Neural and Behavioral Correlates of Peritraumatic Dissociation in an Acutely Traumatized Sample

Neural and Behavioral Correlates of Peritraumatic Dissociation in an Acutely Traumatized Sample

Judith K. Daniels, PhD; Nick J. Coupland, MD; Kathy M. Hegadoren, PhD; Brian H. Rowe, MD, MSc; Maria Densmore, BSc; Richard W. J. Neufeld, PhD; and Ruth A. Lanius, MD, PhD, FRCPC

Although many people experience traumatic events, only some subsequently develop posttraumatic stress disorder (PTSD). Previously, dissociative responses during the traumatic incident have been identified as a strong predictor of PTSD.1-3 This so-called peritraumatic dissociation typically comprises perceptual alterations, emotional detachment from one’s surroundings, and a loss of agency. Two complementary trajectories of the adverse effects of peritraumatic dissociation have been discussed (for a review, see Waelde et al4). It has been hypothesized that peritraumatic dissociation causes (1) alterations in memory formation during the traumatic event, which lead to intrusions,1,2 and (2) the persistence of dissociative reactions upon exposure to trauma cues after the traumatic event, which predicts PTSD development over and above peritraumatic dissociation.5

Peritraumatic Dissociation and Memory Formation

Etiologic theories of PTSD state that peritraumatic dissociation leads to alterations in memory encoding and storage, which in turn cause intrusions as well as partial amnesias typical for PTSD.1,2,6 Intrusions are considered a recall of memory fragments that lack temporal and spatial contextualization and carry a high load of sensory associations. Posttraumatic stress disorder severity is strongly correlated with distress associated with intrusions, lack of context, and the sense that the memories are being relived.7 These characteristics predict the severity of PTSD 6 months later over and above initial diagnostic status and appear to be related to the presence of PTSD rather than to be general characteristics of trauma memories. Different theorists have proposed dual-representation memory models that might be helpful in elucidating the underlying neurobiology of intrusive memory recall.1,8 These models assume that an event will be encoded both in a sensory format lacking a contextual framework and as autobiographical memories embedded in the continuous stream of personal memories. Conway8 proposed that intrusions constitute involuntary memory recall from an imagery-based memory system in the temporal-occipital region storing the sensory aspects of an event. In this view, peritraumatic dissociation may be the causal agent behind intrusions, as it is assumed that the integration into the autobiographical memory system is inhibited during dissociative processing.2

Persistent Dissociation Upon Exposure to Trauma Cues

Persistent dissociation is a common feature of chronic PTSD and typically consists of depersonalization, derealization, alterations in time sense, and analgesia.9,10 In persons who experienced acute dissociative responses to psychological trauma, persistent dissociation can be evoked by reminders of the original trauma and minor stressors.11 Recently, it has been proposed to differentiate a dissociative subtype of PTSD,12 as a subset of PTSD patients showing differential autonomic reactions13,14 and brain activation patterns during exposure to trauma cues15,16 has been identified. Typically, autonomic hypoarousal, instead of hyperarousal, is associated with dissociative reactions,17 which seems to interfere with emotional learning.18 This suggests that persistent dissociation might impair extinction learning and that highly dissociative patients may need therapeutic modules focusing on emotion regulation before being able to fully profit from standard, exposure-based psychotherapies.19

Childhood Abuse and Dissociation

Two meta-analyses20,21 identified prior traumatization as a major risk factor for the development of PTSD after an acute traumatic event during adulthood, and, in the National Comorbidity Survey, physical and sexual childhood abuse were uniquely related to adult PTSD.22 Repeated childhood sexual or physical abuse and emotional neglect have been associated with the development of dissociative symptoms,23,24 raising the question whether the relationship between childhood maltreatment and PTSD development is mediated by peritraumatic and persistent dissociation in acutely traumatized, adult subjects. Specifically, it is unknown whether the adverse effects of peritraumatic dissociation are predominantly due to the alterations in memory formation during the traumatic event or, alternatively, to the persistence of dissociative reactions upon exposure to trauma cues after the traumatic event.

