Abstract
Emerging evidence indicates that acute exercise improves executive function, but its effects on higher-order executive functioning skills among people with a risk of Alzheimer’s disease are not well understood. This study addressed the effects of acute exercise on the planning dimension of executive function among late middle-age adults who carried Apolipoprotein (APOE)-ɛ4. Exercise volume was kept constant, but exercise intensity and duration were manipulated. Eighteen adults in the age range 55–70 years who carried APOE-ɛ4 were recruited for a laboratory-based study set in a within-subjects, counterbalanced design. There was a reading control condition along with three exercise conditions: Acute cycle exercise at a moderate intensity for 30 min (MI-30); higher intensity exercise of a shorter duration (16 min); and lower intensity exercise of a longer duration (40 min). Exercise volume was set with reference to energy expenditure in MI-30. The Tower of London Test was administered at the end of each condition. Acute aerobic exercise improved cognitive performance in regard to move-related scores and time-related scores, but not violation-related scores, when compared to the control condition. There was no difference in terms of the facilitation effect among the three exercise conditions. The present findings indicate that acute aerobic exercise, regardless of intensity/duration manipulation, facilitates higher-order executive function in late middle-aged APOE-ɛ4 carriers. Practitioners should, accordingly, consider exercise as a suitable intervention for those at risk of Alzheimer’s disease.
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Data Availability
The datasets generated during and/or analysed in this study are available from the corresponding author on reasonable request.
References
Ai, J. Y., Chen, F. T., Hsieh, S. S., Kao, S. C., Chen, A. G., Hung, T. M., & Chang, Y. K. (2021). The effect of acute high-intensity interval training on executive function: A systematic review. International Journal of Environmental Research and Public Health, 18(7), Article 3593. https://doi.org/10.3390/ijerph18073593
American College of Sports Medicine. (2022). ACSM’s Guidelines for Exercise Testing and Prescription (11th ed.). Lippincott Williams and Wilkins. https://www.acsm.org/education-resources/books/guidelines-exercise-testing-prescription.
Basso, J. C., & Suzuki, W. A. (2017). The effects of acute exercise on mood, cognition, neurophysiology, and neurochemical pathways: A review. Brain Plasticity, 2(2), 127–152. https://doi.org/10.3233/BPL-160040
Belloy, M. E., Napolioni, V., & Greicius, M. D. (2019). A quarter century of APOE and Alzheimer’s disease: Progress to date and the path forward. Neuron, 101(5), 820–838. https://doi.org/10.1016/j.neuron.2019.01.056
Ben Ayed, I., Castor-Guyonvarch, N., Amimour, S., Naija, S., Aouichaoui, C., Ben Omor, S., Tabka, Z., & El Massioui, F. (2021). Acute exercise and cognitive function in Alzheimer’s disease. Journal of Alzheimer’s Disease, 82(2), 749–760. https://doi.org/10.3233/jad-201317
Bharani, K. L., Ledreux, A., Gilmore, A., Carroll, S. L., & Granholm, A. C. (2020). Serum pro-BDNF levels correlate with phospho-tau staining in Alzheimer’s disease. Neurobiology of Aging, 87, 49–59. https://doi.org/10.1016/j.neurobiolaging.2019.11.010
Bolat, H., Ünsel-Bolat, G., Özgül, S., Parıltay, E., Tahıllıoğlu, A., Rohde, L. A., Akın, H., & Ercan, E. S. (2022). Investigation of possible associations of the BDNF, SNAP-25 and SYN III genes with the neurocognitive measures: BDNF and SNAP-25 genes might be involved in attention domain, SYN III gene in executive function. Nordic Journal of Psychiatry, 1–6. https://doi.org/10.1080/08039488.2022.2027518
Borg, G. A. (1982). Psychophysical bases of perceived exertion. Medicine & Science in Sports & Exercise, 14(5), 377–381.
