Top

Social Psychiatry and Psychiatric Epidemiology

Published in:

01-04-2014 | Invited Reviews

The neurobiology of social environmental risk for schizophrenia: an evolving research field

Authors: Ceren Akdeniz, Heike Tost, Andreas Meyer-Lindenberg

Published in: Social Psychiatry and Psychiatric Epidemiology | Issue 4/2014

Abstract

Introduction

Schizophrenia is a severe and complex brain disorder that usually manifests in early adulthood and disturbs a wide range of human functions. More than 100 years after its initial description, the pathophysiology of the disorder is still incompletely understood. Many epidemiological studies strongly suggest a complex interaction between genetic and environmental risk factors for the development of the disorder. While there is considerable evidence for a social environmental component of this risk, the links between adverse social factors and altered brain function have just come into focus.

Methods

In the present review, we first summarize epidemiological evidence for the significance of social environmental risk factors, outline the role of altered social stress processing in mental illness, and review the latest experimental evidence for the neural correlates of social environmental risk for schizophrenia.

Conclusions

The studies we have discussed in this review provide a selection of the current work in the field. We suggest that many of the social environmental risk factors may impact on perceived social stress and engage neural circuits in the brain whose functional and structural architecture undergoes detrimental change in response to prolonged exposure. We conclude that multidisciplinary approaches involving various fields and thoroughly constructed longitudinal designs are necessary to capture complex structure of social environmental risks.

Insel TR (2010) Rethinking schizophrenia. Nature 468(7321):187–193. doi:10.1038/nature09552 PubMedCrossRef

Tost H, Meyer-Lindenberg A (2012) Puzzling over schizophrenia: schizophrenia, social environment and the brain. Nat Med 18(2):211–213. doi:10.1038/nm.2671 PubMedCrossRef

Messias EL, Chen CY, Eaton WW (2007) Epidemiology of schizophrenia: review of findings and myths. Psychiatr Clin North Am 30(3):323–338. doi:10.1016/j.psc.2007.04.007 PubMedCentralPubMedCrossRef

McGrath JJ, Susser ES (2009) New directions in the epidemiology of schizophrenia. Med J Aust 190(4 Suppl):S7–S9 pii:mcg107045_fmPubMed

McGrath J, Saha S, Welham J, El Saadi O, MacCauley C, Chant D (2004) A systematic review of the incidence of schizophrenia: the distribution of rates and the influence of sex, urbanicity, migrant status and methodology. BMC Med 2:13. doi:10.1186/1741-7015-2-13 PubMedCentralPubMedCrossRef

Bhugra D (2005) The global prevalence of schizophrenia. PLoS Med 2(5):e151; quiz e175. doi:10.1371/journal.pmed.0020151

Saha S, Chant D, Welham J, McGrath J (2005) A systematic review of the prevalence of schizophrenia. PLoS Med 2(5):e141. doi:10.1371/journal.pmed.0020141 PubMedCentralPubMedCrossRef

McGuffin P, Gottesman II (1999) Risk factors for schizophrenia. N Engl J Med 341(5):370–371; author reply 372

van Os J, Rutten BP, Poulton R (2008) Gene–environment interactions in schizophrenia: review of epidemiological findings and future directions. Schizophr Bull 34(6):1066–1082. doi:10.1093/schbul/sbn117 PubMedCentralPubMedCrossRef

10.

Svrakic DM, Zorumski CF, Svrakic NM, Zwir I, Cloninger CR (2013) Risk architecture of schizophrenia: the role of epigenetics. Curr Opin Psychiatry 26(2):188–195. doi:10.1097/YCO.0b013e32835d8329 PubMedCrossRef

11.

Brown AS (2011) The environment and susceptibility to schizophrenia. Prog Neurobiol 93(1):23–58. doi:10.1016/j.pneurobio.2010.09.003 PubMedCentralPubMedCrossRef

12.

Sullivan PF, Kendler KS, Neale MC (2003) Schizophrenia as a complex trait: evidence from a meta-analysis of twin studies. Arch Gen Psychiatry 60(12):1187–1192. doi:10.1001/archpsyc.60.12.1187 PubMedCrossRef

13.

Kirkbride JB, Jones PB (2011) The prevention of schizophrenia—what can we learn from eco-epidemiology? Schizophr Bull 37(2):262–271. doi:10.1093/schbul/sbq120 PubMedCentralPubMedCrossRef

14.

van Os J, Kenis G, Rutten BP (2010) The environment and schizophrenia. Nature 468(7321):203–212. doi:10.1038/nature09563 PubMedCrossRef

15.

Sullivan PF, Daly MJ, O’Donovan M (2012) Genetic architectures of psychiatric disorders: the emerging picture and its implications. Nat Rev Genet 13(8):537–551. doi:10.1038/nrg3240 PubMedCrossRef

16.

