Tired and apprehensive: anxiety amplifies the impact of sleep loss on aversive brain anticipation - PubMed (original) (raw)

Tired and apprehensive: anxiety amplifies the impact of sleep loss on aversive brain anticipation

Andrea N Goldstein et al. J Neurosci. 2013.

Abstract

Anticipation is an adaptive process, aiding preparatory responses to potentially threatening events. However, excessive anticipatory responding and associated hyper-reactivity in the amygdala and insula are integral to anxiety disorders. Despite the co-occurrence of sleep disruption and anxiety disorders, the impact of sleep loss on affective anticipatory brain mechanisms, and the interaction with anxiety, remains unknown. Here, we demonstrate that sleep loss amplifies preemptive responding in the amygdala and anterior insula during affective anticipation in humans, especially for cues with high predictive certainty. Furthermore, trait anxiety significantly determined the degree of such neural vulnerability to sleep loss: individuals with highest trait anxiety showed the greatest increase in anticipatory insula activity when sleep deprived. Together, these data support a neuropathological model in which sleep disruption may contribute to the maintenance and/or exacerbation of anxiety through its impact on anticipatory brain function. They further raise the therapeutic possibility that targeted sleep restoration in anxiety may ameliorate excessive anticipatory responding and associated clinical symptomatology.

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Figures

Figure 1.

Figure 1.

Study design. A, Time course of experiment for both the sleep-deprived and sleep-rested conditions. B, fMRI anticipation reactivity task trial types. Each trial consisted of an anticipatory cue followed by either an emotional negative or neutral picture stimulus. For negative trials, the anticipation cue was a red “−” symbol that was always followed by a negative picture. For the neutral trials, the anticipation cue was a yellow “O” symbol that was always followed by a neutral picture. For ambiguous trials, the anticipation cue was a white “?” symbol, which was followed by either a negative or a neutral picture at exactly a 50:50 ratio. C, An example anticipation reactivity task trial with timing. Each anticipation trial lasted an average of 8.75 s. Following a fixation screen, the trial proceeded with (1) the cued anticipation phase, in which one of the three warning cues were presented using a variable jittered time duration for optimal signal estimation (maximum, 5.6 s; minimum, 2.5 s; mean, 4.5 s) (Dale, 1999); (2) the stimulus reactivity phase, in which the emotionally negative or neutral image was presented (1 s); and (3) the response period, where subjects made a categorical emotionality judgment using a button-press rating (negative/neutral; 2.5 s), also confirming wakefulness. Pseudorandomly interspersed between these anticipation trials were null trial events (data not shown), where 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 both a baseline condition as well as modulating intertrial interval variability for optimal modeling of trial events.

Figure 2.

Figure 2.

A, Brain maps displaying ROI mask (left brain image) and the ANOVA main effect of condition (sleep deprivation, sleep rested; right brain image) from the voxelwise ROI analysis in bilateral amygdala across all three cue types (negative, neutral, and ambiguous) [peak MNI coordinates (x, y, z); left: −18, −6, −16; right: 24, −2, −16]. Right side bar graphs illustrate the difference in average parameter estimates across the 6 mm ROI spheres between the sleep-deprivation and sleep-rested conditions, and average signal for each condition, respectively. B, Brain maps displaying ROI mask (left brain image) and the ANOVA condition–cue type (negative, neutral, and ambiguous) interaction results from the voxelwise ROI analysis in the right anterior insula for the three cue types [peak MNI coordinates (x, y, z); 32, 20, 14], together with equivalent bar graphs as in A. No significant main effect of condition or cue type interaction was observed in the left anterior insula at FWE p < 0.05. Error bars represent SEM. Within-region statistics: *p < 0.05, **p < 0.01.

Figure 3.

Figure 3.

A, Brain maps displaying anterior insula ROI mask (left brain image) and the voxelwise ROI regression between STAI trait anxiety and the relative sleep deprivation induced increase in anticipatory response in anterior insula for all cues [peak MNI coordinates (x, y, z); 34, 18, 18; T = 4.04, p < 0.001]. Regression thresholded at p < 0.05 FWE-corrected for multiple comparisons. B, Scatterplot displaying this same relationship using the average parameter estimates across the 6 mm ROI anterior insula ROI mask (left brain image).

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