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Original Investigation |

Neuroimaging Evidence for a Role of Neural Social Stress Processing in Ethnic Minority–Associated Environmental Risk

Ceren Akdeniz, MSc1; Heike Tost, MD, PhD1; Fabian Streit, MSc1; Leila Haddad, MSc1; Stefan Wüst, PhD1,2; Axel Schäfer, PhD1; Michael Schneider, MD1; Marcella Rietschel, MD, PhD1; Peter Kirsch, PhD1; Andreas Meyer-Lindenberg, MD, PhD1
[+] Author Affiliations
1Central Institute of Mental Health, University of Heidelberg, Medical Faculty Mannheim, Mannheim, Germany
2now with Institute of Experimental Psychology, University of Regensburg, Regensburg, Germany
JAMA Psychiatry. 2014;71(6):672-680. doi:10.1001/jamapsychiatry.2014.35.
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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.

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Figure 1.
Experimental Setup of the Social Stress Paradigm

In the social stress condition, shown here, investigators faced the participants, directed their attention to the participant’s performance, and provided disapproving visual feedback after incorrect or slow responses. This was done by pressing a buzzer-shaped button device visible on live video stream, which prompted negative visual feedback on the task screen (“Error!” or “Respond faster!”). In addition, after the first of 2 runs, participants received negative verbal feedback indicating that the participant’s performance was below average. In the control condition (not shown), investigators disengaged their attention from the participant and no feedback was provided. To account for the ethnic social distance of participants to the experimenters, experiments were conducted by either German (A) or Turkish (B) investigator teams.

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Figure 2.
Altered Neural Stress Processing in Perigenual Anterior Cingulate Cortex in Ethnic Minority Individuals and Relationship to Perceived Group Discrimination

A, Significant increase in perigenual anterior cingulate cortex (pACC) activation in an ethnic minority sample compared with a German sample during stress processing (t = 4.18; family-wise error–corrected [FWE] P = .005, region of interest corrected) displayed on sagittal (left) and coronal (right) sections of a structural-template magnetic resonance image. Functional maps are thresholded at P = .001, uncorrected, for presentation purposes. MNI indicates Montreal Neurological Institute. B, Mean contrast estimates extracted from the peak voxel of the analysis. The MNI coordinates are x = 6, y = 44, z = 0. Error bars indicate standard error of the mean. C, Significant correlation of ventral striatum (t = 5.65; PFWE = .02, whole brain corrected) and pACC activation (t = 5.33; PFWE = .001, region of interest corrected) with perceived group discrimination in ethnic minority individuals. Functional maps are thresholded at P = .001, uncorrected, for presentation purposes and are displayed on sagittal (left) and coronal (right) sections of a structural-template magnetic resonance image. D, Scatterplot of the correlation of ventral striatum parameter estimates extracted from the peak voxel (MNI coordinates are x = −9, y = 5, z = −9) and perceived discrimination scores.

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Figure 3.
Altered Perigenual Anterior Cingulate Cortex–Dorsal Anterior Cingulate Cortex Functional Connectivity in Ethnic Minority Individuals

A, Significant increase in perigenual anterior cingulate cortex–dorsal anterior cingulate cortex (dACC) functional connectivity during social stress in ethnic minority individuals compared with German comparison participants during stress processing (t = 3.70; family-wise error–corrected P = .01, region of interest corrected) displayed on sagittal (left) and coronal (right) sections of a structural-template magnetic resonance image. Functional maps are thresholded at P = .005, uncorrected, for presentation purposes. MNI indicates Montreal Neurological Institute. B, Mean contrast estimates extracted from the peak voxel (MNI coordinates are x = 6, y = 14, z = 25). Error bars indicate standard error of the mean.

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