Cited by 509Sleep and Work-Related FatigueSleep and Wakefulness ResearchNeural and Behavioral Psychology Studies

Functional Imaging of Working Memory after 24 Hr of Total Sleep Deprivation

Open access
Chee, Michael W. L., Choo, Wei Chieh·2004·The Journal of Neuroscience

Abstract

The neurobehavioral effects of 24 hr of total sleep deprivation (SD) on working memory in young healthy adults was studied using functional magnetic resonance imaging. Two tasks, one testing maintenance and the other manipulation and maintenance, were used. After SD, response times for both tasks were significantly slower. Performance was better preserved in the more complex task. Both tasks activated a bilateral, left hemisphere-dominant frontal-parietal network of brain regions reflecting the engagement of verbal working memory. In both states, manipulation elicited more extensive and bilateral (L>R) frontal, parietal, and thalamic activation. After SD, there was reduced blood oxygenation level-dependent signal response in the medial parietal region with both tasks. Reduced deactivation of the anterior medial frontal and posterior cingulate regions was observed with both tasks. Finally, there was disproportionately greater activation of the left dorsolateral prefrontal cortex and bilateral thalamus when manipulation was required. This pattern of changes in activation and deactivation bears similarity to that observed when healthy elderly adults perform similar tasks. Our data suggest that reduced activation and reduced deactivation could underlie cognitive impairment after SD and that increased prefrontal and thalamic activation may represent compensatory adaptations. The additional left frontal activation elicited after SD is postulated to be task dependent and contingent on task complexity. Our findings provide neural correlates to explain why task performance in relatively more complex tasks is better preserved relative to simpler ones after SD.

AI snapshot

Written from the paper’s full text.

TL;DR

After 24 hr of total sleep deprivation, healthy young adults showed slower working-memory response times and reduced medial parietal activation, alongside reduced deactivation in anterior medial frontal and posterior cingulate regions. More complex manipulation recruited disproportionately greater left dorsolateral prefrontal and bilateral thalamic activation after sleep deprivation, which the authors interpret as possible compensation.

Key findings

  • Sleep deprivation increased subjective sleepiness (ESS, 4.1 ± 4.1 to 17.1 ± 4.0; p < 0.001) and slowed response times for both maintenance (LTR: 825 ± 80 to 883 ± 110 msec; p < 0.05) and manipulation-plus-maintenance (PLUS: 786 ± 119 to 860 ± 144 msec; p < 0.05).
  • Accuracy declined after sleep deprivation for LTR (0.959 ± 0.049 to 0.902 ± 0.097; p < 0.05) but not for PLUS (0.957 ± 0.055 to 0.926 ± 0.086), and omitted responses increased for LTR (0.2 ± 0.5% to 4.0 ± 6.3%; p < 0.05) but not PLUS.
  • Both tasks activated a bilateral, left-hemisphere-dominant frontal-parietal network; manipulation elicited more extensive bilateral frontal, parietal, and thalamic activation than maintenance in both states.
  • After sleep deprivation, both tasks showed reduced BOLD signal in medial parietal/precuneus regions and reduced deactivation in anterior medial frontal and posterior cingulate regions; manipulation after sleep deprivation produced disproportionately greater left dorsolateral prefrontal and bilateral thalamic activation.

Methods

  • Fourteen right-handed healthy undergraduate volunteers (five women; mean age 23 years; range 19–24) were scanned twice, once during rested wakefulness and once after 24 hr of total sleep deprivation, with sessions 1 week apart and order counterbalanced.
  • Two verbal working-memory tasks were used: LTR tested maintenance, and PLUS tested manipulation plus maintenance; each had a matched perceptual-motor control condition.
  • fMRI data were acquired on a 3T scanner and analyzed with a general linear model, random-effects whole-brain voxel-by-voxel contrasts, and region-of-interest analyses; whole-brain contrasts used p < 0.005 uncorrected with a nine-contiguous-voxel cluster threshold. One subject’s in-scanner data were lost because of a technical error.

