Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Review Article
  • Published:

Environmental influence in the brain, human welfare and mental health

Abstract

The developing human brain is shaped by environmental exposures—for better or worse. Many exposures relevant to mental health are genuinely social in nature or believed to have social subcomponents, even those related to more complex societal or area-level influences. The nature of how these social experiences are embedded into the environment may be crucial. Here we review select neuroscience evidence on the neural correlates of adverse and protective social exposures in their environmental context, focusing on human neuroimaging data and supporting cellular and molecular studies in laboratory animals. We also propose the inclusion of innovative methods in social neuroscience research that may provide new and ecologically more valid insight into the social-environmental risk architecture of the human brain.

This is a preview of subscription content, access via your institution

Access options

Buy this article

Prices may be subject to local taxes which are calculated during checkout

Figure 1: Neural correlates of ethnic minority status.
Figure 2: Neural correlates of urban life.
Figure 3: Ecologically enhanced methods for social neuroscience.

Similar content being viewed by others

References

  1. Meyer-Lindenberg, A. & Tost, H. Neural mechanisms of social risk for psychiatric disorders. Nat. Neurosci. 15, 663–668 (2012).

    Article  CAS  PubMed  Google Scholar 

  2. Tost, H. & Meyer-Lindenberg, A. Puzzling over schizophrenia: schizophrenia, social environment and the brain. Nat. Med. 18, 211–213 (2012).

    Article  CAS  PubMed  Google Scholar 

  3. Russo, S.J., Murrough, J.W., Han, M.H., Charney, D.S. & Nestler, E.J. Neurobiology of resilience. Nat. Neurosci. 15, 1475–1484 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Zammit, S. et al. Individuals, schools, and neighborhood: a multilevel longitudinal study of variation in incidence of psychotic disorders. Arch. Gen. Psychiatry 67, 914–922 (2010).

    Article  PubMed  Google Scholar 

  5. Swain, J.E., Perkins, S.C., Dayton, C.J., Finegood, E.D. & Ho, S.S. Parental brain and socioeconomic epigenetic effects in human development. Behav. Brain Sci. 35, 378–379 (2012).

    Article  PubMed  PubMed Central  Google Scholar 

  6. Herman, J.P. & Cullinan, W.E. Neurocircuitry of stress: central control of the hypothalamo-pituitary-adrenocortical axis. Trends Neurosci. 20, 78–84 (1997).

    Article  CAS  PubMed  Google Scholar 

  7. Flinn, M.V., Nepomnaschy, P.A., Muehlenbein, M.P. & Ponzi, D. Evolutionary functions of early social modulation of hypothalamic-pituitary-adrenal axis development in humans. Neurosci. Biobehav. Rev. 35, 1611–1629 (2011).

    Article  CAS  PubMed  Google Scholar 

  8. McEwen, B.S. The brain on stress: toward an integrative approach to brain, body, and behavior. Perspect. Psychol. Sci. 8, 673–675 (2013).

    Article  PubMed  PubMed Central  Google Scholar 

  9. Champagne, F.A. Early environments, glucocorticoid receptors, and behavioral epigenetics. Behav. Neurosci. 127, 628–636 (2013).

    Article  PubMed  Google Scholar 

  10. Carpenter, L.L., Shattuck, T.T., Tyrka, A.R., Geracioti, T.D. & Price, L.H. Effect of childhood physical abuse on cortisol stress response. Psychopharmacology (Berl.) 214, 367–375 (2011).

    Article  CAS  Google Scholar 

  11. Calhoun, C.D. et al. Relational victimization, friendship, and adolescents' hypothalamic-pituitary-adrenal axis responses to an in vivo social stressor. Dev. Psychopathol. 26, 605–618 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  12. Steinheuser, V., Ackermann, K., Schonfeld, P. & Schwabe, L. Stress and the city: impact of urban upbringing on the (re)activity of the hypothalamus-pituitary-adrenal axis. Psychosom. Med. 76, 678–685 (2014).

    Article  CAS  PubMed  Google Scholar 

  13. Gatzke-Kopp, L.M. The canary in the coalmine: the sensitivity of mesolimbic dopamine to environmental adversity during development. Neurosci. Biobehav. Rev. 35, 794–803 (2011).

    Article  CAS  PubMed  Google Scholar 

  14. Alcaro, A., Huber, R. & Panksepp, J. Behavioral functions of the mesolimbic dopaminergic system: an affective neuroethological perspective. Brain Res. Rev. 56, 283–321 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Zoli, M. et al. Nerve cell clusters in dorsal striatum and nucleus accumbens of the male rat demonstrated by glucocorticoid receptor immunoreactivity. J. Chem. Neuroanat. 3, 355–366 (1990).

