Effects of stress on functional connectivity during verbal processing

Abstract

Effects of stress on functional connectivity (FC) in specific language processing regions of the brain during verbal fluency tasks were explored. Roles of gender and serotonin transporter gene polymorphisms (5-HTTLPR), associated with stress susceptibility, were also examined to understand their effect. Forty-five healthy volunteers (Mean age: 19.6 ± 1.6 years; 28 females) participated. Functional magnetic resonance imaging was carried out while participants performed letter and category fluency tasks. These tasks were interposed with the Montreal Imaging Stress Test to induce stress or a no-stress control task. Buccal swabs collected were used to genotype for the presence of polymorphisms on the SLC6A4 gene known to contribute to atypical stress responses. Significant variations in strength of FC were noted between several ROIs, including left inferior frontal gyrus and left middle temporal gyrus. Overall, males showed regional increases in FC strength over long and short distances during task under stress. Additionally, variability in effects of stress on task performance was associated with effects of stress on FC. Results suggest that long distance FC may be strengthened to compensate for additional cognitive load of the stressor but that specific short distance functional connections may be strengthened in a gender specific manner. Additionally, FC may serve as a marker for effects of stress on performance. This is the first study exploring stress effects on language tasks with imaging markers. Future studies will need to explore stress susceptible populations and establish the role of FC as a marker, with implications for targeted therapeutic interventions.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

References

  1. Admon, R., Leykin, D., Lubin, G., Engert, V., Andrews, J., Pruessner, J., & Hendler, T. (2013). Stress-induced reduction in hippocampal volume and connectivity with the ventromedial prefrontal cortex are related to maladaptive responses to stressful military service. Human Brain Mapping, 34(11), 2808–2816. https://doi.org/10.1002/hbm.22100.

    Article  PubMed  Google Scholar 

  2. Aldwin, C., Sutton, K., Chiara, G., & Avron, S. (1996). Age differences in stress, coping, and appraisal: Findings from the normative aging study. Journal of Gerontology: Psychological Sciences, 5(4), 79–188. https://doi.org/10.1093/geronb/51B.4.P179.

    Article  Google Scholar 

  3. 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. https://doi.org/10.1162/jocn.2007.19.3.468.

    Article  PubMed  Google Scholar 

  4. Andrews, J., Ali, N., & Pruessner, J. C. (2013). Reflections on the interaction of psychogenic stress systems in humans: The stress coherence/compensation model. Psychoneuroendocrinology, 38(7), 947–961. https://doi.org/10.1016/j.psyneuen.2013.02.010.

    Article  PubMed  Google Scholar 

  5. Andrews, J., & Pruessner, J. C. (2013). The combined propranolol/TSST paradigm—A new method for psychoneuroendocrinology. PLoS One, 8(2). https://doi.org/10.1371/journal.pone.0057567.

  6. Bartha, L., Brenneis, C., Schocke, M., Trinka, E., Koylu, B., Trieb, T., et al. (2003). Medial temporal lobe activation during semantic language processing: fMRI findings in healthy left- and right-handers. Cognitive Brain Research, 17, 339–346.

    Article  PubMed  Google Scholar 

  7. Bebbington, P. E. (1998). Sex and depression. Psychological Medicine, 28(1), 1–8. https://doi.org/10.1017/S0033291797006065.

    Article  CAS  PubMed  Google Scholar 

  8. Bell, E. C., Willson, M. C., Wilman, A. H., Dave, S., & Silverstone, P. H. (2006). Males and females differ in brain activation during cognitive tasks. NeuroImage, 30, 529–538. https://doi.org/10.1016/j.neuroimage.2005.09.049.

    Article  PubMed  Google Scholar 

  9. Bengel, D., Murphy, D. L., Andrews, A. M., Wichems, C. H., Feltner, D., Heils, A., et al. (1998). Altered brain serotonin homeostasis and locomotor insensitivity to 3, 4-methylenedioxymethamphetamine (“Ecstasy”) in serotonin transporter-deficient mice. Molecular Pharmacology, 53(4), 649–655. https://doi.org/10.1124/MOL.53.4.649.

