Skip to main content
Log in

Acute social stress modulates coherence regional homogeneity

  • Original Research
  • Published:
Brain Imaging and Behavior Aims and scope Submit manuscript

Abstract

It is a generally accepted observation that individuals act differently under stress. Recent task-based neuroimaging studies have shown that individuals under stress favor the intuitive and fast system over the deliberative and reflective system. In the present study, using a within-subjects design in thirty young adults, we examined whether and how acute social stress impacts regional neural activity in resting state. The results showed that stress induced lower coherence regional homogeneity (Cohe-ReHo) values in left hippocampus and right superior frontal gyrus, both of which are regions associated with deliberative decision making. Stress-induced cortisol change was significantly and positively correlated with the change in Cohe-ReHo value in the right midbrain, a region involved in habitual decision making. These results extend previous findings by demonstrating that stress modulates local synchrony in brain regions implicated in deliberative and intuitive decision making. Our findings might be useful in understanding the neural mechanisms underlying stress-related mental disorders.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Alexander, J. K., Hillier, A., Smith, R. M., Tivarus, M. E., & Beversdorf, D. Q. (2007). Beta-adrenergic modulation of cognitive flexibility during stress. Journal of Cognitive Neuroscience, 19(3), 468–478.

    Article  PubMed  Google Scholar 

  • Alfarez, D., Wiegert, O., Joels, M., & Krugers, H. (2002). Corticosterone and stress reduce synaptic potentiation in mouse hippocampal slices with mild stimulation. Neuroscience, 115(4), 1119–1126.

    Article  CAS  PubMed  Google Scholar 

  • Amunts, K., Kedo, O., Kindler, M., Pieperhoff, P., Mohlberg, H., Shah, N. J., Habel, U., Schneider, F., & Zilles, K. (2005). Cytoarchitectonic mapping of the human amygdala, hippocampal region and entorhinal cortex: Intersubject variability and probability maps. Anatomy and Embryology, 210(5–6), 343–352.

    Article  CAS  PubMed  Google Scholar 

  • Ances, B. M., Leontiev, O., Perthen, J. E., Liang, C., Lansing, A. E., & Buxton, R. B. (2008). Regional differences in the coupling of cerebral blood flow and oxygen metabolism changes in response to activation: Implications for BOLD-fMRI. NeuroImage, 39(4), 1510–1521.

    Article  PubMed  Google Scholar 

  • Arnold Anteraper, S., Triantafyllou, C., Sawyer, A. T., Hofmann, S. G., Gabrieli, J. D., & Whitfield-Gabrieli, S. (2014). Hyper-connectivity of subcortical resting-state networks in social anxiety disorder. Brain Connectivity, 4(2), 81–90.

    Article  PubMed  Google Scholar 

  • Arnsten, A. F. (2009). Stress signalling pathways that impair prefrontal cortex structure and function. Nature Reviews Neuroscience, 10(6), 410–422.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ashburner, J. (2007). A fast diffeomorphic image registration algorithm. NeuroImage, 38(1), 95–113.

    Article  PubMed  Google Scholar 

  • Atsak, P., Guenzel, F. M., Kantar-Gok, D., Zalachoras, I., Yargicoglu, P., Meijer, O. C., Quirarte, G. L., Wolf, O. T., Schwabe, L., & Roozendaal, B. (2016). Glucocorticoids mediate stress-induced impairment of retrieval of stimulus-response memory. Psychoneuroendocrinology, 67, 207–215.

    Article  CAS  PubMed  Google Scholar 

  • Bomyea, J., & Lang, A. J. (2016). Accounting for intrusive thoughts in PTSD: Contributions of cognitive control and deliberate regulation strategies. Journal of Affecitive Disorder, 192, 184–190.

    Article  Google Scholar 

  • Brown, S. M., Henning, S., & Wellman, C. L. (2005). Mild, short-term stress alters dendritic morphology in rat medial prefrontal cortex. Cerebral Cortex, 15(11), 1714–1722.

    Article  PubMed  Google Scholar 

  • Brunson, K. L. (2005). Mechanisms of late-onset cognitive decline after early-life stress. Journal of Neuroscience, 25(41), 9328–9338.

    Article  CAS  PubMed  Google Scholar 

  • Buckner, R. L., & Wheeler, M. E. (2001). The cognitive neuroscience of remembering. Nature Reviews Neuroscience, 2(9), 624–634.

