Sleep deprivation effects on brain state dynamics are associated with dopamine D2 receptor availability via network control theory

Abstract

BackgroundSleep 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. MethodsWe used functional MRI to examine resting brain state dynamics after one night of SD compared to rested wakefulness (RW) and assessed their association with striatal brain dopamine D2 receptor availability (D2R) measured by PET-[11C]raclopride using network control theory. ResultsSD 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 frontal parietal 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 RW and accounted for SD-induced changes in transition probabilities. Alteration in the energy landscape was associated with SD-induced changes in striatal D2R distribution. ConclusionsThese 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 D2R.