Introduction

Sleep disturbances and posttraumatic stress disorder (PTSD) are highly comorbid and there is a bidirectional relationship between the two [1, 2]. PTSD is characterised by: 1) reexperiencing symptoms (e.g. intrusive memories, nightmares); 2) avoidance of trauma-related reminders; 3) negative alterations in cognition and mood; and 4) altered arousal and reactivity, including sleep disturbance, making this a disorder of considerable functional impairment [3]. The hallmark symptom of PTSD is the unwanted, distressing, and intrusive memories of the trauma [4]. As it is well established that sleep plays a critical role in the processing and consolidation of emotional memories [5,6,7], it is likely sleep plays a central role in the development and maintenance of trauma-related intrusive memories. Therefore, the aim of this review is to summarise recent findings examining the relationship between sleep and the development of trauma-related intrusive memories. We first discuss intrusive memories and consider how theoretical models of PTSD account for their development. Second, we outline the role of sleep in memory consolidation. Third, we review evidence for a relationship between sleep and intrusive trauma-related memories, focusing on three recent meta-analyses. Fourth, we discuss how these results align with clinical samples and current theoretical models of intrusive memory development, considering possible mechanisms explaining a relationship between sleep and intrusive memories. Finally, we provide future directions for studying sleep and intrusive trauma-related memory development.

Intrusive Memories

Involuntary intrusions of thoughts, mental imagery, and memories are a common experience in the general population [8]. Following trauma, intrusive memories may contain vivid sensory impressions [9], such as visual images, sounds, smells, or bodily sensations [10] and may comprise the most distressing moments of a traumatic event [9]. For most people, intrusions following trauma tend to dissipate over weeks and months and become less distressing over time [4], although in those who develop PTSD, intrusions continue to be difficult to control, repetitive and distressing [9]. Intrusive memories occurring in the context of PTSD, relative to those that dissipate over time, are associated with a sense of ‘nowness’ when experiencing an intrusion and having a broad range of cues triggering them [11]. They may also be fragmented or disconnected from contextual information [12] and other autobiographical memories [13]. Consequently, one aim of psychotherapeutic interventions is to facilitate integration of the trauma memory into an individuals’ existing network of autobiographical memories (i.e., the memories of our own individual history [14]). This integration, in turn, is thought to reduce intrusiveness of the trauma memory [12].

Models of Intrusive Memories in PTSD

As intrusive memories are a hallmark symptom of PTSD, memory is at the centre of cognitive models of PTSD [9]. Prominent models of PTSD postulate a lack of integration of the trauma memory into existing autobiographical memories as a key factor in the development of intrusive memories. There are several models describing the emergence of PTSD, however here we will focus on three models specifically accounting for the emergence and maintenance of intrusive memories. One seminal model informing treatment for PTSD, Emotional Processing Theory [15,16,17], proposes the trauma memory is inadequately processed due to high levels of distress. This results in a trauma memory network separate from other memory systems which is activated by a variety of stimuli associated with the trauma [18]. An aim of treatment, therefore, is to activate this memory network and integrate new information into the trauma memory (e.g. during exposure therapy, integrating new information that is inconsistent with the individual’s expectations of harm) [15, 19, 20].

The Dual Representation Theory [21, 22] proposes two independent memory systems form during an experience. These include sensory representations (e.g. visual images, sounds) and contextual representations of the experience (e.g. relevant information about time or place). Encoding of a non-traumatic event involves the creation of both sensory and contextual representations. For such events, vivid sensory representations will decay quickly. In contrast, during an experience of trauma, stress is believed to enhance the encoding of sensory information via potentiation of amygdala functioning and impaired hippocampal functioning. Due to this enhanced encoding of sensory representations, and therefore retention of high sensory detail, involuntary intrusions containing this detail are more readily cued by situational factors (internal, such as feelings and external, such as smells or sounds) and continue to have less reference to contextual representations and connections with autobiographical and semantic memory. This in turn may account for these memories having a sense of ‘nowness’ [22].

The cognitive model of PTSD [11] postulates inadequate integration of the trauma memory into existing autobiographical knowledge systems [23] contributes to producing a sense of current threat, which maintains PTSD [4]. This leads to increased perceptual priming [24] and cueing of trauma memories from a wider range of situations [11]. Like the Dual Representation Theory, the ‘nowness’ of intrusions is accounted for by a lack of integration of the trauma memory with other autobiographical memories [11]. An individual with PTSD may, therefore, find it difficult to experience the trauma memory as having occurred in the past, rather than as an experience occurring in the present [25•]. The combination of current sense of threat, increased cueing of intrusive memories and associated distress may perpetuate limited access to other contextual parts of the memory, possibly accounting for why intrusions persist even if the individual has learned or obtained important contextual information after the trauma [4, 11].