    Article  CAS  PubMed  Google Scholar 

  10. Beversdorf, D. Q. (2019) Neuropsychopharmacological regulation of performance on creativity-related tasks. Current Opinion in Behavioral Sciences 27:55–63

  11. Beversdorf, D. Q., Carpenter, A. L., Alexander, J., Jenkins, N., Tilley, M. R., White, C., et al. (2018). Exploratory pilot study of influence of serotonin transporter genotype on the effect of psychosocial stress on cognitive performance. Cognitive and Behavioral Neurology, 31, 79-85.

  12. Beversdorf, D. Q., White, D. M., Chever, D. C., Hughes, J. D., & Bornstein, R. A. (2002). Central beta-adrenergic modulation of cognitive flexibility. NeuroReport, 13(18), 2505–2507. https://doi.org/10.1097/01.wnr.0000048923.00321.a7.

    Article  CAS  PubMed  Google Scholar 

  13. Bromet, E., Andrade, L. H., Hwang, I., Sampson, N. A., Alonso, J., de Girolamo, G., et al. (2011). Cross-national epidemiology of DSM-IV major depressive episode. BMC Medicine, 9(1), 90. https://doi.org/10.1186/1741-7015-9-90.

    Article  PubMed  PubMed Central  Google Scholar 

  14. Campbell, H. L., Tivarus, M. E., Hillier, A., & Beversdorf, D. Q. (2008). Increased task difficulty results in greater impact of noradrenergic modulation of cognitive flexibility. Pharmacology Biochemistry and Behavior, 88, 222–229. https://doi.org/10.1016/j.pbb.2007.08.003.

    Article  CAS  Google Scholar 

  15. Caspi, A., Hariri, A. R., Holmes, A., Uher, R., & Moffitt, T. (2010). Genetic sensitivity to the environment: The case of the serotonin transporter gene and its implications for studying complex diseases and traits. American Journal of Psychiatry, 167, 509–527.

    Article  PubMed  Google Scholar 

  16. Chamberlain, S. R., & Robbins, T. W. (2013). Noradrenergic modulation of cognition: Therapeutic implications. Journal of Psychopharmacology, 27(8), 694–718. https://doi.org/10.1177/0269881113480988.

    Article  CAS  PubMed  Google Scholar 

  17. Cohen, S., Janicki-deverts, D., & Miller, G. E. (2007). Psychological stress and disease. JAMA, 298(14), 1685–1687.

    Article  CAS  PubMed  Google Scholar 

  18. Costafreda, S. G., Fu, C. H. Y., Lee, L., Everitt, B., Brammer, M. J., & David, A. S. (2006). A systematic review and quantitative appraisal of fMRI studies of verbal fluency: Role of the left inferior frontal Gyrus. Human Brain Mapping, 27, 799–810. https://doi.org/10.1002/hbm.20221.

    Article  PubMed  PubMed Central  Google Scholar 

  19. Dedovic, K., Aguiar, C. D., & Pruessner, J. C. (2009). What stress does to your brain: A review of neuroimaging studies. La Revue Canadienne de Psychiatrie, 54(1), 6–15.

    Google Scholar 

  20. 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(5), 319–325.

    PubMed  PubMed Central  Google Scholar 

  21. Devlin, J. T., Jamison, H. L., Gonnerman, L. M., & Matthews, P. M. (2006). The role of the posterior fusiform gyrus in reading. Journal of Cognitive Neuroscience, 18(6), 911–922. https://doi.org/10.1162/jocn.2006.18.6.911.The.

    Article  PubMed  PubMed Central  Google Scholar 

  22. Dimsdale, J. E. (2008). Psychological stress and cardiovascular disease. Journal of the American College of Cardiology, 51(13), 1237–1246. https://doi.org/10.1016/j.jacc.2007.12.024.

