Apes communicate about absent and displaced objects: methodology matters.

Displaced reference is the ability to refer to an item that has been moved (displaced) in space and/or time, and has been called one of the true hallmarks of referential communication. Several studies suggest that nonhuman primates have this capability, but a recent experiment concluded that in a specific situation (absent entities), human infants display displaced reference but chimpanzees do not. Here, we show that chimpanzees and bonobos of diverse rearing histories are capable of displaced reference to absent and displaced objects. It is likely that some of the conflicting findings from animal cognition studies are due to relatively minor methodological differences, but are compounded by interpretation errors. Comparative studies are of great importance in elucidating the evolution of human cognition; however, greater care must be taken with methodology and interpretation for these studies to accurately reflect species differences.

Communicative signaling activates 'Broca's' homolog in chimpanzees.

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. 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.

The role of socio-communicative rearing environments in the development of social and physical cognition in apes.

The cultural intelligence hypothesis (CIH) claims that humans' advanced cognition is a direct result of human culture and that children are uniquely specialized to absorb and utilize this cultural experience (Tomasello, 2000). Comparative data demonstrating that 2.5-year-old human children outperform apes on measures of social cognition but not on measures of physical cognition support this claim (Herrmann et al., 2007). However, the previous study failed to control for rearing when comparing these two species. Specifically, the human children were raised in a human culture whereas the apes were raised in standard sanctuary settings. To further explore the CIH, here we compared the performance on multiple measures of social and physical cognition in a group of standard reared apes raised in conditions typical of zoo and biomedical laboratory settings to that of apes reared in an enculturated socio-communicatively rich environment. Overall, the enculturated apes significantly outperformed their standard reared counterparts on the cognitive tasks and this was particularly true for measures of communication. Furthermore, the performance of the enculturated apes was very similar to previously reported data from 2.5-year-old children. We conclude that apes who are reared in a human-like socio-communicatively rich environment develop superior communicative abilities compared to apes reared in standard laboratory settings, which supports some assumptions of the cultural intelligence hypothesis.

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.

Poor receptive joint attention skills are associated with atypical gray matter asymmetry in the posterior superior temporal gyrus of chimpanzees (Pan troglodytes).

Clinical and experimental data have implicated the posterior superior temporal gyrus as an important cortical region in the processing of socially relevant stimuli such as gaze following, eye direction, and head orientation. Gaze following and responding to different socio-communicative signals is an important and highly adaptive skill in primates, including humans. Here, we examined whether individual differences in responding to socio-communicative cues was associated with variation in either gray matter (GM) volume and asymmetry in a sample of chimpanzees. Magnetic resonance image scans and behavioral data on receptive joint attention (RJA) was obtained from a sample of 191 chimpanzees. We found that chimpanzees that performed poorly on the RJA task had less GM in the right compared to left hemisphere in the posterior but not anterior superior temporal gyrus. We further found that middle-aged and elderly chimpanzee performed more poorly on the RJA task and had significantly less GM than young-adult and sub-adult chimpanzees. The results are consistent with previous studies implicating the posterior temporal gyrus in the processing of socially relevant information.

Corpus callosal microstructure influences intermanual transfer in chimpanzees.

Learning a new motor skill with one hand typically results in performance improvements in the alternate hand. The neural substrates involved with this skill acquisition are poorly understood. We combined behavioral testing and non-invasive brain imaging to study how the organization of the corpus callosum was related to intermanual transfer performance in chimpanzees. Fifty-three chimpanzees were tested for intermanual transfer of learning using a bent-wire task. Magnetic resonance and diffusion tensor images were collected from 39 of these subjects. The dominant hand showed greater performance benefits than the nondominant hand. Further, performance was associated with structural integrity of the motor and sensory regions of the CC. Subjects with better intermanual transfer of learning had lower fractional anisotropy values. The results are consistent with the callosal access model of motor programming.

The neural and cognitive correlates of aimed throwing in chimpanzees: a magnetic resonance image and behavioural study on a unique form of social tool use.

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.

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.