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Memory suppression can help after trauma

Therapists have discussed for a long time whether attempts to voluntarily suppress the intrusion of trauma memories are helpful to combat the distressing impacts of trauma. Mary et al. studied survivors of the 2015 Paris terrorist attacks who developed posttraumatic stress disorder and those who did not (see the Perspective by Ersche). Using functional magnetic resonance imaging, they investigated the neural networks underlying the control and suppression of memory retrieval. The results suggest that the characteristic symptoms of the disorder are not related to the memory itself but to its maladaptive control. These results offer new insights into the development of post-traumatic stress disorder and potential avenues for treatment.
Science, this issue p. eaay8477; see also p. 734

Structured Abstract

INTRODUCTION

One of the fundamental questions in clinical neuroscience is why some individuals can cope with traumatic events, while others remain traumatized by a haunting past they cannot get rid of. The expression and persistence of vivid and distressing intrusive memories is a central feature of posttraumatic stress disorder (PTSD). Current understanding of PTSD links this persistence to a failure to reduce the fear associated with the trauma, a deficit rooted in the dysfunction of memory. In this study, we investigated whether this deficit may additionally be rooted in the disruption of the brain system that normally allows control over memory.

RATIONALE

To test this hypothesis in a laboratory setting, we implemented neutral and inoffensive intrusive memories paired with a reminder cue in a group of 102 individuals exposed to the 2015 Paris terrorist attacks and in a group of 73 nonexposed individuals (i.e., individuals who did not experience the attacks). The exposed group was composed of 55 individuals suffering from PTSD symptoms (denoted PTSD+) and 47 individuals showing no noticeable impairment after the trauma (denoted PTSD−). We used functional magnetic resonance imaging to measure how the dorsolateral prefrontal cortex (DLPFC), a core hub of the brain control system, regulated and suppressed memory activity during the reexperiencing of these intrusive memories. We focused our analyses on both the functional and causal dependency between control and memory neural circuits during attempts to suppress the reemergence of these intrusive memories.

RESULTS

In healthy individuals (PTSD− and nonexposed), attempts to prevent the unwanted emergence of intrusive memory into consciousness was associated with a significant reduction of the functional coupling between control and memory systems, compared with situations where the reminder did not trigger such intrusion. In contrast, there was a near-absence of such a decrease in connectivity in PTSD+. Additional analyses focusing on the directionality of the underlying neural flow communications revealed that the suppression of intrusive memories in healthy individuals arose from the regulation of the right anterior DLPFC, which tuned the response of memory processes to reduce their responses. Notably, this regulation was directed at two key regions previously associated with the reexperiencing of traumatic memories: the hippocampus and the precuneus.

CONCLUSION

We observed a generalized disruption in PTSD of the regulation signal that controls the reactivation of unwanted memories. This disruption could constitute a central factor in the persistence of traumatic memories, undercutting the ability to deploy the necessary coping resources that maintain healthy memory. Such a deficit may explain maladaptive and unsuccessful suppression attempts often seen in PTSD. Our study suggests that the general mental operations typically engaged to banish and suppress the intrusive expression of unwanted memories might contribute to positive adaptation in the aftermath of a traumatic event, paving the way for new treatments.
Mechanisms of memory suppression after trauma.
(A) Exposed individuals with or without PTSD were asked to suppress the reexperiencing of neutral intrusive memories. (B) Analyses focused on the functional and causal dependencies between control and memory systems during suppression attempts. (C) Extensive decreased coupling to counteract intrusion was seen in nonexposed and PTSD− groups but not in the PTSD+ group. SFG, superior frontal gyrus; MFG, middle frontal gyrus; IFG, inferior frontal gyrus; CC, cingulate cortex; Hipp, hippocampus; PhG, parahippocampal gyrus; FusG, fusiform gyrus; PCun, precuneus. (D) This decreased coupling was mediated by top-down regulation of involuntary memory processing arising from the right DLPFC.

Abstract

In the aftermath of trauma, little is known about why the unwanted and unbidden recollection of traumatic memories persists in some individuals but not others. We implemented neutral and inoffensive intrusive memories in the laboratory in a group of 102 individuals exposed to the 2015 Paris terrorist attacks and 73 nonexposed individuals, who were not in Paris during the attacks. While reexperiencing these intrusive memories, nonexposed individuals and exposed individuals without posttraumatic stress disorder (PTSD) could adaptively suppress memory activity, but exposed individuals with PTSD could not. These findings suggest that the capacity to suppress memory is central to positive posttraumatic adaptation. A generalized disruption of the memory control system could explain the maladaptive and unsuccessful suppression attempts often seen in PTSD, and this disruption should be targeted by specific treatments.
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Supplementary Material

Summary

Figs. S1 to S5
Tables S1 to S15

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Volume 367Issue 647914 February 2020
PubMed: 32054733

