is paralleled by great apes in many tasks dealing with the physical world. Recent studies suggested that members of a songbird family—corvids—also evolved complex cognitive skills but a detailed understanding of the full scope of their cognition was, until now, not existent. Furthermore, relatively little is known about their cognitive development. Here, we conducted the first systematic, quantitative large-scale assessment of physical and social cognitive performance of common ravens with a special focus on development. To do so, we fine-tuned one of the most comprehensive experimental test-batteries, the Primate Cognition Test Battery (PCTB), to raven features enabling also a direct, quantitative comparison with the cognitive performance of two great ape species. Full-blown cognitive skills were already present at the age of four months with subadult ravens’ cognitive performance appearing very similar to that of adult apes in tasks of physical (quantities, and causality) and social cognition (social learning, communication, and theory of mind). These unprecedented findings strengthen recent assessments of ravens’ general intelligence, and aid to the growing evidence that the lack of a specific cortical architecture does not hinder advanced cognitive skills. Difficulties in certain cognitive scales further emphasize the quest to develop comparative test batteries that tap into true species rather than human specific cognitive skills, and suggest that socialization of test individuals may play a crucial role. We conclude to pay more attention to the impact of personality on cognitive output, and a currently neglected topic in Animal Cognition—the linkage between ontogeny and cognitive performance.

Age-related changes in chimpanzee (Pan troglodytes) cognition: Cross-sectional and longitudinal analyses.

Chimpanzees are the species most closely related to humans, yet age-related changes in brain and cognition remain poorly understood. The lack of studies on age-related changes in cognition in chimpanzees is particularly unfortunate in light of the recent evidence demonstrating that this species naturally develops Alzheimer's disease (AD) neuropathology. Here, we tested 213 young, middle-aged, and elderly captive chimpanzees on the primate cognitive test battery (PCTB), a set of 13 tasks that assess physical and social cognition in nonhuman primates. A subset of these chimpanzees (n = 146) was tested a second time on a portion of the PCTB tasks as a means of evaluating longitudinal changes in cognition. Cross-sectional analyses revealed a significant quadratic association between age and cognition with younger and older chimpanzees performing more poorly than middle-aged individuals. Longitudinal analyses showed that the oldest chimpanzees at the time of the first test showed the greatest decline in cognition, although the effect was mild. The collective data show that chimpanzees, like other nonhuman primates, show age-related decline in cognition. Further investigations into whether the observed cognitive decline is associated with AD pathologies in chimpanzees would be invaluable in understanding the comparative biology of aging and neuropathology in primates.

The lemur baseline: how lemurs compare to monkeys and apes in the Primate Cognition Test Battery.

Primates have relatively larger brains than other mammals even though brain tissue is energetically costly. Comparative studies of variation in cognitive skills allow testing of evolutionary hypotheses addressing socioecological factors driving the evolution of primate brain size. However, data on cognitive abilities for meaningful interspecific comparisons are only available for haplorhine primates (great apes, Old- and New World monkeys) although strepsirrhine primates (lemurs and lorises) serve as the best living models of ancestral primate cognitive skills, linking primates to other mammals. To begin filling this gap, we tested members of three lemur species (Microcebus murinus, Varecia variegata, Lemur catta) with the Primate Cognition Test Battery, a comprehensive set of experiments addressing physical and social cognitive skills that has previously been used in studies of haplorhines. We found no significant differences in cognitive performance among lemur species and, surprisingly, their average performance was not different from that of haplorhines in many aspects. Specifically, lemurs’ overall performance was inferior in the physical domain but matched that of haplorhines in the social domain. These results question a clear-cut link between brain size and cognitive skills, suggesting a more domain-specific distribution of cognitive abilities in primates, and indicate more continuity in cognitive abilities across primate lineages than previously thought.

Primate cognition test battery in parrots

Abstract Systematic, broad phylogenetic comparisons of diverse cognitive abilities are essential to understand cognitive evolution. Few studies have examined multiple skills comparatively, using identical tasks across species. Previous research centered on primates, but recent evidence suggests that complex cognition may have evolved in distantly related taxa. We administered the tasks of the primate cognition test battery (PCTB) to 4 parrot species for a first direct comparison with primates. The parrots did not perform significantly worse than the previously tested primates in all but one of the test scales, but remained at chance levels throughout. Chimpanzees outperformed them in the physical but not the social domain. No differences between the domains nor across the parrot species were detected. It remains questionable whether the chance level performance reflects the parrots’ cognitive capacity or results from task constraints, which would limit the suitability of PCTB for phylogenetic comparisons. Possible implications for the field are discussed.

