Distributed harmonic patterns of structure-function dependence orchestrate human consciousness

• DOI: 10.1101/2020.08.10.244459
• Publication Date: 2020-08-11T09:37:01Z
• Authors: Andrea I. Luppi; Jakub Vohryzek; Morten L. Kringel...; Pedro A.M. Mediano; Michael M. Craig; Ram Adapa; Robin L. Carhart-...; Leor Roseman; Ioannis Pappas; Alexander R.D. Pe...; Anne E. Manktelow; Barbara J. Sahakian; Paola Finoia; Guy B. Williams; Judith Allanson; John D. Pickard; David K. Menon; Selen Atasoy; Emmanuel A. Stama...
• Keywords: 0301 basic medicine; 570; /631/378/116/1925; Biomedical and clinical sciences; Consciousness; QH301-705.5; 1.1 Normal biological development and functioning; 610; Article; 03 medical and health sciences; 0302 clinical medicine; Underpinning research; Dynamical systems; Connectome; Humans; Biology (General); Network models; Biomedical and Clinical Sciences; Neurosciences; article; Brain; Biological Sciences; Magnetic Resonance Imaging; Brain Disorders; 3. Good health; Biological sciences; /631/378/116/2393; /631/378/2649/1398; Neurological; Hallucinogens; /59/57; /59/36

AbstractA central question in neuroscience is how consciousness arises from the dynamic interplay of brain structure and function. Departing from the predominant location- centric view in neuroimaging, here we provide an alternative perspective on the neural signatures of human consciousness: one that is intrinsically centered on how the distributed network architecture of the human structural connectome shapes functional activation across scales. We decompose cortical dynamics of resting-state functional MRI into fundamental distributed patterns of structure- function association: the harmonic modes of the human structural connectome. We contrast wakefulness with a wide spectrum of states of consciousness, spanning chronic disorders of consciousness but also pharmacological perturbations of consciousness induced with the anaesthetic propofol and the psychoactive drugs ketamine and LSD. Decomposing this wide spectrum of states of consciousness in terms of “connectome harmonics” reveals a generalisable structure-function signature of loss of consciousness, whether due to anaesthesia or brain injury. A mirror-reverse of this harmonic signature characterises the altered state induced by LSD or ketamine, reflecting psychedelic-induced decoupling of brain function from structure. The topology and neuroanatomy of the human connectome are crucial for shaping the repertoire of connectome harmonics into a fine-tuned indicator of consciousness, correlating with physiological and subjective scores across datasets and capable of discriminating between behaviourally indistinguishable sub-categories of brain-injured patients, tracking the presence of covert consciousness. Overall, connectome harmonic decomposition identifies meaningful relationships between neurobiology, brain function, and conscious experience.