Sulcal Morphology in Cingulate Cortex is Associated with Voluntary Oro-Facial Motor Control and Gestural Communication in Chimpanzees (Pan troglodytes).

Individual differences in sulcal variation within the anterior and mid-cingulate cortex of the human brain, particularly the presence or absence of a paracingulate sulcus (PCGS), are associated with various motor and cognitive processes. Recently, it has been reported that chimpanzees possess a PCGS, previously thought to be a unique feature of the human brain. Here, we examined whether individual variation in the presence or absence of a PCGS as well as the variability in the intralimbic sulcus (ILS) are associated with oro-facial motor control, handedness for manual gestures, and sex in a sample of MRI scans obtained in 225 chimpanzees. Additionally, we quantified the depth of the cingulate sulcus (CGS) along the anterior-posterior axis and tested for association with oro-facial motor control, handedness, and sex. Chimpanzees with better oro-facial motor control were more likely to have a PCGS, particularly in the left hemisphere compared to those with poorer control. Male chimpanzees with better oro-facial motor control showed increased leftward asymmetries in the depth of the anterior CGS, whereas female chimpanzees showed the opposite pattern. Significantly, more chimpanzees had an ILS in the left compared to the right hemisphere, but variability in this fold was not associated with sex, handedness, or oro-facial motor control. Finally, significant population-level leftward asymmetries were found in the anterior portion of the CGS, whereas significant rightward biases were evident in the posterior regions. The collective results suggest that the emergence of a PCGS and enhanced gyrification within the anterior and mid-cingulate gyrus may have directly or indirectly evolved in response to selection for increasing oro-facial motor control in primates.

Predicting their past: Machine language learning can discriminate the brains of chimpanzees with different early-life social rearing experiences.

Early life experiences, including separation from caregivers, can result in substantial, persistent effects on neural, behavioral, and physiological systems as is evidenced in a long-standing literature and consistent findings across species, populations, and experimental models. In humans and other animals, differential rearing conditions can affect brain structure and function. We tested for whole brain patterns of morphological difference between 108 chimpanzees reared typically with their mothers (MR; N = 54) and those reared decades ago in a nursery with peers, human caregivers, and environmental enrichment (NR; N = 54). We applied support vector machine (SVM) learning to archival MRI images of chimpanzee brains to test whether we could, with any degree of significant probability, retrospectively classify subjects as MR and NR based on variation in gray matter within the entire brain. We could accurately discriminate MR and NR chimpanzee brains with nearly 70% accuracy. The combined brain regions discriminating the two rearing groups were widespread throughout the cortex. We believe this is the first report using machine language learning as an analytic method for discriminating nonhuman primate brains based on early rearing experiences. In this sense, the approach and findings are novel, and we hope they stimulate application of the technique to studies on neural outcomes associated with early experiences. The findings underscore the potential for infant separation from caregivers to leave a long-term mark on the developing brain.

Heritability of Gray Matter Structural Covariation and Tool Use Skills in Chimpanzees (Pan troglodytes): A Source-Based Morphometry and Quantitative Genetic Analysis.

Nonhuman primates, and great apes in particular, possess a variety of cognitive abilities thought to underlie human brain and cognitive evolution, most notably, the manufacture and use of tools. In a relatively large sample (N = 226) of captive chimpanzees (Pan troglodytes) for whom pedigrees are well known, the overarching aim of the current study was to investigate the source of heritable variation in brain structure underlying tool use skills. Specifically, using source-based morphometry (SBM), a multivariate analysis of naturally occurring patterns of covariation in gray matter across the brain, we investigated (1) the genetic contributions to variation in SBM components, (2) sex and age effects for each component, and (3) phenotypic and genetic associations between SBM components and tool use skill. Results revealed important sex- and age-related differences across largely heritable SBM components and associations between structural covariation and tool use skill. Further, shared genetic mechanisms appear to account for a heritable link between variation in both the capacity to use tools and variation in morphology of the superior limb of the superior temporal sulcus and adjacent parietal cortex. Findings represent the first evidence of heritability of structural covariation in gray matter among nonhuman primates.

Genetic Factors and Orofacial Motor Learning Selectively Influence Variability in Central Sulcus Morphology in Chimpanzees (Pan troglodytes).