    CAS  PubMed  Google Scholar 

  16. Barik, J. et al. Chronic stress triggers social aversion via glucocorticoid receptor in dopaminoceptive neurons. Science 339, 332–335 (2013).

    Article  CAS  PubMed  Google Scholar 

  17. Niwa, M. et al. Adolescent stress-induced epigenetic control of dopaminergic neurons via glucocorticoids. Science 339, 335–339 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Meyer-Lindenberg, A., Domes, G., Kirsch, P. & Heinrichs, M. Oxytocin and vasopressin in the human brain: social neuropeptides for translational medicine. Nat. Rev. Neurosci. 12, 524–538 (2011).

    Article  CAS  PubMed  Google Scholar 

  19. Freeman, S.M., Inoue, K., Smith, A.L., Goodman, M.M. & Young, L.J. The neuroanatomical distribution of oxytocin receptor binding and mRNA in the male rhesus macaque (Macaca mulatta). Psychoneuroendocrinology 45, 128–141 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Ross, H.E. & Young, L.J. Oxytocin and the neural mechanisms regulating social cognition and affiliative behavior. Front. Neuroendocrinol. 30, 534–547 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Feldman, R., Weller, A., Zagoory-Sharon, O. & Levine, A. Evidence for a neuroendocrinological foundation of human affiliation: plasma oxytocin levels across pregnancy and the postpartum period predict mother-infant bonding. Psychol. Sci. 18, 965–970 (2007).

    Article  PubMed  Google Scholar 

  22. Smith, A.S. & Wang, Z. Salubrious effects of oxytocin on social stress-induced deficits. Horm. Behav. 61, 320–330 (2012).

    Article  CAS  PubMed  Google Scholar 

  23. Cardoso, C., Kingdon, D. & Ellenbogen, M.A. A meta-analytic review of the impact of intranasal oxytocin administration on cortisol concentrations during laboratory tasks: moderation by method and mental health. Psychoneuroendocrinology 49, 161–170 (2014).

    Article  CAS  PubMed  Google Scholar 

  24. Stoop, R., Hegoburu, C. & van den Burg, E. New opportunities in vasopressin and oxytocin research: a perspective from the amygdala. Annu. Rev. Neurosci. 38, 369–388 (2015).

    Article  CAS  PubMed  Google Scholar 

  25. Champagne, F., Diorio, J., Sharma, S. & Meaney, M.J. Naturally occurring variations in maternal behavior in the rat are associated with differences in estrogen-inducible central oxytocin receptors. Proc. Natl. Acad. Sci. USA 98, 12736–12741 (2001).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Peña, C.J., Neugut, Y.D. & Champagne, F.A. Developmental timing of the effects of maternal care on gene expression and epigenetic regulation of hormone receptor levels in female rats. Endocrinology 154, 4340–4351 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Wang, H., Duclot, F., Liu, Y., Wang, Z. & Kabbaj, M. Histone deacetylase inhibitors facilitate partner preference formation in female prairie voles. Nat. Neurosci. 16, 919–924 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Keebaugh, A.C. & Young, L.J. Increasing oxytocin receptor expression in the nucleus accumbens of pre-pubertal female prairie voles enhances alloparental responsiveness and partner preference formation as adults. Horm. Behav. 60, 498–504 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Peña, C.J., Neugut, Y.D., Calarco, C.A. & Champagne, F.A. Effects of maternal care on the development of midbrain dopamine pathways and reward-directed behavior in female offspring. Eur. J. Neurosci. 39, 946–956 (2014).

    Article  PubMed  Google Scholar 

  30. Liu, Y. & Wang, Z.X. Nucleus accumbens oxytocin and dopamine interact to regulate pair bond formation in female prairie voles. Neuroscience 121, 537–544 (2003).

    Article  CAS  PubMed  Google Scholar 

  31. Riem, M.M., Alink, L.R., Out, D., Van Ijzendoorn, M.H. & Bakermans-Kranenburg, M.J. Beating the brain about abuse: empirical and meta-analytic studies of the association between maltreatment and hippocampal volume across childhood and adolescence. Dev. Psychopathol. 27, 507–520 (2015).

    Article  PubMed  Google Scholar 

  32. Shonkoff, J.P. Leveraging the biology of adversity to address the roots of disparities in health and development. Proc. Natl. Acad. Sci. USA 109 (suppl. 2): 17302–17307 (2012).

