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Research Articles, Behavioral/Cognitive

The Pain of Sleep Loss: A Brain Characterization in Humans

Adam J. Krause, Aric A. Prather, Tor D. Wager, Martin A. Lindquist and Matthew P. Walker
Journal of Neuroscience 20 March 2019, 39 (12) 2291-2300; https://doi.org/10.1523/JNEUROSCI.2408-18.2018
Adam J. Krause
1Center for Human Sleep Science, Department of Psychology, University of California, Berkeley, California 94720-1650,
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Aric A. Prather
2Department of Psychiatry, University of California, San Francisco, California 94103,
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Tor D. Wager
3Department of Psychology and Neuroscience, University of Colorado, Boulder, Colorado 80302,
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Martin A. Lindquist
4Department of Biostatistics, Johns Hopkins University, Baltimore, Maryland 21205, and
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Matthew P. Walker
1Center for Human Sleep Science, Department of Psychology, University of California, Berkeley, California 94720-1650,
5Helen Wills Neuroscience Institute, University of California, Berkeley, California 94720-1650
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    Figure 1.

    Experimental design. A, Design of the in-laboratory repeated-measures counterbalanced study involving one night of sleep deprivation and one night of sleep, followed by an fMRI scanning session involving a pain-evoking task. B, Design of the online study involving daily sleep diaries for two consecutive nights tracking habitual variations in sleep time, followed later by daily pain assessment.

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    Figure 2.

    Thermal pain threshold. Following sleep deprivation, there was an increase in pain sensitivity demonstrated by a significant lowering of pain thresholds, relative to sleep-rested. Sleep-deprived mean ± SD = 42.47 ± 3.22°C; Sleep-rested mean ± SD = 43.89 ± 3.49°C. *p < 0.0002.

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    Figure 3.

    Changes in pain-related brain activity. Data are mean ± SD. A–C, Brain maps (left) displaying pain-related ROIs that were significantly altered by sleep deprivation, relative to sleep-rested (all FDR-corrected). Bar plots represent brain activity (Pain > No Pain) contrast estimates. Somatosensory: sleep-deprived mean = 0.09 ± 0.34; sleep-rested mean = −0.34 ± 0.46. NAcc: sleep-deprived mean = 0.02 ± 0.18; sleep-rested mean = 0.19 ± 0.21. Thalamus: sleep-deprived mean = −0.21 ± 0.81; sleep-rested mean = 0.79 ± 1.06. Anterior insula: sleep-deprived mean = 0.12 ± 0.82; sleep-rested mean = 0.79 ± 0.8. Middle insula: sleep-deprived mean = 0.08 ± 0.12; sleep-rested mean = 0.21 ± 0.17. Error bars indicate SEM. *p < 0.005. Nucleus Accumbens (NAcc); Anterior and middle insula (A. Insula and M. Insula, respectively). Threshold for display set to p < 0.005 (whole-brain, uncorrected).

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    Figure 4.

    Pain reactivity and subjective pain sensitivity. Scatterplot represents significant positive correlation between sleep loss-related increases in (A) somatosensory and (B) thalamic pain reactivity (Pain > No Pain), and the sleep loss-related increases in subjective pain sensitivity (change in pain threshold). Threshold for display set to p < 0.005 (whole-brain, uncorrected).

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    Figure 5.

    Online study results. Data are mean ± SD. Bar graph represents participants experiencing a decrease (red bar) or increase (black) in measures of sleep efficiency (SE) (Night 2 to Night 1 mean decreased SE = −3.8 ± 5.6%; Night 2 to Night 1 mean increased SE = 10.1 ± 11.1%), quality (SQ) (Night 2 to Night 1 mean decreased SQ = −0.48 ± 0.75; Night 2 to Night 1 mean increased SQ = 1.7 ± 0.81), and duration (Night 2 to Night 1 mean decreased duration = −54.375 ± 45.7 min; Night 2 to Night 1 mean increased duration = 90.7 ± 48.9 min). Error bars indicate SEM. Each point represents a single-subject's change in reported pain from day 1 to day 2. Night-to-night decreases in sleep efficiency and quality, but not duration, resulted in corresponding higher pain from one day to the next, relative to those with night-to-night increases in these sleep measures. *p < 0.05.

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    Table 1.

    ROI analysisa

    Region (L/R)Radius (mm)xyzpr
    Sleep deprivation > sleep-rested
        Somatosensory (R)b836−45590.0040.55
        Dorsal ACC (R)816−7390.020.04
        Superior parietal (R)526−42660.51−0.04
    Sleep-rested > sleep-deprived
        Middle insula (R)b8324110.0005−0.02
        Thalamus (L)b4−106100.005−0.54
        Anterior insula (L)b8−272500.0050.24
        NAccb6±92−70.0050.23
        Operculum (R)557150.04−0.36
        Substantia nigra (R)410−8120.09−0.31
        Caudate4±18−2240.38−0.32
        IFG (R)46424−60.47−0.47
        Middle cingulate/SMA106−6480.480.01
        Precuneus (R)44−54480.600.32
        ACC (R)61228280.630.36
        DLPFC (R)83335420.900.10
    • ↵aBrain ROI analysis showing radius, MNI coordinates, and p and r values of extracted spheres. r, Pearson correlations between pain-related brain changes (sleep-deprived vs sleep-rested) and changes in thermal pain threshold (sleep-rested vs sleep-deprived). ACC, Anterior cingulate cortex; IFG, inferior frontal gyrus; SMA, supplementary motor area; DLPFC, dorsolateral prefrontal cortex.

    • ↵bSignificant, following FDR correction, for paired comparison (sleep-rested </> sleep-deprived) of pain-related brain activity.

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The Journal of Neuroscience: 39 (12)
Journal of Neuroscience
Vol. 39, Issue 12
20 Mar 2019
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The Pain of Sleep Loss: A Brain Characterization in Humans
Adam J. Krause, Aric A. Prather, Tor D. Wager, Martin A. Lindquist, Matthew P. Walker
Journal of Neuroscience 20 March 2019, 39 (12) 2291-2300; DOI: 10.1523/JNEUROSCI.2408-18.2018

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The Pain of Sleep Loss: A Brain Characterization in Humans
Adam J. Krause, Aric A. Prather, Tor D. Wager, Martin A. Lindquist, Matthew P. Walker
Journal of Neuroscience 20 March 2019, 39 (12) 2291-2300; DOI: 10.1523/JNEUROSCI.2408-18.2018
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Keywords

  • fMRI
  • pain
  • sleep deprivation

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