The study of hominin brain evolution relies mostly on evaluation of the endocranial morphology of fossil skulls. However, only some general features of external brain morphology are evident from endocasts, and many anatomical details can be difficult or impossible to examine. In this study, we use geometric morphometric techniques to evaluate inter- and intraspecific differences in cerebral morphology in a sample of in vivo magnetic resonance imaging scans of chimpanzees and humans, with special emphasis on the study of asymmetric variation. Our study reveals that chimpanzee–human differences in cerebral morphology are mainly symmetric; by contrast, there is continuity in asymmetric variation between species, with humans showing an increased range of variation. Moreover, asymmetric variation does not appear to be the result of allometric scaling at intraspecific levels, whereas symmetric changes exhibit very slight allometric effects within each species. Our results emphasize two key properties of brain evolution in the hominine clade: first, evolution of chimpanzee and human brains (and probably their last common ancestor and related species) is not strongly morphologically constrained, thus making their brains highly evolvable and responsive to selective pressures; second, chimpanzee and, especially, human brains show high levels of fluctuating asymmetry indicative of pronounced developmental plasticity. We infer that these two characteristics can have a role in human cognitive evolution.
chimpanzee; hominin; EvoDevo; geometric morphometrics; neuroanatomy
In the past 20–25 years, there have been a number of studies published on handedness in nonhuman primates. The goal of these studies has been to evaluate whether monkeys and apes show patterns of hand preference that resemble the right-handedness found in the human species. The extant findings on handedness in nonhuman primates have revealed inconsistent evidence for population-level handedness within and between species. In this article, I discuss some of the methodological and statistical challenges to comparative studies of handedness in human and nonhuman primates. I further offer a framework for developing some consensus on evaluating the validity of different handedness measures and the characterization of individual hand preferences.
handedness; primates; laterality; measurement validity; comparative analysis
Most humans are right-handed and, like many behavioral traits, there is good evidence that genetic factors play a role in handedness. Many researchers have argued that nonhuman animal limb or hand preferences are not under genetic control but instead are determined by random, non-genetic factors. We used quantitative genetic analyses to estimate the genetic and environmental contributions to three measures of chimpanzee handedness. Results revealed significant population-level handedness for two of the three measures --- the tube task and manual gestures. Furthermore, significant additive genetic effects for the direction and strength of handedness were found for all three measures, with some modulation due to early social rearing experiences. These findings challenge historical and contemporary views of the mechanisms underlying handedness in nonhuman animals.
Many historical and contemporary theorists have proposed that population-level behavioral and brain asymmetries are unique to humans and evolved as a consequence of human-specific adaptations such as language, tool manufacture and use, and bipedalism. Recent studies in nonhuman animals, notably primates, have begun to challenge this view. Here, I summarize comparative data on neuroanatomical asymmetries in the planum temporale (PT) and inferior frontal gyrus (IFG) of humans and chimpanzees, regions considered the morphological equivalents to Broca’s and Wernicke’s areas. I also review evidence of population-level handedness in captive and wild chimpanzees. When similar methods and landmarks are used to define the PT and IFG, humans and chimpanzees show similar patterns of asymmetry in both cortical regions, though humans show more pronounced directional biases. Similarly, there is good evidence that chimpanzees show population-level handedness, though, again, the expression of handedness is less robust compared to humans. These results stand in contrast to reported claims of significant differences in the distribution of handedness in humans and chimpanzees, and I discuss some possible explanations for the discrepancies in the neuroanatomical and behavioral data.
brain asymmetry; language; handedness
Lack of independence of data points or the pooling fallacy has been suggested as a potential problem in the study of handedness in nonhuman primates, particularly as it relates to whether hand use responses should be recorded as individual events or bouts of activity. Here, I argue that there is no evidence that the concept of statistical independence of data points or the pooling fallacy is a problem in the evaluation of population-level handedness in previous studies in nonhuman primates. I further argue these statistical concepts have been misapplied to the characterization of individual hand preferences. Finally, I argue that recording hand use responses as bouts rather than events has no significant effect on reports of hand use in nonhuman primates and, in fact, may unintentionally bias hand use toward the null hypothesis. Several suggestions for improvement in the measurement and statistical determination of individual handedness are offered in the paper.
