Neural changes that occurred during human evolution to support language are poorly understood. As a basis of comparison to humans, we used design-based stereological methods to estimate volumes, total neuron numbers, and neuron densities in Brodmann's areas 44 and 45 in both cerebral hemispheres of 12 chimpanzees (Pan troglodytes), one of our species’ closest living relatives. We found that the degree of interindividual variation in the topographic location and quantitative cytoarchitecture of areas 44 and 45 in chimpanzees was comparable to that seen in humans from previous studies. However, in contrast to the documented asymmetries in humans, we did not find significant population-level hemispheric asymmetry for any measures of areas 44 and 45 in chimpanzees. Furthermore, there was no relationship between asymmetries of stereological data and magnetic resonance imaging–based measures of inferior frontal gyrus morphology or hand preference on 2 different behavioral tasks. These findings suggest that Broca's area in the left hemisphere expanded in relative size during human evolution, possibly as an adaptation for our species’ language abilities.
cytoarchitecture; evolution; great ape; handedness; stereology
Magnetic resonance images of the brain were obtained from 2 gorillas (Gorilla gorilla gorilla), 4 orangutans (Pongo pygmaeus), 14 chimpanzees (Pan troglodytes), and 4 bonobos (Pan paniscus). The region on the motor cortex of humans identified as responsible for motor skill of the hand (the “knob”) was identified in this sample on consecutive 1-mm axial scans. The shape of the knob area was traced on each scan from both hemispheres, and the area from all scans was summed to calculate the knob volume. The width of the knob was also measured and correlated highly with knob volume. A significant population-level leftward asymmetry in the volume and width of the knob was revealed (p < .05). Species differences in knob asymmetry and overall volume were not significant, but the variability in overall volume between species was substantial. Selection for the evolution of a neuroanatomical representation of the hand in primates and an evolutionary trend toward population-level right handedness are discussed.
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
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
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
The planum temporale (PT) is the bank of tissue that lies posterior to Heschl’s gyrus and is considered a key 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 in approximately 2/3rds of individuals, particularly among right-handed individuals. Here we examined whether chimpanzees show asymmetries in the PT for grey matter volume and surface area in a sample of 103 chimpanzees from magnetic resonance images. The results indicated that, overall, the chimpanzees showed population-level leftward asymmetries for both surface area and grey matter volumes. Furthermore, chimpanzees that prefer to gesture with their right-handed had significantly greater leftward grey matter asymmetries compared to ambiguously- and left-handed apes. When compared to previously published data in humans, the direction and magnitude of PT grey matter asymmetries were similar between humans and apes; however, for the surface area measures, the human showed more pronounced leftward asymmetries. These results suggest that leftward asymmetries in the PT were present in the common ancestor of chimpanzees and humans.
chimpanzees; planum temporale; brain asymmetry; handedness; gestural communication
The evolutionary origin of human language and its neurobiological foundations has long been the object of intense scientific debate. Although a number of theories have been proposed, one particularly contentious model suggests that human language evolved from a manual gestural communication system in a common ape-human ancestor. Consistent with a gestural origins theory are data indicating that chimpanzees intentionally and referentially communicate via manual gestures, and the production of manual gestures, in conjunction with vocalizations, activates the chimpanzee Broca’s area homologue – a region in the human brain that is critical for the planning and execution of language. However, it is not known if this activity observed in the chimpanzee Broca’s area is the result of the chimpanzees producing manual communicative gestures, communicative sounds, or both. This information is critical for evaluating the theory that human language evolved from a strictly manual gestural system. To this end, we used positron emission tomography (PET) to examine the neural metabolic activity in the chimpanzee brain. We collected PET data in 4 subjects, all of whom produced manual communicative gestures. However, 2 of these subjects also produced so-called attention-getting vocalizations directed towards a human experimenter. Interestingly, only the two subjects that produced these attention-getting sounds showed greater mean metabolic activity in the Broca’s area homologue as compared to a baseline scan. The two subjects that did not produce attention-getting sounds did not. These data contradict an exclusive “gestural origins” theory for they suggest that it is vocal signaling that selectively activates the Broca’s area homologue in chimpanzees. In other words, the activity observed in the Broca’s area homologue reflects the production of vocal signals by the chimpanzees, suggesting thast this critical human language region was involved in vocal signaling in the common ancestor of both modern humans and chimpanzees.
