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General anaesthesia decreases the uniqueness of brain functional connectivity across individuals and species.

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Peer-reviewed

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Abstract

The human brain is characterized by idiosyncratic patterns of spontaneous thought, rendering each brain uniquely identifiable from its neural activity. However, deep general anaesthesia suppresses subjective experience. Does it also suppress what makes each brain unique? Here we used functional MRI scans acquired under the effects of the general anaesthetics sevoflurane and propofol to determine whether anaesthetic-induced unconsciousness diminishes the uniqueness of the human brain, both with respect to the brains of other individuals and the brains of another species. Using functional connectivity, we report that under anaesthesia individual brains become less self-similar and less distinguishable from each other. Loss of distinctiveness is highly organized: it co-localizes with the archetypal sensory-association axis, correlating with genetic and morphometric markers of phylogenetic differences between humans and other primates. This effect is more evident at greater anaesthetic depths, reproducible across sevoflurane and propofol and reversed upon recovery. Providing convergent evidence, we show that anaesthesia shifts the functional connectivity of the human brain closer to the functional connectivity of the macaque brain in a low-dimensional space. Finally, anaesthesia diminishes the match between spontaneous brain activity and cognitive brain patterns aggregated from the Neurosynth meta-analytic engine. Collectively, the present results reveal that anaesthetized human brains are not only less distinguishable from each other, but also less distinguishable from the brains of other primates, with specifically human-expanded regions being the most affected by anaesthesia.

Description

Journal Title

Nat Hum Behav

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Journal ISSN

2397-3374
2397-3374

Volume Title

Publisher

Springer Science and Business Media LLC

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Except where otherwised noted, this item's license is described as Attribution 4.0 International
Sponsorship
We acknowledge the support of the Natural Sciences and Engineering Research Council of Canada (NSERC), (funding reference number 202209BPF-489453-401636, Banting Postdoctoral Fellowship) [A.I.L]; FRQNT Strategic Clusters Program (2020-RS4-265502 - Centre UNIQUE - Union Neuroscience & Artificial Intelligence - Quebec) via the UNIQUE Neuro-AI Excellence Award [A.I.L]; the Brain Canada Foundation, through the Canada Brain Research Fund with the support of Health Canada [to D.B.]; the National Institutes of Health (grants no. NIH R01 AG068563A and NIH R01 R01DA053301-01A1) [to D.B.]; the Canadian Institute of Health Research (grants no. CIHR 438531 and CIHR 470425) [to D.B.]; the Healthy Brains Healthy Lives initiative (Canada First Research Excellence fund) [to D.B.]; Google (Research Award, Teaching Award) [to D.B.]; the CIFAR Artificial Intelligence Chairs programme (Canada Institute for Advanced Research) [to D.B.]; the Stephen Erskine Fellowship of Queens College, Cambridge [to E.A.S.]; the Canada Excellence Research Chairs program (215063) [to A.M.O.]; the L’Oreal- Unesco for Women in Science Excellence Research Fellowship [to L.N.]; the Natural Sciences and Engineering Research Council of Canada (NSERC) [to B.M)]; the Canadian Institutes of Health Research (CIHR) [to B.M)]; Brain Canada Foundation Future Leaders Fund [to B.M)]; the Canada Research Chairs Program [to B.M)]; the Michael J. Fox Foundation [to B.M)]; the Healthy Brains for Healthy Lives initiative [to B.M)]; the SNSF Ambizione project "Fingerprinting the brain: network science to extract features of cognition, behaviour and dysfunction" (grant number PZ00P2-185716) [to E.A.]. The seveoflurane data were acquired with the support of the Technical University Munich. Human connectome data were provided by the Human Connectome Project, WU–Minn Consortium (1U54MH091657; Principal Investigators David Van Essen and Kamil Ugurbil) funded by the 16 National Institutes of Health (NIH) institutes and centers that support the NIH Blueprint for Neuroscience Research, and by the McDonnell Center for Systems Neuroscience at Washington University. The funders had no role in study design, data collection and analysis, decision to publish or preparation of the manuscript.