Abstract
As humans, we face a variety of social stressors on a regular basis. Given the established role of social stress in influencing physical and psychological functioning, researchers have focused immense efforts on understanding the psychological and physiological changes induced by exposure to acute social stressors. With the advancement of functional magnetic resonance imaging (fMRI), more recent work has sought to identify the neural correlates of processing acute social stress. In this review, we provide an overview of research on the neural underpinnings of social stress processing to date. Specifically, we summarize research that has examined the neural underpinnings of three types of social stressors commonly studied in the literature: social rejection, social evaluation, and racism-related stress. Within our discussion of each type of social stressor, we describe the methods used to induce stress, the brain regions commonly activated among studies investigating that type of stress, and recommendations for future work. This review of the current literature identifies activity in midline regions in both prefrontal and parietal cortices, as well as lateral prefrontal regions, as being associated with processing social rejection. Activity in the insula, thalamus, and inferior frontal gyrus is often found in studies using social evaluation tasks. Finally, racism-related stress is associated with activity in the ventrolateral prefrontal cortex and rostral anterior cingulate cortex. We conclude by taking a “30,000-foot view” of this area of research to provide suggestions for the future of research on the neuroscience of social stress.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
References
Akdeniz C, Tost H, Streit F, Haddad L, Wüst S, Schäfer A et al (2014) Neuroimaging evidence for a role of neural social stress processing in ethnic minority-associated environmental risk. JAMA Psychiat 71(6):672–680. https://doi.org/10.1001/jamapsychiatry.2014.35
Bailey ZD, Krieger N, Agénor M, Graves J, Linos N, Bassett MT (2017) Structural racism and health inequities in the USA: evidence and interventions. Lancet 389(10077):1453–1463. https://doi.org/10.1016/S0140-6736(17)30569-X
Bassett DS, Sporns O (2017) Network neuroscience. Nat Neurosci 20(3):353–364. https://doi.org/10.1038/nn.4502
Bassett DS, Zurn P, Gold JI (2018) On the nature and use of models in network neuroscience. Nat Rev Neurosci 19(9):566–578. https://doi.org/10.1038/s41583-018-0038-8
Berretz G, Packheiser J, Kumsta R, Wolf OT, Ocklenburg S (2021) The brain under stress – a systematic review and activation likelihood estimation meta-analysis of changes in BOLD signal associated with acute stress exposure. Neurosci Biobehav Rev. https://doi.org/10.1016/j.neubiorev.2021.01.001
Blascovich J, Tomaka J (1996) The biopsychosocial model of arousal regulation. Adv Exp Soc Psychol 28:1–51
Boyle CC, Stanton AL, Eisenberger NI, Seeman TE, Bower JE (2020) Effects of stress-induced inflammation on reward processing in healthy young women. Brain Behav Immun 83:126–134. https://doi.org/10.1016/j.bbi.2019.09.023
Brondolo E, Gallo LC, Myers HF (2009) Race, racism and health: disparities, mechanisms, and interventions. J Behav Med 32(1):1–8. https://doi.org/10.1007/s10865-008-9190-3
Buhle JT, Silvers JA, Wager TD, Lopez R, Onyemekwu C, Kober H et al (2013) Cognitive reappraisal of emotion: a meta-analysis of human neuroimaging studies. Cereb Cortex. https://doi.org/10.1093/cercor/bht154
Cohen JR (2018) The behavioral and cognitive relevance of time-varying, dynamic changes in functional connectivity. Neuroimage 180(Pt B):515–525. https://doi.org/10.1016/j.neuroimage.2017.09.036
Cohen JR, D’Esposito M (2016) The segregation and integration of distinct brain networks and their relationship to cognition. J Neurosci 36(48):12083–12094. https://doi.org/10.1523/JNEUROSCI.2965-15.2016
