Scaling Principles of White Matter Connectivity in the Human and Nonhuman Primate Brain.


Journal

Cerebral cortex (New York, N.Y. : 1991)
ISSN: 1460-2199
Titre abrégé: Cereb Cortex
Pays: United States
ID NLM: 9110718

Informations de publication

Date de publication:
16 06 2022
Historique:
received: 27 05 2021
revised: 23 09 2021
accepted: 24 09 2021
pubmed: 2 12 2021
medline: 6 7 2022
entrez: 1 12 2021
Statut: ppublish

Résumé

Brains come in many shapes and sizes. Nature has endowed big-brained primate species like humans with a proportionally large cerebral cortex. Comparative studies have suggested, however, that the total volume allocated to white matter connectivity-the brain's infrastructure for long-range interregional communication-does not keep pace with the cortex. We investigated the consequences of this allometric scaling on brain connectivity and network organization. We collated structural and diffusion magnetic resonance imaging data across 14 primate species, describing a comprehensive 350-fold range in brain size across species. We show volumetric scaling relationships that indeed point toward a restriction of macroscale connectivity in bigger brains. We report cortical surface area to outpace white matter volume, with larger brains showing lower levels of overall connectedness particularly through sparser long-range connectivity. We show that these constraints on white matter connectivity are associated with longer communication paths, higher local network clustering, and higher levels of asymmetry in connectivity patterns between homologous areas across the left and right hemispheres. Our findings reveal conserved scaling relationships of major brain components and show consequences for macroscale brain circuitry, providing insights into the connectome architecture that could be expected in larger brains such as the human brain.

Identifiants

pubmed: 34849623
pii: 6438119
doi: 10.1093/cercor/bhab384
pmc: PMC9247419
doi:

Types de publication

Journal Article Research Support, Non-U.S. Gov't Research Support, N.I.H., Extramural

Langues

eng

Sous-ensembles de citation

IM

Pagination

2831-2842

Subventions

Organisme : Wellcome Trust
ID : 203139/Z/16/Z
Pays : United Kingdom
Organisme : NINDS NIH HHS
ID : R24 NS092988
Pays : United States
Organisme : EPA
ID : EP-C-16-015
Pays : United States
Organisme : Wellcome Trust
Pays : United Kingdom
Organisme : NIA NIH HHS
ID : P01 AG026423
Pays : United States
Organisme : NIH HHS
ID : P51 OD011132
Pays : United States

Informations de copyright

© The Author(s) 2021. Published by Oxford University Press.

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Auteurs

Dirk Jan Ardesch (DJ)

Department of Complex Trait Genetics, Center for Neurogenomics and Cognitive Research, Vrije Universiteit Amsterdam, Amsterdam Neuroscience, 1081 HV, Amsterdam, the Netherlands.

Lianne H Scholtens (LH)

Department of Complex Trait Genetics, Center for Neurogenomics and Cognitive Research, Vrije Universiteit Amsterdam, Amsterdam Neuroscience, 1081 HV, Amsterdam, the Netherlands.

Siemon C de Lange (SC)

Department of Complex Trait Genetics, Center for Neurogenomics and Cognitive Research, Vrije Universiteit Amsterdam, Amsterdam Neuroscience, 1081 HV, Amsterdam, the Netherlands.
Department of Sleep and Cognition, Netherlands Institute for Neuroscience (NIN), an institute of the Royal Netherlands Academy of Arts and Sciences, 1105 BA Amsterdam, the Netherlands.

Lea Roumazeilles (L)

Wellcome Centre for Integrative Neuroimaging, Department of Experimental Psychology, University of Oxford, Oxford OX1 3SR, UK.

Alexandre A Khrapitchev (AA)

Medical Research Council Oxford Institute for Radiation Oncology, University of Oxford, Oxford OX3 7DQ, UK.

Todd M Preuss (TM)

Yerkes National Primate Research Center, Emory University, Atlanta, GA 30329, USA.
Center for Translational Social Neuroscience, Emory University, Atlanta, GA 30329, USA.
Department of Pathology and Laboratory Medicine, Emory University School of Medicine, Atlanta, GA 30307, USA.

James K Rilling (JK)

Yerkes National Primate Research Center, Emory University, Atlanta, GA 30329, USA.
Center for Translational Social Neuroscience, Emory University, Atlanta, GA 30329, USA.
Department of Anthropology, Emory University, Atlanta, GA 30322, USA.
Silvio O. Conte Center for Oxytocin and Social Cognition, Emory University, Atlanta, GA 30322, USA.
Department of Psychiatry and Behavioral Sciences, Emory University, Atlanta, GA 30322, USA.

Rogier B Mars (RB)

Donders Institute for Brain, Cognition and Behaviour, Radboud University Nijmegen, AJ 6525, Nijmegen, the Netherlands.
Wellcome Centre for Integrative Neuroimaging, Centre for fMRI of the Brain (FMRIB), Nuffield Department of Clinical Neurosciences, John Radcliffe Hospital, University of Oxford, Oxford OX3 9DU, UK.

Martijn P van den Heuvel (MP)

Department of Complex Trait Genetics, Center for Neurogenomics and Cognitive Research, Vrije Universiteit Amsterdam, Amsterdam Neuroscience, 1081 HV, Amsterdam, the Netherlands.
Department of Child Psychiatry, Amsterdam UMC, Vrije Universiteit Amsterdam, Amsterdam Neuroscience, 1081 HV, Amsterdam, the Netherlands.

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