The Effects of Acute Physical Exercise on Memory, Peripheral BDNF, and Cortisol in Young Adults

Kirsten Hötting, Nadine Schickert, Jochen Kaiser, Brigitte Röder, Maren Schmidt-Kassow, Kirsten Hötting, Nadine Schickert, Jochen Kaiser, Brigitte Röder, Maren Schmidt-Kassow

Abstract

In animals, physical activity has been shown to induce functional and structural changes especially in the hippocampus and to improve memory, probably by upregulating the release of neurotrophic factors. In humans, results on the effect of acute exercise on memory are inconsistent so far. Therefore, the aim of the present study was to assess the effects of a single bout of physical exercise on memory consolidation and the underlying neuroendocrinological mechanisms in young adults. Participants encoded a list of German-Polish vocabulary before exercising for 30 minutes with either high intensity or low intensity or before a relaxing phase. Retention of the vocabulary was assessed 20 minutes after the intervention as well as 24 hours later. Serum BDNF and salivary cortisol were measured at baseline, after learning, and after the intervention. The high-intensity exercise group showed an increase in BDNF and cortisol after exercising compared to baseline. Exercise after learning did not enhance the absolute number of recalled words. Participants of the high-intensity exercise group, however, forgot less vocabulary than the relaxing group 24 hours after learning. There was no robust relationship between memory scores and the increase in BDNF and cortisol, respectively, suggesting that further parameters have to be taken into account to explain the effects of exercise on memory in humans.

Figures

Figure 1
Figure 1
Overview of the experimental learning session with the timing of blood and saliva collection, learning, exercise intervention, and vocabulary tests.
Figure 2
Figure 2
Memory for newly learned vocabulary. (a) Mean number of correctly recalled words at day one (60 minutes after learning) and at day two (24 h after learning), separately for the high-intensity group, the low-intensity group, and the relaxing group. (b) Retention after 24 hours, defined as the difference between numbers of correctly recalled words at day one minus day two. Error bars depict ±1 standard error of the mean.
Figure 3
Figure 3
(a) Mean serum BDNF at baseline (t0), after learning (t1), and after exercising/relaxing (t2) separately for the high-intensity exercise group, the low-intensity exercise group, and the relaxing group. (b) Mean changes in BDNF from baseline to the assessment after exercising/relaxing. Positive values indicate an increase in BDNF. Error bars depict ±1 standard error of the mean.
Figure 4
Figure 4
(a) Mean saliva cortisol at baseline (t0), after learning (t1), after exercising/relaxing (t2), and 20 minutes after exercising (t3), separately for the high-intensity exercise group, the low-intensity exercise group, and the relaxing group. (b) Mean changes in cortisol from baseline to the assessment 20 minutes after exercising/relaxing. Positive values indicate an increase in cortisol. Error bars depict ±1 standard error of the mean.

References

    1. Hötting K., Röder B. Beneficial effects of physical exercise on neuroplasticity and cognition. Neuroscience and Biobehavioral Reviews. 2013;37(9):2243–2257. doi: 10.1016/j.neubiorev.2013.04.005.
    1. Smith P. J., Blumenthal J. A., Hoffman B. M., et al. Aerobic exercise and neurocognitive performance: a meta-analytic review of randomized controlled trials. Psychosomatic Medicine. 2010;72(3):239–252. doi: 10.1097/psy.0b013e3181d14633.
    1. Hötting K., Reich B., Holzschneider K., et al. Differential cognitive effects of cycling versus stretching/coordination training in middle-aged adults. Health Psychology. 2012;31(2):145–155. doi: 10.1037/a0025371.
    1. Hötting K., Schauenburg G., Röder B. Long-term effects of physical exercise on verbal learning and memory in middle-aged adults: results of a one-year follow-up study. Brain Sciences. 2012;2(4):332–346. doi: 10.3390/brainsci2030332.
    1. Ruscheweyh R., Willemer C., Krüger K., et al. Physical activity and memory functions: an interventional study. Neurobiology of Aging. 2011;32(7):1304–1319. doi: 10.1016/j.neurobiolaging.2009.08.001.
    1. Stroth S., Hille K., Spitzer M., Reinhardt R. Aerobic endurance exercise benefits memory and affect in young adults. Neuropsychological Rehabilitation. 2009;19(2):223–243. doi: 10.1080/09602010802091183.
