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

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.

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

Claims the paper makes

0 of 48 cited sources checked · 0 supported · 0 flagged

  • Findingown data

    The extent of the biased increase in pleasant judgments exclusively correlated with activity in mesolimbic regions.

    “the extent of which exclusively correlated with activity in mesolimbic regions”
    Quote in the paperSubstantial claim
    • Rests on an assumption: 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.
    • Rests on an assumption: The positive bias score validly indexes biased appraisal of positive emotional experiences.
  • Findingown data

    The neural changes were accompanied by a biased increase in the number of emotional stimuli judged as pleasant in the sleep-deprived group.

    “These neural changes were accompanied by a biased increase in the number of emotional stimuli judged as pleasant in the sleep-deprived group”
    • Also stated in: § Behavior · plain
      “Together, these data describe a lopsided bias in the proportion of positive emotional stimulus judgments in the sleep-deprived group relative to the control group.”
    Quote in the paperSubstantial claim
    • Rests on an assumption: 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.
    • Rests on an assumption: The positive bias score validly indexes biased appraisal of positive emotional experiences.
  • Findingown data

    Sleep deprivation amplifies reactivity throughout human mesolimbic reward brain networks in response to pleasure-evoking stimuli.

    “Using fMRI, here we demonstrate that sleep deprivation amplifies reactivity throughout human mesolimbic reward brain networks in response to pleasure-evoking stimuli.”
    • Also stated in: § fMRI – activation differences · hedged
      “Supporting the original hypothesis, significantly greater activation was identified in the deprivation group in a restricted portion of a priori mesolimbic regions previously implicated in mediating reward-driven behavior”
    Quote in the paperSubstantial claim
    • Rests on an assumption: 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.
    • Rests on an assumption: The sleep-deprivation and sleep-control groups are comparable on relevant baseline characteristics other than sleep deprivation.
  • Findingown data

    The amplified reactivity was associated with a reduction in coupling with medial- and orbito-frontal regions.

    “yet with a reduction in coupling with medial- and orbito-frontal regions”
    Quote in the paperSubstantial claim
    • Rests on an assumption: 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.
  • Findingown data

    The amplified reactivity was associated with enhanced connectivity in early primary visual processing pathways and extended limbic regions.

    “this amplified reactivity was associated with enhanced connectivity in early primary visual processing pathways and extended limbic regions”
    Quote in the paperSubstantial claim
    • Rests on an assumption: 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.
  • May combine two claims. 29
  • The quote only partly states this claim. 1
  • Classified as probably not a substantial claim. 19
  • May combine two claims.

    Findingown data

    There was no main effect of Group or Emotional Response, but there was a significant Group x Emotional Response interaction (F(1, 25) = 4.09, P = 0.04).

    “The distribution of responses categorizing stimuli as either pleasant or neutral, displayed in Figure 1A, demonstrated no main effect of Group [sleep control, sleep deprivation] or Emotional Response [neutral, positive] (significance provided in figure), yet a significant Group x Emotional Response interaction (F(1, 25) = 4.09, P = 0.04).”
    Quote in the paperSubstantial claim
  • The quote only partly states this claim.

    Findingown data

    Significantly greater activation was identified in the sleep-deprivation group in a restricted portion of a priori mesolimbic regions, including an area consistent with the ventral tegmental area (VTA) and the left putamen of the dorsal striatum.

    “significantly greater activation was identified in the deprivation group in a restricted portion of a priori mesolimbic regions previously implicated in mediating reward-driven behavior, including an area consistent with the ventral tegmental area (VTA) of the brain stem”
    • Also stated in: § fMRI – activation differences · plain
      “and the left putamen of the dorsal striatum”
    Quote in the paperSubstantial claim
    • Rests on an assumption: 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.
    • Rests on an assumption: The sleep-deprivation and sleep-control groups are comparable on relevant baseline characteristics other than sleep deprivation.
  • May combine two claims.

    Findingown data

    The fusiform area exhibited stronger connectivity with the left anterior temporal pole, similar to the VTA, with additional regions of increased connectivity in left superior insula and left lateral prefrontal cortex.