• Peritraumatic dissociation is a risk factor for the development of posttraumatic stress disorder and can help to determine who is at risk and should thus be offered close monitoring or early interventions in the acute period following a traumatic event.
• Peritraumatic dissociation therefore constitutes an important marker that should be routinely assessed shortly after the traumatic event.
• Subjects who experience peritraumatic dissociation are most likely to exhibit persistent dissociation following the traumatic event and may therefore require treatment that focuses on a reduction of dissociative processing.

Neural Correlates of Dissociative Processing

Neuroimaging studies of dissociation occurring during the scan in PTSD have shown altered activation of brain regions implicated in arousal modulation and emotion regulation, especially the medial prefrontal cortex (Brodmann areas [BAs] 9 and 10), the anterior cingulate cortex (BAs 32 and 24), and the limbic system including the amygdala.15,16,25 Convergent with evidence that activation of the medial prefrontal cortex correlates negatively with amygdala activity during script-driven imagery,26 these studies suggest that the activation pattern during acute dissociation may be described as one of overmodulation12 of limbic activity.

Aims of the Study

The aim of this study was to clarify the mechanism by which peritraumatic dissociation is related to PTSD development and to explore the neural correlates of peritraumatic dissociation during posttraumatic adjustment. To this end, we combined a prospective questionnaire study with assessments at 1 to 2 weeks, 5 to 6 weeks, and 3 months post trauma with a neuroimaging paradigm in an acutely traumatized sample. In the functional magnetic resonance imaging (fMRI) investigation, we contrasted the neural correlates of peritraumatic dissociation and dissociation elicited by script-driven trauma recall during the scan. We hypothesized that peritraumatic dissociation would be associated with activation in either memory-related areas as seen during intrusive recall or emotion regulation areas as seen during dissociation elicited by traumatic script-driven imagery.15,26

In addition, the predictive power of accounts of childhood abuse and posttraumatic dissociative symptoms were examined comparatively by using self-report measures

METHOD

Participants and Procedure

This study included 121 subjects (mean ± SD age = 38.2 ± 13.7 years; women, n = 84) who presented consecutively to the emergency department at the London Health Sciences Center in London, Ontario, Canada, or to the Department of Emergency Medicine at the University of Alberta in Edmonton, Canada, after they had been involved in a motor vehicle crash (n = 104), workplace accident (n = 9), physical assault (n = 4), or other traumatic events (n = 4). Subjects were assessed shortly after admission, and those meeting DSM-IV criterion A for PTSD were included in the study. Subjects were assessed 3 times within the first 3 months post trauma. A convenience subsample of 21 subjects (mean ± SD age = 38.2 ± 12.1 years; women, n = 17; motor vehicle crash, n = 16; workplace accident, n = 3; physical assault, n = 1; other traumatic event, n = 1) underwent an fMRI scan 2 to 4 months post trauma. Exclusion criteria included (1) significant head injury; (2) history of neurologic disorders; (3) lifetime history of bipolar disorder or schizophrenia; and (4) psychotropic or steroid medication (for the fMRI sample only). The study was approved by the research ethics boards at University of Western Ontario and University of Alberta. Informed written consent was obtained from all participants.

Functional Imaging Paradigm

The script-driven imagery procedure was adapted to fMRI according to well-established methods.27

fMRI Procedures

Magnetic resonance scans were performed on a 4-Tesla whole-body Varian/Siemens imaging system with a 90-cm diameter horizontal bore and a whole-body 68-cm diameter gradient set with a maximum strength of 40 mT/m and a slew rate of 120 mT/m per second. A whole-head hybrid birdcage radio frequency coil was used for transmission and detection of signals. Each functional brain volume was acquired by using a navigator echo-corrected, interleaved multishot (4 shots), echo-planar imaging pulse sequence with a 128 ח 128 matrix size and a total volume acquisition time of 5 seconds (echo time = 15 milliseconds, flip angle = 45°, field of view = 24.0 cm). The volume acquired covered the whole brain and consisted of 12 transverse slices, 6 mm thick (voxel size = 1.87 ח 1.87 ח 6 mm).

Image Processing

For each series, all volumes were realigned to the first volume of series to reduce the effects of head motion using SPM 2 (Wellcome Department of Imaging Neuroscience, London, England). The realigned functional images were then spatially normalized to an echo-planar imaging template supplied by SPM 2. The functional data were spatially smoothed with an 8-mm (full width at half maximum) isotropic Gaussian kernel.

