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1.  Multimodal Communication in Chimpanzees 
American journal of primatology  2015;77(11):1143-1148.
A fundamental characteristic of human language is multimodality. In other words, humans use multiple signaling channels concurrently when communicating with one another. For example, people frequently produce manual gestures while speaking, and the words a person perceives are impacted by visual information. For this study, we hypothesized that similar to the way that humans regularly couple their spoken utterances with gestures and facial expressions, chimpanzees regularly produce vocalizations in conjunction with other communicative signals. To test this hypothesis, data were collected from 101 captive chimpanzees living in mixed-sex social groupings of seven to twelve individuals. A total of 2,869 vocal events were collected. The data indicate that approximately 50% of the vocal events were produced in conjunction with another communicative modality. In addition, approximately 68% were directed to a specific individual, and these directed vocalizations were more likely to include a signal from another communicative modality than were vocalizations that were not directed to a specific individual. These results suggest that, like humans, chimpanzees often pair their vocalizations with signals from other communicative modalities. In addition, chimpanzees appear to use their communicative signals strategically to meet specific socio-communicative ends, providing support for the growing literature that indicates that at least some chimpanzee vocal signaling is intentional.
PMCID: PMC5038593  PMID: 26212686
chimpanzees; vocal communication; multimodal communication; language origins
2.  Neocortical grey matter distribution underlying voluntary, flexible vocalizations in chimpanzees 
Scientific Reports  2016;6:34733.
Vocal learning is a key property of spoken language, which might also be present in nonhuman primate species, such as chimpanzees (Pan troglodytes), to a limited degree. While understanding the origins of vocal learning in the primate brain may help shed light on the evolution of speech and language, little is still known regarding the neurobiological correlates of vocal flexibility in nonhuman primates. The current study used voxel-based morphometry (VBM) to assess whether the cerebral cortex of captive chimpanzees that learned to voluntarily produce sounds to attract the attention of a human experimenter (attention-getting sounds) differs in grey matter distribution compared to chimpanzees that do not exhibit this behavior. It was found that chimpanzees that produce attention-getting sounds were characterized by increased grey matter in the ventrolateral prefrontal and dorsal premotor cortices. These findings suggest that the evolution of the capacity to flexibly modulate vocal output may be associated with reorganization of regions for motor control, including orofacial movements, in the primate brain.
PMCID: PMC5050423  PMID: 27703216
3.  Vocal learning of a communicative signal in captive chimpanzees, Pan troglodytes 
Brain and language  2013;127(3):520-525.
We hypothesized that chimpanzees could learn to produce attention-getting (AG) sounds via positive reinforcement. We conducted a vocal assessment in 76 captive chimpanzees for their use of AG sounds to acquire the attention of an otherwise inattentive human. Fourteen individuals that did not produce AG sounds during the vocal assessment were evaluated for their ability to acquire the use of an AG sound through operant conditioning and to employ these sounds in an attention-getting context. Nine of the 14 chimpanzees were successfully shaped using positive reinforcement to produce an AG sound. In a post-training vocal assessment, eight of the nine individuals that were successfully trained to produce AG sounds generalized the use of these newly acquired signals to communicatively relevant situations. Chimpanzees possess the ability to acquire the use of a communicative signal via operant conditioning and can generalize the use of this newly acquired signal to appropriate communicative contexts.
PMCID: PMC3982915  PMID: 24144730
Chimpanzee; vocal learning; human language origins; speech
4.  Delay of gratification is associated with white matter connectivity in the dorsal prefrontal cortex: a diffusion tensor imaging study in chimpanzees (Pan troglodytes) 
Individual variability in delay of gratification (DG) is associated with a number of important outcomes in both non-human and human primates. Using diffusion tensor imaging (DTI), this study describes the relationship between probabilistic estimates of white matter tracts projecting from the caudate to the prefrontal cortex (PFC) and DG abilities in a sample of 49 captive chimpanzees (Pan troglodytes). After accounting for time between collection of DTI scans and DG measurement, age and sex, higher white matter connectivity between the caudate and right dorsal PFC was found to be significantly associated with the acquisition (i.e. training phase) but not the maintenance of DG abilities. No other associations were found to be significant. The integrity of white matter connectivity between regions of the striatum and the PFC appear to be associated with inhibitory control in chimpanzees, with perturbations on this circuit potentially leading to a variety of maladaptive outcomes. Additionally, results have potential translational implications for understanding the pathophysiology of a number of psychiatric and clinical outcomes in humans.
PMCID: PMC4590457  PMID: 26041344
delay of gratification; diffusion tensor imaging; probabilistic tractography; prefrontal cortex; chimpanzees
5.  Visualizing Vocal Perception in the Chimpanzee Brain 
Cerebral Cortex (New York, NY)  2008;19(5):1151-1157.