Limitations

  • The paper does not include a formal limitations section; it states that short-term total sleep deprivation is artificial and that the experiments were relatively short because the benefit of task complexity is often temporary.
  • Evident from the text: the sample was small (14 participants, with one subject’s in-scanner data lost), limited to young healthy right-handed undergraduates, and the sleep-deprivation manipulation was acute rather than chronic.
  • Evident from the text: some whole-brain state-by-task interaction findings were reported at a less stringent threshold of p < 0.005 uncorrected, although the left dorsolateral prefrontal interaction was confirmed with ROI analysis (F(1,12) = 17.4; p < 0.001).

Model-written summary. Check it against the paper before relying on it.

Integrity signals

Registry

Crossref · 10.1523/jneurosci.0007-04.2004

Cites

57 of 57 references verified0 citation errors · 0 not checkable

Statistics

Nothing to recompute.

Claims the paper makes

0 of 66 cited sources checked · 0 supported · 0 flagged

  • Findingown data

    Subjects reported a greater subjective sense of sleepiness after sleep deprivation, reflected by an increase in ESS (t(13)=9.4; p<0.001).

    “Subjects reported a greater subjective sense of sleepiness after SD, reflected by the increase in ESS (t (13) ϭ 9.4; p Ͻ 0.001) (Table 1).”
    Quote in the paperNot a substantial claim
  • Findingown data

    After sleep deprivation, there was reduced BOLD signal response in the medial parietal region with both tasks.

    “After SD, there was reduced blood oxygenation level-dependent signal response in the medial parietal region with both tasks.”
    • Also stated in: § Activation after SD in comparison with RW · plain
      “Voxel-by-voxel analysis showed that after SD, both LTR and PLUS elicited a smaller task-related BOLD signal in the parietal region (bilateral BA 7; inclusive of the precuneus) than during RW (Fig. 4).”
    Quote in the paperSubstantial claim
    • Rests on an assumption: BOLD signal changes reflect neural activity.
  • Findingown data

    There was no difference in mean reaction times during the simple reaction time task across states.

    “The variability of RTs during SRT was greater after SD (t (13) ϭ 2.2; p Ͻ 0.05), although there was no difference in mean RTs across states.”
    Quote in the paperNot a substantial claim
  • Findingown data

    Both working memory tasks activated a bilateral, left hemisphere-dominant frontal-parietal network of brain regions.

    “Both tasks activated a bilateral, left hemisphere-dominant frontal-parietal network of brain regions reflecting the engagement of verbal working memory.”
    Quote in the paperNot a substantial claim
    • Rests on an assumption: BOLD signal changes reflect neural activity.
  • Findingown data

    During rested wakefulness, LTR elicited bilateral, left hemisphere-dominant activation in the prefrontal (BA 9/46) and precentral (BA 6) regions, insula (BA 13), and thalamus.

    “During RW, LTR elicited bilateral, left hemisphere-dominant activation in the prefrontal [Brodmann's area (BA) 9/46] and precentral (BA 6) regions, insula (BA 13), and thalamus (Fig. 2.).”
    Quote in the paperSubstantial claim
    • Rests on an assumption: BOLD signal changes reflect neural activity.
  • May combine two claims. 16
  • Classified as probably not a substantial claim. 18
  • May combine two claims.

    Findingown data

    ROI analysis of activation in the thalamus showed main effects of state (F(1,13)=6.8; p<0.05) and task (F(1,13)=11.6; p<0.005).

    “ROI analysis of activation in the thalamus showed main effects of state (F (1,13) ϭ 6.8; p Ͻ 0.05) and task (F (1,13) ϭ 11.6; p Ͻ 0.005).”
    Quote in the paperNot a substantial claim
    • Rests on an assumption: BOLD signal changes reflect neural activity.
  • May combine two claims.