    Article  PubMed  PubMed Central  Google Scholar 

  23. Drabant, E. M., Ramel, W., Edge, M. D., Hyde, L. W., Kuo, J. R., Goldin, P. R., et al. (2012). Neural mechanisms underlying 5-HTTLPR-related sensitivity to acute stress. Am J Psychiatry, AJP in Adv, 1–9.

  24. Dukal, H., Frank, J., Lang, M., Treutlein, J., Gilles, M., Wolf, I. A. C., et al. (2015). New-born females show higher stress- and genotype-independent methylation of SLC6A4 than males. Borderline Personality Disorder and Emotion Dysregulation, 2(8), 4–11. https://doi.org/10.1186/s40479-015-0029-6.

    Article  Google Scholar 

  25. Duman, E. A., & Canli, T. (2015). Influence of life stress, 5-HTTLPR genotype, and SLC6A4 methylation on gene expression and stress response in healthy Caucasian males. Biology of Mood and Anxiety Disorders, 5(2), 1–14. https://doi.org/10.1186/s13587-015-0017-x.

    Article  CAS  Google Scholar 

  26. Easterbrook, J. A. (1959). The effect of emotion on cue utilization and the organization of behavior. Psychological Review, 66(3), 183–201. https://doi.org/10.1037/h0047707.

    Article  CAS  PubMed  Google Scholar 

  27. Epel, E. S., Blackburn, E. H., Lin, J., Dhabhar, F. S., Adler, N. E., Morrow, J. D., & Cawthon, R. M. (2004). Accelerated telomere shortening in response to life stress. PNAS, 101(49), 17312–17315.

    Article  CAS  PubMed  Google Scholar 

  28. Faigel, H. C. (1987). The effect of beta blockade on scholastic aptitude test scores in adolescents. Journal of Adolescent Health Care, 8(3), 304.

    Article  Google Scholar 

  29. Faigel, H. C. (1991). The effect of beta blockade on stress-induced cognitive dysfunction in adolescents. Clinical Pediatrics, 30(7), 441–445.

    Article  CAS  PubMed  Google Scholar 

  30. Fan, Y., Herrera-Melendez, A. L., Pestke, K., Feeser, M., Aust, S., Otte, C., et al. (2014). Early life stress modulates amygdala-prefrontal functional connectivity: Implications for oxytocin effects. Human Brain Mapping, 35(10), 5328–5339. https://doi.org/10.1002/hbm.22553.

    Article  PubMed  PubMed Central  Google Scholar 

  31. Fan, Y., Pestke, K., Feeser, M., Aust, S., Pruessner, J. C., Böker, H., et al. (2015). Amygdala-hippocampal connectivity changes during acute psychosocial stress: Joint effect of early life stress and oxytocin. Neuropsychopharmacology, 40(12), 2736–2744. https://doi.org/10.1038/npp.2015.123.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Fiez, J. (1997). Phonology, semantics and the tole of the left inferior prefrontal cortex. Human Brain Mapping, 5(March), 79–83.

    Article  CAS  PubMed  Google Scholar 

  33. Flinker, A., Korzeniewska, A., Shestyuk, A. Y., Franaszczuk, P. J., & Dronkers, N. F. (2015). Redefining the role of Broca’s area in speech. PNAS, 112(9), 2871–2875. https://doi.org/10.1073/pnas.1414491112.

    Article  CAS  PubMed  Google Scholar 

  34. Franklin, T. B., Saab, B. J., & Mansuy, I. M. (2012). Neural mechanisms of stress resilience and vulnerability. Neuron, 75(5), 747–761. https://doi.org/10.1016/j.neuron.2012.08.016.

    Article  CAS  PubMed  Google Scholar 

  35. Friedman, L., Kenny, J. T., Wise, A. L., Wu, D., Stuve, T. A., Miller, D. A., Jesberger, J. A., & Lewin, J. S. (1998). Brain activation during silent word generation evaluated with functional MRI. Brain and Language, 64, 231–256.

