White matter microstructure mediates the relationship between cardiorespiratory fitness and spatial working memory in older adults - PubMed (original) (raw)
doi: 10.1016/j.neuroimage.2015.09.053. Epub 2015 Oct 9.
Timothy D Verstynen 2, Agnieszka Z Burzynska 3, Michelle W Voss 4, Ruchika Shaurya Prakash 5, Laura Chaddock-Heyman 6, Chelsea Wong 6, Jason Fanning 7, Elizabeth Awick 7, Neha Gothe 8, Siobhan M Phillips 9, Emily Mailey 10, Diane Ehlers 7, Erin Olson 11, Thomas Wojcicki 12, Edward McAuley 7, Arthur F Kramer 6, Kirk I Erickson 13
Affiliations
- PMID: 26439513
- PMCID: PMC4826637
- DOI: 10.1016/j.neuroimage.2015.09.053
White matter microstructure mediates the relationship between cardiorespiratory fitness and spatial working memory in older adults
Lauren E Oberlin et al. Neuroimage. 2016.
Abstract
White matter structure declines with advancing age and has been associated with a decline in memory and executive processes in older adulthood. Yet, recent research suggests that higher physical activity and fitness levels may be associated with less white matter degeneration in late life, although the tract-specificity of this relationship is not well understood. In addition, these prior studies infrequently associate measures of white matter microstructure to cognitive outcomes, so the behavioral importance of higher levels of white matter microstructural organization with greater fitness levels remains a matter of speculation. Here we tested whether cardiorespiratory fitness (VO2max) levels were associated with white matter microstructure and whether this relationship constituted an indirect pathway between cardiorespiratory fitness and spatial working memory in two large, cognitively and neurologically healthy older adult samples. Diffusion tensor imaging was used to determine white matter microstructure in two separate groups: Experiment 1, N=113 (mean age=66.61) and Experiment 2, N=154 (mean age=65.66). Using a voxel-based regression approach, we found that higher VO2max was associated with higher fractional anisotropy (FA), a measure of white matter microstructure, in a diverse network of white matter tracts, including the anterior corona radiata, anterior internal capsule, fornix, cingulum, and corpus callosum (PFDR-corrected<.05). This effect was consistent across both samples even after controlling for age, gender, and education. Further, a statistical mediation analysis revealed that white matter microstructure within these regions, among others, constituted a significant indirect path between VO2max and spatial working memory performance. These results suggest that greater aerobic fitness levels are associated with higher levels of white matter microstructural organization, which may, in turn, preserve spatial memory performance in older adulthood.
Keywords: Aging; Fitness; Memory; White matter.
Copyright © 2015 Elsevier Inc. All rights reserved.
Figures
Figure 1
Shown are significant associations between cardiorespiratory fitness (CRF), fractional anisotropy (FA), and mean spatial working memory performance from Experiment 1. (A) Clusters of voxels where fitness was significantly associated with FA. Warm-colored voxels show positive associations, cool-colored voxels demonstrate negative associations. Side panels indicate slice placements. Age, gender, and years of education were included as covariates. Clusters are thresholded to k≥20 contiguous voxels and a false discovery rate of 0.05. The z-plane coordinates of each slice, in MNI space, are presented at the bottom. For visualization purposes, tbss_fill was used to dilate statistical maps. (B) For illustration purposes, scatterplots and best-fit lines for the relationship between CRF and FA in selected regions. (C) Spatial distribution of indirect path voxel clusters. Cyan-colored voxel clusters show a positive indirect effect, brown voxel clusters indicate a negative indirect effect. Ant, anterior; IC, internal capsule; CC, corpus callosum; Ext, external; FA, fractional anisotropy.
Figure 2
Shown are associations between cardiorespiratory fitness (CRF), fractional anisotropy (FA), and spatial working memory performance from Experiment 2, with the same plotting conventions as Figure 1. Ant, anterior; FA, fractional anisotropy; CC, corpus callosum; IC, internal capsule; CR, corona radiata.
Figure 3A
Shown are results from the conjunction analysis of the relationship between fitness and FA in Experiment 1 and Experiment 2.
Figure 3B
Shown are the results from the conjunction analysis of the indirect path voxels in Experiment 1 and Experiment 2.
Similar articles
- Effect of aerobic exercise on white matter microstructure in the aging brain.
Clark CM, Guadagni V, Mazerolle EL, Hill M, Hogan DB, Pike GB, Poulin MJ. Clark CM, et al. Behav Brain Res. 2019 Nov 5;373:112042. doi: 10.1016/j.bbr.2019.112042. Epub 2019 Jul 4. Behav Brain Res. 2019. PMID: 31279793 - The relationship between white matter microstructure, cardiovascular fitness, gross motor skills, and neurocognitive functioning in children.