Statistical Mapping

Images were analyzed using a 2-stage mixed-effects analysis. At the first level, each subject’s functional data were analyzed separately by modeling the evoked blood oxygen level-dependant (BOLD) responses for each task epoch of interest as a boxcar function convolved with a hemodynamic response function. Baseline brain activation was calculated on the basis of the average activation patterns 60 seconds before each recollection of the traumatic event, and brain activation during the recall was calculated on the basis of the average activation patterns during the final 30 seconds of recall. For each subject, a contrast of trauma script greater than neutral script was created. These contrasts were entered into a second-level analysis, and correlations with the Detailed Assessment of Posttraumatic Stress31 peritraumatic dissociation scores and Responses to Script-Driven Imagery Scale17 acute dissociation scores were conducted separately and as partial correlation analysis with the Responses to Script-Driven Imagery Scale scores and results were masked with the Detailed Assessment of Posttraumatic Stress correlation. All analyses were thresholded at κ > 10 and P = .001, requiring contiguous voxels to meet the small-volume correction according to random field theory. In addition, the time since the traumatic event was used as a covariate in all analyses.

Measures

The Acute Stress Disorder Scale28 (α = .945) is a 19-item questionnaire measuring the severity of acute stress disorder symptoms on a 5-point Likert scale (1 = not at all, 5 = very much; cutoff of 56 to establish diagnostic status 1 to 2 weeks post trauma).28

The Clinician-Administered PTSD Scale29 (α = .952) is a semistructured clinical interview assessing posttraumatic symptoms as defined in DSM-IV, and a cutoff score of 50 was employed to establish diagnostic status at 5 to 6 weeks and 3 months post trauma. Severity scores were calculated as the sum of frequency and intensity ratings across all DSM-IV symptoms of PTSD.

The Childhood Trauma Questionnaire Short Form30 consists of 25 clinical items assessing emotional abuse, emotional neglect, physical abuse, physical neglect, and sexual abuse on a 5-point Likert scale (1 = never true to 5 = very often true).

The Detailed Assessment of Posttraumatic Stress31 is a 104-item inventory assessing peritraumatic and posttraumatic symptoms. The subscale peritraumatic dissociation consists of 6 items scored on a 5-point Likert scale (0 = not at all to 5 = very much) and was assessed at 5 to 6 weeks post trauma as a retrospective report of dissociation during the traumatic event (“Your mind went blank”; “Things around you felt unreal or strange”). In 13 subjects not available at this time, the Detailed Assessment of Posttraumatic Stress was filled out 3 months post trauma.

The Multiscale Dissociation Inventory32 is a standardized self-report test of dissociative symptomatology (“Knowing you must be upset, but not being able to feel it”; “Feeling like you were in a dream”). Using a 5-point Likert scale (0 = never to 5 = very often), it measures the frequency of 6 types of dissociative responses within the last month: disengagement, depersonalization, derealization, emotional constriction, memory disturbance, and identity dissociation. This scale was used as a measure of persistent dissociation at 5 to 6 weeks post trauma.

The Responses to Script-Driven Imagery Scale17 is an 11-item self-report measure of PTSD and dissociative symptoms evoked by script-driven imagery using a 7-point Likert scale (0 = not at all to 6 = a great deal). The dissociation subscale consists of 4 items specifically assessing dissociation during the fMRI scan, ie, the extent to which the subject acutely experiences derealization, depersonalization, and a sense of disconnection from his or her body during the scan (“Did you feel like you were in a fog?” “Did you feel like you were a spectator watching what was happening to you, like an observer or outsider?”). This measure was administered immediately following the scan to assess the level of dissociation induced by the exposure to individualized trauma scripts during the scanning procedure.

Statistics

Group statistics were calculated as Spearman rank correlations and 2-sample Mann-Whitney U test due to extensive positive skew in most variables. A stepwise, binary logistic regression analysis with Wald χ2 statistics was employed to predict diagnostic status. Variables were entered in blocks in order of occurrence, so the first block contained Childhood Trauma Questionnaire Short Form scores, the second block contained Detailed Assessment of Posttraumatic Stress scores, and the third block contained Multiscale Dissociation Inventory scores. Statistical analyses were carried out using Statistical Package for Social Sciences, Version 15.0 (SPSS Inc, Chicago, Illinois).

