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Species-specific calls activate homologs of Broca's and Wernicke's areas in the macaque

Abstract

The origin of brain mechanisms that support human language—whether these originated de novo in humans or evolved from a neural substrate that existed in a common ancestor—remains a controversial issue. Although the answer is not provided by the fossil record, it is possible to make inferences by studying living species of nonhuman primates. Here we identified neural systems associated with perceiving species-specific vocalizations in rhesus macaques using H215O positron emission tomography (PET). These vocalizations evoke distinct patterns of brain activity in homologs of the human perisylvian language areas. Rather than resulting from differences in elementary acoustic properties, this activity seems to reflect higher order auditory processing. Although parallel evolution within independent primate species is feasible, this finding suggests the possibility that the last common ancestor of macaques and humans, which lived 25–30 million years ago, possessed key neural mechanisms that were plausible candidates for exaptation during the evolution of language.

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Figure 1: MRI-based anatomically segmented STG atlas.
Figure 2: Illustration of acoustic analysis.
Figure 3: Selective activation elicited by species-specific vocalizations in the macaque.
Figure 4: Histograms illustrating mean (± s.e.m.) normalized rCBF per monkey, derived from ventral premotor cortex (PMv), Tpt and posterior parietal cortex (PPC).
Figure 5: Histograms illustrating mean (± s.e.m.) normalized rCBF per monkey, derived from areas R and A1.

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Acknowledgements

We wish to thank S. Suomi (US National Institutes of Health, Bethesda, Maryland, USA) for providing the monkeys; S.P. Wise, P. Gannon, T. Hackett, A. Poremba, R. Saunders and L. Ungerleider for help with the neuroanatomy; M.D. Hauser for providing his recordings of rhesus macaque conspecific calls; J. O'Malley, L. Prevost, S. Antonio, B. Forrest and J. Fellows for assistance with animal care and training; D. Robinson for help with preparation of the animal protocol; R. Carson, P. Herscovitch, J. Jacobs, T. Howe, J. Bacon, J. Chincuanco, T. San Juan and S. Conant for help in the design and execution of the PET experiments; and J. Solomon, J. Quinlivan, J. Officewala, N. Mesgarani, B. Swett, N. Jeffries and S. Milleville for assistance with data analysis. We also wish to thank M. Mishkin, S.P. Wise, L. Ungerleider, W.T. Fitch and M.D. Hauser, who reviewed the manuscript and provided valuable comments. This work was supported by the National Institute on Deafness and Other Communication Disorders Division of Intramural Research Programs (DIRP), by the National Institute of Mental Health DIRP and by a grant from Fundação para a Ciência e Tecnologia.

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Authors

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R.G.C. designed the studies, designed the equipment, created the stimuli blocks, trained the animals, ran the experiments, performed the image processing, organized and performed the data analysis, reviewed the results and wrote the paper; A.M. designed the studies, organized the data analysis, reviewed the results and wrote the paper; M.A.L. assisted in study design, designed the equipment, created the stimuli blocks, trained the animals, ran the experiments and performed the image processing and part of the data analysis; M.M. assisted with the neuroanatomy and created the MRI atlas; J.B.F. assisted in study design and performed the acoustic analysis; A.R.B. designed the studies, organized the data analysis, reviewed the results and wrote the paper.

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Correspondence to Allen R Braun.

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The authors declare no competing financial interests.

Supplementary information

Supplementary Fig. 1

Replication of the Poremba et al. (2004) analysis (ref. 6 in main report). (PDF 90 kb)

Supplementary Table 1

Division of the STG into 9 architectonic areas as represented in the MRI-based anatomically segmented atlas (Fig. 1) and described in the Methods section. (PDF 82 kb)

Supplementary Note (PDF 108 kb)

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Gil-da-Costa, R., Martin, A., Lopes, M. et al. Species-specific calls activate homologs of Broca's and Wernicke's areas in the macaque. Nat Neurosci 9, 1064–1070 (2006). https://doi.org/10.1038/nn1741

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