Primate cognition test battery in parrots

AbstractSystematic, broad phylogenetic comparisons of diverse cognitive abilities are essential to understand cognitive evolution. Few studies have examined multiple skills comparatively, using identical tasks across species. Previous research centered on primates, but recent evidence suggests that complex cognition may have evolved in distantly related taxa. We administered the tasks of the primate cognition test battery (PCTB) to 4 parrot species for a first direct comparison with primates. The parrots did not perform significantly worse than the previously tested primates in all but one of the test scales, but remained at chance levels throughout. Chimpanzees outperformed them in the physical but not the social domain. No differences between the domains nor across the parrot species were detected. It remains questionable whether the chance level performance reflects the parrots’ cognitive capacity or results from task constraints, which would limit the suitability of PCTB for phylogenetic comparisons. Possible implications for the field are discussed.

Tool-use training temporarily enhances cognitive performance in long-tailed macaques (Macaca fascicularis).

Tool use relies on numerous cognitive functions, including sustained attention and understanding of causality. In this study, we investigated the effects of tool-use training on cognitive performance in primates. Specifically, we applied the Primate Cognition Test Battery to three long-tailed macaques (Macaca fascicularis) at different stages of a training procedure that consisted of using a rake to retrieve out-of-reach food items. In addition, we evaluated a control group (n = 3) performing a grasping task, in order to account for possible effects related to a simple motor act. Our results showed that tool-use training enhances mean performance in the physical cognition domain, i.e. the understanding of spatial relations, numerosity and causality. In particular, causal cognition (evaluating noise- and shape-related causality and understanding of tool properties) showed significant improvement after training, whereas spatial cognition (evaluating spatial memory, object permanence, rotation and transposition) showed a trend to improvement. Despite these findings, none of our trained monkeys succeeded in the tool-use task of the Primate Cognition Test Battery, which involved an unfamiliar tool. Some training-related effects did not persist after a 35-day resting period, suggesting that continuous practice may be necessary, or that a longer training period before resting may be needed to better maintain cognitive performance. In contrast with the training group, the control group did not display any change in cognitive performance. This finding paves the way to further investigation into the link between tool-use behaviour and the evolution of primate cognition.

Self-Control in Chimpanzees Relates to General Intelligence

For humans, there appears to be a clear link between general intelligence and self-control behavior, such as sustained delay of gratification [1-9]. Chimpanzees also delay gratification [10-12] and can be given tests of general intelligence (g) [13-15], but these two constructs have never been compared within the same sample of nonhuman animals. We presented 40 chimpanzees with the hybrid delay task (HDT) [16, 17], which measures inter-temporal choices and the capacity for sustained delay of gratification, and the primate cognitive test battery (PCTB), which measures g in chimpanzees [13-15]. Importantly, none of the sub-tasks in the PCTB directly assesses self-control or other forms of behavioral inhibition. Rather, they assess areas of physical cognition (e.g., quantity discrimination) or social cognition (e.g., gaze following). In three phases of testing, we consistently found that the strongest relation was between chimpanzee g scores and efficiency in the HDT. Chimpanzee g was not most closely related to the proportion of trials the chimpanzees chose to try to wait for delayed rewards, but rather most closely related to how good they were at waiting for those rewards when they chose to do so. We also found the same strong relation between HDT efficiency and those factors in the PCTB that loaded most strongly on chimpanzee g. These results highlight that, as with humans, there is a strong relation between chimpanzees' self-control and overall intelligence-a relation that likely reflects the role of successful inhibitory control during cognitive processing of information and intelligent decision-making.

The association between imitation recognition and socio-communicative competencies in chimpanzees (Pan troglodytes).

Imitation recognition provides a viable platform from which advanced social cognitive skills may develop. Despite evidence that non-human primates are capable of imitation recognition, how this ability is related to social cognitive skills is unknown. In this study, we compared imitation recognition performance, as indicated by the production of testing behaviors, with performance on a series of tasks that assess social and physical cognition in 49 chimpanzees. In the initial analyses, we found that males were more responsive than females to being imitated and engaged in significantly greater behavior repetitions and testing sequences. We also found that subjects who consistently recognized being imitated performed better on social but not physical cognitive tasks, as measured by the Primate Cognitive Test Battery. These findings suggest that the neural constructs underlying imitation recognition are likely associated with or among those underlying more general socio-communicative abilities in chimpanzees. Implications regarding how imitation recognition may facilitate other social cognitive processes, such as mirror self-recognition, are discussed.

