Divergent connectomic organization delineates genetic evolutionary traits in the human brain

Elisenda Bueichekú,Federico D’Oleire Uquillas,Ibai Diez,William Orwig,Elena Ortiz-Teran,Laura Ortiz-Teran,Silvia Basaia,Jose M Gonzalez-De-Echavarri,Jorge Sepulcre,Victor Montal,Chan-Mi Kim,Lola De Marcos

doi:10.1038/s41598-021-99082-6

Abstract

The relationship between human brain connectomics and genetic evolutionary traits remains elusive due to the inherent challenges in combining complex associations within cerebral tissue. In this study, insights are provided about the relationship between connectomics, gene expression and divergent evolutionary pathways from non-human primates to humans. Using in vivo human brain resting-state data, we detected two co-existing idiosyncratic functional systems: the segregation network, in charge of module specialization, and the integration network, responsible for information flow. Their topology was approximated to whole-brain genetic expression (Allen Human Brain Atlas) and the co-localization patterns yielded that neuron communication functionalities—linked to Neuron Projection—were overrepresented cell traits. Homologue-orthologue comparisons using dN/dS-ratios bridged the gap between neurogenetic outcomes and biological data, summarizing the known evolutionary divergent pathways within the Homo Sapiens lineage. Evidence suggests that a crosstalk between functional specialization and information flow reflects putative biological qualities of brain architecture, such as neurite cellular functions like axonal or dendrite processes, hypothesized to have been selectively conserved in the species through positive selection. These findings expand our understanding of human brain function and unveil aspects of our cognitive trajectory in relation to our simian ancestors previously left unexplored.

Highlights

The relationship between human brain connectomics and genetic evolutionary traits remains elusive due to the inherent challenges in combining complex associations within cerebral tissue
The objective of the connectomics analysis was to investigate the spatiotemporal configuration of the human brain connectome as minimal graphs
The results found support that the Neuron projection functionality has been conserved through the human lineage, as the brain phenotype map used for the connectomics and genetics information represented both the early-mergers network and the late-mergers network, its positive expression would be related to the early-mergers network

Summary

Introduction

The relationship between human brain connectomics and genetic evolutionary traits remains elusive due to the inherent challenges in combining complex associations within cerebral tissue. Using in vivo human brain restingstate data, we detected two co-existing idiosyncratic functional systems: the segregation network, in charge of module specialization, and the integration network, responsible for information flow Their topology was approximated to whole-brain genetic expression (Allen Human Brain Atlas) and the co-localization patterns yielded that neuron communication functionalities—linked to Neuron Projection—were overrepresented cell traits. Graph theory principles have helped advance the field of cognitive neuroscience to formalize connectivity principles[28,39], making it possible to quantitatively define its hierarchical spatial organization and temporal d ynamics[25,40,41] Resources such as the Allen Human Brain Atlas ( AHBA42) have presented new possibilities to link neuroimaging phenotypes and in situ brain genetic information, offering whole-brain genome-wide expression p atterns[27,42]

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Conclusion