Dynamic Repertoire of Intrinsic Brain States Is Reduced in Propofol-Induced Unconsciousness

Abstract

The richness of conscious experience is thought to scale with the size of the repertoire of causal brain states, and it may be diminished in anesthesia. We estimated the state repertoire from dynamic analysis of intrinsic functional brain networks in conscious sedated and unconscious anesthetized rats. Functional resonance images were obtained from 30-min whole-brain resting-state blood oxygen level-dependent (BOLD) signals at propofol infusion rates of 20 and 40 mg/kg/h, intravenously. Dynamic brain networks were defined at the voxel level by sliding window analysis of regional homogeneity (ReHo) or coincident threshold crossings (CTC) of the BOLD signal acquired in nine sagittal slices. The state repertoire was characterized by the temporal variance of the number of voxels with significant ReHo or positive CTC. From low to high propofol dose, the temporal variances of ReHo and CTC were reduced by 78% -20% and 76% -20%, respectively. Both baseline and propofol-induced reduction of CTC temporal variance increased from lateral to medial position. Group analysis showed a 20% reduction in the number of unique states at the higher propofol dose. Analysis of temporal variance in 12 anatomically defined regions of interest predicted that the largest changes occurred in visual cortex, parietal cortex, and caudate-putamen. The results suggest that the repertoire of large-scale brain states derived from the spatiotemporal dynamics of intrinsic networks is substantially reduced at an anesthetic dose associated with loss of consciousness.

Dynamic Connectivity Patterns in Conscious and Unconscious Brain

“…6A). This result is consistent with the notion that the awake state is associated with a richer functional repertoire (Barttfeld et al, Hudetz et al, 2015). The averaged absolute connectivity strength as a function of physical distance between ROIs was shown in Figure 6B for all three dRSFC patterns.…”

“…These methods have made it feasible to investigate the brain network dynamics at different states of consciousness (Barttfeld et al, 2015;Liang et al, 2015a). Indeed, with these approaches, it has been shown that the dynamic properties of brain network connectivity may constitute key characteristics of consciousness (Barttfeld et al, 2015;Breshears et al, 2010;Hudetz et al, 2015).…”

Signature of consciousness in the dynamics of resting-state brain activity

“…Such simulations have established that, for low coupling strength between brain areasa configuration that resembles the sedated condition-spontaneous neuronal activity is still present but mostly traces the fixed network defined by structural connectivity, and as a result, only a single stable spontaneous connectivity pattern occurs (16,17). As the coupling strength increases, a qualitative change in the dynamics occurs: instead of having a single stable state, the system becomes multistable; functional activity spontaneously breaks down into a diversity of states that is sequentially explored in a stochastic manner (16,21,23,37,38). It has been argued that the brain operates precisely at the edge of this dynamical change-or critical state (39)-in which the system is maximally sensitive to external stimulation.…”

“…simulations of resting state brain activity (16,(21)(22)(23)(24), is that signatures of the conscious state lie in the dynamics of spontaneous brain activity. When averaged across a long time period, functional brain activity may appear similar in wakefulness and anesthesia (10,11,25), due to the existence of a backbone anatomical connectivity.…”

“…The awake condition should be characterized by an active exploration of a high diversity of network states (22)(23)(24), forming the ceaselessly fluctuating "stream of consciousness" described by William James. During the nonconscious condition, however, spontaneous activity should reduce to the circulation of a more random pattern of neural activity shaped and constrained by the anatomical connectivity (17,21).…”