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Differential brain activity as a function of social evaluative stress in early adolescence: Brain function and salivary cortisol

Published online by Cambridge University Press:  11 January 2021

Max P. Herzberg ,
Ruskin H. Hunt ,
Kathleen M. Thomas  and
Megan R. Gunnar
Max P. Herzberg
Affiliation:
Institute of Child Development, University of Minnesota, Minneapolis, MN, USA
Ruskin H. Hunt
Affiliation:
Institute of Child Development, University of Minnesota, Minneapolis, MN, USA
Kathleen M. Thomas*
Affiliation:
Institute of Child Development, University of Minnesota, Minneapolis, MN, USA
Megan R. Gunnar
Affiliation:
Institute of Child Development, University of Minnesota, Minneapolis, MN, USA
*
Author for Correspondence: Kathleen Thomas, Institute of Child Development, 51 East River Road, Minneapolis, MN55455, USA; E-mail: thoma114@umn.edu
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Abstract

Understanding individual differences in neural responses to stressful environments is an important avenue of research throughout development. These differences may be especially critical during adolescence, which is characterized by opportunities for healthy development and increased susceptibility to the development of psychopathology. While the neural correlates of the psychosocial stress response have been investigated in adults, these links have not been explored during development. Using a new task, the Minnesota Imaging Stress Test in Children (MISTiC), differences in activation are found in fusiform gyrus, superior frontal gyrus, insula, and anterior cingulate cortex when comparing a stressful math task to a nonstressful math task. The MISTiC task successfully elicits cortisol responses in a similar proportion of adolescents as in behavioral studies while collecting brain imaging data. Cortisol responders and nonresponders did not differ in their perceived stress level or behavioral performance during the task despite differences in neuroendocrine function. Future research will be able to leverage the MISTiC task for many purposes, including probing associations between individual differences in stress responses with environmental conditions, personality differences, and the development of psychopathology.

Keywords

adolescencebrain functioncortisolsocially evaluative stress
Type
Special Section 2: Early Adversity and Development: Contributions from the Field
Information
Development and Psychopathology , Volume 32 , Special Issue 5: Early Adversity, Stress, and Neurobehavioral Development: Honoring Megan R. Gunnar's Contributions to Developmental Science , December 2020 , pp. 1926 - 1936
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Copyright
Copyright © Cambridge University Press 2020