    Findingown data

    The present study showed that after sleep deprivation, increased as well as decreased cortical activation and decreased deactivation occurred relative to activation elicited during rested wakefulness.

    “The present study showed that after SD, increased as well as decreased cortical activation and decreased deactivation occurred relative to activation elicited during RW.”
    Quote in the paperSubstantial claim
    • Rests on an assumption: BOLD signal changes reflect neural activity.
  • May combine two claims.

    Findingown data

    There was a trend suggestive of a state-by-task interaction in the thalamus, but it did not reach statistical significance (F(1,13)=2.3; p<0.15).

    “Although there was a trend suggestive of a state-by-task interaction, this did not reach statistical significance (F (1,13) ϭ 2.3; p Ͻ 0.15) (Fig. 6).”
    Quote in the paperNot a substantial claim
    • Rests on an assumption: BOLD signal changes reflect neural activity.
  • May combine two claims.

    Findingown data

    Neither the anterior medial frontal nor the posterior cingulate region showed a significant state-by-task interaction.

    “Neither of these areas showed a significant state-by-task interaction.”
    Quote in the paperNot a substantial claim
    • Rests on an assumption: BOLD signal changes reflect neural activity.
  • May combine two claims.

    Findingown data

    ROI analysis based on individual subject data showed a significant state-by-task interaction (F(1,12)=17.4; p<0.001) in the left dorsolateral prefrontal cortex, in addition to main effects of state (F(1,12)=6.6; p<0.05) and task (F(1,12)=38.0; p<0.001).

    “To confirm that these results were not spurious, the results of the ROI analysis based on the individual subject's data showed significant state-by-task interaction (F (1,12) ϭ 17.4; p Ͻ 0.001) in addition to main effects of state (F (1,12) ϭ 6.6; p Ͻ 0.05) and task (F (1,12) ϭ 38.0; p Ͻ 0.001) (Fig. 5).”
    Quote in the paperSubstantial claim
    • Rests on an assumption: BOLD signal changes reflect neural activity.
  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Study design and conductnone given

    The order of scanning was counterbalanced across subjects to reduce the potential influence of practice, learning, and order effects on cortical activation.

    “The order of scanning was counterbalanced across subjects to reduce the potential influence of practice, learning, and order effects on cortical activation.”
    Quote in the paperNot a substantial claim
  • Classified as probably not a substantial claim.

    Premisecitation

    The benefit of task complexity is often temporary.

    “The experiments were relatively short because the benefit of task complexity is often temporary.”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites Wilkinson, 1965

      Not checked in the free run.

  • Classified as probably not a substantial claim.

    Study design and conductnone given

    The control condition was designed to match for perceptual and motor responses.

    “The control condition was designed to match for perceptual and motor responses.”
    Quote in the paperSubstantial claim
  • Classified as probably not a substantial claim.

    Study design and conductcitation

    The two scanning sessions were conducted 1 week apart to minimize the possibility of residual effects of sleep deprivation affecting cognition.

    “The two scanning sessions were conducted 1 week apart to minimize the possibility of residual effects of SD affecting cognition of volunteers who underwent a SD scan before a RW scan (Van Dongen et al., 2003).”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites Van Dongen 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

    Subjective difficulty may have been excluded as a potential source of divergent imaging results, but this assertion has not been tested explicitly.

    “Subjective difficulty may have been excluded as a potential source of divergent imaging results (Drummond and Brown, 2001), but this assertion has not been tested explicitly.”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Drummond and Brown, 2001

      Not checked in the free run.

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

    Premisecitation

    Even within a particular cognitive domain, frontal activation may increase with task difficulty up to a point and then decrease.

    “Even within a particular cognitive domain, frontal activation may increase with task difficulty up to a point and then decrease (Callicott et al., 1999), reflecting an overwhelming of processing capacity, a loss of motivation (Jaeggi et al., 2003), or both.”
    Quote in the paperNot a substantial claim0 of 2 sources checked
    • cites Callicott et al., 1999

      Not checked in the free run.

