Literature DB >> 28473646

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

William D Hopkins1,2,3,4, Oliver Coulon5, Adrien Meguerditchian4,6, Michelle Autrey2, Kendall Davidek2, Lindsay Mahovetz2, Sarah Pope2, Mary Catherine Mareno7, Steven J Schapiro7.   

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.
Copyright © 2017 the authors 0270-6474/17/375476-09$15.00/0.

Entities:  

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

Mesh:

Year:  2017        PMID: 28473646      PMCID: PMC5452339          DOI: 10.1523/JNEUROSCI.2641-16.2017

Source DB:  PubMed          Journal:  J Neurosci        ISSN: 0270-6474            Impact factor:   6.167


  32 in total

1.  Chimpanzees Differentially Produce Novel Vocalizations to Capture the Attention of a Human.

Authors:  William D Hopkins; Jared Taglialatela; David A Leavens
Journal:  Anim Behav       Date:  2007-02       Impact factor: 2.844

Review 2.  Evolution in the social brain.

Authors:  R I M Dunbar; Susanne Shultz
Journal:  Science       Date:  2007-09-07       Impact factor: 47.728

3.  Social learning of a communicative signal in captive chimpanzees.

Authors:  Jared P Taglialatela; Lisa Reamer; Steven J Schapiro; William D Hopkins
Journal:  Biol Lett       Date:  2012-03-21       Impact factor: 3.703

4.  Differential use of attentional and visual communicative signaling by orangutans (Pongo pygmaeus) and gorillas (Gorilla gorilla) in response to the attentional status of a human.

Authors:  Sarah R Poss; Chris Kuhar; Tara S Stoinski; William D Hopkins
Journal:  Am J Primatol       Date:  2006-10       Impact factor: 2.371

5.  Relaxed genetic control of cortical organization in human brains compared with chimpanzees.

Authors:  Aida Gómez-Robles; William D Hopkins; Steven J Schapiro; Chet C Sherwood
Journal:  Proc Natl Acad Sci U S A       Date:  2015-11-16       Impact factor: 11.205

6.  Evolution of the central sulcus morphology in primates.

Authors:  William D Hopkins; Adrien Meguerditchian; Olivier Coulon; Stephanie Bogart; Jean-François Mangin; Chet C Sherwood; Mark W Grabowski; Allyson J Bennett; Peter J Pierre; Scott Fears; Roger Woods; Patrick R Hof; Jacques Vauclair
Journal:  Brain Behav Evol       Date:  2014-08-13       Impact factor: 1.808

7.  Chimpanzee vocal signaling points to a multimodal origin of human language.

Authors:  Jared P Taglialatela; Jamie L Russell; Jennifer A Schaeffer; William D Hopkins
Journal:  PLoS One       Date:  2011-04-20       Impact factor: 3.240

8.  Anatomic brain asymmetry in vervet monkeys.

Authors:  Scott C Fears; Kevin Scheibel; Zvart Abaryan; Chris Lee; Susan K Service; Matthew J Jorgensen; Lynn A Fairbanks; Rita M Cantor; Nelson B Freimer; Roger P Woods
Journal:  PLoS One       Date:  2011-12-21       Impact factor: 3.240

9.  Left hemisphere specialization for oro-facial movements of learned vocal signals by captive chimpanzees.

Authors:  Elizabeth A Reynolds Losin; Jamie L Russell; Hani Freeman; Adrien Meguerditchian; William D Hopkins
Journal:  PLoS One       Date:  2008-06-25       Impact factor: 3.240

10.  Bonobos modify communication signals according to recipient familiarity.

Authors:  Emilie Genty; Christof Neumann; Klaus Zuberbühler
Journal:  Sci Rep       Date:  2015-11-10       Impact factor: 4.379

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  6 in total

1.  In-vivo diffusion MRI protocol optimization for the chimpanzee brain and examination of aging effects on the primate optic nerve at 3T.

Authors:  Xiaodong Zhang; Chun-Xia Li; Yumei Yan; Govind Nair; James K Rilling; James G Herndon; Todd M Preuss; Xiaoping Hu; Longchuan Li
Journal:  Magn Reson Imaging       Date:  2020-12-23       Impact factor: 2.546

2.  Sulcal Morphology in Cingulate Cortex is Associated with Voluntary Oro-Facial Motor Control and Gestural Communication in Chimpanzees (Pan troglodytes).

Authors:  William D Hopkins; Emmanuel Procyk; Michael Petrides; Steven J Schapiro; Mary Catherine Mareno; Celine Amiez
Journal:  Cereb Cortex       Date:  2021-05-10       Impact factor: 5.357

3.  Sulcal organization in the medial frontal cortex provides insights into primate brain evolution.

Authors:  Céline Amiez; Jérôme Sallet; William D Hopkins; Adrien Meguerditchian; Fadila Hadj-Bouziane; Suliann Ben Hamed; Charles R E Wilson; Emmanuel Procyk; Michael Petrides
Journal:  Nat Commun       Date:  2019-07-31       Impact factor: 14.919

4.  The role of early social rearing, neurological, and genetic factors on individual differences in mutual eye gaze among captive chimpanzees.

Authors:  William D Hopkins; Michele M Mulholland; Lisa A Reamer; Mary Catherine Mareno; Steven J Schapiro
Journal:  Sci Rep       Date:  2020-05-04       Impact factor: 4.379

5.  Sociality predicts orangutan vocal phenotype.

Authors:  Adriano R Lameira; Guillermo Santamaría-Bonfil; Deborah Galeone; Marco Gamba; Madeleine E Hardus; Cheryl D Knott; Helen Morrogh-Bernard; Matthew G Nowak; Gail Campbell-Smith; Serge A Wich
Journal:  Nat Ecol Evol       Date:  2022-03-21       Impact factor: 19.100

6.  Coupled whole-body rhythmic entrainment between two chimpanzees.

Authors:  Adriano R Lameira; Tuomas Eerola; Andrea Ravignani
Journal:  Sci Rep       Date:  2019-12-12       Impact factor: 4.379

  6 in total

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