Handedness; Nonhuman primates; Methods; Statistics
In developing human children, joint attention is an important preverbal skill fundamental to the development of language. Poor joint attention skills have been described as a behavioral risk factor for some neurodevelopmental disorders, such as autism spectrum disorder. It has been hypothesized that the anterior cingulate cortex (ACC) plays an important role in the development of joint attention in human children. Here, we tested whether the morphometry and lateralization of the ACC differed between chimpanzees that were classified as either consistently or inconsistently engaging in joint attention with a human experimenter. Results showed that chimpanzees that performed poorly on the joint attention task had larger grey matter volumes in the ACC compared to apes that performed well on the task. In addition, both population-level asymmetries and sex differences in the volume of GM were found within the ACC. Specifically, females had relatively larger GM volumes in two of the three subregions of the ACC compared to males, and significant leftward asymmetries were found for two of the subregions whereas a rightward biases was observed in the third. Based on these findings, we suggest that the ACC plays in important role in mediating joint attention, not just in humans, but also chimpanzees. We further suggest that the differences found between groups may reflect inherent differences in the amount of white matter within the ACC, thereby suggesting reduced connectivity between the ACC and other cortical regions in chimpanzees with poor joint attention skills.
One of the major contributions of recent personality psychology is the finding that traits are related to each other in an organized hierarchy. To date, however, researchers have yet to investigate this hierarchy in nonhuman primates. Such investigations are critical in confirming the cross-species nature of trait personality helping to illuminate personality as neurobiologically-based and evolutionarily-derived dimensions of primate disposition. Investigations of potential genetic polymorphisms associated with hierarchical models of personality among nonhuman primates represent a critical first step. The current study examined the hierarchical structure of chimpanzee personality as well as sex-specific associations with a polymorphism in the promoter region of the vasopressin V1a receptor gene (AVPR1A), a gene associated with dispositional traits, among 174 chimpanzees. Results confirmed a hierarchical structure of personality across species and, despite differences in early rearing experiences, suggest a sexually dimorphic role of AVPR1A polymorphisms on hierarchical personality profiles at a higher-order level.
We examined the relationship of corpus callosum morphology and organization to hand preference and performance on a motor skill task in chimpanzees. Handedness was assessed using a complex tool use task that simulated termite fishing. Chimpanzees were initially allowed to perform the task wherein they could choose which hand to use (preference measure); then they were required to complete trials using each hand (performance measure). Two measures were used to assess the corpus callosum: midsagittal area obtained from in vivo magnetic resonance images and density of transcallosal connections as determined by fractional anisotropy values obtained from diffusion tensor imaging. We hypothesized that chimpanzees would perform better on their preferred hand compared to the non-preferred hand, and that strength of behavioral lateralization (rather the direction) on this task would be negatively correlated to regions of the corpus callosum involved in motor processing. Our results indicate that the preferred hand was the most adept hand. Performance asymmetries correlated with FA measures but not area measures of the CC.
Corpus callosum; DTI; chimpanzee; handedness; tool use
Recent advances in structural magnetic resonance imaging technology and analysis now allows for accurate in vivo measurement of cortical thickness, an important aspect of cortical organization that has historically only been conducted on post-mortem brains. In this study, for the first time, we examined regional and lateralized cortical thickness in a sample of 71 chimpanzees for comparison to previously reported findings in humans. We also measured grey and white matter volumes for each subject. The results indicated that chimpanzees showed significant regional variation in cortical thickness with lower values in primary motor and sensory cortex compared to association cortex. Furthermore, chimpanzees showed significant rightward asymmetries in cortical thickness for a number of regions of interest throughout the cortex and leftward asymmetries in white but not grey matter volume. We also found that total and region specific cortical thickness was significantly negatively correlated with white matter volume. Thus, chimpanzees with greater white matter volumes had thinner cortical thickness. The collective findings are discussed within the context of previous findings in humans and theories on the evolution of cortical organization and lateralization in primates.