RESULTS

fMRI Results

During script-driven imagery of the traumatic versus the neutral event, Responses to Script-Driven Imagery Scale ratings for dissociation during the scan correlated positively with BOLD signal intensity in the bilateral prefrontal cortex (Table 1 and Figure 1), ie, the left middle frontal (BA 10) and the right superior frontal gyri (BA 8). Peritraumatic dissociation scores were positively correlated with activation in the right occipital lobe, ie, the lingual (BA 18), fusiform (BA 19), and parahippocampal (BA 19) gyri. After covariation of dissociation during the scan, peritraumatic dissociation remained positively correlated with activation in the right lingual (BA 18) and fusiform (BA 19) gyri.

Descriptive Statistics and Zero-Order Correlations

Descriptive statistics for all scales are listed in Table 2. Thirty-three of the 90 subjects (36.7%) assessed with the Acute Stress Disorder Scale 1 to 2 weeks post trauma met the diagnostic cutoff for acute stress disorder. Five to 6 weeks post trauma, 25 of the 102 subjects (24.5%) who underwent the Clinician-Administered PTSD Scale interview were diagnosed with PTSD. At 3 months post trauma, 92 subjects were available for interviewing with the Clinician-Administered PTSD Scale, 12 (13.0%) of whom met diagnostic criteria for PTSD. The subgroup undergoing fMRI scanning did not differ significantly from the remaining sample in terms of psychopathology (see Table 2).

The Detailed Assessment of Posttraumatic Stress scores for peritraumatic dissociation were significantly related to symptom severity at 1 to 2 weeks (r = 0.656), 5 to 6 weeks (r = 0.320), and 3 months (r = 0.410) post trauma (Table 3). These correlations indicate that stronger peritraumatic dissociation was related to more severe PTSD symptomatology throughout the first 3 months after the traumatic event. Peritraumatic dissociation was not significantly correlated with exposure to childhood trauma as measured with the Childhood Trauma Questionnaire Short Form (r = 0.175, P = .072). In turn, Childhood Trauma Questionnaire Short Form scores were significantly correlated with PTSD symptom severity at 1 to 2 weeks (r = 0.266), 5 to 6 weeks (r = 0.326), and 3 months (r = 0.307) post trauma. Both Childhood Trauma Questionnaire Short Form scores and Detailed Assessment of Posttraumatic Stress scores for peritraumatic dissociation correlated significantly with severity of dissociative symptoms at 5 to 6 weeks post trauma on all Multiscale Dissociation Inventory subscales, except for the one measuring identity dissociation.

Regression Analyses

In a stepwise, binary logistic regression analysis, both Childhood Trauma Questionnaire Short Form scores and Detailed Assessment of Posttraumatic Stress scores were identified as significant predictors of diagnostic status at 5 to 6 weeks post trauma. In the third block containing all Multiscale Dissociation Inventory subscales, only the subscale identity dissociation was identified as a predictor, but it failed to reach significance (Table 4). In the prediction of diagnostic status 3 months after the traumatic event, Childhood Trauma Questionnaire Short Form scores were a significant predictor in the first block, but they were rendered insignificant by the inclusion of the Detailed Assessment of Posttraumatic Stress peritraumatic dissociation scores.

DISCUSSION

To our knowledge, this is the first study investigating the neural correlates of peritraumatic dissociation during trauma recall in an acutely traumatized sample. The neuroimaging results suggest that peritraumatic dissociation is associated with greater activation of the right occipital lobe (BAs 18 and 19), regions previously implicated in vivid autobiographical memory recall of highly emotional events. These findings may indicate that peritraumatic dissociation directly leads to the formation of intrusive memories. In conjunction, we analyzed the predictive value of peritraumatic and persistent dissociation in a prospective questionnaire study. Results suggest that peritraumatic dissociation does not fully mediate the relationship between childhood trauma and posttraumatic adjustment; however, both variables constitute significant predictors for the development of PTSD at 5 to 6 weeks after the traumatic event. For the prediction of diagnostic status 3 months post trauma, only peritraumatic dissociation was identified as a significant predictor.

