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Genetic Factors and Orofacial Motor Learning Selectively Influence Variability in Central Sulcus Morphology in Chimpanzees (Pan troglodytes)

Authors :
Oliver Coulon
William D. Hopkins
Steven J. Schapiro
Mary Catherine Mareno
Kendall Davidek
Lindsay M. Mahovetz
Michelle M. Autrey
Adrien Meguerditchian
Sarah M. Pope
Institute for Advanced Studies - Aix-Marseille University (IMéRA)
Institute of Language, Communication and the Brain (ILCB)
Aix Marseille Université (AMU)-Centre National de la Recherche Scientifique (CNRS)
Laboratoire des Sciences de l'Information et des Systèmes (LSIS)
Centre National de la Recherche Scientifique (CNRS)-Arts et Métiers Paristech ENSAM Aix-en-Provence-Université de Toulon (UTLN)-Aix Marseille Université (AMU)
Station de Primatologie, CNRS, UPS846, 13790 Rousset, France
Centre National de la Recherche Scientifique (CNRS)
Laboratoire de psychologie cognitive (LPC)
Centre National de la Recherche Scientifique (CNRS)-Aix Marseille Université (AMU)
Station de primatologie (SP)
Georgia State University
University System of Georgia (USG)
Michale E. Keeling Center for Comparative Medicine and Research
The University of Texas Health Science Center at Houston (UTHealth)
University of Texas-Pan
ANR-16-CONV-0002,ILCB,ILCB: Institute of Language Communication and the Brain(2016)
Aix Marseille Université (AMU)-Université de Toulon (UTLN)-Arts et Métiers Paristech ENSAM Aix-en-Provence-Centre National de la Recherche Scientifique (CNRS)
Source :
Journal of Neuroscience, Journal of Neuroscience, Society for Neuroscience, 2017, 37 (22), pp.5475-5483. ⟨10.1523/JNEUROSCI.2641-16.2017⟩, Journal of Neuroscience, 2017, 37 (22), pp.5475-5483. ⟨10.1523/JNEUROSCI.2641-16.2017⟩
Publication Year :
2017
Publisher :
HAL CCSD, 2017.

Abstract

Captive chimpanzees (Pan troglodytes) have been shown to learn the use of novel attention-getting (AG) sounds to capture the attention of humans as a means of requesting or drawing their attention to a desired object or food. There are significant individual differences in the use of AG sounds by chimpanzees and, here, we examined whether changes in cortical organization of the central sulcus (CS) were associated with AG sound production. MRI scans were collected from 240 chimpanzees, including 122 that reliably produced AG sounds and 118 that did not. For each subject, the depth of CS was quantified along the superior–inferior plane with specific interest in the inferior portion corresponding to the region of the motor cortex where the mouth and orofacial movements are controlled. Results indicated that CS depth in the inferior, but not superior, portion was significantly greater in chimpanzees that reliably produced AG sounds compared with those who did not. Quantitative genetic analyses indicated that overall CS surface area and depth were significantly heritable, particularly in the superior regions, but less so in the inferior and central portions. Further, heritability in CS depth was altered as a function of acquisition of AG sounds. The collective results suggest that learning to produce AG sounds resulted in region-specific cortical reorganization within the inferior portion of the CS, a finding previously undocumented in chimpanzees or any nonhuman primate.SIGNIFICANCE STATEMENTRecent studies in chimpanzees (Pan troglodytes) have shown that some can learn to produce novel sounds by configuring different orofacial movement patterns and these sounds are used in communicatively relevant contexts. Here, we examined the neuromorphological correlates in the production of these sounds in chimpanzees. We show that chimpanzees that have learned to produce these sounds show significant differences in central sulcus (CS) morphology, particularly in the inferior region. We further show that overall CS morphology and regions within the superior portion are significantly heritable, whereas central and inferior portions of the CS are not. The collective findings suggest chimpanzees exhibit cortical plasticity in regions of the brain that were central to the emergence of speech functions in humans.

Details

Language :
English
ISSN :
02706474 and 15292401
Database :
OpenAIRE
Journal :
Journal of Neuroscience, Journal of Neuroscience, Society for Neuroscience, 2017, 37 (22), pp.5475-5483. ⟨10.1523/JNEUROSCI.2641-16.2017⟩, Journal of Neuroscience, 2017, 37 (22), pp.5475-5483. ⟨10.1523/JNEUROSCI.2641-16.2017⟩
Accession number :
edsair.doi.dedup.....742980a9683878ad485d73610c614dd8
Full Text :
https://doi.org/10.1523/JNEUROSCI.2641-16.2017⟩