Neuroimaging evidence for a role of neural social stress processing in ethnic minority-associated environmental risk

JAMA Psychiatry. 2014 Jun;71(6):672-80. doi: 10.1001/jamapsychiatry.2014.35.

Abstract

Importance: Relative risk for the brain disorder schizophrenia is more than doubled in ethnic minorities, an effect that is evident across countries and linked to socially relevant cues such as skin color, making ethnic minority status a well-established social environmental risk factor. Pathoepidemiological models propose a role for chronic social stress and perceived discrimination for mental health risk in ethnic minorities, but the neurobiology is unexplored.

Objective: To study neural social stress processing, using functional magnetic resonance imaging, and associations with perceived discrimination in ethnic minority individuals.

Design, setting, and participants: Cross-sectional design in a university setting using 3 validated paradigms to challenge neural social stress processing and, to probe for specificity, emotional and cognitive brain functions. Healthy participants included those with German lineage (n = 40) and those of ethnic minority (n = 40) from different ethnic backgrounds matched for sociodemographic, psychological, and task performance characteristics. Control comparisons examined stress processing with matched ethnic background of investigators (23 Turkish vs 23 German participants) and basic emotional and cognitive tasks (24 Turkish vs 24 German participants).

Main outcomes and measures: Blood oxygenation level-dependent response, functional connectivity, and psychological and physiological measures.

Results: There were significant increases in heart rate (P < .001), subjective emotional response (self-related emotions, P < .001; subjective anxiety, P = .006), and salivary cortisol level (P = .004) during functional magnetic resonance imaging stress induction. Ethnic minority individuals had significantly higher perceived chronic stress levels (P = .02) as well as increased activation (family-wise error-corrected [FWE] P = .005, region of interest corrected) and increased functional connectivity (PFWE = .01, region of interest corrected) of perigenual anterior cingulate cortex (ACC). The effects were specific to stress and not explained by a social distance effect. Ethnic minority individuals had significant correlations between perceived group discrimination and activation in perigenual ACC (PFWE = .001, region of interest corrected) and ventral striatum (PFWE = .02, whole brain corrected) and mediation of the relationship between perceived discrimination and perigenual ACC-dorsal ACC connectivity by chronic stress (P < .05).

Conclusions and relevance: Epidemiologists proposed a causal role of social-evaluative stress, but the neural processes that could mediate this susceptibility effect were unknown. Our data demonstrate the potential of investigating associations from epidemiology with neuroimaging, suggest brain effects of social marginalization, and highlight a neural system in which environmental and genetic risk factors for mental illness may converge.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Brain Mapping
  • Corpus Striatum / physiopathology*
  • Cross-Sectional Studies
  • Emotions / physiology
  • Ethnicity / psychology*
  • Gyrus Cinguli / physiopathology*
  • Heart Rate / physiology
  • Humans
  • Hydrocortisone / metabolism
  • Magnetic Resonance Imaging
  • Minority Groups / psychology*
  • Psychological Distance
  • Saliva / metabolism
  • Social Discrimination / psychology*
  • Stress, Psychological / physiopathology*
  • Stress, Psychological / psychology*

Substances

  • Hydrocortisone