    • cites Jaeggi et al., 2003

      Not checked in the free run.

  • May combine two claims.

    Interpretationown data

    The additional left frontal activation elicited after sleep deprivation is task dependent and contingent on task complexity.

    “The additional left frontal activation elicited after SD is postulated to be task dependent and contingent on task complexity.”
    Quote in the paperSubstantial claim
    • Rests on an assumption: BOLD signal changes reflect neural activity.
  • Probably not a substantial claim: may not pass S2 (checkable), S4 (based).

    Interpretationnone given

    Short-term total sleep deprivation, although artificial, affords better experimental control.

    “Short-term total SD, although artificial (chronic SD is more common and has greater general relevance), affords better experimental control.”
    Quote in the paperNot a substantial claim
  • Classified as probably not a substantial claim.

    Study design and conductreasoning

    To verify that the task-by-state interaction observed in the left prefrontal region at p < 0.005 was not spurious, a functional ROI analysis of individual subject activation in the left dorsolateral prefrontal cortex was performed.

    “To verify that the task by state interaction observed in the left prefrontal region at a slightly lenient threshold of p Ͻ 0.005 was not spurious, we performed a functional ROI analysis of activation in this region by obtaining parameter estimates of the individual subject's activation within the region of the left dorsolateral prefrontal cortex (corresponding to the middle frontal gyrus).”
    Quote in the paperSubstantial claim
  • May combine two claims.

    Premisecitation

    Frontal and parietal activation after sleep deprivation has been shown to increase in experiments involving verbal learning, decrease in experiments involving serial subtraction, or show no change in an experiment testing attention.

    “For example, frontal and parietal activation after SD has been shown to increase in experiments involving verbal learning (Drummond et al., 2000(Drummond et al., , 2001)), decrease in experiments involving serial subtraction (Drummond et al., 1999;Thomas et al., 2000), or show no change in an experiment testing attention (Portas et al., 1998).”
    Quote in the paperSubstantial claim0 of 3 sources checked
    • cites Drummond et al., 2000

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    • cites Drummond et al., 1999

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    • cites Portas et al., 1998

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

    Premisecitation

    Thalamic activation is modulated by an increase in sustained attention.

    “Thalamic activation is also modulated by an increase in sustained attention (Kinomura et al., 1996;Coull, 1998), and it is conceivable that either or both these mechanisms could contribute to the task-related difference in thalamic activation observed here.”
    Quote in the paperNot a substantial claim0 of 2 sources checked
    • cites Kinomura et al., 1996

      Not checked in the free run.

    • cites Coull, 1998

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  • May combine two claims.

    Interpretationcitation

    The present findings are consistent with the notion that these regions are disengaged during performance of cognitive tasks and that magnitude of deactivation may increase with processing demands.

    “The present findings are consistent with the notion that these regions are disengaged during the performance of cognitive tasks and that the magnitude of deactivation may increase in accordance with processing demands (McKiernan et al., 2003).”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites McKiernan et al., 2003

      Not checked in the free run.

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

    Premisecitation

    Prior working-memory experiments have demonstrated thalamic activation in association with increased working memory demand.

    “Prior working-memory experiments have demonstrated thalamic activation in association with increased working memory demand (Barch et al., 1997;Callicott et al., 1999;Manoach et al., 2003).”
    Quote in the paperNot a substantial claim0 of 3 sources checked
    • cites Barch et al., 1997

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    • cites Callicott et al., 1999

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    • cites Manoach et al., 2003

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    This parietal region has been activated in several previous experiments examining working memory and may be involved in retrieval operations specific to working memory.

    “This region has been activated in several previous experiments examining working memory (Schumacher et al., 1996;Cabeza et al., 2002) and may be involved in retrieval operations specific to working memory (Cabeza et al., 2002).”
    Quote in the paperSubstantial claim0 of 2 sources checked
    • cites Schumacher et al., 1996

      Not checked in the free run.