Dedovic K, Renwick R, Mahani NK, Engert V, Lupien SJ, Pruessner JC (2005) The Montreal imaging stress task: using functional imaging to investigate the effects of perceiving and processing psychosocial stress in the human brain. J Psychiatry Neurosci 30(5):319–325
Dedovic K, D’Aguiar C, Pruessner JC (2009a) What stress does to your brain: a review of neuroimaging studies. Can J Psychiatry 54(1):6–15. https://doi.org/10.1177/070674370905400104
Dedovic K, Rexroth M, Wolff E, Duchesne A, Scherling C, Beaudry T et al (2009b) Neural correlates of processing stressful information: an event-related fMRI study. Brain Res 1293:49–60. https://doi.org/10.1016/j.brainres.2009.06.044
Dickerson SS, Kemeny ME (2004) Acute stressors and cortisol responses: a theoretical integration and synthesis of laboratory research. Psychol Bull 130(3):355–391. https://doi.org/10.1037/0033-2909.130.3.355
Eisenbarth H, Chang LJ, Wager TD (2016) Multivariate brain prediction of heart rate and skin conductance responses to social threat. J Neurosci 36(47):11987–11998. https://doi.org/10.1523/JNEUROSCI.3672-15.2016
Eisenberger NI, Lieberman MD, Williams KD (2003) Does rejection hurt? An FMRI study of social exclusion. Science 302(5643):290–292. https://doi.org/10.1126/science.1089134
Eisenberger NI, Inagaki TK, Muscatell KA, Byrne Haltom KE, Leary MR (2011) The neural sociometer: brain mechanisms underlying state self-esteem. J Cogn Neurosci 23(11):3448–3455. https://doi.org/10.1162/jocn_a_00027
Gianaros PJ, Jennings JR (2018) Host in the machine: a neurobiological perspective on psychological stress and cardiovascular disease. Am Psychol 73(8):1031–1044. https://doi.org/10.1037/amp0000232
Ginty AT, Kraynak TE, Fisher JP, Gianaros PJ (2017) Cardiovascular and autonomic reactivity to psychological stress: neurophysiological substrates and links to cardiovascular disease. Autono Neurosci 207:2–9. https://doi.org/10.1016/j.autneu.2017.03.003
Guyer AE, Lau JYF, McClure-Tone EB, Parrish J, Shiffrin ND, Reynolds RC et al (2008) Amygdala and ventrolateral prefrontal cortex function during anticipated peer evaluation in pediatric social anxiety. Arch Gen Psychiatry 65(11):1303–1312. https://doi.org/10.1001/archpsyc.65.11.1303
Jolly E, Chang LJ (2019) The flatland fallacy: moving beyond low-dimensional thinking. Top Cogn Sci 11(2):433–454. https://doi.org/10.1111/tops.12404
Jones CP (2000) Levels of racism: a theoretic framework and a gardener’s tale. Am J Public Health 90(8):1212–1215. https://doi.org/10.2105/ajph.90.8.1212
Kirschbaum C, Pirke K-M, 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. https://doi.org/10.1159/000119004
Kraynak TE, Marsland AL, Wager TD, Gianaros PJ (2018) Functional neuroanatomy of peripheral inflammatory physiology: a meta-analysis of human neuroimaging studies. Neurosci Biobehav Rev 94:76–92. https://doi.org/10.1016/j.neubiorev.2018.07.013
Kross E, Ayduk O (2011) Making meaning out of negative experiences by self-distancing. Curr Dir Psychol Sci 20(3):187–191. https://doi.org/10.1177/0963721411408883
Kross E, Berman MG, Mischel W, Smith EE, Wager TD (2011) Social rejection shares somatosensory representations with physical pain. Proc Natl Acad Sci U S A 108(15):6270–6275. https://doi.org/10.1073/pnas.1102693108
Kross E, Bruehlman-Senecal E, Park J, Burson A, Dougherty A, Shablack H et al (2014) Self-talk as a regulatory mechanism: how you do it matters. J Pers Soc Psychol 106(2):304–324. https://doi.org/10.1037/a0035173
Kucyi A, Tambini A, Sadaghiani S, Keilholz S, Cohen JR (2018) Spontaneous cognitive processes and the behavioral validation of time-varying brain connectivity. Netw Neurosci 2(4):397–417. https://doi.org/10.1162/netn_a_00037
Lederbogen F, Kirsch P, Haddad L, Streit F, Tost H, Schuch P et al (2011) City living and urban upbringing affect neural social stress processing in humans. Nature 474(7352):498–501. https://doi.org/10.1038/nature10190
Lindquist KA, Wager TD, Kober H, Bliss-Moreau E, Barrett LF (2012) The brain basis of emotion: a meta-analytic review. Behav Brain Sci 35(3):121–143. https://doi.org/10.1017/S0140525X11000446