    “the fusiform area, which demonstrated greater reactivity in the sleep deprived participants at the overall group level, exhibited stronger connectivity with the left anterior temporal pole, similar to the VTA, with additional regions of increased connectivity in left superior insula and left lateral prefrontal cortex”
    Quote in the paperNot a substantial claim
    • Rests on an assumption: 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.
    • Rests on an assumption: The sleep-deprivation and sleep-control groups are comparable on relevant baseline characteristics other than sleep deprivation.
  • May combine two claims.

    Findingown data

    Relative to the null hypothesis of equal categorical assignment (50/50), sleep-deprived participants rated significantly more images as pleasant and significantly fewer images as neutral.

    “Specifically, relative to the null hypothesis of equal categorical assignment (50/50), sleep-deprived participants rated significantly more images as pleasant, and significantly fewer images as neutral (both paired t-test, t(13) > 3.06, P < 0.009).”
    Quote in the paperSubstantial claim
    • Rests on an assumption: The positive bias score validly indexes biased appraisal of positive emotional experiences.
  • May combine two claims.

    Findingown data

    Behaviorally, these neural changes were accompanied by a significant bias in the number of stimuli rated as emotionally pleasant in the sleep-deprived group, and the extent of this bias correlated with overlapping regions in reward- and affect-associated networks.

    “Behaviorally, these neural changes were accompanied by a significant bias in the number of stimuli rated as emotionally pleasant in the sleep-deprived group, the extent of which correlated with overlapping regions in these reward- and affect-associated networks.”
    Quote in the paperSubstantial claim
  • May combine two claims.

    Findingown data

    The enhanced reactivity in the VTA, insula and amygdala in the deprivation group was associated with decreased coupling in midline prefrontal and orbitofrontal cortices, yet increased connectivity with related mesolimbic and early sensory perceptual regions.

    “Therefore, in addition to enhanced reactivity in the VTA, insula and amygdala in the deprivation group, differences in functional connectivity of these regions were also observed, associated with decreased coupling in midline prefrontal and orbitofrontal cortices, yet increased connectivity with related mesolimbic and early sensory perceptual regions.”
    Quote in the paperSubstantial claim
  • May combine two claims.

    Findingown data

    The bilateral amygdala ROIs showed significant decreases in connectivity with medial prefrontal cortex and bilateral orbitofrontal cortex in the deprivation group, together with decreased coupling in the left fusiform gyrus.

    “The bilateral amygdala ROIs, which demonstrated increased reactivity in the deprivation condition at the overall group level, showed significant decreases in connectivity with medial prefrontal cortex and bilateral orbitofrontal cortex in the deprivation group, together with decreased coupling in the left fusiform gyrus (Figure 5C).”
    Quote in the paperSubstantial claim
    • Rests on an assumption: 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.
    • Rests on an assumption: The sleep-deprivation and sleep-control groups are comparable on relevant baseline characteristics other than sleep deprivation.
  • May combine two claims.

    Findingown data

    Regions exhibiting significantly greater reactivity in sleep-deprived participants at the overall group level were common and overlapping with those regions that demonstrated a significant correlation with the positive bias score in the sleep-deprived group.

    “Overlaying the two contrasts—the group-level differences in activation between the two groups, and the regions correlating with the positive bias score in the sleep-deprivation group—demonstrated homology in several areas”
    Quote in the paperSubstantial claim
    • Rests on an assumption: 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.
    • Rests on an assumption: The positive bias score validly indexes biased appraisal of positive emotional experiences.
  • May combine two claims.

    Findingown data

    These regional increases in reactivity were associated with a reduction in functional connectivity in medial and orbitofrontal cortex, yet enhanced coupling in early primary visual processing pathways and extended limbic regions.

    “Moreover, these regional increases were additionally associated with a reduction in functional connectivity in medial and orbitofrontal cortex, yet an enhanced coupling in early primary visual processing pathways and extended limbic regions.”
    Quote in the paperSubstantial claim
  • May combine two claims.