A left larger than right planum temporale (PT) is a neuroanatomical asymmetry common to both humans and chimpanzees. A similar asymmetry was observed in the human parietal operculum (PO), and the convergence of PT and PO asymmetries is strongly associated with right-handedness. Here, we assessed whether this combination also exists in common chimpanzees. Magnetic resonance scans were obtained in 83 captive subjects. PT was quantified following procedures previously employed and PO was defined as the maximal linear distance between the end point of the sylvian fissure and the central sulcus. Handedness was assessed using 2 tasks that were designed to simulate termite fishing of wild chimpanzees and to elicit bimanual coordination without tool use. Chimpanzees showed population-level leftward asymmetries for both PT and PO. As in humans, these leftward asymmetries were not correlated. Handedness for tool use but not for nontool use motor actions mediated the expression of asymmetries in PT and PO, with right-handed apes showing more pronounced leftward asymmetries. Consistent PT and PO asymmetry combinations were observed in chimpanzees. The proportions of individuals showing these combinations were comparable in humans and chimpanzees; however, interaction between handedness and patterns of combined PO and PT asymmetries differed between the 2 species.
apes; brain asymmetries; handedness; parietal operculum; planum temporale
Clinical and experimental data have implicated the posterior superior temporal gyrus as an important cortical region in the processing of socially relevant stimuli such as gaze following, eye direction, and head orientation. Gaze following and responding to different socio-communicative signals is an important and highly adaptive skill in primates, including humans. Here, we examined whether individual differences in responding to socio-communicative cues was associated with variation in either gray matter (GM) volume and asymmetry in a sample of chimpanzees. Magnetic resonance image scans and behavioral data on receptive joint attention (RJA) was obtained from a sample of 191 chimpanzees. We found that chimpanzees that performed poorly on the RJA task had less GM in the right compared to left hemisphere in the posterior but not anterior superior temporal gyrus. We further found that middle-aged and elderly chimpanzee performed more poorly on the RJA task and had significantly less GM than young-adult and sub-adult chimpanzees. The results are consistent with previous studies implicating the posterior temporal gyrus in the processing of socially relevant information.
joint attention; chimpanzees; superior temporal gyrus; brain asymmetry in cognition; brain development
Despite their genetic similarity to humans, our understanding of the role of genes on cognitive traits in chimpanzees remains virtually unexplored. Here, we examined the relationship between genetic variation in the arginine vasopressin V1a receptor gene (AVPR1A) and social cognition in chimpanzees. Studies have shown that chimpanzees are polymorphic for a deletion in a sequence in the 5′ flanking region of the AVPR1A, DupB, which contains the variable RS3 repetitive element, which has been associated with variation in social behavior in humans. Results revealed that performance on the social cognition task was significantly heritable. Furthermore, males with one DupB+ allele performed significantly better and were more responsive to socio-communicative cues than males homozygous for the DupB- deletion. Performance on a non-social cognition task was not associated with the AVPR1A genotype. The collective findings show that AVPR1A polymorphisms are associated with individual differences in performance on a receptive joint attention task in chimpanzees.
