Abstract
Memory of a traumatic event becomes consolidated within hours. Intrusive memories can then flash back repeatedly into the mind’s eye and cause distress. We investigated whether reconsolidation—the process during which memories become malleable when recalled—can be blocked using a cognitive task and whether such an approach can reduce these unbidden intrusions. We predicted that reconsolidation of a reactivated visual memory of experimental trauma could be disrupted by engaging in a visuospatial task that would compete for visual working memory resources. We showed that intrusive memories were virtually abolished by playing the computer game
Keywords
Psychological trauma is prevalent around the world (World Health Organization, 2013), from terrorist attacks to motor vehicle accidents. Most people will experience a traumatic event during their life. Some will develop “recurrent, involuntary and intrusive distressing memories of the traumatic event(s)” (
Effective mental-health interventions soon after trauma are lacking (Roberts, Kitchiner, Kenardy, & Bisson, 2010). Disaster-response aid can be mobilized 24 to 48 hr after an event (American Red Cross, 2010), but within the first 6 hr, emotional memories are already consolidated and change resistant (McGaugh, 2000). Procedures that could alter a consolidated trauma memory are critical for reducing posttraumatic symptoms. It is time to profit from advances in the science of memory to devise innovative psychological treatments (Holmes, Craske, & Graybiel, 2014).
People may wish to forget traumatic memories, but counterintuitively, they may benefit from recalling them under certain conditions—those which render them less intrusive. Reconsolidation is the process whereby reactivation of a previously consolidated memory renders it malleable, and restabilization is required for the memory to persist (Misanin, Miller, & Lewis, 1968; Nader, Schafe, & LeDoux, 2000). Memory changes when an intervention disrupts or enhances restabilization. For reconsolidation to occur, the memory must be reactivated via a retrieval cue (Merlo, Milton, Goozee, Theobald, & Everitt, 2014). While it is malleable, the reactivated memory can be updated—weakened or strengthened (or unchanged)—for example, by pharmacological agents. Intracranially delivered protein-synthesis inhibitors block reconsolidation and weaken fear memory in animals (Nader et al., 2000) but are toxic in humans. Studies in humans have used the beta-blocker propranolol to reduce physiological responses to conditioned fear cues in healthy volunteers (Kindt, Soeter, & Vervliet, 2009). Clinical findings are mixed, and translation to PTSD requires caution (Lonergan, Olivera-Figueroa, Pitman, & Brunet, 2013).
Various nonpharmacological techniques have been employed in experimental trials with humans. Electroconvulsive therapy has been used to disrupt reconsolidation of episodic memories (Kroes et al., 2014), although this sort of therapy is distressing. Memory extinction during reconsolidation has been used to reduce conditioned fear to picture cues (e.g., blue squares) in healthy participants with long-lasting effects (Schiller et al., 2010) and concomitant changes in amygdala activity (Ågren et al., 2012). However, it remains to be shown whether the frequency of intrusive memories of an experimental analogue of traumatic events can be reduced by targeting reconsolidation. This is important because intrusive memory (rather than deliberately recalled episodic memory) is central to clinical posttraumatic distress. Furthermore, it remains to be demonstrated that simple, noninvasive cognitive techniques might reduce intrusions. Such techniques could be readily administered in the aftermath of real trauma.
We predicted that engaging in a visuospatial task during memory reconsolidation would compete for working memory resources with visual imagery and interfere with the reconsolidation of intrusive memories. There are dual-task experiments indicating that when similar cognitive tasks compete for shared resources, they interfere with each other and thereby impede memory processing; for example, a visuospatial pattern-tapping task interfered with holding a visual mental image in mind (rendering it less vivid and emotional), whereas counting aloud did not (Baddeley & Andrade, 2000). Conversely, counting aloud had a detrimental effect on an auditory memory, whereas visuospatial tapping did not. Such a dual-task capacity limitation provides an advantage by which to limit resources allocated to maladaptive forms of cognition. Intrusive memories of trauma consist of mental images such as visual scenes from the event (Brewin, 2014), for example, the sight of a red car moments before a crash. Therefore, a visuospatial task performed when memory is labile (during consolidation or reconsolidation) should interfere with visual memory storage (as well as restorage) and reduce subsequent intrusions.