    Findingown data

    The increases in activation in the sleep-deprivation group were not due to a generalized or non-specific amplified reactivity to any and all stimulus kinds, as confirmed by subset analysis showing consistent between-group reactivity differences for the most positive stimuli set but not the most neutral stimuli.

    “That these increases in activation in the sleep-deprivation group were not due to a generalized or non-specific amplified reactivity to any and all stimulus kinds was confirmed by a subset analysis of the upper quartile stimulus set (most positive) and lower quartile stimulus set (most neutral).”
    • Also stated in: § fMRI – activation differences · boosted
      “The analyses, described in detail in Figure 3, demonstrate consistent between-group reactivity differences for the most positive stimuli set, but not the most neutral stimuli.”
    Quote in the paperSubstantial claim
    • Rests on an assumption: 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.
    • Rests on an assumption: The sleep-deprivation and sleep-control groups are comparable on relevant baseline characteristics other than sleep deprivation.
  • May combine two claims.

    Findingown data

    Participants in the sleep-deprived group demonstrated a strong positive ratings bias, while those in the control group showed no such significant shift in response tendency, with these scores being significantly different between groups (t(25) = 2.17, P = 0.04).

    “Participants in the sleep-deprived group demonstrated a strong positive ratings bias, while those in the control group showed no such significant shift in response tendency, with these scores being significantly different between groups (Figure 1B; two-sample t-test, t (25) = 2.17, P = 0.04).”
    Quote in the paperSubstantial claim
    • Rests on an assumption: The positive bias score validly indexes biased appraisal of positive emotional experiences.
  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

    Findingown data

    Greater activation of the visual processing pathway was observed in the left fusiform gyrus, although this none a priori region did not survive a more conservative statistical threshold correction.

    “Greater activation of the visual processing pathway in the left fusiform gyrus, although this none a priori region did not survive a more conservative statistical threshold correction (Table 1).”
    Quote in the paperNot a substantial claim
    • Rests on an assumption: 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.
    • Rests on an assumption: The sleep-deprivation and sleep-control groups are comparable on relevant baseline characteristics other than sleep deprivation.
  • May combine two claims.

    Findingown data

    The fusiform gyrus showed significantly greater reactivity in sleep-deprived relative to sleep-rested subjects, and this reactivity showed a conjunctive overlap with the positive response bias score in sleep-deprived participants.

    “we also identified significantly greater reactivity in the fusiform gyrus in sleep-deprived relative to sleep-rested subjects, which similarly showed a conjunctive overlap with the positive response bias score in sleep-deprived participants.”
    Quote in the paperSubstantial claim
  • Classified as probably not a substantial claim.

    Premisecitation

    Reward mechanisms are supported, in part, by activity in mesolimbic reward pathways including the ventral tegmental nuclei and striatum, as well as the amygdala.

    “Experimental paradigms have demonstrated that these reward mechanisms are supported, in part, by activity in mesolimbic reward pathways including the ventral tegmental nuclei and striatum (Schultz, 2006), as well as the amygdala (Berridge and Robinson, 2003; Murray, 2007).”
    Quote in the paperSubstantial claim0 of 3 sources checked
    • cites Schultz, 2006

      Not checked in the free run.

    • cites Berridge and Robinson, 2003

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    • cites Murray, 2007

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  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

    Premisecitation

    Sleep loss disrupts consolidation of negative emotional memories, resulting in persistent amygdala reactivity during later recollection.

    “Sleep loss also disrupts consolidation of negative emotional memories, resulting in persistent amygdala reactivity during later recollection (Sterpenich et al., 2007).”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Sterpenich et al., 2007

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  • May combine two claims.

    Study design and conductown data

    The amount of sleep obtained during the period prior to the study did not differ between the sleep deprivation group and the sleep rested group in either average number of hours or variability.