    Article  CAS  PubMed  Google Scholar 

  36. Gauthier, C. T., Duyme, M., Zanca, M., & Capron, C. (2009). Sex and performance level effects on brain activation during a verbal fluency task: A functional magnetic resonance imaging study. CORTEX, 45, 164–176. https://doi.org/10.1016/j.cortex.2007.09.006.

    Article  PubMed  Google Scholar 

  37. Grimm, S., Pestke, K., Feeser, M., Aust, S., Weigand, A., Wang, J., et al. (2014). Early life stress modulates oxytocin effects on limbic system during acute psychosocial stress. Social Cognitive and Affective Neuroscience, 9(11), 1828–1835. https://doi.org/10.1093/scan/nsu020.

    Article  PubMed  PubMed Central  Google Scholar 

  38. Gyawali, S., Subaran, R., Weissman, M. M., Hershkowitz, D., McKenna, M. C., Talari, A., et al. (2010). Association of a polyadenylation polymorphism in the serotonin transporter and panic disorder. Biological Psychiatry, 67(4), 331–338. https://doi.org/10.1016/j.biopsych.2009.10.015.Association.

    Article  CAS  PubMed  Google Scholar 

  39. Hagoort, P. (2014). Nodes and networks in the neural architecture for language: Broca’s region and beyond. Current Opinion in Neurobiology, 28, 136–141. https://doi.org/10.1016/j.conb.2014.07.013.

    Article  CAS  Google Scholar 

  40. Hariri, A. R., Mattay, V. S., Tessitore, A., Kolachana, B. S., Fera, F., Goldman, D., et al. (2002). Serotonin transporter genetic variation and the response of the human amygdala. Science, 297, 400–404.

    Article  CAS  PubMed  Google Scholar 

  41. Hayashi, T., Mizuno-Matsumoto, Y., Okamoto, E., Kato, M., & Murata, T. (2012). An fMRI study of brain processing related to stress states. World Automation Congress, 1–6.

  42. Hecht, P. M., Hudson, M., Connors, S. L., Tilley, M. R., Liu, X., & Beversdorf, D. Q. (2016). Maternal serotonin transporter genotype affects risk for ASD with exposure to prenatal stress. Autism Research, 9, 1151–1160. https://doi.org/10.1002/aur.1629.

    Article  PubMed  Google Scholar 

  43. Hecht, P. M., Will, M. J., Schachtman, T. R., Welby, L. M., & Beversdorf, D. Q. (2014). Beta-adrenergic antagonist effects on a novel cognitive flexibility task in rodents. Behavioural Brain Research, 260, 148–154. https://doi.org/10.1016/j.bbr.2013.11.041.

    Article  CAS  PubMed  Google Scholar 

  44. Heilman, K. M., Nadeau, S. E., & Beversdorf, D. O. (2003). Creative innovation: Possible brain mechanisms. Neurocase, 9(5), 369–379. https://doi.org/10.1076/neur.9.5.369.16553.

    Article  PubMed  Google Scholar 

  45. 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(November), 1151–1154.

    Article  CAS  PubMed  Google Scholar 

  46. Hernaus, D., Collip, D., Lataster, J., Ceccarini, J., Kenis, G., Booij, L., et al. (2013). COMT Val158Met genotype selectively alters prefrontal [18F]Fallypride displacement and subjective feelings of stress in response to a psychosocial stress challenge. PLoS One, 8(6). https://doi.org/10.1371/journal.pone.0065662.

  47. Hillier, A., Alexander, J. K., & Beversdorf, D. Q. (2006). The effect of auditory stressors on cognitive flexibility. Neurocase, 12, 228–231. https://doi.org/10.1080/13554790600878887.

  48. Hirshorn, E. A., & Thompson-schill, S. L. (2006). Role of the left inferior frontal gyrus in covert word retrieval: Neural correlates of switching during verbal fluency. Neuropsychologia, 44, 2547–2557. https://doi.org/10.1016/j.neuropsychologia.2006.03.035.

