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A synergistic core for human brain evolution and cognition

journal contribution
posted on 2024-03-27, 15:39 authored by Andrea I Luppi, Pedro A M Mediano, Fernando Ernesto Rosas De AndracaFernando Ernesto Rosas De Andraca, Negin Holland, Tim D Fryer, John T O’Brien, James B Rowe, David K Menon, Daniel Bor, Emmanuel A Stamatakis
How does the organization of neural information processing enable humans’ sophisticated cognition? Here we decompose functional interactions between brain regions into synergistic and redundant components, revealing their distinct information-processing roles. Combining functional and structural neuroimaging with meta-analytic results, we demonstrate that redundant interactions are predominantly associated with structurally coupled, modular sensorimotor processing. Synergistic interactions instead support integrative processes and complex cognition across higher-order brain networks. The human brain leverages synergistic information to a greater extent than nonhuman primates, with high-synergy association cortices exhibiting the highest degree of evolutionary cortical expansion. Synaptic density mapping from positron emission tomography and convergent molecular and metabolic evidence demonstrate that synergistic interactions are supported by receptor diversity and human-accelerated genes underpinning synaptic function. This information-resolved approach provides analytic tools to disentangle information integration from coupling, enabling richer, more accurate interpretations of functional connectivity, and illuminating how the human neurocognitive architecture navigates the trade-off between robustness and integration.

History

Publication status

  • Published

File Version

  • Accepted version

Journal

Nature Neuroscience

ISSN

1097-6256

Publisher

Springer Science and Business Media LLC

Issue

6

Volume

25

Page range

771-782

Department affiliated with

  • Informatics Publications

Institution

University of Sussex

Peer reviewed?

  • Yes