Effects of city living on the mesolimbic reward system-An fmri study

Abstract

Based on higher prevalence rates of several mental disorders for city dwellers, psychosocial stress effects of urban living have been proposed as an environmental risk factor contributing to the development of mental disorders. Recently, it was shown that amygdala activation differs between city dwellers and rural residents in response to a cognitive-social stressor. Besides its influence on the amygdala, chronic stress also affects mesocorticolimbic brain regions involved in reward processing, and stress-related dysregulation of the mesocorticolimbic dopamine system is thought to contribute to onset and manifestation of psychiatric disorders. Here, we investigated differences in reward systems functioning in 147 healthy subjects living either in cities or in less urban areas by means of functional magnetic resonance imaging during performance of the desire-reason-dilemma paradigm, which permits a targeted investigation of bottom-up activation and top-down regulation of the reward circuit. Compared with subjects from less urban areas, city dwellers showed an altered activation and modulation capability of the midbrain (VTA) dopamine system. City dwellers also revealed increased responses in other brain regions involved in reward processing and in the regulation of stress and emotions, such as amygdala, orbitofrontal, and pregenual anterior cingulate cortex. These results provide further evidence for effects of an urban environment on the mesolimbic dopamine system and the limbic system which may increase the risk to develop mental disorders. Hum Brain Mapp 38:3444-3453, 2017. © 2017 Wiley Periodicals, Inc.

Keywords: affective disorders; environmental factors; neuroimaging; schizophrenic disorders; stress.

Figure 1

The desire‐reason dilemma paradigm. Participants performed the task with two target colors presented at the beginning of each block. Successful performance of this task was the superordinate goal to gain 50 points per block. In the Desire Context (DC: top row), participants were allowed to also accept reward colors (e.g., green) to gain additional 10 bonus points. The contingency between color and reward was established before the experiment. By contrast, in the Reason Context (RC: bottom row), these reward stimuli had to be rejected if they did not match one of the target colors. The error to accept conditioned reward stimuli during the RC block led to the loss of the 50 points. [Color figure can be viewed at http://wileyonlinelibrary.com]

Figure 2

Relationship between city living and VTA activation by rewards (full sample, N = 147). Reduced bottom–up activation of left VTA by conditioned reward stimuli in low vs high urbanicity subjects [−4; −16; −14], t ₂₉₀ = 3.26, P = 0.009 svc in DC; image shown at P < 0.001. [Color figure can be viewed at http://wileyonlinelibrary.com]

Figure 3

Reduced modulation capability of left VTA in participants with high current urbanicity (CU) scores (full sample, N = 147). Compared to participants living in small town/rural areas, the ones living in cities (high CU) showed both decreased bottom–up activation and reduced top–down suppression of reward‐related activity in the left VTA. Bars show the parameter estimates of the left VTA when subjects with low CU (left bars) and high CU (right bars) accepted the conditioned reward stimuli in the DC and rejected it in the RC; error bars denote standard error.

Figure 4

Effects of city living on amygdala activity in the desire context (DC) (full sample, N = 147). T‐map shows the result of the post‐hoc comparison between subjects with high versus low urbanicity score when they accepted the additional reward in desire context. Significantly higher amygdala activation (blue circles, left [−20; −2; −16] t ₂₉₀ = 2.76, P = 0.032 svc; right [22; −2; −18], t ₂₉₀ = 3.64, P = 0.002 svc) was observed for subjects with high urbanicity scores. Crosshair at 0 −2 −18; for display purposes, the image is shown at P < 0.005 uncorrected. [Color figure can be viewed at http://wileyonlinelibrary.com]