    “The amount of sleep obtained during the period prior to the study did not differ between the sleep deprivation group and the sleep rested group in either average number of hours (mean: 7.75 and 7.61, respectively: two-sample t-test, t (25) = 0.28, P = 0.78) or variability, as assessed in standard deviation across nights (mean: 0.46 and 0.53, respectively: t (25) = 0.66, P = 0.43).”
    Quote in the paperSubstantial claim
  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    Larger pupillary responses have been reported under conditions of sleep deprivation, specifically during the viewing of negative emotional picture stimuli.

    “Furthermore, larger pupillary responses have been reported under conditions of sleep deprivation, specifically during the viewing of negative emotional picture stimuli (Franzen et al., 2009).”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Franzen et al., 2009

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    Study design and conductown data

    Omitted response trials did not differ significantly in number between the sleep-control and sleep-deprivation groups.

    “Omitted response trials were modeled separately, and did not differ significantly in number between the sleep-control and sleep-deprivation groups (mean: 0.62 [s.d.±0.75] and 1.07 [s.d.±2.26], respectively, two-sample t-test, t(25) = 0.89, P = 0.38).”
    Quote in the paperNot a substantial claim
  • Probably not a substantial claim: may not pass S2 (checkable), S3 (load-bearing).

    Premisecitation

    Optimal evaluation and interpretation of pleasurable, rewarding experiences allows for the development of actions and decisions towards fitness-enhancing outcomes.

    “Optimal evaluation and interpretation of pleasurable, rewarding experiences allows for the development of actions and decisions towards fitness-enhancing outcomes”
    Quote in the paperNot a substantial claim0 of 3 sources checked
    • cites Berridge and Robinson, 2003

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    • cites Schultz, 2006

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    • cites Knutson and Wimmer, 2007

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  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Study design and conductown data

    Participants in the sleep-control group obtained a mean of 7.7 hr of sleep the night prior to the fMRI session, as measured using actigraphy.

    “Participants in the sleep-control group obtained a mean of 7.7 hr (s.d.±1.23) of sleep the night prior to the fMRI session, as measured using actigraphy.”
    Quote in the paperNot a substantial claim
  • May combine two claims.

    Premisecitation

    Chronic sleep restriction increases mood disturbance and escalates complaints of emotional difficulties.

    “Chronic sleep restriction has been shown to increase mood disturbance and escalate complaints of emotional difficulties (Dinges et al., 1997; Zohar et al., 2005).”
    Quote in the paperNot a substantial claim0 of 2 sources checked
    • cites Dinges et al., 1997

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    • cites Zohar et al., 2005 source

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  • Classified as probably not a substantial claim.

    Study design and conductown data

    Subjects in the sleep-deprivation group accumulated a mean of 31.9 hr total sleep deprivation prior to the scanning session.

    “Subjects in the deprivation group were continuously monitored in the laboratory throughout the enforced waking period by trained personnel, independently confirmed using actigraphy monitoring, accumulating a mean of 31.9 hr (s.d.±1.31) total sleep deprivation prior to the scanning session.”
    Quote in the paperSubstantial claim
  • May combine two claims.

    Premisecitation

    Acute sleep deprivation significantly amplifies amygdala reactivity in response to negative emotional stimuli, associated with a loss of medial prefrontal cortex (mPFC) connectivity.

    “Moreover, acute sleep deprivation significantly amplifies amygdala reactivity in response to negative emotional stimuli, associated with a loss of medial prefrontal cortex (mPFC) connectivity (Yoo et al., 2007b).”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Yoo et al., 2007b

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  • May combine two claims.

    Premisecitation

    The beneficial mood-elevating effect of sleep deprivation is paralleled by reports of emotional lability in healthy adults under conditions of sleep loss, commonly describing episodes of inappropriate euphoria and giddiness, and oscillating periods of lopsided positive emotional reactivity.

    “Interestingly, this beneficial mood-elevating effect is paralleled by reports of emotional lability in healthy adults under conditions of sleep loss, commonly describing episodes of inappropriate euphoria and giddiness, and oscillating periods of lopsided positive emotional reactivity (Bliss et al., 1959; Horne, 1993; Dahl, 1996).”
    Quote in the paperNot a substantial claim0 of 3 sources checked
    • cites Bliss et al., 1959 source

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    • cites Horne, 1993

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    • cites Dahl, 1996

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    Premisecitation

    The antidepressant benefit of sleep deprivation is rapidly reversed following recovery sleep, implying a transient functional basis for the short-term clinical improvement.