    Article  PubMed  Google Scholar 

  49. 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.

    Article  PubMed  Google Scholar 

  50. Jenkinson, M., & Smith, S. (2001). A global optimisation method for robust affine registration of brain images. Medical Image Analysis, 5(2), 143–156. https://doi.org/10.1016/S1361-8415(01)00036-6.

    Article  CAS  PubMed  Google Scholar 

  51. Jonides, J., Schumacher, E. H., Smith, E. E., Koeppe, R. A., Awh, E., Reuter-Lorenz, P. A., et al. (1998). The role of parietal cortex in verbal working memory. Journal of Neuroscience.

  52. Just, M. A. (2004). Cortical activation and synchronization during sentence comprehension in high-functioning autism: evidence of underconnectivity. Brain 127(8):1811–1821

  53. Karg, K., Burmeister, M., Shedden, K., & Sen, S. (2011). The serotonin transporter promoter variant (5-HTTLPR), stress, and depression meta-analysis revisited. Archives of General Psychiatry, 68(5), 444–454. https://doi.org/10.1001/archgenpsychiatry.2010.189.

    Article  PubMed  PubMed Central  Google Scholar 

  54. Kelley, B. J., Yeager, K. R., Pepper, T. H., Bornstein, R. A., & Beversdorf, D. Q. (2007). The effect of propranolol on cognitive flexibility and memory in acute cocaine withdrawal. Neurocase, 13, 320–327. https://doi.org/10.1080/13554790701846148.

    Article  PubMed  Google Scholar 

  55. Kemeny, M. E. (2003). The psychobiology of stress. Current Directions in Psychological Science, 12(4), 124–129.

    Article  Google Scholar 

  56. Kenna, G. A., Roder-hanna, N., Leggio, L., Zywiak, W. H., Clifford, J., Edwards, S., et al. (2012). Association of the 5-HTT gene-linked promoter region (5-HTTLPR ) polymorphism with psychiatric disorders: review of psychopathology and pharmacotherapy. Pharmacogenomics and Personalized Medicine, 5, 19–35.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Kessler, R. C. (2003). Epidemiology of women and depression. Journal of Affective Disorders, 74(1), 5–13. https://doi.org/10.1016/S0165-0327(02)00426-3.

    Article  PubMed  Google Scholar 

  58. Kessler, R. C., McGonagle, K. A., Swartz, M., Blazer, D. G., & Nelson, C. B. (1993). Sex and depression in the National Comorbidity Survey I: Lifetime prevalence, chronicity and recurrence. Journal of Affective Disorders, 29(2–3), 85–96. https://doi.org/10.1016/0165-0327(93)90026-G.

    Article  CAS  PubMed  Google Scholar 

  59. Khalili-Mahani, N., Dedovic, K., Engert, V., Pruessner, M., & Pruessner, J. C. (2010). Hippocampal activation during a cognitive task is associated with subsequent neuroendocrine and cognitive responses to psychological stress. Hippocampus, 20(2), 323–334. https://doi.org/10.1002/hipo.20623.

    Article  PubMed  Google Scholar 

  60. Kirschbaum, C., Pirke, K.-M., & Hellhammer, D. (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 

  61. Klein, L. C., & Corwin, E. J. (2002). Seeing the unexpected: How sex differences in stress responses may provide a new perspective on the manifestation of psychiatric disorders. Current Psychiatry Reports, 4, 441–448.

    Article  PubMed  Google Scholar 

  62. Kogler, L., Seidel, E. M., Metzler, H., Thaler, H., Boubela, R. N., Pruessner, J. C., et al. (2017). Impact of self-esteem and sex on stress reactions. Scientific Reports, 7(1), 1–9. https://doi.org/10.1038/s41598-017-17485-w.

