Acute stress alters the ‘default’ brain processing (original) (raw)

Abstract

Active adaptation to acute stress is essential for coping with daily life challenges. The stress hormone cortisol, as well as large scale reallocations of brain resources have been implicated in this adaptation. Stress-induced shifts between large-scale brain networks, including salience (SN), central executive (CEN) and default mode networks (DMN), have however been demonstrated mainly under task-conditions. It remains unclear whether such network shifts also occur in the absence of ongoing task-demands, and most critically, whether these network shifts are predictive of individual variation in the magnitude of cortisol stress-responses. In a sample of 335 healthy participants, we investigated stress-induced functional connectivity changes (delta-FC) of the SN, CEN and DMN, using resting-state fMRI data acquired before and after a socially evaluated coldpressor test and a mental arithmetic task. To investigate which network changes are associated with acute stress, we evaluated the association between cortisol increase and delta-FC of each network. Stress-induced cortisol increase was associated with increased connectivity within the SN, but with decreased coupling of DMN at both local (within network) and global (synchronization with brain regions also outside the network) levels. These findings indicate that acute stress prompts immediate connectivity changes in large-scale resting-state networks, including the SN and DMN in the absence of explicit ongoing task-demands. Most interestingly, this brain reorganization is coupled with individuals' cortisol stress-responsiveness. These results suggest that the observed stress-induced network reorganization might function as a neural mechanism determining individual stress reactivity and, therefore, it could serve as a promising marker for future studies on stress resilience and vulnerability.

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References (64)

  1. Admon, R., Milad, M.R., Hendler, T., 2013. A causal model of post-traumatic stress disorder: Disentangling predisposed from acquired neural abnormalities. Trends Cognit. Sci. 17 (7), 337-347. https://doi.org/10.1016/j.tics.2013.05.005.
  2. Andersson, J.L.R., Jenkinson, M., Smith, S., 2007. Non-linear registration, aka spatial normalisation. FMRIB Technial Report TR07JA2. Oxford Centre for Functional Magnetic Resonance Imaging of the Brain, Department of Clinical Neurology. Oxford University, Oxford, UK.
  3. Andrews-Hanna, J.R., Reidler, J.S., Sepulcre, J., Poulin, R., Buckner, R.L., 2010. Functional-anatomic fractionation of the brain's default network. Neuron 65 (4), 550-562. https://doi.org/10.1016/j.neuron.2010.02.005.
  4. Bartova, L., Meyer, B.M., Diers, K., Rabl, U., Scharinger, C., Popovic, A., et al., 2015. Reduced default mode network suppression during a working memory task in remitted major depression. J. Psychiatr. Res. 64, 9-18. https://doi.org/10.1016/j. jpsychires.2015.02.025.
  5. Beckmann, C.F., Smith, S.M., 2005. Tensorial extensions of independent component analysis for multisubject FMRI analysis. Neuroimage 25 (1), 294-311. https://doi. org/10.1016/j.neuroimage.2004.10.043.
  6. Birn, R.M., Molloy, E.K., Patriat, R., Parker, T., Meier, T.B., Kirk, G.R., et al., 2013. The effect of scan length on the reliability of resting-state fMRI connectivity estimates. Neuroimage 83, 550-558. https://doi.org/10.1016/j.neuroimage.2013.05.099.
  7. Boubela, R.N., Kalcher, K., Nasel, C., Moser, E., 2014. Scanning fast and slow: current limitations of 3 Tesla functional MRI and future potential. Front. Phys. 2. https://doi. org/10.3389/fphy.2014.00001.
  8. Bozovic, D., Racic, M., Ivkovic, N., 2013. Salivary Cortisol Levels as a Biological Marker of Stress Reaction. Med. Arch. 67, 374. https://doi.org/10.5455/medarh.2013.67.374- 377.
  9. Buckner, R.L., Andrews-Hanna, J.R., Schacter, D.L., 2008. The brain's default network: Anatomy, function, and relevance to disease. Ann. N. Y. Acad. Sci. 1124, 1-38. https://doi.org/10.1196/annals.1440.011.
  10. Caballero-Gaudes, C., Reynolds, R.C., 2017. Methods for cleaning the BOLD fMRI signal. Neuroimage 154, 128-149. https://doi.org/10.1016/j.neuroimage.2016.12.018.
