Abstract
We examined the moderating role of sex on the relationship between salivary cortisol and alpha-amylase (sAA) and a diverse battery of cognitive outcomes including measures of working memory capacity, executive functioning, and prospective memory in addition to a more traditional memory measure (episodic memory). The final sample for the analyses included 144 participants (34 men and 110 women). Multiple regressions were performed to test the moderating role of sex on the stress biomarker-cognition relationship. For backward counting performance, higher cortisol levels were related to worse performance in men, but not women. Higher cortisol levels were also related to lower word recall, but only in men. Finally, men, but not women, had higher switching costs in the Trail Making task as levels of sAA rose. The results provide evidence that sex moderates the stress biomarker-cognition relationship in a variety of cognitive outcomes. Although not part of the primary analysis, sAA and cortisol interacted such that increased sAA levels were only negatively related to backward counting performance when cortisol levels were low. The findings are discussed primarily in terms of biological sex differences in the stress response.
Similar content being viewed by others
Notes
We ran the all of the regression analyses controlling for self-reported health and the results were the same. The more parsimonious findings (excluding health as a covariate) are reported.
While immediate and delayed recall may produce different results, we chose to combine these measures due to the high correlation between these episodic memory outcomes (see Zelinski et al. 1993 for a similar result in a sex difference study). Even so, we ran the regression analyses separately for immediate and delayed recall performance and the results were the same as the averaged findings. Therefore, the more parsimonious findings (using the average) are presented.
Due to the added complexity of this task, we scored the number of correct digits versus the more traditional number of correct sequences to avoid restricting the range of scores. We examined the effect using the more traditional scoring and the results were the same.
We did not include age in the primary analyses, but rather controlled for it in the regression analyses. Thus, any fundamental age differences between men and women should be controlled for in the statistical analyses. The goal was not to examine age differences in this paper, but rather sex differences that are independent of age. We are currently preparing a manuscript about age differences in the cortisol/sAA-cognition relationship. In addition, the lower number of men in the study made it difficult to analyze sex by age by stress biomarker interactions.
References
Andreano, J. M., & Cahill, L. (2006). Glucocorticoid release and memory consolidation in men and women. Psychological Science, 17, 466–470.
Andreano, J. M., & Cahill, L. (2009). Sex influences on the neurobiology of learning and memory. Learning and Memory, 16, 248–266.
Andreano, J. M., Arjomandi, H., & Cahill, L. (2008). Menstrual cycle modulation of the relationship between cortisol and long-term memory. Psychoneuroendocrinology, 33, 874–882.
Arnsten, A. F. (2009). Stress signaling pathways that impair prefrontal cortex structure and function. Nature Reviews Neuroscience, 10, 410–422.
Beckner, V. E., Tucker, D. M., Delville, Y., & Mohr, D. C. (2006). Stress facilitates consolidation of verbal memory for a film but does not affect retrieval. Behavioral Neuroscience, 120, 518–526.
Benbow, C. P., & Stanley, J. C. (2000). Sex differences in mathematical ability. Psychology of Education: The School Curriculum, 3, 294.
Berry, D., Blair, C., Willoughby, M., & Granger, D. A. (2012). Salivary alpha-amylase and cortisol in infancy and toddlerhood: direct and indirect relations with executive functioning and academic ability in childhood. Psychoneuroendocrinology, 37, 1700–1711.
Buchanan, T. W., & Tranel, D. (2008). Stress and emotional memory retrieval: effects of sex and cortisol response. Neurobiology of Learning and Memory, 89, 134–141.
Cahill, L., Gorski, L., & Le, K. (2003). Enhanced human memory consolidation with post-learning stress: interaction with the degree of arousal at encoding. Learning and Memory, 10, 270–274.
Callister, R., Suwarno, N. O., & Seals, D. R. (1992). Sympathetic activity is influenced by task difficulty and stress perception during mental challenge in humans. The Journal of Physiology, 454, 373–387.
Cerqueira, J. J., Mailliet, F., Almeida, O. F., Jay, T. M., & Sousa, N. (2007). The prefrontal cortex as a key target of the maladaptive response to stress. The Journal of Neuroscience, 27, 2781–2787.
Cohen, B. H. (2008). Explaining psychological statistics (3rd ed.). New York, NY: Wiley.
