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Articles, Behavioral/Cognitive

Sleep Deprivation Impairs the Human Central and Peripheral Nervous System Discrimination of Social Threat

Andrea N. Goldstein-Piekarski, Stephanie M. Greer, Jared M. Saletin and Matthew P. Walker
Journal of Neuroscience 15 July 2015, 35 (28) 10135-10145; DOI: https://doi.org/10.1523/JNEUROSCI.5254-14.2015
Andrea N. Goldstein-Piekarski
1Helen Wills Neuroscience Institute and
2Department of Psychology, University of California, Berkeley, California 94720
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  • ORCID record for Andrea N. Goldstein-Piekarski
Stephanie M. Greer
1Helen Wills Neuroscience Institute and
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Jared M. Saletin
2Department of Psychology, University of California, Berkeley, California 94720
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Matthew P. Walker
1Helen Wills Neuroscience Institute and
2Department of Psychology, University of California, Berkeley, California 94720
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  • Figure 1.
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    Figure 1.

    Study design. A, Time course of experiment for both the sleep-deprived and sleep-rested conditions. B, Example of the emotional face stimuli gradient ranging from not threatening to increasingly threatening. C, Schematic for the threat discrimination fMRI task. Each trial lasted an average of 5.75 s. Trials began with a brief fixation screen that was presented using a variable jittered duration time for optimal signal estimation (maximum = 2.3 s, minimum = 1.3 s, mean = 1.8 s; Dale, 1999). After the fixation cross, each trial proceeded with a 1.5 s face stimulus followed by a 2.25 s response period in which participants were asked to classify the prior face as either “threatening” or “not threatening.” Pseudorandomly interspersed between these threat trials were null trial events (data not shown) in which a fixation point was displayed on the screen for a jittered duration (maximum = 5 s, minimum = 1.5 s, mean = 2.5 s), serving as a baseline condition and modulating intertrial interval variability for optimal modeling of trial events.

  • Figure 2.
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    Figure 2.

    Behavioral results. A, Mean proportion of stimuli categorized as either threatening or not threatening in the sleep-rested (SR) and sleep-deprived (SD) conditions. B, Corresponding change in response tendency characterized as a threat discrimination index represented as the subtracted difference in the proportion of not threatening items relative to the portion of threatening items in the SR and SD conditions. A zero value represents equal number of stimuli assigned to threatening and not threatening categories, whereas a positive score represents a greater proportion of stimuli as rated as threatening relative to not threatening. A paired t test demonstrated a significant increase in the proportion of faces rated as threatening in the SD condition compared with the SR condition (t = 2.36, p = 0.03). Error bars indicate SEM. *p < 0.05.

  • Figure 3.
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    Figure 3.

    fMRI results. A, Brain maps displaying the condition: sleep deprivation (SD), sleep-rested (SR) × threat (threatening, not threatening) repeated-measures ANOVA interaction from the voxelwise ROI analysis in the dACC (peak MNI coordinates [x, y, z] = 6, 26, 42) thresholded at FWE p < 0.05 corrected for multiple comparisons. B, Bar graph illustrating the difference in average parameter estimates across the 5 mm dACC ROI sphere mask and the average signal for each condition, respectively. In the sleep-rested condition, there was significantly greater activation across the dACC 5 mm ROI for threatening faces relative to nonthreatening. However, under conditions of sleep deprivation, the dACC reactivity did not differentiate between threatening and nonthreatening faces. C, Threat discrimination index represented as the subtracted difference of the average activity across the dACC 5 mm ROI for not threatening faces subtracted from the activity to threatening faces in the SD and SR conditions. A zero value represents equal activation to threatening and nonthreatening faces, whereas a positive score represents a greater activation to threatening relative to nonthreatening. D, Brain maps displaying the condition × threat repeated-measures ANOVA interaction from the voxelwise ROI analysis in the anterior insula (peak MNI coordinates: left, −38, 20, −8; right, 32, 18, −8. E, F, Equivalent bar graphs as in B and C using the average of 5 mm spheres centered over bilateral anterior insula demonstrating strong threat discrimination ability in the rested condition and impaired threat responding in the deprived condition. Error bars indicate SEM. Within-region statistics: *p < 0.05, **p < 0.01. Correlations between regions of the viscerosensory network discrimination activity are presented independently for the sleep-rested and sleep-deprived condition in Table 4. Tables 2 and 3 display exploratory whole-brain activation differences for the threat × condition interaction, as well as threat reactivity in the sleep-rested session beyond our a priori ROIs.