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References

Buhle, J. T., Silvers, J. A., Wage, T. D., Lopez, R., Onyemekwu, C., Kober, H., … Ochsner, K. N. (2014). Cognitive reappraisal of emotion: A meta-analysis of human neuroimaging studies. Cerebral Cortex, 24, 2981–2990. doi:10.1093/cercor/bht154CrossRefGoogle ScholarPubMed
Buske-Kirschbaum, A., Jobst, S., Wustmans, A., Kirschbaum, C., Rauh, W., & Hellhammer, D. (1997). Attenuated free cortisol response to psychosocial stress in children with atopic dermatitis. Psychosomatic Medicine, 59, 419–426. doi:10.1097/00006842-199707000-00012CrossRefGoogle ScholarPubMed
Casey, B. J. (2015). Beyond simple models of self-control to circuit-based accounts of adolescent behavior. Annual Review of Psychology, 66, 295–319. doi:10.1146/annurev-psych-010814-015156CrossRefGoogle ScholarPubMed
Collins, A., & Frankenhaeuser, M. (1978). Stress responses in male and female engineering students. Journal of Human Stress, 4, 43–48. doi:10.1080/0097840X.1978.9934986CrossRefGoogle ScholarPubMed
Dahl, R. E., & Gunnar, M. R. (2009). Heightened stress responsiveness and emotional reactivity during pubertal maturation: Implications for psychopathology. Development and Psychopathology, 21, 1–6. doi:10.1017/S0954579409000017CrossRefGoogle ScholarPubMed
Dedovic, K., Renwick, R., Mahani, N. K., Engert, V., Lupien, S. J., & Pruessner, J. C. (2005). The Montreal imaging stress task: using functional imaging to investigate the effects of perceiving and processing psychosocial stress in the human brain. Journal of Psychiatry and Neuroscience, 30, 319–325. Retrieved from papers2://publication/uuid/8CB2D146-A393-451E-BCFE-64783DE6BA92.Google ScholarPubMed
Dedovic, K., Rexroth, M., Wolff, E., Duchesne, A., Scherling, C., Beaudry, T., … Pruessner, J. C. (2009). Neural correlates of processing stressful information: An event-related fMRI study. Brain Research, 1293, 49–60. doi:10.1016/j.brainres.2009.06.044CrossRefGoogle ScholarPubMed
Dickerson, S. S., & Kemeny, M. E. (2004). Acute stressors and cortisol responses: A theoretical integration and synthesis of laboratory research. Psychological Bulletin, 130, 355–391. doi:10.1037/0033-2909.130.3.355CrossRefGoogle ScholarPubMed
Ditzen, B., Neumann, I. D., Bodenmann, G., von Dawans, B., Turner, R. A., Ehlert, U., & Heinrichs, M. (2007). Effects of different kinds of couple interaction on cortisol and heart rate responses to stress in women. Psychoneuroendocrinology, 32, 565–574. doi:10.1016/j.psyneuen.2007.03.011CrossRefGoogle ScholarPubMed
Doom, J. R., Doyle, C. M., & Gunnar, M. R. (2017). Social stress buffering by friends in childhood and adolescence: Effects on HPA and oxytocin activity. Social Neuroscience, 12, 8–21. doi:10.1080/17470919.2016.1149095CrossRefGoogle ScholarPubMed
Eisenberger, N. I. (2012). The pain of social disconnection: Examining the shared neural underpinnings of physical and social pain. Nature Reviews Neuroscience, 13, 421–434. doi:10.1038/nrn3231CrossRefGoogle ScholarPubMed
Eisenberger, N. I. (2015). Meta-analytic evidence for the role of the anterior cingulate cortex in social pain. Social Cognitive and Affective Neuroscience, 10, 1–2. doi:10.1093/scan/nsu120CrossRefGoogle ScholarPubMed
Frankenhaeuser, M., von Wright, M. R., Collins, A., von Wright, J., Sedvall, G., & Swahn, C. G. (1978). Sex differences in psychoneuroendocrine reactions to examination stress. Psychosomatic Medicine, 40, 334–343. doi:10.1097/00006842-197806000-00006CrossRefGoogle ScholarPubMed
Frisch, J. U., Häusser, J. A., & Mojzisch, A. (2015). The Trier Social Stress Test as a paradigm to study how people respond to threat in social interactions. Frontiers in Psychology, 6(FEB), 1–15. doi:10.3389/fpsyg.2015.00014CrossRefGoogle ScholarPubMed
Gunnar, M. R., & Thomas, K. M. (2017). [Development of social evaluative stress task in fMRI environment during early adolescence]. Unpublished raw data.Google Scholar
Heinrichs, M., Baumgartner, T., Kirschbaum, C., & Ehlert, U. (2003). Social support and oxytocin interact to suppress cortisol and subjective responses to psychosocial stress. Biological Psychiatry, 54, 1389–1398. doi:10.1016/S0006-3223(03)00465-7CrossRefGoogle ScholarPubMed
Hostinar, C. E., Johnson, A. E., & Gunnar, M. R. (2015). Parent support is less effective in buffering cortisol stress reactivity for adolescents compared to children. Developmental Science, 18, 281–297. doi:10.1111/desc.12195CrossRefGoogle ScholarPubMed
Jenkinson, M., Beckmann, C. F., Behrens, T. E. J., Woolrich, M. W., & Smith, S. M. (2012). FSL. NeuroImage, 62, 782–790. doi:10.1016/j.neuroimage.2011.09.015CrossRefGoogle ScholarPubMed
Kirschbaum, C., Pirke, K.-M., & Hellhammer, D. H. (1993). The “Trier social stress test” - a tool for investigating psychobiological stress responses in a laboratory setting. Neuropsychobiology, 28, 76–81.CrossRefGoogle Scholar
