Neural Responsivity to Reward Versus Punishment Shortly After Trauma Predicts Long-Term Development of Posttraumatic Stress Symptoms

  • Ziv Ben-Zion
    Affiliations
    Sagol Brain Institute Tel Aviv, Wohl Institute for Advanced Imaging, Tel Aviv Sourasky Medical Center, Tel Aviv, Israel

    Sagol School of Neuroscience, Tel Aviv University, Tel Aviv, Israel

    Departments of Comparative Medicine and Psychiatry, Yale University School of Medicine, New Haven, Connecticut

    U.S. Department of Veterans Affairs National Center for Posttraumatic Stress Disorder, The Clinical Neurosciences Division, VA Connecticut Healthcare System, West Haven, Connecticut
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  • Ofir Shany
    Affiliations
    Sagol Brain Institute Tel Aviv, Wohl Institute for Advanced Imaging, Tel Aviv Sourasky Medical Center, Tel Aviv, Israel

    School of Psychological Sciences, Faculty of Social Sciences, Tel Aviv University, Tel Aviv, Israel
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  • Roee Admon
    Affiliations
    School of Psychological Sciences, University of Haifa, Haifa, Israel

    Integrated Brain and Behavior Research Center, University of Haifa, Haifa, Israel
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  • Nimrod Jackob Keynan
    Affiliations
    Sagol Brain Institute Tel Aviv, Wohl Institute for Advanced Imaging, Tel Aviv Sourasky Medical Center, Tel Aviv, Israel

    Department of Psychiatry and Behavioral Sciences, Stanford University School of Medicine, Stanford, California
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  • Netanell Avisdris
    Affiliations
    Sagol Brain Institute Tel Aviv, Wohl Institute for Advanced Imaging, Tel Aviv Sourasky Medical Center, Tel Aviv, Israel

    School of Computer Science and Engineering, Hebrew University of Jerusalem, Jerusalem, Israel
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  • Shira Reznik Balter
    Affiliations
    Sagol Brain Institute Tel Aviv, Wohl Institute for Advanced Imaging, Tel Aviv Sourasky Medical Center, Tel Aviv, Israel
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  • Arieh Y. Shalev
    Affiliations
    Department of Psychiatry, NYU Langone Medical Center, New York, New York
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  • Israel Liberzon
    Affiliations
    Department of Psychiatry, Texas A&M Health Science Center, Texas
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  • Talma Hendler
    Correspondence
    Address correspondence to Talma Hendler, M.D. Ph.D.
    Affiliations
    Sagol Brain Institute Tel Aviv, Wohl Institute for Advanced Imaging, Tel Aviv Sourasky Medical Center, Tel Aviv, Israel

    Sagol School of Neuroscience, Tel Aviv University, Tel Aviv, Israel

    Sackler Faculty of Medicine, Tel Aviv University, Tel Aviv, Israel

    School of Psychological Sciences, Faculty of Social Sciences, Tel Aviv University, Tel Aviv, Israel
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Published:September 14, 2021DOI:https://doi.org/10.1016/j.bpsc.2021.09.001

      Abstract

      Background

      Processing negatively and positively valenced stimuli involves multiple brain regions including the amygdala and ventral striatum (VS). Posttraumatic stress disorder (PTSD) is often associated with hyperresponsivity to negatively valenced stimuli, yet recent evidence also points to deficient positive valence functioning. It is yet unclear what the relative contribution is of such opposing valence processing shortly after trauma to the development of chronic PTSD.

      Methods

      Neurobehavioral indicators of motivational positive versus negative valence sensitivities were longitudinally assessed in 171 adults (87 females, age = 34.19 ± 11.47 years) at 1, 6, and 14 months following trauma exposure (time point 1 [TP1], TP2, and TP3, respectively). Using a gambling functional magnetic resonance imaging paradigm, amygdala and VS functionality (activity and functional connectivity with the prefrontal cortex) in response to rewards versus punishments were assessed with relation to PTSD severity at different time points. The effect of valence processing was depicted behaviorally by the amount of risk taken to maximize reward.

      Results

      PTSD severity at TP1 was associated with greater neural functionality in the amygdala (but not in the VS) toward punishments versus rewards, and with fewer risky choices. PTSD severity at TP3 was associated with decreased neural functionality in both the VS and the amygdala toward rewards versus punishments at TP1 (but not with risky behavior). Explainable machine learning revealed the primacy of VS-biased processing, over the amygdala, in predicting PTSD severity at TP3.

      Conclusions

      These results highlight the importance of biased neural responsivity to positive relative to negative motivational outcomes in PTSD development. Novel therapeutic strategies early after trauma may thus target both valence fronts.

      Keywords

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