  • Figure 4.
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    Figure 4.

    Cardiac threat-discrimination results. A, Instantaneous heart rate response to threatening and not threatening face stimuli for sleep-rested (SR) and sleep-deprived (SD) conditions. B, Cardiac threat discrimination index represented as the subtracted difference of the cardiac response to nonthreatening faces subtracted from the cardiac response to threatening faces. A zero value represents equal cardiac responding to threatening and nonthreatening faces, whereas a positive score represents a greater activation to threatening relative to nonthreatening. Error bars indicate SEM. *p < 0.05.

  • Figure 5.
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    Figure 5.

    A, Brain maps displaying the voxelwise ROI regression between the cardiac discrimination index and the sleep-rested dACC discrimination ability (threatening > not threatening contrast; peak MNI coordinates: 10, 22, 44 thresholded at FWE p < 0.05 corrected for multiple comparisons). Scatterplot on far right displays this same relationship using the average parameter estimates across the 5 mm dorsal anterior cingulate ROI mask. Equivalent brain maps and regression plots for the anterior insula (B; peak MNI coordinates: right: 38, 24, −4) and amygdala (C; peak MNI coordinates: 18, 2, −16) ROIs. No significant relationships were found for the left amygdala (r = −0.09, p = 0.75) or the left anterior insula (r = 0.42, p = 0.12).

  • Figure 6.
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    Figure 6.

    A, EEG topographic plot of log-transformed relative gamma activity (30–40 Hz) during REM sleep. B, Brain maps displaying the voxelwise ROI regression between relative REM gamma activity over frontal electrodes and the sleep-rested dACC discrimination ability (threatening > not threatening contrast) (peak MNI coordinates: 4, 22, 40 thresholded at FWE p < 0.05 corrected for multiple comparisons). Scatterplot on far right displays this same relationship using the average parameter estimates across the 5 mm dorsal anterior cingulate ROI mask. Equivalent brain maps and regression plots for the anterior insula (C; peak MNI coordinates: left, −36, 18, −10; right, 40, 22, −4) and amygdala (D; peak MNI coordinates: −20, 0, −14) ROIs.

Tables

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    Table 1.

    Polysomnography sleep-stage values for the sleep rested session (mean ± SD)

    Sleep time (min)% Total sleep timeObtained by % of participants
    Total sleep time469.43 ± 38.7
    Stage 125.72 ± 10.45.53 ± 2.4100%
    Stage 2253.15 ± 34.153.87 ± 5.2100%
    SWS90.35 ± 28.419.41 ± 6.7100%
    REM100.20 ± 24.821.20 ± 4.3100%
    • SWS, NREM stage 3 and 4.

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    Table 2.