Borror, A. (2017). Brain-derived neurotrophic factor mediates cognitive improvements following acute exercise. Medical Hypotheses, 106, 1–5. https://doi.org/10.1016/j.mehy.2017.06.024
Boyne, P., Meyrose, C., Westover, J., Whitesel, D., Hatter, K., Reisman, D. S., Cunningham, D., Carl, D., Jansen, C., Khoury, J. C., Gerson, M., Kissela, B., & Dunning, K. (2019). Exercise intensity affects acute neurotrophic and neurophysiological responses poststroke. Journal of Applied Physiology, 126(2), 431–443. https://doi.org/10.1152/japplphysiol.00594.2018
Chang, Y. K., Chu, I. H., Chen, F. T., & Wang, C. C. (2011a). Dose-response effect of acute resistance exercise on Tower of London in middle-aged adults. Journal of Sport & Exercise Psychology, 33(6), 866–883. https://doi.org/10.1123/jpah.2021-0688
Chang, Y. K., Tsai, C. L., Hung, T. M., So, E. C., Chen, F. T., & Etnier, J. L. (2011b). Effects of acute exercise on executive function: A study with a Tower of London Task. Journal of Sport and Exercise Psychology, 33(6), 847–865. https://doi.org/10.1123/jsep.33.6.847
Chang, Y. K., Ku, P. W., Tomporowski, P. D., Chen, F. T., & Huang, C. C. (2012a). Effects of acute resistance exercise on late-middle-aged adults’ goal planning. Medicine & Science in Sports & Exercise, 44(9), 1773–1779. https://doi.org/10.1249/MSS.0b013e3182574e0b
Chang, Y. K., Labban, J. D., Gapin, J. I., & Etnier, J. L. (2012b). The effects of acute exercise on cognitive performance: A meta-analysis. Brain Research, 1453, 87–101. https://doi.org/10.1016/j.brainres.2012.02.068
Chang, Y. K., Chu, C. H., Wang, C. C., Wang, Y. C., Song, T. F., Tsai, C. L., & Etnier, J. L. (2015). Dose-response relation between exercise duration and cognition. Medicine & Science in Sports & Exercise, 47(1), 159–165. https://doi.org/10.1249/MSS.0000000000000383
Chang, Y. K., Alderman, B. L., Chu, C. H., Wang, C. C., Song, T. F., & Chen, F. T. (2017). Acute exercise has a general facilitative effect on cognitive function: A combined ERP temporal dynamics and BDNF study. Psychophysiology, 54, 289–300. https://doi.org/10.1111/psyp.12784
Chang, Y. K., Erickson, K. I., Stamatakis, E., & Hung, T. M. (2019). How the 2018 US Physical Activity Guidelines are a call to promote and better understand acute physical activity for cognitive function gains. Sports Medicine, 49(11), 1625–1627. https://doi.org/10.1007/s40279-019-01190-x
Chen, F. T., Etnier, J. L., Chan, K. H., Chiu, P. K., Hung, T. M., & Chang, Y. K. (2020). Exercise training interventions on executive function in older adults: A systematic review and meta-analysis. Sports Medicine, 50(8), 1451–1467. https://doi.org/10.1007/s40279-020-01292-x
Crous-Bou, M., Minguillón, C., Gramunt, N., & Molinuevo, J. L. (2017). Alzheimer’s disease prevention: From risk factors to early intervention. Alzheimer’s Research & Therapy, 9(1), 1–9. https://doi.org/10.1186/s13195-017-0297-z
Culbertson, W. C., & Zillmer, E. A. (1998). The construct validity of the Tower of London DX as a measure of the executive functioning of ADHD children. Assessment, 5(3), 215–226. https://doi.org/10.1177/107319119800500302
Culbertson, W. C., & Zillmer, E. A. (2005). Tower of London Drexel University: 2nd Edition (TOLDX-2). Multi-Health Systems Inc. https://storefront.mhs.com/collections/toldx-2nd-ed.
