Cited by 491Sleep and Wakefulness ResearchSleep and Work-Related FatigueNeurotransmitter Receptor Influence on Behavior

The DOI matches its Crossref record; 75 of the 76 references it cites were found in a registry or an index; none of the 48 sources its claims cite is checked for support yet.

Sleep Deprivation Amplifies Reactivity of Brain Reward Networks, Biasing the Appraisal of Positive Emotional Experiences

Open access
Gujar, Ninad, Yoo, Seung-Schik, Hu, Peter, Walker, Matthew P.·2011·The Journal of Neuroscience

Abstract

Appropriate interpretation of pleasurable, rewarding experiences favors decisions that enhance survival. Conversely, dysfunctional affective brain processing can lead to life-threatening risk behaviors (e.g., addiction) and emotion imbalance (e.g., mood disorders). The state of sleep deprivation continues to be associated with maladaptive emotional regulation, leading to exaggerated neural and behavioral reactivity to negative, aversive experiences. However, such detrimental consequences are paradoxically aligned with the perplexing antidepressant benefit of sleep deprivation, elevating mood in a proportion of patients with major depression. Nevertheless, it remains unknown how sleep loss alters the dynamics of brain and behavioral reactivity to rewarding, positive emotional experiences. Using functional magnetic resonance imaging (fMRI), here we demonstrate that sleep deprivation amplifies reactivity throughout human mesolimbic reward brain networks in response to pleasure-evoking stimuli. In addition, this amplified reactivity was associated with enhanced connectivity in early primary visual processing pathways and extended limbic regions, yet with a reduction in coupling with medial frontal and orbitofrontal regions. These neural changes were accompanied by a biased increase in the number of emotional stimuli judged as pleasant in the sleep-deprived group, the extent of which exclusively correlated with activity in mesolimbic regions. Together, these data support a view that sleep deprivation not only is associated with enhanced reactivity toward negative stimuli, but imposes a bidirectional nature of affective imbalance, associated with amplified reward-relevant reactivity toward pleasure-evoking stimuli also. Such findings may offer a neural foundation on which to consider interactions between sleep loss and emotional reactivity in a variety of clinical mood disorders.

Overview

AI snapshot

Written from the paper’s full text.

TL;DR

Sleep deprivation amplified fMRI reactivity in mesolimbic reward networks to pleasure-evoking stimuli and biased behavioral appraisal toward rating more images as pleasant. These neural and behavioral changes were linked to altered functional connectivity, including reduced coupling with medial/orbitofrontal regions.

Key findings

  • Sleep-deprived participants showed greater activation to increasing positive stimulus valence in a priori reward/affect regions including the VTA, left putamen, amygdala, and left insula; less activation was observed in right posterior hippocampus, precuneus, and left middle occipital gyrus, though these non-a priori regions did not survive conservative FDR correction.
  • Behaviorally, there was a significant Group × Emotional Response interaction, F(1, 25) = 4.09, P = 0.04. Sleep-deprived participants rated significantly more images as pleasant and fewer as neutral (paired t(13) > 3.06, P < 0.009), whereas controls showed no such difference (paired t(12) < 0.63, P > 0.54); positive bias scores differed between groups, t(25) = 2.17, P = 0.04.
  • In the sleep-deprived group, positive bias scores correlated with activity in the VTA, left fusiform gyrus, and left insula, with conjunction analysis confirming overlap with group-level activation differences.
  • Connectivity analyses showed stronger VTA coupling with left amygdala and left anterior temporal pole, stronger insula coupling with visual cortex regions and posterior insula, and reduced amygdala connectivity with medial prefrontal cortex and bilateral orbitofrontal cortex; no putamen connectivity differences were found.

Methods

  • Twenty-seven healthy participants age 18–30 yr (mean 23.6, s.d. ±1.4) were assigned to sleep deprivation (n = 14, 7 males) or sleep control (n = 13, 6 males). The deprivation group accumulated a mean of 31.9 hr (s.d. ±1.31) total sleep deprivation before scanning; controls obtained a mean of 7.7 hr (s.d. ±1.23) of sleep the prior night.
  • Event-related fMRI used 100 International Affective Picture System stimuli ranging from neutral to increasingly pleasant; participants made binary “pleasant” or “neutral” judgments.
  • Analyses used SPM5 general linear models with parametric modulation by standardized valence, second-level random effects, small-volume correction for a priori reward/affect ROIs, psychophysiological interaction connectivity, regression with positive bias scores, and conjunction analysis.

Limitations

  • Stated: the study lacked polysomnographic sleep assessments, so it could not inform qualitative sleep-stage measures.
  • Stated: several non-a priori regions did not survive more conservative FDR correction, and future work manipulating both valence and arousal in the same experiment is needed to dissociate those factors.
  • Evident from the text: the sample was small (n = 14 sleep-deprived, n = 13 control), the design was a between-group comparison without a same-paradigm negative-valence condition, and the brain–behavior relationships are correlational rather than causal; no direct dopaminergic or neurochemical measure was obtained.

