Organization of extrastriate and temporal cortex in chimpanzees compared to humans and macaques

• Type of Material: Article
• Authors: Katherine Bryant, Emory University; Matthew F. Glasser, Washington University; Longchuan Li, Emory University; Jason Jae-Cheol Bae, Emory University; Nadine J. Jacquez, Emory University; Laura Alarcon, Emory University; Archie Fields, III, University of Calgary; Todd Preuss, Emory University
• Language: English
• Date: 2019-09-01
• Publisher: Elsevier Masson, Corporation Office
• Publication Version: Author Accepted Manuscript (After Peer Review)
• Copyright Statement: © 2019 Elsevier Ltd. All rights reserved.
• License: Creative Commons Attribution-NonCommercial-NoDerivs 4.0 International
• Final Published Version (URL): http://dx.doi.org/10.1016/j.cortex.2019.02.010
• Title of Journal or Parent Work: Cortex
• Volume: 118
• Start Page: 223
• End Page: 243
• Grant/Funding Information: This study was supported by NIH/NIDCD (RO1 DC04318), the National Chimpanzee Brain Resource (R24 NS092988), the James S. McDonnell Foundation (JSMF 21002093), and the John Templeton Foundation (Award 40463), the NIH Office of Research Infrastructure Programs (OD P510D1132), and the Yerkes National Primate Research Center base grant (2P51 RR000165–51) and NIMH (P50, MH100029).
• Keywords: Science & Technology; Psychology; Life Sciences & Biomedicine; Tractography; Striate cortex; Neural systems; Evolution; Social Sciences; Neurosciences & Neurology; Visual area MT; Neurosciences; Longitudinal fasciculus; Psychology, Experimental; Diffusion tractography; Visual cortex; Corticocortical connections; Retinotopic organization; Auditory cortex; Behavioral Sciences; Brain areas; Diffusion
• Research Categories: Health Sciences, Radiology; Biology, Neuroscience; Psychology, Behavioral; Health Sciences, Pathology

Abstract

There is evidence for enlargement of association cortex in humans compared to other primate species. Expansion of temporal association cortex appears to have displaced extrastriate cortex posteriorly and inferiorly in humans compared to macaques. However, the details of the organization of these recently expanded areas are still being uncovered. Here, we used diffusion tractography to examine the organization of extrastriate and temporal association cortex in chimpanzees, humans, and macaques. Our goal was to characterize the organization of visual and auditory association areas with respect to their corresponding primary areas (primary visual cortex and auditory core) in humans and chimpanzees. We report three results: (1) Humans, chimpanzees, and macaques show expected retinotopic organization of primary visual cortex (V1) connectivity to V2 and to areas immediately anterior to V2; (2) In contrast to macaques, chimpanzee and human V1 shows apparent connectivity with lateral, inferior, and anterior temporal regions, beyond the retinotopically organized extrastriate areas; (3) Also in contrast to macaques, chimpanzee and human auditory core shows apparent connectivity with temporal association areas, with some important differences between humans and chimpanzees. Diffusion tractography reconstructs diffusion patterns that reflect white matter organization, but does not definitively represent direct anatomical connectivity. Therefore, it is important to recognize that our findings are suggestive of species differences in long-distance white matter organization rather than demonstrations of direct connections. Our data support the conclusion that expansion of temporal association cortex, and the resulting posterior displacement of extrastriate cortex, occurred in the human lineage after its separation from the chimpanzee lineage. It is possible, however, that some expansion of the temporal lobe occurred prior to the separation of humans and chimpanzees, reflected in the reorganization of long white matter tracts in the temporal lobe that connect occipital areas to the fusiform gyrus, middle temporal gyrus, and anterior temporal lobe.