Disrupted neural variability during propofol‐induced sedation and unconsciousness

Abstract

Variability quenching is a widespread neural phenomenon in which trial-to-trial variability (TTV) of neural activity is reduced by repeated presentations of a sensory stimulus. However, its neural mechanism and functional significance remain poorly understood. Recurrent network dynamics are suggested as a candidate mechanism of TTV, and they play a key role in consciousness. We thus asked whether the variability-quenching phenomenon is related to the level of consciousness. We hypothesized that TTV reduction would be compromised during reduced level of consciousness by propofol anesthetics. We recorded functional magnetic resonance imaging signals of resting-state and stimulus-induced activities in three conditions: wakefulness, sedation, and unconsciousness (i.e., deep anesthesia). We measured the average (trial-to-trial mean, TTM) and variability (TTV) of auditory stimulus-induced activity under the three conditions. We also examined another form of neural variability (temporal variability, TV), which quantifies the overall dynamic range of ongoing neural activity across time, during both the resting-state and the task. We found that (a) TTM deceased gradually from wakefulness through sedation to anesthesia, (b) stimulus-induced TTV reduction normally seen during wakefulness was abolished during both sedation and anesthesia, and (c) TV increased in the task state as compared to resting-state during both wakefulness and sedation, but not anesthesia. Together, our results reveal distinct effects of propofol on the two forms of neural variability (TTV and TV). They imply that the anesthetic disrupts recurrent network dynamics, thus prevents the stabilization of cortical activity states. These findings shed new light on the temporal dynamics of neuronal variability and its alteration during anesthetic-induced unconsciousness.

Atypical Temporal Dynamics of Resting State Shapes Stimulus-Evoked Activity in Depression—An EEG Study on Rest–Stimulus Interaction

“…The decreased responsiveness to task-relevant external stimuli—seen in the decreased TTV and LZC changes—may thus be related to instability in the spontaneous activity during the stimulus period. This can be seen in the increased FS and PS; TTV changes are theorized to have the purpose of changing ongoing spontaneous activity as a way to increase the signal-to-noise ratio in favor of the stimulus (26, 27, 29, 82, 84). Further support for this is the correlation of TTV with both FS and PS in alpha and theta.…”

The temporal signature of self: Temporal measures of resting‐state EEG predict self‐consciousness

“…To account for the multiple correlations performed in this study, the Benjamini-Hochberg False Discovery Rate (FDR) (Benjamini & Hochberg, 1995) was applied to all p-values, as was done in recent articles (Arazi et al, 2017;Cruzat et al, 2018;Huang et al, 2018). All statistical tests from the study were listed together and the FDR was applied to all p-values at once.…”

Mathematics and the Brain: A Category Theoretical Approach to Go Beyond the Neural Correlates of Consciousness

“…In terms of the response amplitude, low prestimulus activity levels lead to relatively higher poststimulus activity levels than high prestimulus activity levels [ 84 , 85 , 87 ]. Importantly, recent studies in MEG [ 72 , 73 ] and fMRI [ 87 ] demonstrate that prestimulus variance and its nonadditive impact on poststimulus amplitude and variance are related to conscious contents [ 70 , 72 , 73 , 88 ] and the level and state of consciousness [ 87 ]. Most interestingly, a recent study demonstrated that prepoststimulus variance changes are accompanied by the Lempel–Zev complexity (LZC) in the prestimulus interval [ 89 , 90 ].…”