fMRI Study

Consistent with previous reports,15,16,25 dissociation during the scan was strongly correlated with bilateral activations of prefrontal cortex regions implicated in emotion regulation.33,34 The left-sided activation in the middle frontal gyrus (BA 10) is consistent with the extensive activations characterizing dissociative versus intrusive PTSD symptoms reported by Hopper et al16 and directly coincides with regions implicated in modulation of emotion.33,34

Peritraumatic dissociation was correlated with BOLD signal intensity in the right occipital lobe. This association remained significant in the right medial lingual and fusiform gyri after covariation of dissociation during the scan. Previous studies have implicated these regions in emotional autobiographic memory recall (for a meta-analysis see Svoboda et al35) as well as visual imagery.36,37 In a study by Shergill et al,38 activation in the fusiform region was correlated with visual imagery characterized by a first-person perspective. Convergently, Gilboa et al39 reported a relationship between BOLD signal intensity in the lingual gyrus and greater vividness of the autobiographical memory recall. The overlap in areas of visual processing and autobiographic memory during trauma recall could be interpreted as enhanced visual processing for highly emotional arousing events, possibly driven by feed-forward amygdala connectivity.40 In conjunction, these results indicate that peritraumatic dissociation is associated with brain activations underlying intrusive trauma recall in this script-driven paradigm and thus strongly support the model proposed by Conway.8 Interestingly, similar activations in the fusiform gyrus have previously been associated with the recall of unresolved life events in a sample of patients with borderline personality disorder41—a population that is characterized by high rates of traumatization.

Childhood Trauma, Peritraumatic Dissociation, and PTSD Symptoms

Childhood trauma was significantly correlated with symptom severity at all 3 time points as well as with dissociative symptoms as measured with all Multiscale Dissociation Inventory subscales except identity dissociation. The significant correlations between childhood trauma and persistent dissociation explain why the results reported here differ from those reported previously5: after accounting for childhood trauma and peritraumatic dissociation, persistent dissociation, as measured with the Multiscale Dissociation Inventory, did not improve the prediction of PTSD. This indicates that even in an acutely traumatized sample of adult subjects, childhood trauma accounts for such a significant portion of variance in persistent dissociation that persistent dissociation is rendered insignificant in the prediction of PTSD development. This finding is in line with earlier studies23,24 demonstrating a direct link between childhood trauma and the development of persistent dissociation. Childhood trauma was positively correlated with peritraumatic dissociation, but it failed to reach statistical significance. Peritraumatic dissociation, in turn, was positively correlated with symptom severity at all 3 time points as well as with persistent dissociation, including dissociative amnesia. A nonsignificant correlation emerged between the Multiscale Dissociation Inventory subscale identity dissociation measuring symptoms indicative of dissociative identity disorder and peritraumatic dissociation. This may result from a sampling bias, as this disorder is likely underrepresented in an acutely traumatized sample recruited in the emergency department.

Limitations

First, due to the nature of traumatic events, it is difficult to assess peritraumatic dissociation at the time of occurrence. While some authors have argued that the posttraumatic assessment might lead to a scoring bias, a recent meta-analysis has shown that the predictive value of peritraumatic dissociation assessments did not vary with the assessment date.42

Second, we did not include acute stress disorder symptoms in the regression analysis, as it has been shown before that the symptom overlap with peritraumatic dissociation is so substantial that acute stress disorder as the more proximal predictor eliminates the predictive value of peritraumatic dissociation scores.43 However, it would be most informative to differentiate between the influence of dissociation strictly occurring peritraumatic and dissociation occurring within the first days of posttraumatic adjustment. Future studies should therefore assess dissociation repeatedly within the first 2 weeks post trauma.

Third, this pilot investigation relies on a comparatively small number of patients from 2 centers. This is particularly true for the assessment of symptom severity at 3 months post trauma and the neuroimaging study. The small sample size and associated limited power may have prevented us from detecting additional brain regions associated with peritraumatic dissociation and prevented us from analyzing the predictive value of the fMRI data. Future studies should therefore seek to predict symptom severity on the basis of BOLD signal changes in a larger sample. In addition, we cannot rule out that the use of a convenience sample in the neuroimaging study introduced a systematic bias. Therefore, generalizations can only be accepted with caution.