Concurrent tasks may interfere with each other, and such interference can influence their consolidation into memory. A task performed after an event may retroactively interfere with memory for that event (Wixted, 2004). Consistent with this hypothesis, previous studies have shown that visuospatial tasks, such as the computer game
We used the traumatic-film paradigm because it is a well-established prospective experimental tool for investigating intrusive-memory development (Holmes & Bourne, 2008; Horowitz, 1969). In this paradigm, which has been used to study intrusions in behavioral studies (e.g., Deeprose et al., 2012; Hagenaars & Arntz, 2012; Holmes et al., 2009; Holmes et al., 2010) and neuroimaging studies (Bourne, Mackay, & Holmes, 2013), participants are shown short films containing scenes depicting traumatic events. Such films reliably induce intrusions over the following week. Notably, a correlational study found that repeatedly viewing media related to the Boston Marathon bombing (6 hr or more daily) was associated with higher acute stress symptoms than direct exposure to that event (Holman, Garfin, & Silver, 2014). Prospective longitudinal data suggest that TV-related exposure to the events of September 11, 2001, was associated with posttraumatic stress symptoms over the following 3 years (Silver et al., 2013).
We hypothesized that 24 hr after experimental trauma-film exposure, a group that completed a reactivation task for memory of the film (to initiate reconsolidation) followed by
Experiment 1
In Experiment 1, we compared two experimental groups, predicting that a group that completed a memory-reactivation task plus
Method
Participants
Fifty-two participants (31 females, 21 males; age range = 18–51 years) were recruited from two local university campuses and from the general public via advertisements in an online newspaper and in the community. Sixty-five percent of participants were students, 21% were employed, and 14% were unemployed. Participants described their ethnicity as 52% White British, 19% White other, 12% Asian Indian, 4% Chinese, 4% Asian Pakistani, 2% Black African, 2% Black American, 2% Latin American, 2% White American, and 2% White Asian. For ethical considerations, the recruitment material gave information about the nature of the film, specifically, that it contained scenes of a traumatic or potentially distressing nature. All participants provided written informed consent prior to testing, were reminded that they could end the experiment at any point, and were reimbursed for their participation. Participants were required to complete all three lab sessions (on Days 0, 1, and 7) and keep the diary in between sessions. No participants had been involved previously in related studies. Ethical approval was obtained from the University of Oxford Central University Research Ethics Committee (reference number: MSD/IDREC/C1/2010/104).
Tasks and measures
Trauma film
The 12-min trauma film consisted of 11 different scenes involving actual or threatened death, as well as serious injury; the film functioned as an experimental analogue of viewing a traumatic event in real life (APA, 2013). Scenes contained different types of context; examples include a young girl hit by a car with blood dripping out of her ear, a man drowning in the sea, and a van hitting a teenage boy while he was using his mobile phone crossing the road. This film footage has been used in previous studies to evoke intrusive memories (e.g., Holmes et al., 2009; Holmes et al., 2010). The film was projected on a 100-cm × 133-cm screen using an NEC LT25 projector. Viewing distance was approximately 175 cm.
Memory-reactivation task
The memory-reactivation task had two components: (a) presentation of still film images then (b) a 10-min break with a standardized filler task. For the first part of the task, 11 static visual images, one from each of the scenes in the film were presented once each on a black background for 2 s using PowerPoint. Examples included a young girl sitting up at the side of the road (just before the moment in the film clip when she is hit by a car), a man from the torso up striding through the sea (just before the moment in the film where he drowns), and the face and shoulders of a teenage boy smiling at the camera (just before he replies to a text message while being hit by a van). Images were taken from a moment just prior to the worst part of a given scene (i.e., those which typically yield intrusive memories; cf. Michael & Ehlers, 2007).
The images were intended as reminder cues for the trauma film (though there was no explicit instruction to this effect, and there was no explicit instruction to deliberately recall the film). Images were projected with the same equipment and procedure as during film viewing. The images were presented in the same fixed order as the scenes had occurred in the film. Second, as part of the task, and to allow time for memory reconsolidation processes to be initiated, we provided a 10-min interval after the presentation of the images but before the blockade (
Tetris
In the PC game
Intrusion diary
Participants were given a pen-and-paper diary to record any intrusive memories of the film content for the first 24 hr (Day 0) and again for Days 1 to 7 (Holmes et al., 2004; Holmes et al., 2009). Participants were advised (both verbally and by written instructions in the diary) that intrusive memories were defined as scenes of the film that appeared spontaneously and unbidden in their mind. They were not to include memories that they deliberately recalled. Participants were also given instructions about the form of intrusive memories, that is mental images (e.g., “in the form of pictures in your mind’s eye”) rather than solely verbal thoughts in the form of words or phrases (only those with image-based content were scored). They were asked to describe the content of each of their intrusions in the diary (e.g., a silver car crushing couple against a wall) so that the experimenter could later confirm whether or not the intrusion related to the film. Each day of the diary was labeled and split into three sections (morning, afternoon, and evening), and participants were asked to mark in a box in the appropriate section when they experienced an intrusive memory (or to indicate that they had not), and then to write the content of the intrusion overleaf. They were asked to record all intrusions immediately and to set aside regular time slots to check that their diary was up to date each day. If participants had experienced no intrusions during any time period, they were asked to enter zero in the diary.
