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Author Notes:

Correspondence should be addressed to Erin E. Hecht, Department of Anthropology, Emory University, 1557 Dickey Drive, 114 Anthropology Building, Atlanta, GA 30322.ehecht@emory.edu

Author contributions: E.E.H., J.R.V., D.M.S., G.A.O., D.S., and L.A.P. designed research

E.E.H., L.E.M., and D.S. performed research

T.M.P. contributed unpublished reagents/analytic tools; E.E.H., L.E.M., D.A.G., T.M.P., D.S., and L.A.P. analyzed data

E.E.H. wrote the paper.

We thank the staffs of the Yerkes Imaging Center, Biomedical Imaging Technology Center, Wesley Woods Imaging Center, animal care facility, machine shop, and veterinary facility and James Rilling for sharing no-task chimpanzee control PET scans.

The authors declare no competing financial interests.

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Research Funding:

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work was supported by the National Institutes of Health (Grant #RR-00165 to the Yerkes National Primate Research Center superceded by Office of Research Infrastructure Programs/OD P51OD11132; Grants #MH58922 and #F31MH086179-01 to E.E.H.; and Grants #5P01 AG026423-03 and RO1 MH068791 to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.).

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

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Journal Title:

Journal of Neuroscience

Volume:

Volume 33, Number 35

Publisher:

, Pages 14117-14134

Type of Work:

Article | Final Publisher PDF

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.

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© 2013 the authors 0270-6474/13/3314117-18$15.00/0

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