Effect of the Level of Physical Activity on Prefrontal Cortex Hemodynamics in Older Adults During Single- and Dual-Task Walking

in Journal of Aging and Physical Activity

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Charles GermainCIAMS, Université Paris-Saclay, Orsay, France
CIAMS, Université d’Orleans, Orleans, France

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Alexandra PerrotCIAMS, Université Paris-Saclay, Orsay, France
CIAMS, Université d’Orleans, Orleans, France

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Christophe TomasinoDepartment of Neurology, Regional Hospital of Orleans, Orleans, France

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Julien BonnalDepartment of Neurology, Regional Hospital of Orleans, Orleans, France

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Canan OzsancakDepartment of Neurology, Regional Hospital of Orleans, Orleans, France

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Pascal AuzouDepartment of Neurology, Regional Hospital of Orleans, Orleans, France

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Fabrice PrieurCIAMS, Université Paris-Saclay, Orsay, France
CIAMS, Université d’Orleans, Orleans, France

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The present study aimed to examine the impact of the level of physical activity on prefrontal cortex activation in older adults during single- and dual-task walking. Thirty physically inactive and 36 active older adults (60–85 years old) performed six 2-min tasks on a treadmill: two static cognitive tasks, two single-task walking tests, and two dual-task walking tests. Hemodynamics at the level of the prefrontal cortex were measured continuously using functional near-infrared spectroscopy to evaluate cortical activation. The perceived difficulty of the task, cognitive performance, and gait parameters were also measured. During the walking tasks, the level of prefrontal cortex activation, the perceived difficulty of the task, cognitive performance, and motor parameters were not significantly different between active and inactive older adults. This unchanged activation with physical activity was likely the consequence of a similar motor and cognitive load and cardiorespiratory fitness in both active and inactive older adults.

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  • Abou-Dest, A., Albinet, C.T., Boucard, G., & Audiffren, M. (2012). Swimming as a positive moderator of cognitive aging: A cross-sectional study with a multitask approach. Journal of Aging Research, 2012, 112. https://doi.org/10.1155/2012/273185

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Agbangla, N., Audiffren, M., Pylouster, J., & Albinet, C. (2019). Working memory, cognitive load and cardiorespiratory fitness: Testing the CRUNCH model with near-infrared spectroscopy. Brain Sciences, 9(2), 38. https://doi.org/10.3390/brainsci9020038

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Agbangla, N.F., Maillot, P., & Vitiello, D. (2021). Mini-review of studies testing the cardiorespiratory hypothesis with Near-Infrared Spectroscopy (NIRS): Overview and perspectives. Frontiers in Neuroscience, 15, 699948. https://doi.org/10.3389/fnins.2021.699948

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Albinet, C.T., Mandrick, K., Bernard, P.L., Perrey, S., & Blain, H. (2014). Improved cerebral oxygenation response and executive performance as a function of cardiorespiratory fitness in older women: A fNIRS study. Frontiers in Aging Neuroscience, 6, 273185. https://doi.org/10.3389/fnagi.2014.00272

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Baddeley, A. (1996). Exploring the central executive. The Quarterly Journal of Experimental Psychology Section A, 49(1), 528. https://doi.org/10.1080/713755608

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Borg, G. (1998). Borg’s perceived exertion and pain scales (p. viii, 104). Human Kinetics.

  • Boucard, G.K., Albinet, C.T., Bugaiska, A., Bouquet, C.A., Clarys, D., & Audiffren, M. (2012). Impact of physical activity on executive functions in aging: A selective effect on inhibition among old adults. Journal of Sport and Exercise Psychology, 34(6), 808827. https://doi.org/10.1123/jsep.34.6.808

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Brigadoi, S., Ceccherini, L., Cutini, S., Scarpa, F., Scatturin, P., Selb, J., Gagnon, L., Boas, D.A., & Cooper, R.J. (2014). Motion artifacts in functional near-infrared spectroscopy: A comparison of motion correction techniques applied to real cognitive data. NeuroImage, 85, 181191. https://doi.org/10.1016/j.neuroimage.2013.04.082

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Caspersen, C.J., Powell, K.E., & Christenson, G.M. (1985). Physical activity, exercise, and physical fitness: Definitions and distinctions for health-related research. Public Health Reports, 100(2), 126.

