Cross-species cortical alignment identifies different types of neuroanatomical reorganization in the temporal lobe of higher primates

Abstract

Evolutionary modifications of the temporo-parietal cortex are considered to be a critical adaptation of the human brain. Cortical adaptations, however, can affect different aspects of brain architecture, including areal expansion or changes in connectivity profiles. We propose to distinguishing different types of brain reorganization using a computational neuroanatomy approach. We investigate the extent to which between-species alignment based on cortical myelin can predict changes in connectivity patterns across macaque, chimpanzee and human. We show that expansion and relocation of brain areas are sufficient to predict terminations of several white matter tracts in temporo-parietal cortex, including the middle and superior longitudinal fasciculus, but not of the arcuate fasciculus. This demonstrates that the arcuate fasciculus underwent additional evolutionary modifications affecting the connectivity pattern of the temporal lobe. The presented approach can flexibly be extended to include other features of cortical organization and other species, allowing direct tests of comparative hypotheses of brain organization.

Cross-species Functional Alignment Reveals Evolutionary Hierarchy Within the Connectome

“…Our cross species joint-embedding is part of an emerging trend toward the use of common high dimensional spaces as a tool to understand the evolutionary changes across species. Recent efforts have developed strategies for alignment based on white matter tracts, or myelin (T1w/T2w) maps 15,16 , as well as task-based activations during movie viewing 8 . We anticipate that the joint-embedding approach used in this paper should be readily extensible to diffusion imaging data and encourage future work in this direction 75,76 .…”

“…myelination) in humans versus other species 3,[14][15][16][17] . This approach has allowed comparing human cortex to non-human primates including macaques, marmosets and chimpanzees, leading to the identification and comparison of putative 'homologue' regions across species 14,15,18,19 . This use of anatomical features has revolutionized our understanding of the organization of the mammalian cortex.…”

XTRACT - Standardised protocols for automated tractography in the human and macaque brain

“…Fornix (FX): The fornix connects the hippocampus with the mammillary bodies, the anterior thalamic nuclei, and the hypothalamus (Catani et al, 2013). The tract was reconstructed using a seed in the body of the fornix at the level of the middle of the corpus callosum and a target in the hippocampus.…”

“…To ensure generalisability of the protocols across species, we also utilised diffusion MRI data from the macaque brain. This data consisted of an extended set of animals used in (Eichert et al, 2019a;Mars et al, 2018b). In total, the datasets we considered consist of 1065 subjects from the HCP (all available HCP S1200 subjects that had diffusion MRI data), 1000 subjects from the UK Biobank and ex vivo high-resolution datasets from 6 macaques.…”

“…Diffusion tractography is a unique tool for extracting white matter (WM) pathways non-invasively and in vivo. The virtual dissection of major WM tracts enables the study of brain organisation (Catani et al, 2013;Jbabdi et al, 2015) and offers a probe to brain development (Huppi and Dubois, 2006) and WM pathology (Ciccarelli et al, 2008;Griffa et al, 2013). It further allows explorations of individual variations (Assaf et al, 2017) and crossspecies variations (Mars et al, 2018b) in anatomy and connectivity.…”