    “Unfortunately, the antidepressant benefit of sleep deprivation is rapidly reversed following recovery sleep, implying a transient (functional) basis for the short-term clinical improvement (Wirz-Justice and Van den Hoofdakker, 1999).”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Wirz-Justice and Van den Hoofdakker, 1999

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  • May combine two claims.

    Interpretationown data

    Sleep deprivation is not only associated with enhanced reactivity towards negative stimuli, but imposes a bi-directional nature of affective imbalance, associated with amplified reward-relevant reactivity towards pleasure-evoking stimuli also.

    “Together, these data support a view that sleep deprivation is not only associated with enhanced reactivity towards negative stimuli, but imposes a bi-directional nature of affective imbalance, associated with amplified reward-relevant reactivity towards pleasure-evoking stimuli also.”
    Quote in the paperSubstantial claim
    • Rests on an assumption: 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.
    • Rests on an assumption: The positive bias score validly indexes biased appraisal of positive emotional experiences.
  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

    Study design and conductown data

    On the night prior to deprivation, participants in the sleep-deprivation group obtained a mean of 7.4 hr of sleep, not significantly different to that of the control group (7.1 hr).

    “On the night prior to deprivation, participants in the sleep-deprivation group obtained a mean of 7.4 hr (s.d.±0.98) of sleep, not significantly different to that of the control group (7.1 hr; s.d.±1.11: t (25) = 0.75, P = 0.46).”
    Quote in the paperNot a substantial claim
  • May combine two claims.

    Interpretationcitation

    A lack of appropriate engagement of limbic-related PFC regions may contribute to altered positive emotional sensitivity and regulatory control under conditions of sleep loss, with cognition being driven more by subcortical affective circuits.

    “A lack of appropriate engagement of these limbic-related PFC regions may therefore contribute to altered positive emotional sensitivity and regulatory control under conditions of sleep loss, with cognition being driven more by subcortical affective circuits (Killgore et al., 2006; Killgore et al., 2007; Venkatraman et al., 2007).”
    Quote in the paperSubstantial claim0 of 3 sources checked
    • cites Killgore et al., 2006

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    • cites Killgore et al., 2007 source

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    • cites Venkatraman et al., 2007 source

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    Interpretationreasoning

    The lack of correlation between the positive bias score and reward-related areas in the sleep-control group may be related to the limited degree of positive bias expressed by these participants.

    “The lack of correlation between the positive bias score and reward-related areas in the sleep-control group may be related to the limited degree of positive bias expressed by these participants.”
    Quote in the paperNot a substantial claim
  • May combine two claims.

    Interpretationcitation

    Changes in OFC connectivity were selectively identified in the current study using positive valence stimuli, and not evident in previous work using negative valence stimuli.

    “However, this seems not to be the case for changes in OFC connectivity, which was selectively identified in the current study using positive valence stimuli, and not evident in previous work using negative valence stimuli (Yoo et al., 2007b).”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites Yoo et al., 2007b

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  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Interpretationreasoning

    The increased putamen activation identified in the deprivation group may reflect a stronger mapping to, or learned association with, the positive stimulus response choices.

    “Therefore, beyond necessarily coding reward value, which more ventral aspects of the striatum may represent (Knutson and Wimmer, 2007), the increased putamen activation identified in the deprivation group may reflect a stronger mapping to, or learned association with, the positive stimulus response choices.”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Knutson and Wimmer, 2007

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  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

    Premisecitation

    The striatum (including the caudate, nucleus accumbens and putamen) has consistently been implicated in motivation and emotion regulation, and can respond in a scaled, parametric way to increasing positive-reward valence.