Cornelisse, S., van Stegeren, A. H., & Joëls, M. (2011). Implications of psychosocial stress on memory formation in a typical male versus female student sample. Psychoneuroendocrinology, 36, 569–578.
Drag, L. L., & Bieliauskas, L. A. (2010). Contemporary review 2009: cognitive aging. Journal of Psychiarty and Neurology, 23, 75–93.
Dufouil, C., Alperovitch, A., & Tzourio, C. (2003). Influence of education on the relationship between white matter lesions and cognition. Neurology, 60, 831–836.
Earles, J. L., & Kersten, A. W. (1998). Influences of age and perceived activity difficulty on activity recall. The Journals Of Gerontology: Series B: Psychological Sciences And Social Sciences, 53B, P324–P328.
Felmingham, K. L., Tran, T. P., Fong, W. C., & Bryant, R. A. (2012). Sex differences in emotional memory consolidation: the effect of stress-induced salivary alpha-amylase and cortisol. Biological Psychology, 89, 539–544.
Fiocco, A. J., Joober, R., & Lupien, S. J. (2007). Education modulates cortisol reactivity to the Trier Social Stress Test in middle-aged adults. Psychoneuroendocrinology, 32, 1158–1163.
Folstein, M. F., Folstein, S. E., & McHugh, P. R. (1975). Mini-mental state: a practical method for grading the cognitive state of patients for the clinician. Journal of Psychiatric Research, 12, 189–198.
Franz, C. E., O’Brien, R. C., Hauger, R. L., Mendoza, S. P., Panizzon, M. S., Prom-Wormley, E., et al. (2011). Cross-sectional and 35-year longitudinal assessment of salivary cortisol and cognitive functioning: the Vietnam era twin study of aging. Psychoneuroendocrinology, 36, 1040–1052.
Gabriel, K. I., Hong, S. M., Chandra, M., Lonborg, S. D., & Barkley, C. L. (2011). Gender differences in the effects of acute stress on spatial ability. Sex Roles, 64, 81–89.
Granger, D. A., Kivlighan, K. T., Blair, C., El-Sheikh, M., Mize, J., Lisonbee, J. A., et al. (2006). Integrating the measurement of salivary α-amylase into studies of child health, development, and social relationships. Journal of Social and Personal Relationships, 23, 267–290.
Håkansson, K., Rovio, S., Helkala, E. L., Vilska, A. R., Winblad, B., Soininen, H., et al. (2009). Association between mid-life marital status and cognitive function in later life: population based cohort study. BMJ [British Medical Journal], 339, b2462.
Harmon, A. G., Towe-Goodman, N. R., Fortunato, C. K., & Granger, D. A. (2008). Differences in saliva collection location and disparities in baseline and diurnal rhythms of alpha-amylase: a preliminary note of caution. Hormones and Behavior, 54, 592–596.
Hayes, A. F. (2013). Introduction to mediation, moderation, and conditional process analysis: A regression-based approach. New York, NY: The Guilford Press.
Healy, A. F., & Nairne, J. S. (1985). Short-term memory processes in counting. Cognitive Psychology, 17, 417–444.
Herbert, J., Goodyer, I. M., Grossman, A. B., Hastings, M. H., de Kloet, E. R., Lightman, S. L., et al. (2006). Do corticosteroids damage the brain? Journal of Neuroendocrinology, 18, 393–411.
Herlitz, A., Nilsson, L. G., & Bäckman, L. (1997). Gender differences in episodic memory. Memory & Cognition, 25, 801–811.
Hertzog, C., Dixon, R. A., & Hultsch, D. F. (1990). Relationships between metamemory, memory predictions, and memory task performance in adults. Psychology and Aging, 5, 215–227.
Howard, D. V. (1980). Category norms: a comparison of the Battig and Montague (1969) norms with the responses of adults between the ages of 20 and 80. Journal of Gerontology, 35, 225–231.
Hui, G. K., Figueroa, I. R., Poytress, B. S., Roozendaal, B., McGaugh, J. L., & Weinberger, N. M. (2004). Memory enhancement of classical fear conditioning by post-training injections of corticosterone in rats. Neurobiology of Learning and Memory, 81, 67–74.
Jaccard, J., & Turrisi, R. (2003). Interaction Effects in Multiple Regression (2nd ed.). Sage University Papers Series on Quantitative Applications in the Social Sciences, 07-072. Thousand Oaks, CA: Sage.