    • Search Google Scholar
    • Export Citation
  • Ciprandi, D., Bertozzi, F., Zago, M., Ferreira, C.L.P., Boari, G., Sforza, C., & Galvani, C. (2017). Study of the association between gait variability and physical activity. European Review of Aging and Physical Activity, 14(1), 19. https://doi.org/10.1186/s11556-017-0188-0

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Clark, D.J., Christou, E.A., Ring, S.A., Williamson, J.B., & Doty, L. (2014). Enhanced somatosensory feedback reduces prefrontal cortical activity during walking in older adults. The Journals of Gerontology, Series A: Biological Sciences and Medical Sciences, 69(11), 14221428. https://doi.org/10.1093/gerona/glu125

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Colcombe, S.J., Erickson, K.I., Raz, N., Webb, A.G., Cohen, N.J., McAuley, E., & Kramer, A.F. (2003). Aerobic fitness reduces brain tissue loss in aging humans. The Journals of Gerontology, Series A: Biological Sciences and Medical Sciences, 58(2), M176M180. https://doi.org/10.1093/gerona/58.2.M176

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Delignières, D. Famose, J.-P., & Genty, J.G. (1994). Validation d’une échelle de catégories pour la perception de la difficulté. Staps, 13, 7788.

    • Search Google Scholar
    • Export Citation
  • Domingos, C., Pêgo, J.M., & Santos, N.C. (2021). Effects of physical activity on brain function and structure in older adults: A systematic review. Behavioural Brain Research, 402, 113061. https://doi.org/10.1016/j.bbr.2020.113061

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Dupuy, O., Gauthier, C.J., Fraser, S.A., Desjardins-Crèpeau, L., Desjardins, M., Mekary, S., Lesage, F., Hoge, R.D., Pouliot, P., & Bherer, L. (2015). Higher levels of cardiovascular fitness are associated with better executive function and prefrontal oxygenation in younger and older women. Frontiers in Human Neuroscience, 9, 66. https://doi.org/10.3389/fnhum.2015.00066

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Egerton, T., Paterson, K., & Helbostad, J.L. (2017). The association between gait characteristics and ambulatory physical activity in older people: A cross-sectional and longitudinal observational study using generation 100 data. Journal of Aging and Physical Activity, 25(1), 1019. https://doi.org/10.1123/japa.2015-0252

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Ekkekakis, P. (2009). Illuminating the black box: Investigating prefrontal cortical hemodynamics during exercise with near-infrared spectroscopy. Journal of Sport and Exercise Psychology, 31(4), 505553. https://doi.org/10.1123/jsep.31.4.505

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Hamacher, D., Herold, F., Wiegel, P., Hamacher, D., & Schega, L. (2015). Brain activity during walking: A systematic review. Neuroscience & Biobehavioral Reviews, 57, 310327. https://doi.org/10.1016/j.neubiorev.2015.08.002

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Harada, T., Miyai, I., Suzuki, M., & Kubota, K. (2009). Gait capacity affects cortical activation patterns related to speed control in the elderly. Experimental Brain Research, 193(3), 445454. https://doi.org/10.1007/s00221-008-1643-y

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Hausdorff, J.M. (2005). Gait variability: Methods, modeling and meaning. Journal of NeuroEngineering and Rehabilitation, 2, 662. https://doi.org/10.1186/1743-0003-2-19

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Hawkins, K.A., Fox, E.J., Daly, J.J., Rose, D.K., Christou, E.A., McGuirk, T.E., Otzel, D.M., Butera, K.A., Chatterjee, S.A., & Clark, D.J. (2018). Prefrontal over-activation during walking in people with mobility deficits: Interpretation and functional implications. Human Movement Science, 59, 4655. https://doi.org/10.1016/j.humov.2018.03.010

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Herold, F., Aye, N., Hamacher, D., & Schega, L. (2019). Towards the neuromotor control processes of steady-state and speed-matched treadmill and overground walking. Brain Topography, 32(3), 472476. https://doi.org/10.1007/s10548-019-00699-8

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Holtzer, R., Epstein, N., Mahoney, J.R., Izzetoglu, M., & Blumen, H.M. (2014). Neuroimaging of mobility in aging: A targeted review. The Journals of Gerontology, Series A: Biological Sciences and Medical Sciences, 69(11), 13751388. https://doi.org/10.1093/gerona/glu052

