Differences in Neural Activation for Object-Directed Grasping in Chimpanzees and Humans

• Type of Material: Article
• Authors: Erin E. Hecht, Emory University; Lauren E. Murphy, Emory University; David Andrew Gutman, Emory University; John R Votaw, Emory University; David M Schuster, Emory University; Todd M Preuss, Emory University; Guy A. Orban, 9Department of Neuroscience, University of Parma, Italy; Dietrich Stout, Emory University; Lisa Parr, Emory University
• Language: English
• Date: 2013-08-28
• Publisher: Society for Neuroscience
• Publication Version: Final Published Version
• Copyright Statement: © 2013 the authors 0270-6474/13/3314117-18$15.00/0
• Final Published Version (URL): http://www.jneurosci.org/content/33/35/14117
• Title of Journal or Parent Work: Journal of Neuroscience
• ISSN: 0270-6474
• Volume: 33
• Issue: 35
• Start Page: 14117
• End Page: 14134
• Grant/Funding Information: This work was supported by the National Institutes of Health (Grant #RR-00165 to the Yerkes National Primate Research Center superceded by Office of Research Infrastructure Programs/OD P51OD11132; Grants #MH58922 and #F31MH086179-01 to E.E.H.; and Grants #5P01 AG026423-03 and RO1 MH068791 to L.A.P.), the Wenner-Gren Foundation (Dissertation Fieldwork Grant and Osmundsen Initiative Award 7699 Reference #3681 to E.E.H.), and the Emory Center for Systems Imaging (Pilot Grants #PET.HRRT.PS.001.12 and #MRI.3T.PS.001.12 to D.S.).
• Research Categories: Biology, Neuroscience

Abstract

The human faculty for object-mediated action, including tool use and imitation, exceeds that of even our closest primate relatives and is a key foundation of human cognitive and cultural uniqueness. In humans and macaques, observing object-directed grasping actions activates a network of frontal, parietal, and occipitotemporal brain regions, but differences in human and macaque activation suggest that this system has been a focus of selection in the primate lineage. To study the evolution of this system, we performed functional neuroimaging in humans' closest living relatives, chimpanzees. We compare activations during performance of an object-directed manual grasping action, observation of the same action, and observation of a mimed version of the action that consisted of only movements without results. Performance and observation of the same action activated a distributed frontoparietal network similar to that reported in macaques and humans. Like humans and unlike macaques, these regions were also activated by observing movements without results. However, in a direct chimpanzee/human comparison, we also identified unique aspects of human neural responses to observed grasping. Chimpanzee activation showed a prefrontal bias, including significantly more activity in ventrolateral prefrontal cortex, whereas human activation was more evenly distributed across more posterior regions, including significantly more activation in ventral premotor cortex, inferior parietal cortex, and inferotemporal cortex. This indicates a more “bottom-up” representation of observed action in the human brain and suggests that the evolution of tool use, social learning, and cumulative culture may have involved modifications of frontoparietal interactions.