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Integrity signals

Registry

Crossref · 10.1523/jneurosci.3220-10.2011

Cites

75 of 75 references verified0 citation errors · 0 not checkable

Statistics

8 tests recomputed · 0 with the reported and recomputed p on opposite sides of .05

Verification

Claims the paper makes

36 Own result · 29 Not checked yet · 6 Own interpretation · 5 Own method

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Show all 34 claims

  • It may state two separate claims as one. 29
  • The quote only partly states this claim. 1
  • Probably not a substantial claim. 19
42 of 42
  • The paper relies on this without support.

    The between-group differences in brain reactivity and behavioral ratings are attributable to sleep deprivation rather than to circadian/time-of-day or other uncontrolled differences between the groups.

    “In the sleep-deprivation group, subjects were awake across Day-1, Night-1 and Day-2, prior to fMRI scanning on Day-2 (5PM). In the sleep-control group, subjects slept normally at home across Night-1 prior to scanning on Day-2 (5PM).”
  • The paper relies on this without support.

    The positive bias score validly indexes biased appraisal of positive emotional experiences.

    “The second was a positive bias score, which utilized these values, and represented the subtracted difference in the proportion of picture stimuli categorized by the participants as “neutral” from the proportion of picture stimuli categorized as “pleasant.””
  • The paper relies on this without support.

    Prior assessment of emotional brain reactivity under conditions of sleep deprivation has focused on negative valenced stimuli, leaving it unknown how sleep loss alters reactivity to positive emotional experiences.

    “However, to date, the assessment of emotional brain reactivity under conditions of sleep deprivation has focused on negative valenced stimuli.”
  • The paper relies on this without support.

    The sleep-deprivation and sleep-control groups are comparable on relevant baseline characteristics other than sleep deprivation.

    “Twenty-seven healthy participants age 18–30 yr (mean 23.6, s.d.±1.4) were assigned to either a sleep-deprivation group (n=14, 7 males) or sleep-control group (n=13, 6 males).”
4 of 4

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Statistics that don’t add up

Each reported p-value recomputed from its test statistic and degrees of freedom.

2 of 2

Statistics recomputed

Every reported test result, recomputed from its test statistic and degrees of freedom. A result shows as not adding up only once an independent check has confirmed it.

  • Doesn’t add upt(25) = 0.66reported p = .43 · recomputed p = .515

    “t (25) = 0.66, p = .43”

  • Doesn’t add upF(1, 25) = 4.09reported p = .04 · recomputed p = .054

    “F(1, 25) = 4.09, p = .04”

  • Consistentt(25) = 0.28reported p = .78 · recomputed p = .782

    “t (25) = 0.28, p = .78”

  • Consistentt(25) = 0.75reported p = .46 · recomputed p = .460

    “t (25) = 0.75, p = .46”

  • Consistentt(25) = 0.89reported p = .38 · recomputed p = .382

    “t(25) = 0.89, p = .38”

  • Consistentt(13) > 3.06reported p < .009 · recomputed p = .009

    “t(13) > 3.06, p < .009”

  • Consistentt(12) < 0.63reported p > .54 · recomputed p = .541

    “t(12) < 0.63, p > .54”

  • Consistentt(25) = 2.17reported p = .04 · recomputed p = .040

    “t (25) = 2.17, p = .04”

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Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

Each contradiction between two passages listed here was confirmed by an independent check.

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Metadata

Authors
Gujar, N., Yoo, S.-S., Hu, P., & Walker, M. P.
Affiliations
  • University of California, Berkeley (US)
  • Brigham and Women's Hospital (US)
Corresponding author
Walker, Matthew P.
Venue
The Journal of Neuroscience
Published
2011-03-23
Volume
31
Issue
12
Pages
4466-4474
ISSN
  • 0270-6474 (ISSN-L)
  • 1529-2401
OpenAlex
W1968748283
Cited by
491
References
76
Citations by year
2026: 26 · 2025: 28 · 2024: 32 · 2023: 22 · 2022: 21 · 2021: 40 · 2020: 37 · 2019: 51 · 2018: 24 · 2017: 33 · 2016: 29 · 2015: 49 · 2014: 34 · 2013: 37 · 2012: 23
FWCI
16.08
Type
journal article
Language
en
Open access
Locations
  • Journal of Neuroscience (publishedVersion, cc-by-nc-sa)
  • PubMed Central (publishedVersion)
  • PubMed (publishedVersion)
Funders
  • National Institutes of Health
  • National Institute on Aging (AG31164, R01AG031164)
  • National Institute of Mental Health (R01MH093537)
Topics
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Sleep and Wakefulness Research
  • Social Sciences › Psychology › Experimental and Cognitive Psychology › Sleep and Work-Related Fatigue
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
Keywords
sleep deprivation, reward processing, emotional reactivity, primary visual cortex, orbitofrontal cortex, medial prefrontal cortex, mood disorders, major depressive disorder
MeSH terms
Adolescent, Adult, Brain, Brain Mapping, Emotions, Female, Humans, Limbic System, Magnetic Resonance Imaging, Male, Nerve Net, Neural Pathways, Psychomotor Performance, Reinforcement, Psychology, Reward, Sleep Deprivation, Linear Models, Young Adult

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