CONCLUSION

The results of the regression analysis indicate that both childhood trauma and peritraumatic dissociation are valuable predictors of future PTSD symptom development and therefore can guide the identification of individuals at risk. However, peritraumatic dissociation is a more proximal variable and carried greater predictive power of chronic PTSD in the current sample. Further evidence for the latter stems from the neuroimaging data that link peritraumatic dissociation to intrusive memory recall and strongly support the model proposed by Conway8; in this model, intrusions represent vivid memory recall from an episodic memory system in the posterior temporal-occipital regions storing the sensory aspects of the traumatic event.

Author affiliations: Departments of Psychiatry (Drs Daniels and Lanius and Ms Densmore) and Psychology (Dr Neufeld), The University of Western Ontario, London, Ontario; Department of Psychiatry (Dr Coupland), Faculty of Nursing (Dr Hegadoren), Department of Emergency Medicine and School of Public Health (Dr Rowe), The University of Alberta, Edmonton, Alberta, Canada; and Department of Psychiatry, Universitפtsklinik Charité, Berlin, Germany (Dr Daniels).

Potential conflicts of interest: None reported.

Funding/support: The work presented in the article was supported by grants from The Canadian Institutes of Health Research and the Workplace Safety and Insurance Board. Drs Hegadoren and Rowe are supported by 21st Century Canada Research Chairs from the Government of Canada (Ottawa, Ontario). Dr Coupland is supported by The Alberta Heritage Foundation for Medical Research (Edmonton, Alberta). The work of Dr Daniels was funded by the VW foundation grant number II/84051.

Acknowledgments: The authors would like to thank Suzy Southwell (University of Western Ontario) for her help with acquisition of subjects and Stephanie Nevill, MA (University of Western Ontario), for her help with diagnostic assessments. Mss Southwell and Nevill have no potential conflicts of interest related to the subject of this article.

REFERENCES

1. Brewin CR, Gregory JD, Lipton M, et al. Intrusive images in psychological disorders: characteristics, neural mechanisms, and treatment implications. Psychol Rev. 2010;117(1):210-232. PubMed doi:10.1037/a0018113

2. van der Kolk BA, Fisler R. Dissociation and the fragmentary nature of traumatic memories: overview and exploratory study. J Trauma Stress. 1995;8(4):505-525. PubMed doi:10.1002/jts.2490080402

3. Bryant RA. Does dissociation further our understanding of PTSD? J Anxiety Disord. 2007;21(2):183-191. PubMed doi:10.1016/j.janxdis.2006.09.012

4. Waelde LC, Silvern L, Carlson EB, et al. Dissociation in PTSD. In: Dell PF, O’ Neil J, Somer E, eds. Dissociation and the Dissociative Disorders: DSM-V and Beyond. New York, NY: Routledge; 2009:447-456.

5. Briere J, Scott C, Weathers F. Peritraumatic and persistent dissociation in the presumed etiology of PTSD. Am J Psychiatry. 2005;162(12):2295-2301. PubMed doi:10.1176/appi.ajp.162.12.2295

6. Foa EB, Rothbaum BO. Treating the Trauma of Rape: Cognitive-Behavioral Therapy for PTSD. New York, NY: Guilford Press; 1998.

7. Hackmann A, Ehlers A, Speckens A, et al. Characteristics and content of intrusive memories in PTSD and their changes with treatment. J Trauma Stress. 2004;17(3):231-240. PubMed doi:10.1023/B:JOTS.0000029266.88369.fd

8. Conway MA. Episodic memories. Neuropsychologia. 2009;47(11):2305-2313. PubMed doi:10.1016/j.neuropsychologia.2009.02.003

9. Morgan CA 3rd, Hazlett G, Wang S, et al. Symptoms of dissociation in humans experiencing acute, uncontrollable stress: a prospective investigation. Am J Psychiatry. 2001;158(8):1239-1247. PubMed doi:10.1176/appi.ajp.158.8.1239