Captive chimpanzees (Pan troglodytes) have been shown to learn the use of novel attention-getting (AG) sounds to capture the attention of humans as a means of requesting or drawing their attention to a desired object or food. There are significant individual differences in the use of AG sounds by chimpanzees and, here, we examined whether changes in cortical organization of the central sulcus (CS) were associated with AG sound production. MRI scans were collected from 240 chimpanzees, including 122 that reliably produced AG sounds and 118 that did not. For each subject, the depth of CS was quantified along the superior-inferior plane with specific interest in the inferior portion corresponding to the region of the motor cortex where the mouth and orofacial movements are controlled. Results indicated that CS depth in the inferior, but not superior, portion was significantly greater in chimpanzees that reliably produced AG sounds compared with those who did not. Quantitative genetic analyses indicated that overall CS surface area and depth were significantly heritable, particularly in the superior regions, but less so in the inferior and central portions. Further, heritability in CS depth was altered as a function of acquisition of AG sounds. The collective results suggest that learning to produce AG sounds resulted in region-specific cortical reorganization within the inferior portion of the CS, a finding previously undocumented in chimpanzees or any nonhuman primate.SIGNIFICANCE STATEMENT Recent studies in chimpanzees (Pan troglodytes) have shown that some can learn to produce novel sounds by configuring different orofacial movement patterns and these sounds are used in communicatively relevant contexts. Here, we examined the neuromorphological correlates in the production of these sounds in chimpanzees. We show that chimpanzees that have learned to produce these sounds show significant differences in central sulcus (CS) morphology, particularly in the inferior region. We further show that overall CS morphology and regions within the superior portion are significantly heritable, whereas central and inferior portions of the CS are not. The collective findings suggest chimpanzees exhibit cortical plasticity in regions of the brain that were central to the emergence of speech functions in humans.

Socially transmitted diffusion of a novel behavior from subordinate chimpanzees.

Chimpanzees (Pan troglodytes) demonstrate much cultural diversity in the wild, yet a majority of novel behaviors do not become group-wide traditions. Since many such novel behaviors are introduced by low-ranking individuals, a bias toward copying dominant individuals ("rank-bias") has been proposed as an explanation for their limited diffusion. Previous experimental work showed that chimpanzees (Pan troglodytes) preferentially copy dominant over low-rank models. We investigated whether low ranking individuals may nevertheless successfully seed a beneficial behavior as a tradition if there are no "competing" models. In each of four captive groups, either a single high-rank (HR, n = 2) or a low-rank (LR, n = 2) chimpanzee model was trained on one method of opening a two-action puzzle-box, before demonstrating the trained method in a group context. This was followed by 8 hr of group-wide, open-access to the puzzle-box. Successful manipulations and observers of each manipulation were recorded. Barnard's exact tests showed that individuals in the LR groups used the seeded method as their first-choice option at significantly above chance levels, whereas those in the HR groups did not. Furthermore, individuals in the LR condition used the seeded method on their first attempt significantly more often than those in the HR condition. A network-based diffusion analysis (NBDA) revealed that the best supported statistical models were those in which social transmission occurred only in groups with subordinate models. Finally, we report an innovation by a subordinate individual that built cumulatively on existing methods of opening the puzzle-box and was subsequently copied by a dominant observer. These findings illustrate that chimpanzees are motivated to copy rewarding novel behaviors that are demonstrated by subordinate individuals and that, in some cases, social transmission may be constrained by high-rank demonstrators.

Genetic basis in motor skill and hand preference for tool use in chimpanzees (Pan troglodytes).

Chimpanzees are well known for their tool using abilities. Numerous studies have documented variability in tool use among chimpanzees and the role that social learning and other factors play in their development. There are also findings on hand use in both captive and wild chimpanzees; however, less understood are the potential roles of genetic and non-genetic mechanisms in determining individual differences in tool use skill and laterality. Here, we examined heritability in tool use skill and handedness for a probing task in a sample of 243 captive chimpanzees. Quantitative genetic analysis, based on the extant pedigrees, showed that overall both tool use skill and handedness were significantly heritable. Significant heritability in motor skill was evident in two genetically distinct populations of apes, and between two cohorts that received different early social rearing experiences. We further found that motor skill decreased with age and that males were more commonly left-handed than females. Collectively, these data suggest that though non-genetic factors do influence tool use performance and handedness in chimpanzees, genetic factors also play a significant role, as has been reported in humans.

