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Neural patterns differentiate traumatic from sad autobiographical memories in PTSD

Nature Neuroscience volume 26, pages 2226–2236 (2023)Cite this article

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Abstract

For people with post-traumatic stress disorder (PTSD), recall of traumatic memories often displays as intrusions that differ profoundly from processing of ‘regular’ negative memories. These mnemonic features fueled theories speculating a unique cognitive state linked with traumatic memories. Yet, to date, little empirical evidence supports this view. Here we examined neural activity of patients with PTSD who were listening to narratives depicting their own memories. An intersubject representational similarity analysis of cross-subject semantic content and neural patterns revealed a differentiation in hippocampal representation by narrative type: semantically similar, sad autobiographical memories elicited similar neural representations across participants. By contrast, within the same individuals, semantically similar trauma memories were not represented similarly. Furthermore, we were able to decode memory type from hippocampal multivoxel patterns. Finally, individual symptom severity modulated semantic representation of the traumatic narratives in the posterior cingulate cortex. Taken together, these findings suggest that traumatic memories are an alternative cognitive entity that deviates from memory per se.

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Fig. 1: Experimental paradigm and semantic analysis framework.
Fig. 2: Semantic similarity across script types.
Fig. 3: Semantic-to-neural similarity analysis of hippocampal patterns.
Fig. 4: Memory type can be decoded from hippocampal patterns.
Fig. 5: Symptom severity modulates PCC representation of PTSD memory.

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Data availability

Data supporting the findings of this present study are deposited at https://osf.io/dc7jb. The Harvard–Oxford atlas is available at https://neurovault.org/collections/262. The Willard atlas is available at https://pyhrf.github.io/manual/parcellation_mask.html. The set of analyses described in the present study was not preregistered.

Code availability

The scripts used for data analysis are available at https://osf.io/dc7jb. The fMRI preprocessing was done in fMRIPrep and analyses were conducted primarily in MATLAB R2018b, R2020a and R2021a (MathWorks).

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Acknowledgements

We thank T. Orederu and Y. Yeshurun for helpful discussions. We also thank A. Ben Yakov and A. Ravia for their advice on analysis and preprocessing. The main source of funding for the present study was provided by: Independent Investigator Grant (no. 23260) from the Brain and Behavior Research Foundation (Institute of Human Relations (IHR)), Clinical Neurosciences Division of the National Center for PTSD (IHR), a private donation from the American Brain Society (IHR) and the Yale Center for Clinical Investigation, supported by a CTSA grant from the National Center for Advancing Translational Science, a component of the National Institutes of Health (NIH). Funding was also provided by the NIH (grant nos. R01MH122611 and R01MH123069) and The Ream Foundation to D.S. The contents of the manuscript are solely the responsibility of the authors and do not necessarily represent the official view of the NIH.

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Author notes

  1. These authors contributed equally: Ilan Harpaz-Rotem, Daniela Schiller.

Authors and Affiliations

  1. Center for Computational Psychiatry, Icahn School of Medicine at Mount Sinai, New York, NY, USA

    Ofer Perl, Kaustubh R. Kulkarni & Daniela Schiller

  2. Department of Psychiatry, Icahn School of Medicine at Mount Sinai, New York, NY, USA

    Ofer Perl & Kaustubh R. Kulkarni

  3. Nash Family Department of Neuroscience, Icahn School of Medicine at Mount Sinai, New York, NY, USA

    Ofer Perl, Kaustubh R. Kulkarni & Daniela Schiller

  4. Department of Epidemiology, Biostatistics and Community Health Sciences, School of Public Health, Ben-Gurion University of the Negev, Beer-Sheva, Israel

    Or Duek

  5. Department of Psychiatry, Yale University School of Medicine, New Haven, CT, USA

    Or Duek, Charles Gordon, John H. Krystal & Ilan Harpaz-Rotem

  6. The National Center for PTSD, VA CT Healthcare System, West Haven, CT, USA

    Or Duek, Charles Gordon, John H. Krystal & Ilan Harpaz-Rotem

  7. Departments of Comparative Medicine and Neuroscience, Yale University, New Haven, CT, USA

    Ifat Levy

  8. Department of Psychology and the Wu Tsai Institute, Yale University, New Haven, CT, USA

    Ifat Levy & Ilan Harpaz-Rotem

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Contributions

O.P. conceptualized analyses, conducted and interpreted analyses and visualization, wrote the original draft and edited the paper. O.D. collected data, interpreted data analyses and edited the final paper. K.R.K. analyzed the data. C.G. collected data. J.H.K. obtained funding and edited the final paper. I.L. designed the study, interpreted data analyses and cowrote the paper. I.H.R. designed the study, obtained funding, collected data, interpreted the data analyses and cowrote the paper. D.S. conceptualized analyses, interpreted analyses, obtained funding, wrote the original draft and edited the paper.

Corresponding authors

Correspondence to Ilan Harpaz-Rotem or Daniela Schiller.

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Nature Neuroscience thanks Choong-Wan Woo and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.

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Supplementary Figs. 1–14 and Tables 1–3.

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Perl, O., Duek, O., Kulkarni, K.R. et al. Neural patterns differentiate traumatic from sad autobiographical memories in PTSD. Nat Neurosci 26, 2226–2236 (2023). https://doi.org/10.1038/s41593-023-01483-5

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