10. Spiegel D. Recognizing traumatic dissociation. Am J Psychiatry. 2006;163(4):566-568. PubMed doi:10.1176/appi.ajp.163.4.566

11. Butler LD, Duran RE, Jasiukaitis P, et al. Hypnotizability and traumatic experience: a diathesis-stress model of dissociative symptomatology. Am J Psychiatry. 1996;153(suppl):42-63. PubMed

12. Lanius RA, Vermetten E, Loewenstein RJ, et al. Emotion modulation in PTSD: clinical and neurobiological evidence for a dissociative subtype. Am J Psychiatry. 2010;167(6):640-647. PubMed

13. Griffin MG, Resick PA, Mechanic MB. Objective assessment of peritraumatic dissociation: psychophysiological indicators. Am J Psychiatry. 1997;154(8):1081-1088. PubMed

14. Sack M, Hopper JW, Lamprecht F. Low respiratory sinus arrhythmia and prolonged psychophysiological arousal in posttraumatic stress disorder: heart rate dynamics and individual differences in arousal regulation. Biol Psychiatry. 2004;55(3):284-290. PubMed doi:10.1016/S0006-3223(03)00677-2

15. Frewen PA, Lanius RA. Toward a psychobiology of posttraumatic self-dysregulation: reexperiencing, hyperarousal, dissociation, and emotional numbing. Ann N Y Acad Sci. 2006;1071(1):110-124. PubMed doi:10.1196/annals.1364.010

16. Hopper JW, Frewen PA, van der Kolk BA, et al. Neural correlates of reexperiencing, avoidance, and dissociation in PTSD: symptom dimensions and emotion dysregulation in responses to script-driven trauma imagery. J Trauma Stress. 2007;20(5):713-725. PubMed doi:10.1002/jts.20284

17. Hopper JW, Frewen PA, Sack M, et al. The Responses to Script-Driven Imagery Scale (RSDI): assessment of state posttraumatic symptoms for psychobiological and treatment research. J Psychopathol Behav Assess. 2007;29(4):249-268. doi:10.1007/s10862-007-9046-0

18. Ebner-Priemer UW, Mauchnik J, Kleindienst N, et al. Emotional learning during dissociative states in borderline personality disorder. J Psychiatry Neurosci. 2009;34(3):214-222. PubMed

19. Cloitre M, Koenen KC, Cohen LR, et al. Skills training in affective and interpersonal regulation followed by exposure: a phase-based treatment for PTSD related to childhood abuse. J Consult Clin Psychol. 2002;70(5):1067-1074. PubMed doi:10.1037/0022-006X.70.5.1067

20. Ozer EJ, Best SR, Lipsey TL, et al. Predictors of posttraumatic stress disorder and symptoms in adults: a meta-analysis. Psychol Bull. 2003;129(1):52-73. PubMed doi:10.1037/0033-2909.129.1.52

21. Brewin CR, Andrews B, Valentine JD. Meta-analysis of risk factors for posttraumatic stress disorder in trauma-exposed adults. J Consult Clin Psychol. 2000;68(5):748-766. PubMed doi:10.1037/0022-006X.68.5.748

22. Cougle JR, Timpano KR, Sachs-Ericsson N, et al. Examining the unique relationships between anxiety disorders and childhood physical and sexual abuse in the National Comorbidity Survey-Replication. Psychiatry Res 2010;177(1-2):150-155. PubMed

23. Hetzel MD, McCanne TR. The roles of peritraumatic dissociation, child physical abuse, and child sexual abuse in the development of posttraumatic stress disorder and adult victimization. Child Abuse Negl. 2005;29(8):915-930. PubMed doi:10.1016/j.chiabu.2004.11.008

24. Roe-Sepowitz D, Bedard LE, Pate K. The impact of child abuse on dissociative symptoms: a study of incarcerated women. J Trauma Dissociation. 2007;8(3):7-26. PubMed doi:10.1300/J229v08n03_02

25. Felmingham K, Kemp AH, Williams L, et al. Dissociative responses to conscious and non-conscious fear impact underlying brain function in post-traumatic stress disorder. Psychol Med. 2008;38(12):1771-1780. PubMed doi:10.1017/S0033291708002742