    Article  CAS  PubMed  Google Scholar 

  • Diamond, D. M., Campbell, A. M., Park, C. R., Halonen, J., & Zoladz, P. R. (2007). The temporal dynamics model of emotional memory processing: A synthesis on the neurobiological basis of stress-induced amnesia, flashbulb and traumatic memories, and the yerkes-Dodson law. Neural Plasticity, 2007, 1–33.

    Article  Google Scholar 

  • Evans, J. S. B., & Frankish, K. E. (2009). In two minds: Dual processes and beyond. Oxford University Press.

  • Evans, J. S. B., & Stanovich, K. E. (2013). Dual-process theories of higher cognition: Advancing the debate. Perspectives on Psychological Science, 8(3), 223–241.

    Article  PubMed  Google Scholar 

  • Fleisher, A. S., Podraza, K. M., Bangen, K. J., Taylor, C., Sherzai, A., Sidhar, K., Liu, T. T., Dale, A. M., & Buxton, R. B. (2009a). Cerebral perfusion and oxygenation differences in Alzheimer's disease risk. Neurobiology of Aging, 30(11), 1737–1748.

    Article  CAS  PubMed  Google Scholar 

  • Fleisher, A. S., Sherzai, A., Taylor, C., Langbaum, J. B., Chen, K., & Buxton, R. B. (2009b). Resting-state BOLD networks versus task-associated functional MRI for distinguishing Alzheimer's disease risk groups. NeuroImage, 47(4), 1678–1690.

    Article  PubMed  PubMed Central  Google Scholar 

  • Friston, K. J., Williams, S., Howard, R., Frackowiak, R. S., & Turner, R. (1996). Movement-related effects in fMRI time-series. Magnetic Resonance in Medicine, 35(3), 346–355.

    Article  CAS  PubMed  Google Scholar 

  • Gray, J. D., Rubin, T. G., Hunter, R. G., & McEwen, B. S. (2014). Hippocampal gene expression changes underlying stress sensitization and recovery. Molecular Psychiatry, 19(11), 1171–1178.

    Article  CAS  PubMed  Google Scholar 

  • Haeffel, G. J., Abramson, L. Y., Brazy, P. C., Shah, J. Y., Teachman, B. A., & Nosek, B. A. (2007). Explicit and implicit cognition: A preliminary test of a dual-process theory of cognitive vulnerability to depression. Behaviour Research and Therapy, 45(6), 1155–1167.

    Article  PubMed  Google Scholar 

  • Hamilton, J. P., Furman, D. J., Chang, C., Thomason, M. E., Dennis, E., & Gotlib, I. H. (2011). Default-mode and task-positive network activity in major depressive disorder: Implications for adaptive and maladaptive rumination. Biological Psychiatry, 70(4), 327–333.

    Article  PubMed  PubMed Central  Google Scholar 

  • Hermans, E. J., Henckens, M. J., Joels, M., & Fernandez, G. (2014). Dynamic adaptation of large-scale brain networks in response to acute stressors. Trends in Neuroscience, 37(6), 304–314.

    Article  CAS  Google Scholar 

  • Hu, J., Lee, D., Hu, S., Zhang, S., Chao, H., & Li, C. S. (2016). Individual variation in the neural processes of motor decisions in the stop signal task: The influence of novelty seeking and harm avoidance personality traits. Brain Structure and Function, 221(5), 2607–2618.

    Article  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • de Kloet, E. R., Sibug, R. M., Helmerhorst, F. M., & Schmidt, M. V. (2005). Stress, genes and the mechanism of programming the brain for later life. Neuroscience and Biobehavior Review, 29(2), 271–281.

    Article  CAS  Google Scholar 

  • Kruse, O., León, I. T., Stalder, T., Stark, R., & Klucken, T. (2017). Altered reward learning and hippocampal connectivity following psychosocial stress. NeuroImage, 171, 15–25.

    Article  PubMed  Google Scholar 

  • Lee, T., Jarome, T., Li, S.-J., Kim, J. J., & Helmstetter, F. J. (2009). Chronic stress selectively reduces hippocampal volume in rats: A longitudinal magnetic resonance imaging study. Neuroreport, 20(17), 1554–1558.

