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Total sleep deprivation reduces top-down regulation of emotion without altering bottom-up affective processing.

ABSTRACT: Sleep loss is reported to influence affective processing, causing changes in overall mood and altering emotion regulation. These aspects of affective processing are seldom investigated together, making it difficult to determine whether total sleep deprivation has a global effect on how affective stimuli and emotions are processed, or whether specific components of affective processing are affected selectively. Sixty healthy adults were recruited for an in-laboratory study and, after a monitored night of sleep and laboratory acclimation, randomly assigned to either a total sleep deprivation condition (n = 40) or a rested control condition (n = 20). Measurements of mood, vigilant attention to affective stimuli, affective working memory, affective categorization, and emotion regulation were taken for both groups. With one exception, measures of interest were administered twice: once at baseline and again 24 hours later, after the sleep deprived group had spent a night awake (working memory was assessed only after total sleep deprivation). Sleep deprived individuals experienced an overall reduction in positive affect with no significant change in negative affect. Despite the substantial decline in positive affect, there was no evidence that processing affectively valenced information was biased under total sleep deprivation. Sleep deprived subjects did not rate affective stimuli differently from rested subjects, nor did they show sleep deprivation-specific effects of affect type on vigilant attention, working memory, and categorization tasks. However, sleep deprived subjects showed less effective regulation of negative emotion. Overall, we found no evidence that total sleep deprivation biased the processing of affective stimuli in general. By contrast, total sleep deprivation appeared to reduce controlled processing required for emotion regulation.

SUBMITTER: Stenson AR

PROVIDER: S-EPMC8412406 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:ObjectivePosttraumatic stress disorder (PTSD) is associated with decreased top-down emotion modulation from medial prefrontal cortex (mPFC) regions, a pathophysiology accompanied by hyperarousal and hyperactivation of the amygdala. By contrast, PTSD patients with the dissociative subtype (PTSD + DS) often exhibit increased mPFC top-down modulation and decreased amygdala activation associated with emotional detachment and hypoarousal. Crucially, PTSD and PTSD + DS display distinct functional connectivity within the PFC, amygdala complexes, and the periaqueductal gray (PAG), a region related to defensive responses/emotional coping. However, differences in directed connectivity between these regions have not been established in PTSD, PTSD + DS, or controls.MethodsTo examine directed (effective) connectivity among these nodes, as well as group differences, we conducted resting-state stochastic dynamic causal modeling (sDCM) pairwise analyses of coupling between the ventromedial (vm)PFC, the bilateral basolateral and centromedial (CMA) amygdala complexes, and the PAG, in 155 participants (PTSD [n = 62]; PTSD + DS [n = 41]; age-matched healthy trauma-unexposed controls [n = 52]).ResultsPTSD was characterized by a pattern of predominant bottom-up connectivity from the amygdala to the vmPFC and from the PAG to the vmPFC and amygdala. Conversely, PTSD + DS exhibited predominant top-down connectivity between all node pairs (from the vmPFC to the amygdala and PAG, and from the amygdala to the PAG). Interestingly, the PTSD + DS group displayed the strongest intrinsic inhibitory connections within the vmPFC.ConclusionsThese results suggest the contrasting symptom profiles of PTSD and its dissociative subtype (hyper- vs. hypo-emotionality, respectively) may be driven by complementary changes in directed connectivity corresponding to bottom-up defensive fear processing versus enhanced top-down regulation. Hum Brain Mapp 38:5551-5561, 2017. © 2017 Wiley Periodicals, Inc.

Project description:Emotional stress throughout the day is known to affect objective sleep physiology and subjective sleep quality. In the interplay between emotions and sleep, emotion regulation plays a critical role in the recovery from stressful, emotional events and subsequent sleep. While the effects of top-down emotion regulation strategies such as cognitive reappraisal on sleep have been studied before, the impact of bottom-up emotion regulation strategies such as experiential emotion regulation is understudied. Cognitive reappraisal reflects the cognitive reinterpretation of the meaning of a stressful event, while experiential emotion regulation involves an active, non-intervening, accepting, open and welcoming approach of acknowledging awareness of raw sensory affective experiences or 'experiential awareness' in a first phase and expression in a second phase. The present study aims to investigate the effects of experiential emotion regulation and cognitive reappraisal on the recovery from pre-sleep emotional stress measured by (1) negative affect and (2) sleep structure. Sleep of forty-three healthy Dutch-speaking participants (22 females, 21 males) has been assessed using EEG polysomnography. Stress was triggered using a pre-sleep emotional failure induction, after which emotion regulation by experiential emotion regulation versus cognitive reappraisal versus control was induced twice. The control condition consisted of the reallocation of attention towards the neutral aspects of the emotional event. The results indicated that recovery from negative affect of the failure experience after single or repeated deployment of experiential emotion regulation and cognitive reappraisal was not significantly different from the control condition. Moreover, after repeated deployment, sleep physiology did not significantly differ between experiential emotion regulation, cognitive reappraisal, and the control condition in the impact of the regulation of the failure experience. The implications of the distinctive impact of experiential emotion regulation and cognitive reappraisal on both the pre-sleep emotional experience and follow-up sleep physiology are discussed.

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Total sleep deprivation reduces top-down regulation of emotion without altering bottom-up affective processing.

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