Mortensen PB, Pedersen CB, Westergaard T, Wohlfahrt J, Ewald H, Mors O, Andersen PK, Melbye M (1999) Effects of family history and place and season of birth on the risk of schizophrenia. N Engl J Med 340(8):603–608. doi:10.1056/NEJM199902253400803 PubMedCrossRef

17.

Meyer-Lindenberg A (2010) From maps to mechanisms through neuroimaging of schizophrenia. Nature 468(7321):194–202. doi:10.1038/nature09569 PubMedCrossRef

18.

Cooper B (2005) Schizophrenia, social class and immigrant status: the epidemiological evidence. Epidemiol Psichiatr Soc 14(3):137–144PubMedCrossRef

19.

Mallett R, Leff J, Bhugra D, Pang D, Zhao JH (2002) Social environment, ethnicity and schizophrenia. A case–control study. Soc Psychiatry Psychiatr Epidemiol 37(7):329–335. doi:10.1007/s00127-002-0557-4 PubMedCrossRef

20.

Hester R, Nestor L, Garavan H (2009) Impaired error awareness and anterior cingulate cortex hypoactivity in chronic cannabis users. Neuropsychopharmacology 34(11):2450–2458. doi:10.1038/npp.2009.67 PubMedCentralPubMedCrossRef

21.

Werner S, Malaspina D, Rabinowitz J (2007) Socioeconomic status at birth is associated with risk of schizophrenia: population-based multilevel study. Schizophr Bull 33(6):1373–1378. doi:10.1093/schbul/sbm032 PubMedCentralPubMedCrossRef

22.

Harrison G, Gunnell D, Glazebrook C, Page K, Kwiecinski R (2001) Association between schizophrenia and social inequality at birth: case–control study. Br J Psychiatry 179:346–350PubMedCrossRef

23.

Meyer-Lindenberg A, Tost H (2012) Neural mechanisms of social risk for psychiatric disorders. Nat Neurosci 15(5):663–668. doi:10.1038/nn.3083 PubMedCrossRef

24.

McEwen BS (2012) Brain on stress: how the social environment gets under the skin. Proc Natl Acad Sci USA 109(Suppl 2):17180–17185. doi:10.1073/pnas.1121254109 PubMedCentralPubMedCrossRef

25.

McEwen BS (2009) The brain is the central organ of stress and adaptation. Neuroimage 47(3):911–913. doi:10.1016/j.neuroimage.2009.05.071 PubMedCentralPubMedCrossRef

26.

Cohen S, Janicki-Deverts D, Miller GE (2007) Psychological stress and disease. JAMA 298(14):1685–1687. doi:10.1001/jama.298.14.1685 PubMedCrossRef

27.

McEwen BS (1998) Protective and damaging effects of stress mediators. N Engl J Med 338(3):171–179. doi:10.1056/NEJM199801153380307 PubMedCrossRef

28.

Gerritsen L, Tendolkar I, Franke B, Vasquez AA, Kooijman S, Buitelaar J, Fernandez G, Rijpkema M (2012) BDNF Val66Met genotype modulates the effect of childhood adversity on subgenual anterior cingulate cortex volume in healthy subjects. Mol Psychiatry 17(6):597–603. doi:10.1038/mp.2011.51 PubMedCrossRef

29.

Lazarus RS (1966) Psychological stress and the coping process. McGraw-Hill series in psychology. McGraw-Hill, New York

30.

McEwen BS (2007) Physiology and neurobiology of stress and adaptation: central role of the brain. Physiol Rev 87(3):873–904. doi:10.1152/physrev.00041.2006 PubMedCrossRef

31.

Kirschbaum C, Hellhammer DH (1994) Salivary cortisol in psychoneuroendocrine research: recent developments and applications. Psychoneuroendocrinology 19(4):313–333 pii:0306-4530(94)90013-2PubMedCrossRef

32.

de Kloet ER, Joels M, Holsboer F (2005) Stress and the brain: from adaptation to disease. Nat Rev Neurosci 6(6):463–475. doi:10.1038/nrn1683 PubMedCrossRef

33.

Cohen S, Line S, Manuck SB, Rabin BS, Heise ER, Kaplan JR (1997) Chronic social stress, social status, and susceptibility to upper respiratory infections in nonhuman primates. Psychosom Med 59(3):213–221PubMed

34.

Gruenewald TL, Kemeny ME, Aziz N, Fahey JL (2004) Acute threat to the social self: shame, social self-esteem, and cortisol activity. Psychosom Med 66(6):915–924. doi:10.1097/01.psy.0000143639.61693.ef PubMedCrossRef

35.

McEwen BS, Wingfield JC (2003) The concept of allostasis in biology and biomedicine. Horm Behav 43(1):2–15 pii:S0018506X02000247PubMedCrossRef

36.

