Beta spectral power during sleep is associated with impaired recall of extinguished fear

Abstract

The failure to retain memory for extinguished fear plays a major role in the maintenance of post-traumatic stress disorder (PTSD), with successful extinction recall necessary for symptom reduction. Disturbed sleep, a hallmark symptom of PTSD, impairs fear extinction recall. However, our understanding of the electrophysiological mechanisms underpinning sleeps role in extinction retention remain underdetermined. We examined the relationship between the microarchitecture of sleep and extinction recall in healthy humans (n=46, both male and females included) and a pilot study in individuals with PTSD (n=12). Participants underwent a fear conditioning and extinction protocol over two days, with sleep recording occurring between conditioning and extinction. Twenty-four hours after extinction learning, participants underwent extinction recall. Power spectral density (PSD) was computed for pre- and post-extinction learning sleep. Increased beta band PSD ([~]17-26Hz) during pre-extinction learning sleep was associated with worse extinction recall in healthy participants (r=.41, p=.004). Beta PSD was highly stable across three nights of sleep (intraclass correlations (ICC)>0.92). Individuals with PTSD were found to have increased beta PSD compared to healthy controls (ps < .039), and beta PSD correlated with extinction recall in the PTSD group at a similar magnitude to controls (r=.39). Results suggest beta band PSD is elevated in PTSD, and is specifically implicated in difficulties recalling extinguished fear. Significance statementDisturbed sleep is a hallmark feature of posttraumatic stress disorder (PTSD). Certain neural oscillations that occur during sleep have been shown to be altered in PTSD. These include increased 15-30Hz beta oscillations, which are believed to index cortical hyperarousal. Alongside sleep disturbances, patients also show difficulty in recalling extinguished fear. Although prior studies have linked sleep with extinction retention, no studies have investigated the role that neural oscillations during sleep play in this process. Here, we show in both healthy participants and PTSD patients, that increased beta oscillatory power during sleep is associated with impaired extinction retention. Therefore, this study provides new evidence that electrophysiological changes in the sleep EEG of PTSD patients is also implicated in extinction recall processes.