Gray matter asymmetries in chimpanzees as revealed by voxel-based morphometry

Abstract

Determination of whether nonhuman primates exhibit neuroanatomical asymmetries would inform our understanding of the evolution of traits in humans that show functional hemispheric dominance, including language and handedness. Here we report the first evidence of population-level asymmetries in the chimpanzee neocortex using voxel-based morphology (VBM). MRI scans of the brain were collected in a sample of 31 chimpanzees including 9 males and 22 females, and the resulting images were segmented into gray matter, white matter and CSF. Gray matter images were then co-registered to a template and these normally oriented volumes were flipped on the left-right axis to create mirror volumes. In total, significant asymmetries were found in 13 regions including several that have been described previously in great apes using traditional region-of-interest approaches. The results from this VBM analysis support previous reports of hemispheric lateralization in chimpanzees and reinforce the view that asymmetries in the central nervous system are not uniquely human.Dating back to the time of Dax, Broca and Wernicke, it has been well documented that the human brain is asymmetrically organized, particularly for regions associated with handedness and language functions. For example, the planum temporale (PT) and frontal operculum (FO), regions corresponding to the classically-defined language centers of the human cerebral cortex, tend to be larger in the left compared to right hemisphere, particularly among right-handed individuals (Beaton, 1997;Foundas et al., 1998;Shapleske et al., 1999). Historically, the presence of behavioral and neuroanatomical asymmetries has been considered unique to hominin evolution (Corballis, 1992;Ettlinger, 1988;Warren, 1980); however, recent studies in nonhuman animals, and particularly nonhuman primates, have challenged this view (Hopkins, 2007;Rogers and Andrew, 2002). For instance, post-mortem and in vivo imaging studies have revealed population-level leftward asymmetries in the PT and FO of great ape brains (Cantalupo and Hopkins, 2001;Cantalupo et al., 2003; Gannon et al., 1998), suggesting Correspondence and reprint requests should be addressed to Dr. William D. Hopkins, Division of Psychobiology, Yerkes National Primate Research Center, Emory University, Atlanta, Georgia 30322. E-mail: whopkin@emory.edu or whopkins@agnesscott.edu. Publisher's Disclaimer: This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final citable form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain. that neuroanatomical asymmetries are not uniquely human but rather reflect a shared trait that was present in the last common ancestor of humans and great apes. These...

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