Reward-Related Brain Function and Sleep in Pre/Early Pubertal and Mid/Late Pubertal Adolescents

Abstract

Purpose The onset of adolescence is a time of dramatic changes, including changes in sleep, and a time of new health concerns related to increases in risk-taking, sensation-seeking, depression, substance use, and accidents. As part of a larger study examining puberty-specific changes in adolescents' reward-related brain function, the current paper focuses on the relationship between functional neuroimaging measures of reward and measures of sleep. Methods 58 healthy participants age 11-13 completed a functional magnetic resonance imaging scan using a guessing task with monetary rewards and four-days of at home actigraphy and self-reported sleep ratings. Sleep variables included actigraph measures of mean weekend minutes asleep, sleep onset time, and sleep offset time, as well as self-reported sleep quality. Results During reward anticipation, less activation in the caudate (part of the ventral striatum) was associated with fewer minutes asleep, later sleep onset time, and lower sleep quality. During reward outcome, less caudate activation was associated with later sleep onset time, earlier sleep offset time, and lower sleep quality. Conclusions It has been hypothesized that adolescents' low reactivity in reward-related brain areas could lead to compensatory increases in reward-driven behavior. This study's findings suggest that sleep could contribute to such behavior. Because decreased sleep has been associated with risky behavior and negative mood, these findings raise concerns about a negative spiral whereby the effects of puberty and sleep deprivation may have synergistic effects on reward processing, contributing to adolescent behavioral and emotional health problems.

Sleep and Addictions

“…This is consistent with findings showing less activation in the ventral striatum, during reward anticipation, associated with more chronically disturbed sleep (Holm et al, 2009). 3.…”

“…For example, insomnia and daytime sleepiness were associated with impulsivity in a cohort of college students (Schmidt, Gay, & Van der Linden, 2008); and in adolescents, sleep difficulty was associated with attention problems (FernandezMendoza et al, 2010) and higher frequency of externalizing problems, such as alcohol and substance use (Johnson & Breslau, 2001). Further, acute sleep deprivation was associated with risky decision-making (Acheson, Richards, & de Wit, 2007;Killgore, 2007), while neural response to reward anticipation in the dorsal striatum was positively correlated with subjective sleep quality (Holm et al, 2009).…”

Prospective Relationships Between Sleep Problems and Substance Use, Internalizing and Externalizing Problems

“…A functional Magnetic Resonance Imaging (fMRI) study investigated the effect of sleep deprivation on reward-related brain function and found that adolescents with less adequate sleep displayed less activity in the caudate during reward anticipation and reward outcome (Holm et al 2009). It is speculated that adolescents with less activity in reward related brain circuits have a tendency to compensate for this lack by engaging in rewarddriven behaviour.…”

Asymmetrical frontal cortical activity associated with differential risk for mood and anxiety disorder symptoms: An RDoC perspective

“…Reward processing and approach motivation have not been directly implicated in cognitive activity , and thus, hypomanic/ manic symptoms of elation and expansiveness, as well as cognitive symptoms involving distractibility and flight of ideas, should be less related to relative left frontal activity than the proposed cluster of approach-related hypomanic/manic symptoms. Decreased need for sleep is included in this cluster of approach-related hypomanic/manic symptoms given the coupling of reward processing and approach motivation with sleep variables (Holm et al, 2009;Murray et al, 2009), circadian influences (Murray et al, 2009;Hasler et al, 2010) and circadian genes (Forbes et al, 2011). Increased confidence is included in this cluster given that elevated reward sensitivity, approach motivation, and bipolar spectrum disorders are linked with elevated confidence following goal-attainment (Eisner et al, 2008;Johnson and Jones, 2009;Meyer, et al, 2010).…”