    Article  CAS  Google Scholar 

  63. Koob, G. F., Cole, B. J., Swerdlow, N. R., Le Moal, M., & Britton, K. T. (1990). Stress, performance, and arousal: Focus on CRF. NIDA Research Monograph, 97, 163–176.

    CAS  PubMed  Google Scholar 

  64. Laverdure, B., & Boulenger, J.-P. (1991). Medications beta-bloquantes et anxiete Un interest therapeutique certain. L’Encephale, XVII, 481–492.

    Google Scholar 

  65. Lesch, K.-P., Bengel, D., Heils, A., Sabol, S. Z., Greenberg, B. D., Petri, S., et al. (1996). Association of anxiety-related traits with a polymorphism in the serotonin transporter gene regulatory region. Science (New York, N.Y.), 274(5292), 1527–1531 Retrieved from http://www.ncbi.nlm.nih.gov/pubmed/8929413%0Ahttp://www.jstor.org/stable/289226.

    Article  CAS  Google Scholar 

  66. Liston, C., Mcewen, B. S., & Casey, B. J. (2009). Psychosocial stress reversibly disrupts prefrontal processing and attentional control. PNAS, 106(3), 912–917. https://doi.org/10.1073/pnas.0807041106.

    Article  CAS  PubMed  Google Scholar 

  67. Lucassen, P. J., Pruessner, J., Sousa, N., Almeida, O. F. X., Marie, A., Rajkowska, G., et al. (2014). Neuropathology of stress. Acta Neuropathologica, 127, 109–135. https://doi.org/10.1007/s00401-013-1223-5.

    Article  CAS  PubMed  Google Scholar 

  68. Matud, M. P. (2004). Gender differences in stress and coping styles. Personality and Individual Differences, 37, 1401–1415. https://doi.org/10.1016/j.paid.2004.01.010.

    Article  Google Scholar 

  69. McEwen, B. S. (2007). Physiology and neurobiology of stress and adaptation: Central role of theBrain. Physiological Reviews, 87, 873–904. https://doi.org/10.1152/physrev.00041.2006.

    Article  PubMed  Google Scholar 

  70. McEwen, B. S., & Saplosky, R. M. (1995). Stress and cognitive function. Current Opinion in Neurobiology, 5, 205–216.

    Article  CAS  PubMed  Google Scholar 

  71. Mcguffin, P., Alsabban, S., & Uher, R. (2011). The truth about genetic variation in the serotonin transporter gene and response to stress and medication. The British Journal of Psychiatry, 198, 424–427. https://doi.org/10.1192/bjp.bp.110.085225.

    Article  PubMed  Google Scholar 

  72. Murphy, D. L., & Moya, P. R. (2011). Human serotonin transporter gene (SLC6A4) variants: Their contributions to understanding Pharmacogenomic and other functional G x G and G x E differences in health and disease. Current Opinion in Pharmacology, 11(1), 3–10. https://doi.org/10.1016/j.coph.2011.02.008.Human.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  73. Narayanan, A., White, C. A., Saklayen, S., Scaduto, M. J., Carpenter, A. L., Abduljalil, A., & …Beversdorf, D. Q. (2010). Effect of propranolol on functional connectivity in autism spectrum disorder-a pilot study. Brain Imaging and Behavior, 4(2), 189–197. https://doi.org/10.1007/s11682-010-9098-8.

  74. Neubauer, A. C., & Fink, A. (2009). Intelligence and neural efficiency. Neuroscience and Biobehavioral Reviews, 33(7), 1004–1023. https://doi.org/10.1016/j.neubiorev.2009.04.001.

    Article  PubMed  Google Scholar 

  75. Ossewaarde, L., Qin, S., Van Marle, H. J. F., van Wingen, G. A., Fernández, G., & Hermans, E. J. (2011). Stress-induced reduction in reward-related prefrontal cortex function. NeuroImage, 55(1), 345–352. https://doi.org/10.1016/j.neuroimage.2010.11.068.

