Losing Control: Sleep Deprivation Impairs the Suppression of Unwanted Thoughts

Unwanted memories often enter conscious awareness when individuals confront reminders. People vary widely in their talents at suppressing such memory intrusions; however, the factors that govern suppression ability are poorly understood. We tested the hypothesis that successful memory control requires sleep. Following overnight sleep or total sleep deprivation, participants attempted to suppress intrusions of emotionally negative and neutral scenes when confronted with reminders. The sleep-deprived group experienced significantly more intrusions (unsuccessful suppressions) than the sleep group. Deficient control over intrusive thoughts had consequences: Whereas in rested participants suppression reduced behavioral and psychophysiological indices of negative affect for aversive memories, it had no such salutary effect for sleep-deprived participants. Our findings raise the possibility that sleep deprivation disrupts prefrontal control over medial temporal lobe structures that support memory and emotion. These data point to an important role of sleep disturbance in maintaining and exacerbating psychiatric conditions characterized by persistent, unwanted thoughts.

Memories of unpleasant experiences and thoughts can intrude into conscious awareness when reminders to them are confronted. Individuals suffering from psychiatric conditions such as posttraumatic stress disorder (PTSD) and major depressive disorder (MDD) typically experience a disproportionate number of unwanted memory intrusions, and difficulties in limiting the duration and recurrence of these intrusions compound negative mood and affective dysregulation (Brewin, Gregory, Lipton, & Burgess, 2010; Mihailova & Jobson, 2018; Moritz et al., 2014; Newby & Moulds, 2011; Payne, Kralj, Young, & Meiser-Stedman, 2019). One’s capacity for inhibiting intrusive thoughts might therefore play a fundamental role in maintaining mental health and well-being (Gagnepain, Hulbert, & Anderson, 2017).

The ability to control intrusive memories and thoughts can be studied in the laboratory by measuring people’s success at suppressing memory retrieval when confronted with reminders to unwanted thoughts. For example, one widely used task, known as the think/no-think (TNT) paradigm (Anderson & Green, 2001), requires participants to either actively engage (think) or suppress (no-think) memory retrieval when presented with reminder cues to associated memories, often aversive images. An intrusion occurs when participants’ attempts to suppress retrieval during no-think trials fail and the reminder cue triggers an involuntary retrieval of the associated memory. Reminder cues typically elicit an intrusion less than 50% of the time (Gagnepain et al., 2017; Hellerstedt, Johansson, & Anderson, 2016; Levy & Anderson, 2012; van Schie & Anderson, 2017), but people vary widely in memory control ability (Levy & Anderson, 2008). The factors contributing to this variability are poorly understood. Identifying determinants of successful retrieval suppression could contribute to the understanding of vulnerability to disorders characterized by intrusive thoughts (Brewin et al., 2010; Mary et al., 2020; Moritz et al., 2014; Streb, Mecklinger, Anderson, Johanna, & Michael, 2016).

Retrieval suppression ability is thought to be intrinsically linked to inhibitory control. According to the inhibitory deficit hypothesis (Levy & Anderson, 2008), individual differences in regulating intrusive memories originate from variation in underlying inhibition function. This hypothesis predicts that conditions that strain inhibitory control will likewise undermine the ability to suppress unwanted thoughts. In healthy adults, sleep deprivation impairs cognitive functioning (Alhola & Polo-Kantola, 2007; Walker, 2009; Wild, Nichols, Battista, Stojanoski, & Owen, 2018), especially executive control (Drummond, Paulus, & Tapert, 2006; Nilsson et al., 2005), making sleep loss an important candidate factor mediating fluctuations in thought control. Indeed, mental fatigue arising from sustaining an effortful task can increase the frequency of intrusions during the TNT task (van Schie & Anderson, 2017). Moreover, the prefrontal–medial temporal lobe (MTL) networks involved in retrieval suppression (Benoit, Hulbert, Huddleston, & Anderson, 2015; Gagnepain et al., 2017; Levy & Anderson, 2012) are disrupted by sleep loss (Yoo, Gujar, Hu, Jolesz, & Walker, 2007), which suggests that losing sleep may heighten people’s vulnerability to intrusive thoughts (Chee, 2004; Mazur, Pace-Schott, & Hobson, 2002; Thomas et al., 2000, 2003; van Schie & Anderson, 2017; Yoo et al., 2007). Chronic sleep disturbance is also a formal symptom of most psychiatric conditions, particularly PTSD (Maher, Rego, & Asnis, 2006) and MDD (Riemann, Berger, & Voderholzer, 2001).

