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ABSTRACT ObjectivesMost human brains exhibit left hemisphere asymmetry for planum temporale (PT) surface area and gray matter volume, which is interpreted as cerebral lateralization for language. Once considered a uniquely human feature, PT asymmetries have now been documented in chimpanzees and olive baboons. The goal of the current study was to further investigate the evolution of PT asymmetries in nonhuman primates. Materials and MethodsWe measured PT surface area in chimpanzees (Pan troglodytes,n = 90), bonobos (Pan paniscus,n = 21), gorillas (Gorilla gorilla,n = 34), orangutans (Pongospp.,n = 33), olive baboons (Papio anubis,n = 105), rhesus macaques (Macaca mulatta,n = 144), and tufted capuchins (Sapajus apella,n = 29) from magnetic resonance imaging scans. ResultsOur findings reveal significant leftward biases in PT surface area among chimpanzees, gorillas, olive baboons, rhesus macaques, and capuchins. We did not find significant population‐level asymmetries among orangutans and bonobos, which could be due, in part, to small sample sizes. We also detected significant age effects for rhesus macaques only, and no significant sex effects for any species. DiscussionThe observation of a population‐level leftward bias for PT surface area among not only hominids (chimpanzees and gorillas), but also two cercopithecoids (olive baboons and rhesus macaques) and one platyrrhine (tufted capuchins) suggests that PT lateralization was likely present in some early anthropoid primate ancestors and relatives. This provides further evidence that human brains have since undergone changes to the size and connectivity of the PT in response to selection for the cognitive processes needed to support the evolution of language and speech. 

Abstract Among human and nonhuman primates, mutual eye gaze (MEG) and gaze following are believed to be important for social cognition and communicative signaling. The goals of this study were to examine how early rearing experiences contribute to individual variation in MEG and to examine the potential role of genetic factors underlying this variation. Subjects included 93 female and 23 male baboons (Papio anubis) ranging from 3 to 20 years of age. Within the sample, there were 55 mother‐reared (MR) and 61 nursery‐reared (NR) baboons. MEG was assessed in four 60‐s test sessions. For each session, the duration, frequency, and bout length were recorded. Mean values were then calculated for each individual from the four sessions. A multivariate analysis of covariance revealed an overall significant main effect for rearing. Subsequent univariate analyses revealed significant rearing effects on mean bout length, but not mean duration or mean frequency, with MR baboons having longer bout lengths compared to NR baboons. Furthermore, mean bout length was found to be significantly heritable. These results indicate that rearing experiences, and to a small extent, genetic factors, affect patterns of mutual eye gaze ‐ in particular, bout length. These results differ from previous findings in MR and NR chimpanzees, further suggesting that rearing may impact MEG in a species‐specific manner that reflects the function of gaze in different primate species. 

Abstract Autism spectrum disorder (ASD) is a developmental disorder characterized by stereotypies or repetitive behaviors and impairments in social behavior and socio-communicative skills. One hallmark phenotype of ASD is poor joint attention skills compared to neurotypical controls. In addition, individuals with ASD have lower scores on several of the Big 5 personality dimensions, including Extraversion. Here, we examine these traits in a nonhuman primate model (chimpanzees;Pan troglodytes) to further understand the relationship between personality and joint attention skills, as well as the genetic and neural systems that contribute to these phenotypes. We used archival data including receptive joint attention (RJA) performance, personality based on caretaker ratings, and magnetic resonance images from 189 chimpanzees. We found that, like humans, chimpanzees who performed worse on the RJA task had lower Extraversion scores. We also found that joint attention skills and several personality dimensions, including Extraversion, were significantly heritable. There was also a borderline significant genetic correlation between RJA and Extraversion. A conjunction analysis examining gray matter volume showed that there were five main brain regions associated with both higher levels of Extraversion and social cognition. These regions included the right posterior middle and superior temporal gyrus, bilateral inferior frontal gyrus, left inferior frontal sulcus, and left superior frontal sulcus, all regions within the social brain network. Altogether, these findings provide further evidence that chimpanzees serve as an excellent model for understanding the mechanisms underlying social impairment related to ASD. Future research should further examine the relationship between social cognition, personality, genetics, and neuroanatomy and function in nonhuman primate models. 

Abstract Joint attention (JA) is an important milestone in human infant development and is predictive of the onset of language later in life. Clinically, it has been reported that children at risk for or with a diagnosis of autism spectrum disorder (ASD) perform more poorly on measures of JA compared to neurotypical controls. JA is not unique to humans but has also been reported in great apes and to a lesser extent in more distantly related monkeys. Further, individual differences in JA among chimpanzees are associated with polymorphisms in the vasopressin and oxytocin genes,AVPR1AandOXTR. Here, we tested whether individual variation in DNA methylation ofOXTRandAVPR1Awere associated with performance on JA tasks in chimpanzees. We found that individual differences in JA performance was associated withAVPR1Amethylation, but notOXTRmethylation in the chimpanzees. The collective results provide further evidence of the role ofAVPR1Ain JA abilities in chimpanzees. The results further suggest that methylation values forAVPR1Amay be useful biomarkers for identifying individuals at risk for ASD or related neurodevelopmental disorders associated with impairments in JA abilities. 

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. Independentt-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. 

Methylation levels have been shown to change with age at sites across the human genome. Change at some of these sites is so consistent across individuals that it can be used as an ‘epigenetic clock’ to predict an individual's chronological age to within a few years. Here, we examined how the pattern of epigenetic ageing in chimpanzees compares with humans. We profiled genome-wide blood methylation levels by microarray for 113 samples from 83 chimpanzees aged 1–58 years (26 chimpanzees were sampled at multiple ages during their lifespan). Many sites (greater than 65 000) showed significant change in methylation with age and around one-third (32%) of these overlap with sites showing significant age-related change in humans. At over 80% of sites showing age-related change in both species, chimpanzees displayed a significantly faster rate of age-related change in methylation than humans. We also built a chimpanzee-specific epigenetic clock that predicted age in our test dataset with a median absolute deviation from known age of only 2.4 years. However, our chimpanzee clock showed little overlap with previously constructed human clocks. Methylation at CpGs comprising our chimpanzee clock showed moderate heritability. Although the use of a human microarray for profiling chimpanzees biases our results towards regions with shared genomic sequence between the species, nevertheless, our results indicate that there is considerable conservation in epigenetic ageing between chimpanzees and humans, but also substantial divergence in both rate and genomic distribution of ageing-associated sites. This article is part of the theme issue ‘Evolution of the primate ageing process'.