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Distributed harmonic patterns of structure-function dependence orchestrate human consciousness.

Andrea I Luppi, Jakub Vohryzek, Morten L Kringelbach, Pedro A M Mediano, Michael M Craig, Ram Adapa, Robin L Carhart-Harris, Leor Roseman, Ioannis Pappas, Alexander R D Peattie, Anne E Manktelow, Barbara J Sahakian, Paola Finoia, Guy B Williams, Judith Allanson, John D Pickard, David K Menon, Selen Atasoy, Emmanuel A Stamatakis

Communications biology January 28, 2023 DOI: 10.1038/s42003-023-04474-1 via PubMed

Summary

AI-generated from the abstract

Consciousness depends on how tightly brain function follows the brain's physical wiring. Using MRI scans, researchers measured structure-function coupling across spatial scales in people who were unconscious from anesthesia or brain injury and in people under psychedelics (LSD or ketamine). During loss of consciousness, function more closely tracked the brain's structural connections, a signature that could distinguish behaviorally similar brain-injured patients and detect covert consciousness. In contrast, psychedelics decoupled function from structure, and this decoupling correlated with physiological and subjective scores. The findings suggest that connectome harmonic decomposition reveals how neuromodulation and network architecture jointly shape consciousness.

Study at a glance

Characteristics Observational cohort Peer reviewed
Population Humans under anesthesia, brain-injured patients, and individuals given LSD or ketamine
Interventions LSD ketamine
Keywords Neuroscience Consciousness Brain research Psychedelics Cognitive science
Citations 98
Key finding Structure-function coupling increases across scales during loss of consciousness and decreases during psychedelic-induced altered states.

Abstract

A central question in neuroscience is how consciousness arises from the dynamic interplay of brain structure and function. Here we decompose functional MRI signals from pathological and pharmacologically-induced perturbations of consciousness into distributed patterns of structure-function dependence across scales: the harmonic modes of the human structural connectome. We show that structure-function coupling is a generalisable indicator of consciousness that is under bi-directional neuromodulatory control. We find increased structure-function coupling across scales during loss of consciousness, whether due to anaesthesia or brain injury, capable of discriminating between behaviourally indistinguishable sub-categories of brain-injured patients, tracking the presence of covert consciousness. The opposite harmonic signature characterises the altered state induced by LSD or ketamine, reflecting psychedelic-induced decoupling of brain function from structure and correlating with physiological and subjective scores. Overall, connectome harmonic decomposition reveals how neuromodulation and the network architecture of the human connectome jointly shape consciousness and distributed functional activation across scales.

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