Article Figures & Data
Figures
- Figure 1.
Stimulus ratings. A, The proportion of stimuli categorized as either positive (pleasant) or neutral in the sleep-control (SC) and sleep-deprivation (SD) groups. A mixed-design ANOVA [between-subject factor of group (sleep control, sleep deprivation) and within-subjects factor of emotional response (pleasant, neutral)] demonstrated no significant main effect of group (F(1,25) = 0.19, p = 0.67) and no significant main effect of emotional response (F(1,25) = 2.02, p = 0.16), but a significant group × emotional response interaction (F(1,25) = 4.09, p = 0.04; across group and condition comparison). Post hoc tests within each group (symbol above bar) represent comparisons of each category to the null hypothesis of equal categorical assignment (50%), with significance values provided in the main text. B, The corresponding change in response tendency, characterized as positive bias score, represented as the subtracted difference in the proportion of positive items relative to the proportion of neutral items in the sleep-control and sleep-deprivation group. A zero value represents equal numbers of stimuli assigned to neutral and pleasant categories, while a positive score represents a greater proportion of stimuli rated as pleasant relative to neutral (and vice versa). Comparison reflects significance at p < 0.05 (*) and p < 0.01 (**). n.s., Nonsignificant. Error bars represent s.e.m. Corresponding response times and analyses are provided in supplemental Table 1 (available at www.jneurosci.org as supplemental material).
- Figure 2.
fMRI group-level activation differences. A, B, Statistical activation maps demonstrating regions of significantly increased activation (red box surround) in response to the positive emotion stimulus gradient in the sleep-deprivation group, relative to the sleep-control group, in the amygdala (A), VTA (B), fusiform gyrus (C), putamen (D and E), and insular cortex (D and F) (A), and corresponding regions of significantly less activation (blue box surround) in the sleep-deprivation group, relative to the sleep-control group, in the occipital cortex (G), hippocampus (H), and precuneus (I) (B). Significant difference displayed on T1 anatomical slices (MNI slice number lower left). Histograms of parameter estimates (effect size) for averaged activity for regions of significant difference are provided in supplemental Figure 1 (available at www.jneurosci.org as supplemental material), with coordinates provided in Table 1. Images are displayed in neurological convention, with left side corresponding to left hemisphere. Effects are displayed at whole brain uncorrected cortex p < 0.001; ≥5 contiguous voxels, with corrected significance reported in Table 1.
- Figure 3.
Histograms of parameter estimates (effect size) for nonparametrically modulated activity in regions of group-level difference, displayed in Figure 2, but for a subset analysis of the 25 most neutral and 25 most positive images. To determine whether increases in activation observed in the sleep-deprivation group were due to a generalized (nonspecific) amplified reactivity to all stimulus kinds, independent of emotion strength, a further subset analysis of the upper quartile stimulus set (most positive) and lower quartile stimulus set (most neutral) was performed for regions identified as different between the two groups. A, For all regions described as more reactive in the deprivation group (Fig. 2A), the subset analyses revealed similar activation levels between the two groups in response to the most neutral pictures, yet highly significant differences between groups for the most positive pictures. Between-group statistical t test comparisons are provided within the figure. All within-group comparisons between the most neutral and most positive stimuli were significant in the deprivation group (all p < 0.04), yet nonsignificant in the control group (all p > 0.12), with the exception of activity in the right amygdala, which showed a trend toward significance (p = 0.07). Therefore, across all regions showing greater reactivity in the deprivation group across the entire stimulus set, a condition-specific relationship was observed, expressly in response to positive stimuli, while reactivity to more neutral images was similar in the two groups. B, This was also true for the reduction in activity identified in the hippocampus and left occipital gyrus in the deprivation group. However, it was not the case for the remaining region showing decreased reactivity at the overall group level in the sleep-deprived participants—the precuneus—which demonstrated nonspecific reductions in reactivity for both neutral and negative stimulus subsets, relative to the control group. Between-group statistical t test comparisons are provided within figure. All within-group comparisons between the most neutral and most positive stimuli were significant in the control group and deprivation group (all p < 0.03), with the exception of activity in the precuneus in the control group (p = 0.56). All between group comparisons reflect significance at p < 0.05 (*) and p < 0.005 (**). Error bars represent s.e.