    • cites Cabeza et al., 2002

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  • Classified as probably not a substantial claim.

    Premisecitation

    Healthy volunteers with a higher memory span showed greater activation in this region relative to those with a lower memory span.

    “Healthy volunteers with a higher memory span showed greater activation in this region relative to those with a lower memory span (Mecklinger et al., 2003).”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites Mecklinger et al., 2003

      Not checked in the free run.

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

    Interpretationcitation

    Under different contexts, increases in task-related regional cortical activation may relate to more or less efficient processing.

    “In using this framework, we are cognizant that, under different contexts, increases in task-related regional cortical activation may relate to more (Gray et al., 2003;Mecklinger et al., 2003) or less (Reuter-Lorenz, 2002;Cabeza et al., 2004) efficient processing.”
    Quote in the paperNot a substantial claim0 of 3 sources checked
    • cites Gray et al., 2003

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    • cites Mecklinger et al., 2003

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    • cites Reuter-Lorenz, 2002

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  • May combine two claims.

    Premisecitation

    In tasks that the elderly can perform, frontal activation is often increased and frequently bilateral.

    “In tasks that the elderly can perform (Grady et al., 1994;Esposito et al., 1999;Madden et al., 1999;Rypma and D'Esposito, 2000;Cabeza et al., 2004), frontal activation is often increased and frequently bilateral.”
    Quote in the paperSubstantial claim0 of 3 sources checked
    • cites Grady et al., 1994

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    • cites Esposito et al., 1999

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    • cites Cabeza et al., 2004

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

    Premisecitation

    Such reduction in occipital activation has been observed in at least three previous studies.

    “However, such reduction in occipital activation has been observed (but not highlighted) in at least three previous studies (Drummond et al., 1999(Drummond et al., , 2001;;Habeck et al., 2004).”
    Quote in the paperNot a substantial claim0 of 3 sources checked
    • cites Drummond et al., 1999

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    • cites Drummond et al., 2001

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    • cites Habeck et al., 2004

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

    Premisecitation

    A relative reduction of occipital lobe activation has been observed in the elderly, and this finding appears to be task independent.

    “A relative reduction of occipital lobe activation (Grady et al., 1994;Madden et al., 1996;Cabeza et al., 1997) has been observed in the elderly, and this finding appears to be task independent (Cabeza et al., 2004).”
    Quote in the paperNot a substantial claim0 of 3 sources checked
    • cites Grady et al., 1994

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    • cites Madden et al., 1996

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    • cites Cabeza et al., 2004

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

    Premisecitation

    This framework of interpreting functional imaging results has been applied to studies on healthy aging.

    “This framework of interpreting functional imaging results has been applied to studies on healthy aging (Reuter-Lorenz, 2002;Cabeza et al., 2004).”
    Quote in the paperNot a substantial claim0 of 2 sources checked
    • cites Reuter-Lorenz, 2002

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    • cites Cabeza et al., 2004

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

    Interpretationcitation

    The engagement of compensatory neural responses may be contingent on the use of specific mental operations or strategies.

    “This suggests that the engagement of compensatory neural responses may be contingent on the use of specific mental operations or strategies.”
    Quote in the paperNot a substantial claim
  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

    Premisecitation

    When encoding words without specific instruction, elderly volunteers exhibited reduced frontal activation and poor memory retrieval.

    “An informative illustration: when encoding words without specific instruction, elderly volunteers exhibited reduced frontal activation and poor memory retrieval.”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Logan et al., 2002

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    Both SD and healthy aging result in a decline in working memory.

    “Both SD and healthy aging result in a decline in working memory (Harrison et al., 2000).”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites Harrison et al., 2000

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  • May combine two claims.

    Interpretationreasoning

    The three types of activity modulation observed in young SD individuals have parallels in healthy elderly adults, suggesting common mechanisms may underlie cognitive decline in both conditions.