Recent studies have shown that great ape species possess patterns of macrostructural neocortical asymmetries that are similar to those found in humans. However, little is known about the asymmetry of subcortical structures in great apes. To address this lack of data, the authors assessed left–right asymmetry of the anterior and posterior aspects of cerebellum from MRI brain scans of 53 chimpanzees (Pan troglodytes). No population-level bias was found for either the anterior or the posterior region of the cerebellum. However, a significant inverse association was found in the asymmetry quotients of the anterior and posterior regions, indicating that the cerebellum was torqued at the individual level. Additionally, handedness for tool use but not other measures was associated with variation in cerebellar asymmetries. Last, older chimpanzees had a smaller cerebellum after brain volume was adjusted for. The results are discussed in the context of brain changes in primate evolution related to tool use.
cerebellum; torque; tool use; handedness; chimpanzee
We examined the distribution of neurons immunoreactive for neuropeptide Y (NPY) in the posterior part of the superior temporal cortex (Brodmann's area 22 or area Tpt) of humans and nonhuman haplorrhine primates. NPY has been implicated in learning and memory and the density of NPY-expressing cortical neurons and axons is reduced in depression, bipolar disorder, schizophrenia, and Alzheimer's disease. Due to the role that NPY plays in both cognition and neurodegenerative diseases, we tested the hypothesis that the density of cortical and interstitial neurons expressing NPY was increased in humans relative to other primate species. The study sample included great apes (chimpanzee and gorilla), Old World monkeys (pigtailed macaque, moor macaque, and baboon) and New World monkeys (squirrel monkey and capuchin). Stereologic methods were used to estimate the density of NPY-immunoreactive (-ir) neurons in layers I-VI of area Tpt and the subjacent white matter. Adjacent Nissl-stained sections were used to calculate local densities of all neurons. The ratio of NPY-ir neurons to total neurons within area Tpt and the total density of NPY-ir neurons within the white matter were compared among species. Overall, NPY-ir neurons represented only an average of 0.006% of the total neuron population. While there were significant differences among species, phylogenetic trends in NPY-ir neuron distributions were not observed and humans did not differ from other primates. However, variation among species warrants further investigation into the distribution of this neuromodulator system.
Wernicke's area; area Tpt; area 22; evolution; NPY
The frontal operculum—classically considered to be Broca's area—has special significance and interest in clinical, cognitive, and comparative neuroscience given its role in spoken language and the long-held assumption that structural asymmetry of this region of cortex may be related to functional lateralization of human language. We performed a detailed morphological and morphometric analysis of this area of the brain in humans and chimpanzees using identical image acquisition parameters, image analysis techniques, and consistent anatomical boundaries in both species. We report great inter-individual variability of the sulcal contours defining the operculum in both species, particularly discontinuity of the inferior frontal sulcus in humans and bifurcation of the inferior precentral sulcus in chimpanzees. There was no evidence of population-based asymmetry of the frontal opercular gray matter in humans or chimpanzees. The diagonal sulcus was only identified in humans, and its presence was significantly (F = 12.782, p < 0.001) associated with total volume of the ipsilateral operculum. The findings presented here suggest that there is no population-based interhemispheric macroscopic asymmetry of Broca's area in humans or Broca's area homolog in chimpanzees. However, given that previous studies have reported asymmetry in the cytoarchitectonic fields considered to represent Broca's area—which is important given that cytoarchitectonic boundaries are more closely related to the regional functional properties of cortex relative to sulcal landmarks—it may be that the gross morphology of the frontal operculum is not a reliable indicator of Broca's area per se.
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.
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.
Determination of whether nonhuman primates exhibit neuroanatomical asymmetries would inform our understanding of the evolution of traits in humans that show functional hemispheric dominance, including language and handedness. Here we report the first evidence of population-level asymmetries in the chimpanzee neocortex using voxel-based morphology (VBM). MRI scans of the brain were collected in a sample of 31 chimpanzees including 9 males and 22 females, and the resulting images were segmented into gray matter, white matter and CSF. Gray matter images were then co-registered to a template and these normally oriented volumes were flipped on the left-right axis to create mirror volumes. In total, significant asymmetries were found in 13 regions including several that have been described previously in great apes using traditional region-of-interest approaches. The results from this VBM analysis support previous reports of hemispheric lateralization in chimpanzees and reinforce the view that asymmetries in the central nervous system are not uniquely human.
Our two closest living primate relatives, chimpanzees (Pan troglodytes) and bonobos (Pan paniscus), exhibit significant behavioral differences despite belonging to the same genus and sharing a very recent common ancestor. Differences have been reported in multiple aspects of social behavior, including aggression, sex, play and cooperation. However, the neurobiological basis of these differences has only been minimally investigated and remains uncertain. Here, we present the first ever comparison of chimpanzee and bonobo brains using diffusion tensor imaging, supplemented with a voxel-wise analysis of T1-weighted images to specifically compare neural circuitry implicated in social cognition. We find that bonobos have more gray matter in brain regions involved in perceiving distress in both oneself and others, including the right dorsal amygdala and right anterior insula. Bonobos also have a larger pathway linking the amygdala with the ventral anterior cingulate cortex, a pathway implicated in both top–down control of aggressive impulses as well as bottom–up biases against harming others. We suggest that this neural system not only supports increased empathic sensitivity in bonobos, but also behaviors like sex and play that serve to dissipate tension, thereby limiting distress and anxiety to levels conducive with prosocial behavior.
chimpanzee; bonobo; brain; social cognition
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
Neuroanatomical asymmetries have been identified in chimpanzee frontal and temporal lobes including regions believed to be homologous to human Broca's and Wernicke's areas. This study examined whether or not neuroanatomical asymmetries in chimpanzees are associated with hand use during gestural communication. Analyses revealed that those chimpanzees that reliably employ their right hand for manual gestures have larger inferior frontal gyri in the left hemisphere than those apes that do not show consistent hand use for gestures. These findings are the first to provide a direct link between neuroanatomical asymmetries and the production of lateralized communicative behavior in non-human primates.
chimpanzee; gesture; inferior frontal gyrus; language evolution; neuroanatomical asymmetry
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
The left hemisphere of the human brain is dominant in the production of speech and signed language. Whether similar lateralization of function for communicative signal production is present in other primates remains a topic of considerable debate. In the current study, we examined whether oro-facial movements associated with the production of learned attention-getting sounds are differentially lateralized compared to facial expressions associated with the production of species-typical emotional vocalizations in chimpanzees.
