A connectomics-based taxonomy of mammals

Author:

Suarez Laura E12ORCID,Yovel Yossi3,van den Heuvel Martijn P4,Sporns Olaf5,Assaf Yaniv3ORCID,Lajoie Guillaume2,Misic Bratislav1ORCID

Affiliation:

1. Montréal Neurological Institute, McGill University

2. Mila - Quebec Artificial Intelligence Institute

3. School of Neurobiology, Biochemistry and Biophysics, Tel Aviv University

4. Center for Neurogenomics and Cognitive Research, Vrije Universiteit Amsterdam

5. Psychological and Brain Sciences, Indiana University

Abstract

Mammalian taxonomies are conventionally defined by morphological traits and genetics. How species differ in terms of neural circuits and whether inter-species differences in neural circuit organization conform to these taxonomies is unknown. The main obstacle to the comparison of neural architectures has been differences in network reconstruction techniques, yielding species-specific connectomes that are not directly comparable to one another. Here, we comprehensively chart connectome organization across the mammalian phylogenetic spectrum using a common reconstruction protocol. We analyse the mammalian MRI (MaMI) data set, a database that encompasses high-resolution ex vivo structural and diffusion MRI scans of 124 species across 12 taxonomic orders and 5 superorders, collected using a unified MRI protocol. We assess similarity between species connectomes using two methods: similarity of Laplacian eigenspectra and similarity of multiscale topological features. We find greater inter-species similarities among species within the same taxonomic order, suggesting that connectome organization reflects established taxonomic relationships defined by morphology and genetics. While all connectomes retain hallmark global features and relative proportions of connection classes, inter-species variation is driven by local regional connectivity profiles. By encoding connectomes into a common frame of reference, these findings establish a foundation for investigating how neural circuits change over phylogeny, forging a link from genes to circuits to behaviour.

Funder

Natural Sciences and Engineering Research Council of Canada

Canadian Institutes of Health Research

Fondation Brain Canada

Canada Research Chairs

Michael J. Fox Foundation for Parkinson's Research

Healthy Brains for Healthy Lives

Canadian Institute for Advanced Research

National Science Foundation - BSF

National Institute of Mental Health

Publisher

eLife Sciences Publications, Ltd

Subject

General Immunology and Microbiology,General Biochemistry, Genetics and Molecular Biology,General Medicine,General Neuroscience

Reference136 articles.

1. A species-level timeline of mammal evolution integrating phylogenomic data;Álvarez-Carretero;Nature,2021

2. Scaling principles of white matter brain connectivity;Ardesch;Neuroscience,2021

3. Conservation of brain connectivity and wiring across the mammalian class;Assaf;Nature Neuroscience,2020

4. Network morphospace;Avena-Koenigsberger;Journal of the Royal Society, Interface,2015

5. Communication dynamics in complex brain networks;Avena-Koenigsberger;Nature Reviews. Neuroscience,2017

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