Diamond, A. (2013). Executive functions. Annual Review of Psychology, 64, 135–168. https://doi.org/10.1146/annurev-psych-113011-143750
Dinoff, A., Herrmann, N., Swardfager, W., & Lanctôt, K. L. (2017). The effect of acute exercise on blood concentrations of brain-derived neurotrophic factor in healthy adults: A meta-analysis. European Journal of Neuroscience, 46(1), 1635–1646. https://doi.org/10.1111/ejn.13603
Faul, F., Erdfelder, E., Buchner, A., & Lang, A. G. (2009). Statistical power analyses using G* Power 3.1: Tests for correlation and regression analyses. Behavior Research Methods, 41(4), 1149–1160. https://doi.org/10.3758/BRM.41.4.1149
Ferguson, C. J. (2016). An effect size primer: A guide for clinicians and researchers. In A. E. Kazdin (Ed.), Methodological issues and strategies in clinical research (4th ed., pp. 301–310). American Psychological Association. https://doi.org/10.1037/14805-020
Golding, L. A. (1989). YMCA Fitness Testing and Assessment Manual. Human Kinetics.
Gustavson, D. E., Reynolds, C. A., Hohman, T. J., Jefferson, A. L., Elman, J. A., Panizzon, M. S., Lyons, M. J., Franz, C. E., & Kremen, W. S. (2021). Alzheimer’s disease polygenic scores predict changes in executive function across 12 years in late middle age. Alzheimer’s & Dementia, 17(S3), Article e056045. https://doi.org/10.1002/alz.056045
Hoffmann, C. M., Petrov, M. E., & Lee, R. E. (2021). Aerobic physical activity to improve memory and executive function in sedentary adults without cognitive impairment: A systematic review and meta-analysis. Preventive Medicine Reports, 23, Article 101496. https://doi.org/10.1016/j.pmedr.2021.101496
Hung, T. M., Tsai, C. L., Chen, F. T., Wang, C. C., & Chang, Y. K. (2013). The immediate and sustained effects of acute exercise on planning aspect of executive function. Psychology of Sport and Exercise, 14(5), 728–736. https://doi.org/10.1016/j.psychsport.2013.05.004
Ishihara, T., Drollette, E. S., Ludyga, S., Hillman, C. H., & Kamijo, K. (2021). The effects of acute aerobic exercise on executive function: A systematic review and meta-analysis of individual participant data. Neuroscience and Biobehavioral Reviews, 128, 258–269. https://doi.org/10.1016/j.neubiorev.2021.06.026
Kao, S. C., Cadenas-Sanchez, C., Shigeta, T. T., Walk, A. M., Chang, Y. K., Pontifex, M. B., & Hillman, C. H. (2020a). A systematic review of physical activity and cardiorespiratory fitness on P3b. Psychophysiology, 57(7), Article e13425. https://doi.org/10.1111/psyp.13425
Kao, S. C., Wang, C. H., & Hillman, C. H. (2020b). Acute effects of aerobic exercise on response variability and neuroelectric indices during a serial n-back task. Brain and Cognition, 138, Article 105508. https://doi.org/10.1016/j.bandc.2019.105508
Kao, S. C., Westfall, D. R., Soneson, J., Gurd, B., & Hillman, C. H. (2017). Comparison of the acute effects of high-intensity interval training and continuous aerobic walking on inhibitory control. Psychophysiology, 54(9), 1335–1345. https://doi.org/10.1111/psyp.12889
Kivipelto, M., Mangialasche, F., & Ngandu, T. (2018). Lifestyle interventions to prevent cognitive impairment, dementia and Alzheimer disease. Nature Reviews Neurology, 14(11), 653–666. https://doi.org/10.1038/s41582-018-0070-3
Knaepen, K., Goekint, M., Heyman, E. M., & Meeusen, R. (2010). Neuroplasticity–exercise-induced response of peripheral brain-derived neurotrophic factor: A systematic review of experimental studies in human subjects. Sports Medicine, 40(9), 765–801. https://doi.org/10.2165/11534530-000000000-00000
