Associations between urban upbringing and cortical thickness and gyrification.

Urbanicity has been linked to several psychiatric disorders, especially schizophrenia. Recent studies suggest effects of urban upbringing and stress on brain structure and function. Here, we used surface-based and voxel-based morphometry to study the effects of urban upbringing in different environments on variation in brain structure in a non-clinical sample. We recruited 85 young and healthy individuals from the community and recorded urban vs. rural background in their first 15 years of live. All participants underwent T1-weighted 3T MRI, which were then processed via CAT12 toolbox (in SPM12) to analyse cortical volume, thickness and gyrification. These parameters were correlated with an established measure of cumulative childhood and adolescence exposure to urban environments. We found significant (p < 0.05, FWE-corrected) negative correlations of cortical thickness with higher index of urban upbringing in the left dorsolateral prefrontal cortex, bilateral medial prefrontal cortices, as well as temporal cortices including the left superior temporal and left parahippocampal cortex. In contrast, results for volume and gyrification (incl. left posterior cingulate cortex) did not survive correction for multiple comparisons. We show a strong association of early-life urbanicity with cortical thickness in several areas, which are also impaired in schizophrenia patients. Along with other findings, these results converge on the dorsolateral prefrontal cortex as an area mediating this environmental risk.

[1]  Dinggang Shen,et al.  Surface Vulnerability of Cerebral Cortex to Major Depressive Disorder , 2015, PloS one.

[2]  Anders M. Dale,et al.  An automated labeling system for subdividing the human cerebral cortex on MRI scans into gyral based regions of interest , 2006, NeuroImage.

[3]  Stephen M. Smith,et al.  Threshold-free cluster enhancement: Addressing problems of smoothing, threshold dependence and localisation in cluster inference , 2009, NeuroImage.

[4]  Peter Kirsch,et al.  Brain structure correlates of urban upbringing, an environmental risk factor for schizophrenia. , 2015, Schizophrenia bulletin.

[5]  R. C. Oldfield The assessment and analysis of handedness: the Edinburgh inventory. , 1971, Neuropsychologia.

[6]  Lachlan T. Strike,et al.  Cortical abnormalities in adults and adolescents with major depression based on brain scans from 20 cohorts worldwide in the ENIGMA Major Depressive Disorder Working Group , 2016, Molecular Psychiatry.

[7]  J. Peen,et al.  The current status of urban‐rural differences in psychiatric disorders , 2010, Acta psychiatrica Scandinavica.

[8]  R. McCarley,et al.  A review of MRI findings in schizophrenia , 2001, Schizophrenia Research.

[9]  Rainer Goebel,et al.  Default Mode Network Connectivity as a Function of Familial and Environmental Risk for Psychotic Disorder , 2015, PloS one.

[10]  H. Sauer,et al.  Patterns of cortical thinning in different subgroups of schizophrenia. , 2015, The British journal of psychiatry : the journal of mental science.

[11]  Jagath C. Rajapakse,et al.  Statistical approach to segmentation of single-channel cerebral MR images , 1997, IEEE Transactions on Medical Imaging.

[12]  S. Sarkar,et al.  Urban living and psychosis--an overview. , 2014, Asian journal of psychiatry.

[13]  R. Faris Mental disorders in urban areas , 1939 .

[14]  L. Derogatis,et al.  The SCL-90 and the MMPI: A Step in the Validation of a New Self-Report Scale , 1976, British Journal of Psychiatry.

[15]  R. Poulton,et al.  Gene-environment interactions in schizophrenia: review of epidemiological findings and future directions. , 2008, Schizophrenia bulletin.

[16]  L. Opler,et al.  The Positive and Negative Syndrome Scale (PANSS): Rationale and Standardisation , 1989, British Journal of Psychiatry.

[17]  L. Petersen,et al.  IQ, the Urban Environment, and Their Impact on Future Schizophrenia Risk in Men , 2017, Schizophrenia bulletin.

[18]  John Ashburner,et al.  A fast diffeomorphic image registration algorithm , 2007, NeuroImage.

[19]  Yuguo Yu,et al.  Enhanced functional connectivity properties of human brains during in-situ nature experience , 2016, PeerJ.

[20]  M. Nordentoft,et al.  A comparison of selected risk factors for unipolar depressive disorder, bipolar affective disorder, schizoaffective disorder, and schizophrenia from a danish population-based cohort. , 2007, The Journal of clinical psychiatry.

[21]  A. David,et al.  Schizophrenia and city life , 1992, The Lancet.

[22]  A. Caspi,et al.  Why Are Children in Urban Neighborhoods at Increased Risk for Psychotic Symptoms? Findings From a UK Longitudinal Cohort Study , 2016, Schizophrenia bulletin.