In summary, each PTSD model considers the trauma memory to be partly maintained by a lack of integration into autobiographical memory. This lack of integration is further amplified by maladaptive cognitive (i.e. attempts to suppress) and behavioural (i.e. avoidance) strategies in which an individual engages while attempting to alleviate their distress [11]. Thus, the presence of distressing intrusive memories leads to a pattern of mutually reinforcing symptoms in PTSD. These theories have been influential in informing evidence-based interventions for PTSD, with the consolidation and integration of the trauma memory being a key target in treatment [12]. Targeting the trauma memory in PTSD interventions results in the inclusion of important contextual and semantic information when deliberately recalling the trauma memory [9, 12]. This integration is suggested to enhance the ability to distinguish the trauma memory from future trauma-related situations or stimuli [26] possibly reducing overgeneralisation of the trauma memory [27•].

Sleep Disturbance and PTSD

Sleep disturbance is conceptualised as both a symptom of PTSD and a comorbid disorder [28]. There is substantial evidence demonstrating a relationship between poor sleep and different stages of PTSD [29]. Poor sleep prior to trauma is an identified predictor of PTSD [30, 31]. For example, within a military cohort, short sleepers (< 6 h sleep per night) and those with insomnia prior to deployment were at increased risk for developing PTSD post-deployment [32]. This relationship appears to be bidirectional with insomnia symptoms in the aftermath of trauma also linked to the later development of PTSD [33].

Individuals with active PTSD experience a higher level of disordered sleep [34], including having more fragmented [35], lighter [36], and more variable sleep [37] than the general population. Indeed, up to 90% of patients with PTSD report such sleep disturbances [38]. More pronounced sleep disturbances also predict poorer functioning post-treatment [39]. Additionally, as the previous nights’ sleep predicts severity of post-traumatic symptoms the following day [40], chronic sleep disturbances may maintain PTSD symptoms over time [33]. Given this evidence of a relationship between sleep problems and development and maintenance of PTSD, sleep is now viewed as a comorbid condition, rather than purely a secondary symptom [2, 28].

Sleep’s role as a predictive mechanism of PTSD is yet to be fully elucidated. However, one reason sleep is so strongly related to PTSD may be related to sleep’s role in the consolidation of newly acquired information [5]. For example, there is strong evidence sleep plays a role in development and maintenance of both safety and fear extinction memories [41,42,43]. Relevant for intrusive memories in PTSD, sleep also plays a critical role in the processing and storage of emotional information [44,45,46]. As the presence of persistent and distressing intrusive memories in PTSD is considered to be a disorder of memory, the role of sleep in emotional memory consolidation may point to a causal role for sleep in the development of intrusive memories in PTSD.

Sleep and Traumatic Memory Consolidation

Role for Sleep in Memory Consolidation

It is well known sleep plays an important role in memory consolidation [47]. Memory consolidation is the transformation of recent unstable memories into more stable, persistent memories strengthened and integrated into an existing network of long-term memory [48]. New information is encoded (and retrieved) during wake, whereas sleep appears optimal for consolidation of memories due to reduced processing of external stimuli [49]. A two-stage memory system provides an explanation for how a neuronal network can retain older information in the context of continuously arising new information and memories [50]. Initially, memories are stored in such a way that allows quick encoding, forming a temporary memory trace via the hippocampus. Then, memories are gradually consolidated into long-term storage within the neocortex via repeated reactivation occurring across periods of sleep [49].

In addition to memory in general, sleep is suggested to have specific effects on the consolidation of emotional memories. The ‘sleep to forget, sleep to remember’ hypothesis developed by Walker and van der Helm [51] proposes sleep facilitates the decoupling of affect from memory. The potential mechanism is suggested to occur primarily over periods of REM sleep, where memories are reactivated during a state of reduced physiological arousal [51, 52]. Thus, emotional distress associated with memories may be maintained if sleep is disrupted [53]. However, evidence for sleep reducing emotional tone is mixed, with some research demonstrating opposing results, whereby sleep seemingly strengthens affect associated with a memory [54]. See Davidson and Pace-Schott [52] for a comprehensive review on sleep, emotional tone, and intrusiveness of emotional memories. Currently, there is no clear explanation for this conflicting evidence regarding sleep’s effect on emotional memories.