Although the basic morphological characteristics of neurons in the cerebellar cortex have been documented in several species, virtually nothing is known about the quantitative morphological characteristics of these neurons across different taxa. To that end, the present study investigated cerebellar neuronal morphology among eight different, large-brained mammalian species comprising a broad phylogenetic range: afrotherians (African elephant, Florida manatee), carnivores (Siberian tiger, clouded leopard), cetartiodactyls (humpback whale, giraffe) and primates (human, common chimpanzee). Specifically, several neuron types (e.g., stellate, basket, Lugaro, Golgi, and granule neurons; N = 317) of the cerebellar cortex were stained with a modified rapid Golgi technique and quantified on a computer-assisted microscopy system. There was a 64-fold variation in brain mass across species in our sample (from clouded leopard to the elephant) and a 103-fold variation in cerebellar volume. Most dendritic measures tended to increase with cerebellar volume. The cerebellar cortex in these species exhibited the trilaminate pattern common to all mammals. Morphologically, neuron types in the cerebellar cortex were generally consistent with those described in primates (Fox et al., 1967) and rodents (Palay and Chan-Palay, 1974), although there was substantial quantitative variation across species. In particular, Lugaro neurons in the elephant appeared to be disproportionately larger than those in other species. To explore potential quantitative differences in dendritic measures across species, MARSplines analyses were used to evaluate whether species could be differentiated from each other based on dendritic characteristics alone. Results of these analyses indicated that there were significant differences among all species in dendritic measures.
dendrite; morphometry; Golgi method; brain evolution; cerebellum
There remain considerable questions regarding the evidence for population-level handedness in nonhuman primates when compared with humans. One challenge in comparing human and nonhuman primate handedness involves the procedures used to characterize individual handedness. Studies of human handedness use consistency in hand use within and between tasks as a basis for hand preference classification. In contrast, studies of handedness in nonhuman primates use statistical criteria for classifying handedness. In this study, we examined within- and between-task consistency in hand use as a means of characterizing individual handedness in a sample of 300 captive chimpanzees (Pan troglodytes). Chimpanzees showed population-level right-handedness for both within- and between-tasks consistency, though the proportion of right-handed chimpanzees was lower than what has typically been reported for humans. We further found that there were small, but significant, associations in hand use between measures. There were no significant sex or colony effects on the distribution of handedness. The results are discussed in the context of theories on the evolution of handedness in nonhuman primates.
handedness; chimpanzees; motor skill; evolution; primates
There is considerable interest in comparative research on different species’ abilities to respond to human communicative cues such as gaze and pointing. It has been reported that some canines perform significantly better than monkeys and apes on tasks requiring the comprehension of either declarative or imperative pointing and these differences have been attributed to domestication in dogs. Here we tested a sample of chimpanzees on a task requiring comprehension of an imperative request and show that, though there are considerable individual differences, the performance by the apes rival those reported in pet dogs. We suggest that small differences in methodology can have a pronounced influence on performance on these types of tasks. We further suggest that basic differences in subject sampling, subject recruitment and rearing experiences have resulted in a skewed representation of canine abilities compared to those of monkeys and apes.
Studies involving oro-facial asymmetries in nonhuman primates have largely demonstrated a right hemispheric dominance for communicative signals and conveyance of emotional information. A recent study on chimpanzee reported the first evidence of significant left-hemispheric dominance when using attention-getting sounds and rightward bias for species-typical vocalizations (Losin, Russell, Freeman, Meguerditchian, Hopkins & Fitch, 2008). The current study sought to extend the findings from Losin et al. (2008) with additional oro-facial assessment in a new colony of chimpanzees. When combining the two populations, the results indicated a consistent leftward bias for attention-getting sounds and a right lateralization for species-typical vocalizations. Collectively, the results suggest that both voluntary- controlled oro-facial and gestural communication might share the same left-hemispheric specialization and might have coevolved into a single integrated system present in a common hominid ancestor.
