Article Figures & Data
Figures
- 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.
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.
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.
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.
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.
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
Sleep time (min) % Total sleep time Obtained by % of participants Total sleep time 469.43 ± 38.7 Stage 1 25.72 ± 10.4 5.53 ± 2.4 100% Stage 2 253.15 ± 34.1 53.87 ± 5.2 100% SWS 90.35 ± 28.4 19.41 ± 6.7 100% REM 100.20 ± 24.8 21.20 ± 4.3 100% SWS, NREM stage 3 and 4.
Region (BA) Cluster size (mm3) x y z Peak Z score Sleep-rested threatening > not threatening Inferior frontal gyrus (BA 47)-L 45369 −38 20 −10 5.95 Inferior frontal gyrus (BA 47)-L −48 20 0 5.6 Middle frontal gyrus (BA 47)-L −50 38 −4 4.16 Inferior frontal gyrus (BA 47)-R 29422 42 26 −8 5.21 Inferior frontal gyrus (BA 47)-R 40 20 −14 4.87 Inferior frontal gyrus (BA 47)-R 32 22 −8 4.85 Superior frontal gyrus (BA 8)-L 33556 −6 24 56 4.84 Medial frontal gyrus (BA 8)-L −6 24 46 4.42 Medial frontal gyrus (BA 9)-L −2 40 32 4.05 Lateral globus pallidus-L 284 −18 −2 −12 3.5 Superior temporal gyrus (BA 22)-R 416 48 −30 −2 3.38 Middle frontal gyrus (BA 6)-R 306 42 0 60 3.37 Sleep-rested not threatening > threatening Medial frontal gyrus (BA 10)-L 14788 −6 50 −8 4.72 Anterior cingulate (BA 32)-R 8 36 −10 3.91 Medial frontal gyrus (BA 10)-R 12 52 −6 3.85 Middle frontal gyrus (BA 9)-R 12141 26 24 36 4.66 Superior frontal gyrus (BA 6)-R 22 12 52 3.97 Precuneus (BA 19)-L 4878 −38 −76 34 4.19 Superior frontal gyrus (BA 8)-L 4900 −24 14 54 3.77 Middle frontal gyrus (BA 8)-L −22 26 38 3.66 Middle frontal gyrus (BA 8)-L −22 22 46 3.55 Precuneus (BA 7)-R 6234 4 −52 52 3.76 Precuneus (BA 7)-R 0 −48 46 3.56 Superior temporal gyrus (BA 22)-L 1094 −56 −6 −4 3.73 Precentral gyrus (BA 6)-L 3063 −44 −12 34 3.69 Insula (BA 13)-L −42 −14 22 3.5 Cingulate gyrus (BA 31)-R 2253 14 −36 40 3.65 Subcallosal gyrus (BA 25)-R 744 6 20 −14 3.58 Superior temporal gyrus (BA 22)-R 634 58 0 −4 3.31 Inferior parietal lobule (BA 40)-L 153 −68 −32 32 3.26 Insula (BA 13)-R 88 38 −12 20 3.23 Precentral gyrus (BA 6)-R 263 46 −8 38 3.23 Cingulate gyrus (BA 31)-L 153 −10 −32 44 3.19 Postcentral gyrus (BA 3)-L 44 −16 −42 66 3.14 Middle temporal gyrus (BA 21)-L 22 −66 −10 −8 3.09 Caudate head-L 22 −16 26 8 3.09 Uncorrected p < 0.001, >10 mm3 contiguous cluster extent.
Region (BA) Cluster size (mm3) x y z Peak Z score Insula (BA 13)-R 1619 32 18 −8 3.54 Inferior frontal gyrus (BA 47)-R 32 18 −18 3.34 Inferior frontal gyrus (BA 47)-L 744 −38 20 −8 3.36 Precuneus (BA 19)-L 306 −38 −78 36 3.35 Insula (BA 13)-R 175 36 −12 20 3.29 Inferior frontal gyrus (BA 47)-R 263 42 20 −16 3.26 Inferior frontal gyrus (BA 47)-L 175 −50 18 −4 3.23 Anterior cingulate (BA 33)-L 88 −6 22 20 3.2 Uncorrected p < 0.001, >10 mm3 contiguous cluster extent.
- Table 4.
Pearson correlation of discrimination activity across brain regions in sleep-rested and sleep-deprived conditions
L. amygdala R. amygdala dACC L. insula R. insula Network Sleep-rested L. amygdala 1 0.38 0.27 0.15 0.06 0.41 R. amygdala 1 0.37 0.51 0.35 0.68 dACC 1 0.83 0.80 0.88 L. insula 1 0.86 0.92 R. insula 1 0.80 Network 1 Sleep-deprived L. amygdala 1 0.51 0.44 0.32 0.46 0.61 R. amygdala 1 0.67 0.48 0.37 0.73 dACC 1 0.84 0.61 0.91 L. insula 1 0.78 0.90 R. insula 1 0.80 Network 1 Significant correlations using a threshold of p < 0.05 are displayed in bold font.
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