Joëls, M., Pu, Z., Wiegert, O., Oitzl, M. S., & Krugers, H. J. (2006). Learning under stress: how does it work? Trends in Cognitive Science, 10, 152–158.
Johnson, H. J., Barnard-Brak, L., Saxon, T. F., & Johnson, M. K. (2012). An experimental study of the effects of stereotype threat and stereotype lift on men and women’s performance in mathematics. The Journal of Experimental Education, 80, 137–149.
Keller, P. S., El-Sheikh, M., Granger, D. A., & Buckhalt, J. A. (2012). Interactions between salivary cortisol and alpha-amylase as predictors of children’s cognitive functioning and academic performance. Physiology & Behavior, 105, 987–995.
Kemeny, M. E. (2003). The psychobiology of stress. Current Directions in Psychological Science, 12, 124–129.
Kirschbaum, C., Wolf, O. T., May, M., & Wippich, W. (1996). Stress- and treatment-induced elevations of cortisol levels associated with impaired declarative memory in healthy adults. Life Sciences, 58, 1475–1483.
Kubzansky, L. D., Mendes, W. B., Appleton, A. A., Block, J., & Adler, G. K. (2012). A heartfelt response: oxytocin effects on response to social stress in men and women. Biological Psychology, 90, 1–9.
Kuhlmann, S., & Wolf, O. T. (2005). Cortisol and memory retrieval in women: influence of menstrual cycle and oral contraceptives. Psychopharmacology, 183, 65–71.
Kuhlmann, S., Piel, M., & Wolf, O. T. (2005). Impaired memory retrieval after psychosocial stress in healthy young men. The Journal of Neuroscience, 25, 2977–2982.
Lewin, C., Wolgers, G., & Herlitz, A. (2001). Sex differences favoring women in verbal but not in visuospatial episodic memory. Neuropsychology, 15, 165–173.
Lupien, S., Lecours, A. R., Lussier, I., & Schwartz, G. (1994). Basal cortisol levels and cognitive deficits in human aging. The Journal of Neuroscience, 14, 2893–2903.
Lupien, S. J., de Leon, M., De Santi, S., Convit, A., Tarshish, C., Nair, N. P. V., et al. (1998). Cortisol levels during human aging predict hippocampal atrophy and memory deficits. Nature Neuroscience, 1, 69–73.
Lupien, S. J., Wilkinson, C. W., Briere, S., Menard, C., Ng King Kin, N. M. K., & Nair, N. P. V. (2002). The modulatory effects of corticosteroids on cognition: studies in young human populations. Psychoneuroendocrinology, 27, 401–416.
Lupien, S. J., McEwen, B. S., Gunnar, M. R., & Heim, C. (2009). Effects of stress throughout the lifespan on the brain, behaviour and cognition. Nature Reviews Neuroscience, 10, 434–445.
McEwen, B. S. (1999). Stress and the aging hippocampus. Frontiers in Neuroendocrinology, 20, 49–70.
McEwen, B. S. (2002). Sex, stress and the hippocampus: allostasis, allostatic load and the aging process. Neurobiology of Aging, 23, 921–939.
Meeks, J. T., & Marsh, R. L. (2010). Implementation intentions about nonfocal event-based prospective memory tasks. Psychological Research, 74, 82–89.
Miyake, A., Friedman, N. P., Emerson, M. J., Witzki, A. H., Howerter, A., & Wager, T. D. (2000). The unity and diversity of executive functions and their contributions to complex “frontal lobe” tasks: a latent variable analysis. Cognitive Psychology, 41, 49–100.
Nater, U. M., & Rohleder, N. (2009). Salivary alpha-amylase as a non-invasive biomarker for the sympathetic nervous system: current state of research. Psychoneuroendocrinology, 34, 486–496.
Nater, U. M., Rohleder, N., Gaab, J., Berger, S., Jud, A., Kirschbaum, C., et al. (2005). Human salivary alpha-amylase reactivity in a psychosocial stress paradigm. International Journal of Psychophysiology, 55, 333–342.
Nater, U. M., Rohleder, N., Schlotz, W., Ehlert, U., & Kirschbaum, C. (2007). Determinants of the diurnal course of salivary alpha-amylase. Psychoneuroendocrinology, 32, 392–401.
