A transient cortical state with sleep-like sensory responses precedes emergence from general anesthesia in humans.

Laura D Lewis,Patrick L Purdon,Giovanni Piantoni,Linda S Aglio,Oluwaseun Akeju,Emery N Brown,Emad N Eskandar,Eran A Mukamel,Priscilla Grace Harrell,Sydney S Cash,Robert A Peterfreund

doi:10.7554/elife.33250

Abstract

During awake consciousness, the brain intrinsically maintains a dynamical state in which it can coordinate complex responses to sensory input. How the brain reaches this state spontaneously is not known. General anesthesia provides a unique opportunity to examine how the human brain recovers its functional capabilities after profound unconsciousness. We used intracranial electrocorticography and scalp EEG in humans to track neural dynamics during emergence from propofol general anesthesia. We identify a distinct transient brain state that occurs immediately prior to recovery of behavioral responsiveness. This state is characterized by large, spatially distributed, slow sensory-evoked potentials that resemble the K-complexes that are hallmarks of stage two sleep. However, the ongoing spontaneous dynamics in this transitional state differ from sleep. These results identify an asymmetry in the neurophysiology of induction and emergence, as the emerging brain can enter a state with a sleep-like sensory blockade before regaining responsivity to arousing stimuli.

Highlights

During emergence from general anesthesia, the brain transitions out of the unconscious state and recovers its ability to process complex sensory information and coordinate behavioral responses
The sleep spectra exhibited clear spindle power (10–14 Hz) peaks across cortical regions, whereas the emergence spectra exhibited either no peak or a spatially restricted frontal alpha (~10 Hz) peak characteristic of deep propofol anesthesia (Figure 6c). These results demonstrate that while some common neurophysiological events can be observed in stage two sleep and in this transient emergence period, emergence is a distinct brain state that is not identical to sleep. Using both intracranial ECoG and scalp EEG recordings, we found that emergence from general anesthesia is accompanied by a transient state in which auditory stimuli can evoke large potentials (LPs) corresponding to all-or-none cortical suppressions lasting several hundred milliseconds
LPs strongly resemble the K-complexes observed in N2 sleep, the neural dynamics of emergence from general anesthesia represent a distinct state

Summary

Introduction

During emergence from general anesthesia, the brain transitions out of the unconscious state and recovers its ability to process complex sensory information and coordinate behavioral responses. General anesthesia causes a profound disruption of information processing across large-scale cortical (Alkire et al, 2008; Liu et al, 2012; Hudetz, 2012; Lewis et al, 2012; Dehaene et al, 2014; Sarasso et al, 2014) and thalamocortical networks (Alkire et al, 2000; Ching et al, 2010; Mhuircheartaigh et al, 2010; Nı Mhuircheartaigh et al, 2013; Vijayan et al, 2013; Akeju et al, 2014; Baker et al, 2014; Flores et al, 2017), and suppression of arousal systems When infusions of the anesthetic drug stop, patients gradually recover consciousness and awaken, a process called emergence. How the brain switches between the anesthetized and awake states is not well understood

Methods

Results

Conclusion