    Article  PubMed  PubMed Central  Google Scholar 

  33. Murgatroyd, C. et al. Dynamic DNA methylation programs persistent adverse effects of early-life stress. Nat. Neurosci. 12, 1559–1566 (2009).

    Article  CAS  PubMed  Google Scholar 

  34. Rice, C.J., Sandman, C.A., Lenjavi, M.R. & Baram, T.Z. A novel mouse model for acute and long-lasting consequences of early life stress. Endocrinology 149, 4892–4900 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Wang, X.D. et al. Forebrain CRF(1) modulates early-life stress-programmed cognitive deficits. J. Neurosci. 31, 13625–13634 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Roth, T.L., Lubin, F.D., Funk, A.J. & Sweatt, J.D. Lasting epigenetic influence of early-life adversity on the BDNF gene. Biol. Psychiatry 65, 760–769 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Liu, D., Diorio, J., Day, J.C., Francis, D.D. & Meaney, M.J. Maternal care, hippocampal synaptogenesis and cognitive development in rats. Nat. Neurosci. 3, 799–806 (2000).

    Article  CAS  PubMed  Google Scholar 

  38. Liu, D. et al. Maternal care, hippocampal glucocorticoid receptors, and hypothalamic-pituitary-adrenal responses to stress. Science 277, 1659–1662 (1997).

    Article  CAS  PubMed  Google Scholar 

  39. Weaver, I.C. et al. Epigenetic programming by maternal behavior. Nat. Neurosci. 7, 847–854 (2004).

    Article  CAS  PubMed  Google Scholar 

  40. Cao, Y. et al. Neonatal paternal deprivation impairs social recognition and alters levels of oxytocin and estrogen receptor alpha mRNA expression in the MeA and NAcc, and serum oxytocin in mandarin voles. Horm. Behav. 65, 57–65 (2014).

    Article  CAS  PubMed  Google Scholar 

  41. Seidel, K., Poeggel, G., Holetschka, R., Helmeke, C. & Braun, K. Paternal deprivation affects the development of corticotrophin-releasing factor-expressing neurones in prefrontal cortex, amygdala and hippocampus of the biparental Octodon degus. J. Neuroendocrinol. 23, 1166–1176 (2011).

    Article  CAS  PubMed  Google Scholar 

  42. Biggio, F. et al. Maternal separation attenuates the effect of adolescent social isolation on HPA axis responsiveness in adult rats. Eur. Neuropsychopharmacol. 24, 1152–1161 (2014).

    Article  CAS  PubMed  Google Scholar 

  43. Champagne, D.L. et al. Maternal care and hippocampal plasticity: evidence for experience-dependent structural plasticity, altered synaptic functioning, and differential responsiveness to glucocorticoids and stress. J. Neurosci. 28, 6037–6045 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Hart, H. & Rubia, K. Neuroimaging of child abuse: a critical review. Front. Hum. Neurosci. 6, 52 (2012).

    Article  PubMed  PubMed Central  Google Scholar 

  45. McEwen, B.S. Stress, sex, and neural adaptation to a changing environment: mechanisms of neuronal remodeling. Ann. NY Acad. Sci. 1204 (suppl.), E38–E59 (2010).

    Article  PubMed  Google Scholar 

  46. Woon, F.L. & Hedges, D.W. Hippocampal and amygdala volumes in children and adults with childhood maltreatment-related posttraumatic stress disorder: a meta-analysis. Hippocampus 18, 729–736 (2008).

    Article  PubMed  Google Scholar 

  47. Andersen, S.L. & Teicher, M.H. Delayed effects of early stress on hippocampal development. Neuropsychopharmacology 29, 1988–1993 (2004).

    Article  PubMed  Google Scholar 

  48. Lim, L., Radua, J. & Rubia, K. Gray matter abnormalities in childhood maltreatment: a voxel-wise meta-analysis. Am. J. Psychiatry 171, 854–863 (2014).

    Article  PubMed  Google Scholar 

  49. Pechtel, P., Lyons-Ruth, K., Anderson, C.M. & Teicher, M.H. Sensitive periods of amygdala development: the role of maltreatment in preadolescence. Neuroimage 97, 236–244 (2014).

    Article  PubMed  Google Scholar 

  50. Herringa, R.J. et al. Childhood maltreatment is associated with altered fear circuitry and increased internalizing symptoms by late adolescence. Proc. Natl. Acad. Sci. USA 110, 19119–19124 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Wan, M.W. et al. The neural basis of maternal bonding. PLoS ONE 9, e88436 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Krol, K.M., Rajhans, P., Missana, M. & Grossmann, T. Duration of exclusive breastfeeding is associated with differences in infants' brain responses to emotional body expressions. Front. Behav. Neurosci. 8, 459 (2014).