Nielsen, S. E., Segal, S. K., Worden, I. V., Yim, I. S., & Cahill, L. (2013). Hormonal contraception use alters stress responses and emotional memory. Biological Psychology, 92, 257–266.
O’Donnell, K., Kammerer, M., O’Reilly, R., Taylor, A., & Glover, V. (2009). Salivary α-amylase stability, diurnal profile and lack of response to the cold hand test in young women. Stress: The International Journal on the Biology of Stress, 12, 549–554.
Pearman, A. (2009). Basic cognition in adulthood: combined effects of sex and personality. Personality and Individual Differences, 47, 357–362.
Qin, S., Hermans, E. J., van Marle, H. J. F., Luo, J., & Fernández, G. (2009). Acute psychological stress reduces working memory-related activity in the dorsolateral prefrontal cortex. Biological Psychiatry, 66, 25–32.
Reitan, R. M., & Wolfson, D. (1985). The Halstead–Reitan neuropsychological test battery. Tucson, AZ: Neuropsychological Press.
Rohleder, N., Nater, U. M., Wolf, J. M., Ehlert, U., & Kirschbaum, C. (2004). Psychosocial stress‐induced activation of salivary alpha‐amylase: an indicator of sympathetic activity? Annals of the New York Academy of Sciences, 1032, 258–263.
Roozendaal, B., Okuda, S., de Quervain, D. J.-F., & McGaugh, J. L. (2006). Glucocorticoids interact with emotion-induced noradrenergic activation in influencing different memory functions. Neuroscience, 138, 901–910.
Rosnick, C. B., Rawson, K. S., Butters, M. A., & Lenze, E. J. (2013). Association of cortisol with neuropsychological assessment in older adults with generalized anxiety disorder. Aging & Mental Health. doi:10.1080/13607863.2012.761673. Advanced online publication.
Sanchez-Cubillo, I., Perianez, J. A., Adrover-Roig, D., Rodriguez-Sanchez, J. M., Rios-Lago, M., Tirapu, J., et al. (2009). Construct validity of the Trail Making test: role of task-switching, working memory, inhibition/interference control, and visuomotor abilities. Journal of the International Neuropsychological Society, 15, 438.
Sapolsky, R. M., Romero, L. M., & Munck, A. U. (2000). How do glucocorticoids influence stress responses? Integrating permissive, suppressive, stimulatory, and preparative actions. Endocrine Reviews, 21, 55–89.
Saxbe, D. E., Repetti, R. L., & Nishina, A. (2008). Marital satisfaction, recovery from work, and diurnal cortisol among men and women. Health Psychology, 27, 15.
Schmeichel, B. J. (2007). Attention control, memory updating, and emotion regulation temporarily reduce the capacity for executive control. Journal of Experimental Psychology: General, 136, 241–255.
Schoofs, D., & Wolf, O. T. (2009). Stress and memory retrieval in women: no strong impairing effect during the luteal phase. Behavioral Neuroscience, 123, 547–554.
Schoofs, D., Preuß, D., & Wolf, O. T. (2008). Psychosocial stress induces working memory impairments in an n-back paradigm. Psychoneuroendocrinology, 33, 643–653.
Schwabe, L., Römer, S., Richter, S., Dockendorf, S., Bilak, B., & Schächinger, H. (2009). Stress effects on declarative memory retrieval are blocked by a β-adrenoceptor antagonist in humans. Psychoneuroendocrinology, 34, 446–454.
Searls, D. T. (1966). An estimator for a population mean which reduces the effect of large true observations. Journal of the American Statistical Association, 61, 1200–1204.
Seeman, T. E., McEwen, B. S., Singer, B. H., Albert, M. S., & Rowe, J. W. (1997). Increase in urinary cortisol excretion and memory declines: MacArthur studies of successful aging. The Journal of Clinical Endocrinology and Metabolism, 82, 2458–2465.
Smeets, T., Otgaar, H., Candel, I., & Wolf, O. T. (2008). True or false? Memory is differentially affected by stress-induced cortisol elevations and sympathetic activity at consolidation and retrieval. Psychoneuroendocrinology, 33, 1378–1386.
Tagler, M. J. (2012). Choking under the pressure of a positive stereotype: gender identification and self-consciousness moderate men’s math test performance. The Journal of social psychology, 152(4), 401–416.
