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J Neurosci. 2017 May 31;37(22):5475-5483. doi: 10.1523/JNEUROSCI.2641-16.2017. Epub 2017 May 4.

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

Author information

1
Division of Developmental and Cognitive Neuroscience, Yerkes National Primate Research Center, Atlanta, Georgia 30322, whopkin@emory.edu whopkins4@gsu.edu.
2
Neuroscience Institute and Language Research Center, Georgia State University, Atlanta, Georgia 30302.
3
IMéRA Institut d'Etudes Avancées, Aix-Marseille University, 13004 Marseille, France.
4
Brain Language Research Institute, Aix-Marseille University, Centre National de la Recherche Scientifique (CNRS), 13604 Aix-en-Provence, France.
5
Laboratoire des Sciences de l'Information et des Systèmes, Unité Mixte de Recherche (UMR) 7296, Aix-Marseille Universite, Centre Nationale de la Recherche Scientifque, Institut de Neuroscience de La Timone, Marseille, France 13288.
6
Laboratoire de Psychologie Cognitive, UMR 7290, Aix-Marseille University, CNRS, Marseille, France, and.
7
National Center for Chimpanzee Care, Department of Veterinary Sciences, The University of Texas M.D. Anderson Cancer Center, Bastrop, Texas 78602.

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 STATEMENT Recent 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.

KEYWORDS:

central sulcus; chimpanzee; heritability; language; orofacial movements; vocal learning

PMID:
28473646
PMCID:
PMC5452339
DOI:
10.1523/JNEUROSCI.2641-16.2017
[Indexed for MEDLINE]
Free PMC Article

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