Sleep Deprivation Effects on Brain State Dynamics Are Associated With Dopamine D2 Receptor Availability Via Network Control Theory

Background

Sleep deprivation (SD) negatively affects brain function. Most brain imaging studies have investigated the effects of SD on static brain function. SD effects on functional brain dynamics and their relationship with molecular changes remain relatively unexplored.

Methods

We used functional magnetic resonance imaging to examine resting-brain state dynamics after one night of SD compared with rested wakefulness (N = 41) and assessed the association of brain state dynamics with striatal brain dopamine D₂ receptor availability measured by positron emission tomography [¹¹C]raclopride using network control theory.

Results

SD reduced dwell time and persistence probabilities, with the strongest effects in two brain states, one characterized by high default mode network and low dorsal attention network activity and the other by high frontoparietal network and low somatomotor network activity. Using network control theory, we showed that after SD, there was an overall increase in the control energy required for brain state transitions, with effects varying for different brain state transitions. Control energy requirement was negatively associated with transition probabilities under SD and restful wakefulness and accounted for SD-induced changes in transition probabilities. Alteration in the energy landscape was associated with SD-induced changes in striatal D₂ receptor distribution.

Conclusions

These findings demonstrate altered occurrence of internally and externally oriented brain states following acute SD and suggest an association with energy requirements for brain state transitions modulated by striatal D₂ receptors.