These observations led us to consider whether the established link between psychiatric conditions and disturbed sleep may be mediated partially by sleep deficits compromising a person’s ability to regulate emotion by suppressing retrieval of aversive thoughts. For example, suppressing retrieval of aversive scenes reduces people’s emotional response to those scenes later on, as revealed by changes in subjective affect ratings for the suppressed stimuli and the relationship of those changes to prefrontally driven down-regulation of the amygdala during memory intrusions (Gagnepain et al., 2017). This impact of retrieval suppression on perceived emotion (referred to hereafter as affect suppression) suggests that retrieval suppression contributes to affective homeostasis by reducing the negative tone of unpleasant events. If sleep loss compromises memory control, it may diminish the impact that retrieval suppression has on affective responses to unwanted thoughts, a possibility consistent with the well-documented negative consequences of sleep loss on mood (Dinges et al., 1997; Short & Louca, 2015; Zohar, Tzischinsky, Epstein, & Lavie, 2005). Whether sleep loss disrupts affect suppression arising from memory control and whether affect suppression effects are mirrored in psychophysiological reactivity to suppressed thoughts have never been examined.

To determine whether sleep deficits could contribute to the pathogenesis and maintenance of intrusive symptoms, we investigated the impact of sleep deprivation on memory control in healthy adults. Participants learned associations between faces and emotionally negative or neutral scenes before an overnight interval of sleep or total sleep deprivation (Fig. 1a). The following morning, participants completed a TNT task for the face-scene associations (Fig. 1b). On each trial of this task, a face was presented alone in either a green or red frame, instructing participants to either actively retrieve (think) or suppress (no-think) the associated scene, respectively. Attempts to suppress retrieval of the scene often initially fail, leading the scene to intrude into participants’ awareness involuntarily despite efforts to stop it. Because involuntary retrievals in the TNT paradigm are, as in real life, unobservable events private to the individual, it was necessary to identify their occurrence through intrusion reports. After each trial, participants reported, using a 3-point scale (never, briefly, often), whether the associated scene had entered awareness. We then quantified variations in memory control success by using the proportion of no-think trials that triggered any awareness of the associated scene, reflecting a momentary failure of retrieval suppression (i.e., reports of briefly or often; referred to hereafter as intrusions).

Intrusion reports provide a validated index of involuntary retrieval. Researchers using functional MRI (fMRI) to measure intrusion reports have established that in rested individuals, intrusion trials (unsuccessful suppression attempts) trigger greater activation in the right dorsolateral prefrontal cortex (rDLPFC), greater negative coupling of rDLPFC with both the hippocampus and amygdala, and greater down-regulation of activity in the latter structures, consistent with a reactive engagement of top-down inhibitory control to suppress the intrusive content (Benoit et al., 2015; Gagnepain et al., 2017; Levy & Anderson, 2012). Moreover, research in which electroencephalogram (EEG) was used established that reports of intrusions are associated with a brief increase in event-related-potential markers of working memory storage (Hellerstedt et al., 2016), followed by their rapid elimination, consistent with a reactive purging of the intrusion. In contrast, trials that attracted intrusion reports of never (successful suppression attempts) instead have shown significant increases in beta frequency power, consistent with successful proactive control of retrieval (Castiglione, Wagner, Anderson, & Aron, 2019). Given these intrusion indices, we predicted that sleep-deprived participants would report more intrusions for no-think scenes than would participants who slept and would exhibit impaired ability to reduce the frequency of intrusions over time.

