The Spectral Fingerprint of Sleep Problems in Post-Traumatic Stress Disorder

Boer, M. de; Nijdam, Mirjam J.; Jongedijk, Ruud A.; Olff, Miranda; Hofman, W.F.; Talamini, Lucia M.

doi:10.1101/209452

Cited by 6 publications

(7 citation statements)

References 76 publications

(67 reference statements)

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“…Twin studies have shown that sleep spectral power is highly heritable (Ambrosius et al, 2008; De Gennaro et al, 2008; Purcell et al, 2017), with beta-band power exhibiting the highest heritability estimates of the canonical sleep EEG frequency bands (Ambrosius et al, 2008). Higher beta power during sleep (relative to healthy controls) has been documented in a number of psychopathologies, including PTSD (de Boer et al, 2020; Germain et al, 2006; Woodward et al, 2000). Notably, when individuals with PTSD are compared to trauma-exposed, non-PTSD participants, higher beta power is not always observed (Cohen et al, 2013; Denis et al, 2021; Mellman et al, 2007).…”

Section: Discussionmentioning

confidence: 99%

“…Theta power has been shown to be elevated in trauma-exposed individuals who were resilient to, compared to those diagnosed with, PTSD (Cowdin et al, 2014; though see Denis et al, 2021). Similarly, electroencephalographic spectral power in in the beta frequency range (∼20-30Hz) during sleep has also been shown to be elevated in PTSD compared to those without PTSD (de Boer et al, 2020; Germain et al, 2006; Wang et al, 2020; Woodward et al, 2000), and has been theorized as a marker of hyperarousal (Hall et al, 2007; Krystal et al, 2002; Perlis et al, 2001; Riedner et al, 2016; Spiegelhalder et al, 2012). In contrast however, beta power during sleep has also been associated with reduced risk of PTSD development (Mellman et al, 2007) and reduced symptomatology in healthy participants and those with PTSD (Denis et al, 2021).…”

Section: Introductionmentioning

confidence: 97%

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

Denis

Bottary

Cunningham

et al. 2022

Preprint

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Background: 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 sleep's role in extinction retention remain underdetermined. Methods: We reanalyzed data from two existing datasets examining the relationship between the microarchitecture of sleep and extinction recall in healthy controls (Study 1, n = 46) and a pilot study in individuals with PTSD (Study 2, n = 12). In both studies, participants underwent a fear conditioning and extinction protocol over the course of two days, with polysomnography sleep recording occurring between conditioning and extinction. Twenty-four hours after extinction learning, participants underwent extinction recall. Power spectral density (PSD) was computed for NREM and REM sleep during both pre- and post-extinction learning. Results: Increased PSD in frequencies spanning the canonical beta band during pre-extinction learning sleep were associated with worse extinction recall in healthy participants (r = .41, p = .004). Beta PSD was shown to be highly stable across three nights of sleep (NREM intraclass correlation (ICC) = 0.93; REM ICC = 0.94). Individuals with PTSD were found to have increased beta PSD compared to healthy controls (NREM: p = .038; REM: p = .007), and beta PSD correlated with extinction recall in the PTSD group at a similar magnitude to controls (r = .39). Conclusions: The present findings suggest that beta band PSD may be a trait-like feature of the sleep EEG that is heightened in PTSD and associated with impaired fear extinction recall. Thus, beta PSD during sleep may reflect a trait marker for vulnerability to PTSD, specifically implicated in difficulties recalling extinguished fear.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 97%

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

Denis

Bottary

Cunningham

et al. 2022

Preprint

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“…According to DSM-5, SD represents prominent clinical feature of the disorder with very high prevalence (American Psychiatric Association, 2013 ; Germain et al, 2008 ; Spoormaker & Montgomery, 2008 ), and is often closely related to severity of overall PTSD symptoms (Clum, Nishith, & Resick, 2001 ; Nishith, Resick, & Mueser, 2001 ) and resistant to first-line treatments (Belleville, Guay, & Marchand, 2011 ; Schoenfeld, Deviva, & Manber, 2012 ; Zayfert & DeViva, 2004 ). SD observed in PTSD are associated with sleep-related arousal regulation (Mellman, 1997 ) and include insomnia, nightmares, hyperarousal states, sleep terrors and nocturnal anxiety attacks, body-movement and breathing-related sleep disorders (Harvey, Jones, & Schmidt, 2003 ; Maher, Rego, & Asnis, 2006 ; Mellman & Hipolito, 2006 ; Pillar, Malhotra, & Lavie, 2000 ; Spoormaker & Montgomery, 2008 ; Westermeyer et al, 2010 ), with heightened sympathovagal tone during rapid-eye-movement (REM) sleep, fragmented REM sleep patterns, reduced REM theta activity (Cowdin, Kobayashi, & Mellman, 2014 ; Germain, 2013 ; Germain et al, 2008 ; Kobayashi, Boarts, & Delahanty, 2007 ; Lamarche & De Koninck, 2007 ; Mellman et al, 2002 ; Mellman & Hipolito, 2006 ) and altered EEG spectral topology (de Boer et al, 2019 ). Interestingly, SD (e.g., disrupted REM sleep, self-reported insomnia and general sleep quality problems) immediately after (Koren, Arnon, Lavie, & Klein, 2002 ; Luik, Iyadurai, Gebhardt, & Holmes, 2019 ; Mellman et al, 2002 , Mellman & Hipolito, 2006 ), as well as prior to trauma exposure could both increase the risk of PTSD development (Acheson et al, 2019 , Bryant, Creamer, O’Donnell, Silove, & McFarlane, 2010 , Koffel, Polusny, Arbisi, & Erbes, 2013 ).…”

