Preliminary Evidence That Circadian Alignment Predicts Neural Response to Monetary Reward in Late Adolescent Drinkers

Abstract

BackgroundRobust evidence links sleep and circadian rhythm disturbances to alcohol use and alcohol-related problems, with a growing literature implicating reward-related mechanisms. However, the extant literature has been limited by cross-sectional designs, self-report or behavioral proxies for circadian timing, and samples without substantive alcohol use. Here, we employed objective measures of sleep and circadian rhythms, and an intensive prospective design, to assess whether circadian alignment predicts the neural response to reward in a sample of late adolescents reporting regular alcohol use.MethodsParticipants included 31 late adolescents (18–22 y/o; 19 female participants) reporting weekly alcohol use. Participants completed a 14-day protocol including pre- and post-weekend (Thursday and Sunday) circadian phase assessments via the dim light melatonin onset (DLMO), in counterbalanced order. Sleep-wake timing was assessed via actigraphy. Circadian alignment was operationalized as the DLMO-midsleep interval; secondary analyses considered social jet lag based on weekday-weekend differences in midsleep or DLMO. Neural response to reward (anticipation and outcome) was assessed via a monetary reward fMRI task (Friday and Monday scans). Alcohol use was assessed at baseline and via ecological momentary assessment. Mean BOLD signal was extracted from two regions-of-interest (striatum and medial prefrontal cortex, mPFC) for analyses in regression models, accounting for age, sex, racial identity, and scan order.ResultsIn primary analyses, shorter DLMO-midsleep intervals (i.e., greater misalignment) on Thursday predicted lower striatal and mPFC responses to anticipated reward, but not reward outcome, on Friday. Lower neural (striatum and mPFC) responses to anticipated reward on Friday correlated with more binge-drinking episodes at baseline, but were not associated with alcohol use in the post-scan weekend. In secondary analyses, greater social jet lag (particularly larger weekend delays in midsleep or DLMO) was associated with lower neural responses to reward anticipation on Monday.ConclusionFindings provide preliminary evidence of proximal associations between objectively determined circadian alignment and the neural response to anticipated monetary reward, which is linked in turn to patterns of problematic drinking. Replication in a larger sample and experimental designs will be important next steps to determining the extent to which circadian misalignment influences risk for alcohol involvement via alterations in reward function.

Sleep variability and regularity as contributors to obesity and cardiometabolic health in adolescence

“…All these forms of circadian misalignment may have a direct impact on adolescent health and, in addition, may lead to insufficient sleep, which will further impact the ability to perform during the day [28]. Research also shows that the impact of a misaligned circadian timing of sleep and of insufficient sleep extends beyond academic outcomes, having been linked to mood disorders [29], substance use [30], behavioral problems [31], and adverse cardiometabolic health outcomes, as reviewed in the following sections [32,33]. In fact, evidence for the cardiometabolic health impact of various forms of circadian misalignment in adults has come from both naturally occurring models (e.g., shift work) [34], as well as experimental studies [34].…”

The circadian neurobiology of reward

“…More specifically, larger differences in weekend–weekday sleep timing (i.e., increased social jetlag) as indicated by actigraphy data were associated with decreased activation in the mPFC and the caudate during reward anticipation and decreased activation in the mPFC and the VS in the reward receipt phase in a sample of healthy adolescents 114 . Moreover, a shorter dim light melatonin onset (DLMO) midsleep interval on Thursday was associated with lower striatal and mPFC response to reward anticipation on Friday, which was in turn associated with problematic drinking 115 . So far, only one study 116 aimed at manipulating circadian rhythmicity in human adolescents in order to estimate causality of the circadian—reward interaction.…”

“…114 Moreover, a shorter dim light melatonin onset (DLMO) midsleep interval on Thursday was associated with lower striatal and mPFC response to reward anticipation on Friday, which was in turn associated with problematic drinking. 115 So far, only one study 116 aimed at manipulating circadian rhythmicity in human adolescents in order to estimate causality of the circadian-reward interaction. Here, circadian misalignment was induced by shifting sleep-wake times for 1 week to the typical school year sleep-wake times (20:00-05:30), which was compared with an "aligned" condition based on typical summer sleep-wake times (00:00-09:30).…”

Preliminary evidence that misalignment between sleep and circadian timing alters risk‐taking preferences

“…Circadian alignment was operationalised as the phase angle (interval) between DLMO and midsleep, with deviations from the median DLMO‐midsleep phase angle interpreted as misalignment. This operationalisation has been utilised in prior research and greater misalignment (most typically shorter DLMO‐midsleep phase angles, although sometimes longer DLMO‐midsleep phase angle) has been linked to worse functional outcomes such as greater depressive symptomology and alcohol use, as well as altered reward‐related brain function (Emens et al, 2009; Hasler, 2022; Hasler et al, 2019; Lewy et al, 2007) .…”

“…The project employed data from 36 late adolescent participants who completed two overnight in‐laboratory assessments of circadian timing (i.e., dim‐light melatonin onset [DLMO]), were administered risky decision‐making tasks, and wore wrist actigraphs to assess sleep over 14 days. The DLMO and actigraphy data allow, for the first time in the decision‐making literature, estimation of objective circadian alignment via the DLMO‐midsleep phase angle (Emens, Lewy, Kinzie, Arntz, & Rough, 2009; Hasler, 2022; Hasler et al, 2019; Lewy et al, 2007). The use of three distinct decision‐making tasks (the lottery choice task, the unusual disease task, and the guessing game task [Nagel, 1995; Smith, Dickhaut, McCabe, & Pardo, 2002; Tversky & Kahneman, 1981]) allows for consideration of a range of decision‐making processes that relate to high‐level decision making and risky choice.…”