City living and urban upbringing affect neural social stress processing in humans

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Abstract

More than half of the world’s population now lives in cities, making the creation of a healthy urban environment a major policy priority1. Cities have both health risks and benefits1, but mental health is negatively affected: mood and anxiety disorders are more prevalent in city dwellers2 and the incidence of schizophrenia is strongly increased in people born and raised in cities3,4,5,6. Although these findings have been widely attributed to the urban social environment2,3,7,8, the neural processes that could mediate such associations are unknown. Here we show, using functional magnetic resonance imaging in three independent experiments, that urban upbringing and city living have dissociable impacts on social evaluative stress processing in humans. Current city living was associated with increased amygdala activity, whereas urban upbringing affected the perigenual anterior cingulate cortex, a key region for regulation of amygdala activity, negative affect9 and stress10. These findings were regionally and behaviourally specific, as no other brain structures were affected and no urbanicity effect was seen during control experiments invoking cognitive processing without stress. Our results identify distinct neural mechanisms for an established environmental risk factor, link the urban environment for the first time to social stress processing, suggest that brain regions differ in vulnerability to this risk factor across the lifespan, and indicate that experimental interrogation of epidemiological associations is a promising strategy in social neuroscience.

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Figure 1: Relationship between current urbanicity and amygdala activation.
Figure 2: Relationship between early life urbanicity scores and pACC activation.

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Acknowledgements

We thank D. Gass and C. Niemeyer for technical assistance. We also thank C. Sauer, O. Grimm, M. Plichta and A. Schäfer for support on data analyses. The research leading to these results has received funding from the European Community’s Seventh Framework Programme under grant agreement No. HEALTH-F2-2010-241909 (Project EU-GEI), German Research Foundation (Deutsche Forschungsgemeinschaft SFB 636-B7) and Federal Ministry of Education and Research (MooDS) to A.M.L. EU-GEI is an acronym for the project “European network of National Schizophrenia Networks Studying Gene–Environment Interactions”. F.S. is a member of the International Research Training Group “Psychoneuroendocrinology of Stress”, Institute of Psychobiology, University of Trier, Germany, granted by the German Research Foundation.

Author information

F.L., P.K and L.H. designed and performed experiments, analysed data and wrote the paper; F.S., P.S. and S.W. designed and performed experiments, analysed data and reviewed the manuscript; H.T. analysed data and reviewed the manuscript; M.D. and M.R. designed experiments and reviewed the manuscript; J.C.P. developed the MIST paradigm and reviewed the manuscript. A.M.-L. obtained funding, designed the study and experiments and wrote the paper.

Correspondence to Andreas Meyer-Lindenberg.

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The authors declare no competing financial interests.

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Supplementary Information

This file contains Supplementary Methods, with additional references, Supplementary Tables 1-3 and Supplementary Figures 1-3 with legends. (PDF 766 kb)

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