Studies that employ the TNT paradigm often measure the consequences of thought suppression for memory accessibility via a recall test administered after the TNT assessment phase. These studies have shown that suppressing a memory often impairs its later accessibility (suppression-induced forgetting; for review, see Anderson & Hanslmayr, 2014). However, our primary objective here was instead to test how sleep deprivation influenced the ability to down-regulate unwanted thoughts and, consequently, affect suppression for the intruding content. To investigate how the predicted failures in intrusion control following sleep loss influenced affect suppression, we acquired emotional ratings for the scenes both before the overnight delay and also after the TNT phase the following morning (Fig. 1c). We also measured SCRs to scene presentations to examine whether psychophysiological measures of sympathetic arousal mirrored suppression-induced changes in subjective affect. We predicted that retrieval suppression would attenuate both subjective and psychophysiological reactivity to negative scenes in the sleep group. Critically, however, if our hypothesis about the role of sleep loss in the pathogenesis of psychiatric disorders is correct, this salutary effect of suppression on negative affect should be significantly reduced in otherwise healthy participants randomly assigned to our sleep-deprivation group.

We also measured the physiological correlates of memory control by collecting heart rate variability (HRV) recordings before and after the TNT assessment phase. Spectral analysis of HRV has previously identified two reliable components: high-frequency HRV (HF-HRV; 0.15–0.40 Hz) and low-frequency HRV (LF-HRV; 0.04–0.15 Hz). Note that higher HF-HRV is linked to superior executive functioning (for review, see Thayer & Lane, 2009), including memory control (Gillie, Vasey, & Thayer, 2014), whereas LF-HRV instead increases with fatigue (Tran, Wijesuriya, Tarvainen, Karjalainen, & Craig, 2009). Given these observations and given the hypothesized disruption to inhibitory control with sleep deprivation, we predicted that higher HF-HRV would be associated with superior affect suppression and intrusion control in the sleep group but not the sleep-deprivation group. We further predicted significantly higher LF-HRV following sleep deprivation than after a night of sleep, providing physiological confirmation of extreme fatigue.

Acknowledgements Study data are available at https://osf.io/95dbh/. We are grateful to Rhiannon Pearce, Tomas Vaitkus, and Hanna Weiers for their assistance with data collection and to Steven J. Lynn and another anonymous reviewer for their helpful comments on an earlier version of this manuscript.

Transparency Action Editor: Scott O. Lilienfeld Editor: Scott O. Lilienfeld Author Contributions M. O. Harrington, S. A. Cairney, and M. C. Anderson designed the study. M. O. Harrington and J. E. Ashton performed the experiments. M. O. Harrington S. Sankarasubramanian, M. C. Anderson, and S. A. Cairney analyzed the data. M. O. Harrington wrote the manuscript, and all the authors revised the manuscript. All of the authors approved the final manuscript for submission. Declaration of Conflicting Interests

The author(s) declared that there were no conflicts of interest with respect to the authorship or the publication of this article. Funding

This work was supported by Medical Research Council Career Development Award MR-P020208-1 (to S. A. Cairney) and Medical Research Council Grant MC-A060-5PR00 (to M. C. Anderson). Open Practices

All data have been made publicly available via OSF and can be accessed at https://osf.io/apv8y/. The complete Open Practices Disclosure for this article can be found at http://journals.sagepub.com/doi/suppl/10.1177/2167702620951511. This article has received the badge for Open Data. More information about the Open Practices badges can be found at https://www.psychologicalscience.org/publications/badges.

Marcus O. Harrington https://orcid.org/0000-0002-6292-7595 Supplemental Material

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