Brain network integration dynamics are associated with loss and recovery of consciousness induced by sevoflurane

Abstract

The dynamic interplay of integration and segregation in the brain is at the core of leading theoretical accounts of consciousness. The human brain dynamically alternates between a sub‐state where integration predominates, and a predominantly segregated sub‐state, with different roles in supporting cognition and behaviour. Here, we combine graph theory and dynamic functional connectivity to compare resting‐state functional MRI data from healthy volunteers before, during, and after loss of responsiveness induced with different concentrations of the inhalational anaesthetic, sevoflurane. We show that dynamic states characterised by high brain integration are especially vulnerable to general anaesthesia, exhibiting attenuated complexity and diminished small‐world character. Crucially, these effects are reversed upon recovery, demonstrating their association with consciousness. Higher doses of sevoflurane (3% vol and burst‐suppression) also compromise the temporal balance of integration and segregation in the human brain. Additionally, we demonstrate that reduced anticorrelations between the brain's default mode and executive control networks dynamically reconfigure depending on the brain's state of integration or segregation. Taken together, our results demonstrate that the integrated sub‐state of brain connectivity is especially vulnerable to anaesthesia, in terms of both its complexity and information capacity, whose breakdown represents a generalisable biomarker of loss of consciousness and its recovery.

Distributed harmonic patterns of structure-function dependence orchestrate human consciousness

“…Complementing extensive previous studies that have sought to implicate specific neuroanatomical regions in supporting consciousness (Boveroux et al, 2010; Hannawi et al, 2015; Huang et al, 2020; Luppi et al, 2019, 2021b; MacDonald et al, 2015; di Perri et al, 2018; Ranft et al, 2016; Spindler et al, 2021; Vanhaudenhuyse et al, 2010; Warnaby et al, 2016), our results reveal that the range of states of consciousness considered here can be characterised by their specific patterns of connectome harmonics, regardless of how they are induced. Despite their different molecular mechanisms of action, ketamine (at psychedelic- like dosage) and the serotonergic psychedelic LSD increase the contribution of high-frequency (fine-grained) connectome harmonics, whereas propofol- and brain injury-induced unconsciousness lead to reduced high-frequency and increased low-frequency connectome harmonics - demonstrating the value of CHD as a neural marker of conscious state across datasets.…”

Capacity for consciousness under ketamine anaesthesia is selectively associated with activity in posteromedial cortex in rats

“…Recently, several measures aiming to objectively assess global states of consciousness independently of motor or sensory functions have been developed (see for example Luppi et al. 2021 ), with a notable convergence in evaluating the complexity of brain activity as indication of the capacity for consciousness ( Sarasso et al.…”

LSD and psilocybin flatten the brain’s energy landscape: insights from receptor-informed network control theory

“…It is well-known that even at rest the brain is not static, but rather it dynamically alternates between a number of recurrent states [9][10][11][12][13][14][15][16] . Such recurrent brain-states may be relevant for cognition [17][18][19][20] and even consciousness [21][22][23][24][25][26][27] , and have been shown to undergo prominent reorganization during the psychedelic state induced by LSD 5,6 and psilocybin 7,28 . Crucially, network control theory approaches enable mapping of the brain's energy landscape by quantifying the energy required to transition between these recurrent states (Figure 1a,b).…”