    Article  PubMed  PubMed Central  Google Scholar 

  • Liu, D., Yan, C., Ren, J., Yao, L., Kiviniemi, V. j., & Zang, Y. (2010). Using coherence to measure regional homogeneity of resting-state fMRI signal. Frontier in Systems Neuroscience, 4, 24.

    Google Scholar 

  • Liu, F., Hu, M., Wang, S., Guo, W., Zhao, J., Li, J., et al. (2012). Abnormal regional spontaneous neural activity in first-episode, treatment-naive patients with late-life depression: A resting-state fMRI study. Progress in Neuro-Psychopharmacology and Biological Psychiatry, 39(2), 326–331.

  • Liu, Y., Zhao, X., Cheng, Z., Zhang, F., Chang, J., Wang, H., Xie, R., Wang, Z., Cao, L., & Wang, G. (2017). Regional homogeneity associated with overgeneral autobiographical memory of first-episode treatment-naive patients with major depressive disorder in the orbitofrontal cortex: Aresting-state fMRI study. Journal of Affective Disorder, 209, 163–168.

    Article  Google Scholar 

  • Lovallo, W. R., Robinson, J. L., Glahn, D. C., & Fox, P. T. (2010). Acute effects of hydrocortisone on the human brain: An fMRI study. Psychoneuroendocrinology, 35(1), 15–20.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Luethi, M., Meier, B., & Sandi, C. (2009). Stress effects on working memory, explicit memory, and implicit memory for neutral and emotional stimuli in healthy men. Frontiers in Behavioral Neuroscience, 2, 5.

    PubMed  PubMed Central  Google Scholar 

  • Maier, S. U., Makwana, A. B., & Hare, T. A. (2015). Acute stress impairs self-control in goal-directed choice by altering multiple functional connections within the brain's decision circuits. Neuron, 87(3), 621–631.

    Article  CAS  PubMed  Google Scholar 

  • McEwen, B. S. (1999). Stress and the aging hippocampus. Frontiers in Neuroendocrinology, 20(1), 49–70.

    Article  CAS  PubMed  Google Scholar 

  • McEwen, B. S., Bowles, N. P., Gray, J. D., Hill, M. N., Hunter, R. G., Karatsoreos, I. N., & Nasca, C. (2015). Mechanisms of stress in the brain. Nature Neuroscience, 18(10), 1353–1363.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • McEwen, B. S., Nasca, C., & Gray, J. D. (2016). Stress effects on neuronal structure: Hippocampus, amygdala, and prefrontal cortex. Neuropsychopharmacology, 41(1), 3–23.

    Article  CAS  PubMed  Google Scholar 

  • Mobbs, D., Petrovic, P., Marchant, J. L., Hassabis, D., Weiskopf, N., Seymour, B., Dolan, R. J., & Frith, C. D. (2007). When fear is near: Threat imminence elicits prefrontal-periaqueductal gray shifts in humans. Science, 317(5841), 1079–1083.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mobbs, D., Marchant, J. L., Hassabis, D., Seymour, B., Tan, G., Gray, M., Petrovic, P., Dolan, R. J., & Frith, C. D. (2009). From threat to fear: The neural organization of defensive fear systems in humans. Journal of Neuroscience, 29(39), 12236–12243.

    Article  CAS  PubMed  Google Scholar 

  • Mobbs, D., Hagan, C. C., Dalgleish, T., Silston, B., & Prévost, C. (2015). The ecology of human fear: Survival optimization and the nervous system. Frontiers in Neuroscience, 9.

  • Nguyen, E. T., Streicher, J., Berman, S., Caldwell, J. L., Ghisays, V., Estrada, C. M., Wulsin, A. C., & Solomon, M. B. (2017). A mixed glucocorticoid/mineralocorticoid receptor modulator dampens endocrine and hippocampal stress responsivity in male rats. Physiology & Behavior, 178, 82–92.

    Article  CAS  Google Scholar 

  • Oei, N. Y. L., Elzinga, B. M., Wolf, O. T., de Ruiter, M. B., Damoiseaux, J. S., Kuijer, J. P. A., Veltman, D. J., Scheltens, P., & Rombouts, S. A. R. B. (2007). Glucocorticoids decrease hippocampal and prefrontal activation during declarative memory retrieval in young men. Brain Imaging and Behavior, 1(1–2), 31–41.