The study of nonhuman primate vocal–auditory behavior continues to provide novel insights into the origins of human language. However, data on the neural systems involved in the perception and processing of conspecific vocalizations in great apes are virtually absent in the scientific literature, yet are critical for understanding the evolution of language. Here we used positron emission tomography to examine the neurological mechanisms associated with the perception of species-specific vocalizations in chimpanzees. The data indicate right-lateralized activity in the chimpanzee posterior temporal lobe, including the planum temporale, in response to certain calls, but not others. In addition, important differences are apparent when these data are compared with those published previously from monkey species suggesting that there may be marked differences in the way chimpanzees and macaque monkeys perceive and process conspecific vocalizations. These results provide the first evidence of the neural correlates of auditory perception in chimpanzees and offer unprecedented information concerning the origins of hemispheric specialization in humans.
PMCID: PMC2665158  PMID: 18787228
ape communication; language evolution; positron emission tomography; vocalization
6.  Sex differences in asymmetry of the planum parietale in chimpanzees (Pan troglodytes) 
Behavioural brain research  2007;184(2):185-191.
Magnetic resonance images were collected in 76 chimpanzees and the sylvian fissure was examined for the presence of a posterior bifurcation. A bilateral bifurcation of the sylvian fissure into an ascending and descending ramus was identified in 58 of the subjects. The posterior ascending ramus was measured in both hemispheres in order to evaluate the presence, magnitude, and direction of a planum parietale asymmetry. Statistical analysis revealed a main effect for sex. Specifically, females showed a significant rightward bias, whereas males did not. Moreover, an examination of posterior bifurcation patterns of the sylvian fissure revealed differences between the left and right hemispheres. In humans, subject handedness and sex have been found to have an effect on planum parietale asymmetry. To determine if this was also the case in our chimpanzee subjects, we evaluated whether or not planum parietale asymmetry was related to subject handedness. Although subject handedness was not directly related to planum parietale asymmetry quotients, significant differences in the pattern of posterior bifurcation of the sylvian fissure were found between males and females. These results support the view that asymmetries in the peri-sylvian language areas were present in the common ancestor of humans and chimpanzees.
PMCID: PMC2141691  PMID: 17765336
planum parietale; chimpanzee; brain asymmetry; lateralization; handedness; language
7.  Using naturalistic utterances to investigate vocal communication processing and development in human and non-human primates 
Hearing research  2013;305:10.1016/j.heares.2013.08.009.
Humans and several non-human primates possess cortical regions that are most sensitive to vocalizations produced by their own kind (conspecifics). However, the use of speech and other broadly defined categories of behaviorally relevant natural sounds has led to many discrepancies regarding where voice-sensitivity occurs, and more generally the identification of cortical networks, “proto-networks” or protolanguage networks, and pathways that may be sensitive or selective for certain aspects of vocalization processing. In this prospective review we examine different approaches for exploring vocal communication processing, including pathways that may be, or become, specialized for conspecific utterances. In particular, we address the use of naturally produced non-stereotypical vocalizations (mimicry of other animal calls) as another category of vocalization for use with human and non-human primate auditory systems. We focus this review on two main themes, including progress and future ideas for studying vocalization processing in great apes (chimpanzees) and in very early stages of human development, including infants and fetuses. Advancing our understanding of the fundamental principles that govern the evolution and early development of cortical pathways for processing non-verbal communication utterances is expected to lead to better diagnoses and early intervention strategies in children with communication disorders, improve rehabilitation of communication disorders resulting from brain injury, and develop new strategies for intelligent hearing aid and implant design that can better enhance speech signals in noisy environments.
PMCID: PMC3839530  PMID: 23994296
hearing perception; spoken language; protolanguage; evolution; proto-networks; fMRI
8.  The Chimpanzee Brain Shows Human-Like Perisylvian Asymmetries in White Matter 
Modern neuroimaging technologies allow scientists to uncover inter-species differences and similarities in hemispheric asymmetries that may shed light onto the origin of brain asymmetry and its functional correlates. We analyzed asymmetries in white to grey matter ratios of the lateral aspect of the lobes of the brains of chimpanzees. We found marked leftward asymmetries for all lobar regions. This asymmetry was particularly pronounced in the frontal region and was found to be related to handedness for communicative manual gestures as well as for tool use. These results point to a continuity in asymmetry patterns between the human and chimpanzee brain, and support the notion that the anatomical substrates for lateralization of communicative functions and complex manipulative activities may have been present in the common hominid ancestor.
PMCID: PMC4195238  PMID: 19614754
hemispheric asymmetry; white matter; gray matter; tool use; handedness; chimpanzee
9.  Initiation of Joint Attention is Associated with Morphometric Variation in the Anterior Cingulate Cortex of Chimpanzees (Pan troglodytes) 
American journal of primatology  2013;75(5):441-449.
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.