    1. Erickson K. I., Voss M. W., Prakash R. S., et al. Exercise training increases size of hippocampus and improves memory. Proceedings of the National Academy of Sciences of the United States of America. 2011;108(7):3017–3022. doi: 10.1073/pnas.1015950108.
    1. Pajonk F.-G., Wobrock T., Gruber O., et al. Hippocampal plasticity in response to exercise in schizophrenia. Archives of General Psychiatry. 2010;67(2):133–143. doi: 10.1001/archgenpsychiatry.2009.193.
    1. Lambourne K., Tomporowski P. The effect of exercise-induced arousal on cognitive task performance: a meta-regression analysis. Brain Research. 2010;1341:12–24. doi: 10.1016/j.brainres.2010.03.091.
    1. Tomporowski P. D. Effects of acute bouts of exercise on cognition. Acta Psychologica. 2003;112(3):297–324. doi: 10.1016/s0001-6918(02)00134-8.
    1. Chang Y. K., Labban J. D., Gapin J. I., Etnier J. L. The effects of acute exercise on cognitive performance: a meta-analysis. Brain Research. 2012;1453:87–101. doi: 10.1016/j.brainres.2012.02.068.
    1. Nader K., Hardt O. A single standard for memory: the case for reconsolidation. Nature Reviews Neuroscience. 2009;10(3):224–234. doi: 10.1038/nrn2590.
    1. Nadel L., Hupbach A., Gomez R., Newman-Smith K. Memory formation, consolidation and transformation. Neuroscience and Biobehavioral Reviews. 2012;36(7):1640–1645. doi: 10.1016/j.neubiorev.2012.03.001.
    1. McGaugh J. L. Memory—a century of consolidation. Science. 2000;287(5451):248–251. doi: 10.1126/science.287.5451.248.
    1. McGaugh J. L. Time-dependent processes in memory storage. Science. 1966;153(3742):1351–1358. doi: 10.1126/science.153.3742.1351.
    1. Labban J. D., Etnier J. L. Effects of acute exercise on long-term memory. Research Quarterly for Exercise and Sport. 2011;82(4):712–721. doi: 10.1080/02701367.2011.10599808.
    1. Schmidt-Kassow M., Kulka A., Gunter T. C., Rothermich K., Kotz S. A. Exercising during learning improves vocabulary acquisition: behavioral and ERP evidence. Neuroscience Letters. 2010;482(1):40–44. doi: 10.1016/j.neulet.2010.06.089.
    1. Schmidt-Kassow M., Deusser M., Thiel C., et al. Physical exercise during encoding improves vocabulary learning in young female adults: a neuroendocrinological study. PLoS ONE. 2013;8(5) doi: 10.1371/journal.pone.0064172.e64172
    1. Schmidt-Kassow M., Zink N., Mock J., et al. Treadmill walking during vocabulary encoding improves verbal long-term memory. Behavioral and Brain Functions. 2014;10, article 24 doi: 10.1186/1744-9081-10-24.
    1. Winter B., Breitenstein C., Mooren F. C., et al. High impact running improves learning. Neurobiology of Learning and Memory. 2007;87(4):597–609. doi: 10.1016/j.nlm.2006.11.003.
    1. McNerney M. W., Radvansky G. A. Mind racing: the influence of exercise on long-term memory consolidation. Memory. 2015;23(8):1140–1151. doi: 10.1080/09658211.2014.962545.
    1. Segal S. K., Cotman C. W., Cahill L. F. Exercise-induced noradrenergic activation enhances memory consolidation in both normal aging and patients with amnestic mild cognitive impairment. Journal of Alzheimer's Disease. 2012;32(4):1011–1018. doi: 10.3233/JAD-2012-121078.
    1. Roig M., Skriver K., Lundbye-Jensen J., Kiens B., Nielsen J. B. A single bout of exercise improves motor memory. PLoS ONE. 2012;7(9) doi: 10.1371/journal.pone.0044594.e44594
    1. Phillips C., Baktir M. A., Srivatsan M., Salehi A. Neuroprotective effects of physical activity on the brain: a closer look at trophic factor signaling. Frontiers in Cellular Neuroscience. 2014;8, article 170 doi: 10.3389/fncel.2014.00170.
    1. Bekinschtein P., Cammarota M., Medina J. H. BDNF and memory processing. Neuropharmacology. 2014;76:677–683. doi: 10.1016/j.neuropharm.2013.04.024.
    1. Vivar C., Potter M. C., van Praag H. All about running: synaptic plasticity, growth factors and adult hippocampal neurogenesis. Current Topics in Behavioral Neurosciences. 2012;15:189–210. doi: 10.1007/7854_2012_220.
