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
Summary
The human brain's consciousness operates like an intricate symphony, where structure and function harmonize in distinct patterns. Researchers discovered that consciousness levels can be measured by analyzing how closely brain structure and function work together. During unconsciousness - whether from anesthesia or injury - brain activity becomes more rigidly tied to structural pathways. Interestingly, psychedelics like LSD create the opposite effect, loosening this structure-function relationship and enabling more flexible brain activity patterns.
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.