    Article  PubMed  PubMed Central  Google Scholar 

  • Olver, J. S., Pinney, M., Maruff, P., & Norman, T. R. (2015). Impairments of spatial working memory and attention following acute psychosocial stress. Stress and Health, 31(2), 115–123.

    Article  PubMed  Google Scholar 

  • Pittenger, C., & Duman, R. S. (2008). Stress, depression, and neuroplasticity: A convergence of mechanisms. Neuropsychopharmacology, 33(1), 88–109.

    Article  CAS  PubMed  Google Scholar 

  • Power, J. D., Mitra, A., Laumann, T. O., Snyder, A. Z., Schlaggar, B. L., & Petersen, S. E. (2014). Methods to detect, characterize, and remove motion artifact in resting state fMRI. NeuroImage, 84, 320–341.

    Article  PubMed  Google Scholar 

  • Radley, J. J., Rocher, A. B., Miller, M., Janssen, W. G., Liston, C., Hof, P. R., McEwen, B., & Morrison, J. H. (2005). Repeated stress induces dendritic spine loss in the rat medial prefrontal cortex. Cerebral Cortex, 16(3), 313–320.

    Article  PubMed  Google Scholar 

  • Roley, M. E., Claycomb, M. A., Contractor, A. A., Dranger, P., Armour, C., & Elhai, J. D. (2015). The relationship between rumination, PTSD, and depression symptoms. Journal of Affective Disorder, 180, 116–121.

    Article  Google Scholar 

  • Rubin, L. H., Meyer, V. J., J. Conant, R., Sundermann, E. E., Wu, M., Weber, K. M., et al. (2016). Prefrontal cortical volume loss is associated with stress-related deficits in verbal learning and memory in HIV-infected women. Neurobiology of Disease, 92, 166–174.

  • Sandi, C. (2013). Stress and cognition. Wiley Interdisciplinary Reviews: Cognitive Science, 4(3), 245–261.

    PubMed  Google Scholar 

  • Sapolsky, R. M. (2000). The possibility of neurotoxicity in the hippocampus in major depression: A primer on neuron death. Biological Psychiatry, 48, 755–765.

    Article  CAS  PubMed  Google Scholar 

  • Schwabe, L., & Bolam, P. (2017). Memory under stress: From single systems to network changes. European Journal of Neuroscience, 45(4), 478–489.

    Article  PubMed  Google Scholar 

  • Schwabe, L., & Wolf, O. T. (2012). Stress modulates the engagement of multiple memory systems in classification learning. Journal of Neuroscience, 32(32), 11042–11049.

    Article  CAS  PubMed  Google Scholar 

  • Schwabe, L., & Wolf, O. T. (2013). Stress and multiple memory systems: From ‘thinking’ to ‘doing’. Trends in Cognitive Sciences, 17(2), 60–68.

    Article  PubMed  Google Scholar 

  • Schwabe, L., Dalm, S., Schächinger, H., & Oitzl, M. S. (2008). Chronic stress modulates the use of spatial and stimulus-response learning strategies in mice and man. Neurobiology of Learning and Memory, 90(3), 495–503.

    Article  PubMed  Google Scholar 

  • Schwabe, L., Oitzl, M. S., Richter, S., & Schächinger, H. (2009). Modulation of spatial and stimulus–response learning strategies by exogenous cortisol in healthy young women. Psychoneuroendocrinology, 34(3), 358–366.

    Article  CAS  PubMed  Google Scholar 

  • Schwabe, L., Joëls, M., Roozendaal, B., Wolf, O. T., & Oitzl, M. S. (2012). Stress effects on memory: An update and integration. Neuroscience & Biobehavioral Reviews, 36(7), 1740–1749.

    Article  Google Scholar 

  • Schwabe, L., Tegenthoff, M., Höffken, O., & Wolf, O. T. (2013). Mineralocorticoid receptor blockade prevents stress-induced modulation of multiple memory systems in the human brain. Biological Psychiatry, 74(11), 801–808.

    Article  CAS  PubMed  Google Scholar 

  • Simonovic, B., Stupple, E. J., Gale, M., & Sheffield, D. (2017). Stress and risky decision making: Cognitive reflection, emotional learning or both. Journal of Behavioral Decision Making, 30(2), 658–665.