    1. Zagrebelsky M., Korte M. Form follows function: BDNF and its involvement in sculpting the function and structure of synapses. Neuropharmacology. 2014;76:628–638. doi: 10.1016/j.neuropharm.2013.05.029.
    1. Griffin É. W., Bechara R. G., Birch A. M., Kelly Á. M. Exercise enhances hippocampal-dependent learning in the rat: evidence for a BDNF-related mechanism. Hippocampus. 2009;19(10):973–980. doi: 10.1002/hipo.20631.
    1. O'Callaghan R. M., Griffin É. W., Kelly Á. M. Long-term treadmill exposure protects against age-related neurodegenerative change in the rat hippocampus. Hippocampus. 2009;19(10):1019–1029. doi: 10.1002/hipo.20591.
    1. Pan W., Banks W. A., Fasold M. B., Bluth J., Kastin A. J. Transport of brain-derived neurotrophic factor across the blood-brain barrier. Neuropharmacology. 1998;37(12):1553–1561. doi: 10.1016/S0028-3908(98)00141-5.
    1. Karege F., Schwald M., Cisse M. Postnatal developmental profile of brain-derived neurotrophic factor in rat brain and platelets. Neuroscience Letters. 2002;328(3):261–264. doi: 10.1016/s0304-3940(02)00529-3.
    1. Lanz T. A., Bove S. E., Pilsmaker C. D., et al. Robust changes in expression of brain-derived neurotrophic factor (BDNF) mRNA and protein across the brain do not translate to detectable changes in BDNF levels in CSF or plasma. Biomarkers. 2012;17(6):524–531. doi: 10.3109/1354750X.2012.694476.
    1. Cho H.-C., Kim J., Kim S., Son Y. H., Lee N., Jung S. H. The concentrations of serum, plasma and platelet BDNF are all increased by treadmill VO2max performance in healthy college men. Neuroscience Letters. 2012;519(1):78–83. doi: 10.1016/j.neulet.2012.05.025.
    1. Ferris L. T., Williams J. S., Shen C.-L. The effect of acute exercise on serum brain-derived neurotrophic factor levels and cognitive function. Medicine and Science in Sports and Exercise. 2007;39(4):728–734. doi: 10.1249/mss.0b013e31802f04c7.
    1. Gold S. M., Schulz K.-H., Hartmann S., et al. Basal serum levels and reactivity of nerve growth factor and brain-derived neurotrophic factor to standardized acute exercise in multiple sclerosis and controls. Journal of Neuroimmunology. 2003;138(1-2):99–105. doi: 10.1016/S0165-5728(03)00121-8.
    1. Heyman E., Gamelin F.-X., Goekint M., et al. Intense exercise increases circulating endocannabinoid and BDNF levels in humans—possible implications for reward and depression. Psychoneuroendocrinology. 2012;37(6):844–851. doi: 10.1016/j.psyneuen.2011.09.017.
    1. Schmidt-Kassow M., Schädle S., Otterbein S., et al. Kinetics of serum brain-derived neurotrophic factor following low-intensity versus high-intensity exercise in men and women. NeuroReport. 2012;23(15):889–893. doi: 10.1097/WNR.0b013e32835946ca.
    1. Tsai C.-L., Chen F.-C., Pan C.-Y., Wang C.-H., Huang T.-H., Chen T.-C. Impact of acute aerobic exercise and cardiorespiratory fitness on visuospatial attention performance and serum BDNF levels. Psychoneuroendocrinology. 2014;41:121–131. doi: 10.1016/j.psyneuen.2013.12.014.
    1. Schmolesky M. T., Webb D. L., Hansen R. A. The effects of aerobic exercise intensity and duration on levels of brain- derived neurotrophic factor in healthy men. Journal of Sports Science and Medicine. 2013;12(3):502–511.
    1. Tang S. W., Chu E., Hui T., Helmeste D., Law C. Influence of exercise on serum brain-derived neurotrophic factor concentrations in healthy human subjects. Neuroscience Letters. 2008;431(1):62–65. doi: 10.1016/j.neulet.2007.11.019.
    1. Mastorakos G., Pavlatou M., Diamanti-Kandarakis E., Chrousos G. P. Exercise and the stress system. Hormones. 2005;4(2):73–89.