  11. Cole, M.W., Anticevic, A., Repovs, G., Barch, D., 2011. Variable global dysconnectivity and individual differences in schizophrenia. Biol. Psychiatry 70 (1), 43-50. https:// doi.org/10.1016/j.biopsych.2011.02.010.
  12. Cole, M.W., Yarkoni, T., Repovs, G., Anticevic, A., Braver, T.S., 2012. Global connectivity of prefrontal cortex predicts cognitive control and intelligence. J. Neurosci. 32 (26), 8988-8999. https://doi.org/10.1523/JNEUROSCI.0536-12.2012.
  13. Cousijn, H., Rijpkema, M., Qin, S., van Marle, H.J.F., Franke, B., Hermans, E.J., et al., 2010. Acute stress modulates genotype effects on amygdala processing in humans. Proc. Natl. Acad. Sci. Unit. States Am. 107 (21), 9867-9872. https://doi.org/10\. 1073/pnas.1003514107.
  14. Craig, a. D., 2002. How do you feel? Interoception: the sense of the physiological condition of the body. Nat. Rev. Neurosci. 3 (8), 655-666. https://doi.org/10.1038/ nrn894. Critchley, H.D., Wiens, S., Rotshtein, P., € Ohman, A., Dolan, R.J., 2004. Neural systems supporting interoceptive awareness. Nat. Neurosci. 7 (2), 189-195. https://doi.org/ 10.1038/nn1176.
  15. De Kloet, E.R., Jo€ els, M., Holsboer, F., 2005. Stress and the brain: From adaptation to disease. Nat. Rev. Neurosci. 6, 463-475. https://doi.org/10.1038/nrn1683.
  16. Dosenbach, N.U.F., Fair, D.A., Miezin, F.M., Cohen, A.L., Wenger, K.K., Dosenbach, R.A.T., et al., 2007. Distinct brain networks for adaptive and stable task control in humans. Proc. Natl. Acad. Sci. Unit. States Am. 104 (26), 11073-11078. https://doi.org/10.1073/pnas.0704320104.
  17. Etkin, A., Egner, T., Kalisch, R., 2011. Emotional processing in anterior cingulate and medial prefrontal cortex. Trends Cognit. Sci. 15, 85-93. https://doi.org/10.1016/j. tics.2010.11.004.
  18. Etkin, A., Wager, T.D., 2007. Functional neuroimaging of anxiety: a meta-analysis of emotional processing in PTSD, social anxiety disorder, and specific phobia. Am. J. Psychiatry 164 (10), 1476-1488. https://doi.org/10.1176/appi.ajp.2007.07030504.
  19. Finn, E.S., Scheinost, D., Finn, D.M., Shen, X., Papademetris, X., Constable, R.T., 2017. Can brain state be manipulated to emphasize individual differences in functional connectivity? Neuroimage 160, 140-151. https://doi.org/10.1016/j.neuroimage. 2017.03.064.
  20. Friston, K.J., Williams, S., Howard, R., Frackowiak, R.S.J., Turner, R., 1996. Movement- Related effects in fMRI time-series. Magn. Reson. Med. 35 (3), 346-355. https://doi. org/10.1002/mrm.1910350312.
  21. Gignac, G.E., Szodorai, E.T., 2016. Effect size guidelines for individual differences researchers. Pers. Indiv. Differ. 102, 74-78. https://doi.org/10.1016/j.paid.2016.06\. 069. Gonzalez-Castillo, J., Hoy, C.W., Handwerker, D.A., Robinson, M.E., Buchanan, L.C., Saad, Z.S., Bandettini, P.A., 2015. Tracking ongoing cognition in individuals using brief, whole-brain functional connectivity patterns. Proc. Natl. Acad. Sci. Unit. States Am. 112 (28), 8762-8767. https://doi.org/10.1073/pnas.1501242112.
  22. Greve, D.N., Fischl, B., 2009. Accurate and robust brain image alignment using boundary- based registration. Neuroimage 48 (1), 63-72. https://doi.org/10.1016/j. neuroimage.2009.06.060.
  23. Hedge, C., Powell, G., Sumner, P., 2017. The reliability paradox: Why robust cognitive tasks do not produce reliable individual differences. Behav. Res. Methods 1-21. https://doi.org/10.3758/s13428-017-0935-1.
  24. Hellhammer, D.H., Wüst, S., Kudielka, B.M., 2009. Salivary cortisol as a biomarker in stress research. Psychoneuroendocrinology 34 (2), 163-171. https://doi.org/10\. 1016/j.psyneuen.2008.10.026.
