Research Article

Resilience after trauma: The role of memory suppression

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Science  14 Feb 2020:
Vol. 367, Issue 6479, eaay8477
DOI: 10.1126/science.aay8477
  • 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.

  • Fig. 1 Experimental design.

    (A) Timeline and procedure of inclusion of the participants exposed to the 13 November 2015 Paris terrorist attacks. The dates of the first and last inclusion are 13 June 2016 and 7 June 2017, respectively. Participants with a similar degree of exposure were diagnosed as non-PTSD or PTSD. (B) After learning word-object pairs, participants underwent fMRI scanning as they performed the think/no-think (TNT) task. For think items (in green), participants recalled a detailed visual memory of the associated picture. For no-think items (in red), they were asked to prevent the picture from entering awareness. After no-think trial cues ended, participants reported the presence or absence of intrusive memories that further trigger reactive inhibitory process. At the behavioral level, the effect of suppression was measured using a perceptual identification task including novel unprimed objects. (C) Intrusion proportions (i.e., the proportion of trials in which the associated memory entered into awareness on no-think trials) as measured by our trial-by-trial intrusion report measure (see materials and methods) over the eight suppression attempts of the TNT phase. Shaded error bands represent 95% bootstrapped confidence intervals.

  • Fig. 2 Decrease in functional connectivity during suppression of intrusive memories between control and memory brain regions.

    (A) Suppression-induced functional connectivity was analyzed between prefrontal control (seed) and memory (target) regions of interest (ROIs). The control and memory target ROIs are represented as shown in the color key on the right. (B) The contrast between intrusion and nonintrusion shows an extensive decrease in connectivity for both the nonexposed and non-PTSD groups. The matrices represent connectivity changes (t-statistic) in each group, between the ROIs of the control and memory systems. Circles, triangles, and stars in the matrices represent significant changes in connection at PFDR < 0.05, P < 0.01, and P < 0.05, respectively. In the circular connectograms, the colors of the edges are defined by the prefrontal control ROIs that predicted activity of memory sites in the gPPI model [color key in (A) applies here]. The size of the edges reflects the Bayes factors for connections associated with a significant decrease in connectivity during the regulation of intrusive compared with nonintrusive memories. SFG, superior frontal gyrus; MFG, middle frontal gyrus; IFG, inferior frontal gyrus; CC, cingulate cortex; Hipp, hippocampus; rHipp, rostral hippocampus; cHipp, caudal hippocampus; PhG, parahippocampal gyrus; FusG, fusiform gyrus; PCun, precuneus; pm, posterior medial; am, anterior medial; post, posterior; ant, anterior; dl, dorsolateral; rc, rostrocaudal; vl, ventrolateral.

  • Fig. 3 Connectivity modulation between right anterior MFG and memory systems during memory suppression.

    Connectivity differences during the suppression of intrusive versus nonintrusive memories, between the right anterior MFG (seed) and target memory regions in the left (top panel) and right (bottom panel) hemispheres. Error bars reflect 95% bootstrapped confidence intervals and indicate significance when they do not encompass zero. Black and white stars indicate PFDR < 0.05 and P < 0.05, respectively. rost., rostral; caud., caudal; cx., cortex; vent., ventral.

  • Fig. 4 Suppression-induced connectivity against rest.

    Connectivity differences induced by the suppression of intrusive (A) and nonintrusive (B) memories against a resting-state baseline, using the right anterior MFG as seed and memory regions as targets. Error bars reflect 95% bootstrapped confidence intervals and indicate significance when they do not encompass zero. Black and white stars indicate PFDR < 0.05 and P < 0.05, respectively.

  • Fig. 5 DCM model space and coupling parameters.

    (A) Bottom-up and top-down influences between the right anterior MFG and memory regions during suppression attempts were measured across seven DCM models capturing different connection pathways. The modulatory input acting on these connections reflected the difference in coupling between intrusive and nonintrusive memories. Memory target regions included rostral hippocampus (Hip), parahippocampal cortex (PhC), and precuneus (PC). (B) Bayesian model averaging across model space of the top-down and bottom-up modulatory parameters. Error bars reflect 95% confidence intervals and indicate significance when they do not encompass zero.

  • Resilience after trauma: The role of memory suppression

    Alison Mary, Jacques Dayan, Giovanni Leone, Charlotte Postel, Florence Fraisse, Carine Malle, Thomas Vallée, Carine Klein-Peschanski, Fausto Viader, Vincent de la Sayette, Denis Peschanski, Francis Eustache, Pierre Gagnepain

    Materials/Methods, Supplementary Text, Tables, Figures, and/or References

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    • Figs. S1 to S5 
    • Tables S1 to S15

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