    Article  PubMed  Google Scholar 

  76. Pruessner, J. C., Dedovic, K., Khalili-mahani, N., Engert, V., Pruessner, M., Buss, C., et al. (2008). Deactivation of the limbic system during acute psychosocial stress: Evidence from positron emission tomography and functional magnetic resonance imaging studies. Biol Psychiatry, 63, 234–240. https://doi.org/10.1016/j.biopsych.2007.04.041.

    Article  PubMed  Google Scholar 

  77. Qin, S., Cousijn, H., Rijpkema, M., Luo, J., Franke, B., Hermans, E. J., & Fernández, G. (2012a). The effect of moderate acute psychological stress on working memory-related neural activity is modulated by a genetic variation in catecholaminergic function in humans. Frontiers in Integrative Neuroscience, 6(May), 1–12. https://doi.org/10.3389/fnint.2012.00016.

    Article  Google Scholar 

  78. Qin, S., Hermans, E. J., van Marle, H. J. F., & Fernandez, G. (2012b). Understanding low reliability of memories for neutral information encoded under stress: Alterations in memory-related activation in the Hippocampus and midbrain. Journal of Neuroscience, 32(12), 4032–4041. https://doi.org/10.1523/JNEUROSCI.3101-11.2012.

    Article  CAS  PubMed  Google Scholar 

  79. Renner, K. H., & Beversdorf, D. Q. (2010). Effects of naturalistic stressors on cognitive flexibility and working memory task performance. Neurocase, 16(4), 293–300. https://doi.org/10.1080/13554790903463601.

    Article  PubMed  Google Scholar 

  80. Risch, N., Herrell, R., Lehner, T., Liang, K.-Y., Eaves, L., Hoh, J., Griem, A., Kovacs, M., Ott, J., & Merikangas, K. R. (2009). Interaction between the serotonin transporter gene (5-HTTLPR), stressful life events, and risk of depression. JAMA, 301(23), 2462–2471.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  81. Rodríguez-Aranda, C., & Martinussen, M. (2006). Age-related differences in performance of phonemic verbal fluency measured by controlled Oral word association task (COWAT): A meta-analytic study. Developmental Neuropsychology, 30(2), 697–717. https://doi.org/10.1207/s15326942dn3002_3.

    Article  PubMed  Google Scholar 

  82. Rudolph, K. D., & Hammen, C. (1999). Age and gender as determinants of stress exposure, generation, and reactions in youngsters: A transactional perspective. Published by: Wiley on behalf of the Society for Research in Child Development. Child Development, 70(3), 660–677.

    Article  CAS  PubMed  Google Scholar 

  83. Sandi, C. (2013). Stress and cognition. WIREs Cogn Science, 4, 245–261. https://doi.org/10.1002/wcs.1222.

    Article  Google Scholar 

  84. Sapolsky, R. M., Krey, L. C., & McEwen, B. S. (1986). The neuroendocrinology of stress and aging: The glucocorticoid Cascade hypothesis. Endocrine Reviews, 7(3), 284–301. https://doi.org/10.1210/edrv-7-3-284.

    Article  CAS  PubMed  Google Scholar 

  85. Schlosser, R., Hutchinson, M., Joseffer, S., Rusinek, H., Saarimaki, A., Stevenson, J., Dewey, S. L., & Brodie, J. D. (1998). Functional magnetic resonance imaging of human brain activity in a verbal fluency task. Journal of Neurology, Neurosurgery, and Psychiatry, 64, 492–498.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  86. Smith, S. M. (2002). Fast robust automated brain extraction. Human Brain Mapping, 17(3), 143–155. https://doi.org/10.1002/hbm.10062.

    Article  PubMed  PubMed Central  Google Scholar 

  87. Strauss, E., Sherman, E. M., & Spreen, O. (1998). A compendium of neuropsychological tests: Administration, norms, and commentary. Oxford: Oxford University Press.

