Cortical functional connectivity indexes arousal state during sleep and anesthesia.

Summary

Disruption of cortical connectivity likely contributes to loss of consciousness during sleep and general anesthesia, but the degree of overlap in mechanisms is unclear. Using intracranial recordings from five adult neurosurgical patients, alpha-band connectivity (measured by weighted phase lag index) was compared across natural sleep stages and propofol anesthesia. In wake states, alpha-band connectivity within the temporal lobe was dominant, a pattern largely unchanged in light sleep (N1, REM) and sedated states. Transitions into states of reduced consciousness (deep sleep N2/N3 and anesthesia-induced unresponsiveness) showed dramatic shifts, with dominant connections moving to prefrontal cortex. The findings suggest common mechanisms of loss of consciousness in sleep and anesthesia.

Study at a glance

Abstract

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.