Sleep and Intrusive Memories

As outlined above, prominent PTSD models hypothesise disordered encoding and consolidation of the trauma memory contribute to the development of intrusive memories. As memory consolidation is a core sleep function, it makes sense to investigate sleep’s role in development of intrusive trauma-related memories. Recent studies utilising a trauma film paradigm have suggested sleep disturbance may play an important role in the development of intrusive memories [55••]. The trauma film paradigm has been used as an analogue of trauma and is a well-established paradigm for studying intrusive memories [56]. More recently, researchers have employed this paradigm to study the role of sleep in the development of intrusive memories. In these studies, participants view a distressing film and are allocated to either a sleep or control (e.g. daytime wake, total or partial sleep deprivation) condition following the film. Participants then report on film-related intrusions and associated distress for up to seven days [57]. This is done using an intrusive memory diary, either a pen and paper [58] or an electronic version [27•]. Participants report the number of intrusive memories and provide details of the content of the intrusion (so this can be matched to the film) as well as the level of distress elicited by the intrusive memory (e.g. 0 ‘not at all’ to 10 ‘extremely’) [58]. While the use of this paradigm for investigating the role of sleep in the development of intrusions is relatively new, there was some initial inconsistency regarding the direction of the effect. For example, an early study suggested sleep deprivation after analogue trauma reduced intrusive memories [58], while several later studies showed sleep deprivation increased intrusive memories [12, 27•, 59]. Three meta-analyses of studies investigating the role of sleep in the development of intrusive memories have now been published, providing some consensus on this relationship [55••, 60••, 61••].

In their meta-analysis, Davidson and Marcusson-Clavertz [55••] included six experimental studies comparing sleep and wake groups, measuring intrusions via daily diaries. They found sleep reduces the number of intrusions up to a week after analogue trauma, albeit with a small effect size (Hedges’ g =-0.26). There was no significant difference between groups for distress associated with intrusions. Larson et al. [60••] included eight studies in their meta-analysis, including studies measuring intrusions via diaries and/or intrusion triggering tasks (where intrusions are elicited following exposure to fragments of the trauma film). They also concluded sleep reduces intrusion frequency following analogue trauma (Hedges’ g = 0.29), but not distress associated with intrusions. A third meta-analysis reviewed nine studies examining the role of sleep in intrusive memory development, combining individual participant data (for eight of the reviewed studies) due to low number of studies [61••]. In agreement with the conclusions made by both previously published meta-analyses, this review also found sleep supported a reduced number of intrusions following analogue trauma, with a small effect size (log-transformed ratio of means = 0.25) [61••]. Further narrative synthesis of the effect of sleep on trauma memory found some evidence sleep also enhanced explicit trauma memory (e.g. accurate recognition of trauma stimuli). A narrative synthesis of the relationship between sleep physiology (e.g. SWS, REM) and intrusions yielded mixed results [61••], as found in another recent review [52]. Although, as exposure to analogue trauma alters sleep architecture [62], it may be difficult to disentangle the effect of the event on an individual’s sleep from the effect of sleep on intrusive memories without experimental manipulation of sleep stages [52]. Overall, across all three meta-analyses, whilst there was variation in study design and methodology, each review found small effect sizes for sleep reducing the number of intrusive memories. However, sleep following viewing the trauma film did not reduce distress associated with intrusions compared to participants who had remained awake.

Examining neural correlates has also provided further insight into the relationship between sleep and intrusive memories. When exposed to trauma-related stimuli, individuals with PTSD have increased activation of posterior cortical mid-line regions such as the precuneus and retrosplenial cortex [63]. Of note, midline areas are thought to be involved in autobiographical memory and self-referential processing [63, 64] and are also implicated in the retrieval of trauma-related memories in healthy populations [24] (see Sartory et al. [63], for a meta-analysis of functional neuroimaging studies investigating re-experiencing symptoms). A recent study used the trauma film paradigm to investigate the neural correlates of sleep on processing of traumatic memories [25•]. Participants viewed a trauma or neutral film, either napped or remained awake, and then completed an implicit memory task (which involved presentation of film stills during a working memory task) during functional magnetic resonance imaging. Consistent with other trauma paradigm research [59], participants who napped following viewing the trauma film reported fewer intrusions across the week compared those who stayed awake. During the implicit memory tasks, there was increased activation in the anterior and posterior cingulate cortex, retrosplenial cortex and precuneus, for those watching the trauma film compared to control groups who watched neutral films. However, this increased activation was only present in the wake group. Thus, sleep, compared to wake, appeared to reduce activation when exposed to reminders of an analogue trauma [25•] in a network very similar to the one showing increased activation in PTSD vs controls [63]. In reference to theories of intrusive memory development, such as the Dual Representation Theory [21, 22] and the Cognitive Model of PTSD [11], the authors concluded sleep potentially facilitated integration of analogue trauma memory into existing memory networks, which led to the reduced activation in specific areas of the brain when participants were exposed to trauma-related stimuli [25•].