    Google Scholar 

  88. Tivarus, M. E., Hillier, A., Schmalbrock, P., & Beversdorf, D. Q. (2008). Functional connectivity in an fMRI study of semantic and phonological processes and the effect of L -Dopa. Brain and Language, 104(1), 42–50. https://doi.org/10.1016/j.bandl.2007.02.007.

    Article  PubMed  Google Scholar 

  89. Tomasi, D., & Volkow, N. D. (2012). Resting functional connectivity of language networks: Characterization and reproducibility. Molecular Psychiatry, 17(8), 841–854. https://doi.org/10.1038/mp.2011.177.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  90. Uttl, B. (2002). North American adult Reading test: Age norms, reliability, and validity. Journal of Clinical and Experimental Neuropsychology, 24(8), 1123–1137.

    Article  PubMed  Google Scholar 

  91. van der Meer, D., Hartman, C. A., Pruim, R. H. R., Mennes, M., Heslenfeld, D., Oosterlaan, J., et al. (2016). The interaction between 5-HTTLPR and stress exposure influences connectivity of the executive control and default mode brain networks. Brain Imaging and Behavior, 11, 1–11. https://doi.org/10.1007/s11682-016-9633-3.

    Article  Google Scholar 

  92. van Marle, H. J. F., Hermans, E. J., Qin, S., & Fernández, G. (2010). Enhanced resting-state connectivity of amygdala in the immediate aftermath of acute psychological stress. NeuroImage, 53(1), 348–354. https://doi.org/10.1016/j.neuroimage.2010.05.070.

    Article  PubMed  Google Scholar 

  93. Volman, I., Verhagen, L., den Ouden, H. E. M., Fernandez, G., Rijpkema, M., Franke, B., et al. (2013). Reduced serotonin transporter availability decreases prefrontal control of the amygdala. Journal of Neuroscience, 33(21), 8974–8979. https://doi.org/10.1523/JNEUROSCI.5518-12.2013.

    Article  CAS  PubMed  Google Scholar 

  94. Weiss, E. M., Hofer, A., Golaszewski, S., Siedentopf, C., Brinkhoff, C., Kremser, C., Felber, S., & Fleischhacker, W. W. (2004). Brain activation patterns during a verbal fluency test—A functional MRI study in healthy volunteers and patients with schizophrenia. Schizophrenia Research, 70, 287–291. https://doi.org/10.1016/j.schres.2004.01.010.

    Article  PubMed  Google Scholar 

  95. Weissman, M. M., & Klerman, G. L. (1977). Sex differences and the epidemiology of depression. Archives of General Psychiatry, 34(1), 98–111. https://doi.org/10.1001/archpsyc.1977.01770130100011.

    Article  CAS  PubMed  Google Scholar 

  96. Worsley, K. J. (2001). Statistical analysis of activation images. In Functional MRI: An introduction to methods. Oxford University Press (p. Chapter 14).

Download references

Acknowledgements

The authors would like to thank Katarina Devovic and Jens C. Pruessner for their generous donation of the MIST software. We would also like to thank Nick Hopkins, MD, Alanna Bauer, Katie Huddlestonsmith, and Emily Hover for their contributions to the project.

Funding and disclosures

This research is supported by a grant from the University of Missouri Research Board and the University of Missouri Mission Enhancement Fund.

Author information

Affiliations

Authors

Corresponding author

Correspondence to David Q. Beversdorf.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Informed consent statement

All procedures followed were in accordance with the ethical standards of the responsible committee on human experimentation (institutional and national) with the Helsinki Declaration of 1975, and the applicable revisions at the time of the investigation. Informed consent was obtained from all patients for being included in the study.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Nair, N., Hegarty, J.P., Ferguson, B.J. et al. Effects of stress on functional connectivity during verbal processing. Brain Imaging and Behavior 14, 2708–2723 (2020). https://doi.org/10.1007/s11682-019-00221-5

Download citation

Keywords

  • Stress
  • Verbal fluency
  • fMRI
  • Functional connectivity
  • Serotonin transporter
  • Gender