Section: Stress and Circadian Dysregulationmentioning

confidence: 99%

Traumatic stress and the circadian system: neurobiology, timing and treatment of posttraumatic chronodisruption

Agorastos

Olff

2020

European Journal of Psychotraumatology

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Background: Humans have an evolutionary need for a well-preserved internal 'clock', adjusted to the 24-hour rotation period of our planet. This intrinsic circadian timing system enables the temporal organization of numerous physiologic processes, from gene expression to behaviour. The human circadian system is tightly and bidirectionally interconnected to the human stress system, as both systems regulate each other's activity along the anticipated diurnal challenges. The understanding of the temporal relationship between stressors and stress responses is critical in the molecular pathophysiology of stress-and trauma-related diseases, such as posttraumatic stress disorder (PTSD). Objectives/Methods: In this narrative review, we present the functional components of the stress and circadian system and their multilevel interactions and discuss how traumatic stress can affect the harmonious interplay between the two systems. Results: Circadian dysregulation after trauma exposure (posttraumatic chronodisruption) may represent a core feature of trauma-related disorders mediating enduring neurobiological correlates of traumatic stress through a loss of the temporal order at different organizational levels. Posttraumatic chronodisruption may, thus, affect fundamental properties of neuroendocrine, immune and autonomic systems, leading to a breakdown of biobehavioral adaptive mechanisms with increased stress sensitivity and vulnerability. Given that many traumatic events occur in the late evening or night hours, we also describe how the time of day of trauma exposure can differentially affect the stress system and, finally, discuss potential chronotherapeutic interventions. Conclusion: Understanding the stress-related mechanisms susceptible to chronodisruption and their role in PTSD could deliver new insights into stress pathophysiology, provide better psychochronobiological treatment alternatives and enhance preventive strategies in stressexposed populations.

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“…NREM sleep in patients with post-traumatic stress disorder showed decreased slow oscillation power and increased higher frequency activity compared to that in control subjects. On the contrary, the slow oscillation power during REM sleep increased in the occipital area [36]. In addition, a study comparing sleep EEG among subjects with primary insomnia, chronic fatigue syndrome, and normal controls showed consistently lower proportion of slow oscillation power during slow wave sleep in primary insomnia and chronic fatigue syndrome, although the proportion of slow wave sleep duration varied among the groups [37].…”

Section: Discussionmentioning

confidence: 95%

Relationship between the Spectral Power Density of Sleep Electroencephalography and Psychiatric Symptoms in Patients with Breathing-related Sleep Disorder

Kang

Cho

Lee

et al. 2021

Clin Psychopharmacol Neurosci

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Objective: Patients with breathing-related sleep disorder (BRSD) often complain of psychiatric symptoms such as depression in addition to snoring, excessive sleepiness, and disturbed sleep. However, the relationship between psychiatric symptoms and severity of sleep apnea in BRSD is controversial. We conducted this study to investigate the relationship between psychiatric symptoms and sleep electroencephalography (EEG) findings in BRSD patients using spectral analysis. Methods: All participants underwent polysomnography and evaluation using Symptom Checklist-90-Revised (SCL-90-R) scale. We analyzed the absolute spectral power density values of standard EEG frequency bands in the participants (n = 169) with BRSD during the non-rapid eye movement (NREM) sleep period. We performed correlation analysis between the domain scores of SCL-90-R scale and the absolute values of the EEG frequency bands. Results: Significant positive correlation was observed between the absolute spectral power density values in the slow oscillation band and the degree of paranoid ideation (r = 0.226, p = 0.028) and depression (r = 0.216, p = 0.044) in SCL-90-R. The multiple linear regression model showed that higher paranoid ideation domain score (B = 0.007, p = 0.020), younger age (B = −0.011, p ＜ 0.001), and female sex (B = 0.213, p = 0.004) were associated with higher slow oscillation power during NREM sleep. Conclusion:The results of the present study suggested a relationship between sleep EEG and psychiatric symptoms in patients with BRSD. This relationship needs to be validated with further studies.

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The Spectral Fingerprint of Sleep Problems in Post-Traumatic Stress Disorder

Cited by 6 publications

References 76 publications

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

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

Traumatic stress and the circadian system: neurobiology, timing and treatment of posttraumatic chronodisruption

Relationship between the Spectral Power Density of Sleep Electroencephalography and Psychiatric Symptoms in Patients with Breathing-related Sleep Disorder

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