How do these Results Align with Clinical Samples?

An important consideration is how well the results of trauma film studies can be generalised to individuals experiencing intrusive memories following actual trauma. Larson et al. [60••] noted that whilst the results of their meta-analysis pertain to analogue trauma, they are consistent with findings showing sleep disturbances are highly associated with development of PTSD symptoms, including intrusive memories [65]. For instance, self-reported sleep disturbances in veterans prior to deployment have been observed to predict PTSD diagnosis three to six months [66] and two years post-deployment [53]. Sleep disturbance early after trauma also predicts both development and severity of PTSD [53, 67]. Regarding intrusive memories specifically, there is limited research [30, 68]. However, Luik et al. [65] found a relationship between sleep disturbance and intrusive memories in the week after experiencing or witnessing a motor vehicle accident. Many years after trauma exposure, disturbed sleep the previous night is still associated with more intrusive memories the following day [68]. The relationship is also observed in the other direction, with intrusive memories affecting sleep onset and maintenance [69], pointing to a bidirectional relationship between sleep and intrusive memories. Overall, combining findings of experimental trauma film paradigm studies and research examining clinical populations, healthy sleep after trauma appears to be beneficial for reducing the number of intrusive memories. In PTSD though, intrusions are both repetitive and distressing [3, 9], yet findings from trauma film studies demonstrate that distress associated with intrusions does not differ between sleep and wake groups [27•, 59]. It is unknown whether this is due to the low level of distress elicited by the trauma film paradigm or because sleep does not reduce distress associated with the trauma memory.

How do Trauma Film Results Fit with Current Models of Intrusive Memories in PTSD and Emotional Memory Consolidation over Periods of Sleep?

The mechanism by which sleep reduces intrusive memories remains unknown. Several studies argue the main finding of reduced intrusions is due to memory consolidation over a period of sleep [12, 27•, 70, 71]. This conclusion aligns with models of intrusive memory development in PTSD, which propose consolidation of the trauma memory into autobiographical memory networks reduces intrusive memories [11, 21, 22]. Integration of the trauma memory is also thought to be indicated by enhanced explicit memory, such as the incorporation of updated information into the voluntary recall of trauma memory [12] and improved ability to distinguish between experienced trauma stimuli and similar (new) trauma stimuli [26, 27•]. Sleep enhancing explicit memory of analogue trauma was partially supported in the narrative synthesis by Schäfer et al. [61••]. However, that evidence should be interpreted with caution as explicit memory tasks and timing of memory assessment differed across the individual studies [27•, 70,71,72].

Nap studies also provide evidence for consolidation as the mechanism behind reduced intrusive memories after sleep, where 60 – 90-min naps, as opposed to wake, resulted in reduced intrusions across the week [25•, 59]. Thus, even a brief period of sleep may be sufficient for consolidation processes to occur [59]. This benefit of naps for reducing intrusive memories also aligns with the theory that sleep provides a critical time window for consolidation to occur [27•, 49, 55••] and is consistent with research investigating non-traumatic memory consolidation over periods of sleep [73,74,75,76,77]. Consensus on whether naps enhance explicit trauma memory in addition to reducing intrusive memories would further strengthen this consolidation account.

The main finding of reduced number of intrusions after sleep, but not reduced distress associated with intrusions, does not appear to fit with the “sleep to forget, sleep to remember” hypothesis. Thus, sleep’s role in reducing number of intrusive memories may not be due to an emotion regulation effect of sleep per se, or a decoupling of emotion from the memory [52]. Instead, this may be an outcome of adequate consolidation over a period of sleep. However, consolidation and attenuation of affect may not necessarily be separate mechanisms or may be outcomes of the same mechanism occurring over multiple periods of sleep. One limitation of this line of work impacting our ability to fully understand sleep-related mechanisms underlying intrusive memory, relates to external validity. The trauma film paradigm does not typically elicit a significant level of distress. Thus, there may not be a strong enough emotional component to the memory to require ‘decoupling’ during sleep. If true, that might explain why sleep has not been associated with a decrease in distress associated with analogue trauma-related intrusions. Alternatively, whether a separate process or an outcome of improved consolidation over periods of sleep, reduced distress related to intrusions may simply take longer to emerge than current studies have examined [25•, 78].

