Individual Differences in the Neural Basis of Response Inhibition After Sleep Deprivation Are Mediated by Chronotype

Abstract

Sleep deprivation (SD) has been reported to severely affect executive function, and interindividual differences in these effects may contribute to the SD-associated cognition impairment. However, it is unclear how individual differences in chronotypes (morning-type, MT; evening-type, ET) influence neurobehavioral functions after SD. To address this question, we used functional magnetic resonance imaging (fMRI) to evaluate whether 24 h of SD differentially affect response inhibition, a core component of executive function, in MT and ET individuals. Accordingly, MT and ET participants were instructed to follow their preferred 7–9-h sleep schedule for 2 weeks at home both prior to and throughout the course of the study, and then performed a go/no-go task during fMRI scanning at 08:00 a.m. both at rested wakefulness (RW) and following SD. We also examined whether the neurobehavioral inhibition differences in the chronotypes in each session can be predicted by subjective ratings (sleepiness, mood, and task) or objective attention. Behaviorally, SD led to an increased response time of go trials (hit RT), more attentional lapses, higher subjective sleepiness, and worse mood indices, but it did not impair the accuracy of go trials (hit rate) and no-go trials (stop rate). Regardless of the presence of SD, ET individuals exhibited a lower stop rate, higher subjective ratings of sleepiness, exhausted mood, and task difficulty in comparison with MT individuals. On the neural level, SD resulted in decreased inhibition-related activation of the right lateral inferior frontal gyrus (rIFG) in MT individuals and increased rIFG activation in ET individuals. Moreover, the rIFG activation in ET individuals after SD was positively correlated to the subjective ratings of sleepiness and effort put into the task, which was considered as a compensatory response to the adverse effects of SD. These findings suggest that individual differences in inhibition-related cerebral activation after SD are influenced by chronotypes. In addition, ET individuals may be vulnerable to response inhibition. Thus, it is essential to take into consideration the chronotype in SD research and sleep medicine.

The impact of social jetlag and chronotype on attention, inhibition and decision making in healthy adults

“…Coutinho et al (2015) reported that short‐term jetlag results in greater default mode network (DMN) activation, deactivation of which is associated with goal‐directed behaviour, target detection and attention in which phasic dopamine release has a crucial modulatory role. In light of the current findings it seems plausible that SJL may promote non‐optimal regulation of frontal cortex processes, as has been indicated for later chronotypes (Song et al, 2019). Further experimental work involving behavioural and imaging techniques as well as studies that replicate the present findings are required to understand how SJL may impact on neural substrates of attention and impulsivity.…”

“…As SJL represents a putative state of chronic circadian misalignment and constrained workday sleep, our findings have implications for the later circadian typology frequently noted in studies examining impulsive traits and in ADHD (Coogan & McGowan, 2017). Our findings suggest that studies that associate impulsivity with later chronotype/delayed circadian function (McGowan & Coogan, 2018; Song et al, 2019) may reflect an effect of greater SJL typically experienced by later chronotypes. Further, there may be differential impacts of chronotype and/or SJL on attention and/or impulsivity in ADHD populations compared to healthy controls.…”

“…Song et al, 2019). Further experimental work involving behavioural and imaging techniques as well as studies that replicate the present findings are required to understand how SJL may impact on neural substrates of attention and impulsivity.Regarding IGT performance, decision making differed as a function of subjective sleep quality, but not chronotype or SJL.…”

Effects of Sleep Restriction on Self-Reported Putting Performance in Golf

“…First, MEQ scores positively correlated with the degree of lateral misalignment in the SR condition, consistent with prior findings of relationships between better visuospatial ability and eveningness (vs. morningness) when performance occurred at times that were incongruent with the performer’s circadian rhythm preference (Barclay &Myachykov, 2017; Nishida et al, 2021). Recent studies showed that inhibition-related cerebral activation after sleep deprivation was modulated by chronotype, involving a compensatory mechanism to cope with the sleep deprivation-induced adverse effects (Song et al, 2019). Among athletes, a robust association between sport and chronotype groups was found, with a higher frequency of morning types involved in sports that required morning performance (Lastella et al, 2016).…”

“…Sleep influences on golf may include not only its decreased duration but also the player's chronotype, often referred to as the circadian preference that describes an individual's predisposition toward morning or evening tee-off times (Roenneberg et al, 2007). Previous neuroimaging studies demonstrated that chronotypes influence cerebral activation related to executive function after sleep deprivation, and this appears to be essential for putting performance (Song et al, 2019).…”