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Differential Roles of Positive and Negative Valence Systems in the Development of Post-Traumatic Stress Psychopathology

View ORCID ProfileZiv Ben-Zion, View ORCID ProfileOfir Shany, View ORCID ProfileRoee Admon, View ORCID ProfileNimrod Jackob Keynan, View ORCID ProfileNetanell Avisdris, View ORCID ProfileShira Reznik Balter, View ORCID ProfileArieh Y. Shalev, View ORCID ProfileIsrael Liberzon, View ORCID ProfileTalma Hendler
doi: https://doi.org/10.1101/2021.03.08.434335
Ziv Ben-Zion
1Sagol Brain Institute Tel-Aviv, Wohl Institute for Advanced Imaging, Tel Aviv Sourasky Medical Center, Tel-Aviv, Israel
2Sagol School of Neuroscience, Tel-Aviv University, Tel-Aviv, Israel
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  • For correspondence: zivbenzion@mail.tau.ac.il zivbz1@gmail.com talma@tlvmc.gov.il thendler@post.tau.ac.il
Ofir Shany
1Sagol Brain Institute Tel-Aviv, Wohl Institute for Advanced Imaging, Tel Aviv Sourasky Medical Center, Tel-Aviv, Israel
3School of Psychological Sciences, Faculty of Social Sciences, Tel-Aviv University, Tel-Aviv, Israel
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Roee Admon
4School of Psychological Sciences, University of Haifa, Haifa, Israel
5The Integrated Brain and Behavior Research Center (IBBRC), University of Haifa, Haifa, Israel
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Nimrod Jackob Keynan
1Sagol Brain Institute Tel-Aviv, Wohl Institute for Advanced Imaging, Tel Aviv Sourasky Medical Center, Tel-Aviv, Israel
6Department of Psychiatry and Behavioral Sciences, Stanford University School of Medicine, Stanford, CA, USA
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Netanell Avisdris
1Sagol Brain Institute Tel-Aviv, Wohl Institute for Advanced Imaging, Tel Aviv Sourasky Medical Center, Tel-Aviv, Israel
7School of Computer Science and Engineering, the Hebrew University of Jerusalem, Jerusalem, Israel
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Shira Reznik Balter
1Sagol Brain Institute Tel-Aviv, Wohl Institute for Advanced Imaging, Tel Aviv Sourasky Medical Center, Tel-Aviv, Israel
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Arieh Y. Shalev
8Department of Psychiatry, NYU Langone Medical Center, New York, NY, USA
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Israel Liberzon
9Department of Psychiatry, Texas A&M Health Science Center, TX, USA
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Talma Hendler
1Sagol Brain Institute Tel-Aviv, Wohl Institute for Advanced Imaging, Tel Aviv Sourasky Medical Center, Tel-Aviv, Israel
2Sagol School of Neuroscience, Tel-Aviv University, Tel-Aviv, Israel
3School of Psychological Sciences, Faculty of Social Sciences, Tel-Aviv University, Tel-Aviv, Israel
10Sackler Faculty of Medicine, Tel-Aviv University, Tel-Aviv, Israel
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Abstract

Negative and positive valence systems (NVS and PVS) pertain to processing of aversive and rewarding stimuli, respectively. Post-Traumatic Stress Disorder (PTSD) has been typically associated with hyper-responsivity of the NVS, and more recently, with deficient PVS functionality. The respective roles of these systems in early PTSD development have yet to be resolved. Here, we assessed neurobehavioral indicators of PVS and NVS longitudinally among 171 adult civilians at 1-, 6-, and 14-months following trauma exposure (TP1, TP2, and TP3). Using the ‘Safe or Risky Domino Choice’ (SRDC) game during fMRI, NVS and PVS functionality (i.e., activity and connectivity) were indicated by the amygdala and ventral striatum (VS) responses to punishments and rewards, respectively. The complementary functionality of these systems was behaviorally assessed as the percentage of risky choices taken during the game. Results revealed that increased amygdala functionality at TP1 was associated with greater PTSD severity at TP1 and TP3, specifically with hyperarousal and intrusion. Decreased VS functionality at TP1 was associated with greater PTSD severity at TP3, specifically with avoidance. Explainable machine learning revealed the primacy of PVS over NVS functionality at TP1 in predicting PTSD severity at TP3. Behaviorally, fewer risky choices were associated with more severe symptoms at TP1, especially with intrusion and avoidance. Overall, these results suggest a differential and potentially complementary involvement of NVS and PVS in PTSD development following trauma. Early therapeutics for PTSD in the immediate aftermath of trauma may thus target both negative and positive valence processing.

Competing Interest Statement

The authors have declared no competing interest.

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Posted March 15, 2021.
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Differential Roles of Positive and Negative Valence Systems in the Development of Post-Traumatic Stress Psychopathology
Ziv Ben-Zion, Ofir Shany, Roee Admon, Nimrod Jackob Keynan, Netanell Avisdris, Shira Reznik Balter, Arieh Y. Shalev, Israel Liberzon, Talma Hendler
bioRxiv 2021.03.08.434335; doi: https://doi.org/10.1101/2021.03.08.434335
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Differential Roles of Positive and Negative Valence Systems in the Development of Post-Traumatic Stress Psychopathology
Ziv Ben-Zion, Ofir Shany, Roee Admon, Nimrod Jackob Keynan, Netanell Avisdris, Shira Reznik Balter, Arieh Y. Shalev, Israel Liberzon, Talma Hendler
bioRxiv 2021.03.08.434335; doi: https://doi.org/10.1101/2021.03.08.434335

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