Distal Communication by Chimpanzees (Pan troglodytes): Evidence for Common Ground?

van der Goot et al. (2014) proposed that distal, deictic communication indexed the appreciation of the psychological state of a common ground between a signaler and a receiver. In their study, great apes did not signal distally, which they construed as evidence for the human uniqueness of a sense of common ground. This study exposed 166 chimpanzees to food and an experimenter, at an angular displacement, to ask, "Do chimpanzees display distal communication?" Apes were categorized as (a) proximal or (b) distal signalers on each of four trials. The number of chimpanzees who communicated proximally did not statistically differ from the number who signaled distally. Therefore, contrary to the claim by van der Goot et al., apes do communicate distally.

Age-related effects in the neocortical organization of chimpanzees: gray and white matter volume, cortical thickness, and gyrification.

Among primates, humans exhibit the most profound degree of age-related brain volumetric decline in particular regions, such as the hippocampus and the frontal lobe. Recent studies have shown that our closest living relatives, the chimpanzees, experience little to no volumetric decline in gray and white matter over the adult lifespan. However, these previous studies were limited with a small sample of chimpanzees of the most advanced ages. In the present study, we sought to further test for potential age-related decline in cortical organization in chimpanzees by expanding the sample size of aged chimpanzees. We used the BrainVisa software to measure total brain volume, gray and white matter volumes, gray matter thickness, and gyrification index in a cross-sectional sample of 219 captive chimpanzees (8-53 years old), with 38 subjects being 40 or more years of age. Mean depth and cortical fold opening of 11 major sulci of the chimpanzee brains were also measured. We found that chimpanzees showed increased gyrification with age and a cubic relationship between age and white matter volume. For the association between age and sulcus depth and width, the results were mostly non-significant with the exception of one negative correlation between age and the fronto-orbital sulcus. In short, results showed that chimpanzees exhibit few age-related changes in global cortical organization, sulcus folding and sulcus width. These findings support previous studies and the theory that the age-related changes in the human brain is due to an extended lifespan.

Neuroanatomical correlates of individual differences in the object choice task in chimpanzees (Pan troglodytes).

Declarative and imperative joint attention or joint engagement are important milestones in human infant development. These have been shown to be a significant predictor of later language development and are impaired in some individuals with, or at risk for, a diagnosis of autism spectrum disorder. Comparatively, while chimpanzees and other great apes have been reported to engage in imperative joint attention, evidence of declarative joint attention remains unclear based on existing studies. Some have suggested that differences in methods of assessing joint attention may have an influence on performance in nonhuman primates. Here, we report data on a measure of receptive joint attention (object choice task) in a sample of captive chimpanzees. Chimpanzees, as a group, performed significantly better than chance. By contrast, when considering individual performance, there was no significant difference in the number of those who passed and those who failed. Using quantitative genetic analyses, we found that performance on the object choice task was not significantly heritable nor were there any significant effects of sex, rearing history, or colony. Lastly, we found significant differences in gray matter covariation, between those who passed or failed the task. Those who passed contributed more to gray matter covariation in several brain regions within the social brain network, consistent with hypotheses regarding the importance of these regions in human and nonhuman primate social cognition.

Are conspecific social videos rewarding to chimpanzees (Pan troglodytes)? A test of the social motivation theory.

Many claim that social stimuli are rewarding to primates, but few, if any, studies have explicitly demonstrated their reward value. Here, we examined whether chimpanzees would produce overt responses for the opportunity to view conspecific social, compared to dynamic (video: Experiment 1) and static (picture: Experiment 2) control content. We also explored the relationships between variation in social reward and social behavior and cognition. We provided captive chimpanzees with access to a touchscreen during four, one-hour sessions (two 'conspecific social' and two 'control'). The sessions consisted of ten, 15-second videos (or pictures in Experiment 2) of either chimpanzees engaging in a variety of behaviors (social condition) or vehicles, humans, or other animals engaged in some activity (control condition). For each chimpanzee, we recorded the number of responses to the touchscreen and the frequency of watching the stimuli. Independent t-tests revealed no sex or rearing differences in touching and watching the social or control videos (p>0.05). Repeated measures ANOVAs showed chimpanzees touched and watched the screen significantly more often during the social compared to control video sessions. Furthermore, although chimpanzees did not touch the screen more often during social than control picture sessions in Experiment 2, they did watch the screen more often. Additionally, chimpanzees that previously performed better on a task of social cognition and engaged in more affiliative behavior watched a higher percentage of social videos during the touchscreen task. These results are consistent with the social motivation theory, and indicate social stimuli are intrinsically rewarding, as chimpanzees made more overt responses for the opportunity to view conspecific social, compared to control, content.

