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

• Published in: The Journal of neuroscience Vol. 37; no. 22; pp. 5475 - 5483
• Main Authors: Hopkins, William D., Coulon, Oliver, Meguerditchian, Adrien, Autrey, Michelle, Davidek, Kendall, Mahovetz, Lindsay, Pope, Sarah, Mareno, Mary Catherine, Schapiro, Steven J.
• Format: Journal Article
• Language: English
• Published: United States Society for Neuroscience 31.05.2017
• Subjects: Acoustics; Animal Communication; Animals; Chimpanzees; Cognitive science; Cortex (motor); Female; Genetic analysis; Genetic factors; Genetic Variation - genetics; Genetic Variation - physiology; Heritability; Magnetic resonance imaging; Male; Monkeys & apes; Morphology; Motor Cortex - anatomy & histology; Motor Cortex - physiology; Motor skill learning; Motors; Mouth - physiology; Neuronal Plasticity - physiology; Pan troglodytes; Psychology; Psychomotor Performance - physiology; Quantitative genetics; Sound production; chimpanzee; language; vocal learning; central sulcus; orofacial movements; heritability
• DOI: 10.1523/JNEUROSCI.2641-16.2017
• ISSN: 0270-6474; 1529-2401

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.