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

Ziv Ben-Zion, Ofir Shany, Roee Admon, Nimrod Jackob Keynan, Netanell Avisdris, Shira Reznik Balter, Arieh Y. Shalev, Israel Liberzon, Talma Hendler

Research output: Contribution to journalArticlepeer-review

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.

Original languageEnglish
Pages (from-to)150-161
Number of pages12
JournalBiological Psychiatry: Cognitive Neuroscience and Neuroimaging
Volume7
Issue number2
Early online date15 Sep 2021
DOIs
StatePublished - Feb 2022

Bibliographical note

Publisher Copyright:
© 2021 Society of Biological Psychiatry

Keywords

  • Amygdala
  • Functional MRI
  • Negative valence system
  • PTSD
  • Positive valence system
  • Posttraumatic stress disorder
  • Ventral striatum
  • fMRI

ASJC Scopus subject areas

  • Radiology Nuclear Medicine and imaging
  • Cognitive Neuroscience
  • Clinical Neurology
  • Biological Psychiatry

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