Kowiański, P., Lietzau, G., Czuba, E., Waśkow, M., Steliga, A., & Moryś, J. (2018). BDNF: A key factor with multipotent impact on brain signaling and synaptic plasticity. Cellular and Molecular Neurobiology, 38(3), 579–593. https://doi.org/10.1007/s10571-017-0510-4
Liou, Y. M., Jwo, J. C., Yao, K. P., Chiang, L. C., & Huang, L. H. (2008). Selection of appropriate Chinese terms to represent intensity and types of physical activity terms for use in the Taiwan version of IPAQ. Journal of Nursing Research, 16(4), 252–263. https://doi.org/10.1097/01.jnr.0000387313.20386.0a
Liu, C. C., Liu, C. C., Kanekiyo, T., Xu, H., & Bu, G. (2013). Apolipoprotein E and Alzheimer disease: Risk, mechanisms and therapy. Nature Reviews Neurology, 9(2), 106–118. https://doi.org/10.1038/nrneurol.2012.263
Liu, S., Yu, Q., Li, Z., Cunha, P. M., Zhang, Y., Kong, Z., Lin, W., Chen, S., & Cai, Y. (2020). Effects of acute and chronic exercises on executive function in children and adolescents: A systemic review and meta-analysis. Frontiers in Psychology, 11, Article 554915. https://doi.org/10.3389/fpsyg.2020.554915
Ludyga, S., Gerber, M., Brand, S., Holsboer-Trachsler, E., & Pühse, U. (2016). Acute effects of moderate aerobic exercise on specific aspects of executive function in different age and fitness groups: A meta-analysis. Psychophysiology, 53(11), 1611–1626. https://doi.org/10.1111/psyp.12736
Mahley, R. W., & Huang, Y. (2012). Apolipoprotein e sets the stage: Response to injury triggers neuropathology. Neuron, 76(5), 871–885. https://doi.org/10.1016/j.neuron.2012.11.020
Mangine, G. T., Kliszczewicz, B. M., Boone, J. B., Williamson-Reisdorph, C. M., & Bechke, E. E. (2019). Pre-anticipatory anxiety and autonomic nervous system response to two unique fitness competition workouts. Sports, 7(9), Article 199. https://doi.org/10.3390/sports7090199
McMorris, T., Hale, B. J., Corbett, J., Robertson, K., & Hodgson, C. I. (2015). Does acute exercise affect the performance of whole-body, psychomotor skills in an inverted-U fashion? A meta-analytic investigation. Physiology & Behavior, 141, 180–189. https://doi.org/10.1016/j.physbeh.2015.01.010
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(1), 49–100. https://doi.org/10.1006/cogp.1999.0734
Neu, S. C., Pa, J., Kukull, W., Beekly, D., Kuzma, A., Gangadharan, P., Wang, L., Romero, K., Arneric, S. P., & Redolfi, A. (2017). Apolipoprotein E genotype and sex risk factors for Alzheimer disease: A meta-analysis. JAMA Neurology, 74(10), 1178–1189. https://doi.org/10.1001/jamaneurol.2017.2188
Nichols, J. B., Malek-Ahmadi, M., Tariot, P. N., Serrano, G. E., Sue, L. I., & Beach, T. G. (2021). Vascular lesions, APOE ε4, and tau pathology in Alzheimer disease. Journal of Neuropathology and Experimental Neurology, 80(3), 240–246. https://doi.org/10.1093/jnen/nlaa160
Pangman, V. C., Sloan, J., & Guse, L. (2000). An examination of psychometric properties of the Mini-Mental State Examination and the Standardized Mini-Mental State Examination: Implications for clinical practice. Applied Nursing Research, 13(4), 209–213. https://doi.org/10.1053/apnr.2000.9231
Physical Activity Guidelines Advisory Committee. (2018). Physical Activity Guidelines Advisory Committee Scientific Report. US Department of Health and Human Services. https://health.gov/sites/default/files/2019-09/PAG_Advisory_Committee_Report.pdf.