    Voxelwise whole-brain results for the sleep-rested condition

    Region (BA)Cluster size (mm3)xyzPeak Z score
    Sleep-rested threatening > not threatening
        Inferior frontal gyrus (BA 47)-L45369−3820−105.95
        Inferior frontal gyrus (BA 47)-L−482005.6
        Middle frontal gyrus (BA 47)-L−5038−44.16
        Inferior frontal gyrus (BA 47)-R294224226−85.21
        Inferior frontal gyrus (BA 47)-R4020−144.87
        Inferior frontal gyrus (BA 47)-R3222−84.85
        Superior frontal gyrus (BA 8)-L33556−624564.84
        Medial frontal gyrus (BA 8)-L−624464.42
        Medial frontal gyrus (BA 9)-L−240324.05
        Lateral globus pallidus-L284−18−2−123.5
        Superior temporal gyrus (BA 22)-R41648−30−23.38
        Middle frontal gyrus (BA 6)-R306420603.37
    Sleep-rested not threatening > threatening
        Medial frontal gyrus (BA 10)-L14788−650−84.72
        Anterior cingulate (BA 32)-R836−103.91
        Medial frontal gyrus (BA 10)-R1252−63.85
        Middle frontal gyrus (BA 9)-R121412624364.66
        Superior frontal gyrus (BA 6)-R2212523.97
        Precuneus (BA 19)-L4878−38−76344.19
        Superior frontal gyrus (BA 8)-L4900−2414543.77
        Middle frontal gyrus (BA 8)-L−2226383.66
        Middle frontal gyrus (BA 8)-L−2222463.55
        Precuneus (BA 7)-R62344−52523.76
        Precuneus (BA 7)-R0−48463.56
        Superior temporal gyrus (BA 22)-L1094−56−6−43.73
        Precentral gyrus (BA 6)-L3063−44−12343.69
        Insula (BA 13)-L−42−14223.5
        Cingulate gyrus (BA 31)-R225314−36403.65
        Subcallosal gyrus (BA 25)-R744620−143.58
        Superior temporal gyrus (BA 22)-R634580−43.31
        Inferior parietal lobule (BA 40)-L153−68−32323.26
        Insula (BA 13)-R8838−12203.23
        Precentral gyrus (BA 6)-R26346−8383.23
        Cingulate gyrus (BA 31)-L153−10−32443.19
        Postcentral gyrus (BA 3)-L44−16−42663.14
        Middle temporal gyrus (BA 21)-L22−66−10−83.09
        Caudate head-L22−162683.09
    • Uncorrected p < 0.001, >10 mm3 contiguous cluster extent.

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    Table 3.

    Voxelwise whole-brain results for the ANOVA condition–threat interaction

    Region (BA)Cluster size (mm3)xyzPeak Z score
    Insula (BA 13)-R16193218−83.54
    Inferior frontal gyrus (BA 47)-R3218−183.34
    Inferior frontal gyrus (BA 47)-L744−3820−83.36
    Precuneus (BA 19)-L306−38−78363.35
    Insula (BA 13)-R17536−12203.29
    Inferior frontal gyrus (BA 47)-R2634220−163.26
    Inferior frontal gyrus (BA 47)-L175−5018−43.23
    Anterior cingulate (BA 33)-L88−622203.2
    • Uncorrected p < 0.001, >10 mm3 contiguous cluster extent.

    • View popup
    Table 4.

    Pearson correlation of discrimination activity across brain regions in sleep-rested and sleep-deprived conditions

    L. amygdalaR. amygdaladACCL. insulaR. insulaNetwork
    Sleep-rested
        L. amygdala10.380.270.150.060.41
        R. amygdala10.370.510.350.68
        dACC10.830.800.88
        L. insula10.860.92
        R. insula10.80
        Network1
    Sleep-deprived
        L. amygdala10.510.440.320.460.61
        R. amygdala10.670.480.370.73
        dACC10.840.610.91
        L. insula10.780.90
        R. insula10.80
        Network1
    • Significant correlations using a threshold of p < 0.05 are displayed in bold font.

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The Journal of Neuroscience: 35 (28)
Journal of Neuroscience
Vol. 35, Issue 28
15 Jul 2015
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Sleep Deprivation Impairs the Human Central and Peripheral Nervous System Discrimination of Social Threat
Andrea N. Goldstein-Piekarski, Stephanie M. Greer, Jared M. Saletin, Matthew P. Walker
Journal of Neuroscience 15 July 2015, 35 (28) 10135-10145; DOI: 10.1523/JNEUROSCI.5254-14.2015

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Sleep Deprivation Impairs the Human Central and Peripheral Nervous System Discrimination of Social Threat
Andrea N. Goldstein-Piekarski, Stephanie M. Greer, Jared M. Saletin, Matthew P. Walker
Journal of Neuroscience 15 July 2015, 35 (28) 10135-10145; DOI: 10.1523/JNEUROSCI.5254-14.2015
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Keywords

  • amygdala
  • anterior cingulate cortex
  • anterior insula
  • emotion
  • sleep deprivation
  • social threat

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