Korte, S. M., Koolhaas, J. M., Wingfield, J. C., & McEwen, B. S. (2005). The Darwinian concept of stress: Benefits of allostasis and costs of allostatic load and the trade-offs in health and disease. Neuroscience and Biobehavioral Reviews, 29(1 SPEC. ISS.), 3–38. doi:10.1016/j.neubiorev.2004.08.009CrossRefGoogle ScholarPubMed
Lupien, S. J., King, S., Meaney, M. J., & McEwen, B. S. (2001). Can poverty get under your skin? Basal cortisol levels and cognitive function in children from low and high socioeconomic status. The Science of Mental Health: Stress and the Brain, 13, 37–60.Google ScholarPubMed
Ochsner, K. N., Ray, R. D., Cooper, J. C., Robertson, E. R., Chopra, S., Gabrieli, J. D. E., & Gross, J. J. (2004). For better or for worse: Neural systems supporting the cognitive down- and up-regulation of negative emotion. NeuroImage, 23, 483–499. doi:10.1016/j.neuroimage.2004.06.030CrossRefGoogle ScholarPubMed
Paus, T., Keshavan, M., & Giedd, J. N. (2008). Why do many psychiatric disorders emerge during adolescence? Nature Reviews Neuroscience, 9, 947–957. doi:10.1038/nrn2513CrossRefGoogle ScholarPubMed
Pruessner, J. C., Dedovic, K., Khalili-Mahani, N., Engert, V., Pruessner, M., Buss, C., … Lupien, S. (2008). Deactivation of the limbic system during acute psychosocial stress: Evidence from positron emission tomography and functional magnetic resonance imaging studies. Biological Psychiatry, 63, 234–240. doi:10.1016/j.biopsych.2007.04.041CrossRefGoogle ScholarPubMed
Pruessner, J. C., Kirschbaum, C., Meinlschmid, G., & Hellhammer, D. H. (2003). Two formulas for computation of the area under the curve represent measures of total hormone concentration versus time-dependent change. Psychoneuroendocrinology, 28, 916–931. doi:10.1016/S0306-4530(02)00108-7CrossRefGoogle ScholarPubMed
R Core Team. (2013). R: A language and environment for statistical computing.Google Scholar
Rinne, L. F., & Mazzocco, M. M. M. (2014). Knowing right from wrong in mental arithmetic judgments: Calibration of confidence predicts the development of accuracy. PLoS ONE, 9, 1–11. doi:10.1371/journal.pone.0098663CrossRefGoogle ScholarPubMed
Spear, L. P. (2000). The adolescent brain and age-related behavioral manifestations. Neuroscience & Biobehavioral Reviews, 24, 417–463. Retrieved from https://linkinghub.elsevier.com/retrieve/pii/S0149763400000142%0Apapers3://publication/doi/10.1016/S0149-7634(00)00014-2CrossRefGoogle ScholarPubMed
Suleiman, A. B., & Dahl, R. E. (2017). Leveraging neuroscience to inform adolescent health: The need for an innovative transdisciplinary developmental science of adolescence. Journal of Adolescent Health, 60, 240–248. doi:10.1016/j.jadohealth.2016.12.010CrossRefGoogle ScholarPubMed
Sumter, S. R., Bokhorst, C. L., Miers, A. C., Van Pelt, J., & Westenberg, P. M. (2010). Age and puberty differences in stress responses during a public speaking task: Do adolescents grow more sensitive to social evaluation? Psychoneuroendocrinology, 35, 1510–1516. doi:10.1016/j.psyneuen.2010.05.004CrossRefGoogle ScholarPubMed
Takahashi, T., Ikeda, K., Ishikawa, M., Kitamura, N., Tsukasaki, T., Nakama, D., & Kameda, T. (2005). Anxiety, reactivity, and social stress-induced cortisol elevation in humans. Neuroendocrinology Letters, 26, 351–354.Google ScholarPubMed
Van Cauter, E., & Refetoff, S. (1985). Evidence for two subtypes of Cushing's disease based on the analysis of episodic cortisol secretion. New England Journal of Medicine, 312, 1343–1349. doi:10.1056/NEJM198505233122102CrossRefGoogle ScholarPubMed
Vijayakumar, N., Pfeifer, J. H., Flournoy, J. C., Hernandez, L. M., & Dapretto, M. (2019). Affective reactivity during adolescence: Associations with age, puberty and testosterone. Cortex, 117, 336–350. doi:10.1016/j.cortex.2019.04.024CrossRefGoogle ScholarPubMed
Wickham, H. (2016). ggplot2: Elegant graphics for data analysis. Retrieved from https://ggplot2.tidyverse.org.CrossRefGoogle Scholar
Woolrich, M. W., Behrens, T. E. J., Beckmann, C. F., Jenkinson, M., & Smith, S. M. (2004). Multilevel linear modelling for FMRI group analysis using Bayesian inference. NeuroImage, 21, 1732–1747. doi:10.1016/j.neuroimage.2003.12.023CrossRefGoogle ScholarPubMed
Woolrich, M. W., Ripley, B. D., Brady, M., & Smith, S. M. (2001). Temporal autocorrelation in univariate linear modeling of FMRI data. NeuroImage, 14, 1370–1386. doi:10.1006/nimg.2001.0931CrossRefGoogle ScholarPubMed
Yim, I. S., Quas, J. A., Cahill, L., & Hayakawa, C. M. (2010). Children's and adults’ salivary cortisol responses to an identical psychosocial laboratory stressor. Psychoneuroendocrinology, 35, 241–248. doi:10.1016/j.psyneuen.2009.06.014CrossRefGoogle Scholar
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