Reas, E. T., Laughlin, G. A., Bergstrom, J., Kritz-Silverstein, D., Barrett-Connor, E., & McEvoy, L. K. (2019). Effects of APOE on cognitive aging in community-dwelling older adults. Neuropsychology, 33(3), 406–416. https://doi.org/10.1037/neu0000501
Robinson, J. L., Richardson, H., Xie, S. X., Suh, E., Van Deerlin, V. M., Alfaro, B., Loh, N., Porras-Paniagua, M., Nirschl, J. J., Wolk, D., Lee, V. M., Lee, E. B., & Trojanowski, J. Q. (2021). The development and convergence of co-pathologies in Alzheimer’s disease. Brain, 144(3), 953–962. https://doi.org/10.1093/brain/awaa438
Rouch, I., Padovan, C., Boublay, N., Pongan, E., Laurent, B., Trombert-Paviot, B., Krolak-Salmon, P., & Dorey, J. M. (2020). Association between executive function and the evolution of behavioral disorders in Alzheimer’s disease. International Journal of Geriatric Psychiatry, 35(9), 1043–1050. https://doi.org/10.1002/gps.5327
Satler, C., Guimarães, L., & Tomaz, C. (2017). Planning ability impairments in probable Alzheimer’s disease patients: Evidence from the Tower of London test. Dementia & Neuropsychologia, 11(2), 137–144. https://doi.org/10.1590/1980-57642016dn11-020006
Sen, A., Nelson, T. J., & Alkon, D. L. (2017). ApoE isoforms differentially regulates cleavage and secretion of BDNF. Molecular Brain, 10(1), Article 19. https://doi.org/10.1186/s13041-017-0301-3
Serrano-Pozo, A., Frosch, M. P., Masliah, E., & Hyman, B. T. (2011). Neuropathological alterations in Alzheimer disease. Cold Spring Harbor Perspectives in Medicine, 1(1), Article a006189. https://doi.org/10.1101/cshperspect.a006189
Shepherd, A., Lim, J. K. H., Wong, V. H. Y., Zeleznikow-Johnston, A. M., Churilov, L., Nguyen, C. T. O., Bui, B. V., Hannan, A. J., & Burrows, E. L. (2021). Progressive impairments in executive function in the APP/PS1 model of Alzheimer’s disease as measured by translatable touchscreen testing. Neurobiology of Aging, 108, 58–71. https://doi.org/10.1016/j.neurobiolaging.2021.08.004
Shigeta, T. T., Morris, T. P., Henry, D. H., Kucyi, A., Bex, P., Kramer, A. F., & Hillman, C. H. (2021). Acute exercise effects on inhibitory control and the pupillary response in young adults. International Journal of Psychophysiology, 170, 218–228. https://doi.org/10.1016/j.ijpsycho.2021.08.006
Taren, A. A., Gianaros, P. J., Greco, C. M., Lindsay, E. K., Fairgrieve, A., Brown, K. W., Rosen, R. K., Ferris, J. L., Julson, E., Marsland, A. L., & Creswell, J. D. (2017). Mindfulness meditation training and executive control network resting state functional connectivity: A randomized controlled trial. Psychosomatic Medicine, 79(6), 674–683. https://doi.org/10.1097/psy.0000000000000466
Tiel, C., Sudo, F. K., & Calmon, A. B. (2019). Neuropsychiatric symptoms and executive function impairments in Alzheimer’s disease and vascular dementia: The role of subcortical circuits. Dementia & Neuropsychologia, 13(3), 293–298. https://doi.org/10.1590/1980-57642018dn13-030005
Tsai, C. L., Ukropec, J., Ukropcová, B., & Pai, M. C. (2018). An acute bout of aerobic or strength exercise specifically modifies circulating exerkine levels and neurocognitive functions in elderly individuals with mild cognitive impairment. NeuroImage: Clinical, 17, 272–284. https://doi.org/10.1016/j.nicl.2017.10.028
U.S. Department of Health and Human Services. (2018). Physical Activity Guidelines for Americans, 2nd edition. https://health.gov/sites/default/files/2019-09/Physical_Activity_Guidelines_2nd_edition.pdf.