History

Received: 25 July 2019
Accepted: 12 December 2019

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Acknowledgments

We thank all participants for volunteering in this study and the associations of victims who have supported this project. We thank the medical doctors, especially M. Mialon and E. Duprey, and the staff at Cyceron (Biomedical Imaging Platform in Caen). We also thank the researchers; psychologists M. Deschamps, P. Billard, B. Marteau, R. Copalle, and C. Becquet; technicians; and administrative staff at U1077 (Caen), at “Programme 13-Novembre” in Paris, at INSERM “Délégation Régionale Nord-Ouest” (Lille), and at INSERM “Pôle Recherche Clinique”, especially K. Ammour. Funding: This study was funded by the French Commissariat-General for Investment (CGI) via the National Research Agency (ANR) and the “Programme d’investissement pour l’Avenir (PIA).” The study was realized within the framework of “Programme 13-Novembre” (EQUIPEX Matrice) headed by D.P. and F.E. This program is sponsored by the CNRS and INSERM and supported administratively by HESAM Université, bringing together 35 partners (see www.memoire13novembre.fr). A.M. is funded by a 3-year postdoctoral fellowship from the Normandy region. Author contributions: J.D., D.P., F.E., and P.G. designed the study. J.D., D.P., F.E., C.K.-P., and P.G. obtained the financial support. A.M., C.P., and T.V. performed the data acquisition. C.M. and F.F. managed and coordinated the research activity planning and execution. F.V. and V.d.l.S. supervised MRI data collection on human participants and medical interviews. V.d.l.S. supervised the medical aspects of the study, and J.D. supervised SCID interviews and psychiatric examinations. A.M. and P.G. analyzed the behavioral and functional data with the help of G.L. and C.P. A.M. and P.G. wrote the original draft. All authors reviewed and edited the manuscript. Competing interests: The authors declare no competing interests. Data and materials availability: The data and code that support the conclusions of this study are available in the main text and the supplementary material.

Authors

Affiliations

Normandie Université, UNICAEN, PSL Research University, EPHE, INSERM, U1077, CHU de Caen, GIP Cyceron, Neuropsychologie et Imagerie de la Mémoire Humaine, 14000 Caen, France.
Jacques Dayan
Normandie Université, UNICAEN, PSL Research University, EPHE, INSERM, U1077, CHU de Caen, GIP Cyceron, Neuropsychologie et Imagerie de la Mémoire Humaine, 14000 Caen, France.
Pôle Hospitalo-Universitaire de Psychiatrie de l’Enfant et de l’Adolescent, Centre Hospitalier Guillaume Régnier, Université Rennes 1, 35700 Rennes, France.
Giovanni Leone
Normandie Université, UNICAEN, PSL Research University, EPHE, INSERM, U1077, CHU de Caen, GIP Cyceron, Neuropsychologie et Imagerie de la Mémoire Humaine, 14000 Caen, France.
Normandie Université, UNICAEN, PSL Research University, EPHE, INSERM, U1077, CHU de Caen, GIP Cyceron, Neuropsychologie et Imagerie de la Mémoire Humaine, 14000 Caen, France.
Florence Fraisse
Normandie Université, UNICAEN, PSL Research University, EPHE, INSERM, U1077, CHU de Caen, GIP Cyceron, Neuropsychologie et Imagerie de la Mémoire Humaine, 14000 Caen, France.
Carine Malle
Normandie Université, UNICAEN, PSL Research University, EPHE, INSERM, U1077, CHU de Caen, GIP Cyceron, Neuropsychologie et Imagerie de la Mémoire Humaine, 14000 Caen, France.
Thomas Vallée
Normandie Université, UNICAEN, PSL Research University, EPHE, INSERM, U1077, CHU de Caen, GIP Cyceron, Neuropsychologie et Imagerie de la Mémoire Humaine, 14000 Caen, France.
Université Paris I Panthéon Sorbonne, HESAM Université, EHESS, CNRS, UMR8209, 75231 Paris, France.
Fausto Viader
Normandie Université, UNICAEN, PSL Research University, EPHE, INSERM, U1077, CHU de Caen, GIP Cyceron, Neuropsychologie et Imagerie de la Mémoire Humaine, 14000 Caen, France.
Normandie Université, UNICAEN, PSL Research University, EPHE, INSERM, U1077, CHU de Caen, GIP Cyceron, Neuropsychologie et Imagerie de la Mémoire Humaine, 14000 Caen, France.
Université Paris I Panthéon Sorbonne, HESAM Université, EHESS, CNRS, UMR8209, 75231 Paris, France.
Normandie Université, UNICAEN, PSL Research University, EPHE, INSERM, U1077, CHU de Caen, GIP Cyceron, Neuropsychologie et Imagerie de la Mémoire Humaine, 14000 Caen, France.
Normandie Université, UNICAEN, PSL Research University, EPHE, INSERM, U1077, CHU de Caen, GIP Cyceron, Neuropsychologie et Imagerie de la Mémoire Humaine, 14000 Caen, France.

Notes

*Corresponding author. Email: [email protected]

Funding Information

Conseil régional de Normandie:
Agence Nationale de la Recherche, Programme d'investissements d'avenir: 10-EQPX-21-01

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Science
Volume 367|Issue 6479
14 February 2020
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Received:25 July 2019
Accepted:12 December 2019
Published in print:14 February 2020
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