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A synergistic core for human brain evolution and cognition

Abstract:
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.
Publication status:
Published
Peer review status:
Peer reviewed

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Publisher copy:
10.1038/s41593-022-01070-0

Authors

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Institution:
University of Oxford
Division:
MSD
Department:
Psychiatry
Role:
Author
ORCID:
0000-0002-3461-6431
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Role:
Author
ORCID:
0000-0003-1789-5894
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Role:
Author
ORCID:
0000-0001-7790-6183
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Role:
Author
ORCID:
0000-0003-1555-9790


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Funder identifier:
https://ror.org/03x94j517
Grant:
MR/M009041/1
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Funder identifier:
https://ror.org/00nc7q809
Grant:
RG99368
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Funder identifier:
https://ror.org/0187kwz08
Grant:
146281
More from this funder
Funder identifier:
https://ror.org/029chgv08
Grant:
210920/Z/18/Z
More from this funder
Funder identifier:
https://ror.org/033sn5p83
Grant:
OPP1144


Publisher:
Springer Nature
Journal:
Nature Neuroscience More from this journal
Volume:
25
Issue:
6
Pages:
771-782
Place of publication:
United States
Publication date:
2022-05-26
Acceptance date:
2022-03-30
DOI:
EISSN:
1546-1726
ISSN:
1097-6256
Pmid:
35618951


Language:
English
Keywords:
Pubs id:
2352509
Local pid:
pubs:2352509
Source identifiers:
W4281567855
Deposit date:
2026-02-13
ARK identifier:

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