Intrusion-provocation task (IPT)
Stimuli for the IPT consisted of 11 blurred static visual images created using GIMP (Version 2.1.1; Free Software Foundation, 2010) software (Gaussian Blur set at 2.0). There was one image from each scene of the trauma film. The images were presented for 2 s each on a 17-in. color monitor on a white background; participants sat at a viewing distance of approximately 75 cm. Images were presented in a fixed random order. Immediately afterwards for the next 2 min, participants recorded any intrusive memories triggered of the film by pressing a button. Intrusive memories were defined as in the diary. The total frequency yielded the IPT intrusion score.
Recognition memory tests
The verbal recognition memory test comprised 32 true/false written statements relating to the 11 scenes in the trauma film. Examples included “Scene 1: The little girl has blood coming from one of her nostrils” and “Scene 7: A man swims out to retrieve an inflatable lilo [beach air mattress]” (Holmes et al., 2009; Holmes et al., 2010).
The visual recognition memory test consisted of 22 static visual images—11 were taken from throughout the film (1 per scene, different images from those used in the IPT), and 11 were unviewed images presented as filler. Images were presented individually for 5 s each. For both visual and verbal recognition memory tests, participants indicated yes or no (on paper) as to whether or not they recognized the image (visual recognition memory test) or written statement (verbal recognition memory test) as being from the film watched 8 days earlier.
Self-report questionnaires
Prior trauma history was reported using the Traumatic Experience Questionnaire (TEQ), a 12-item checklist adapted from the Criterion A list of the Posttraumatic Diagnostic Scale (Foa, 1995), as per previous studies (e.g., Holmes et al., 2010). Participants indicated whether or not they had experienced or witnessed each of a series of traumatic events. “Yes” answers were summed and could range from 0 (
Depressive symptomatology was measured using the second edition of the Beck Depression Inventory (BDI-II; Beck, Steer, & Brown, 1996). The BDI-II is a 21-item self-report measure. Each item is measured on a scale from 0 to 3, with total scores ranging from 0 to 63; higher scores indicate greater levels of depression. The BDI-II has high internal consistency in clinical outpatients (α = .92) and student samples (α = .93; Beck et al., 1996).
Trait anxiety was measured using the trait scale of the Spielberger State-Trait Anxiety Inventory (STAI-T; Spielberger, Gorsuch, Lushene, Vagg, & Jacobs, 1983). The STAI-T is a 20-item self-report measure. Each item is rated on a 4-point scale, with scores range from 20 to 80; higher scores represent greater levels of trait anxiety.
Participants also completed the Intrusion subscale of the Impact of Event Scale—Revised (IES-R; Weiss & Marmer, 1997) as an additional exploratory measure. Participants responded to eight items in reference to the film (e.g., “Pictures about
Procedure
The experiment involved three laboratory sessions as well as the completion of a pen-and-paper diary at home to record the daily frequency of intrusive memories (both over 24 hr and then for an additional 7 days). The first laboratory session (Day 0) consisted of film viewing, and in the second session (Day 1), participants were assigned to experimental groups. The two sessions were conducted 24 hr apart to within 2 hr of the original testing time. The third experimental session occurred 7 days later, also to within 2 hr of the original testing time (Day 7).
On Day 0, participants provided written informed consent then completed information on their age, gender, occupation, and ethnicity, as well as the BDI-II, STAI-T, and TEQ. All participants were then asked to practice playing
Next, participants watched the trauma film alone in a darkened room. They were asked to pay close attention and to “imagine you are there, as a bystander at the scene.” Participants rated how sad, hopeless, depressed, fearful, horrified, and anxious they felt “right at this very moment” on six visual-analogue scales given both before and after the film. Ratings were made on scales from “
Immediately prior to their return to the laboratory for the second session, participants were randomly allocated to two groups (reactivation-plus-
All participants were then reminded of the instructions for keeping the diary and were asked to keep the diary daily for a further 7 days. Seven days later (on Day 7), participants returned to the laboratory for the third and final session with their completed diary. In this session, they completed the IPT. They also rated how accurately they had completed their diary (diary compliance) from 1 (
Statistical analysis
On the basis of a between-groups effect size of
To investigate the time-course of intrusions, we ran a repeated measures analysis of covariance (ANCOVA) followed by nonlinear time-series analysis. Counts of the number of intrusive memories for each participant (
where
Results
Groups were equivalent at baseline for age and gender, as well as self-report-questionnaire scores for trait anxiety, depression, and trauma history. Mood deterioration during film viewing, self-reported postfilm distress, attention to the film, demand ratings, and diary compliance also did not differ significantly between groups (see the Supplemental Material).