Kirschbaum C, Pirke KM, Hellhammer DH (1993) The ‘Trier Social Stress Test’—a tool for investigating psychobiological stress responses in a laboratory setting. Neuropsychobiology 28(1–2):76–81 pii:119004PubMedCrossRef

37.

Kudielka BM, Schommer NC, Hellhammer DH, Kirschbaum C (2004) Acute HPA axis responses, heart rate, and mood changes to psychosocial stress (TSST) in humans at different times of day. Psychoneuroendocrinology 29(8):983–992. doi:10.1016/j.psyneuen.2003.08.009 PubMedCrossRef

38.

Kudielka BM, Buske-Kirschbaum A, Hellhammer DH, Kirschbaum C (2004) HPA axis responses to laboratory psychosocial stress in healthy elderly adults, younger adults, and children: impact of age and gender. Psychoneuroendocrinology 29(1):83–98 pii:S0306453002001464PubMedCrossRef

39.

Jones SR, Fernyhough C (2007) A new look at the neural diathesis–stress model of schizophrenia: the primacy of social-evaluative and uncontrollable situations. Schizophr Bull 33(5):1171–1177. doi:10.1093/schbul/sbl058 PubMedCentralPubMedCrossRef

40.

Dickerson SS, Kemeny ME (2004) Acute stressors and cortisol responses: a theoretical integration and synthesis of laboratory research. Psychol Bull 130(3):355–391. doi:10.1037/0033-2909.130.3.355 PubMedCrossRef

41.

Dickerson SS, Gruenewald TL, Kemeny ME (2004) When the social self is threatened: shame, physiology, and health. J Pers 72(6):1191–1216. doi:10.1111/j.1467-6494.2004.00295.x PubMedCrossRef

42.

Pruessner JC, Dedovic K, Pruessner M, Lord C, Buss C, Collins L, Dagher A, Lupien SJ (2010) Stress regulation in the central nervous system: evidence from structural and functional neuroimaging studies in human populations—2008 Curt Richter Award Winner. Psychoneuroendocrinology 35(1):179–191. doi:10.1016/j.psyneuen.2009.02.016 PubMedCrossRef

43.

Pruessner JC, Baldwin MW, Dedovic K, Renwick R, Mahani NK, Lord C, Meaney M, Lupien S (2005) Self-esteem, locus of control, hippocampal volume, and cortisol regulation in young and old adulthood. NeuroImage 28(4):815–826. doi:10.1016/j.neuroimage.2005.06.014 PubMedCrossRef

44.

Dedovic K, D’Aguiar C, Pruessner JC (2009) What stress does to your brain: a review of neuroimaging studies. Can J Psychiatry 54(1):6–15PubMed

45.

Wager TD, Waugh CE, Lindquist M, Noll DC, Fredrickson BL, Taylor SF (2009) Brain mediators of cardiovascular responses to social threat: part I: reciprocal dorsal and ventral sub-regions of the medial prefrontal cortex and heart-rate reactivity. Neuroimage 47(3):821–835. doi:10.1016/j.neuroimage.2009.05.043 PubMedCentralPubMedCrossRef

46.

Arnsten AF (2009) Stress signalling pathways that impair prefrontal cortex structure and function. Nat Rev Neurosci 10(6):410–422. doi:10.1038/nrn2648 PubMedCentralPubMedCrossRef

47.

Luethi M, Meier B, Sandi C (2008) Stress effects on working memory, explicit memory, and implicit memory for neutral and emotional stimuli in healthy men. Front Behav Neurosci 2:5. doi:10.3389/neuro.08.005.2008 PubMedCentralPubMedCrossRef

48.

Qin S, Hermans EJ, van Marle HJ, Luo J, Fernandez G (2009) Acute psychological stress reduces working memory-related activity in the dorsolateral prefrontal cortex. Biol Psychiatry 66(1):25–32. doi:10.1016/j.biopsych.2009.03.006 PubMedCrossRef

49.

Cook SC, Wellman CL (2004) Chronic stress alters dendritic morphology in rat medial prefrontal cortex. J Neurobiol 60(2):236–248. doi:10.1002/neu.20025 PubMedCrossRef

50.

Lupien SJ, McEwen BS, Gunnar MR, Heim C (2009) Effects of stress throughout the lifespan on the brain, behaviour and cognition. Nat Rev Neurosci 10(6):434–445. doi:10.1038/nrn2639 PubMedCrossRef

51.

Brown SM, Henning S, Wellman CL (2005) Mild, short-term stress alters dendritic morphology in rat medial prefrontal cortex. Cereb Cortex 15(11):1714–1722. doi:10.1093/cercor/bhi048 PubMedCrossRef

52.

Liston C, McEwen BS, Casey BJ (2009) Psychosocial stress reversibly disrupts prefrontal processing and attentional control. Proc Natl Acad Sci USA 106(3):912–917. doi:10.1073/pnas.0807041106 PubMedCentralPubMedCrossRef

53.