    Article  Google Scholar 

  • Song, X. W., Dong, Z. Y., Long, X. Y., Li, S. F., Zuo, X. N., Zhu, C. Z., He, Y., Yan, C. G., & Zang, Y. F. (2011). REST: A toolkit for resting-state functional magnetic resonance imaging data processing. PLoS One, 6(9), e25031.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sterlemann, V., Ganea, K., Liebl, C., Harbich, D., Alam, S., Holsboer, F., Müller, M. B., & Schmidt, M. V. (2008). Long-term behavioral and neuroendocrine alterations following chronic social stress in mice: Implications for stress-related disorders. Hormones and Behavior, 53(2), 386–394.

    Article  CAS  PubMed  Google Scholar 

  • Stokes, M. G., Kusunoki, M., Sigala, N., Nili, H., Gaffan, D., & Duncan, J. (2013). Dynamic coding for cognitive control in prefrontal cortex. Neuron, 78(2), 364–375.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Travis, S. G., Coupland, N. J., Hegadoren, K., Silverstone, P. H., Huang, Y., Carter, R., Fujiwara, E., Seres, P., & Malykhin, N. V. (2016). Effects of cortisol on hippocampal subfields volumes and memory performance in healthy control subjects and patients with major depressive disorder. Journal of Affective Disorder, 201, 34–41.

    Article  CAS  Google Scholar 

  • Tzourio-Mazoyer, N., Hervé, P. Y., & Mazoyer, B. (2007). Neuroanatomy: Tool for functional localization, key to brain organization. NeuroImage, 37(4), 1059–1060.

    Article  CAS  PubMed  Google Scholar 

  • Vinkers, C. H., Joels, M., Milaneschi, Y., Kahn, R. S., Penninx, B. W., & Boks, M. P. (2014). Stress exposure across the life span cumulatively increases depression risk and is moderated by neuroticism. Depression and Anxiety, 31(9), 737–745.

    Article  PubMed  Google Scholar 

  • Vogel, S., Fernández, G., Joëls, M., & Schwabe, L. (2016). Cognitive adaptation under stress: A case for the mineralocorticoid receptor. Trends in Cognitive Sciences, 20(3), 192–203.

    Article  PubMed  Google Scholar 

  • Wellman, C. L. (2001). Dendritic reorganization in pyramidal neurons in medial prefrontal cortex after chronic corticosterone administration. Developmental Neurobiology, 49(3), 245–253.

    Article  CAS  Google Scholar 

  • Yan, C. G., Wang, X. D., Zuo, X. N., & Zang, Y. F. (2016). DPABI: Data processing & analysis for (resting-state) brain imaging. Neuroinformatics, 14(3), 339–351.

    Article  PubMed  Google Scholar 

  • Youssef, F. F., Dookeeram, K., Basdeo, V., Francis, E., Doman, M., Mamed, D., Maloo, S., Degannes, J., Dobo, L., Ditshotlo, P., & Legall, G. (2012). Stress alters personal moral decision making. Psychoneuroendocrinology, 37(4), 491–498.

    Article  PubMed  Google Scholar 

  • Yu, R. (2016). Stress potentiates decision biases: A stress induced deliberation-to-intuition (SIDI) model. Neurobiology of Stress, 3, 83–95.

    Article  PubMed  PubMed Central  Google Scholar 

  • Zang, Y., Jiang, T., Lu, Y., He, Y., & Tian, L. (2004). Regional homogeneity approach to fMRI data analysis. NeuroImage, 22(1), 394–400.

    Article  PubMed  Google Scholar 

  • Zhong, Y., Zhang, R., Li, K., Qi, R., Zhang, Z., Huang, Q., & Lu, G. (2015). Altered cortical and subcortical local coherence in PTSD: Evidence from resting-state fMRI. Acta Radiologica, 56(6), 746–753.

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

We thank J. Hu for collecting the data.

Funding

This study was funded by Natural Scientific Foundation of China (No. 81771186) and MOE Tier 2 (MOE2016-T2–1-015) to RY, and by the Scientific Research Foundation of School of Psychology at South China Normal University (hsxly2017003) to J. Chang.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Rongjun Yu.

Ethics declarations

Conflict of interest

Both authors have no conflict of interest.

Ethical approval

All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Chang, J., Yu, R. Acute social stress modulates coherence regional homogeneity. Brain Imaging and Behavior 13, 762–770 (2019). https://doi.org/10.1007/s11682-018-9898-9

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11682-018-9898-9

Keywords

Navigation