Finally, it has also been proposed that sleep disturbances may influence disruptive spontaneous cognition (e.g. mind wandering), which in turn accounts for the involuntary intrusion of trauma memories into awareness [55••, 79]. Mind wandering occurs when instead of being focused on task relevant demands, attention is captured by internal stream of thought [80]. Increased mind wandering has been observed following both self-reported poor sleep [81] and experimental sleep deprivation [55••, 82] and may occur via sleep’s effect on reduced executive control [79]. See Cárdenas-Egúsquiza and Berntsen [79] for a comprehensive review of the relationship between sleep and spontaneous cognition. Spontaneous cognition not only involves task unrelated thoughts, but also autobiographical remembering [83], which may include traumatic memories intruding into awareness. From the perspective of the Dual Representation Theory [9], intrusions are more readily cued by situational factors due to enhanced encoding of sensory information during trauma and corresponding impaired consolidation into autobiographical memory. However, a reduced top-down executive control over these sensory representations might also increase the likelihood of their intrusion, possibly exacerbated by sleep deprivation.

It is clear sleep influences the number of thoughts arising in awareness [81] and given sleep’s role in memory consolidation, clearly sleep also plays a role in consolidating memory of traumatic experiences. Thus, both processes may be important for development and maintenance of intrusions, whether at the same or different stages. For example, the relationship between sleep-dependent consolidation and intrusive memories may be most important in early consolidation (e.g. in the first 24 h) but become less important over successive periods of sleep. Similarly, perhaps an increase in spontaneous cognition (including intrusive memories) due to persistent sleep disturbance becomes particularly important in the maintenance of intrusive memories [68].

Future Directions

There are several challenges for future research investigating the mechanisms explaining the relationship between sleep and intrusive trauma-related memory development and maintenance. As mentioned previously, it may be difficult (and unethical) for the trauma film paradigm to generate a high enough level of distress to explore how sleep might modulate this. This is important as intrusive memories in PTSD are both intrusive and distressing [84] and lead to avoidance of memories or reminders that might elicit them [3]. Davidson and Marcusson-Clavertz [55••] suggested use of physiological measures of arousal may rule out issues with self-report, particularly if distress elicited in analogue trauma associated intrusions is low [55••]. Second, experimental manipulation of sleep stages is necessary to disentangle the effects of (analogue) trauma on sleep from the effect of sleep on trauma memory processing [52]. Certain stages of sleep are thought to have differing roles in emotional memory processing [85, 86] and PTSD patients have certain patterns of deficits in sleep architecture [18], including REM sleep abnormalities [87]. Understanding the relationships of these specific features and stages of sleep to intrusive memory may help to explain both development and maintenance of intrusive memories in PTSD, adding to theories driving clinical treatment. This may be particularly important for cohorts likely to experience both trauma and sleep disturbance (e.g. first responders) [2].

Third, investigating the role of sleep at different stages of emotional or traumatic memory processing (e.g. prior to encoding, early and extended consolidation) [88], might help to disentangle differing accounts of intrusive memory development. Fourth, neurophysiology and neuroimaging findings may further bridge the fields of sleep and trauma memory research in explaining intrusive memory development. Further research should endeavour to link altered neural activation, sleep physiology and multiple behavioural outcomes beyond number of intrusions (e.g. recall and distinguishing between trauma and trauma-related stimuli). Finally, whilst it is not possible to examine sleep’s role in the development of intrusive memories in those with PTSD (as they are already experiencing intrusive memories), further examining sleep and the relationship with intrusive memories on a day-to-day basis in clinical populations is needed.

Conclusions

Sleep disturbance has a modulating effect on symptoms of PTSD and may have a causal role in the development of intrusive memories. Despite some earlier inconsistencies, meta-analytic results and theoretical considerations from the PTSD literature argue sleep deprivation is unlikely to be beneficial in the aftermath of trauma. Whilst sleep is associated with reduced intrusions following analogue trauma, the mechanisms explaining this relationship are yet to be elucidated. Future studies should attempt to disentangle to what degree consolidation, executive control over spontaneous cognition, or other mechanisms are affected by sleep and contribute to development of intrusive memories. Examining this at different temporal stages of PTSD may further elucidate the role of different mechanisms. As sleep is not one uniform process, another aim of future studies should involve experimentally manipulating sleep stages, as deficits seen in different sleep stages may have specific effects on experience of intrusive memories. Relationships between sleep architecture and intrusive memories in clinical populations also warrants investigation to increase external validity. Given the small number of studies examining the role of sleep in intrusive memory development, pre-registering experimental studies and meta-analyses is also needed to reduce risk of bias. Ultimately, further experimental work including those investigating the mechanism(s) explaining the relationship between sleep and intrusive memories may open new avenues for intervention following trauma, both from the perspective of treating sleep disturbance and the potential to treat the underlying mechanisms of intrusive memories (e.g. executive control over spontaneous cognition).