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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.

SUBMITTER: Luppi AI

PROVIDER: S-EPMC7614771 | biostudies-literature | 2022 Jun

REPOSITORIES: biostudies-literature

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A synergistic core for human brain evolution and cognition.

Luppi Andrea I AI Mediano Pedro A M PAM Rosas Fernando E FE Holland Negin N Fryer Tim D TD O'Brien John T JT Rowe James B JB Menon David K DK Bor Daniel D Stamatakis Emmanuel A EA

Nature neuroscience 20220526 6

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 inste ...[more]

PMID: 35618951

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Project description:Genomic drivers of human-specific neurological traits remain largely undiscovered. Duplicated genes expanded uniquely in the human lineage likely contributed to brain evolution, including the increased complexity of synaptic connections between neurons and the dramatic expansion of the neocortex. Discovering duplicate genes is challenging because the similarity of paralogs makes them prone to sequence-assembly errors. To mitigate this issue, we analyzed a complete telomere-to-telomere human genome sequence (T2T-CHM13) and identified 213 duplicated gene families likely containing human-specific paralogs (>98% identity). Positing that genes important in universal human brain features should exist with at least one copy in all modern humans and exhibit expression in the brain, we narrowed in on 362 paralogs with at least one copy across thousands of ancestrally diverse genomes and present in human brain transcriptomes. Of these, 38 paralogs co-express in gene modules enriched for autism-associated genes and potentially contribute to human language and cognition. We narrowed in on 13 duplicate gene families with human-specific paralogs that are fixed among modern humans and show convincing brain expression patterns. Using long-read DNA sequencing revealed hidden variation across 200 modern humans of diverse ancestries, uncovering signatures of selection not previously identified, including possible balancing selection of CD8B. To understand the roles of duplicated genes in brain development, we generated zebrafish CRISPR "knockout" models of nine orthologs and transiently introduced mRNA-encoding paralogs, effectively "humanizing" the larvae. Morphometric, behavioral, and single-cell RNA-seq screening highlighted, for the first time, a possible role for GPR89B in dosage-mediated brain expansion and FRMPD2B function in altered synaptic signaling, both hallmark features of the human brain. Our holistic approach provides important insights into human brain evolution as well as a resource to the community for studying additional gene expansion drivers of human brain evolution.

Dataset Information

A synergistic core for human brain evolution and cognition.

Publications

A synergistic core for human brain evolution and cognition.

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