Intrusive memories preintervention
As expected, prior to the intervention (at baseline: Day 0), we confirmed that the two groups experienced a similar number of intrusive memories of the film in daily life,

Results from Experiment 1: mean number of intrusive memories recorded in the diary during the first 24 hr following viewing of the experimental trauma film (i.e., preintervention; a), mean number of intrusive memories recorded in the diary totaled over the 7-day period after the intervention (b), and mean score on the intrusion-provocation task on Day 7 (c). In each graph, results are shown separately for the two groups. Asterisks indicate a significant difference between groups (**
Intrusive memories postintervention
Critically and as predicted, after the intervention (Days 1–7; Fig. 1b), participants in the reactivation-plus-
Time course of intrusions
To illustrate the trajectory of intrusive memories over time, we conducted a nonlinear time-series analysis using generalized additive models. The number of intrusive memories declined faster in the reactivation-plus-

Results from Experiment 1: frequency scatter plots showing the time course of the mean number of intrusive memories reported in the diary daily from Day 0 (prior to intervention) to Day 7, separately for the two groups. Note that the intervention was on Day 1. The solid lines are the results of a generalized additive model (see Equation 1). The size of the bubbles represents the number of participants who reported the indicated number of intrusive memories on that particular day.

Results of the time-series analysis in Experiment 1: Poisson distribution of the predicted likelihood of intrusive memories in the no-task control group (top row) and the reactivation-plus-
Recognition memory
As expected on the basis of previous studies,
Discussion
There were fewer intrusive memories of the trauma film in the reactivation-plus-
Experiment 2
In Experiment 2, we compared four experimental groups. Two of the groups replicated those in Experiment 1: the reactivation-plus-
The procedure in Experiment 1 was repeated, with two additions: a
Method
Participants
Seventy-two participants (47 females, 25 males; age range = 18–62 years) were recruited using the same methodology as in Experiment 1. Sixty-four percent of participants were students, 26% were employed, 7% were unemployed, and 3% were retired. Participants described their ethnicity as 57% White British, 22% White other, 4% other mixed background, 4% Chinese, 3% mixed White and Black Caribbean, 3% mixed White and Black African, 3% Black African, 1% Mixed White and Asian, 1% Indian, and 1% other Asian background. Ethical approval was obtained from the University of Oxford Central University Research Ethics Committee (reference number: MSD/IDREC/C1/2010/104).
Procedure
The first two groups were identical to those in Experiment 1; reactivation-plus-
Statistical analysis
On the basis of the effect size of
One-way ANOVAs followed by planned comparisons were undertaken for intrusive-memory frequency across Days 1 to 7 (equal variances not assumed) and IPT intrusion score. Gender was analyzed between groups using a chi-square test. To assess mood deterioration resulting from viewing the trauma film, we conducted a two-way repeated measures ANOVA with main factors of time (pre- vs. postfilm) and group (reactivation-plus-
Results
Groups were matched at baseline for age and gender, as well as self-report-questionnaire scores for trait anxiety, depression, and trauma history. Mood deterioration during film viewing, postfilm distress, attention to the film, demand ratings, and diary compliance were also matched (see the Supplemental Material).