Taylor, S. E., Klein, L. C., Lewis, B. P., Gruenewald, T. L., Gurung, R. A. R., & Updegraff, J. A. (2000). Biobehavioral responses to stress in females: tend-and-befriend, not fight-or- flight. Psychological Review, 107, 411–429.
Unsworth, N., Heitz, R. P., Schrock, J. C., & Engle, R. W. (2005). An automated version of the operation span task. Behavior Research Methods, 37, 498–505.
van Exel, E., Gussekloo, J., de Craen, A. J. M., Bootsma-van der Wiel, A., Houx, P., Knook, D. L., et al. (2001). Cognitive function in the oldest old: women perform better than men. Journal of Neurology, Neurosurgery, and Psychiatry, 71, 29–32.
van Hooren, S. A. H., Valentijn, A. M., Bosma, H., Ponds, R. W. H. M., van Boxtel, M. P. J., & Jolles, J. (2007). Cognitive functioning in healthy older adults aged 64–81: a cohort study into the effects of age, sex, and education. Aging, Neuropsychology, and Cognition, 14, 40–54.
Wang, J., Korczykowski, M., Rao, H., Fan, Y., Pluta, J., Gur, R., et al. (2007). Gender difference in neural response to psychological stress. Social Cognitive and Affective Neuroscience, 2, 227–239.
Weiss, E. M., Kemmler, G., Deisenhammer, E. A., Fleischhacker, W. W., & Delazer, M. (2003). Sex differences in cognitive functions. Personality and Individual Differences, 35, 863–875.
Weiss, E. M., Ragland, J. D., Brensinger, C. M., Bilker, W. B., Deisenhammer, E. A., & Delazer, M. (2006). Sex differences in clustering and switching in verbal fluency tasks. Journal of the International Neuropsychological Society, 12, 502–509.
Wilcox, R. R. (2010). Fundamentals of modern statistical methods: Substantially improving power and accuracy. New York, NY: Springer.
Wingenfeld, K., Schulz, M., Damkroeger, A., Philippsen, C., Rose, M., & Driessen, M. (2010). The diurnal course of salivary alpha-amylase in nurses: an investigation of potential confounders and associations with stress. Biological Psychology, 85, 179–181.
Wolf, O. T. (2012). Immediate recall influences the effects of pre-encoding stress on emotional episodic long-term memory consolidation in healthy young men. Stress, 15, 272–280.
Wolf, O. T., Kudielka, B. M., Hellhammer, D. H., Hellhammer, J., & Kirschbaum, C. (1998). Opposing effects of DHEA replacement in elderly subjects on declarative memory and attention after exposure to a laboratory stressor. Psychoneuroendocrinology, 23, 617–629.
Wolf, O. T., Schommer, N. C., Hellhammer, D. H., McEwen, B. S., & Kirschbaum, C. (2001). The relationship between stress induced cortisol levels and memory differs between men and women. Psychoneuroendocrinology, 26, 711–720.
Young, L. J., Muns, S., Wang, Z., & Insel, T. R. (1997). Changes in oxytocin receptor mRNA in rat brain during pregnancy and the effects of estrogen and interleukin-6. Journal of Neuroendocrinology, 9, 859–865.
Zelinski, E. M., Gilewski, M. J., & Schaie, K. W. (1993). Individual differences in cross-sectional and 3-year longitudinal memory performance across the adult life span. Psychology and Aging, 8, 176.
Acknowledgments
This work was supported by the Washington University Institute of Clinical and Translational Sciences Clinical Research Training Center Postdoctoral Program (UL1 TR000448 to C.B.R.) and two internal grants from Southern Illinois University of Edwardsville: 1) Graduate School Seed Grant for Transitional and Exploratory Projects (C.B.R.); and 2) Graduate School New Directions Grant (J.T.M & C.B.R). We would like to thank Vicki Rose and Cheryl Brunsman for their assistance in recruiting the middle-aged and older adult samples. We also would like to thank all of the undergraduate students who assisted with the project.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Meeks, J.T., Rosnick, C.B., Blackhurst, J. et al. Does Sex Matter? The Moderating Role of Sex on the Relationship Between Stress Biomarkers and Cognition. Curr Psychol 33, 199–218 (2014). https://doi.org/10.1007/s12144-014-9206-9
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12144-014-9206-9