    PubMed  Google Scholar 

  53. Deoni, S.C. et al. Breastfeeding and early white matter development: a cross-sectional study. Neuroimage 82, 77–86 (2013).

    Article  PubMed  Google Scholar 

  54. Helliwell, J.F. & Putnam, R.D. The social context of well-being. Phil. Trans. R. Soc. Lond. B 359, 1435–1446 (2004).

    Article  Google Scholar 

  55. Dunbar, R.I. & Shultz, S. Evolution in the social brain. Science 317, 1344–1347 (2007).

    Article  CAS  PubMed  Google Scholar 

  56. House, J.S., Landis, K.R. & Umberson, D. Social relationships and health. Science 241, 540–545 (1988).

    Article  CAS  PubMed  Google Scholar 

  57. Seeman, T.E. & McEwen, B.S. Impact of social environment characteristics on neuroendocrine regulation. Psychosom. Med. 58, 459–471 (1996).

    Article  CAS  PubMed  Google Scholar 

  58. Holt-Lunstad, J., Smith, T.B. & Layton, J.B. Social relationships and mortality risk: a meta-analytic review. PLoS Med. 7, e1000316 (2010).

    Article  PubMed  PubMed Central  Google Scholar 

  59. Kirschbaum, C., Klauer, T., Filipp, S.H. & Hellhammer, D.H. Sex-specific effects of social support on cortisol and subjective responses to acute psychological stress. Psychosom. Med. 57, 23–31 (1995).

    Article  CAS  PubMed  Google Scholar 

  60. Chen, F.S. et al. Common oxytocin receptor gene (OXTR) polymorphism and social support interact to reduce stress in humans. Proc. Natl. Acad. Sci. USA 108, 19937–19942 (2011).

    Article  PubMed  PubMed Central  Google Scholar 

  61. Creswell, K.G. et al. OXTR polymorphism predicts social relationships through its effects on social temperament. Soc. Cogn. Affect. Neurosci. 10, 869–876 (2015).

    Article  PubMed  Google Scholar 

  62. Tost, H. et al. A common allele in the oxytocin receptor gene (OXTR) impacts prosocial temperament and human hypothalamic-limbic structure and function. Proc. Natl. Acad. Sci. USA 107, 13936–13941 (2010).

    Article  PubMed  PubMed Central  Google Scholar 

  63. Kim, H.S. et al. Culture, distress, and oxytocin receptor polymorphism (OXTR) interact to influence emotional support seeking. Proc. Natl. Acad. Sci. USA 107, 15717–15721 (2010).

    Article  PubMed  PubMed Central  Google Scholar 

  64. Tost, H. et al. Neurogenetic effects of OXTR rs2254298 in the extended limbic system of healthy Caucasian adults. Biol. Psychiatry 70, e37–e39; author reply e41–e32 (2011).

    Article  CAS  PubMed  Google Scholar 

  65. Olff, M. et al. The role of oxytocin in social bonding, stress regulation and mental health: an update on the moderating effects of context and interindividual differences. Psychoneuroendocrinology 38, 1883–1894 (2013).

    Article  CAS  PubMed  Google Scholar 

  66. Nagasawa, M. et al. Social evolution. Oxytocin-gaze positive loop and the coevolution of human-dog bonds. Science 348, 333–336 (2015).

    Article  CAS  PubMed  Google Scholar 

  67. Younger, J., Aron, A., Parke, S., Chatterjee, N. & Mackey, S. Viewing pictures of a romantic partner reduces experimental pain: involvement of neural reward systems. PLoS ONE 5, e13309 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  68. Eisenberger, N.I. et al. Attachment figures activate a safety signal-related neural region and reduce pain experience. Proc. Natl. Acad. Sci. USA 108, 11721–11726 (2011).

    Article  PubMed  PubMed Central  Google Scholar 

  69. Eisenberger, N.I. The pain of social disconnection: examining the shared neural underpinnings of physical and social pain. Nat. Rev. Neurosci. 13, 421–434 (2012).

    Article  CAS  PubMed  Google Scholar 

  70. Eisenberger, N.I., Taylor, S.E., Gable, S.L., Hilmert, C.J. & Lieberman, M.D. Neural pathways link social support to attenuated neuroendocrine stress responses. Neuroimage 35, 1601–1612 (2007).

    Article  PubMed  Google Scholar 

  71. Kubota, J.T., Banaji, M.R. & Phelps, E.A. The neuroscience of race. Nat. Neurosci. 15, 940–948 (2012).

    Article  CAS  PubMed  Google Scholar 

  72. Cantor-Graae, E. The contribution of social factors to the development of schizophrenia: a review of recent findings. Can. J. Psychiatry 52, 277–286 (2007).

    Article  PubMed  Google Scholar 

  73. van Os, J., Kenis, G. & Rutten, B.P. The environment and schizophrenia. Nature 468, 203–212 (2010).

    Article  CAS  PubMed  Google Scholar 

  74. Cantor-Graae, E. & Selten, J.P. Schizophrenia and migration: a meta-analysis and review. Am. J. Psychiatry 162, 12–24 (2005).

    Article  PubMed  Google Scholar 

  75. Fearon, P. et al. Incidence of schizophrenia and other psychoses in ethnic minority groups: results from the MRC AESOP Study. Psychol. Med. 36, 1541–1550 (2006).

    Article  PubMed  Google Scholar 

  76. Kirkbride, J.B. et al. Psychoses, ethnicity and socio-economic status. Br. J. Psychiatry 193, 18–24 (2008).

    Article  CAS  PubMed  Google Scholar 

  77. Morgan, C., Charalambides, M., Hutchinson, G. & Murray, R.M. Migration, ethnicity, and psychosis: toward a sociodevelopmental model. Schizophr. Bull. 36, 655–664 (2010).

    Article  PubMed  PubMed Central  Google Scholar 

  78. Akdeniz, C. et al. Neuroimaging evidence for a role of neural social stress processing in ethnic minority-associated environmental risk. JAMA Psychiatry 71, 672–680 (2014).

    Article  PubMed  Google Scholar 

  79. Diorio, D., Viau, V. & Meaney, M.J. The role of the medial prefrontal cortex (cingulate gyrus) in the regulation of hypothalamic-pituitary-adrenal responses to stress. J. Neurosci. 13, 3839–3847 (1993).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  80. van Buuren, M., Vink, M., Rapcencu, A.E. & Kahn, R.S. Exaggerated brain activation during emotion processing in unaffected siblings of patients with schizophrenia. Biol. Psychiatry 70, 81–87 (2011).

    Article  PubMed  Google Scholar 

  81. Grimm, O. et al. Striatal response to reward anticipation: evidence for a systems-level intermediate phenotype for schizophrenia. JAMA Psychiatry 71, 531–539 (2014).

    Article  PubMed  Google Scholar 

  82. de Leeuw, M., Kahn, R.S. & Vink, M. Fronto-striatal dysfunction during reward processing in unaffected siblings of schizophrenia patients. Schizophr. Bull. 41, 94–103 (2015).

    Article  PubMed  Google Scholar 

  83. Francis, D.D., Diorio, J., Plotsky, P.M. & Meaney, M.J. Environmental enrichment reverses the effects of maternal separation on stress reactivity. J. Neurosci. 22, 7840–7843 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  84. Restivo, L. et al. Enriched environment promotes behavioral and morphological recovery in a mouse model for the fragile X syndrome. Proc. Natl. Acad. Sci. USA 102, 11557–11562 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  85. Rampon, C. et al. Effects of environmental enrichment on gene expression in the brain. Proc. Natl. Acad. Sci. USA 97, 12880–12884 (2000).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  86. Champagne, F.A. & Meaney, M.J. Transgenerational effects of social environment on variations in maternal care and behavioral response to novelty. Behav. Neurosci. 121, 1353–1363 (2007).

    Article  PubMed  Google Scholar 

  87. Pournajafi-Nazarloo, H. et al. Effects of social isolation on mRNA expression for corticotrophin-releasing hormone receptors in prairie voles. Psychoneuroendocrinology 36, 780–789 (2011).

    Article  CAS  PubMed  Google Scholar 

  88. Whitaker, L.R., Degoulet, M. & Morikawa, H. Social deprivation enhances VTA synaptic plasticity and drug-induced contextual learning. Neuron 77, 335–345 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  89. Panksepp, J., Burgdorf, J., Beinfeld, M.C., Kroes, R.A. & Moskal, J.R. Brain regional neuropeptide changes resulting from social defeat. Behav. Neurosci. 121, 1364–1371 (2007).

    Article  CAS  PubMed  Google Scholar 

  90. Covington, H.E. III et al. Antidepressant actions of histone deacetylase inhibitors. J. Neurosci. 29, 11451–11460 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  91. Dye, C. Health and urban living. Science 319, 766–769 (2008).

    Article  CAS  PubMed  Google Scholar 

  92. Peen, J., Schoevers, R.A., Beekman, A.T. & Dekker, J. The current status of urban-rural differences in psychiatric disorders. Acta Psychiatr. Scand. 121, 84–93 (2010).

    Article  CAS  PubMed  Google Scholar 

  93. Kelly, B.D. et al. Schizophrenia and the city: a review of literature and prospective study of psychosis and urbanicity in Ireland. Schizophr. Res. 116, 75–89 (2010).

    Article  PubMed  Google Scholar 

  94. Pedersen, C.B. & Mortensen, P.B. Evidence of a dose-response relationship between urbanicity during upbringing and schizophrenia risk. Arch. Gen. Psychiatry 58, 1039–1046 (2001).

    Article  CAS  PubMed  Google Scholar 

  95. Krabbendam, L. & van Os, J. Schizophrenia and urbanicity: a major environmental influence–conditional on genetic risk. Schizophr. Bull. 31, 795–799 (2005).

    Article  PubMed  Google Scholar 

  96. Meyer-Lindenberg, A. From maps to mechanisms through neuroimaging of schizophrenia. Nature 468, 194–202 (2010).

    Article  CAS  PubMed  Google Scholar 

  97. Bentall, R.P. & Fernyhough, C. Social predictors of psychotic experiences: specificity and psychological mechanisms. Schizophr. Bull. 34, 1012–1020 (2008).

    Article  PubMed  PubMed Central  Google Scholar 

  98. Christmas, J.J. Psychological stresses of urban living: new direction for mental health services in the inner city. J. Natl. Med. Assoc. 65, 483–486, passim (1973).

    CAS  PubMed  PubMed Central  Google Scholar 

  99. Kennedy, D.P., Glascher, J., Tyszka, J.M. & Adolphs, R. Personal space regulation by the human amygdala. Nat. Neurosci. 12, 1226–1227 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  100. Graziano, M.S. & Cooke, D.F. Parieto-frontal interactions, personal space, and defensive behavior. Neuropsychologia 44, 2621–2635 (2006).

    Article  PubMed  Google Scholar 

  101. Lederbogen, F. et al. City living and urban upbringing affect neural social stress processing in humans. Nature 474, 498–501 (2011).

    Article  CAS  PubMed  Google Scholar 

  102. Haddad, L. et al. Brain structure correlates of urban upbringing, an environmental risk factor for schizophrenia. Schizophr. Bull. 41, 115–122 (2015).

    Article  PubMed  Google Scholar 

  103. Radua, J. et al. Multimodal meta-analysis of structural and functional brain changes in first episode psychosis and the effects of antipsychotic medication. Neurosci. Biobehav. Rev. 36, 2325–2333 (2012).

    Article  CAS  PubMed  Google Scholar 

  104. Bale, T.L. & Epperson, C.N. What's seXXY about stress: sex differences across the lifespan. Nat. Neurosci. 8, pp–pp (2015).

    Google Scholar 

  105. Federal Statistical Office (Germany). Hintergrundtabelle zur Pressemitteilung vom 25.10.2013 Tabelle 0: Armutsgefährdungsschwelle in Deutschland. (Statistisches Bundesamt, Wiesbaden, 2013). https://www.destatis.de/EN/FactsFigures/SocietyState/IncomeConsumptionLivingConditions/LivingConditionsRiskPoverty/Tables/ArtRiskPoverty_HHTyp_SILC.html.

  106. US Census Bureau. Current population survey: definitions and explanations. (US Census Bureau, 2004). https://www.census.gov/content/dam/Census/library/publications/2014/demo/p60-249.pdf.

  107. Holz, N.E. et al. The long-term impact of early life poverty on orbitofrontal cortex volume in adulthood: results from a prospective study over 25 years. Neuropsychopharmacology 40, 996–1004 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  108. Luby, J. et al. The effects of poverty on childhood brain development: the mediating effect of caregiving and stressful life events. JAMA Pediatr. 167, 1135–1142 (2013).

    Article  PubMed  PubMed Central  Google Scholar 

  109. Shtasel-Gottlieb, Z., Palakshappa, D., Yang, F. & Goodman, E. The relationship between developmental assets and food security in adolescents from a low-income community. J. Adolesc. Health 56, 215–222 (2015).

    Article  PubMed  PubMed Central  Google Scholar 

  110. Kim, P. et al. Effects of childhood poverty and chronic stress on emotion regulatory brain function in adulthood. Proc. Natl. Acad. Sci. USA 110, 18442–18447 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  111. Sripada, R.K., Swain, J.E., Evans, G.W., Welsh, R.C. & Liberzon, I. Childhood poverty and stress reactivity are associated with aberrant functional connectivity in default mode network. Neuropsychopharmacology 39, 2244–2251 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  112. Calderón-Garcidueñas, L., Torres-Jardon, R., Kulesza, R.J., Park, S.B. & D'Angiulli, A. Air pollution and detrimental effects on children's brain. The need for a multidisciplinary approach to the issue complexity and challenges. Front. Hum. Neurosci. 8, 613 (2014).