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Holtzer, R., Mahoney, J.R., Izzetoglu, M., Izzetoglu, K., Onaral, B., & Verghese, J. (2011). FNIRS study of walking and walking while talking in young and old individuals. The Journals of Gerontology, Series A: Biological Sciences and Medical Sciences, 66A(8), 879887. https://doi.org/10.1093/gerona/glr068

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Holtzer, R., Mahoney, J.R., Izzetoglu, M., Wang, C., England, S., & Verghese, J. (2015). Online fronto-cortical control of simple and attention-demanding locomotion in humans. NeuroImage, 112, 152159. https://doi.org/10.1016/j.neuroimage.2015.03.002

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Hoshi, Y., Kobayashi, N., & Tamura, M. (2001). Interpretation of near-infrared spectroscopy signals: A study with a newly developed perfused rat brain model. Journal of Applied Physiology, 90(5), 16571662. https://doi.org/10.1152/jappl.2001.90.5.1657

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Huppert, T.J., Diamond, S.G., Franceschini, M.A., & Boas, D.A. (2009). HomER: A review of time-series analysis methods for near-infrared spectroscopy of the brain. Applied Optics, 48(10), D280. https://doi.org/10.1364/AO.48.00D280

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Klem, G.H., Lüders, H.O., Jasper, H.H., & Elger, C. (1999). The ten-twenty electrode system of the International Federation. The international federation of clinical neurophysiology. Electroencephalography and Clinical NeurophysiologySupplement, 52, 36.

    • Search Google Scholar
    • Export Citation
  • Kriska, A.M., & Caspersen, C.J. (1997). Introduction to a collection of physical activity questionnaires. Medicine & Science in Sports & Exercise, 29(6), 59. https://doi.org/10.1097/00005768-199706001-00003

    • Crossref
    • Search Google Scholar
    • Export Citation
  • la Fougère, C., Zwergal, A., Rominger, A., Förster, S., Fesl, G., Dieterich, M., Brandt, T., Strupp, M., Bartenstein, P., & Jahn, K. (2010). Real versus imagined locomotion: A [18F]-FDG PET-fMRI comparison. NeuroImage, 50(4), 15891598. https://doi.org/10.1016/j.neuroimage.2009.12.060

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Menant, J.C., Maidan, I., Alcock, L., Al-Yahya, E., Cerasa, A., Clark, D.J., de Bruin, E., Fraser, S., Gramigna, V., Hamacher, D., Herold, F., Holtzer, R., Izzetoglu, M., Lim, S., Pantall, A., Pelicioni, P., Peters, S., Rosso, A.L., St George, R., … Mirelman, A. (2020). A consensus guide to using functional near-infrared spectroscopy in posture and gait research. Gait & Posture, 82, 254265. https://doi.org/10.1016/j.gaitpost.2020.09.012

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Mirelman, A., Maidan, I., Bernad-Elazari, H., Shustack, S., Giladi, N., & Hausdorff, J.M. (2017). Effects of aging on prefrontal brain activation during challenging walking conditions. Brain and Cognition, 115, 4146. https://doi.org/10.1016/j.bandc.2017.04.002

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 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), 49100. https://doi.org/10.1006/cogp.1999.0734

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Nóbrega-Sousa, P., Gobbi, L.T.B., Orcioli-Silva, D., Conceição, N.R., Beretta, V.S., & Vitório, R. (2020). Prefrontal cortex activity during walking: Effects of aging and associations with gait and executive function. Neurorehabilitation and Neural Repair, 34(10), 915924. https://doi.org/10.1177/1545968320953824

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Obrig, H., & Villringer, A. (2003). Beyond the visible—Imaging the human brain with light. Journal of Cerebral Blood Flow & Metabolism, 23(1), 118. https://doi.org/10.1097/01.WCB.0000043472.45775.29

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Park, D.C., Polk, T.A., Mikels, J.A., Taylor, S.F., & Marshuetz, C. (2001). Cerebral aging: Integration of brain and behavioral models of cognitive function. Dialogues in Clinical Neuroscience, 3(3), 151165.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Park, D.C., & Reuter-Lorenz, P. (2009). The adaptive brain: Aging and neurocognitive scaffolding. Annual Review of Psychology, 60(1), 173196. https://doi.org/10.1146/annurev.psych.59.103006.093656

