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.

William Hopkins and David Washburn pay tribute to a pioneer in primatology and comparative psychology.

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.

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.

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.

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.

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.

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.

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.

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.

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.

Voxel-based morphometry (VBM) has become an increasingly common method for assessing neuroanatomical asymmetries in human in vivo magnetic resonance imaging (MRI). Here, we employed VBM to examine asymmetries in white matter in a sample of 48 chimpanzees (15 males and 33 females). T1-weighted MRI scans were segmented into white matter using FSL and registered to a common template. The segmented volumes were then flipped in the left-right axis and registered back to the template. The mirror image white matter volumes were then subtracted from the correctly oriented volumes and voxel-by-voxel t tests were performed. Twenty-seven significant lateralized clusters were found, including 18 in the left hemisphere and 9 in the right hemisphere. Several of the asymmetries were found in regions corresponding to well-known white matter tracts including the superior longitudinal fasciculus, inferior longitudinal fasciculus and corticospinal tract.

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.

Human language is distinctive compared with the communication systems of other species. Yet, several questions concerning its emergence and evolution remain unresolved. As a means of evaluating the neuroanatomical changes relevant to language that accompanied divergence from the last common ancestor of chimpanzees, bonobos and humans, we defined the cytoarchitectonic boundaries of area Tpt, a component of Wernicke's area, in 12 common chimpanzee brains and used design-based stereologic methods to estimate regional volumes, total neuron number and neuron density. In addition, we created a probabilistic map of the location of area Tpt in a template chimpanzee brain coordinate space. Our results show that chimpanzees display significant population-level leftward asymmetry of area Tpt in terms of neuron number, with volume asymmetry approaching significance. Furthermore, asymmetry in the number of neurons in area Tpt was positively correlated with asymmetry of neuron numbers in Brodmann's area 45, a component of Broca's frontal language region. Our findings support the conclusion that leftward asymmetry of Wernicke's area originated prior to the appearance of modern human language and before our divergence from the last common ancestor. Moreover, this study provides the first evidence of covariance between asymmetry of anterior and posterior cortical regions that in humans are important to language and other higher order cognitive functions.

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.

This study examined the influence of experimenter position on hand use in gestural communication in a sample of 127 captive chimpanzees. Hand use in gestural communication was recorded while an experimenter was positioned either left, right, or directly in front of the subject. The type of gesture was also recorded as either a food beg or whole hand point. Both hand use and gesture were consistent across experimenter positions. Overall, a significant population-level right hand bias was found, particularly for food beg gestures. These results are consistent with previous findings in chimpanzees and suggest that lateralisation in gestural communication is left hemisphere dominant.

This study examined the communicative behavior of 49 captive chimpanzees (Pan troglodytes), particularly their use of vocalizations, manual gestures, and other auditory- or tactile-based behaviors as a means of gaining an inattentive audience’s attention. A human (Homo sapiens) experimenter held a banana while oriented either toward or away from the chimpanzee. The chimpanzees’ behavior was recorded for 60 s. Chimpanzees emitted vocalizations faster and were more likely to produce vocalizations as their 1st communicative behavior when a human was oriented away from them. Chimpanzees used manual gestures more frequently and faster when the human was oriented toward them. These results replicate the findings of earlier studies on chimpanzee gestural communication and provide new information about the intentional and functional use of their vocalizations.

Behavioral laterality in head orientation while sleeping in either a supine or prone posture was examined in 43 chimpanzees (Pan troglodytes) for the first 3 months of life. An overall significant right-side lateral bias was found for head orientation in the supine posture. A trend toward greater right-side bias in females compared with males was observed but failed to reach significance. These data suggest that asymmetries in head orientation are present early in life in chimpanzees, and they may be correlated with functional asymmetries observed in adulthood.

Heritability of hand preference was tested in a sample of 188 chimpanzees (Pan troglodytes). Hand preference was measured by coordinated bimanual actions, and concordance percentages were compared between parents and offspring and siblings. Among siblings, concordance percentages were compared for dyads in which both individuals were raised by chimpanzees, both were raised by humans, or 1 was raised in each environment. The results indicated population-level right hand preferences for coordinated bimanual actions. There were no significant associations in hand preference between parents and offspring. In full and maternal half siblings, concordance in hand preference was significantly greater than chance in mother- and human-reared individuals but not in cross-fostered dyads. The cumulative results suggest that the direction of hand preference is heritable in chimpanzees but the mechanism of transmission is not genetic. Several environmental explanations are proposed to explain the findings, including the potential role of maternal cradling bias and in utero fetal position.

Hand preferences for a coordinated bimanual task were assessed in a sample of 31 captive gorillas (Gorilla gorilla) and 19 captive orangutans (Pongo pygmaeus) and were compared with chimpanzee (Pan troglodytes) hand preferences in subjects that were matched on the basis of age, sex, and rearing history. The task required that the apes remove food from the inside edges of a symmetrical polyvinyl chloride pipe presented to them in their home cages. The results indicate significant species differences with chimpanzees showing population-level right-handedness and orangutans showing population-level left-handedness. The gorillas showed a nonsignificant trend toward right-handedness. The results are discussed in terms of possible ecological or biomechanical factors that may influence hand preferences in different ape species.

This article describes the distribution and development of handedness for manual gestures in captive chimpanzees. Data on handedness for unimanual gestures were collected in a sample of 227 captive chimpanzees. Handedness for these gestures was compared with handedness for three other measures of hand use: tool use, reaching, and coordinated bimanual actions. Chimpanzees were significantly more right-handed for gestures than for all other measures of hand use. Hand use for simple reaching at 3 to 4 years of age predicted hand use for gestures 10 years later. Use of the right hand for gestures was significantly higher when gestures were accompanied by a vocalization than when they were not. The collective results suggest that left-hemisphere specialization for language may have evolved initially from asymmetries in manual gestures in the common ancestor of chimpanzees and humans, rather than from hand use associated with other, noncommunicative motor actions, including tool use and coordinated bimanual actions, as has been previously suggested in the literature.