Hemispheric specialization; Oro-facial asymmetry; Communicative behaviors; Gestural communication; Oro-facial communication; Emotions; Primates
The corpus callosum (CC) is the major white matter tract that connects the two cerebral hemispheres. Some have theorized that individual differences in behavioral and brain asymmetries are linked to variation in the density of axon fibers that traverse different sections of the CC. In this study, we examined whether variation in axon fiber density in the CC was associated with variation in asymmetries in the planum temporale (PT) in a sample of 20 post-mortem chimpanzee brains. We further tested for sex differences in small and large CC fiber proportions and density in the chimpanzees. We found that the distribution of small and large fibers within the CC of chimpanzees follows a similar pattern to those reported in humans. We also found that chimpanzees with larger asymmetries in the PT had fewer large fibers in the posterior portion of the CC, particularly among females. As has been reported in human brains, the findings reported here indicate that individual differences in brain asymmetries are associated with variation in interhemispheric connectivity as manifest in axon fiber density and size.
Chimpanzees; brain asymmetry; corpus callosum; axon fiber density; planum temporale
Functional and neuroanatomical asymmetries are an important characteristic of the human brain. The evolution of such specializations in the human cortex has provoked great interest in primate brain evolution. Most research on cortical sulci has revolved around linear measurements, which represent only one dimension of sulci organization. Here, we used a software program (BrainVISA) to quantify asymmetries in cortical depth and surface area from magnetic resonance images in a sample of 127 chimpanzees and 49 macaques. Population brain asymmetries were determined from 11 sulci in chimpanzees and seven sulci in macaques. Sulci were taken from the frontal, temporal, parietal, and occipital lobes. Population-level asymmetries were evident in chimpanzees for several sulci, including the fronto-orbital, superior precentral, and sylvian fissure sulci. The macaque population did not reveal significant population-level asymmetries, except for surface area of the superior temporal sulcus. The overall results are discussed within the context of the evolution of higher order cognition and motor functions.
Chimpanzee; Brain asymmetry; Sulci morphology
Vasopressin is a neuropeptide that has been strongly implicated in the development and evolution of complex social relations and cognition in mammals. Recent studies in voles have shown that polymorphic variation in the promoter region of the arginine vasopressin V1a receptor gene (avpr1a) is associated with different dimensions of sociality. In humans, variation in a repetitive sequence element in the 5’ flanking region of the AVPR1A, known as RS3, have also been associated with variation in AVPR1a gene expression, brain activity and social behavior. Here, we examined the association of polymorphic variation in this same 5’ flanking region of the AVPR1A on subjective ratings of personality in a sample of 83 chimpanzees (Pan troglodytes). Initial analyses indicated that 34 females and 19 males were homozygous for the short allele, which lacks RS3(DupB−/−); while 18 females and 12 males were heterozygous and thus had one copy of the long allele containing RS3 (DupB+/−), yielding overall allelic frequencies of 0.82 for the DupB− allele and 0.18 for the DupB+ allele. DupB+/+ chimpanzees were excluded from the analysis due to the limited number of individuals. Results indicated no significant sex difference in personality between chimpanzees homozygous for the deletion of the RS3-containing DupB region (DupB−/−); however, among chimpanzees carrying one allele with the DupB present (DupB+/−), males had significantly higher dominance and lower conscientiousness scores than females. These findings are the first evidence showing that the AVPR1A gene plays a role in different aspects of personality in male and female chimpanzees.
Handedness is a defining feature of human manual skill and understanding the origin of manual specialization remains a central topic of inquiry in anthropology and other sciences. In this study, we examined hand preference in a sample of wild primates on a task that requires bimanual coordinated actions (tube task) that has been widely used in captive primates. The Sichuan snub-nosed monkey (Rhinopithecus roxellana) is an arboreal Old World monkey species that is endemic to China, and 24 adult individuals from the Qinling Mountains of China were included for the analysis of hand preference in the tube task. All subjects showed strong individual hand preferences and significant group-level left-handedness was found. There were no significant differences between males and females for either direction or strength of hand preference. Strength of hand preferences of adults was significantly greater than juveniles. Use of the index finger to extract the food was the dominant extractive-act. Our findings represent the first evidence of population-level left-handedness in wild Old World monkeys, and broaden our knowledge on evaluating primate hand preference via experimental manipulation in natural conditions.