[23]  Christian Gaser,et al.  Topological correction of brain surface meshes using spherical harmonics , 2010, MICCAI.

[24]  Y. Miyazaki,et al.  Effect of Stimulation by Foliage Plant Display Images on Prefrontal Cortex Activity: A Comparison with Stimulation using Actual Foliage Plants , 2014, Journal of neuroimaging : official journal of the American Society of Neuroimaging.

[25]  Alan C. Evans,et al.  Fast and robust parameter estimation for statistical partial volume models in brain MRI , 2004, NeuroImage.

[26]  M. Rietschel,et al.  A functional variant in the neuropeptide S receptor 1 gene moderates the influence of urban upbringing on stress processing in the amygdala , 2014, Stress.

[27]  Alan C. Evans,et al.  Changes in cortical thickness during the course of illness in schizophrenia. , 2011, Archives of general psychiatry.

[28]  J. Os,et al.  Prevalence of psychotic disorder and community level of psychotic symptoms: an urban-rural comparison. , 2001, Archives of general psychiatry.

[29]  Toshiya Murai,et al.  Distinct Patterns of Cerebral Cortical Thinning in Schizophrenia: A Neuroimaging Data-Driven Approach , 2016, Schizophrenia bulletin.

[30]  M. Keshavan,et al.  The “polyenviromic risk score”: Aggregating environmental risk factors predicts conversion to psychosis in familial high-risk subjects , 2017, Schizophrenia Research.

[31]  Y. Miyazaki,et al.  Physiological and psychological responses of young males during spring-time walks in urban parks , 2014, Journal of Physiological Anthropology.

[32]  A. Granholm,et al.  Long-Term Environmental Enrichment Leads to Regional Increases in Neurotrophin Levels in Rat Brain , 2000, Experimental Neurology.

[33]  C. Pantelis,et al.  Structural neuroimaging across early-stage psychosis: Aberrations in neurobiological trajectories and implications for the staging model , 2017, The Australian and New Zealand journal of psychiatry.

[34]  C. Pantelis,et al.  A review of vulnerability and risks for schizophrenia: Beyond the two hit hypothesis , 2016, Neuroscience & Biobehavioral Reviews.

[35]  Y. Ben-Porath,et al.  Psychotherapeutic outcomes measures: a critical review for practitioners. , 2014, Journal of clinical psychology.

[36]  P. Mortensen,et al.  Evidence of a dose-response relationship between urbanicity during upbringing and schizophrenia risk. , 2001, Archives of general psychiatry.

[37]  Jian Li Wang,et al.  Rural–urban differences in the prevalence of major depression and associated impairment , 2004, Social Psychiatry and Psychiatric Epidemiology.

[38]  Tsutomu Takahashi,et al.  Increased Frontal Gyrification Negatively Correlates with Executive Function in Patients with First‐Episode Schizophrenia , 2016, Cerebral cortex.

[39]  J. van os,et al.  No Evidence of Association between Childhood Urban Environment and Cortical Thinning in Psychotic Disorder , 2017, PloS one.

[40]  J. Dekker,et al.  Is urbanicity an environmental risk-factor for psychiatric disorders? , 2004, The Lancet.

[41]  R. Goebel,et al.  Altered mesocorticolimbic functional connectivity in psychotic disorder: an analysis of proxy genetic and environmental effects , 2015, Psychological Medicine.

[42]  Paul M. Thompson,et al.  A curvature-based approach to estimate local gyrification on the cortical surface , 2006, NeuroImage.

[43]  Yoshifumi Miyazaki,et al.  Effects of stimulation by three-dimensional natural images on prefrontal cortex and autonomic nerve activity: a comparison with stimulation using two-dimensional images , 2014, Cognitive Processing.

[44]  Nikolaus Weiskopf,et al.  A comparison between voxel-based cortical thickness and voxel-based morphometry in normal aging , 2009, NeuroImage.

[45]  K. Lambert,et al.  Brains in the city: Neurobiological effects of urbanization , 2015, Neuroscience & Biobehavioral Reviews.

[46]  I. Gottesman,et al.  The endophenotype concept in psychiatry: etymology and strategic intentions. , 2003, The American journal of psychiatry.

[47]  Katrin Amunts,et al.  Development of cortical folding during evolution and ontogeny , 2013, Trends in Neurosciences.

[48]  Jens C. Pruessner,et al.  City living and urban upbringing affect neural social stress processing in humans , 2011, Nature.

[49]  F. Gage,et al.  Neural consequences of enviromental enrichment , 2000, Nature Reviews Neuroscience.

[50]  H. Sauer,et al.  Prefrontal gyrification in psychotic bipolar I disorder vs. schizophrenia. , 2015, Journal of affective disorders.

[51]  Christian Gaser,et al.  Cortical thickness and central surface estimation , 2013, NeuroImage.