  25. Hemphill, J.F., 2003. Interpreting the Magnitudes of Correlation Coefficients. Am. Psychol. 58, 78-79. https://doi.org/10.1037/0003-066X.58.1.78.
  26. Henckens, M. J. a G., van Wingen, G. a, Jo€ els, M., Fern andez, G., 2012. Corticosteroid induced decoupling of the amygdala in men. Cerebr. Cortex 22 (10), 2336-2345. New York, N.Y. : 1991. https://doi.org/10.1093/cercor/bhr313.
  27. Hermans, E.J., Henckens, M.J.A.G., Jo€ els, M., Fern andez, G., 2014. Dynamic adaptation of large-scale brain networks in response to acute stressors. Trends Neurosci. 37 (6), 304-314. https://doi.org/10.1016/j.tins.2014.03.006.
  28. Hermans, E.J., van Marle, H.J.F., Ossewaarde, L., Henckens, M. J. a. G., Qin, S., van Kesteren, M.T.R., et al., 2011. Stress-related noradrenergic activity prompts large- scale neural network reconfiguration. Science 334 (6059), 1151-1153. https://doi. org/10.1126/science.1209603.
  29. Jenkinson, M., Bannister, P., Brady, M., Smith, S., 2002. Improved optimization for the robust and accurate linear registration and motion correction of brain images. Neuroimage 17 (2), 825-841. https://doi.org/10.1016/S1053-8119(02)91132-8.
  30. Jenkinson, M., Smith, S., 2001. A global optimisation method for robust affine registration of brain images. Med. Image Anal. 5 (2), 143-156. https://doi.org/10\. 1016/S1361-8415(01)00036-6.
  31. Jo€ els, M., Baram, T.Z., 2009. The neuro-symphony of stress. Nat. Rev. Neurosci. 10 (6), 459-466. https://doi.org/10.1038/nrn2632.
  32. Kirschbaum, C., Hellhammer, D.H., 1994. Salivary cortisol in psychoneuroendocrine research: recent developments and applications. Psychoneuroendocrinology 19 (4), 313-333. https://doi.org/10.1016/0306-4530(94)90013-2.
  33. Koch, S.B.J., Klumpers, F., Zhang, W., Hashemi, M.M., Kaldewaij, R., van Ast, V.A., et al., 2017. The role of automatic defensive responses in the development of posttraumatic stress symptoms in police recruits: protocol of a prospective study. Eur. J. Psychotraumatol. 8 (1), 1412226. https://doi.org/10.1080/20008198.2017\. 1412226.
  34. Koch, S.B.J., van Zuiden, M., Nawijn, L., Frijling, J.L., Veltman, D.J., Olff, M., 2016. Aberrant resting-state brain activity in posttraumatic stress disorder: A meta-analysis and systematic review. Depress. Anxiety 33 (7), 592-605. https://doi.org/10.1002/ da.22478.
  35. Kudielka, B., Kirschbaum, C., 2005. Sex differences in HPA axis responses to stress: a review. Biol. Psychol. 69, 113-132. https://doi.org/10.1016/j.biopsycho.2004.11\. 009. Luo, Y., Fern andez, G., Hermans, E., Vogel, S., Zhang, Y., Li, H., Klumpers, F., 2018. How acute stress may enhance subsequent memory for threat stimuli outside the focus of attention: DLPFC-amygdala decoupling. Neuroimage 171, 311-322. https://doi.org/ 10.1016/j.neuroimage.2018.01.010.
  36. Maron-Katz, A., Vaisvaser, S., Lin, T., Hendler, T., Shamir, R., 2016. A large-scale perspective on stress-induced alterations in resting-state networks. Sci. Rep. 6 (February), 21503. https://doi.org/10.1038/srep21503.
  37. Marquand, A.F., Haak, K.V., Beckmann, C.F., 2017. Functional corticostriatal connection topographies predict goal-directed behaviour in humans. Nat. Human Behav. 1 (8). https://doi.org/10.1038/s41562-017-0146.
  38. McEwen, B.S., 1998. Stress, adaptation, and disease: allostasis and allostatic load. Ann. N. Y. Acad. Sci. 840 (1), 33-44. https://doi.org/10.1111/j.1749-6632.1998.tb09546.x.
  39. McMenamin, B.W., Pessoa, L., 2015. Discovering networks altered by potential threat ("anxiety") using quadratic discriminant analysis. Neuroimage 116, 1-9. https://doi. org/10.1016/j.neuroimage.2015.05.002.