Endowment effects in chimpanzees.

Human behavior is not always consistent with standard rational choice predictions. Apparent deviations from rational choice predictions provide a promising arena for the merger of economics and biology [1-6]. Although little is known about the extent to which other species exhibit these seemingly irrational patterns [7-9], similarities across species would suggest a common evolutionary root to the phenomena. The present study investigated whether chimpanzees exhibit an endowment effect, a seemingly paradoxical behavior in which humans tend to value a good they have just come to possess more than they would have only a moment before [10-13]. We show the first evidence that chimpanzees do exhibit an endowment effect, by favoring items they just received more than their preferred items that could be acquired through exchange. Moreover, the effect is stronger for food than for less evolutionarily salient objects, perhaps because of historically greater risks associated with keeping a valuable item versus attempting to exchange it for another [14, 15]. These findings suggest that many seeming deviations from rational choice predictions may be common to humans and chimpanzees and that the evaluation of these through a lens of evolutionary relevance may yield further insights in humans and other species.

Differences in the mutual eye gaze of bonobos (Pan paniscus) and chimpanzees (Pan troglodytes).

Eye gaze is widespread in nonhuman primate taxa and important for social cognition and communicative signaling. Bonobos and chimpanzees, two closely related primate species, differ in social organization, behavior, and cognition. Chimpanzees' eye gaze and gaze following has been studied extensively, whereas less is known about bonobos' eye gaze. To examine species differences using a more ecologically relevant measure than videos or pictures, the current study compared bonobo and chimpanzee mutual eye gaze with a human observer. A multivariate analysis of variance revealed significant species differences in frequency and total duration, but not bout length, of mutual eye gaze (p < .001). Specifically, bonobos engage in mutual eye gaze more frequently and for longer total duration than chimpanzees. These results are likely related to species differences in social behavior and temperament and are consistent with eye-tracking studies in which bonobos looked at the eye region of conspecifics (in pictures and videos) longer than chimpanzees. Future research should examine the relationship between mutual eye gaze and gaze following, as well as examine its genetic and neurological correlates. (PsycInfo Database Record (c) 2020 APA, all rights reserved).

The role of early social rearing, neurological, and genetic factors on individual differences in mutual eye gaze among captive chimpanzees.

Mutual eye gaze plays an important role in primate social development and communication. In the current study, we examined the underlying experiential, genetic, and neuroanatomical basis of mutual eye gaze variation in adult captive chimpanzees. A multivariate analysis of variance revealed a significant rearing effect on bout length, with human-reared chimpanzees engaging in longer bouts of mutual gaze compared to mother-reared and wild-born individuals. Next, we utilized source-based morphometry (SBM) to examine gray matter covariation in magnetic resonance imaging scans and determine the relationship between the resulting gray matter covariation components and mutual eye gaze. One SBM component was negatively correlated with gaze duration (nucleus accumbens and anterior insular cortex), while two components were positively correlated with bout length (posterior cingulate cortex, inferior occipital cortex, middle temporal cortex, hippocampus, and the precentral sulcus). Finally, heritability analyses revealed mutual eye gaze to be modestly heritable and significant genetic correlations between bout length and two gray matter covariation components. This study reveals that non-genetic factors, and to a lesser extent, genetic factors appear to influence mutual eye gaze in adult chimpanzees, and is the first to report neuroanatomical correlates of mutual eye gaze variation in chimpanzees.

Chimpanzees (Pan troglodytes) do not develop contingent reciprocity in an experimental task.

Chimpanzees provide help to unrelated individuals in a broad range of situations. The pattern of helping within pairs suggests that contingent reciprocity may have been an important mechanism in the evolution of altruism in chimpanzees. However, correlational analyses of the cumulative pattern of interactions over time do not demonstrate that helping is contingent upon previous acts of altruism, as required by the theory of reciprocal altruism. Experimental studies provide a controlled approach to examine the importance of contingency in helping interactions. In this study, we evaluated whether chimpanzees would be more likely to provide food to a social partner from their home group if their partner had previously provided food for them. The chimpanzees manipulated a barpull apparatus in which actors could deliver rewards either to themselves and their partners or only to themselves. Our findings indicate that the chimpanzees' responses were not consistently influenced by the behavior of their partners in previous rounds. Only one of the 11 dyads that we tested demonstrated positive reciprocity. We conclude that contingent reciprocity does not spontaneously arise in experimental settings, despite the fact that patterns of behavior in the field indicate that individuals cooperate preferentially with reciprocating partners.