Meijer A, Pouwels PJW, Smith J, Visscher C, Bosker RJ, Hartman E, Oosterlaan J, Königs M. Meijer A, et al. J Neurosci Res. 2021 Sep;99(9):2201-2215. doi: 10.1002/jnr.24851. Epub 2021 May 21. J Neurosci Res. 2021. PMID: 34019710 Free PMC article. Clinical Trial. - The association between physical fitness parameters and white matter microstructure in older adults: A diffusion tensor imaging study.
Chen FT, Erickson KI, Huang H, Chang YK. Chen FT, et al. Psychophysiology. 2020 May;57(5):e13539. doi: 10.1111/psyp.13539. Epub 2020 Feb 6. Psychophysiology. 2020. PMID: 32030777 - A systematic review of MRI studies examining the relationship between physical fitness and activity and the white matter of the ageing brain.
Sexton CE, Betts JF, Demnitz N, Dawes H, Ebmeier KP, Johansen-Berg H. Sexton CE, et al. Neuroimage. 2016 May 1;131:81-90. doi: 10.1016/j.neuroimage.2015.09.071. Epub 2015 Oct 16. Neuroimage. 2016. PMID: 26477656 Free PMC article. Review. - Working Memory: How Important Is White Matter?
Lazar M. Lazar M. Neuroscientist. 2017 Apr;23(2):197-210. doi: 10.1177/1073858416634298. Neuroscientist. 2017. PMID: 30231842 Review.
Cited by
- A systematic review and meta-analysis of the effects of physical exercise on white matter integrity and cognitive function in older adults.
Zhang W, Zhou C, Chen A. Zhang W, et al. Geroscience. 2024 Apr;46(2):2641-2651. doi: 10.1007/s11357-023-01033-8. Epub 2023 Dec 18. Geroscience. 2024. PMID: 38108993 Free PMC article. - Engineering Virtuous health habits using Emotion and Neurocognition: Flexibility for Lifestyle Optimization and Weight management (EVEN FLOW).
Smith PJ, Whitson HE, Merwin RM, O'Hayer CV, Strauman TJ. Smith PJ, et al. Front Aging Neurosci. 2023 Nov 22;15:1256430. doi: 10.3389/fnagi.2023.1256430. eCollection 2023. Front Aging Neurosci. 2023. PMID: 38076541 Free PMC article. Review. - The effect of physical activity on white matter integrity in aging and prodromal to mild Alzheimer's disease with vascular comorbidity.
Konwar S, Manca R, De Marco M, Soininen H, Venneri A. Konwar S, et al. Front Aging Neurosci. 2023 Jun 21;15:1096798. doi: 10.3389/fnagi.2023.1096798. eCollection 2023. Front Aging Neurosci. 2023. PMID: 37520122 Free PMC article. - Enhanced Integrity of White Matter Microstructure in Mind-Body Practitioners: A Whole-Brain Diffusion Tensor Imaging Study.
Xie Y, Cai K, Dai J, Wei G. Xie Y, et al. Brain Sci. 2023 Apr 20;13(4):691. doi: 10.3390/brainsci13040691. Brain Sci. 2023. PMID: 37190656 Free PMC article. - Influence of mild cognitive impairment and body mass index on white matter integrity assessed by diffusion tensor imaging.
Tinney EM, Loui P, Raine LB, Hiscox LV, Delgorio PL, Kramer MK, Schwarb H, Martens CR, Kramer AF, Hillman CH, Johnson CL. Tinney EM, et al. Psychophysiology. 2023 Sep;60(9):e14306. doi: 10.1111/psyp.14306. Epub 2023 Apr 10. Psychophysiology. 2023. PMID: 37038273 Free PMC article.
References
- Burzynska AZ, Preuschhof C, Bäckman L, Nyberg L, Li S-C, Lindenberger U, Heekeren HR. Age-related differences in white matter microstructure: region-specific patterns of diffusivity. NeuroImage. 2010;49:2104–2112. - PubMed
- Charlton R, Barrick T, McIntyre D, Shen Y, O'Sullivan M, Howe F.e., Clark C, Morris R, Markus H. White matter damage on diffusion tensor imaging correlates with age-related cognitive decline. Neurology. 2006;66:217–222. emsp14, al. - PubMed
Publication types
MeSH terms
Grants and funding
- P30 AG024827/AG/NIA NIH HHS/United States
- R37 AG025667/AG/NIA NIH HHS/United States
- R01 AG025032/AG/NIA NIH HHS/United States
- R01 DK095172/DK/NIDDK NIH HHS/United States
- R01 AG025667/AG/NIA NIH HHS/United States
LinkOut - more resources
Full Text Sources
Other Literature Sources
Medical