Skip to main content Accessibility help
×
Home

Neural effects of social environmental stress – an activation likelihood estimation meta-analysis

  • O. Mothersill (a1) (a2) and G. Donohoe (a1) (a2)

Abstract

Background

Social environmental stress, including childhood abuse and deprivation, is associated with increased rates of psychiatric disorders such as schizophrenia and depression. However, the neural mechanisms mediating risk are not completely understood. Functional magnetic resonance imaging (MRI) studies have reported effects of social environmental stress on a variety of brain regions, but interpretation of results is complicated by the variety of environmental risk factors examined and different methods employed.

Method

We examined brain regions consistently showing differences in blood oxygen level-dependent (BOLD) response in individuals exposed to higher levels of environmental stress by performing a coordinate-based meta-analysis on 54 functional MRI studies using activation likelihood estimation (ALE), including an overall sample of 3044 participants. We performed separate ALE analyses on studies examining adults (mean age ⩾18 years) and children/adolescents (mean age <18 years) and a contrast analysis comparing the two types of study.

Results

Across both adult and children/adolescent studies, ALE meta-analysis revealed several clusters in which differences in BOLD response were associated with social environmental stress across multiple studies. These clusters incorporated several brain regions, among which the right amygdala was most frequently implicated.

Conclusions

These findings suggest that a variety of social environmental stressors is associated with differences in the BOLD response of specific brain regions such as the right amygdala in both children/adolescents and adults. What remains unknown is whether these environmental stressors have differential effects on treatment response in these brain regions.

Copyright

Corresponding author

*Address for correspondence: G. Donohoe, School of Psychology, National University of Ireland Galway, University Road, Galway, Republic of Ireland. (Email: gary.donohoe@nuigalway.ie)

