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Longitudinal connections and the organization of the temporal cortex in macaques, great apes, and humans.

ABSTRACT: The temporal association cortex is considered a primate specialization and is involved in complex behaviors, with some, such as language, particularly characteristic of humans. The emergence of these behaviors has been linked to major differences in temporal lobe white matter in humans compared with monkeys. It is unknown, however, how the organization of the temporal lobe differs across several anthropoid primates. Therefore, we systematically compared the organization of the major temporal lobe white matter tracts in the human, gorilla, and chimpanzee great apes and in the macaque monkey. We show that humans and great apes, in particular the chimpanzee, exhibit an expanded and more complex occipital-temporal white matter system; additionally, in humans, the invasion of dorsal tracts into the temporal lobe provides a further specialization. We demonstrate the reorganization of different tracts along the primate evolutionary tree, including distinctive connectivity of human temporal gray matter.

SUBMITTER: Roumazeilles L

PROVIDER: S-EPMC7423156 | biostudies-literature | 2020 Jul

REPOSITORIES: biostudies-literature

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Longitudinal connections and the organization of the temporal cortex in macaques, great apes, and humans.

Roumazeilles Lea L Eichert Nicole N Bryant Katherine L KL Folloni Davide D Sallet Jerome J Vijayakumar Suhas S Foxley Sean S Tendler Benjamin C BC Jbabdi Saad S Reveley Colin C Verhagen Lennart L Dershowitz Lori B LB Guthrie Martin M Flach Edmund E Miller Karla L KL Mars Rogier B RB

PLoS biology 20200731 7

The temporal association cortex is considered a primate specialization and is involved in complex behaviors, with some, such as language, particularly characteristic of humans. The emergence of these behaviors has been linked to major differences in temporal lobe white matter in humans compared with monkeys. It is unknown, however, how the organization of the temporal lobe differs across several anthropoid primates. Therefore, we systematically compared the organization of the major temporal lob ...[more]

PMID: 32735557

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Project description: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.

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Project description:Understanding cellular and molecular differences between human and non-human primates (NHPs) is essential to the basic comprehension of the evolution and diversity of our own species. Until now, preserved tissues have been the main source of most comparative studies between humans, chimpanzees (Pan troglodytes) and bonobos (Pan paniscus). However, these tissue samples do not fairly represent the distinctive traits of live cell behavior, are not amenable to genetic manipulation and do not allow translation of observed differences into phenotypical divergence. We hypothesized that induced pluripotent stem cells (iPSCs) could provide a unique biological resource to elucidate relevant phenotypical differences between human and the great apes and that those differences could have potential adaptation and speciation value. Here, we describe the generation and initial characterization of iPSCs from chimpanzees and bonobos as novel tools to explore our most recent evolution. Comparative gene expression analysis of human and NHP iPSCs revealed differences in regulation of Long Interspersed Nuclear Element (LINE-1 or L1) transposons. A force of change in mammalian evolution, L1 elements are retrotransposons that have remained active during primate evolution. We observed decreased levels of L1 restricting factors APOBEC3B (A3B)7 and PIWIL28 in NHP iPSCs which was correlated with increased human and chimpanzee L1 mobility and endogenous L1 mRNA levels. Moreover, results from manipulation of A3B and PIWIL2 levels in iPSCs suggested a causal inverse relationship between levels of these proteins and L1 activity. Finally, we found increased copy numbers of species-specific L1 elements in the genome of chimpanzees compared to humans, supporting the idea that increased L1 mobility in NHPs is not limited to iPSCs in culture and may have also occurred in the germline during primate evolution. We propose that differences in L1 mobility may have differentially shaped the genomes of humans and NHPs and could have had an adaptive significance.

Dataset Information

Longitudinal connections and the organization of the temporal cortex in macaques, great apes, and humans.

Publications

Longitudinal connections and the organization of the temporal cortex in macaques, great apes, and humans.

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