Selten JP, van der Ven E, Rutten BP, Cantor-Graae E (2013) The social defeat hypothesis of schizophrenia: an update. Schizophr Bull 39(6):1180–1186. doi:10.1093/schbul/sbt134 PubMedCrossRef

54.

Stilo SA, Di Forti M, Mondelli V, Falcone AM, Russo M, O’Connor J, Palmer E, Paparelli A, Kolliakou A, Sirianni M, Taylor H, Handley R, Dazzan P, Pariante C, Marques TR, Zoccali R, David A, Murray RM, Morgan C (2013) Social disadvantage: cause or consequence of impending psychosis? Schizophr Bull 39(6):1288–1295. doi:10.1093/schbul/sbs112 PubMedCentralPubMedCrossRef

55.

Selten JP, Cantor-Graae E (2005) Social defeat: risk factor for schizophrenia? Br J Psychiatry 187:101–102. doi:10.1192/bjp.187.2.101 PubMedCrossRef

56.

Morgan C, Kirkbride J, Hutchinson G, Craig T, Morgan K, Dazzan P, Boydell J, Doody GA, Jones PB, Murray RM, Leff J, Fearon P (2008) Cumulative social disadvantage, ethnicity and first-episode psychosis: a case–control study. Psychol Med 38(12):1701–1715. doi:10.1017/S0033291708004534 PubMedCrossRef

57.

Dettenborn L, Tietze A, Bruckner F, Kirschbaum C (2010) Higher cortisol content in hair among long-term unemployed individuals compared to controls. Psychoneuroendocrinology 35(9):1404–1409. doi:10.1016/j.psyneuen.2010.04.006 PubMedCrossRef

58.

Ockenfels MC, Porter L, Smyth J, Kirschbaum C, Hellhammer DH, Stone AA (1995) Effect of chronic stress associated with unemployment on salivary cortisol: overall cortisol levels, diurnal rhythm, and acute stress reactivity. Psychosom Med 57(5):460–467PubMed

59.

Gianaros PJ, Jennings JR, Sheu LK, Greer PJ, Kuller LH, Matthews KA (2007) Prospective reports of chronic life stress predict decreased grey matter volume in the hippocampus. Neuroimage 35(2):795–803. doi:10.1016/j.neuroimage.2006.10.045 PubMedCentralPubMedCrossRef

60.

Fusar-Poli P, Radua J, McGuire P, Borgwardt S (2012) Neuroanatomical maps of psychosis onset: voxel-wise meta-analysis of antipsychotic-naive VBM studies. Schizophr Bull 38(6):1297–1307PubMedCentralPubMedCrossRef

61.

Hu M, Li J, Eyler L, Guo X, Wei Q, Tang J, Liu F, He Z, Li L, Jin H, Liu Z, Wang J, Liu F, Chen H, Zhao J (2013) Decreased left middle temporal gyrus volume in antipsychotic drug-naive, first-episode schizophrenia patients and their healthy unaffected siblings. Schizophr Res 144(1–3):37–42. doi:10.1016/j.schres.2012.12.018 PubMedCrossRef

62.

Howes OD, McDonald C, Cannon M, Arseneault L, Boydell J, Murray RM (2004) Pathways to schizophrenia: the impact of environmental factors. Int J Neuropsychopharmacol Off Sci J Coll Int Neuropsychopharmacol 7(Suppl 1):S7–S13. doi:10.1017/S1461145704004122

63.

Bebbington P, Wilkins S, Jones P, Foerster A, Murray R, Toone B, Lewis S (1993) Life events and psychosis. Initial results from the Camberwell Collaborative Psychosis Study. Br J Psychiatry 162:72–79PubMedCrossRef

64.

Lodge DJ, Grace AA (2011) Developmental pathology, dopamine, stress and schizophrenia. Int J Dev Neurosci Off J Int Soc Dev Neurosci 29(3):207–213. doi:10.1016/j.ijdevneu.2010.08.002 CrossRef

65.

Howes OD, Kapur S (2009) The dopamine hypothesis of schizophrenia: version III—the final common pathway. Schizophr Bull 35(3):549–562. doi:10.1093/schbul/sbp006 PubMedCentralPubMedCrossRef

66.

Walker EF, Diforio D (1997) Schizophrenia: a neural diathesis-stress model. Psychol Rev 104(4):667–685PubMedCrossRef

67.

Adolphs R (2010) Conceptual challenges and directions for social neuroscience. Neuron 65(6):752–767. doi:10.1016/j.neuron.2010.03.006 PubMedCentralPubMedCrossRef

68.

Stanley DA, Adolphs R (2013) Toward a neural basis for social behavior. Neuron 80(3):816–826. doi:10.1016/j.neuron.2013.10.038 PubMedCentralPubMedCrossRef

69.