Masten CL, Telzer EH, Eisenberger NI (2011) An FMRI investigation of attributing negative social treatment to racial discrimination. J Cogn Neurosci 23(5):1042–1051. https://doi.org/10.1162/jocn.2010.21520
Menon V, Uddin LQ (2010) Saliency, switching, attention and control: a network model of insula function. Brain Struct Funct 214(5–6):655–667. https://doi.org/10.1007/s00429-010-0262-0
Mischkowski D, Kross E, Bushman BJ (2012) Flies on the wall are less aggressive: self-distancing “in the heat of the moment” reduces aggressive thoughts, angry feelings and aggressive behavior. J Exp Soc Psychol 48(5):1187–1191. https://doi.org/10.1016/j.jesp.2012.03.012
Murphy MLM, Slavich GM, Chen E, Miller GE (2015) Targeted rejection predicts decreased anti-inflammatory gene expression and increased symptom severity in youth with asthma. Psychol Sci 26(2):111–121. https://doi.org/10.1177/0956797614556320
Muscatell KA, Eisenberger NI (2012) A social neuroscience perspective on stress and health. Soc Personal Psychol Compass 6(12):890–904. https://doi.org/10.1111/j.1751-9004.2012.00467.x
Muscatell KA, Dedovic K, Slavich GM, Jarcho MR, Breen EC, Bower JE et al (2015) Greater amygdala activity and dorsomedial prefrontal-amygdala coupling are associated with enhanced inflammatory responses to stress. Brain Behav Immun 43:46–53. https://doi.org/10.1016/j.bbi.2014.06.201
Neblett EW (2019) Racism and health: challenges and future directions in behavioral and psychological research. Cultur Divers Ethnic Minor Psychol 25(1):12–20. https://doi.org/10.1037/cdp0000253
Noack H, Nolte L, Nieratschker V, Habel U, Derntl B (2019) Imaging stress: an overview of stress induction methods in the MR scanner. J Neural Transm 126(9):1187–1202. https://doi.org/10.1007/s00702-018-01965-y
Payne BK, Hannay JW (2021) Implicit bias reflects systemic racism. Trends Cogn Sci. https://doi.org/10.1016/j.tics.2021.08.001
Payne BK, Vuletich HA, Lundberg KB (2017) The bias of crowds: how implicit bias bridges personal and systemic prejudice. Psychol Inq 28(4):233–248. https://doi.org/10.1080/1047840X.2017.1335568
Payne BK, Vuletich HA, Brown-Iannuzzi JL (2019) Historical roots of implicit bias in slavery. Proc Natl Acad Sci U S A 116(24):11693–11698. https://doi.org/10.1073/pnas.1818816116
Perini I, Gustafsson PA, Hamilton JP, Kämpe R, Zetterqvist M, Heilig M (2018) The salience of self, not social pain, is encoded by dorsal anterior cingulate and insula. Sci Rep 8(1):6165. https://doi.org/10.1038/s41598-018-24658-8
Poldrack RA, Yarkoni T (2016) From brain maps to cognitive ontologies: informatics and the search for mental structure. Annu Rev Psychol 67:587–612. https://doi.org/10.1146/annurev-psych-122414-033729
Raio CM, Orederu TA, Palazzolo L, Shurick AA, Phelps EA (2013) Cognitive emotion regulation fails the stress test. Proc Natl Acad Sci U S A 110(37):15139–15144. https://doi.org/10.1073/pnas.1305706110
Shermohammed M, Mehta PH, Zhang J, Brandes CM, Chang LJ, Somerville LH (2017) Does psychosocial stress impact cognitive reappraisal? Behavioral and neural evidence. J Cogn Neurosci 29(11):1803–1816. https://doi.org/10.1162/jocn_a_01157
Sin NL, Graham-Engeland JE, Ong AD, Almeida DM (2015) Affective reactivity to daily stressors is associated with elevated inflammation. Health Psychol 34(12):1154–1165. https://doi.org/10.1037/hea0000240
Slavich GM (2020) Social safety theory: a biologically based evolutionary perspective on life stress, health, and behavior. Annu Rev Clin Psychol 16:265–295. https://doi.org/10.1146/annurev-clinpsy-032816-045159
Slavich GM, Thornton T, Torres LD, Monroe SM, Gotlib IH (2009) Targeted rejection predicts hastened onset of major depression. J Soc Clin Psychol 28(2):223–243. https://doi.org/10.1521/jscp.2009.28.2.223
Somerville LH, Heatherton TF, Kelley WM (2006) Anterior cingulate cortex responds differentially to expectancy violation and social rejection. Nat Neurosci 9(8):1007–1008. https://doi.org/10.1038/nn1728