    “The striatum (including the caudate, nucleus accumbens and putamen), has consistently been implicated in motivation and emotion regulation (Knutson and Cooper, 2005; Schultz, 2006), and can respond in a scaled, parametric way to increasing positive-reward valence (Knutson et al., 2000; Knutson et al., 2001; Delgado et al., 2003).”
    Quote in the paperNot a substantial claim0 of 3 sources checked
    • cites Knutson and Cooper, 2005

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    • cites Schultz, 2006

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    • cites Knutson et al., 2000

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  • May combine two claims.

    Interpretationcitation

    The increases in connectivity between reward-associated networks and early sensory perceptual regions may enhance attention to features of the emotional objects, further increasing their perceived salience.

    “Moreover, and in combination with the group-level differences identified in the fusiform gyrus, the increases in connectivity between these reward-associated networks and early sensory perceptual regions may enhance attention to features of the emotional objects, further increasing their perceived salience (Rolls and Grabenhorst, 2008).”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites Rolls and Grabenhorst, 2008

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  • May combine two claims.

    Interpretationcitation

    Such a notion would support the concept of PFC sensitivity to, and hence dis-inhibition induced by, a lack of sleep.

    “Such a notion would support the concept of PFC sensitivity to, and hence dis-inhibition induced by, a lack of sleep (Harrison et al., 2000; Yoo et al., 2007b).”
    Quote in the paperNot a substantial claim0 of 2 sources checked
    • cites Harrison et al., 2000 source

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    • cites Yoo et al., 2007b

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  • May combine two claims.

    Interpretationown data

    Our findings further support the hypothesis that sleep loss is not exclusively associated with enhanced emotional brain reactivity towards threat-relevant negative stimuli, but also appears to impose a labile, bi-directional nature of affective imbalance, including increased neural and behavioral reactivity to positive experiences.

    “Our findings further support the hypothesis that sleep loss is not exclusively associated with enhanced emotional brain reactivity towards threat-relevant negative stimuli (Yoo et al., 2007b; Franzen et al., 2009), but also appears to impose a labile, bi-directional nature of affective imbalance, including increased neural and behavioral reactivity to positive experiences.”
    Quote in the paperSubstantial claim0 of 2 sources checked
    • cites Yoo et al., 2007b

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    • cites Franzen et al., 2009

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    Premisecitation

    The putamen has previously been linked to action-oriented components of reward-driven behavior that are stimulus relevant (rather than automated/habitual).

    “The putamen, situated in the dorsal striatum, has previously been linked to action-oriented components of reward-driven behavior that are stimulus relevant (rather than automated/habitual) (Balleine et al., 2007).”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites Balleine et al., 2007

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  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

    Premisecitation

    Both the amygdala and the insular cortex can preferentially respond to emotional salience, playing a role not only in registering negative valence, but also in reactivity towards, and coding of, positive stimuli.

    “Both the amygdala and the insular cortex can preferentially respond to emotional salience, playing a role not only in registering negative valence, but also in reactivity towards, and coding of, positive stimuli (Berridge and Robinson, 2003; Murray, 2007).”
    Quote in the paperNot a substantial claim0 of 2 sources checked
    • cites Berridge and Robinson, 2003

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    • cites Murray, 2007

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  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    This collection of limbic regions, together with the VTA and striatum, has been proposed as a broad network supporting motivation and reward processing.

    “Indeed, this collection of limbic regions, together with the VTA and striatum, has been proposed as a broad network supporting motivation and reward processing (Camara et al., 2009).”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Camara et al., 2009

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    The anterior temporal pole is a region previously implicated in positive emotion processing.

    “the anterior temporal pole (the latter also a region previously implicated in positive emotion processing [Pelletier et al., 2003])”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Pelletier et al., 2003

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

    Premisecitation

    Striatal regions receive dopaminergic projections from the midbrain VTA, and the modulatory effects of these projections are believed to be important in regulating the brain's response to positive rewards by aiding information integration within the striatum.

    “Striatal regions receive dopaminergic projections from the midbrain ventral tegmental area (VTA), the modulatory effects of which are believed to be important in regulating the brain's response to positive rewards by aiding information integration within the striatum (Knutson and Cooper, 2005; Schultz, 2006).”
    Quote in the paperNot a substantial claim0 of 2 sources checked
    • cites Knutson and Cooper, 2005

      Not checked in the free run.