PMCID: PMC3609881  PMID: 23300067
10.  Social learning of a communicative signal in captive chimpanzees 
Biology Letters  2012;8(4):498-501.
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.
PMCID: PMC3391466  PMID: 22438489
chimpanzee; vocal learning; language evolution
11.  A Voxel-Based Morphometry Analysis of White Matter Asymmetries in Chimpanzees (Pan troglodytes) 
Brain, Behavior and Evolution  2010;76(2):93-100.
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.
PMCID: PMC3202944  PMID: 20881357
Chimpanzees; Brain asymmetry; White matter; Language evolution
12.  Chimpanzee Vocal Signaling Points to a Multimodal Origin of Human Language 
PLoS ONE  2011;6(4):e18852.
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.
PMCID: PMC3080370  PMID: 21533079
13.  Cortical Representation of Lateralized Grasping in Chimpanzees (Pan troglodytes): A Combined MRI and PET Study 
PLoS ONE  2010;5(10):e13383.
Functional imaging studies in humans have localized the motor-hand region to a neuroanatomical landmark call the KNOB within the precentral gyrus. It has also been reported that the KNOB is larger in the hemisphere contralateral to an individual's preferred hand, and therefore may represent the neural substrate for handedness. The KNOB has also been neuronatomically described in chimpanzees and other great apes and is similarly associated with handedness. However, whether the chimpanzee KNOB represents the hand region is unclear from the extant literature. Here, we used PET to quantify neural metabolic activity in chimpanzees when engaged in unilateral reach-and-grasping responses and found significantly lateralized activation of the KNOB region in the hemisphere contralateral to the hand used by the chimpanzees. We subsequently constructed a probabilistic map of the KNOB region in chimpanzees in order to assess the overlap in consistency in the anatomical landmarks of the KNOB with the functional maps generated from the PET analysis. We found significant overlap in the anatomical and functional voxels comprising the KNOB region, suggesting that the KNOB does correspond to the hand region in chimpanzees. Lastly, from the probabilistic maps, we compared right- and left-handed chimpanzees on lateralization in grey and white matter within the KNOB region and found that asymmetries in white matter of the KNOB region were larger in the hemisphere contralateral to the preferred hand. These results suggest that neuroanatomical asymmetries in the KNOB likely reflect changes in connectivity in primary motor cortex that are experience dependent in chimpanzees and possibly humans.
PMCID: PMC2954174  PMID: 20967216
14.  Gray Matter Asymmetries in Chimpanzees as Revealed by Voxel-Based Morphometry 
NeuroImage  2008;42(2):491-497.
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.
PMCID: PMC2569890  PMID: 18586523
15.  Communicative Signaling Activates ‘Broca’s’ Homolog in Chimpanzees 
Current biology : CB  2008;18(5):343-348.
Broca’s area, a cerebral cortical area located in the inferior frontal gyrus (IFG) of the human brain, has been identified as one of several critical regions associated with the motor planning and execution of language. Anatomically, Broca’s area is most often larger in the left hemisphere, and functional imaging studies in humans indicate significant left-lateralized patterns of activation during language-related tasks [1–3]. If, and to what extent, nonhuman primates, particularly chimpanzees, possess a homologous region that is involved in the production of their own communicative signals remains unknown. Here, we show that portions of the IFG as well as other cortical and subcortical regions in chimpanzees are active during the production of communicative signals. These findings are the first to provide direct evidence of the neuroanatomical structures associated with the production of communicative behaviors in chimpanzees. Significant activation in the left IFG in conjunction with other cortical and subcortical brain areas during the production of communicative signals in chimpanzees suggests that the neurological substrates underlying language production in the human brain may have been present in the common ancestor of humans and chimpanzees.
PMCID: PMC2665181  PMID: 18308569
16.  Behavioral and neuroanatomical correlates of white matter asymmetries in chimpanzees (Pan troglodytes) 
The European journal of neuroscience  2007;25(8):2565-2570.
Although behavioral and brain asymmetries have been documented in non-human primates, lateralization in cortical connectivity as reflected in white matter has not been described in any species, despite the intrinsic theoretical interest in white matter expansion during primate brain evolution. Here we report evidence of population-level leftward asymmetries in the white matter of chimpanzees. We further report that lateralization in white matter correlates with their handedness as well as neuroanatomical asymmetries in the precentral gyrus. These findings suggest that chimpanzees show asymmetries in cortical connectivity and these may serve as the foundation for morphological and behavioral laterality in primates, including humans.
PMCID: PMC2654327  PMID: 17445252
brain asymmetry; handedness; non-human primates; white matter
17.  Gesture handedness predicts asymmetry in the chimpanzee inferior frontal gyrus 
Neuroreport  2006;17(9):923-927.
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.
PMCID: PMC2018746  PMID: 16738489
chimpanzee; gesture; inferior frontal gyrus; language evolution; neuroanatomical asymmetry

Results 1-17 (17)