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.
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
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 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.
William Hopkins and David Washburn pay tribute to a pioneer in primatology and comparative psychology.
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
Animals vary in their dispositions, abilities, and moods and demonstrate characteristic behavior patterns that remain consistent across situation and time. This study describes the relationship between measures of personality in the chimpanzee and the structure of the subgenual cingulate cortex (SGCC). Measures of individual traits and personality factors (dominance, extraversion, conscientiousness, and agreeableness) and assessments of percentage of SGCC gray matter (PGM) and asymmetry taken from MRI scans were obtained for 74 chimpanzees housed at the Yerkes National Primate Research Center. PGM in the SGCC was significantly higher for females than for males and was significantly correlated with two personality factors (dominance and conscientiousness) in male apes. There was also a population-level leftward asymmetry in the SGCC. These results are discussed in terms of current models of SGCC function, which suggest that this area may play a role in the biological foundation of personality.
Brain asymmetries, particularly asymmetries within regions associated with language, have been suggested as a key difference between humans and our nearest ancestors. These regions include the planum temporale (PT) - the bank of tissue that lies posterior to Heschl’s gyrus and encompasses Wernicke’s area, an important brain region involved in language and speech in the human brain. In the human brain, both the surface area and grey matter volume of the PT is larger in the left compared to right hemisphere, particularly among right-handed individuals. Here we compared the grey matter volume and asymmetry of the PT in chimpanzees and three other species of nonhuman primate in two Genera including vervet monkeys (Chlorocebus aethiops sabaeus), rhesus macaques (Macaca mulatta) and bonnet macaques (Macaca radiata). We show that the three monkey species do not show population-level asymmetries in this region whereas the chimpanzees do, suggesting that the evolutionary brain development that gave rise to PT asymmetry occurred after our split with the monkey species, but before our split with the chimpanzees.
nonhuman primates; planum temporale; brain asymmetry; laterality; language evolution
Whether or not nonhuman primates exhibit population-level handedness remains a topic of considerable scientific debate. Here, we examined handedness for coordinated bimanual actions in a sample of 777 great apes including chimpanzees, bonobos, gorillas, and orangutans. We found population-level right-handedness in chimpanzees, bonobos and gorillas, but left-handedness in orangutans. Directional biases in handedness were consistent across independent samples of apes within each genus. We suggest that, contrary to previous claims, population-level handedness is evident in great apes but differs among species as a result of ecological adaptations associated with posture and locomotion. We further suggest that historical views of nonhuman primate handedness have been too anthropocentric, and we advocate for a larger evolutionary framework for the consideration of handedness and other aspects of hemispheric specialization among primates.
Great apes; handedness; asymmetry; laterality; language evolution
The acquisition of linguistic competency from more experienced social partners is a fundamental aspect of human language. However, there is little evidence that non-human primates learn to use their vocalizations from social partners. Captive chimpanzees (Pan troglodytes) produce idiosyncratic vocal signals that are used intentionally to capture the attention of a human experimenter. Interestingly, not all apes produce these sounds, and it is unclear what factors explain this difference. We tested the hypothesis that these attention-getting (AG) sounds are socially learned via transmission between mothers and their offspring. We assessed 158 chimpanzees to determine if they produced AG sounds. A significant association was found between mother and offspring sound production. This association was attributable to individuals who were raised by their biological mother—as opposed to those raised by humans in a nursery environment. These data support the hypothesis that social learning plays a role in the acquisition and use of communicative vocal signals in chimpanzees.
chimpanzee; vocal learning; language evolution
Humans throw right-handed, and it has been suggested that the neurophysiological demands of aimed throwing may have served as a precursor to the evolution of left hemisphere specialization for linguistic functions. Although there are descriptions of throwing by wild and captive chimpanzees (Pan troglodytes), systematic observations of aimed throwing and handedness have not been reported. In this article, evidence of population-level right-handedness for throwing is reported in 2 samples of captive chimpanzees. It is further reported that right-handed throwing is more pronounced than other measures of handedness in captive chimpanzees. The implications of these findings are discussed in the context of theories relating throwing to the evolution of lateralization for language functions.
It has been hypothesized that cognitive mechanisms underlying lateralized complex motor actions associated with tool use in chimpanzees may have set the stage for the evolution of left-hemisphere specialization for language and speech in humans. Here we report evidence that asymmetries in the homologues to Broca’s and Wernicke’s areas are associated with handedness for tool use in chimpanzees. These results suggest that the neural substrates of tool use may have served as a preadaptation for the evolution of language and speech in modern humans.
Understanding the evolutionary origins of hemispheric specialization remains a topic of considerable interest in a variety of scientific disciplines. Whether nonhuman primates exhibit population-level limb preferences continues to be a controversial topic. In this study, limb preferences for ascending and descending locomotion were assessed as a means of examining the hypothesis that asymmetries in forelimb bones might be attributed to asymmetries in posture. The results indicated that captive chimpanzees showed a population-level leftward asymmetry in descending locomotion but no group bias for ascending locomotion. The results are consistent with previous behavioral studies in captive chimpanzees as well as studies on skeletal asymmetries of the forelimbs of chimpanzees.
