Reward neurocircuitry predicts longitudinal changes in alcohol use following trauma exposure

Cecilia A Hinojosa; Sanne J H van Rooij; Negar Fani; Robyn A Ellis; Nathaniel G Harnett; Lauren A M Lebois; Timothy D Ely; Tanja Jovanovic; Vishnu P Murty; Stacey L House; Francesca L Beaudoin; Xinming An; Thomas C Neylan; Gari D Clifford; Sarah D Linnstaedt; Laura T Germine; Scott L Rauch; John P Haran; Alan B Storrow; Christopher Lewandowski; Paul I Musey Jr; Phyllis L Hendry; Sophia Sheikh; Christopher W Jones; Brittany E Punches; Lauren A Hudak; Jose L Pascual; Mark J Seamon; Erica Harris; Claire Pearson; David A Peak; Roland C Merchant; Robert M Domeier; Niels K Rathlev; Brian J O'Neil; Paulina Sergot; Steven E Bruce; Diego A Pizzagalli; John F Sheridan; Steven E Harte; Karestan C Koenen; Ronald C Kessler; Samuel A McLean; Kerry J Ressler; Jennifer S Stevens

doi:10.1016/j.bpsc.2024.09.015

Reward neurocircuitry predicts longitudinal changes in alcohol use following trauma exposure

Biol Psychiatry Cogn Neurosci Neuroimaging. 2024 Oct 8:S2451-9022(24)00283-0. doi: 10.1016/j.bpsc.2024.09.015. Online ahead of print.

Authors

Cecilia A Hinojosa¹, Sanne J H van Rooij², Negar Fani², Robyn A Ellis³, Nathaniel G Harnett⁴, Lauren A M Lebois⁴, Timothy D Ely², Tanja Jovanovic⁵, Vishnu P Murty⁶, Stacey L House⁷, Francesca L Beaudoin⁸, Xinming An⁹, Thomas C Neylan¹⁰, Gari D Clifford¹¹, Sarah D Linnstaedt⁹, Laura T Germine¹², Scott L Rauch¹³, John P Haran¹⁴, Alan B Storrow¹⁵, Christopher Lewandowski¹⁶, Paul I Musey Jr¹⁷, Phyllis L Hendry¹⁸, Sophia Sheikh¹⁸, Christopher W Jones¹⁹, Brittany E Punches²⁰, Lauren A Hudak²¹, Jose L Pascual²², Mark J Seamon²³, Erica Harris²⁴, Claire Pearson²⁵, David A Peak²⁶, Roland C Merchant²⁷, Robert M Domeier²⁸, Niels K Rathlev²⁹, Brian J O'Neil³⁰, Paulina Sergot³¹, Steven E Bruce³², Diego A Pizzagalli⁴, John F Sheridan³³, Steven E Harte³⁴, Karestan C Koenen³⁵, Ronald C Kessler³⁶, Samuel A McLean³⁷, Kerry J Ressler⁴, Jennifer S Stevens²