    1. Di Luigi L., Baldari C., Gallotta M. C., et al. Salivary steroids at rest and after a training load in young male athletes: relationship with chronological age and pubertal development. International Journal of Sports Medicine. 2006;27(9):709–717. doi: 10.1055/s-2005-872931.
    1. Schwabe L., Joëls M., Roozendaal B., Wolf O. T., Oitzl M. S. Stress effects on memory: an update and integration. Neuroscience and Biobehavioral Reviews. 2012;36(7):1740–1749. doi: 10.1016/j.neubiorev.2011.07.002.
    1. Oldfield R. C. The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia. 1971;9(1):97–113. doi: 10.1016/0028-3932(71)90067-4.
    1. Frey I., Berg A., Grathwohl D., Keul J. Freiburg Questionnaire of physical activity—development, evaluation and application. Soz Praventivmed. 1999;44(2):55–64.
    1. Besson M., Schön D., Moreno S., Santos A., Magne C. Influence of musical expertise and musical training on pitch processing in music and language. Restorative Neurology and Neuroscience. 2007;25(3-4):399–410.
    1. Chobert J., Marie C., François C., Schön D., Besson M. Enhanced passive and active processing of syllables in musician children. Journal of Cognitive Neuroscience. 2011;23(12):3874–3887. doi: 10.1162/jocn_a_00088.
    1. Francois C., Schön D. Musical expertise boosts implicit learning of both musical and linguistic structures. Cerebral Cortex. 2011;21(10):2357–2365. doi: 10.1093/cercor/bhr022.
    1. Bentley D. J., Newell J., Bishop D. Incremental exercise test design and analysis: implications for performance diagnostics in endurance athletes. Sports Medicine. 2007;37(7):575–586. doi: 10.2165/00007256-200737070-00002.
    1. Grant S., Aitchison T., Henderson E., et al. A comparison of the reproducibility and the sensitivity to change of visual analogue scales, Borg scales, and likert scales in normal subjects during submaximal exercise. Chest. 1999;116(5):1208–1217. doi: 10.1378/chest.116.5.1208.
    1. Storer T. W., Davis J. A., Caiozzo V. J. Accurate prediction of Vo2max in cycle ergometry. Medicine & Science in Sports & Exercise. 1990;22(5):704–712. doi: 10.1249/00005768-199010000-00024.
    1. Garber C. E., Blissmer B., Deschenes M. R., et al. Quantity and quality of exercise for developing and maintaining cardiorespiratory, musculoskeletal, and neuromotor fitness in apparently healthy adults: guidance for prescribing exercise. Medicine and Science in Sports and Exercise. 2011;43(7):1334–1359. doi: 10.1249/mss.0b013e318213fefb.
    1. Dressendörfer R. A., Kirschbaum C., Rohde W., Stahl F., Strasburger C. J. Synthesis of a cortisol-biotin conjugate and evaluation as a tracer in an immunoassay for salivary cortisol measurement. Journal of Steroid Biochemistry and Molecular Biology. 1992;43(7):683–692. doi: 10.1016/0960-0760(92)90294-s.
    1. Roche D. J. O., King A. C., Cohoon A. J., Lovallo W. R. Hormonal contraceptive use diminishes salivary cortisol response to psychosocial stress and naltrexone in healthy women. Pharmacology Biochemistry and Behavior. 2013;109:84–90. doi: 10.1016/j.pbb.2013.05.007.
    1. Warren A. M., Gurvich C., Worsley R., Kulkarni J. A systematic review of the impact of oral contraceptives on cognition. Contraception. 2014;90(2):111–116. doi: 10.1016/j.contraception.2014.03.015.
    1. Pluchino N., Cubeddu A., Begliuomini S., et al. Daily variation of brain-derived neurotrophic factor and cortisol in women with normal menstrual cycles, undergoing oral contraception and in postmenopause. Human Reproduction. 2009;24(9):2303–2309. doi: 10.1093/humrep/dep119.
    1. Dudai Y. The neurobiology of consolidations, or, how stable is the engram? Annual Review of Psychology. 2004;55:51–86. doi: 10.1146/annurev.psych.55.090902.142050.
    1. Roig M., Nordbrandt S., Geertsen S. S., Nielsen J. B. The effects of cardiovascular exercise on human memory: a review with meta-analysis. Neuroscience and Biobehavioral Reviews. 2013;37(8):1645–1666. doi: 10.1016/j.neubiorev.2013.06.012.