laterality; posture; locomotion; chimpanzees
The corpus callosum (CC) is the largest commissural white matter tract in mammalian brains, connecting homotopic and heterotopic regions of the cerebral cortex. Knowledge of the distribution of callosal fibers projecting into specific cortical regions has important implications for understanding the evolution of lateralized structures and functions of the cerebral cortex. No comparisons of CC topography in humans and great apes have yet been conducted. We investigated the topography of the CC in 21 chimpanzees using high-resolution magnetic resonance imaging (MRI) and diffusion tensor imaging (DTI). Tractography was conducted based on fiber assignment by continuous tracking (FACT) algorithm. We expected chimpanzees to display topographical organization similar to humans, especially concerning projections into the frontal cortical regions. Similar to recent studies in humans, tractography identified five clusters of CC fibers projecting into defined cortical regions: prefrontal; premotor and supplementary motor; motor; sensory; parietal, temporal and occipital. Significant differences in fractional anisotropy (FA) were found in callosal regions, with highest FA values in regions projecting to higher-association areas of posterior cortical (including parietal, temporal and occipital cortices) and prefrontal cortical regions (p<0.001). The lowest FA values were seen in regions projecting into motor and sensory cortical areas. Our results indicate chimpanzees display similar topography of the CC as humans, in terms of distribution of callosal projections and microstructure of fibers as determined by anisotropy measures.
It has been hypothesized that neurological adaptations associated with evolutionary selection for throwing may have served as a precursor for the emergence of language and speech in early hominins. Although there are reports of individual differences in aimed throwing in wild and captive apes, to date there has not been a single study that has examined the potential neuroanatomical correlates of this very unique tool-use behaviour in non-human primates. In this study, we examined whether differences in the ratio of white (WM) to grey matter (GM) were evident in the homologue to Broca's area as well as the motor-hand area of the precentral gyrus (termed the KNOB) in chimpanzees that reliably throw compared with those that do not. We found that the proportion of WM in Broca's homologue and the KNOB was significantly higher in subjects that reliably throw compared with those that do not. We further found that asymmetries in WM within both brain regions were larger in the hemisphere contralateral to the chimpanzee's preferred throwing hand. We also found that chimpanzees that reliably throw show significantly better communication abilities than chimpanzees that do not. These results suggest that chimpanzees that have learned to throw have developed greater cortical connectivity between primary motor cortex and the Broca's area homologue. It is suggested that during hominin evolution, after the split between the lines leading to chimpanzees and humans, there was intense selection on increased motor skills associated with throwing and that this potentially formed the foundation for left hemisphere specialization associated with language and speech found in modern humans.
throwing; Broca's area; chimpanzees
Whether lateralization of communicative signalling in non-human primates might constitute prerequisites of hemispheric specialization for language is unclear. In the present study, we examined (i) hand preference for a communicative gesture (clapping in 94 captive chimpanzees from two research facilities) and (ii) the in vivo magnetic resonance imaging brain scans of 40 of these individuals. The preferred hand for clapping was defined as the one in the upper position when the two hands came together. Using computer manual tracing of regions of interest, we measured the neuroanatomical asymmetries for the homologues of key language areas, including the inferior frontal gyrus (IFG) and planum temporale (PT). When considering the entire sample, there was a predominance of right-handedness for clapping and the distribution of right- and left-handed individuals did not differ between the two facilities. The direction of hand preference (right- versus left-handed subjects) for clapping explained a significant portion of variability in asymmetries of the PT and IFG. The results are consistent with the view that gestural communication in the common ancestor may have been a precursor of language and its cerebral substrates in modern humans.
handedness; gestural communication; hemispheric specialization; origins of language; primates
While numerous publications have shown that apes can learn some aspects of human language, one frequently cited difference between humans and apes is the relative infrequency of declaratives (comments and statements) as opposed to imperatives (requests) in ape symbol use. This paper describes the use of declaratives in three language-competent apes and two children. The apes produced a lower proportion of spontaneous declaratives than did the children. However, both groups used declaratives to name objects, to interact and negotiate, and to make comments about other individuals. Both apes and children also made comments about past and future events. However, showing/offering/giving, attention getting, and comments on possession were declarative types made by the children but rarely by the apes.
Chimpanzees produce numerous species-atypical signals when raised in captivity. Here we report contextual elements of the use of two captivity-specific vocal signals, the “raspberry” and the extended grunt. Results demonstrate that these vocalizations are not elicited by the presence of food; rather the data suggest that these vocalizations function as attention-getting signals. These findings demonstrate a heretofore underappreciated category of animal signals: novel signals invented in novel environmental circumstances. The invention and use of species-atypical signals, considered in relation to group differences in signaling repertoires in apes in their natural habitats, may index a generative capacity in these hominoid species without obvious corollary in other primate species.
The central sulcus (CS) divides primary motor and sensory cortex in many mammalian brains. Recent studies have shown that experiential factors can influence the volume and lateralization of the CS in both human and nonhuman primates. In this study, we sought to define specific landmarks and the depth of the CS region corresponding to the motor-hand area of chimpanzees for comparison with humans using a novel, observer independent method applied to sample of 32 MRI scans. Our results showed that the dorsal-ventral location of the motor-hand region is comparable between humans and chimpanzees, though the depth of the CS was significantly greater in humans compared to chimpanzees. We further found that CS area corresponding to the motor-hand area was significantly larger in the hemisphere contralateral to the chimpanzees preferred hand. The methods employed here offer some potential advantages over traditional region-of-interest in the comparative study of cortical organization and gyrification in primates and are discussed.