Cantor-Graae E (2007) The contribution of social factors to the development of schizophrenia: a review of recent findings. Can J Psychiatry 52(5):277–286PubMed

70.

Muntaner C, Eaton WW, Miech R, O’Campo P (2004) Socioeconomic position and major mental disorders. Epidemiol Rev 26:53–62. doi:10.1093/epirev/mxh001 PubMedCrossRef

71.

Pedersen CB, Mortensen PB (2001) Evidence of a dose–response relationship between urbanicity during upbringing and schizophrenia risk. Arch Gen Psychiatry 58(11):1039–1046 pii:yoa20415PubMedCrossRef

72.

Krieger N, Williams DR, Moss NE (1997) Measuring social class in US public health research: concepts, methodologies, and guidelines. Annu Rev Public Health 18:341–378. doi:10.1146/annurev.publhealth.18.1.341 PubMedCrossRef

73.

Hackman DA, Farah MJ, Meaney MJ (2010) Socioeconomic status and the brain: mechanistic insights from human and animal research. Nat Rev Neurosci 11(9):651–659. doi:10.1038/nrn2897 PubMedCentralPubMedCrossRef

74.

Hudson CG (2005) Socioeconomic status and mental illness: tests of the social causation and selection hypotheses. Am J Orthopsychiatry 75(1):3–18. doi:10.1037/0002-9432.75.1.3 PubMedCrossRef

75.

Adler NE, Boyce T, Chesney MA, Cohen S, Folkman S, Kahn RL, Syme SL (1994) Socioeconomic status and health. The challenge of the gradient. Am Psychol 49(1):15–24PubMedCrossRef

76.

Byrne M, Agerbo E, Eaton WW, Mortensen PB (2004) Parental socio-economic status and risk of first admission with schizophrenia—a Danish national register based study. Soc Psychiatry Psychiatr Epidemiol 39(2):87–96. doi:10.1007/s00127-004-0715-y PubMedCrossRef

77.

Adler NE, Epel ES, Castellazzo G, Ickovics JR (2000) Relationship of subjective and objective social status with psychological and physiological functioning: preliminary data in healthy white women. Health Psychol 19(6):586–592PubMedCrossRef

78.

Gianaros PJ, Horenstein JA, Cohen S, Matthews KA, Brown SM, Flory JD, Critchley HD, Manuck SB, Hariri AR (2007) Perigenual anterior cingulate morphology covaries with perceived social standing. Social Cogn Affect Neurosci 2(3):161–173. doi:10.1093/scan/nsm013 CrossRef

79.

Kessler RC, Cleary PD (1980) Social class and psychological distress. Am Sociol Rev 45(3):463–478PubMedCrossRef

80.

Gallo LC, Matthews KA (2003) Understanding the association between socioeconomic status and physical health: do negative emotions play a role? Psychol Bull 129(1):10–51PubMedCrossRef

81.

Sapolsky RM (2004) Social status and health in humans and other animals. Ann Rev Anthropol 33:393–418

82.

Zink CF, Tong Y, Chen Q, Bassett DS, Stein JL, Meyer-Lindenberg A (2008) Know your place: neural processing of social hierarchy in humans. Neuron 58(2):273–283. doi:10.1016/j.neuron.2008.01.025 PubMedCentralPubMedCrossRef

83.

LeDoux JE (2000) Emotion circuits in the brain. Annu Rev Neurosci 23:155–184. doi:10.1146/annurev.neuro.23.1.155 PubMedCrossRef

84.

Diorio D, Viau V, Meaney MJ (1993) The role of the medial prefrontal cortex (cingulate gyrus) in the regulation of hypothalamic-pituitary-adrenal responses to stress. J Neurosci Off J Soc Neurosci 13(9):3839–3847

85.

Gianaros PJ, Horenstein JA, Hariri AR, Sheu LK, Manuck SB, Matthews KA, Cohen S (2008) Potential neural embedding of parental social standing. Soc Cogn Affect Neurosci 3(2):91–96. doi:10.1093/scan/nsn003 PubMedCentralPubMedCrossRef

86.

Hanson JL, Chandra A, Wolfe BL, Pollak SD (2011) Association between income and the hippocampus. PLoS ONE 6(5):e18712. doi:10.1371/journal.pone.0018712 PubMedCentralPubMedCrossRef

87.

McEwen BS, Magarinos AM (1997) Stress effects on morphology and function of the hippocampus. Ann NY Acad Sci 821:271–284PubMedCrossRef

88.

McEwen BS (2001) Plasticity of the hippocampus: adaptation to chronic stress and allostatic load. Ann NY Acad Sci 933:265–277PubMedCrossRef

89.

McEwen BS (2003) Mood disorders and allostatic load. Biol Psychiatry 54(3):200–207PubMedCrossRef

90.