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Patil, A.V., Safaie, J., Moghaddam, H.A., Wallois, F., & Grebe, R. (2011). Experimental investigation of NIRS spatial sensitivity. Biomedical Optics Express, 2(6), 1478. https://doi.org/10.1364/BOE.2.001478

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Pelicioni, P.H.S., Tijsma, M., Lord, S.R., & Menant, J. (2019). Prefrontal cortical activation measured by fNIRS during walking: Effects of age, disease and secondary task. PeerJ, 7, e6833. https://doi.org/10.7717/peerj.6833

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Perrey, S. (2008). Non-invasive NIR spectroscopy of human brain function during exercise. Methods, 45(4), 289299. https://doi.org/10.1016/j.ymeth.2008.04.005

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Rikli, R.E., & Jones, C.J. (2013). Development and validation of criterion-referenced clinically relevant fitness standards for maintaining physical independence in later years. The Gerontologist, 53(2), 255267. https://doi.org/10.1093/geront/gns071

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Schaefer, S., Lövdén, M., Wieckhorst, B., & Lindenberger, U. (2010). Cognitive performance is improved while walking: Differences in cognitive–sensorimotor couplings between children and young adults. European Journal of Developmental Psychology, 7(3), 371389. https://doi.org/10.1080/17405620802535666

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Strangman, G., Culver, J.P., Thompson, J.H., & Boas, D.A. (2002). A quantitative comparison of simultaneous bold fMRI and NIRS recordings during functional brain activation. NeuroImage, 17(2), 719731. https://doi.org/10.1006/nimg.2002.1227

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Stuart, S., Vitorio, R., Morris, R., Martini, D.N., Fino, P.C., & Mancini, M. (2018). Cortical activity during walking and balance tasks in older adults and in people with Parkinson’s disease: A structured review. Maturitas, 113, 5372. https://doi.org/10.1016/j.maturitas.2018.04.011

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Suzuki, M., Miyai, I., Ono, T., & Kubota, K. (2008). Activities in the frontal cortex and gait performance are modulated by preparation. An fNIRS study. NeuroImage, 39(2), 600607. https://doi.org/10.1016/j.neuroimage.2007.08.044

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Suzuki, M., Miyai, I., Ono, T., Oda, I., Konishi, I., Kochiyama, T., & Kubota, K. (2004). Prefrontal and premotor cortices are involved in adapting walking and running speed on the treadmill: An optical imaging study. NeuroImage, 23(3), 10201026. https://doi.org/10.1016/j.neuroimage.2004.07.002

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Tomporowski, P.D., & Audiffren, M. (2014). Dual-task performance in young and older adults: speed-accuracy tradeoffs in choice responding while treadmill walking. Journal of Aging and Physical Activity, 22(4), 557563. https://doi.org/10.1123/JAPA.2012-0241

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Towse, J.N., & Neil, D. (1998). Analyzing human random generation behavior: A review of methods used and a computer program for describing performance. Behavior Research Methods, Instruments, & Computers, 30(4), 583591. https://doi.org/10.3758/BF03209475

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Udina, C., Avtzi, S., Durduran, T., Holtzer, R., Rosso, A.L., Castellano-Tejedor, C., Perez, L.-M., Soto-Bagaria, L., & Inzitari, M. (2020). Functional near-infrared spectroscopy to study cerebral hemodynamics in older adults during cognitive and motor tasks: A review. Frontiers in Aging Neuroscience, 11, 367. https://doi.org/10.3389/fnagi.2019.00367

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Vuillemin, A., Oppert, J.-M., Guillemin, F., Essermeant, L., Fontvieille, A.-M., Galan, P., Kriska, A.M., & Hercberg, S. (2000). Self-administered questionnaire compared with interview to assess past-year physical activity. Medicine & Science in Sports & Exercise, 32(6), 11191124. https://doi.org/10.1097/00005768-200006000-00013

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Wang, R.-Y., Wang, Y.-L., Cheng, F.-Y., Chao, Y.-H., Chen, C.-L., & Yang, Y.-R. (2015). Effects of combined exercise on gait variability in community-dwelling older adults. Age, 37(3), 40. https://doi.org/10.1007/s11357-015-9780-2

    • Crossref
    • Search Google Scholar
    • Export Citation
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