Local orchestration of distributed functional patterns supporting loss and restoration of consciousness in the primate brain

• Published in: Nature communications Vol. 15; no. 1; pp. 2171 - 22
• Main Authors: Luppi, Andrea I., Uhrig, Lynn, Tasserie, Jordy, Signorelli, Camilo M., Stamatakis, Emmanuel A., Destexhe, Alain, Jarraya, Bechir, Cofre, Rodrigo
• Format: Journal Article
• Language: English
• Published: London Nature Publishing Group UK 11.03.2024; Nature Publishing Group; Nature Portfolio
• Subjects: 59/36; 631/378/116/1925; 631/378/116/2393; 631/378/2649/1398; Anesthesia; Anesthetics; Animals; Arousal; Brain; Brain mapping; Cerebral Cortex; Consciousness; Deep brain stimulation; Electrical stimuli; Functional anatomy; Functional magnetic resonance imaging; Humanities and Social Sciences; Ketamine; Life Sciences; multidisciplinary; Neurons and Cognition; Primates; Propofol; Restoration; Science; Science (multidisciplinary); Sevoflurane; Signatures; Stimulation; Structure-function relationships; Thalamic nuclei; Thalamus
• ISSN: 2041-1723; 2041-1723
• DOI: 10.1038/s41467-024-46382-w

A central challenge of neuroscience is to elucidate how brain function supports consciousness. Here, we combine the specificity of focal deep brain stimulation with fMRI coverage of the entire cortex, in awake and anaesthetised non-human primates. During propofol, sevoflurane, or ketamine anaesthesia, and subsequent restoration of responsiveness by electrical stimulation of the central thalamus, we investigate how loss of consciousness impacts distributed patterns of structure-function organisation across scales. We report that distributed brain activity under anaesthesia is increasingly constrained by brain structure across scales, coinciding with anaesthetic-induced collapse of multiple dimensions of hierarchical cortical organisation. These distributed signatures are observed across different anaesthetics, and they are reversed by electrical stimulation of the central thalamus, coinciding with recovery of behavioural markers of arousal. No such effects were observed upon stimulating the ventral lateral thalamus, demonstrating specificity. Overall, we identify consistent distributed signatures of consciousness that are orchestrated by specific thalamic nuclei. The brain’s role in supporting consciousness is unclear. Here, authors show that global markers of consciousness in macaque cortex are suppressed by many anaesthetics, and restored by local stimulation of a thalamic nucleus that also induces awakening.