References

Hide All
Adolphs, R (2001). The neurobiology of social cognition. Current Opinion in Neurobiology 11, 231239.
Belmaker, R, Agam, G (2008). Major depressive disorder. New England Journal of Medicine 358, 5568.
Boecker, R, Holz, NE, Buchmann, AF, Blomeyer, D, Plichta, MM, Wolf, I, Baumeister, S, Meyer-Lindenberg, A, Banaschewski, T, Brandeis, D (2014). Impact of early life adversity on reward processing in young adults: EEG-fMRI results from a prospective study over 25 years. PLOS ONE 9, e104185.
Dannlowski, U, Kugel, H, Huber, F, Stuhrmann, A, Redlich, R, Grotegerd, D, Dohm, K, Sehlmeyer, C, Konrad, C, Baune, BT (2013). Childhood maltreatment is associated with an automatic negative emotion processing bias in the amygdala. Human Brain Mapping 34, 28992909.
Dannlowski, U, Ohrmann, P, Bauer, J, Kugel, H, Arolt, V, Heindel, W, Kersting, A, Baune, BT, Suslow, T (2007 a). Amygdala reactivity to masked negative faces is associated with automatic judgmental bias in major depression: a 3 T fMRI study. Journal of Psychiatry and Neuroscience: JPN 32, 423429.
Dannlowski, U, Ohrmann, P, Bauer, J, Kugel, H, Arolt, V, Heindel, W, Suslow, T (2007 b). Amygdala reactivity predicts automatic negative evaluations for facial emotions. Psychiatry Research: Neuroimaging 154, 1320.
Dannlowski, U, Stuhrmann, A, Beutelmann, V, Zwanzger, P, Lenzen, T, Grotegerd, D, Domschke, K, Hohoff, C, Ohrmann, P, Bauer, J (2012). Limbic scars: long-term consequences of childhood maltreatment revealed by functional and structural magnetic resonance imaging. Biological Psychiatry 71, 286293.
Derubeis, RJ, Siegle, GJ, Hollon, SD (2008). Cognitive therapy versus medication for depression: treatment outcomes and neural mechanisms. Nature Reviews Neuroscience 9, 788796.
Desantis, SM, Baker, NL, Back, SE, Spratt, E, Ciolino, JD, Maria, MS, Dipankar, B, Brady, KT (2011). Gender differences in the effect of early life trauma on hypothalamic–pituitary–adrenal axis functioning. Depression and Anxiety 28, 383392.
Eickhoff, SB, Bzdok, D, Laird, AR, Kurth, F, Fox, PT (2012). Activation likelihood estimation meta-analysis revisited. NeuroImage 59, 23492361.
Eickhoff, SB, Laird, AR, Grefkes, C, Wang, LE, Zilles, K, Fox, PT (2009). Coordinate-based activation likelihood estimation meta-analysis of neuroimaging data: a random-effects approach based on empirical estimates of spatial uncertainty. Human Brain Mapping 30, 29072926.
Eisenberger, NI, Cole, SW (2012). Social neuroscience and health: neurophysiological mechanisms linking social ties with physical health. Nature Neuroscience 15, 669674.
Etkin, A, Klemenhagen, KC, Dudman, JT, Rogan, MT, Hen, R, Kandel, ER, Hirsch, J (2004). Individual differences in trait anxiety predict the response of the basolateral amygdala to unconsciously processed fearful faces. Neuron 44, 10431055.
Evans, KC, Wright, CI, Wedig, MM, Gold, AL, Pollack, MH, Rauch, SL (2008). A functional MRI study of amygdala responses to angry schematic faces in social anxiety disorder. Depression and Anxiety 25, 496505.
Felmingham, K, Williams, LM, Kemp, AH, Liddell, B, Falconer, E, Peduto, A, Bryant, R (2010). Neural responses to masked fear faces: sex differences and trauma exposure in posttraumatic stress disorder. Journal of Abnormal Psychology 119, 241247.
Fu, CH, Williams, SC, Cleare, AJ, Brammer, MJ, Walsh, ND, Kim, J, Andrew, CM, Pich, EM, Williams, PM, Reed, LJ (2004). Attenuation of the neural response to sad faces in major depression by antidepressant treatment: a prospective, event-related functional magnetic resonance imaging study. Archives of General Psychiatry 61, 877889.
Gaffrey, MS, Luby, JL, Belden, AC, Hirshberg, JS, Volsch, J, Barch, DM (2011). Association between depression severity and amygdala reactivity during sad face viewing in depressed preschoolers: an fMRI study. Journal of Affective Disorders 129, 364370.
Gilbert, R, Widom, CS, Browne, K, Fergusson, D, Webb, E, Janson, S (2009). Burden and consequences of child maltreatment in high-income countries. Lancet 373, 6881.
Gold, PW, Drevets, WC, Charney, DS (2002). New insights into the role of cortisol and the glucocorticoid receptor in severe depression. Biological Psychiatry 52, 381385.
Harmon-Jones, E, Beer, JS (2012). Methods in Social Neuroscience. Guilford Press: New York.
