Inhibitory Decay and Supercritical Brain Dynamics During Sleep Deprivation

Sleep deprivation (SD) changes brain-wide dynamics, but the circuit-level perturbation that can generate this systems-level shift remains unclear. We scanned 26 participants at seven time points across 36 h of continuous wakefulness and assessed criticality from resting-state functional Magnetic Resonance Imaging (rs-fMRI) blood-oxygen-level-dependent (BOLD) signals using neuronal avalanche metrics (branching ratio and mean avalanche size). The branching ratio increased from 0.98 at baseline to 1.08 after 36 h, indicating a progressive shift from near-critical to supercritical propagation. Interestingly, the shift was heterogeneous. Visual and sensorimotor networks showed the largest deviations, whereas the limbic network remained close to criticality. Criticality changes tracked accumulated subjective sleep pressure but were largely dissociated from psychomotor vigilance lapses. SD also reshaped functional network organization, with the functional connectivity (FC) degree distribution shifting toward more high-degree nodes. In a recurrent excitatory-inhibitory network model, gamma-band power provided an interpretable proxy for effective gain and inhibitory control. Using this proxy, selectively reducing inhibitory efficacy was sufficient to capture the direction of the near-critical-to-supercritical drift and a limbic-like resilience pattern, supporting inhibitory decay as a plausible candidate circuit-level mechanism linking SD to large-scale propagation instability.