Intrusive memories are a hallmark of posttraumatic stress disorder (PTSD; American Psychiatric Association [APA], 1994) but little is known of what causes them. Previous research has suggested heart rate (HR) falls during the encoding of trauma stimuli that later return as intrusive memories (Holmes, Brewin, & Hennessy, 2004). The current study sought to replicate and extend this finding by distinguishing between images and thoughts, by assessing risk factors such as trait dissociation, and by investigating psychophysiological moderators of this effect.
Heart Rate as an Index of Response to Trauma
In studies of PTSD, HR has been used as an objective measure of reactions to trauma-related stimuli. Most studies have shown a positive association between PTSD severity and HR increases when trauma memories were involuntarily triggered by reminders (e.g., Adenauer, Catani, Keil, Aichinger, & Neuner, 2010; Ehlers et al., 2010; Hetzel-Riggin, 2010). However, studies investigating voluntary retrieval of trauma memory have found reduced HR response among PTSD patients relative to trauma survivors without PTSD (e.g., Halligan, Michael, Wilhelm, Clark, & Ehlers, 2006). Cognitive characteristics commonly seen in PTSD patients such as dissociation and rumination have been related to the above findings of physiological inhibition (e.g., Halligan et al., 2006; Hetzel-Riggin, 2010; Koopman et al., 2004). For example, in a study involving rape victims (Griffin, Resick, & Mechanic, 1997), lower HR during verbal recollection of the trauma was found among individuals with high, compared to those with low peritraumatic dissociation. These results indicated the existence of important individual differences in the psychological and physiological reactions to trauma-related stimuli.
Additionally, HR has been investigated at time points close to traumatic accidents. Studies assessing HR at the time when victims arrived at hospital and onwards (e.g., before discharge) have found associations between higher HR and greater posttraumatic symptoms afterwards (e.g., Bryant, Creamer, O'Donnell, Silove, & McFarlane, 2008; De Young, Kenardy, & Spence, 2007; Kraemer, Mörgeli, Roth, Hepp, & Schnyder, 2008). However, when HR was examined at time points closer to the accidents (e.g., at the accident sites or during ambulance transport), victims later developing more severe PTSD symptoms have sometimes been found to have lower HR (Blanchard, Hickling, Galovski, & Veazey, 2002; O'Donnell, Creamer, Elliott, & Bryant, 2007; for nonsignificant findings, see also Buckley et al., 2004; Ostrowski, Christopher, & Delahanty, 2007). In sum, there is evidence to suggest that the relationship between HR and PTSD may be different at the time when trauma is encoded versus subsequently.
To model the processes underlying the encoding of trauma memories and better control for variability, the trauma film paradigm (reviewed by Holmes & Bourne, 2008) has been widely adopted with healthy volunteers. A previous study (Holmes et al., 2004) adopting this paradigm has found decreases in HR during film viewing, with a greater reduction associated with an increased number of subsequent intrusive images of the film. Moreover, the mean HR during the film sequences matching the contents of intrusions was found to be significantly lower than the sequences that did not intrude. The HR reduction was linked with fear bradycardia and freezing response commonly found in animals in the face of overwhelming threats. However, an alternative explanation of the HR reduction, increased orienting (Adenauer et al., 2010; Sokolov, 1960; Turpin, 1979), has not been ruled out. The current study sought to investigate in more detail the relationship between dissociation, HR, and intrusive memories.
Dual Representation Theory of PTSD
Differences have been proposed between the cognitive mechanisms involved in a resilient versus a pathological memory process. According to the dual representation theory (DRT) of PTSD (Brewin, Dalgleish, & Joseph, 1996; Brewin, Gregory, Lipton, & Burgess, 2010), traumatic events are encoded via two different pathways and give rise to two types of representations with different properties. First, contextualized representations (C-reps) involve focused attention and high-level cognitive processing supported by medial temporal lobe structures including the hippocampus. They contain viewpoint-independent contextual information and “gist” representations (e.g., when, where, how, who) of an event, which are crucial for the formation of episodic memory and abstract meanings. These properties also enable the trauma representations to integrate with personal semantic and autobiographical memory, making them available for verbal thoughts and appraisals. In contrast, sensory-bound representations (S-reps) are processed with the support of lower level sensory cortices. S-reps are viewpoint-dependent and inflexibly depictive of the original sensory details (e.g., images, sound, smell), physiological reactions (e.g., heart pounding, palm sweating), and feelings (e.g., fear, anger) occurring during the event. It is thought that in ordinary situations S-reps decay soon after the events. However, when formed under extreme levels of emotion, S-reps become enduring and intrusive sensory memories thus arise (Brewin et al., 2010).