Harrison, NA, Brydon, L, Walker, C, Gray, MA, Steptoe, A, Critchley, HD (2009). Inflammation causes mood changes through alterations in subgenual cingulate activity and mesolimbic connectivity. Biological Psychiatry 66, 407414.
Heim, C, Binder, EB (2012). Current research trends in early life stress and depression: review of human studies on sensitive periods, gene–environment interactions, and epigenetics. Experimental Neurology 233, 102111.
Heim, C, Newport, DJ, Heit, S, Graham, YP, Wilcox, M, Bonsall, R, Miller, AH, Nemeroff, CB (2000). Pituitary–adrenal and autonomic responses to stress in women after sexual and physical abuse in childhood. JAMA 284, 592597.
Heim, C, Newport, DJ, Mletzko, T, Miller, AH, Nemeroff, CB (2008). The link between childhood trauma and depression: insights from HPA axis studies in humans. Psychoneuroendocrinology 33, 693710.
Hsu, DT, Langenecker, SA, Kennedy, SE, Zubieta, JK, Heitzeg, MM (2010). fMRI BOLD responses to negative stimuli in the prefrontal cortex are dependent on levels of recent negative life stress in major depressive disorder. Psychiatry Research: Neuroimaging 183, 202208.
Inagaki, TK, Muscatell, KA, Irwin, MR, Cole, SW, Eisenberger, NI (2012). Inflammation selectively enhances amygdala activity to socially threatening images. NeuroImage 59, 32223226.
Laird, AR, Fox, PM, Price, CJ, Glahn, DC, Uecker, AM, Lancaster, JL, Turkeltaub, PE, Kochunov, P, Fox, PT (2005). ALE meta-analysis: controlling the false discovery rate and performing statistical contrasts. Human Brain Mapping 25, 155164.
Lee, R, Geracioti, TD Jr., Kasckow, JW, Coccaro, EF (2005). Childhood trauma and personality disorder: positive correlation with adult CSF corticotropin-releasing factor concentrations. Childhood 162, 995997.
Meyer-Lindenberg, A, Tost, H (2012). Neural mechanisms of social risk for psychiatric disorders. Nature Neuroscience 15, 663668.
Minzenberg, MJ, Fan, J, New, AS, Tang, CY, Siever, LJ (2007). Fronto-limbic dysfunction in response to facial emotion in borderline personality disorder: an event-related fMRI study. Psychiatry Research: Neuroimaging 155, 231243.
Mothersill, O, Morris, DW, Kelly, S, Rose, EJ, Bokde, A, Reilly, R, Gill, M, Corvin, AP, Donohoe, G (2014). Altered medial prefrontal activity during dynamic face processing in schizophrenia spectrum patients. Schizophrenia Research 157, 225230.
Nemeroff, CB, Heim, CM, Thase, ME, Klein, DN, Rush, AJ, Schatzberg, AF, Ninan, PT, McCullough, JP, Weiss, PM, Dunner, DL (2003). Differential responses to psychotherapy versus pharmacotherapy in patients with chronic forms of major depression and childhood trauma. Proceedings of the National Academy of Sciences of the United States of America 100, 1429314296.
Norbury, R, Taylor, MJ, Selvaraj, S, Murphy, SE, Harmer, CJ, Cowen, PJ (2009). Short-term antidepressant treatment modulates amygdala response to happy faces. Psychopharmacology 206, 197204.
Pruessner, JC, Champagne, F, Meaney, MJ, Dagher, A (2004). Dopamine release in response to a psychological stress in humans and its relationship to early life maternal care: a positron emission tomography study using [11C]raclopride. Journal of Neuroscience 24, 28252831.
Rauch, SL, Whalen, PJ, Shin, LM, McInerney, SC, Macklin, ML, Lasko, NB, Orr, SP, Pitman, RK (2000). Exaggerated amygdala response to masked facial stimuli in posttraumatic stress disorder: a functional MRI study. Biological Psychiatry 47, 769776.
Rawlings, NB, Norbury, R, Cowen, PJ, Harmer, CJ (2010). A single dose of mirtazapine modulates neural responses to emotional faces in healthy people. Psychopharmacology 212, 625634.
Schneider, S, Peters, J, Bromberg, U, Brassen, S, Menz, MM, Miedl, S, Loth, E, Banaschewski, T, Barbot, A, Barker, G, Conrod, PJ, Dalley, JW, Flor, H, Gallinat, J, Garavan, H, Heinz, A, Itterman, B, Mallik, C, Mann, K, Artiges, E, Paus, T, Poline, JB, Rietschel, M, Reed, L, Smolka, MN, Spanagel, R, Speiser, C, Ströhle, A, Struve, M, Schumann, G, Büchel, C, IMAGEN Consortium (2011). Boys do it the right way: sex-dependent amygdala lateralization during face processing in adolescents. NeuroImage 56, 18471853.
Sehlmeyer, C, Dannlowski, U, Schöning, S, Kugel, H, Pyka, M, Pfleiderer, B, Zwitserlood, P, Schiffbauer, H, Heindel, W, Arolt, V (2011). Neural correlates of trait anxiety in fear extinction. Psychological Medicine 41, 789798.
