Functional neuroimaging of emotionally intense autobiographical memories in post-traumatic stress disorder
Introduction
Neuroimaging studies of traumatic experiences in post-traumatic stress disorder (PTSD) and other disorders (e.g., Driessen et al., 2004, Lanius et al., 2001, Lanius et al., 2004) have observed consistent differences in regions that are frequently recruited during autobiographical memory (AM) retrieval (Cabeza & St. Jacques, 2007), such as the hippocampus, amygdala, and medial prefrontal cortex (PFC). Reduced volume of the hippocampus, a region critical for memory, is frequently observed in PTSD but it is less clear whether there are also functional changes here (Shin et al., 2006). The amygdala, a region critical in the detection of emotion and the generation of physiological response, is hyperactive during negative emotional tasks in PTSD patients and the level of activity here is associated with the severity of symptoms (Etkin and Wager, 2007, Shin et al., 2006). In contrast, the medial PFC, a region associated with controlled emotional processes, is often hypoactive in PTSD patients (Etkin and Wager, 2007, Shin et al., 2006). Moreover, changes in the coupling between the amygdala and medial PFC may underlie emotional dysregulation symptoms in PTSD (Etkin and Wager, 2007, Frewen and Lanius, 2006, Milad and Rauch, 2007, Shin et al., 2006). Confirming the critical role of the amygdala and medial PFC in the pathogenesis of PTSD, a patient study by Koenigs and colleagues (Koenigs et al., 2008) found that isolated lesions to these brain regions were related to reduced occurrence of PTSD in Vietnam War veterans.
The effect of PTSD on brain regions involved in AM suggests that a broader examination of personal memory beyond traumatic experiences is warranted (Lanius et al., 2003). Moreover, in participants with PTSD or high levels of symptom severity, the effects of emotional reactions extend beyond traumatic memories to word-cued, important but non-trauma related, and positive autobiographical memories (Rubin et al., 2008b). Thus, although PTSD diagnosis relies on a single traumatic event the impact of PTSD is more widespread across AM. Little, however, is known about the neural basis of these effects.
In the present study, we investigate the neural mechanisms affected by PTSD symptoms during retrieval of a large sample of emotionally intense AMs. We employed a generic cue method that used emotional words to elicit AMs in order to distinguish early construction and later elaboration phases of retrieval. Further, we acquired online ratings of emotional experience for parametric analysis of functional activations associated with emotionally intense memories. We explored the hypothesis that PTSD would involve reduced recruitment of the hippocampus, increased recruitment of the amygdala and reduced recruitment of the medial PFC when recalling emotionally intense AMs.
Section snippets
Participants
Young adult participants were recruited from Duke University (18–35 years of age). Participants in the control group were recruited from a database of healthy young adults, who had participated in previous fMRI research studies. Inclusion criteria for the control group followed procedures that we have routinely used in behavioral studies in the Durham Veteran’s Association Medical Clinic (VAMC), which do not include having had a previous trauma. This allowed us to examine the effect of PTSD
Behavioral results
Participants were able to recall an event matching the cue on more than 97% of trials (see Table 2 for mean behavioral scores, standard deviations, t-scores, p-values, and effect sizes). There were no group differences in reaction time to retrieve an AM or in the online ratings of reliving or emotional intensity. Post-scan ratings of vividness, significance, physiological response, date of the memory, and type of memory did not differ between the groups. However, as expected (Rubin et al., 2008a
Discussion
The current study presents a novel investigation to examine the neural mechanisms underlying retrieval of a sample of emotionally intense AMs in PTSD. Previous functional neuroimaging studies examining the impact of PTSD on personal memory have primarily focused on the neural mechanisms supporting traumatic memories, often using scripts of traumatic events (although see Driessen et al., 2004; for a review see Francati et al., 2007). Here, we used a generic cue method to elicit spontaneously
Source of funding
This research was supported by a National Institute of Aging RO1 AG023123 and National Institute of Mental Health R01 MH066079 grant to DCR and the Myra and William Waldo Boone and the Philip Jackson Baugh graduate fellowships awarded to PLS. The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health.
Contributors
PLS and DCR designed the study and wrote the protocol. PLS, AM and AB recruited participants conducted the scanning sessions. PLS undertook the statistical analysis and wrote the first draft of the manuscript. All authors contributed to and have approved the final manuscript.
Conflict of interest
None.
Acknowledgments
We thank Polly van de Velde and Gustavo Araujo for help with participant recruitment and screening, and Philip A. Kragel for helpful discussions regarding the analysis. PLS is now at the Department of Psychology, Harvard University, Cambridge, MA, 02138, USA, [email protected] AB is now at the Imagery and Cognitive Neurosciences Laboratory (CNRS, FRE 3289), University of Strasbourg, 67000 Strasbourg, France, and AM is now at the Center on Autobiographical Memory Research, Aarhus
References (47)
- et al.
Self-projection and the brain
Trends in Cognitive Sciences
(2007) - et al.
Functional neuroimaging of autobiographical memory
Trends in Cognitive Sciences
(2007) - et al.
Dissociable effects of arousal and valence on prefrontal activity indexing emotional evaluation and subsequent memory: an event-related fMRI study
Neuroimage
(2004) - et al.
Posttraumatic stress disorder and fMRI activation patterns of traumatic memory in patients with borderline personality disorder
Biological Psychiatry
(2004) - et al.
Probing reward function in post-traumatic stress disorder with beautiful facial images
Psychiatry Research
(2005) - et al.
Co-activation of the amygdala, hippocampus and inferior frontal gyrus during autobiographical memory retrieval
Neuropsychologia
(2005) - et al.
Recall of emotional states in posttraumatic stress disorder: an fMRI investigation
Biological Psychiatry
(2003) - et al.
An automated method for neuroantomic and cytoarchitectonic atlas-based interrogation of fMRI data sets
Neuroimage
(2003) - et al.
The cognitive control of emotion
Trends in Cognitive Sciences
(2005) - et al.
Functional neuroanatomy of emotion: a meta-analysis of emotion activation studies in PET and fMRI
Neuroimage
(2002)
Measuring functional connectivity during distinct stages of a cognitive task
Neuroimage
Dissociation of neural representation of intensity and affective valuation in human gustation
Neuron
The functional neuroanatomy of autobiographical memory: a meta-analysis
Neuropsychologia
Dissociated neural representations of intensity and valence in human olfaction
Nature Neuroscience
Manual for beck depression inventory
Contrasting models of posttraumatic stress disorder: reply to Monroe and Mineka (2008)
Psychological Review
The development of a clinician-administered PTSD scale
Journal of Traumatic Stress
Affective norms for english words (ANEW)
What is autobiographical memory?
The spatiotemporal dynamics of autobiographical memory: neural correlates of recall, emotional intensity, and reliving
Cerebral Cortex
Functional neuroimaging of anxiety: a meta-analysis of emotional processing in PTSD, social anxiety disorder, and specific phobia
American Journal of Psychiatry
Functional neuroimaging studies in posttraumatic stress disorder: review of current methods and findings
Depression and Anxiety
Toward a psychobiology of posttraumatic self-dysregulation: reexperiencing, hyperarousal, dissociation, and emotional numbing
Annals of the New York Academy of Sciences
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