Functional neuroimaging of emotionally intense autobiographical memories in post-traumatic stress disorder

https://doi.org/10.1016/j.jpsychires.2010.10.011Get rights and content

Abstract

Post-traumatic stress disorder (PTSD) affects regions that support autobiographical memory (AM) retrieval, such as the hippocampus, amygdala and ventral medial prefrontal cortex (PFC). However, it is not well understood how PTSD may impact the neural mechanisms of memory retrieval for the personal past. We used a generic cue method combined with parametric modulation analysis and functional MRI (fMRI) to investigate the neural mechanisms affected by PTSD symptoms during the retrieval of a large sample of emotionally intense AMs. There were three main results. First, the PTSD group showed greater recruitment of the amygdala/hippocampus during the construction of negative versus positive emotionally intense AMs, when compared to controls. Second, across both the construction and elaboration phases of retrieval the PTSD group showed greater recruitment of the ventral medial PFC for negatively intense memories, but less recruitment for positively intense memories. Third, the PTSD group showed greater functional coupling between the ventral medial PFC and the amygdala for negatively intense memories, but less coupling for positively intense memories. In sum, the fMRI data suggest that there was greater recruitment and coupling of emotional brain regions during the retrieval of negatively intense AMs in the PTSD group when compared to controls.

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)

  • J. Rissman et al.

    Measuring functional connectivity during distinct stages of a cognitive task

    Neuroimage

    (2004)
  • D.M. Small et al.

    Dissociation of neural representation of intensity and affective valuation in human gustation

    Neuron

    (2003)
  • E. Svoboda et al.

    The functional neuroanatomy of autobiographical memory: a meta-analysis

    Neuropsychologia

    (2006)
  • A.K. Anderson et al.

    Dissociated neural representations of intensity and valence in human olfaction

    Nature Neuroscience

    (2003)
  • A.T. Beck et al.

    Manual for beck depression inventory

    (1996)
  • D. Berntsen et al.

    Contrasting models of posttraumatic stress disorder: reply to Monroe and Mineka (2008)

    Psychological Review

    (2008)
  • D.D. Blake et al.

    The development of a clinician-administered PTSD scale

    Journal of Traumatic Stress

    (1995)
  • M.M. Bradley et al.

    Affective norms for english words (ANEW)

  • W.F. Brewer

    What is autobiographical memory?

  • S.M. Daselaar et al.

    The spatiotemporal dynamics of autobiographical memory: neural correlates of recall, emotional intensity, and reliving

    Cerebral Cortex

    (2008)
  • A. Etkin et al.

    Functional neuroimaging of anxiety: a meta-analysis of emotional processing in PTSD, social anxiety disorder, and specific phobia

    American Journal of Psychiatry

    (2007)
  • V. Francati et al.

    Functional neuroimaging studies in posttraumatic stress disorder: review of current methods and findings

    Depression and Anxiety

    (2007)
  • P.A. Frewen et al.

    Toward a psychobiology of posttraumatic self-dysregulation: reexperiencing, hyperarousal, dissociation, and emotional numbing

    Annals of the New York Academy of Sciences

    (2006)
  • Cited by (83)

    • Review of potential psychedelic treatments for PTSD

      2022, Journal of the Neurological Sciences
      Citation Excerpt :

      Hippocampal/parahippocampal activation is lower than control subjects for PTSD-affected individuals when shown positive stimuli [16]. When shown negative stimuli, hippocampal/parahippocampal activity is heightened [17,18], and this increased activity is correlated with increased amygdala activation in some instances [12,19], though overall, there may be decreased coupling of the hippocampus and amygdala in PTSD [20]. Together, these findings indicate that in PTSD, individuals view negative stimuli as excessively important or salient, have increased reactivity to them, have less frontal lobe mitigation of this reactivity, and may experience stimuli as having more personal or autobiographical significance [21].

    View all citing articles on Scopus
    View full text