Vickerstaff, V., Omar, R. Z., & Ambler, G. (2019). Methods to adjust for multiple comparisons in the analysis and sample size calculation of randomised controlled trials with multiple primary outcomes. BMC Medical Research Methodology, 19(129), 1–13. https://doi.org/10.1186/s12874-019-0754-4
Wang, C. C., Alderman, B., Wu, C. H., Chi, L., Chen, S. R., Chu, I. H., & Chang, Y. K. (2019). Effects of acute aerobic and resistance exercise on cognitive function and salivary cortisol responses. Journal of Sport & Exercise Psychology, 41(2), 73–81. https://doi.org/10.1123/jsep.2018-0244
Wechsler, D. (1997). Wechsler Adult Intelligence Scale-III. Administration and scoring manual. The Psychological Corporation.
Weiss, J., Hossain, S., Maldonado, A. I., Shen, B., Beydoun, H. A., Kivimaki, M., Evans, M. K., Zonderman, A. B., & Beydoun, M. A. (2021). Associations between race, APOE genotype, cognition, and mortality among urban middle-aged white and African American adults. Scientific Reports, 11(1), Article 19849. https://doi.org/10.1038/s41598-021-98117-2
Wu, C. H., Karageorghis, C. I., Wang, C. C., Chu, C. H., Kao, S. C., Hung, T. M., & Chang, Y. K. (2019). Effects of acute aerobic and resistance exercise on executive function: An ERP study. Journal of Science and Medicine in Sport, 22(12), 1367–1372. https://doi.org/10.1016/j.jsams.2019.07.009
Xiong, M., Jiang, H., Serrano, J. R., Gonzales, E. R., Wang, C., Gratuze, M., Hoyle, R., Bien-Ly, N., Silverman, A. P., Sullivan, P. M., Watts, R. J., Ulrich, J. D., Zipfel, G. J., & Holtzman, D. M. (2021). APOE immunotherapy reduces cerebral amyloid angiopathy and amyloid plaques while improving cerebrovascular function. Science Translational Medicine, 13(581), Article eabd7522. https://doi.org/10.1126/scitranslmed.abd7522
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The authors would like to acknowledge support from the Ministry of Science and Technology as well as the Ministry of Education in Taiwan.
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This research was supported by a grant to Yu-Kai Chang from the Ministry of Science and Technology in Taiwan (MOST 107-2628-H-003-003-MY3; 110-2410-H-003-142-MY3) and National Taiwan Normal University via the Higher Education Sprout Project, under the auspices of the Ministry of Education in Taiwan.
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YKC, TMH, CCW, and FTC designed the study protocol. CCW, RHL, FTC, and RYF conducted the data collection. YKC, CIK, TMH, CCW, FTC, and RHL were responsible for data management, screening, and analysis. YKC, CIK, TMH, RYF, and FTC wrote the first draft of the paper. YKC, CIK, TMH, RYF, and RHL substantially revised the manuscript.
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Chang, YK., Karageorghis, C.I., Wang, CC. et al. Effects of exercise intensity and duration at a predetermined exercise volume on executive function among Apolipoprotein E (APOE)-ɛ4 carriers. Curr Psychol 42, 22050–22061 (2023). https://doi.org/10.1007/s12144-022-03257-x
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DOI: https://doi.org/10.1007/s12144-022-03257-x