  40. Menon, V., 2011. Large-scale brain networks and psychopathology: A unifying triple network model. Trends Cognit. Sci. 15 (10), 483-506. https://doi.org/10.1016/j.tics. 2011.08.003.
  41. Miller, R., Stalder, T., Jarczok, M., Almeida, D.M., Badrick, E., Bartels, M., et al., 2016. The CIRCORT database: Reference ranges and seasonal changes in diurnal salivary cortisol derived from a meta-dataset comprised of 15 field studies. Psychoneuroendocrinology 73 (8), 16-23. https://doi.org/10.1016/j.psyneuen. 2016.07.201.
  42. Murphy, K., Birn, R.M., Bandettini, P.A., 2013. Resting-state fMRI confounds and cleanup. Neuroimage 80, 349-359. https://doi.org/10.1016/j.neuroimage.2013.04.001.
  43. Nicholson, A.A., Densmore, M., Frewen, P.A., Th eberge, J., Neufeld, R.W.J., McKinnon, M.C., Lanius, R.A., 2015. The dissociative subtype of posttraumatic stress disorder: unique resting-state functional connectivity of Basolateral and Centromedial Amygdala complexes. Neuropsychopharmacology 40 (10), 2317-2326. https://doi.org/10.1038/npp.2015.79.
  44. Oathes, D.J., Patenaude, B., Schatzberg, A.F., Etkin, A., 2015. Neurobiological signatures of anxiety and depression in resting-state functional magnetic resonance imaging. Biol. Psychiatry 77 (4), 385-393. https://doi.org/10.1016/j.biopsych.2014.08.006.
  45. Parkes, L., Fulcher, B., Yücel, M., Fornito, A., 2018. NeuroImage An evaluation of the ef fi cacy , reliability , and sensitivity of motion correction strategies for resting-state functional MRI. Neuroimage 171, 415-436. July 2017. https://doi.org/10.1016/j. neuroimage.2017.12.073.
  46. Pruim, R.H.R., Mennes, M., van Rooij, D., Llera, A., Buitelaar, J.K., Beckmann, C.F., 2015. ICA-AROMA: A robust ICA-based strategy for removing motion artifacts from fMRI data. Neuroimage 112, 267-277. https://doi.org/10.1016/j.neuroimage.2015.02\. 064. Quaedflieg, C.W.E.M., van de Ven, V., Meyer, T., Siep, N., Merckelbach, H., Smeets, T., 2015. Temporal dynamics of stress-induced alternations of intrinsic amygdala connectivity and neuroendocrine levels. PLoS One 10 (5) e0124141. https://doi.org/ 10.1371/journal.pone.0124141.
  47. Reschke-Hern andez, A.E., Okerstrom, K.L., Bowles Edwards, A., Tranel, D., 2017. Sex and stress: Men and women show different cortisol responses to psychological stress induced by the Trier social stress test and the Iowa singing social stress test. J. Neurosci. Res. 95 (1-2), 106-114. https://doi.org/10.1002/jnr.23851.
  48. Rotge, J.Y., Lemogne, C., Hinfray, S., Huguet, P., Grynszpan, O., Tartour, E., et al., 2015. A meta-analysis of the anterior cingulate contribution to social pain. Soc. Cognit. Affect Neurosci. 10 (1), 19-27. https://doi.org/10.1093/scan/nsu110.
  49. Satterthwaite, T.D., Elliott, M.A., Gerraty, R.T., Ruparel, K., Loughead, J., Calkins, M.E., et al., 2013. An improved framework for confound regression and filtering for control of motion artifact in the preprocessing of resting-state functional connectivity data. Neuroimage 64 (1), 240-256. https://doi.org/10.1016/j.neuroimage.2012.08.052\. Sch€ onbrodt, F.D., Perugini, M., 2013. At what sample size do correlations stabilize? J. Res. Pers. 47 (5), 609-612. https://doi.org/10.1016/j.jrp.2013.05.009.
  50. Schwabe, L., Haddad, L., Schachinger, H., 2008. HPA axis activation by a socially evaluated cold-pressor test. Psychoneuroendocrinology 33 (6), 890-895. https://doi. org/10.1016/j.psyneuen.2008.03.001.