Selten, JP, Cantor-Graae, E (2005). Social defeat: risk factor for schizophrenia? British Journal of Psychiatry 187, 101102.
Selten, J-P, van der Ven, E, Rutten, BP, Cantor-Graae, E (2013). The social defeat hypothesis of schizophrenia: an update. Schizophrenia Bulletin 39, 11801186.
Siegle, GJ, Thompson, W, Carter, CS, Steinhauer, SR, Thase, ME (2007). Increased amygdala and decreased dorsolateral prefrontal bold responses in unipolar depression: related and independent features. Biological Psychiatry 61, 198209.
Spielberg, JM, Galarce, EM, Ladouceur, CD, McMakin, DL, Olino, TM, Forbes, EE, Silk, JS, Ryan, ND, Dahl, RE (2015). Adolescent development of inhibition as a function of SES and gender: converging evidence from behavior and fMRI. Human Brain Mapping 36, 31944203.
Spreng, RN, Mar, RA, Kim, AS (2009). The common neural basis of autobiographical memory, prospection, navigation, theory of mind, and the default mode: a quantitative meta-analysis. Journal of Cognitive Neuroscience 21, 489510.
Streit, F, Haddad, L, Paul, T, Frank, J, Schäfer, A, Nikitopoulos, J, Akdeniz, C, Lederbogen, F, Treutlein, J, Witt, S, Meyer-Lindenberg, A, Rietschel, M, Kirsch, P, Wüst, S (2014). A functional variant in the neuropeptide S receptor 1 gene moderates the influence of urban upbringing on stress processing in the amygdala. Stress 17, 352361.
Surguladze, S, Brammer, MJ, Keedwell, P, Giampietro, V, Young, AW, Travis, MJ, Williams, SC, Phillips, ML (2005). A differential pattern of neural response toward sad versus happy facial expressions in major depressive disorder. Biological Psychiatry 57, 201209.
Tottenham, N, Hare, TA, Quinn, BT, McCarry, TW, Nurse, M, Gilhooly, T, Millner, A, Galvan, A, Davidson, MC, Eigsti, IM (2010). Prolonged institutional rearing is associated with atypically large amygdala volume and difficulties in emotion regulation. Developmental Science 13, 4661.
Turkeltaub, PE, Eden, GF, Jones, KM, Zeffiro, TA (2002). Meta-analysis of the functional neuroanatomy of single-word reading: method and validation. NeuroImage 16, 765780.
Turkeltaub, PE, Eickhoff, SB, Laird, AR, Fox, M, Wiener, M, Fox, P (2012). Minimizing within-experiment and within-group effects in activation likelihood estimation meta-analyses. Human Brain Mapping 33, 113.
Van Os, J, Rutten, BP, Poulton, R (2008). Gene–environment interactions in schizophrenia: review of epidemiological findings and future directions. Schizophrenia Bulletin 34, 10661082.
Van Overwalle, F (2009). Social cognition and the brain: a meta-analysis. Human Brain Mapping 30, 829858.
Van Reekum, CM, Urry, HL, Johnstone, T, Thurow, ME, Frye, CJ, Jackson, CA, Schaefer, HS, Alexander, AL, Davidson, RJ (2007). Individual differences in amygdala and ventromedial prefrontal cortex activity are associated with evaluation speed and psychological well-being. Journal of Cognitive Neuroscience 19, 237248.
Volz, KG, Schubotz, RI, Von Cramon, DY (2005). Variants of uncertainty in decision-making and their neural correlates. Brain Research Bulletin 67, 403412.
Wagner, S, Sebastian, A, Lieb, K, Tüscher, O, Tadić, A (2014). A coordinate-based ALE functional MRI meta-analysis of brain activation during verbal fluency tasks in healthy control subjects. BMC Neuroscience 15, 19.
Widom, CS, Dumont, K, Czaja, SJ (2007). A prospective investigation of major depressive disorder and comorbidity in abused and neglected children grown up. Archives of General Psychiatry 64, 4956.
Windischberger, C, Lanzenberger, R, Holik, A, Spindelegger, C, Stein, P, Moser, U, Gerstl, F, Fink, M, Moser, E, Kasper, S (2010). Area-specific modulation of neural activation comparing escitalopram and citalopram revealed by pharmaco-fMRI: a randomized cross-over study. NeuroImage 49, 11611170.
Yurgelun-Todd, DA, Gruber, SA, Kanayama, G, Killgore, WD, Baird, AA, Young, AD (2000). fMRI during affect discrimination in bipolar affective disorder. Bipolar Disorders 2, 237248.

Keywords

Type Description Title
WORD
Supplementary materials

Mothersill and Donohoe supplementary material
Tables S1-S2

 Word (904 KB)
904 KB

Metrics

Altmetric attention score

Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed