Effect of Aerobic Exercise on White Matter Tract Microstructure in Young and Middle-Aged Healthy Adults

David Predovan, Yunglin Gazes, Seonjoo Lee, Peipei Li, Richard P Sloan, Yaakov Stern, David Predovan, Yunglin Gazes, Seonjoo Lee, Peipei Li, Richard P Sloan, Yaakov Stern

Abstract

Recent evidence suggests that being physically active can mitigate age-related white matter (WM) changes. In a randomized clinical trial, the effect of 6-month aerobic exercise (AE) or stretching/toning interventions on measures of WM microstructure (WMM) was assessed in a sample of 74 adults aged 20-67 years. Major WM pathways were reconstructed. No significant group-level change in WM tract microstructure following an AE training was observed. Without adjustment for multiple comparisons, an increase in fractional anisotropy (FA) and a decrease in mean diffusivity (MD) of the uncinate fasciculus were observed post-intervention in the AE group in comparison with the stretching group. In the AE group, a significant increase in cardiorespiratory fitness was measured but did not correlate with FA and MD change. The present results of this study are in accordance with similar studies in healthy adults that did not show significant benefit on WMM after participating in an AE program. Clinical Trial Registration: Clinicaltrials.gov identifier, NCT01179958.

Keywords: aerobic exercise; aging; cardiorespiratory fitness; cognition; white matter microstructure.

Conflict of interest statement

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Copyright © 2021 Predovan, Gazes, Lee, Li, Sloan and Stern.

Figures

Figure 1
Figure 1
Flowchart.
Figure 2
Figure 2
Sex-difference of the intervention effect in terms of change on the white matter tract fractional anisotropy of the uncinate fasciculus (UNC) and the Cingulum—angular (infracallosal) and bundle (CAB).

References

    1. Alexander A. L., Hurley S. A., Samsonov A. A., Adluru N., Hosseinbor A. P., Mossahebi P., et al. . (2011). Characterization of cerebral white matter properties using quantitative magnetic resonance imaging stains. Brain Connect 1, 423–446. 10.1089/brain.2011.0071
    1. Andersson J. L. R., Sotiropoulos S. N. (2016). An integrated approach to correction for off-resonance effects and subject movement in diffusion MR imaging. Neuroimage 125, 1063–1078. 10.1016/j.neuroimage.2015.10.019
    1. Barha C. K., Davis J. C., Falck R. S., Nagamatsu L. S., Liu-Ambrose T. (2017). Sex differences in exercise efficacy to improve cognition: a systematic review and meta-analysis of randomized controlled trials in older humans. Front. Neuroendocrinol. 46, 71–85. 10.1016/j.yfrne.2017.04.002
    1. Benjamini Y., Hochberg Y. (1995). Controlling the false discovery rate: a practical and powerful approach to multiple testing. J. R. Stat. Soc. Ser. B Methodol. 57, 289–300. 10.1111/j.2517-6161.1995.tb02031.x
    1. Burzynska A. Z., Jiao Y., Knecht A. M., Fanning J., Awick E. A., Chen T., et al. . (2017). White matter integrity declined over 6-months, but dance intervention improved integrity of the fornix of older adults. Front. Aging Neurosci. 9:59. 10.3389/fnagi.2017.00059
    1. Burzynska A. Z., Preuschhof C., Backman L., Nyberg L., Li S. C., Lindenberger U., et al. . (2010). Age-related differences in white matter microstructure: region-specific patterns of diffusivity. Neuroimage 49, 2104–2112. 10.1016/j.neuroimage.2009.09.041
    1. Chapman S. B., Aslan S., Spence J. S., Hart J. J., Jr., Bartz E. K., Didehbani N., et al. . (2015). Neural mechanisms of brain plasticity with complex cognitive training in healthy seniors. Cereb. Cortex 25, 396–405. 10.1093/cercor/bht234
    1. Clark C. M., Guadagni V., Mazerolle E. L., Hill M., Hogan D. B., Pike G. B., et al. . (2019). Effect of aerobic exercise on white matter microstructure in the aging brain. Behav. Brain Res. 373:112042. 10.1016/j.bbr.2019.112042
    1. Colcombe S. J., Erickson K. I., Raz N., Webb A. G., Cohen N. J., McAuley E., et al. . (2003). Aerobic fitness reduces brain tissue loss in aging humans. J. Gerontol. A Biol. Sci. Med. Sci. 58, 176–180. 10.1093/gerona/58.2.M176
    1. Colcombe S. J., Erickson K. I., Scalf P. E., Kim J. S., Prakash R., McAuley E., et al. . (2006). Aerobic exercise training increases brain volume in aging humans. J. Gerontol. A Biol. Sci. Med. Sci. 61, 1166–1170. 10.1093/gerona/61.11.1166
    1. Cox S. R., Lyall D. M., Ritchie S. J., Bastin M. E., Harris M. A., Buchanan C. R., et al. . (2019). Associations between vascular risk factors and brain MRI indices in UK Biobank. Eur. Heart J. 40, 2290–2300. 10.1093/eurheartj/ehz100
    1. Cox S. R., Ritchie S. J., Tucker-Drob E. M., Liewald D. C., Hagenaars S. P., Davies G., et al. . (2016). Ageing and brain white matter structure in 3,513 UK Biobank participants. Nat. Commun. 7:13629. 10.1038/ncomms13629
    1. Damoiseaux J. S. (2017). Effects of aging on functional and structural brain connectivity. Neuroimage 160, 32–40. 10.1016/j.neuroimage.2017.01.077
    1. Erickson K. I., Hillman C., Stillman C. M., Ballard R. M., Bloodgood B., Conroy D. E., et al. . (2019). Physical activity, cognition, and brain outcomes: a review of the 2018 physical activity guidelines. Med. Sci. Sports Exerc. 51, 1242–1251. 10.1249/MSS.0000000000001936
    1. Falck R. S., Davis J. C., Best J. R., Crockett R. A., Liu-Ambrose T. (2019). Impact of exercise training on physical and cognitive function among older adults: a systematic review and meta-analysis. Neurobiol. Aging. 79, 119–130. 10.1016/j.neurobiolaging.2019.03.007
    1. Fischl B., van der Kouwe A., Destrieux C., Halgren E., Segonne F., Salat D. H., et al. . (2004). Automatically parcellating the human cerebral cortex. Cereb. Cortex 14, 11–22. 10.1093/cercor/bhg087
    1. Fox S. M., III., Naughton J. P., Haskell W. L. (1971). Physical activity and the prevention of coronary heart disease. Ann. Clin. Res. 3, 404–432.
    1. Fuhrmann D., Nesbitt D., Shafto M., Rowe J. B., Price D., Gadie A., et al. . (2019). Strong and specific associations between cardiovascular risk factors and white matter micro- and macrostructure in healthy aging. Neurobiol. Aging 74, 46-55. 10.1016/j.neurobiolaging.2018.10.005
    1. Gaertner B., Buttery A. K., Finger J. D., Wolfsgruber S., Wagner M., Busch M. A. (2018). Physical exercise and cognitive function across the life span: results of a nationwide population-based study. J. Sci. Med. Sport 21, 489–494. 10.1016/j.jsams.2017.08.022
    1. Gazes Y., Li P., Sun E., Razlighi Q., Tsapanou A. (2018). Age specificity in fornix-to-hippocampus association. Brain Imaging Behav. 13, 1444–1452. 10.1007/s11682-018-9958-1
    1. Gow A. J., Bastin M. E., Munoz Maniega S., Valdes Hernandez M. C., Morris Z., Murray C., et al. . (2012). Neuroprotective lifestyles and the aging brain: activity, atrophy, and white matter integrity. Neurology 79, 1802–1808. 10.1212/WNL.0b013e3182703fd2
    1. Grieve S. M., Williams L. M., Paul R. H., Clark C. R., Gordon E. (2007). Cognitive aging, executive function, and fractional anisotropy: a diffusion tensor MR imaging study. AJNR Am J Neuroradiol 28, 226–235.
    1. Hawkins S., Wiswell R. (2003). Rate and mechanism of maximal oxygen consumption decline with aging: implications for exercise training. Sports Med. 33, 877–888. 10.2165/00007256-200333120-00002
    1. Hayes S. M., Salat D. H., Forman D. E., Sperling R. A., Verfaellie M. (2015). Cardiorespiratory fitness is associated with white matter integrity in aging. Ann. Clin. Transl. Neurol. 2, 688–698. 10.1002/acn3.204
    1. Holzel B. K., Brunsch V., Gard T., Greve D. N., Koch K., Sorg C., et al. . (2016). Mindfulness-based stress reduction, fear conditioning, and the uncinate fasciculus: a pilot study. Front. Behav. Neurosci. 10:124. 10.3389/fnbeh.2016.00124
    1. Irwin K., Sexton C., Daniel T., Lawlor B., Naci L. (2018). Healthy aging and dementia: two roads diverging in midlife? Front. Aging Neurosci. 10:275. 10.3389/fnagi.2018.00275
    1. Johnson N. F., Kim C., Clasey J. L., Bailey A., Gold B. T. (2012). Cardiorespiratory fitness is positively correlated with cerebral white matter integrity in healthy seniors. Neuroimage 59, 1514–1523. 10.1016/j.neuroimage.2011.08.032
    1. Kennedy K. M., Raz N. (2009). Aging white matter and cognition: differential effects of regional variations in diffusion properties on memory, executive functions, and speed. Neuropsychologia 47, 916–927. 10.1016/j.neuropsychologia.2009.01.001
    1. Li P., Tsapanou A., Qolamreza R. R., Gazes Y. (2018). White matter integrity mediates decline in age-related inhibitory control. Behav. Brain Res. 339, 249–254. 10.1016/j.bbr.2017.11.005
    1. Lim Y. Y., Jaeger J., Harrington K., Ashwood T., Ellis K. A., Stoffler A., et al. . (2013). Three-month stability of the CogState brief battery in healthy older adults, mild cognitive impairment, and Alzheimer's disease: results from the Australian Imaging, Biomarkers, and Lifestyle-rate of change substudy (AIBL-ROCS). Arch. Clin. Neuropsychol. 28, 320–330. 10.1093/arclin/act021
    1. Mori S., Zhang J. (2006). Principles of diffusion tensor imaging and its applications to basic neuroscience research. Neuron 51, 527–539. 10.1016/j.neuron.2006.08.012
    1. Northey J. M., Cherbuin N., Pumpa K. L., Smee D. J., Rattray B. (2018). Exercise interventions for cognitive function in adults older than 50: a systematic review with meta-analysis. Br. J. Sports Med. 52, 154–160. 10.1136/bjsports-2016-096587
    1. Oberlin L. E., Verstynen T. D., Burzynska A. Z., Voss M. W., Prakash R. S., Chaddock-Heyman L., et al. . (2016). White matter microstructure mediates the relationship between cardiorespiratory fitness and spatial working memory in older adults. Neuroimage 131, 91–101. 10.1016/j.neuroimage.2015.09.053
    1. Reuter M., Fischl B. (2011). Avoiding asymmetry-induced bias in longitudinal image processing. Neuroimage 57, 19–21. 10.1016/j.neuroimage.2011.02.076
    1. Reuter M., Rosas H. D., Fischl B. (2010). Highly accurate inverse consistent registration: a robust approach. Neuroimage 53, 1181–1196. 10.1016/j.neuroimage.2010.07.020
    1. Reuter M., Schmansky N. J., Rosas H. D., Fischl B. (2012). Within-subject template estimation for unbiased longitudinal image analysis. Neuroimage 61, 1402–1418. 10.1016/j.neuroimage.2012.02.084
    1. Sampaio-Baptista C., Johansen-Berg H. (2017). White matter plasticity in the adult brain. Neuron 96, 1239–1251. 10.1016/j.neuron.2017.11.026
    1. Sampaio-Baptista C., Khrapitchev A. A., Foxley S., Schlagheck T., Scholz J., Jbabdi S., et al. . (2013). Motor skill learning induces changes in white matter microstructure and myelination. J. Neurosci. 33:19499. 10.1523/JNEUROSCI.3048-13.2013
    1. Scholz J., Klein M. C., Behrens T. E., Johansen-Berg H. (2009). Training induces changes in white-matter architecture. Nat. Neurosci. 12, 1370–1371. 10.1038/nn.2412
    1. Sexton C. E., Betts J. F., Demnitz N., Dawes H., Ebmeier K. P., Johansen-Berg H. (2016). A systematic review of MRI studies examining the relationship between physical fitness and activity and the white matter of the ageing brain. Neuroimage 131, 81–90. 10.1016/j.neuroimage.2015.09.071
    1. Slater D. A., Melie-Garcia L., Preisig M., Kherif F., Lutti A., Draganski B. (2019). Evolution of white matter tract microstructure across the life span. Hum. Brain Mapp. 40, 2252–2268. 10.1002/hbm.24522
    1. Stern Y., Lee S., Predovan D., Sloan R. P. (2019a). Sex moderates the effect of aerobic exercise on some aspects of cognition in cognitively intact younger and middle-age adults. J. Clin. Med. 8:886. 10.3390/jcm8060886
    1. Stern Y., MacKay-Brandt A., Lee S., McKinley P., McIntyre K., Razlighi Q., et al. . (2019b). Effect of aerobic exercise on cognition in younger adults: a randomized clinical trial. Neurology 92, e905–e916. 10.1212/WNL.0000000000007003
    1. Stillman C. M., Esteban-Cornejo I., Brown B., Bender C. M., Erickson K. I. (2020). Effects of exercise on brain and cognition across age groups and health states. Trends Neurosci. 43, 533–543. 10.1016/j.tins.2020.04.010
    1. Stimpson N. J., Davison G., Javadi A. H. (2018). Joggin' the noggin: towards a physiological understanding of exercise-induced cognitive benefits. Neurosci. Biobehav. Rev. 88, 177–186. 10.1016/j.neubiorev.2018.03.018
    1. Streitburger D. P., Moller H. E., Tittgemeyer M., Hund-Georgiadis M., Schroeter M. L., Mueller K. (2012). Investigating structural brain changes of dehydration using voxel-based morphometry. PLoS ONE 7:e44195. 10.1371/journal.pone.0044195
    1. Strommer J. M., Davis S. W., Henson R. N., Tyler L. K., Cam C. A. N., Campbell K. L. (2020). Physical activity predicts population-level age-related differences in frontal white matter. J. Gerontol. A Biol. Sci. Med. Sci. 75, 236–243. 10.1101/311050
    1. Tarumi T., Thomas B. P., Tseng B. Y., Wang C., Womack K. B., Hynan L., et al. . (2020). Cerebral white matter integrity in amnestic mild cognitive impairment: a 1-year randomized controlled trial of aerobic exercise training. J. Alzheimers Dis. 73, 489–501. 10.3233/JAD-190875
    1. Tian Q., Simonsick E. M., Erickson K. I., Aizenstein H. J., Glynn N. W., Boudreau R. M., et al. . (2014). Cardiorespiratory fitness and brain diffusion tensor imaging in adults over 80 years of age. Brain Res. 1588, 63–72. 10.1016/j.brainres.2014.09.003
    1. Trangmar S. J., Gonzalez-Alonso J. (2019). Heat, hydration and the human brain, heart and skeletal muscles. Sports Med. 49(Suppl 1), 69–85. 10.1007/s40279-018-1033-y
    1. Voss M. W., Heo S., Prakash R. S., Erickson K. I., Alves H., Chaddock L., et al. . (2013). The influence of aerobic fitness on cerebral white matter integrity and cognitive function in older adults: results of a one-year exercise intervention. Hum. Brain Mapp. 34, 2972–2985. 10.1002/hbm.22119
    1. Wassenaar T. M., Yaffe K., van der Werf Y. D., Sexton C. E. (2019). Associations between modifiable risk factors and white matter of the aging brain: insights from diffusion tensor imaging studies. Neurobiol. Aging 80, 56–70. 10.1016/j.neurobiolaging.2019.04.006
    1. Yendiki A., Panneck P., Srinivasan P., Stevens A., Zollei L., Augustinack J., et al. . (2011). Automated probabilistic reconstruction of white-matter pathways in health and disease using an atlas of the underlying anatomy. Front. Neuroinform. 5:23. 10.3389/fninf.2011.00023
    1. Yendiki A., Reuter M., Wilkens P., Rosas H. D., Fischl B. (2016). Joint reconstruction of white-matter pathways from longitudinal diffusion MRI data with anatomical priors. Neuroimage 127, 277–286. 10.1016/j.neuroimage.2015.12.003
    1. Zhu N., Jacobs D. R., Jr., Schreiner P. J., Launer L. J., Whitmer R. A., Sidney S., et al. . (2015). Cardiorespiratory fitness and brain volume and white matter integrity: the CARDIA Study. Neurology 84, 2347–2353. 10.1212/WNL.0000000000001658

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