Cohen S, Wills TA (1985) Stress, social support, and the buffering hypothesis. Psychol Bull 98(2):310–357PubMedCrossRef

91.

Leavy RL (1983) Social support and psychological disorder: a review. J Commun Psychol 11(1):3–21CrossRef

92.

Cohen LH, McGowan J, Fooskas S, Rose S (1984) Positive life events and social support and the relationship between life stress and psychological disorder. Am J Community Psychol 12(5):567–587PubMedCrossRef

93.

Whitley R, McKenzie K (2005) Social capital and psychiatry: review of the literature. Harv Rev Psychiatry 13(2):71–84. doi:10.1080/10673220590956474 PubMedCrossRef

94.

McKenzie K, Whitley R, Weich S (2002) Social capital and mental health. Br J Psychiatry 181:280–283PubMedCrossRef

95.

De Silva MJ, McKenzie K, Harpham T, Huttly SR (2005) Social capital and mental illness: a systematic review. J Epidemiol Commun Health 59(8):619–627. doi:10.1136/jech.2004.029678 CrossRef

96.

Helliwell JF, Putnam RD (2004) The social context of well-being. Philos Trans R Soc Lond B Biol Sci 359(1449):1435–1446. doi:10.1098/rstb.2004.1522 PubMedCentralPubMedCrossRef

97.

Kirkbride JB, Morgan C, Fearon P, Dazzan P, Murray RM, Jones PB (2007) Neighbourhood-level effects on psychoses: re-examining the role of context. Psychol Med 37(10):1413–1425. doi:10.1017/S0033291707000499 PubMedCrossRef

98.

Dunbar RI, Shultz S (2007) Evolution in the social brain. Science 317(5843):1344–1347. doi:10.1126/science.1145463 PubMedCrossRef

99.

Seeman TE, McEwen BS (1996) Impact of social environment characteristics on neuroendocrine regulation. Psychosom Med 58(5):459–471PubMed

100.

Eisenberger NI, Taylor SE, Gable SL, Hilmert CJ, Lieberman MD (2007) Neural pathways link social support to attenuated neuroendocrine stress responses. Neuroimage 35(4):1601–1612. doi:10.1016/j.neuroimage.2007.01.038 PubMedCentralPubMedCrossRef

101.

Eisenberger NI (2013) An empirical review of the neural underpinnings of receiving and giving social support: implications for health. Psychosom Med 75(6):545–556. doi:10.1097/PSY.0b013e31829de2e7 PubMedCrossRef

102.

Pezawas L, Meyer-Lindenberg A, Drabant EM, Verchinski BA, Munoz KE, Kolachana BS, Egan MF, Mattay VS, Hariri AR, Weinberger DR (2005) 5-HTTLPR polymorphism impacts human cingulate-amygdala interactions: a genetic susceptibility mechanism for depression. Nat Neurosci 8(6):828–834. doi:10.1038/nn1463 PubMedCrossRef

103.

Ochsner KN, Ludlow DH, Knierim K, Hanelin J, Ramachandran T, Glover GC, Mackey SC (2006) Neural correlates of individual differences in pain-related fear and anxiety. Pain 120(1–2):69–77. doi:10.1016/j.pain.2005.10.014 PubMedCentralPubMedCrossRef

104.

Critchley HD, Melmed RN, Featherstone E, Mathias CJ, Dolan RJ (2002) Volitional control of autonomic arousal: a functional magnetic resonance study. Neuroimage 16(4):909–919 pii:S105381190291147XPubMedCrossRef

105.

Eisenberger NI, Cole SW (2012) Social neuroscience and health: neurophysiological mechanisms linking social ties with physical health. Nat Neurosci 15(5):669–674. doi:10.1038/nn.3086 PubMedCrossRef

106.

Bickart KC, Wright CI, Dautoff RJ, Dickerson BC, Barrett LF (2011) Amygdala volume and social network size in humans. Nat Neurosci 14(2):163–164. doi:10.1038/nn.2724 PubMedCentralPubMedCrossRef

107.

Kennedy DP, Adolphs R (2012) The social brain in psychiatric and neurological disorders. Trends Cogn Sci 16(11):559–572. doi:10.1016/j.tics.2012.09.006 PubMedCentralPubMedCrossRef

108.

Kanai R, Bahrami B, Duchaine B, Janik A, Banissy MJ, Rees G (2012) Brain structure links loneliness to social perception. Current Biol CB 22(20):1975–1979. doi:10.1016/j.cub.2012.08.045 CrossRef

109.

Kanai R, Bahrami B, Roylance R, Rees G (2012) Online social network size is reflected in human brain structure. Proc Biol Sci Royal Soc 279(1732):1327–1334. doi:10.1098/rspb.2011.1959 CrossRef

110.