    1. Cian C., Koulmann N., Barraud P. A., Raphel C., Jimenez C., Melin B. Influence of variations in body hydration on cognitive function: effect of hyperhydration, heat stress, and exercise-induced dehydration. Journal of Psychophysiology. 2000;14(1):29–36. doi: 10.1027//0269-8803.14.1.29.
    1. Covassin T., Weiss L., Powell J., Womack C. Effects of a maximal exercise test on neurocognitive function. British Journal of Sports Medicine. 2007;41(6):370–374. doi: 10.1136/bjsm.2006.032334.
    1. Tomporowski P. D., Ellis N. R., Stephens R. The immediate effects of strenuous exercise on free-recall memory. Ergonomics. 1987;30(1):121–129. doi: 10.1080/00140138708969682.
    1. Rojas Vega S., Strüder H. K., Vera Wahrmann B., Schmidt A., Bloch W., Hollmann W. Acute BDNF and cortisol response to low intensity exercise and following ramp incremental exercise to exhaustion in humans. Brain Research. 2006;1121(1):59–65. doi: 10.1016/j.brainres.2006.08.105.
    1. Seoane A., Tinsley C. J., Brown M. W. Interfering with perirhinal brain-derived neurotrophic factor expression impairs recognition memory in rats. Hippocampus. 2011;21(2):121–126. doi: 10.1002/hipo.20763.
    1. Skriver K., Roig M., Lundbye-Jensen J., et al. Acute exercise improves motor memory: exploring potential biomarkers. Neurobiology of Learning and Memory. 2014;116:46–58. doi: 10.1016/j.nlm.2014.08.004.
    1. Roozendaal B. Stress and memory: opposing effects of glucocorticoids on memory consolidation and memory retrieval. Neurobiology of Learning and Memory. 2002;78(3):578–595. doi: 10.1006/nlme.2002.4080.
    1. Schwabe L., Wolf O. T. Stress and multiple memory systems: from ‘thinking’ to ‘doing’. Trends in cognitive sciences. 2013;17(2):60–68. doi: 10.1016/j.tics.2012.12.001.
    1. Gatti R., De Palo E. F. An update: salivary hormones and physical exercise. Scandinavian Journal of Medicine and Science in Sports. 2011;21(2):157–169. doi: 10.1111/j.1600-0838.2010.01252.x.
    1. Jacks D. E., Sowash J., Anning J., McGloughlin T., Andres F. Effect of exercise at three exercise intensities on salivary cortisol. Journal of Strength and Conditioning Research. 2002;16(2):286–289.
    1. Lupien S. J., McEwen B. S. The acute effects of corticosteroids on cognition: integration of animal and human model studies. Brain Research Reviews. 1997;24(1):1–27. doi: 10.1016/s0165-0173(97)00004-0.
    1. Bos M. G. N., Jacobs van Goethem T. H., Beckers T., Kindt M. Cortisol response mediates the effect of post-reactivation stress exposure on contextualization of emotional memories. Psychoneuroendocrinology. 2014;50:72–84. doi: 10.1016/j.psyneuen.2014.07.030.
    1. Cahill L., Gorski L., Le K. Enhanced human memory consolidation with post-learning stress: interaction with the degree of arousal at encoding. Learning and Memory. 2003;10(4):270–274. doi: 10.1101/lm.62403.
    1. Kirschbaum C., Scherer G., Strasburger C. J. Pituitary and adrenal hormone responses to pharmacological, physical, and psychological stimulation in habitual smokers and nonsmokers. The Clinical Investigator. 1994;72(10):804–810. doi: 10.1007/bf00180552.
    1. Schwabe L., Wolf O. T. Stress impairs the reconsolidation of autobiographical memories. Neurobiology of Learning and Memory. 2010;94(2):153–157. doi: 10.1016/j.nlm.2010.05.001.
    1. Gold P. E., Newman L. A., Scavuzzo C. J., Korol D. L. Modulation of multiple memory systems: from neurotransmitters to metabolic substrates. Hippocampus. 2013;23(11):1053–1065. doi: 10.1002/hipo.22182.
    1. Rooks C. R., Thom N. J., McCully K. K., Dishman R. K. Effects of incremental exercise on cerebral oxygenation measured by near-infrared spectroscopy: a systematic review. Progress in Neurobiology. 2010;92(2):134–150. doi: 10.1016/j.pneurobio.2010.06.002.
    1. Gold P. E. Regulation of memory—from the adrenal medulla to liver to astrocytes to neurons. Brain Research Bulletin. 2014;105:25–35. doi: 10.1016/j.brainresbull.2013.12.012.

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