  51. Seeley, W.W., Menon, V., Schatzberg, A.F., Keller, J., Glover, G.H., Kenna, H., et al., 2007. Dissociable intrinsic connectivity networks for salience processing and executive control. J. Neurosci. 27 (9), 2349-2356. https://doi.org/10.1523/JNEUROSCI.5587- 06.2007.
  52. Shenhav, A., Botvinick, M.M., Cohen, J.D., 2013. The expected value of control: An integrative theory of anterior cingulate cortex function. Neuron 79, 217-240. https:// doi.org/10.1016/j.neuron.2013.07.007.
  53. Shirer, W.R., Ryali, S., Rykhlevskaia, E., Menon, V., Greicius, M.D., 2012. Decoding subject-driven cognitive states with whole-brain connectivity patterns. Cerebr. Cortex 22 (1), 158-165. https://doi.org/10.1093/cercor/bhr099.
  54. Smith, S.M., Nichols, T.E., 2009. Threshold-free cluster enhancement: Addressing problems of smoothing, threshold dependence and localisation in cluster inference. Neuroimage 44 (1), 83-98. https://doi.org/10.1016/j.neuroimage.2008.03.061.
  55. Sripada, R.K., King, A.P., Welsh, R.C., Garfinkel, S.N., Wang, X., Sripada, C.S., Liberzon, I., 2012. Neural dysregulation in posttraumatic stress disorder: evidence for disrupted equilibrium between salience and default mode brain networks. Psychosom. Med. 74 (9), 904-911. https://doi.org/10.1097/PSY.0b013e318273bf33.
  56. Vaisvaser, S., Lin, T., Admon, R., Podlipsky, I., Greenman, Y., Stern, N., et al., 2013. Neural traces of stress: cortisol related sustained enhancement of amygdala- hippocampal functional connectivity. Front. Hum. Neurosci. 7, 313. https://doi.org/ 10.3389/fnhum.2013.00313.
  57. Vaisvaser, S., Modai, S., Farberov, L., Lin, T., Sharon, H., Gilam, A., et al., 2016. Neuro- epigenetic indications of acute stress response in humans: The case of microRNA-29c. PLoS One 11 (1), 1-17. https://doi.org/10.1371/journal.pone.0146236.
  58. van Oort, J., Tendolkar, I., Hermans, E.J., Mulders, P.C., Beckmann, C.F., Schene, A.H., et al., 2017. How the brain connects in response to acute stress: A review at the human brain systems level. Neurosci. Biobehav. Rev. 83 (April), 281-297. https:// doi.org/10.1016/j.neubiorev.2017.10.015.
  59. Vogel, S., Klumpers, F., Krugers, H.J., Fang, Z., Oplaat, K.T., Oitzl, M.S., et al., 2015. Blocking the mineralocorticoid receptor in humans prevents the stress-induced enhancement of centromedial amygdala connectivity with the Dorsal Striatum. Neuropsychopharmacology 40 (4), 947-956. https://doi.org/10.1038/npp.2014.
  60. Vul, E., Harris, C., Winkielman, P., Pashler, H., 2009. Puzzlingly High Correlations in fMRI Studies of Emotion, Personality, and Social Cognition1. Perspect. Psychol. Sci. 4 (3), 274-290. https://doi.org/10.1111/j.1745-6924.2009.01125.x.
  61. Watson, D., Clark, L. a., Tellegan, a., 1988. Worksheet 3.1 the positive and negative affect schedule (PANAS; Watson et al., 1988) PANAS questionnaire. J. Pers. Soc. Psychol. 54, 1063-1070. https://doi.org/10.1521/soco\_2012\_1006.
  62. Winkler, A.M., Ridgway, G.R., Webster, M.A., Smith, S.M., Nichols, T.E., 2014. Permutation inference for the general linear model. Neuroimage 92, 381-397. https://doi.org/10.1016/j.neuroimage.2014.01.060.
  63. Young, C.B., Raz, G., Everaerd, D., Beckmann, C.F., Tendolkar, I., Hendler, T., et al., 2016. Dynamic shifts in large-scale brain network balance as a function of arousal. J. Neurosci. 37, 281-290. https://doi.org/10.1523/JNEUROSCI.1759-16.2016.
  64. Zu Eulenburg, P., Caspers, S., Roski, C., Eickhoff, S.B., 2012. Meta-analytical definition and functional connectivity of the human vestibular cortex. Neuroimage 60 (1), 162-169. https://doi.org/10.1016/j.neuroimage.2011.12.032.