26. Shin LM, Orr SP, Carson MA, et al. Regional cerebral blood flow in the amygdala and medial prefrontal cortex during traumatic imagery in male and female Vietnam veterans with PTSD. Arch Gen Psychiatry. 2004;61(2):168-176. PubMed doi:10.1001/archpsyc.61.2.168

27. Lanius RA, Williamson PC, Densmore M, et al. Neural correlates of traumatic memories in posttraumatic stress disorder: a functional MRI investigation. Am J Psychiatry. 2001;158(11):1920-1922. PubMed doi:10.1176/appi.ajp.158.11.1920

28. Bryant RA, Moulds ML, Guthrie RM. Acute Stress Disorder Scale: a self-report measure of acute stress disorder. Psychol Assess. 2000;12(1):61-68. PubMed doi:10.1037/1040-3590.12.1.61

29. Blake DD, Weathers FW, Nagy LM, et al. The development of a Clinician-Administered PTSD Scale. J Trauma Stress. 1995;8(1):75-90. PubMed doi:10.1002/jts.2490080106

30. Bernstein DP, Stein JA, Newcomb MD, et al. Development and validation of a brief screening version of the Childhood Trauma Questionnaire. Child Abuse Negl. 2003;27(2):169-190. PubMed doi:10.1016/S0145-2134(02)00541-0

31. Briere J. Detailed Assessment of Posttraumatic Stress (DAPS). Odessa, Florida: Psychological Assessment Resources; 2001.

32. Briere J. Multiscale Dissociation Inventory. Odessa, Florida: Psychological Assessment Resources; 2002.

33. Herwig U, Abler B, Walter H, et al. Expecting unpleasant stimuli—an fMRI study. Psychiatry Res. 2007;154(1):1-12. PubMed doi:10.1016/j.pscychresns.2006.02.007

34. Frankenstein UN, Richter W, McIntyre MC, et al. Distraction modulates anterior cingulate gyrus activations during the cold pressor test. Neuroimage. 2001;14(4):827-836. PubMed doi:10.1006/nimg.2001.0883

35. Svoboda E, McKinnon MC, Levine B. The functional neuroanatomy of autobiographical memory: a meta-analysis. Neuropsychologia. 2006;44(12):2189-2208. PubMed doi:10.1016/j.neuropsychologia.2006.05.023

36. Ishai A, Ungerleider LG, Martin A, et al. The representation of objects in the human occipital and temporal cortex. J Cogn Neurosci. 2000;12(suppl 2):35-51. PubMed doi:10.1162/089892900564055

37. Hasnain MK, Fox PT, Woldorff MG. Intersubject variability of functional areas in the human visual cortex. Hum Brain Mapp. 1998;6(4):301-315. PubMed doi:10.1002/(SICI)1097-0193(1998)6:4<301::AID-HBM8>3.0.CO;2-7

38. Shergill SS, Bullmore ET, Brammer MJ, et al. A functional study of auditory verbal imagery. Psychol Med. 2001;31(2):241-253. PubMed doi:10.1017/S003329170100335X

39. Gilboa A, Winocur G, Grady CL, et al. Remembering our past: functional neuroanatomy of recollection of recent and very remote personal events. Cereb Cortex. 2004;14(11):1214-1225. PubMed doi:10.1093/cercor/bhh082

40. Anderson AK, Phelps EA. Lesions of the human amygdala impair enhanced perception of emotionally salient events. Nature. 2001;411(6835):305-309. PubMed doi:10.1038/35077083

41. Beblo T, Driessen M, Mertens M, et al. Functional MRI correlates of the recall of unresolved life events in borderline personality disorder. Psychol Med. 2006;36(6):845-856. PubMed doi:10.1017/S0033291706007227

42. Breh DC, Seidler GH. Is peritraumatic dissociation a risk factor for PTSD? J Trauma Dissociation. 2007;8(1):53-69. PubMed doi:10.1300/J229v08n01_04

43. van der Velden PG, Wittmann L. The independent predictive value of peritraumatic dissociation for PTSD symptomatology after type I trauma: a systematic review of prospective studies. Clin Psychol Rev. 2008;28(6):1009-1020. PubMed doi:10.1016/j.cpr.2008.02.006