- Figure 4.
fMRI correlation and conjunction analyses. A, Regions of task-related activation that were significantly more active in the sleep-deprivation group than in the sleep-control group at the overall group level (green; as described in Fig. 2A), together with regions showing a correlation with the positive bias score within the sleep-deprivation group (red, as above), and the overlap homology between the two (yellow with yellow box surround), identifying the insular, VTA, and fusiform gyrus. Coordinates are provided in supplemental Table 2 (available at www.jneurosci.org as supplemental material). B, Results of the conjunction test confirming the overlap homology shown in Figure 3B (yellow with yellow box surround) in a priori regions of the insular [A; peak MNI space coordinates (x, y, z): −37, 7, 2], the VTA (B; peak: 1, −21, −18), (C; peak: −24, −53, −12). Images are displayed in neurological convention on T1 anatomical axial slices (MNI slice number above), with left side corresponding to left hemisphere.
- Figure 5.
Group-level differences in functional connectivity. A, B, Regions showing significantly greater functional connectivity (red with red box surround) in the sleep-deprivation group relative to the sleep-control group for ROIs in the VTA (seed), in the left anterior temporal pole (MNI peak: −57, 6, −30; Z score = 3.74) and left amygdala (peak: −24, −6, −24; Z score = 3.93) (A); and the insular (seed), in the left lateral occipital cortex (peak: −48, −75, −9; Z score = 3.63), medial fusiform gyrus (peak: −27, −54, −15; Z score = 3.98), posterior insular cortex (peak: −39, −24, −3; Z score = 4.02), posterior middle temporal lobe (peak: −63, −54, 3; Z score = 3.88), and left occipital cortex (peak: −21, −102, 3; Z score = 3.82) (B). C, Regions showing significantly less functional connectivity (yellow with yellow box surround) in the sleep-deprivation group relative to the sleep-control group for bilateral amygdala ROIs in (left seed) the left orbitofrontal cortex (peak: 18, 9, −18; Z score = 4.12), right orbitofrontal cortex (peak: −9, 6, −15; Z score = 3.51), medial prefrontal cortex (peaks: 15, 54, 18, Z score = 4.02; 21, 51, 6, Z score = 3.71; 15, 39, 9, Z score = 3.42), left fusiform gyrus (peak: −36, −57, −18; Z score = 3.72), and (right seed) the midbrain (peak: 9, −12, −18; Z score = 3.35). Images are displayed in neurological convention on T1 anatomical axial slices (MNI slice number above), with left side corresponding to left hemisphere.
Tables
- Table 1.
Anatomical coordinates for regions of significant difference between the sleep control and sleep deprivation groups in response to the emotional stimulus gradient
Region Cluster size (voxels) x y z Peak Z score SVC p Sleep deprivation > sleep control Amygdalaa,b,c L 47 −24 −9 −21 3.65 0.012 R 12 30 3 −18 3.39 0.032 Insular cortex—La,b,c,d 20 −44 4 3 3.60 0.027 Putamen—Lb,d,e 9 −30 5 −2 3.62 0.026 Substantia nigra/ventral tegmental areab,d,f,g,h 9 0 −21 −18 3.51 0.007 Fusiform gyrus—L* 46 −24 −54 −12 4.44 Sleep control > sleep deprivation Posterior hippocampal cortex—R* 7 30 −28 −9 3.51 Precuneus—L* 8 0 −39 57 3.16 Middle occipital gyrus—L* 5 −27 −87 −3 3.12 The x–y–z coordinates are given in peak Montreal Neurological Institute (MNI) space coordinates. L and R denote left and right.
↵* denotes non-a priori regions that were significant at p < 0.001 uncorrected threshold, but did not survive whole-brain FDR correction at p < 0.05. All other areas were of a priori interest, defined by letter (a–g), and all survived SVC correction for multiple comparisons (p < 0.05, 10 mm3 sphere; with the exception of the small substantia nigra/VTA nuclei, which used a 5 mm3 sphere).
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