Intrusive memories preintervention
First, prior to the intervention (over the first 24 hr after viewing the film: Day 0), we confirmed that the four groups experienced a similar number of intrusive memories,

Results from Experiment 2: mean number of intrusive memories recorded in the diary during the first 24 hr following viewing of the experimental trauma film (i.e., preintervention; a), mean number of intrusive memories recorded in the diary across totaled over the 7-day period after the intervention (b), and mean score on the intrusion-provocation task on Day 7 (c). In each graph, results are shown separately for the four groups. Asterisks indicate that results for the reactivation-plus-
Intrusive memories postintervention
Second, and critically, for the 7-day diary postintervention, there was a significant difference between groups in overall intrusion frequency in daily life,
Third, a similar pattern was seen on a convergent measure—the frequency of IPT intrusions on Day 7 in the laboratory, for which there was an overall significant difference between groups,
Time course of intrusions
The trajectory of intrusive memories over time declined faster in the reactivation-plus-

Results from Experiment 2: frequency scatter plots showing the time course of the number of intrusive memories reported in the diary daily from Day 0 (prior to intervention) to Day 7, separately for the four groups. Note that the intervention was on Day 1. The solid lines show the results of a generalized additive model in which the three control groups (no-task control,
From nonlinear time-series analysis, expected Poisson distributions revealed that by Day 2 (24 hr after intervention), the expected probabilities of no intrusive memories for participants in the reactivation-plus-

Results of the time-series analysis in Experiment 2: Poisson distribution of the predicted likelihood of intrusive memories in the combined control group (no-task control,
Recognition memory
Finally, as predicted, there was no significant difference among groups on the tests of either visual,
General Discussion
Overall, the results of the present experiments indicate that the frequency of intrusive memories induced by experimental trauma can be reduced by disrupting reconsolidation via a competing cognitive-task procedure, even for established memories (here, events viewed 24 hours previously). That is, a group that performed a task to reactivate an already consolidated memory of a trauma film (to initiate reconsolidation) 24 hr after film exposure, combined with
Our procedure modified intrusion frequency while leaving recognition memory intact, which indicates that trauma-film memory had not been erased but ceased intruding involuntarily. Although consistent with clinical models (Brewin, 2014), the dissociation between intrusions and recognition is contrary to traditional memory models (e.g., Tulving, 2002)—a paradox requiring future research. Perhaps counterintuitively, it is not people’s ability to deliberately remember trauma (episodic memory) but intrusive memories that are the key problem in PTSD. Deliberate recall is important for legal testimony, autobiographical memory, and future safety.
A limitation of this study is that we used a trauma film as an experimental model for trauma and intrusion development. The film content was of events involving actual or threatened death and serious injury (APA, 2013), though this film viewing itself did not meet criteria for a traumatic event. The
From Marcel Proust’s example of sudden childhood recall after eating a madeleine to flashbacks depicted in war films, involuntary memory has long held fascination. The current work bridges a clinical area of public concern (trauma viewing) with animal and human neuroscience. Reconsolidation offers a mechanism through which memory can be modified (strengthened or weakened) and here harnessed to stem the course of emotional intrusions. Understanding cognitive mechanisms underlying intrusive-memory amelioration may help generate more widely available mental-health treatments (Kazdin, 2007). Results also stimulate challenges to traditional models of memory.
This research is the first to investigate the disruption of involuntary memory for emotional events within a reconsolidation framework, using a cognitive procedure. We propose that after memory reactivation, a visuospatial cognitive task (
Footnotes
Acknowledgements
We thank the British Film Institute National Archives, LyleBailie International, Kino International, and David Large at the Royal College of Surgeons of Edinburgh for use of film clips. We also thank Barry Everitt, Bob Carlyon, and Rik Henson for helpful comments and Peter Watson for statistical help.
Declaration of Conflicting Interests
The authors declared that they had no conflicts of interest with respect to their authorship or the publication of this article.
Funding
E. A. Holmes, L. Hoppitt, and E. L. James are supported by the United Kingdom Medical Research Council (MRC-A060-5PR50); E. A. Holmes received further awards from a Wellcome Trust Clinical Fellowship (WT088217) and National Institute for Health Research Oxford Biomedical Research Centre Programme; E. L. James was supported by the Colt Foundation; and E. M. Tunbridge was supported by a Royal Society University Research Fellowship. Funding to pay the Open Access publication charges for this article was provided by the United Kingdom Medical Research Council.
Open Practices
Key data and materials have been made publicly available via Open Science Framework and can be accessed at osf.io/ideta. The complete Open Practices Disclosure for this article can be found at http://pss.sagepub.com/content/by/supplemental-data. This article has received badges for Open Data and Open Materials. More information about the Open Practices badges can be found at https://osf.io/tvyxz/wiki/1.%20View%20the%20Badges/ and
.
References
Supplementary Material
Please find the following supplemental material available below.
For Open Access articles published under a Creative Commons License, all supplemental material carries the same license as the article it is associated with.
For non-Open Access articles published, all supplemental material carries a non-exclusive license, and permission requests for re-use of supplemental material or any part of supplemental material shall be sent directly to the copyright owner as specified in the copyright notice associated with the article.