Steinhauser M, Maier M, Hübner R (2007) Cognitive control under stress: how stress affects strategies of task-set reconfiguration. Psychol Sci 18(6):540–545. https://doi.org/10.1111/j.1467-9280.2007.01935.x
Streit F, Haddad L, Paul T, Frank J, Schäfer A, Nikitopoulos J et al (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(4):352–361. https://doi.org/10.3109/10253890.2014.921903
Thayer JF, Ahs F, Fredrikson M, Sollers JJ, Wager TD (2012) A meta-analysis of heart rate variability and neuroimaging studies: implications for heart rate variability as a marker of stress and health. Neurosci Biobehav Rev 36(2):747–756. https://doi.org/10.1016/j.neubiorev.2011.11.009
Uddin LQ (2015) Salience processing and insular cortical function and dysfunction. Nat Rev Neurosci 16(1):55–61. https://doi.org/10.1038/nrn3857
Vijayakumar N, Cheng TW, Pfeifer JH (2017) Neural correlates of social exclusion across ages: a coordinate-based meta-analysis of functional MRI studies. Neuroimage 153:359–368. https://doi.org/10.1016/j.neuroimage.2017.02.050
Wager TD, van Ast VA, Hughes BL, Davidson ML, Lindquist MA, Ochsner KN (2009a) Brain mediators of cardiovascular responses to social threat, part II: prefrontal-subcortical pathways and relationship with anxiety. Neuroimage 47(3):836–851. https://doi.org/10.1016/j.neuroimage.2009.05.044
Wager TD, Waugh CE, Lindquist M, Noll DC, Fredrickson BL, Taylor SF (2009b) 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. https://doi.org/10.1016/j.neuroimage.2009.05.043
Wang H, Braun C, Enck P (2017) How the brain reacts to social stress (exclusion) – a scoping review. Neurosci Biobehav Rev 80:80–88. https://doi.org/10.1016/j.neubiorev.2017.05.012
Wheelock MD, Rangaprakash D, Harnett NG, Wood KH, Orem TR, Mrug S et al (2018) Psychosocial stress reactivity is associated with decreased whole-brain network efficiency and increased amygdala centrality. Behav Neurosci 132(6):561–572. https://doi.org/10.1037/bne0000276
Williams DR, Mohammed SA (2013) Racism and health I: pathways and scientific evidence. Am Behav Sci 57(8). https://doi.org/10.1177/0002764213487340
Williams KD, Cheung CKT, Choi W (2000) Cyberostracism: effects of being ignored over the internet. J Pers Soc Psychol 79(5):748–762. https://doi.org/10.1037/0022-3514.79.5.748
Wright KD, Jack AI, Friedman JP, Jones LM, Sattar A, Fresco DM, Moore SM (2020) Neural processing and perceived discrimination stress in african americans. Nurs Res 69(5):331–338. https://doi.org/10.1097/NNR.0000000000000441
Yarkoni T, Poldrack RA, Van Essen DC, Wager TD (2010) Cognitive neuroscience 2.0: building a cumulative science of human brain function. Trends Cogn Sci 14(11):489–496. https://doi.org/10.1016/j.tics.2010.08.004
Zhang W, Llera A, Hashemi MM, Kaldewaij R, Koch SBJ, Beckmann CF et al (2020) Discriminating stress from rest based on resting-state connectivity of the human brain: a supervised machine learning study. Hum Brain Mapp 41(11):3089–3099. https://doi.org/10.1002/hbm.25000
Zöller C, Maroof P, Weik U, Deinzer R (2010) No effect of social exclusion on salivary cortisol secretion in women in a randomized controlled study. Psychoneuroendocrinology 35(9):1294–1298. https://doi.org/10.1016/j.psyneuen.2010.02.019
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2021 The Author(s), under exclusive license to Springer Nature Switzerland AG
About this chapter
Cite this chapter
Muscatell, K.A., Merritt, C.C., Cohen, J.R., Chang, L., Lindquist, K.A. (2021). The Stressed Brain: Neural Underpinnings of Social Stress Processing in Humans. In: Miczek, K.A., Sinha, R. (eds) Neuroscience of Social Stress. Current Topics in Behavioral Neurosciences, vol 54. Springer, Cham. https://doi.org/10.1007/7854_2021_281
Download citation
DOI: https://doi.org/10.1007/7854_2021_281
Published:
Publisher Name: Springer, Cham
Print ISBN: 978-3-031-04255-3
Online ISBN: 978-3-031-04256-0
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)