Zilbovicius M, Meresse I, Chabane N, Brunelle F, Samson Y, Boddaert N (2006) Autism, the superior temporal sulcus and social perception. Trends Neurosci 29(7):359–366. doi:10.1016/j.tins.2006.06.004 PubMedCrossRef

111.

Saitovitch A, Bargiacchi A, Chabane N, Brunelle F, Samson Y, Boddaert N, Zilbovicius M (2012) Social cognition and the superior temporal sulcus: implications in autism. Revue Neurol 168(10):762–770. doi:10.1016/j.neurol.2012.07.017 CrossRef

112.

Dye C (2008) Health and urban living. Science 319(5864):766–769. doi:10.1126/science.1150198 PubMedCrossRef

113.

Peen J, Schoevers RA, Beekman AT, Dekker J (2010) The current status of urban–rural differences in psychiatric disorders. Acta Psychiatr Scand 121(2):84–93. doi:10.1111/j.1600-0447.2009.01438.x PubMedCrossRef

114.

Krabbendam L, van Os J (2005) Schizophrenia and urbanicity: a major environmental influence–conditional on genetic risk. Schizophr Bull 31(4):795–799. doi:10.1093/schbul/sbi060 PubMedCrossRef

115.

March D, Hatch SL, Morgan C, Kirkbride JB, Bresnahan M, Fearon P, Susser E (2008) Psychosis and place. Epidemiol Rev 30:84–100. doi:10.1093/epirev/mxn006 PubMedCrossRef

116.

van Os J, Driessen G, Gunther N, Delespaul P (2000) Neighbourhood variation in incidence of schizophrenia. Evidence for person–environment interaction. Br J Psychiatry 176:243–248PubMedCrossRef

117.

Lederbogen F, Kirsch P, Haddad L, Streit F, Tost H, Schuch P, Wust S, Pruessner JC, Rietschel M, Deuschle M, Meyer-Lindenberg A (2011) City living and urban upbringing affect neural social stress processing in humans. Nature 474(7352):498–501. doi:10.1038/nature10190 PubMedCrossRef

118.

Radua J, Borgwardt S, Crescini A, Mataix-Cols D, Meyer-Lindenberg A, McGuire PK, Fusar-Poli P (2012) Multimodal meta-analysis of structural and functional brain changes in first episode psychosis and the effects of antipsychotic medication. Neurosci Biobehav Rev 36(10):2325–2333. doi:10.1016/j.neubiorev.2012.07.012 PubMedCrossRef

119.

Cantor-Graae E, Selten JP (2005) Schizophrenia and migration: a meta-analysis and review. Am J Psychiatry 162(1):12–24. doi:10.1176/appi.ajp.162.1.12 PubMedCrossRef

120.

Bourque F, van der Ven E, Malla A (2011) A meta-analysis of the risk for psychotic disorders among first- and second-generation immigrants. Psychol Med 41(5):897–910. doi:10.1017/S0033291710001406 PubMedCrossRef

121.

Morgan C, Charalambides M, Hutchinson G, Murray RM (2010) Migration, ethnicity, and psychosis: toward a sociodevelopmental model. Schizophr Bull 36(4):655–664. doi:10.1093/schbul/sbq051 PubMedCentralPubMedCrossRef

122.

Bresnahan M, Begg MD, Brown A, Schaefer C, Sohler N, Insel B, Vella L, Susser E (2007) Race and risk of schizophrenia in a US birth cohort: another example of health disparity? Int J Epidemiol 36(4):751–758. doi:10.1093/ije/dym041 PubMedCrossRef

123.

Veling W, Susser E, van Os J, Mackenbach JP, Selten JP, Hoek HW (2008) Ethnic density of neighborhoods and incidence of psychotic disorders among immigrants. Am J Psychiatry 165(1):66–73. doi:10.1176/appi.ajp.2007.07030423 PubMedCrossRef

124.

Boydell J, van Os J, McKenzie K, Allardyce J, Goel R, McCreadie RG, Murray RM (2001) Incidence of schizophrenia in ethnic minorities in London: ecological study into interactions with environment. BMJ 323(7325):1336–1338PubMedCentralPubMedCrossRef

125.

Allardyce J, Boydell J (2006) Review: the wider social environment and schizophrenia. Schizophr Bull 32(4):592–598. doi:10.1093/schbul/sbl008 PubMedCentralPubMedCrossRef

126.

Williams DR, Neighbors HW, Jackson JS (2008) Racial/ethnic discrimination and health: findings from community studies. Am J Public Health 98(9 Suppl):S29–S37PubMedCentralPubMedCrossRef

127.

Veling W, Susser E (2011) Migration and psychotic disorders. Expert Rev Neurother 11(1):65–76. doi:10.1586/ern.10.91 PubMedCrossRef

128.

Akdeniz C, Tost H, Streit F, Haddad L, Wuest S, Schaefer A, Schneider M, Rietschel M, Kirsch P, Meyer-Lindenberg A (2014) Neuroimaging evidence for a role of neural social stress processing in ethnic minority associated environmental risk. JAMA Psychiatry (in press)

129.

Mohnke S, Erk S, Schnell K, Schutz C, Seiferth N, Grimm O, Haddad L, Pohland L, Garbusow M, Schmitgen MM, Kirsch P, Esslinger C, Rietschel M, Witt SH, Nothen MM, Cichon S, Mattheisen M, Muhleisen T, Jensen J, Schott BH, Maier W, Heinz A, Meyer-Lindenberg A, Walter H (2013) Further evidence for the impact of a genome-wide supported psychosis risk variant in ZNF804A on the theory of mind network. Neuropsychopharmacology. doi:10.1038/npp.2013.321 PubMed

130.

Kuswanto CN, Woon PS, Zheng XB, Qiu A, Sitoh YY, Chan YH, Liu J, Williams H, Ong WY, Sim K (2012) Genome-wide supported psychosis risk variant in ZNF804A gene and impact on cortico-limbic WM integrity in schizophrenia. Am J Med Genet B Neuropsychiatr Genet 159B(3):255–262. doi:10.1002/ajmg.b.32032 PubMedCrossRef

131.

Erk S, Meyer-Lindenberg A, Schnell K, Opitz von Boberfeld C, Esslinger C, Kirsch P, Grimm O, Arnold C, Haddad L, Witt SH, Cichon S, Nothen MM, Rietschel M, Walter H (2010) Brain function in carriers of a genome-wide supported bipolar disorder variant. Arch Gen Psychiatry 67(8):803–811. doi:10.1001/archgenpsychiatry.2010.94 PubMedCrossRef

132.

Meda SA, Jagannathan K, Gelernter J, Calhoun VD, Liu J, Stevens MC, Pearlson GD (2010) A pilot multivariate parallel ICA study to investigate differential linkage between neural networks and genetic profiles in schizophrenia. Neuroimage 53(3):1007–1015. doi:10.1016/j.neuroimage.2009.11.052 PubMedPubMedCentralCrossRef

133.

O’Donovan MC, Craddock NJ, Owen MJ (2009) Genetics of psychosis; insights from views across the genome. Hum Genet 126(1):3–12. doi:10.1007/s00439-009-0703-0 PubMedCrossRef

134.

Young KA, Holcomb LA, Bonkale WL, Hicks PB, Yazdani U, German DC (2007) 5HTTLPR polymorphism and enlargement of the pulvinar: unlocking the backdoor to the limbic system. Biol Psychiatry 61(6):813–818. doi:10.1016/j.biopsych.2006.08.047 PubMedCrossRef

135.

Schaeffer EL, Kuhn F, Schmitt A, Gattaz WF, Gruber O, Schneider-Axmann T, Falkai P, Schmitt A (2013) Increased cell proliferation in the rat anterior cingulate cortex following neonatal hypoxia: relevance to schizophrenia. J Neural Trans 120(1):187–195. doi:10.1007/s00702-012-0859-y CrossRef

136.

McGowan PO, Sasaki A, D’Alessio AC, Dymov S, Labonte B, Szyf M, Turecki G, Meaney MJ (2009) Epigenetic regulation of the glucocorticoid receptor in human brain associates with childhood abuse. Nat Neurosci 12(3):342–348. doi:10.1038/nn.2270 PubMedCentralPubMedCrossRef

Title: The neurobiology of social environmental risk for schizophrenia: an evolving research field
Authors: Ceren Akdeniz
Heike Tost
Andreas Meyer-Lindenberg
Publication date: 01-04-2014
Publisher: Springer Berlin Heidelberg
Published in: Social Psychiatry and Psychiatric Epidemiology / Issue 4/2014
Print ISSN: 0933-7954
Electronic ISSN: 1433-9285
DOI: https://doi.org/10.1007/s00127-014-0858-4

At a glance: The STEP trials

Springer Medicine

The neurobiology of social environmental risk for schizophrenia: an evolving research field

Abstract

Introduction

Methods

Conclusions

At a glance: The STEP trials

Springer Medicine

Abstract

Introduction

Methods

Conclusions

Please log in to get access to this content

Other articles of this Issue 4/2014

Suicide mortality in second-generation migrants, Australia, 2001–2008

A systematic review and meta-analysis of the ethnic density effect in psychotic disorders

A regional approach to understanding farmer suicide rates in Queensland

School effects on risk of non-fatal suicidal behaviour: a national multilevel cohort study

Social support and suicidal ideation in Japan: are home visits by commissioned welfare volunteers associated with a lower risk of suicidal ideation among elderly people in the community?

Money matters: does the reimbursement policy for second-generation antipsychotics influence the number of recorded schizophrenia patients and the burden of stigmatization?