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Reward-Related Brain Function and Sleep in Pre/Early Pubertal and Mid/Late Pubertal Adolescents
Open accessAbstract
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 article focuses on the relationship between functional neuroimaging measures of reward and measures of sleep.Methods A total of 58 healthy participants 11-13 years of age completed a functional magnetic resonance imaging scan using a guessing task with monetary rewards and 4 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.
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Some groups find no evidence of enhanced ventral striatal responses to reward receipt during adolescence, and there is evidence for a post-pubertal decline in striatal reactivity to reward outcome.
“some groups finding no evidence of enhanced ventral striatal responses to receipt of rewards during adolescence (Bjork et al, 2004, 2010a; Holm et al, 2009; Forbes et al, 2010), along with evidence for a post-pubertal decline in striatal reactivity to reward outcome (Forbes et al, 2010).”
From Rewards, aversions and affect in adolescence: emerging convergences across laboratory animal and human data (2011) · cites this paper as Holm et al, 2009
Later sleep timing is associated with reduced medial prefrontal cortex and ventral striatum responses to monetary reward.
“Later sleep timing is also associated with reduced mPFC (81) and VS responses to monetary reward (85).”
From Impact of Sleep and Circadian Rhythms on Addiction Vulnerability in Adolescents (2018) · cites this paper as [85]
Typically-developing adolescents with shorter sleep duration and lower sleep quality exhibit lower caudate response to reward anticipation, greater insula response to risk-taking, and lower functional connectivity between DLPFC and both insula and ventral striatum during risk taking.
“Typically-developing adolescents with shorter sleep duration and lower sleep quality exhibit lower caudate response to reward anticipation (85), greater insula response to risk-taking, and lower functional connectivity between DLPFC and both insula and VS during risk taking (89)”
From Impact of Sleep and Circadian Rhythms on Addiction Vulnerability in Adolescents (2018) · cites this paper as [85]
Only a few developmental studies have examined how sleep influences reward-related brain function in adolescents, and none have examined how sleep impacts risk taking behavior, cognitive control, and related neural circuitry.
“Although neuroimaging research in adults has shown that sleep deprivation impacts brain function related to reward processing, risk-taking, and cognition (Chee et al., 2011; Gujar et al., 2011; Libedinsky et al., 2011; Venkatraman et al., 2011), only a few developmental studies have examined how sleep influences reward-related brain function in adolescents (Hasler et al., 2012; Holm et al., 2009)”
From The effects of poor quality sleep on brain function and risk taking in adolescence (2013) · cites this paper as Holm et al., 2009
Shorter sleep duration and lower sleep quality were associated with reduced striatal response to monetary reward in healthy 11-13-year-olds.
“Holm and colleagues (2009) reported that shorter sleep duration and lower sleep quality were associated with reduced striatal response to monetary reward in healthy 11–13-year-olds.”
From Sleep and circadian contributions to adolescent alcohol use disorder (2015) · cites this paper as Holm et al., 2009
Sleep deficit, commonly exhibited by individuals with ASD, alters reward receptivity, particularly to social rewards.
“sleep deficit, a problem commonly exhibited by individuals with ASD [216], alters reward receptivity, particularly to social rewards [217-219].”
From Social “wanting” dysfunction in autism: neurobiological underpinnings and treatment implications (2012) · cites this paper as [219]
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Metadata
- Authors
- Holm, S. M., Forbes, E. E., Ryan, N. D., Phillips, M. L., Tarr, J. A., & Dahl, R. E.
- Affiliations
- University of Pittsburgh (US)
- Cardiff University (GB)
- Corresponding author
- Dahl, Ronald E.
- Venue
- Journal of Adolescent Health
- Publisher
- Elsevier BV
- Published
- 2009-10
- Volume
- 45
- Issue
- 4
- Pages
- 326-334
- ISSN
- 1054-139X (ISSN-L)
- PMC
- PMC2817965
- OpenAlex
- W2100087641
- Cited by
- 174
- References
- 41
- Citations by year
- 2026: 9 · 2025: 10 · 2024: 9 · 2023: 12 · 2022: 11 · 2021: 9 · 2020: 9 · 2019: 12 · 2018: 6 · 2017: 6 · 2016: 10 · 2015: 15 · 2014: 8 · 2013: 16 · 2012: 10
- FWCI
- 5.00
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Journal of Adolescent Health (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- ORCA Online Research @Cardiff (Cardiff University) (submittedVersion)
- Funders
- National Institutes of Health (5r01mh076971-05)
- U.S. Public Health Service (K01 74769)
- National Institute of Mental Health (R01-MH076971, P50MH080215, K01MH074769)
- National Institute on Drug Abuse (R01DA018910, DA018910)
- Eunice Kennedy Shriver National Institute of Child Health and Human Development (T32HD049354)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Sleep and Wakefulness Research
- Social Sciences › Psychology › Experimental and Cognitive Psychology › Sleep and related disorders
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural and Behavioral Psychology Studies
- Keywords
- reward processing, sleep, puberty, adolescents, caudate nucleus, ventral striatum, sleep latency, sleep quality, sleep deprivation, risk-taking, sensation seeking, actigraphy
- MeSH terms
- Adolescent, Brain, Child, Cognition, Female, Humans, Magnetic Resonance Imaging, Male, Puberty, Reward, Sleep, Task Performance and Analysis
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