    • cites Schultz, 2006

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    The VTA is a structure that can scale in response magnitude with increasing reward value.

    “This increase in reactivity of the VTA—a structure that can also scale in response magnitude with increasing reward value (Fields et al., 2007)–may offer a putative mechanism underlying the increase in the biased number of positive stimulus judgments observed in the deprivation group.”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Fields et al., 2007

      Not checked in the free run.

  • Classified as probably not a substantial claim. May combine two claims.

    Premisecitation

    OFC as well as mPFC regions can aid in coding and representing parameters of value and risk during positive, rewarding experiences.

    “More generally, this paucity of connectivity is of potential relevance considering that OFC as well as mPFC regions can aid in coding and representing parameters of value and risk during positive, rewarding experiences (Wallis, 2007; Rolls and Grabenhorst, 2008).”
    Quote in the paperSubstantial claim0 of 2 sources checked
    • cites Wallis, 2007

      Not checked in the free run.

    • cites Rolls and Grabenhorst, 2008

      Not checked in the free run.

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

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

  • The beneficial effect of sleep deprivation on mood is linked with emotional lability and inappropriate emotional reactivity in healthy adults under sleep deprivation.

    “On the other hand, sleep loss is also related to a compromised consolidation of negative emotional memories (Sterpenich et al., 2007), and this beneficial effect on the mood is linked with emotional lability and inappropriate emotional reactivity in healthy adults under sleep deprivation (Horne, 1988; Dahl, 1996; Gujar et al., 2011).”

    From The Functional Role of Dreaming in Emotional Processes (2019) · cites this paper as Gujar et al., 2011

  • Sleep deprivation disrupts reward neural circuitry, usually enhancing brain reactivity to positive experiences.

    “Sleep deprivation also disrupts reward neural circuitry, usually enhancing brain reactivity to positive experiences.”
  • Sleep deprivation in adults impacts brain function related to reward processing, risk-taking, and cognition.

    “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)”
  • Functional connectivity analyses in adults reveal that poor sleep impairs brain function in affective and cognitive control regions and disrupts cross-talk between these neural networks.

    “Indeed, functional connectivity analyses in adults reveal that poor sleep not only impairs brain function in affective and cognitive control regions but also disrupts cross-talk between these neural networks (Gujar et al., 2011; Venkatraman et al., 2011; Yoo et al., 2007).”
  • Sleep deprived adults show hyperactivation in the insula when processing positive stimuli.

    “During risk taking, adolescents who reported poorer sleep quality showed greater activation in the insula during cash out trials as the reward increased, findings that are consistent with research on sleep deprived adults who show hyperactivation in the insula when processing positive stimuli (Gujar et al., 2011).”

Statistics that don’t add up

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

  • Inconsistent p-value: t (25) = 0.66, p = .43

    Minor

    The paper reports p = .43 here; recomputing from the test statistic and its degrees of freedom gives p = .515 (two-tailed). The check cannot tell whether the statistic or the p-value is the misprint.

    Reported p = .43 · recomputed p = .515

  • Inconsistent p-value: F(1, 25) = 4.09, p = .04

    Minor

    The paper reports p = .04 here; recomputing from the test statistic and its degrees of freedom gives p = .054. The check cannot tell whether the statistic or the p-value is the misprint.

    Reported p = .04 · recomputed p = .054

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”

8 of 8

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.

  • Abstract says the bias correlated exclusively with mesolimbic activity

    Minor

    The abstract calls the correlation exclusive to mesolimbic regions, but the results also identify a correlation in the left fusiform gyrus, which the paper describes as a visual-processing region.

1 of 1

Cites

Flagged first, then by citations

1 of the 76 references couldn’t be matched to a known paper.

Cited by

Sorted by citations

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

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Claims read by deepseek-v4.1-flash under definition version 3 (extract-v3) on 2026-10-10.

Classified by jev-1.13-20260917 (gold-guideline-v0.2) on 2026-10-10.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

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