Neighborhood Disadvantage and Neural Correlates of Threat and Reward Processing in Survivors of Recent Trauma

Author:

Webb E. Kate12,Ely Timothy D.3,Rowland Grace E.1,Lebois Lauren A. M.12,van Rooij Sanne J. H.3,Bruce Steven E.4,Jovanovic Tanja5,House Stacey L.6,Beaudoin Francesca L.78,An Xinming9,Neylan Thomas C.1011,Clifford Gari D.1213,Linnstaedt Sarah D.9,Germine Laura T.21415,Bollen Kenneth A.1617,Rauch Scott L.21518,Haran John P.19,Storrow Alan B.20,Lewandowski Christopher21,Musey Paul I.22,Hendry Phyllis L.23,Sheikh Sophia23,Jones Christopher W.24,Punches Brittany E.2526,Swor Robert A.27,Pascual Jose L.2829,Seamon Mark J.28,Datner Elizabeth M.3031,Pearson Claire32,Peak David A.33,Merchant Roland C.34,Domeier Robert M.35,Rathlev Niels K.36,Sergot Paulina37,Sanchez Leon D.3438,Kessler Ronald C.39,Koenen Karestan C.240,McLean Samuel A.4142,Stevens Jennifer S.3,Ressler Kerry J.12,Harnett Nathaniel G.12

Affiliation:

1. Division of Depression and Anxiety, McLean Hospital, Belmont, Massachusetts

2. Department of Psychiatry, Harvard Medical School, Boston, Massachusetts

3. Department of Psychiatry and Behavioral Sciences, Emory University School of Medicine, Atlanta, Georgia

4. Department of Psychological Sciences, University of Missouri-St Louis

5. Department of Psychiatry and Behavioral Neurosciences, Wayne State University, Detroit, Michigan

6. Department of Emergency Medicine, Washington University School of Medicine, St Louis, Missouri

7. Department of Epidemiology, Brown University, Providence, Rhode Island

8. Department of Emergency Medicine, Brown University, Providence, Rhode Island

9. Institute for Trauma Recovery, Department of Anesthesiology, University of North Carolina at Chapel Hill

10. Department of Psychiatry, University of California, San Francisco

11. Department Neurology, University of California, San Francisco

12. Department of Biomedical Informatics, Emory University School of Medicine, Atlanta, Georgia

13. Department of Biomedical Engineering, Georgia Institute of Technology and Emory University, Atlanta

14. The Many Brains Project, Belmont, Massachusetts

15. Institute for Technology in Psychiatry, Harvard Medical School, Boston, Massachusetts

16. Department of Psychology and Neuroscience, University of North Carolina at Chapel Hill

17. Department of Sociology, University of North Carolina at Chapel Hill

18. Department of Psychiatry, McLean Hospital, Belmont, Massachusetts

19. Department of Emergency Medicine, University of Massachusetts Chan Medical School, Worcester, Massachusetts

20. Department of Emergency Medicine, Vanderbilt University Medical Center, Nashville, TN

21. Department of Emergency Medicine, Henry Ford Health System, Detroit, Michigan

22. Department of Emergency Medicine, Indiana University School of Medicine, Indianapolis

23. Department of Emergency Medicine, University of Florida College of Medicine-Jacksonville

24. Department of Emergency Medicine, Cooper Medical School of Rowan University, Camden, New Jersey

25. Department of Emergency Medicine, Ohio State University College of Medicine, Columbus,

26. College of Nursing, Ohio State University, Columbus

27. Department of Emergency Medicine, Oakland University William Beaumont School of Medicine, Rochester, Michigan

28. Department of Surgery, Division of Traumatology, Surgical Critical Care and Emergency Surgery, Perelman School of Medicine, University of Pennsylvania, Philadelphia

29. Department of Neurosurgery, Perelman School of Medicine, University of Pennsylvania, Philadelphia,

30. Department of Emergency Medicine, Einstein Healthcare Network, Philadelphia, Pennsylvania

31. Department of Emergency Medicine, Sidney Kimmel Medical College, Thomas Jefferson University, Philadelphia, Pennsylvania

