Cortical functional connectivity indexes arousal state during sleep and anesthesia

• Published in: NeuroImage (Orlando, Fla.) Vol. 211; p. 116627
• Main Authors: Banks, Matthew I., Krause, Bryan M., Endemann, Christopher M., Campbell, Declan I., Kovach, Christopher K., Dyken, Mark Eric, Kawasaki, Hiroto, Nourski, Kirill V.
• Format: Journal Article
• Language: English
• Published: United States Elsevier Inc 01.05.2020; Elsevier Limited; Elsevier
• Subjects: Adult; Alpha Rhythm - physiology; Alpha-band connectivity; Anesthesia; Arousal; Brain research; Cerebral Cortex - diagnostic imaging; Cerebral Cortex - physiology; Connectome; Consciousness; Convulsions & seizures; Electrocorticography; Electrodes; Female; Humans; Hypnotics and Sedatives - pharmacology; Information processing; Intracranial electrophysiology; Male; Nerve Net - diagnostic imaging; Nerve Net - physiology; Neural networks; Neurosurgery; Phase lag index; Prefrontal cortex; Prefrontal Cortex - diagnostic imaging; Prefrontal Cortex - physiology; Propofol; Propofol - pharmacology; REM sleep; Sensory integration; Sleep; Sleep and wakefulness; Sleep Stages - physiology; Somatosensory cortex; Surgery; Temporal cortex; Temporal lobe; Unconsciousness - chemically induced; Unconsciousness - diagnostic imaging; Unconsciousness - physiopathology; Young Adult; United States > US; Iowa; Phase lag index; Alpha-band connectivity; Consciousness; Intracranial electrophysiology
• ISSN: 1053-8119; 1095-9572; 1095-9572
• DOI: 10.1016/j.neuroimage.2020.116627

Disruption of cortical connectivity likely contributes to loss of consciousness (LOC) during both sleep and general anesthesia, but the degree of overlap in the underlying mechanisms is unclear. Both sleep and anesthesia comprise states of varying levels of arousal and consciousness, including states of largely maintained conscious experience (sleep: N1, REM; anesthesia: sedated but responsive) as well as states of substantially reduced conscious experience (sleep: N2/N3; anesthesia: unresponsive). Here, we tested the hypotheses that (1) cortical connectivity will exhibit clear changes when transitioning into states of reduced consciousness, and (2) these changes will be similar for arousal states of comparable levels of consciousness during sleep and anesthesia. Using intracranial recordings from five adult neurosurgical patients, we compared resting state cortical functional connectivity (as measured by weighted phase lag index, wPLI) in the same subjects across arousal states during natural sleep [wake (WS), N1, N2, N3, REM] and propofol anesthesia [pre-drug wake (WA), sedated/responsive (S), and unresponsive (U)]. Analysis of alpha-band connectivity indicated a transition boundary distinguishing states of maintained and reduced conscious experience in both sleep and anesthesia. In wake states WS and WA, alpha-band wPLI within the temporal lobe was dominant. This pattern was largely unchanged in N1, REM, and S. Transitions into states of reduced consciousness N2, N3, and U were characterized by dramatic changes in connectivity, with dominant connections shifting to prefrontal cortex. Secondary analyses indicated similarities in reorganization of cortical connectivity in sleep and anesthesia. Shifts from temporal to frontal cortical connectivity may reflect impaired sensory processing in states of reduced consciousness. The data indicate that functional connectivity can serve as a biomarker of arousal state and suggest common mechanisms of LOC in sleep and anesthesia. •Mechanisms of loss of consciousness are key for basic science and clinical practice.•Loss of consciousness during sleep and anesthesia share common mechanisms.•We studied this using intracranial electrophysiology in neurosurgical patients.•Loss of consciousness was characterized by similar shifts in brain connectivity.•The findings will aid improvements in diagnosis of disorders of consciousness.