Supporting the diverse memory representations and processes proposed in the DRT, a previous study (Hagenaars, Brewin, van Minnen, Holmes, & Hoogduin, 2010) has shown that the processes underlying intrusive sensory images are likely different to those underlying intrusive verbal thoughts. Despite being a form of intrusion, the semantic nature of intrusive thoughts suggests the involvement of higher-level cognitive functions and a more prominent involvement of C-reps (Hagenaars et al., 2010). Moreover, a study adopting the trauma film paradigm showed that participants focusing on sensory details during and after the film viewing reported more PTSD-like symptoms compared to those focusing on conceptual information and ideas (Kindt, van den Hout, Arntz, & Drost, 2008). Further, peritraumatic dissociation, which involves a reduction in consciousness, has been hypothesized to lead to weaker C-reps and to impede the normal integration of S-reps and C-reps (Brewin et al., 2010). Agreeing with this argument, peritraumatic dissociation has been found to impair memory performance (Brewin, Ma, & Colson, 2013; Brewin & Mersaditabari, 2013) and to reliably predict PTSD symptoms (Ozer, Best, Lipsey, & Weiss, 2003).
Startle Response and Stress Defense Styles
According to the defense cascade model (Bradley & Lang, 2000), the proximity of a threat elicits an orienting response characterized by cardiac deceleration and information gathering. At the second stage, an immediate threat may elicit an active defense (fight or flight), a reaction associated with the activation of the sympathetic nervous system and increased HR. However, when escape is perceived as impossible, a passive defense mode featured by physical deactivations such as freezing or bradycardia is more likely to be observed (Kaada, 1987).
In human studies, neurobiological characteristics associated with different stress defense behaviors and styles have been explored. For example, exaggerated startle is indicative of hyperexcitable fear circuits (Rosen & Schulkin, 1998; Vaidyanathan, Patrick, & Cuthbert, 2009) and has been observed in PTSD patients (e.g., Cuthbert et al., 2003; Ladwig et al., 2002). On the other hand, reduced startle has also been found among individuals with chronic exposure to trauma (Medina, Mejia, Schell, Dawson, & Margolin, 2001) and prolonged PTSD symptoms (Morgan & Grillon, 1998). A subgroup of PTSD patients with physiological suppression, instead of heightened reactivity, and a tendency to adopt passive stress coping behaviors has thus been suggested (Medina et al., 2001). The current study adopted the trauma film paradigm to examine the effect of individual difference in startle heart rate (sHR) response on the process and development of intrusive traumatic memory.
The Current Study
The current study included healthy adult participants and involved two types of HR measurement and two forms of memory assessment. The sHR response to an auditory startle trigger was assessed followed by examination of HR and psychological states before, during, and after viewing a trauma film. A diary was kept for 7 days to record intrusive memories of the film, and a recognition memory test was introduced after one week.
The first aim of the study was to examine the association between HR and the psychological and memory measures. Low absolute levels of HR have been found to predict the development of PTSD (Blanchard et al., 2002; O'Donnell et al., 2007) and to be associated with peritraumatic dissociation (Griffin et al., 1997). Therefore, we examined the relationships between absolute levels of HR, dissociation, and other psychological states at the memory encoding (perifilm) phase, predicting that lower HR would be correlated with higher dissociation. Additionally, following Holmes et al. (2004), we examined perifilm HR change relative to baseline, as well as during sequences of the film that later became intrusive compared to those that did not intrude. We predicted that greater decreases in both HR measures would be associated with more frequent intrusive memories. The vividness of these images was also assessed given its clinical importance. Further, considering the important theoretical differences between intrusions taking the form of abstract thoughts and sensory images (Hagenaars et al., 2010), and between processes underlying gist and detail memory (Adolphs, Tranel, & Buchanan, 2005), these were assessed separately.
Next, we investigated the role of an exaggerated or diminished startle response: first, whether individuals with different levels of sHR varied in pre-existing anxiety and dissociation levels, as well as in intrusive memories for the trauma film. Second, the role of sHR in the relationships between HR and different psychological responses was examined. As exaggerated startle has been suggested to indicate hyperexcitable fear circuits (Rosen & Schulkin, 1998; Vaidyanathan et al., 2009), individuals with a higher sHR response were predicted to have greater anxiety. In contrast, as a reduced startle response has been associated with passive defense (Medina et al., 2001), those with a diminished sHR response were predicted to have a greater tendency to dissociation. Their lower levels of HR during the trauma film were expected to be a sign of dissociation, and greater reductions in perifilm HR were expected to be predictive of the development of more involuntary memories of the film.