    PubMed  PubMed Central  Google Scholar 

  113. Wilker, E.H. et al. Long-term exposure to fine particulate matter, residential proximity to major roads and measures of brain structure. Stroke 46, 1161–1166 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  114. Peterson, B.S. et al. Effects of prenatal exposure to air pollutants (polycyclic aromatic hydrocarbons) on the development of brain white matter, cognition, and behavior in later childhood. JAMA Psychiatry 72, 531–540 (2015).

    Article  PubMed  PubMed Central  Google Scholar 

  115. Brun, E., Carriere, M. & Mabondzo, A. In vitro evidence of dysregulation of blood-brain barrier function after acute and repeated/long-term exposure to TiO2 nanoparticles. Biomaterials 33, 886–896 (2012).

    Article  CAS  PubMed  Google Scholar 

  116. Fonken, L.K. et al. Air pollution impairs cognition, provokes depressive-like behaviors and alters hippocampal cytokine expression and morphology. Mol.Psychiatry 16, 987–995, 973 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  117. Levesque, S., Surace, M.J., McDonald, J. & Block, M.L. Air pollution and the brain: subchronic diesel exhaust exposure causes neuroinflammation and elevates early markers of neurodegenerative disease. J. Neuroinflammation 8, 105 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  118. Frumkin, H. Beyond toxicity: human health and the natural environment. Am. J. Prev. Med. 20, 234–240 (2001).

    Article  CAS  PubMed  Google Scholar 

  119. Haluza, D., Schonbauer, R. & Cervinka, R. Green perspectives for public health: a narrative review on the physiological effects of experiencing outdoor nature. Int. J. Environ. Res. Public Health 11, 5445–5461 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  120. Maas, J., Verheij, R.A., Groenewegen, P.P., de Vries, S. & Spreeuwenberg, P. Green space, urbanity, and health: how strong is the relation? J. Epidemiol. Community Health 60, 587–592 (2006).

    Article  PubMed  PubMed Central  Google Scholar 

  121. Bowler, D.E., Buyung-Ali, L.M., Knight, T.M. & Pullin, A.S. A systematic review of evidence for the added benefits to health of exposure to natural environments. BMC Public Health 10, 456 (2010).

    Article  PubMed  PubMed Central  Google Scholar 

  122. Fuller, R.A., Irvine, K.N., Devine-Wright, P., Warren, P.H. & Gaston, K.J. Psychological benefits of greenspace increase with biodiversity. Biol. Lett. 3, 390–394 (2007).

    Article  PubMed  PubMed Central  Google Scholar 

  123. Park, B.J., Tsunetsugu, Y., Kasetani, T., Kagawa, T. & Miyazaki, Y. The physiological effects of Shinrin-yoku (taking in the forest atmosphere or forest bathing): evidence from field experiments in 24 forests across Japan. Environ. Health Prev. Med. 15, 18–26 (2010).

    Article  PubMed  Google Scholar 

  124. Park, B.J. et al. Physiological effects of Shinrin-yoku (taking in the atmosphere of the forest)–using salivary cortisol and cerebral activity as indicators. J. Physiol. Anthropol. 26, 123–128 (2007).

    Article  PubMed  Google Scholar 

  125. Caspi, A. & Moffitt, T.E. Gene-environment interactions in psychiatry: joining forces with neuroscience. Nat. Rev. Neurosci. 7, 583–590 (2006).

    Article  CAS  PubMed  Google Scholar 

  126. Montague, P.R. et al. Hyperscanning: simultaneous fMRI during linked social interactions. Neuroimage 16, 1159–1164 (2002).

    Article  PubMed  Google Scholar 

  127. Bilek, E. et al. Information flow between interacting human brains: Identification, validation, and relationship to social expertise. Proc. Natl. Acad. Sci. USA 112, 5207–5212 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  128. Ebner-Priemer, U.W., Eid, M., Kleindienst, N., Stabenow, S. & Trull, T.J. Analytic strategies for understanding affective (in)stability and other dynamic processes in psychopathology. J. Abnorm. Psychol. 118, 195–202 (2009).