Affiliations

¹ Department of Psychiatry and Behavioral Sciences, Emory University School of Medicine, Atlanta, GA, USA. Electronic address: [email protected].
² Department of Psychiatry and Behavioral Sciences, Emory University School of Medicine, Atlanta, GA, USA.
³ McLean Hospital, Belmont, MA, USA; Department of Psychiatry, Harvard Medical School, Boston, MA, USA.
⁴ Department of Psychiatry, Harvard Medical School, Boston, MA, USA; Division of Depression and Anxiety, McLean Hospital, Belmont, MA, USA.
⁵ Department of Psychiatry and Behavioral Neurosciences, Wayne State University, Detroit, MI, USA.
⁶ Department of Psychology, Temple University, Philadelphia, PA, USA.
⁷ Department of Emergency Medicine, Washington University School of Medicine, St. Louis, MO, USA.
⁸ Department of Health Services, Policy, and Practice, The Alpert Medical School of Brown University, Providence, RI, USA; Department of Emergency Medicine, The Alpert Medical School of Brown University, Providence, RI.
⁹ Institute for Trauma Recovery, Department of Anesthesiology, University of North Carolina at Chapel Hill, Chapel Hill, NC, USA.
¹⁰ Departments of Psychiatry and Neurology, University of California San Francisco, San Francisco, CA, USA.
¹¹ Department of Biomedical Informatics, Emory University School of Medicine, Atlanta, GA, USA; Department of Biomedical Engineering, Georgia Institute of Technology and Emory University, Atlanta, GA, USA.
¹² Department of Psychiatry, Harvard Medical School, Boston, MA, USA; Institute for Technology in Psychiatry, McLean Hospital, Belmont, MA, USA; The Many Brains Project, Belmont, MA, USA.
¹³ Department of Psychiatry, Harvard Medical School, Boston, MA, USA; Institute for Technology in Psychiatry, McLean Hospital, Belmont, MA, USA; Department of Psychiatry, McLean Hospital, Belmont, MA, USA.
¹⁴ Department of Emergency Medicine, University of Massachusetts Chan Medical School, Worcester, MA, USA.
¹⁵ Department of Emergency Medicine, Vanderbilt University Medical Center, Nashville, TN, USA.
¹⁶ Department of Emergency Medicine, Henry Ford Health System, Detroit, MI, USA.
¹⁷ Department of Emergency Medicine, Indiana University School of Medicine, Indianapolis, IN, USA.
¹⁸ Department of Emergency Medicine, University of Florida College of Medicine -Jacksonville, Jacksonville, FL, USA.
¹⁹ Department of Emergency Medicine, Cooper Medical School of Rowan University, Camden, NJ, USA.
²⁰ Department of Emergency Medicine, Ohio State University College of Medicine, Columbus, OH, USA; Ohio State University College of Nursing, Columbus, OH, USA.
²¹ Department of Emergency Medicine, Emory University School of Medicine, Atlanta, GA, USA.
²² Department of Surgery, Department of Neurosurgery, University of Pennsylvania, Philadelphia, PA, USA; Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA, USA.
²³ Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA, USA; Department of Surgery, Division of Traumatology, Surgical Critical Care and Emergency Surgery, University of Pennsylvania, Philadelphia, PA, USA.
²⁴ Department of Emergency Medicine, Einstein Medical Center, Philadelphia, PA, USA.
²⁵ Department of Emergency Medicine, Wayne State University, Ascension St. John Hospital, Detroit, MI, USA.
²⁶ Department of Emergency Medicine, Massachusetts General Hospital, Boston, MA, USA.
²⁷ Department of Emergency Medicine, Brigham and Women's Hospital, Boston, MA, USA.
²⁸ Department of Emergency Medicine, Trinity Health-Ann Arbor, Ypsilanti, MI, USA.
²⁹ Department of Emergency Medicine, University of Massachusetts Medical School-Baystate, Springfield, MA, USA.
³⁰ Department of Emergency Medicine, Wayne State University, Detroit Receiving Hospital, Detroit, MI, USA.
³¹ Department of Emergency Medicine, McGovern Medical School at UTHealth, Houston, TX, USA.
³² Department of Psychological Sciences, University of Missouri - St. Louis, St. Louis, MO, USA.
³³ Division of Biosciences, Ohio State University College of Dentistry, Columbus, OH, USA; Institute for Behavioral Medicine Research, OSU Wexner Medical Center, Columbus, OH, USA.
³⁴ Department of Anesthesiology, University of Michigan Medical School, Ann Arbor, MI, USA; Department of Internal Medicine-Rheumatology, University of Michigan Medical School, Ann Arbor, MI, USA.
³⁵ Department of Epidemiology, Harvard T.H. Chan School of Public Health, Harvard University, Boston, MA, USA.
³⁶ Department of Health Care Policy, Harvard Medical School, Boston, MA, USA.
³⁷ Department of Emergency Medicine, University of North Carolina at Chapel Hill, Chapel Hill, NC, USA; Institute for Trauma Recovery, Department of Psychiatry, University of North Carolina at Chapel Hill, Chapel Hill, NC, USA.

PMID: 39389310
DOI: 10.1016/j.bpsc.2024.09.015

Abstract

Background: Trauma is a risk factor for developing maladaptive alcohol use. Preclinical research has shown that stress alters the processing of midbrain and striatal reward and incentive signals. However, little research has been conducted on alterations in reward-related neurocircuitry post-trauma in humans. Neuroimaging markers may be particularly useful as they can provide insight into the mechanisms that may make an individual vulnerable to developing trauma-related psychopathologies. This study aimed to identify reward-related neural correlates associated with changes in alcohol use after trauma exposure.

Methods: Participants were recruited from U.S. emergency departments for the AURORA study (N=286, 178 female). Trauma-related change in alcohol use at 8 weeks post-trauma relative to pre-trauma was quantified as a change in 30-day total drinking per the PhenX Toolkit Alcohol 30-Day Quantity and Frequency Measure. Reward-related neurocircuitry activation and functional connectivity (FC) were assessed 2 weeks post-trauma using fMRI during a monetary reward task using region of interest and whole-brain voxelwise analyses.

Results: Greater increase in alcohol use from pre-trauma to 8 weeks post-trauma was predicted by (1) greater ventral tegmental area (VTA) and (2) greater cerebellum activation during Gain>Loss trials measured 2 weeks post-trauma and (3) greater seed-based FC between the VTA and lateral occipital cortex and precuneus.

Conclusions: Altered VTA activation and FC early post-trauma may be associated with reward-seeking and processing, contributing to greater alcohol use post-trauma. These data provide novel evidence of neural correlates that underlie increased alcohol use early post-trauma that may be targeted via early interventions to prevent the development of maladaptive alcohol use.

Grants and funding

U01 MH110925/MH/NIMH NIH HHS/United States