Further evidence of a left hemisphere specialization and genetic basis for tool use skill in chimpanzees (Pan troglodytes): Reproducibility in two genetically isolated populations of apes.

It has been hypothesized that the evolution of tool use may have served as a preadaptation for the emergence of left hemispheric specialization in motor skill in humans. Here, we tested for intermanual differences in performance on a tool use task in a sample of 206 captive chimpanzees in relation to their sex, age, and hand preference. In addition, we examined heritability in tool use skill for the entire sample, as well as within 2 genetically isolated populations of captive chimpanzees. This was done to determine the degree of reproducibility in heritability on motor performance. The results revealed a significant effect of hand preference on intermanual differences in performance. Right-handed chimpanzees performed the task more quickly with their right compared with left hand. In contrast, no significant intermanual differences in performance were found in left- and ambiguous-handed apes. Tool use performance was found to be significantly heritable for overall performance, as well as separately for the left and right hands. Further, significant heritability in tool use performance was found in both populations of apes, suggesting these results were reproducible. The results are discussed in the context of evolutionary theories of handedness and hemispheric specialization and the genetic mechanisms that underlie their expression in primates, including humans. (PsycINFO Database Record (c) 2019 APA, all rights reserved).

Motor skill for tool-use is associated with asymmetries in Broca's area and the motor hand area of the precentral gyrus in chimpanzees (Pan troglodytes).

Among nonhuman primates, chimpanzees are well known for their sophistication and diversity of tool use in both captivity and the wild. The evolution of tool manufacture and use has been proposed as a driving mechanism for the development of increasing brain size, complex cognition and motor skills, as well as the population-level handedness observed in modern humans. Notwithstanding, our understanding of the neurological correlates of tool use in chimpanzees and other primates remains poorly understood. Here, we assessed the hand preference and performance skill of chimpanzees on a tool use task and correlated these data with measures of neuroanatomical asymmetries in the inferior frontal gyrus (IFG) and the pli-de-passage fronto-parietal moyen (PPFM). The IFG is the homolog to Broca's area in the chimpanzee brain and the PPFM is a buried gyrus that connects the pre- and post-central gyri and corresponds to the motor-hand area of the precentral gyrus. We found that chimpanzees that performed the task better with their right compared to left hand showed greater leftward asymmetries in the IFG and PPFM. This association between hand performance and PPFM asymmetry was particularly robust for right-handed individuals. Based on these findings, we propose that the evolution of tool use was associated with increased left hemisphere specialization for motor skill. We further suggest that lateralization in motor planning, rather than hand preference per se, was selected for with increasing tool manufacture and use in Hominid evolution.

Sex differences in the relationship between planum temporale asymmetry and corpus callosum morphology in chimpanzees (Pan troglodytes): A combined MRI and DTI analysis.

Increases brain size has been hypothesized to be inversely associated with the expression of behavioral and brain asymmetries within and between species. We tested this hypothesis by analyzing the relation between asymmetries in the planum temporale (PT) and different measures of the corpus callosum (CC) including surface area, streamline count as measured from diffusion tensor imaging, fractional anisotropy values and the ratio in the number of fibers to surface area in a sample of chimpanzees. We found that chimpanzees with larger PT asymmetries in absolute terms had smaller CC surface areas, fewer streamlines and a smaller ratio of fibers to surface area. These results were largely specific to male but not female chimpanzees. Our results partially support the hypothesis that brain asymmetries are linked to variation in corpus callosum morphology, although these associations may be sex-dependent.

Social networks in primates: smart and tolerant species have more efficient networks.

Network optimality has been described in genes, proteins and human communicative networks. In the latter, optimality leads to the efficient transmission of information with a minimum number of connections. Whilst studies show that differences in centrality exist in animal networks with central individuals having higher fitness, network efficiency has never been studied in animal groups. Here we studied 78 groups of primates (24 species). We found that group size and neocortex ratio were correlated with network efficiency. Centralisation (whether several individuals are central in the group) and modularity (how a group is clustered) had opposing effects on network efficiency, showing that tolerant species have more efficient networks. Such network properties affecting individual fitness could be shaped by natural selection. Our results are in accordance with the social brain and cultural intelligence hypotheses, which suggest that the importance of network efficiency and information flow through social learning relates to cognitive abilities.