    Article  PubMed  Google Scholar 

  129. Ebner-Priemer, U.W., Koudela, S., Mutz, G. & Kanning, M. Interactive multimodal ambulatory monitoring to investigate the association between physical activity and affect. Front. Psychol. 3, 596 (2012).

    CAS  PubMed  Google Scholar 

  130. Heller, A.S. et al. The neurodynamics of affect in the laboratory predicts persistence of real-world emotional responses. J. Neurosci. 35, 10503–10509 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  131. Diamond, M.C., Krech, D. & Rosenzweig, M.R. The effects of an enriched environment on the histology of the rat cerebral cortex. J. Comp. Neurol. 123, 111–120 (1964).

    Article  CAS  PubMed  Google Scholar 

  132. Nithianantharajah, J. & Hannan, A.J. Enriched environments, experience-dependent plasticity and disorders of the nervous system. Nat. Rev. Neurosci. 7, 697–709 (2006).

    Article  CAS  PubMed  Google Scholar 

  133. Faherty, C.J., Kerley, D. & Smeyne, R.J.A. Golgi-Cox morphological analysis of neuronal changes induced by environmental enrichment. Brain Res. Dev. Brain Res. 141, 55–61 (2003).

    Article  CAS  PubMed  Google Scholar 

  134. Turner, A.M. & Greenough, W.T. Differential rearing effects on rat visual cortex synapses. I. Synaptic and neuronal density and synapses per neuron. Brain Res. 329, 195–203 (1985).

    Article  CAS  PubMed  Google Scholar 

  135. Greenough, W.T., Volkmar, F.R. & Juraska, J.M. Effects of rearing complexity on dendritic branching in frontolateral and temporal cortex of the rat. Exp. Neurol. 41, 371–378 (1973).

    Article  CAS  PubMed  Google Scholar 

  136. Scholz, J., Allemang-Grand, R., Dazai, J. & Lerch, J.P. Environmental enrichment is associated with rapid volumetric brain changes in adult mice. Neuroimage 109, 190–198 (2015).

    Article  PubMed  Google Scholar 

  137. Würbel, H. Ideal homes? Housing effects on rodent brain and behaviour. Trends Neurosci. 24, 207–211 (2001).

    Article  PubMed  Google Scholar 

  138. Beck, K.D. & Luine, V.N. Sex differences in behavioral and neurochemical profiles after chronic stress: role of housing conditions. Physiol. Behav. 75, 661–673 (2002).

    Article  CAS  PubMed  Google Scholar 

  139. Simpson, J. & Kelly, J.P. The impact of environmental enrichment in laboratory rats–behavioural and neurochemical aspects. Behav. Brain Res. 222, 246–264 (2011).

    Article  CAS  PubMed  Google Scholar 

  140. Weissbrod, A. et al. Automated long-term tracking and social behavioural phenotyping of animal colonies within a semi-natural environment. Nat. Commun. 4, 2018 (2013).

    Article  CAS  PubMed  Google Scholar 

  141. Akdeniz, C., Tost, H. & Meyer-Lindenberg, A. The neurobiology of social environmental risk for schizophrenia: an evolving research field. Soc. Psychiatry Psychiatr. Epidemiol. 49, 507–517 (2014).

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

The authors thank E. Bilek, T. Törnros and M. Reichert for help with the figures and U. Reininghaus for epidemiological input. H.T. gratefully acknowledges grant support by the German Federal Ministry of Education and Research, BMBF (01GQ1102). A.M.-L. acknowledges funding from the European Union Seventh Framework Programme under the grant agreements HEALTH-F2-2010-241909 (EU-GEI), 115300 (EU-AIMS) and 602805 (EU-Aggressotype).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Heike Tost.

Ethics declarations

Competing interests

A.M.-L. has received consultant fees and travel expenses from Alexza Pharmaceuticals, AstraZeneca, Bristol-Myers Squibb, Defined Health, Decision Resources, Desitin Arzneimittel, Elsevier, F. Hoffmann-La Roche, Gerson Lehrman Group, Grupo Ferrer, Les Laboratoires Servier, Lilly Deutschland, Lundbeck Foundation, Outcome Sciences, Outcome Europe, PriceSpective and Roche Pharma and has received speaker's fees from Abbott, AstraZeneca, BASF, Bristol-Myers Squibb, GlaxoSmithKline, Janssen-Cilag, Lundbeck, Pfizer Pharma and Servier Deutschland.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Tost, H., Champagne, F. & Meyer-Lindenberg, A. Environmental influence in the brain, human welfare and mental health. Nat Neurosci 18, 1421–1431 (2015). https://doi.org/10.1038/nn.4108

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nn.4108

This article is cited by

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing