The AliveCor KardiaMobile ECG device allows electrocardiogram assessment in awake bonobos (Pan paniscus).

OBJECTIVE: To determine the diagnostic utility of a smartphone-based ECG device (Alivecor KardiaMobile) in awake bonobos (Pan paniscus). ANIMALS: 7 adult bonobos in human care. PROCEDURES: Bonobos were trained with positive reinforcement to hold 1 finger from each hand onto the KardiaMobile sensors for 30 seconds to obtain an ECG reading. Ten ECG tracings were recorded from each bonobo and evaluated by a veterinarian, a veterinary cardiologist, and a human cardiologist for tracing quality, tracing length, heart rate, identification of P-waves, and presence and quantification of premature ventricular or atrial contractions. RESULTS: 6 of the 7 bonobos were trained within 21 weeks to allow the collection of 10 diagnostic quality ECG tracings. The average heart rate recorded was 87 bpm (range = 60 to 118 bpm). Potential abnormalities identified by the KardiaMobile included premature ventricular contractions in 2 male bonobos and 1 premature atrial contraction in another male. There was strong agreement by reviewers in all ECG parameters except for the identification of P-waves. CLINICAL RELEVANCE: The Alivecor KardiaMobile device has diagnostic utility as a screening tool for use in bonobos in human care. The training was accomplished to yield diagnostic ECG readings of acceptable duration in awake bonobos. Given the prevalence of cardiovascular disease in great apes, this technology may identify a subset of great apes who may benefit from early intervention and treatment in an effort to delay the progression of cardiac disease.

Linked OXTR Variants Are Associated with Social Behavior Differences in Bonobos (Pan paniscus).

Single-nucleotide polymorphisms (SNPs) in forkhead box protein P2 (FOXP2) and oxytocin receptor (OXTR) genes have been associated with linguistic and social development in humans, as well as to symptom severity in autism spectrum disorder (ASD). Studying biobehavioral mechanisms in the species most closely related to humans can provide insights into the origins of human communication, and the impact of genetic variation on complex behavioral phenotypes. Here, we aimed to determine if bonobos (Pan paniscus) exhibit individual variation in FOXP2 and OXTR loci that have been associated with human social development and behavior. Although the ASD-related variants were reported in 13-41% of the human population, we did not find variation at these loci in our sample of 13 bonobos. However, we did identify a novel variant in bonobo FOXP2, as well as four novel variants in bonobo OXTR that were 17-184 base pairs from the human ASD variants. We also found the same linked, homozygous allelic combination across the 4 novel OXTR SNPs (homozygous TGTC) in 6 of the 13 bonobos, indicating that this combination may be under positive selection. When comparing the combined OXTR genotypes, we found significant group differences in social behavior; bonobos with zero copies of the TGTC combination were less social than bonobos with one copy of the TGTC combination. Taken together, our findings suggest that these OXTR variants may influence individual-level social behavior in bonobos and support the notion that linked genetic variants are promising risk factors for social communication deficits in humans.

Degraded and computer-generated speech processing in a bonobo.

The human auditory system is capable of processing human speech even in situations when it has been heavily degraded, such as during noise-vocoding, when frequency domain-based cues to phonetic content are strongly reduced. This has contributed to arguments that speech processing is highly specialized and likely a de novo evolved trait in humans. Previous comparative research has demonstrated that a language competent chimpanzee was also capable of recognizing degraded speech, and therefore that the mechanisms underlying speech processing may not be uniquely human. However, to form a robust reconstruction of the evolutionary origins of speech processing, additional data from other closely related ape species is needed. Specifically, such data can help disentangle whether these capabilities evolved independently in humans and chimpanzees, or if they were inherited from our last common ancestor. Here we provide evidence of processing of highly varied (degraded and computer-generated) speech in a language competent bonobo, Kanzi. We took advantage of Kanzi's existing proficiency with touchscreens and his ability to report his understanding of human speech through interacting with arbitrary symbols called lexigrams. Specifically, we asked Kanzi to recognise both human (natural) and computer-generated forms of 40 highly familiar words that had been degraded (noise-vocoded and sinusoidal forms) using a match-to-sample paradigm. Results suggest that-apart from noise-vocoded computer-generated speech-Kanzi recognised both natural and computer-generated voices that had been degraded, at rates significantly above chance. Kanzi performed better with all forms of natural voice speech compared to computer-generated speech. This work provides additional support for the hypothesis that the processing apparatus necessary to deal with highly variable speech, including for the first time in nonhuman animals, computer-generated speech, may be at least as old as the last common ancestor we share with bonobos and chimpanzees.

Bo-NO-bouba-kiki: picture-word mapping but no spontaneous sound symbolic speech-shape mapping in a language trained bonobo.

Humans share the ability to intuitively map 'sharp' or 'round' pseudowords, such as 'bouba' versus 'kiki', to abstract edgy versus round shapes, respectively. This effect, known as sound symbolism, appears early in human development. The phylogenetic origin of this phenomenon, however, is unclear: are humans the only species capable of experiencing correspondences between speech sounds and shapes, or could similar effects be observed in other animals? Thus far, evidence from an implicit matching experiment failed to find evidence of this sound symbolic matching in great apes, suggesting its human uniqueness. However, explicit tests of sound symbolism have never been conducted with nonhuman great apes. In the present study, a language-competent bonobo completed a cross-modal matching-to-sample task in which he was asked to match spoken English words to pictures, as well as 'sharp' or 'round' pseudowords to shapes. Sound symbolic trials were interspersed among English words. The bonobo matched English words to pictures with high accuracy, but did not show any evidence of spontaneous sound symbolic matching. Our results suggest that speech exposure/comprehension alone cannot explain sound symbolism. This lends plausibility to the hypothesis that biological differences between human and nonhuman primates could account for the putative human specificity of this effect.

Comparison of bonobo and chimpanzee brain microstructure reveals differences in socio-emotional circuits.

Despite being closely related, bonobos and chimpanzees exhibit several behavioral differences. For instance, studies indicate that chimpanzees are more aggressive, territorial, and risk-taking, while bonobos exhibit greater social tolerance and higher rates of socio-sexual interactions. To elucidate the potential neuroanatomical variation that accompanies these differences, we examined the microstructure of selected brain areas by quantifying the neuropil fraction, a measure of the relative tissue area occupied by structural elements of connectivity (e.g., dendrites, axons, and synapses) versus cell bodies. In bonobos and chimpanzees, we compared neuropil fractions in the nucleus accumbens (NAc; core and shell), amygdala (whole, accessory basal, basal, central and lateral nuclei), anterior cingulate cortex (ACC; dorsal and subgenual), anterior insular cortex (AIC), and primary motor cortex (M1). In the dorsal ACC and frontoinsular cortex (FI) we also quantified numbers of von Economo neurons (VENs), a unique subset of neurons thought to be involved in rapid information processing during social interactions. We predicted that the neuropil fraction and number of VENs in brain regions associated with socio-emotional processing would be higher in bonobos. In support of this hypothesis, we found that bonobos had significantly greater neuropil in the central and accessory basal nuclei of the amygdala, as well as layers V-VI of the subgenual ACC. However, we did not find a difference in the numbers of VENs between the two species. These findings support the conclusion that bonobo and chimpanzee brains differ in the anatomical organization of socio-emotional systems that may reflect species-specific variation in behavior.

Changes in Frontoparietotemporal Connectivity following Do-As-I-Do Imitation Training in Chimpanzees ( Pan troglodytes).