Bimanual coordination; Hand preference; Task complexity
The neurobiology of hand preferences in nonhuman primates is poorly understood. In this study, the authors report the 1st evidence of an association between hand preference and precentral gyrus morphology in chimpanzees (Pan troglodytes). Hand preferences did not significantly correlate with other asymmetric brain regions associated with language functions in humans including the planum temporale and frontal operculum. The overall results suggest that homologous regions of the motor cortex control hand preferences in humans and apes and that these functions evolved independently of left-hemisphere specialization for language and speech.
Increased connectivity of higher-order association regions in the neocortex has been proposed as a defining feature of human brain evolution. At present, however, there are limited comparative data to examine this claim fully. We tested the hypothesis that the distribution of neuropil across areas of the neocortex of humans differs from that of one of our closest living relatives, the common chimpanzee. The neuropil provides a proxy measure of total connectivity within a local region because it is comprised mostly of dendrites, axons, and synapses. Using image analysis techniques, we quantified the neuropil fraction from both hemispheres in six cytoarchitectonically defined regions including frontopolar cortex (area 10), Broca’s area (area 45), frontoinsular cortex (area FI), primary motor cortex (area 4), primary auditory cortex (area 41/42), and the planum temporale (area 22). Our results demonstrate that humans exhibit a unique distribution of neuropil in the neocortex compared to chimpanzees. In particular, the human frontopolar cortex and the frontoinsular cortex had a significantly higher neuropil fraction than the other areas. In chimpanzees these prefrontal regions did not display significantly more neuropil, but the primary auditory cortex had a lower neuropil fraction than other areas. Our results support the conclusion that enhanced connectivity in the prefrontal cortex accompanied the evolution of the human brain. These species differences in neuropil distribution may offer insight into the neural basis of human cognition, reflecting enhancement of the integrative capacity of the prefrontal cortex.
cytoarchitecture; evolution; brain; asymmetry
The two species of Pan, bonobos and common chimpanzees, have been reported to have different social organization, cognitive and linguistic abilities and motor skill, despite their close biological relationship. Here, we examined whether bonobos and chimpanzee differ in selected brain regions that may map to these different social and cognitive abilities. Eight chimpanzees and eight bonobos matched on age, sex and rearing experiences were magnetic resonance images scanned and volumetric measures were obtained for the whole brain, cerebellum, striatum, motor-hand area, hippocampus, inferior frontal gyrus and planum temporale. Chimpanzees had significantly larger cerebellum and borderline significantly larger hippocampus and putamen, after adjusting for brain size, compared with bonobos. Bonobos showed greater leftward asymmetries in the striatum and motor-hand area compared with chimpanzees. No significant differences in either the volume or lateralization for the so-called language homologs were found between species. The results suggest that the two species of Pan are quite similar neurologically, though some volumetric and lateralized differences may reflect inherent differences in social organization, cognition and motor skills.
brain evolution; bonobos; chimpanzees; laterality; cognition
Learning a new motor skill with one hand typically results in performance improvements in the alternate hand. The neural substrates involved with this skill acquisition are poorly understood. We combined behavioral testing and non-invasive brain imaging to study how the organization of the corpus callosum was related to intermanual transfer performance in chimpanzees. Fifty-three chimpanzees were tested for intermanual transfer of learning using a bent-wire task. Magnetic resonance and diffusion tensor images were collected from 39 of these subjects. The dominant hand showed greater performance benefits than the nondominant hand. Further, performance was associated with structural integrity of the motor and sensory regions of the CC. Subjects with better intermanual transfer of learning had lower fractional anisotropy values. The results are consistent with the callosal access model of motor programming.
intermanual transfer; manual performance; fractional anisotropy; chimpanzees
William Hopkins and David Washburn pay tribute to a pioneer in primatology and comparative psychology.