    “In addition, the three types of activity modulation observed in young SD individuals have parallels in healthy elderly adults, speaking to the possibility that common mechanisms may underlie cognitive decline in both conditions”
    Quote in the paperNot a substantial claim
  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

    Premisecitation

    When provided with environmental support to facilitate encoding, elderly volunteers showed a nonselective (bilateral) increase in frontal activation and improved mnemonic performance relative to younger counterparts.

    “However, when provided with environmental support to facilitate encoding, the elderly volunteers showed a nonselective (bilateral) increase in frontal activation and correspondingly improved mnemonic performance relative to their younger counterparts (Logan et al., 2002).”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Logan et al., 2002

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30 of 30
  • The paper relies on this without support.

    BOLD signal changes reflect neural activity.

    “The time course of the blood oxygenation leveldependent (BOLD) response in each activated or deactivated region was inspected manually to verify the classification of activity change.”
  • The paper relies on this without support.

    The sample of 14 healthy young adults is representative of the broader population of healthy young adults.

    “Fourteen right-handed, healthy undergraduate volunteers (five women; mean age, 23 years; range, 19 -24) participated in the study after giving informed consent.”
  • The paper relies on this without support.

    BOLD signal is comparable across subjects and scanning sessions after normalization.

    “Mean intensity normalization was performed to obtain the same average intensity for each slice across scans.”
3 of 3

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?

  • Sleep deprivation resulted in longer response times on both simple and complex working memory tasks, but performance was only reduced on the simple working memory task; performance on the complex task remained intact due to greater compensation by prefrontal and thalamic brain regions.

    “One neuroimaging study revealed that, although sleep deprivation resulted in longer response times on both simple and complex tasks of working memory, performance was only reduced on the simple working memory task; performance on the complex task remained intact following sleep deprivation due to greater compensation by the prefrontal and thalamic brain regions (Chee and Choo 2004).”

Cites

Flagged first, then by citations

Research works printed but not linked: 3

  1. 1999, Sleep Res Online, 2, 65
  2. Craik FIM (1986) A functional account of age differences in memory. In: Human memory and cognitive capabilities, mechanisms and performances (Klix F, Hagendorf H, eds), pp 409-422: Amsterdam: Elsevier.
  3. 2000, Sleep, 23, 1067

Cited by

Sorted by citations

Authors
Chee, M. W. L., & Choo, W. C.
Affiliations
SingHealth (SG)
Venue
The Journal of Neuroscience
Published
2004-05-12
Volume
24
Issue
19
Pages
4560-4567
ISSN
  • 0270-6474 (ISSN-L)
  • 1529-2401
OpenAlex
W2110930020
Cited by
509
References
57
Citations by year
2026: 7 · 2025: 12 · 2024: 14 · 2023: 20 · 2022: 21 · 2021: 27 · 2020: 19 · 2019: 39 · 2018: 24 · 2017: 30 · 2016: 19 · 2015: 26 · 2014: 21 · 2013: 33 · 2012: 28
FWCI
25.52
Type
journal article
Language
en
Open access
Locations
  • Journal of Neuroscience (publishedVersion, cc-by-nc-sa)
  • PubMed Central (publishedVersion)
  • PubMed (publishedVersion)
Funders
  • Medical Research Council
  • National Medical Research Council
  • Biomedical Research Council
Topics
  • Social Sciences › Psychology › Experimental and Cognitive Psychology › Sleep and Work-Related Fatigue
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Sleep and Wakefulness Research
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Neural and Behavioral Psychology Studies
Keywords
total sleep deprivation, working memory, verbal working memory, frontoparietal network, dorsolateral prefrontal cortex, thalamus, task complexity, cognitive impairment, healthy young adults
MeSH terms
Adult, Brain, Brain Mapping, Female, Humans, Magnetic Resonance Imaging, Male, Memory, Short-Term, Parietal Lobe, Reaction Time, Sleep Deprivation, Sleep Stages, Task Performance and Analysis, Thalamus, Wakefulness, Prefrontal Cortex

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