32. Department of Emergency Medicine, Wayne State University, Ascension St John Hospital, Detroit, Michigan

33. Department of Emergency Medicine, Massachusetts General Hospital, Boston

34. Department of Emergency Medicine, Brigham and Women’s Hospital, Boston, Massachusetts

35. Department of Emergency Medicine, Trinity Health-Ann Arbor, Ypsilanti, Michigan

36. Department of Emergency Medicine, University of Massachusetts Medical School-Baystate, Springfield

37. Department of Emergency Medicine, McGovern Medical School at UTHealth, Houston, Texas

38. Department of Emergency Medicine, Harvard Medical School, Boston, Massachusetts

39. Department of Health Care Policy, Harvard Medical School, Boston, Massachusetts

40. Department of Epidemiology, Harvard T.H. Chan School of Public Health, Harvard University, Boston, Massachusetts

41. Department of Emergency Medicine, University of North Carolina at Chapel Hill

42. Institute for Trauma Recovery, Department of Psychiatry, University of North Carolina at Chapel Hill

Abstract

ImportanceDifferences in neighborhood socioeconomic characteristics are important considerations in understanding differences in risk vs resilience in mental health. Neighborhood disadvantage is associated with alterations in the function and structure of threat neurocircuitry.ObjectiveTo investigate associations of neighborhood disadvantage with white and gray matter and neural reactivity to positive and negative stimuli in the context of trauma exposure.Design, Setting, and ParticipantsIn this cross-sectional study, survivors of trauma who completed sociodemographic and posttraumatic symptom assessments and neuroimaging were recruited as part of the Advancing Understanding of Recovery After Trauma (AURORA) study between September 2017 and June 2021. Data analysis was performed from October 25, 2022, to February 15, 2023.ExposureNeighborhood disadvantage was measured with the Area Deprivation Index (ADI) for each participant home address.Main Outcomes and MeasuresParticipants completed separate threat and reward tasks during functional magnetic resonance imaging. Diffusion-weighted and high-resolution structural images were also collected. Linear models assessed the association of ADI with reactivity, microstructure, and macrostructure of a priori regions of interest after adjusting for income, lifetime trauma, sex at birth, and age. A moderated-mediation model tested whether ADI was associated with neural activity via microstructural changes and if this was modulated by PTSD symptoms.ResultsA total of 280 participants (183 females [65.4%]; mean [SD] age, 35.39 [13.29] years) completed the threat task and 244 participants (156 females [63.9%]; mean [SD] age, 35.10 [13.26] years) completed the reward task. Higher ADI (per 1-unit increase) was associated with greater insula (t274 = 3.20; β = 0.20; corrected P = .008) and anterior cingulate cortex (ACC; t274 = 2.56; β = 0.16; corrected P = .04) threat-related activity after considering covariates, but ADI was not associated with reward reactivity. Greater disadvantage was also associated with altered microstructure of the cingulum bundle (t274 = 3.48; β = 0.21; corrected P = .001) and gray matter morphology of the ACC (cortical thickness: t273 = −2.29; β = −0.13; corrected P = .02; surface area: t273 = 2.53; β = 0.13; corrected P = .02). The moderated-mediation model revealed that ADI was associated with ACC threat reactivity via cingulum microstructural changes (index of moderated mediation = −0.02). However, this mediation was only present in individuals with greater PTSD symptom severity (at the mean: β = −0.17; standard error = 0.06, t= −2.28; P = .007; at 1 SD above the mean: β = −0.28; standard error = 0.08; t = −3.35; P < .001).Conclusions and RelevanceIn this study, neighborhood disadvantage was associated with neurobiology that supports threat processing, revealing associations of neighborhood disadvantage with neural susceptibility for PTSD and suggesting how altered structure-function associations may complicate symptoms. Future work should investigate specific components of neighborhood disadvantage that may be associated with these outcomes.

Publisher

American Medical Association (AMA)

Subject

General Medicine

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