Human imitation is supported by an underlying "mirror system" principally composed of inferior frontal, inferior parietal, and superior temporal cortical regions. Across primate species, differences in frontoparietotemporal connectivity have been hypothesized to explain phylogenetic variation in imitative abilities. However, if and to what extent these regions are involved in imitation in nonhuman primates is unknown. We hypothesized that "Do As I Do" (DAID) imitation training would enhance white matter integrity within and between frontoparietotemporal regions. To this end, four captive chimpanzees ( Pan troglodytes) were trained to reproduce 23 demonstrated actions, and four age-/sex-matched controls were trained to produce basic husbandry behaviors in response to manual cues. Diffusion tensor images were acquired before and after 600 min of training over an average of 112 days. Bilateral and asymmetrical changes in frontoparietotemporal white matter integrity were compared between DAID trained subjects and controls. We found that imitation trained subjects exhibited leftward shifts in both mean fractional anisotropy and tract strength asymmetry measures in brain regions within the mirror system. This is the first report of training-induced changes in white matter integrity in chimpanzees and suggests that frontoparietotemporal connectivity, particularly in the left hemisphere, may have facilitated the emergence of increasingly complex imitation learning abilities.

Neocortical grey matter distribution underlying voluntary, flexible vocalizations in chimpanzees.

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.

Differential serotonergic innervation of the amygdala in bonobos and chimpanzees.

Humans' closest living relatives are bonobos (Pan paniscus) and chimpanzees (Pan troglodytes), yet these great ape species differ considerably from each other in terms of social behavior. Bonobos are more tolerant of conspecifics in competitive contexts and often use sexual behavior to mediate social interactions. Chimpanzees more frequently employ aggression during conflicts and actively patrol territories between communities. Regulation of emotional responses is facilitated by the amygdala, which also modulates social decision-making, memory and attention. Amygdala responsiveness is further regulated by the neurotransmitter serotonin. We hypothesized that the amygdala of bonobos and chimpanzees would differ in its neuroanatomical organization and serotonergic innervation. We measured volumes of regions and the length density of serotonin transporter-containing axons in the whole amygdala and its lateral, basal, accessory basal and central nuclei. Results showed that accessory basal nucleus volume was larger in chimpanzees than in bonobos. Of particular note, the amygdala of bonobos had more than twice the density of serotonergic axons than chimpanzees, with the most pronounced differences in the basal and central nuclei. These findings suggest that variation in serotonergic innervation of the amygdala may contribute to mediating the remarkable differences in social behavior exhibited by bonobos and chimpanzees.

Multimodal communication in chimpanzees.

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.

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.

Why vocal production of atypical sounds in apes and its cerebral correlates have a lot to say about the origin of language.

Ackermann et al. mention the "acquisition of species-atypical sounds" in apes without any discussion. In our commentary, we demonstrate that these atypical sounds in chimpanzees not only include laryngeal sounds, but also have a major significance regarding the origins of language, if we consider looking at their context of use, their social properties, their relations with gestures, their lateralization, and their neurofunctional correlates as well.

Vocal learning of a communicative signal in captive chimpanzees, Pan troglodytes.

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.

Using naturalistic utterances to investigate vocal communication processing and development in human and non-human primates.

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. This article is part of a Special Issue entitled "Communication Sounds and the Brain: New Directions and Perspectives".

Initiation of joint attention is associated with morphometric variation in the anterior cingulate cortex of chimpanzees (Pan troglodytes).

In developing human children, joint attention (JA) is an important preverbal skill fundamental to the development of language. Poor JA 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 JA 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 JA with a human experimenter. Results showed that chimpanzees that performed poorly on the JA task had larger gray matter (GM) 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 bias was observed in the third. Based on these findings, we suggest that the ACC plays an important role in mediating JA, 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 JA skills.

Social learning of a communicative signal in captive chimpanzees.

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 signaling points to a multimodal origin of human language.

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 that this critical human language region was involved in vocal signaling in the common ancestor of both modern humans and chimpanzees.

A voxel-based morphometry analysis of white matter asymmetries in chimpanzees (Pan troglodytes).

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). T(1)-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.

Cortical representation of lateralized grasping in chimpanzees (Pan troglodytes): a combined MRI and PET study.

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.

The chimpanzee brain shows human-like perisylvian asymmetries in white matter.

Modern neuroimaging technologies allow scientists to uncover interspecies differences and similarities in hemispheric asymmetries that may shed light on the origin of brain asymmetry and its functional correlates. We analyzed asymmetries in ratios of white to grey matter in 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.

Visualizing vocal perception in the chimpanzee brain.

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.