Methodology/ Principal Findings
Still images captured from digital video were used to quantify oro-facial asymmetries in the production of two attention-getting sounds and two species-typical vocalizations in a sample of captive chimpanzees. Comparisons of mouth asymmetries during production of these sounds revealed significant rightward biased asymmetries for the attention-getting sounds and significant leftward biased asymmetries for the species-typical sounds.
These results suggest that the motor control of oro-facial movements associated with the production of learned sounds is lateralized to the left hemisphere in chimpanzees. Furthermore, the findings suggest that the antecedents for lateralization of human speech may have been present in the common ancestor of chimpanzees and humans ∼5 mya and are not unique to the human lineage.
Heterochrony, or the evolution of ontogeny, has been well studied in embryology and skeletal development, providing insight into morphological and genetic mechanisms of evolution.1–5 However, heterochronic studies of behavior and cognition lag behind in comparison. In a recent study we investigated the ontogeny of social behavior and cognition in humans’ closest living relatives, chimpanzees (Pan troglodytes) and bonobos (Pan paniscus). These two species are estimated to have had a chimpanzeelike common ancestor between 0.86 and 1.8 mya.6,7 Bonobos have been argued to exhibit morphological indications of paedomorphism relative to chimpanzees, especially in the cranium, and to exhibit paedomorphic behavior as adults.6–11 We found that bonobos exhibit developmental delays relative to chimpanzees in several aspects of their social behavior and cognition. Here, we describe how placing these results in the framework of heterochrony contributes to understanding behavioral and cognitive differences between adults of these two species and to our knowledge of hominid evolution in general.
heterochrony; chimpanzee; bonobo; behavior; cognition; ontogeny; evolution
A comparative study of chimpanzee (Pan troglodytes) and capuchin monkey (Cebus apella) cerebellar asymmetry and its relationship to handedness was conducted. Magnetic resonance images of the brain and behavioral data on a coordinated bimanual task were obtained from 16 chimpanzees and 11 capuchins. Chimpanzees displayed a greater rightward bias of the posterior cerebellum and capuchins displayed a greater leftward bias of the anterior cerebellum. Cerebellar asymmetries were significantly associated with handedness in capuchins but not chimpanzees, and this effect was most pronounced in right-handed capuchins.
Handedness; asymmetry; cerebellum; chimpanzees; capuchins
The neurobiology of handedness is still poorly understood in nonhuman primates. Recently, an association between hand preference and precentral gyrus morphology in chimpanzees was reported. The aim of this study was to further evaluate the association between handedness and asymmetries in the precentral gyrus of chimpanzees (Pan troglodytes) and to evaluate the association between hand preference and brain asymmetry using a different approach to the classification of handedness in chimpanzees. The overall results suggest that differences in handedness groups are specific to a region of the precentral gyrus commonly known as the “knob” and that subjects that show different hand preferences differ in brain asymmetries for specific regions of the primary motor cortex. Moreover, using a continuous scale of measurement rather than discrete classification of handedness, significant associations were found between hand use and asymmetries within the precentral gyrus.
Handedness; Chimpanzees; Asymmetry; Precentral gyrus; Primary motor cortex
It has been suggested from studies in human subjects that sex, handedness, and brain asymmetries influence variation in corpus callosum (CC) size and these differences reflect the degree of connectivity between homotopic regions of the left and right cerebral hemispheres. Here we report that handedness is associated with variation in the size of the CC in chimpanzees. We further report that variation in brain asymmetries in a cortical region homologous to Broca's area is associated with the size of the CC but differs for right- and left-handed individuals. Collectively, the results suggest that individual differences in functional and neuroanatomical asymmetries are associated with CC variation not just in humans but also in chimpanzees and therefore may reflect a common neural basis for laterality in these 2 species.
brain asymmetry; chimpanzees; corpus callosum; handedness
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
Magnetic resonance imaging was used to measure the hippocampal and amygdalar volumes of 60 chimpanzees (Pan troglodytes). An asymmetry quotient (AQ) was then used to calculate the asymmetry for each of the structures. A one-sample t test indicated that there was a population-level right hemisphere asymmetry for the hippocampus. There was no significant population-level asymmetry for the amygdala. An analysis of variance using sex and rearing history as between-group variables showed no significant main effects or interaction effects on the AQ scores; however, males were more strongly lateralized than females. Several of these findings are consistent with results found in the human literature.