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

Serena Bianchi,Laura D Reyes,Chet C Sherwood,Jared P Taglialatela,William D Hopkins

doi:10.1038/srep34733

Abstract

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.

Highlights

T are produced intentionally and voluntarily[11,12,13]
The current study examined differences in grey matter distribution in a population of captive chimpanzees varying in their capacity to voluntary produce sounds to attract the attention of an otherwise inattentive human experimenter
An independent sample t-test assessing differences in grey matter distribution as a function of vocal phenotype in the voxel-based morphometry (VBM) analysis revealed that chimpanzees that produce attention-getting sounds (AG+) had greater grey matter density than chimpanzees that failed to exhibit this behavior (AG−) in the right ventrolateral prefrontal cortex (VLPFC), bordering the anterior bank of the precentral gyrus, and the left dorsal premotor cortex (Table 1 and Fig. 1)

Summary

Introduction

T are produced intentionally and voluntarily[11,12,13]. Taken together, these studies suggest that some forms of learned vocal signals, possibly precursors to the extreme vocal flexibility of human speech, may be present in chimpanzees and related ape species. The current study examined differences in grey matter distribution in a population of captive chimpanzees varying in their capacity to voluntary produce sounds (e.g. extended grunts, raspberries) to attract the attention of an otherwise inattentive human experimenter (attention-getting sounds — AG). Other factors, including age and housing conditions, do not appear to influence the production and use of AG sounds[19,20] Drawing on these intrinsic individual differences in communicative capacities, a voxel-based morphometry (VBM) analysis was conducted[21,22,23] to assess variation in grey matter distribution in the chimpanzee brain as a function of vocal capacities. For this study we preferred a whole-brain approach to a ROI-based approach because of the limited amount of information on regions involved in the production of this atypical form of communication in chimpanzees[14,15]

Methods

Results

Conclusion