Chimpanzee Intelligence Is Heritable

The role that genes play in human intelligence or IQ has remained a point of significant scientific debate dating back to the time of Galton [1]. It has now become increasingly clear that IQ is heritable in humans, but these effects can be modified by nongenetic mechanisms [2-4]. In contrast to human IQ, until recently, views of learning and cognition in animals have largely been dominated by the behaviorist school of thought, originally championed by Watson [5] and Skinner [6]. A large body of accumulated research now demonstrates a variety of cognitive abilities in nonhuman animals and challenges traditional behaviorist interpretations of performance [7, 8]. This, in turn, has led to a renewed interest in the role that social and biological factors might play in explaining individual and phylogenetic differences in cognition [9]. Specifically, aside from early attempts to selectively breed for learning skills in rodents [10-12], studies examining the role that genetic factors might play in individual variation in cognitive abilities in nonhuman animals, particularly nonhuman primates, are scarce. Here, we utilized a modified Primate Cognitive Test Battery [13] in conjunction with quantitative genetic analyses to examine whether cognitive performance is heritable in chimpanzees. We found that some but not all cognitive traits were significantly heritable in chimpanzees. We further found significant genetic correlations between different dimensions of cognitive functioning, suggesting that the genes that explain the variability of one cognitive trait might also explain that of other cognitive traits.

Cognitive and motor aging in female chimpanzees

We present the first longitudinal data on cognitive and motor aging in the chimpanzee (Pan troglodytes). Thirty-eight adult female chimpanzees (10–54 years old) were studied. The apes were tested longitudinally for 3 years in a modified Primate Cognition Test Battery, which comprised 12 tests of physical and social cognition. The chimpanzees were also administered a fine motor task requiring them to remove a steel nut from rods of various complexity. There was little evidence for an age-related decline in tasks of Physical Cognition: for most tasks, performance was either stable or improved with repeated testing across age groups. An exception was Spatial Memory, for which 4 individuals more than 50 years old experienced a significant performance decline across the 3 years of testing. Poorer performance with age was found in 2 tasks of Social Cognition, an attention-getting task and a gaze-following task. A slight motor impairment was also observed, with old chimpanzees improving less than younger animals with repeated testing on the simplest rod. Hormonal status effects were restricted to spatial memory, with non-cycling females outperforming cycling females independently of age. Unexpectedly, older chimpanzees were better than younger individuals in understanding causality relationships based on sound.

Physical and social cognition in domestic dogs: A comparative study

Dogs have shown outstanding social cognitive skills when interacting with humans, especially in situations where social knowledge and communicative skills are needed. On the other hand, when tested on knowledge of objects or understanding of causality, domestic dogs did not prove to be particularly skilled and flexible when compared with other species. Brauer et al. (2006) showed that chimpanzees outperformed dogs in an object choice paradigm when causal cues were provided. However, chimpanzees failed to use social information given by the experimenter, whereas domestic dogs used several social communicative cues to receive a hidden food reward. To test whether these differences in performance hold true over a larger set of cognitive tests covering both physical and social cognition, we tested 97 domestic dogs modifying the Primate Cognition Test Battery (PCTB). This extensive test battery was developed by Herrmann et al. (2007) to investigate the cognitive abilities of great apes and human children and includes tests on knowledge of objects, quantities and causal understanding (physical domain) and social cognitive tasks like social learning, communication and knowledge of others’ actions and minds (social domain). Averaging across all of the tasks in the physical domain, dogs were correct in 45% of the trials, whereas chimpanzees succeeded in 68% of the trials. In the social domain, dogs performed correctly in 34% of the trials, and chimpanzees were correct in 39% of the trials. Statistically, chimpanzees outperformed dogs in physical cognitive tasks as well as in social cognitive tasks. Comparing the particular scales, we did find statistical differences between the species for all 3 scales of physical cognition as well as for tasks requiring knowledge of others’ actions and minds. Although domestic dogs and chimpanzees performed at a similar level over all communicative and social learning tasks, we did find species differences within single tasks. Our results show that chimpanzees outperform dogs not only in causal understanding, but also in a variety of other physical cognitive skills such as knowledge of space and Cognition 49