journal article·2021-04-23Open access

Football Juggling Learning Alters the Working Memory and White Matter Integrity in Early Adulthood: A Randomized Controlled Study

Yifan Shi, Kelong Cai, Hao Zhu, Xiaoxiao Dong, Xuan Xiong, Lina Zhu, Zhiyuan Sun, Aiguo Chen

Applied Sciences· Volume 11· Issue 9

Abstract

Cross-sectional studies suggest that motor skill learning is associated with working memory (WM) and white matter integrity (WMI). However, it has not been established whether motor skill learning improves WM performance, and information on its neural mechanisms have not been clearly elucidated. Therefore, this study compared WM and WMI across time points prior to and following football juggling learning, in early adulthood (18–20 years old), relative to a control group. Study participants in the experimental group were subjected to football juggling for 10 weeks while participants in the control category went on with their routine life activities for the same period of time and were not involved in the learning-related activities. Data on cognitive measurements and that from diffusion tensor imaging (DTI) were collected before and after learning. There was a significant improvement in WM performance of the experimental group after motor learning, although no improvement was observed in the control group. Additionally, after learning, DTI data revealed a significant increase in functional anisotropy (FA) in the genu of corpus callosum (GOCC) and the right anterior corona radiata (R.ACR) in the experimental group. Moreover, the better WM associated with football juggling learning was correlated to a higher FA. Mediation analysis suggested that FA in the GOCC acts as a mediation variable between football juggling learning and WM. These findings show that motor skill learning improves the WM and remodels WMI in early adulthood. With a particular emphasis on the importance of WMI in motor skill learning and WM, this study also revealed the possible neural mechanisms mediated by WMI.
Source: crossref · Quality: baseline

Research context

OpenAlex topics: Advanced Neuroimaging Techniques and Applications · Functional Brain Connectivity Studies · Advanced MRI Techniques and Applications

SciVX discovery tags are terminology-based. OpenAlex topics are source-provided classifications.

Affiliations

College of Physical Education, Yangzhou University, Yangzhou 225127, China

Institute of Sports, Exercise and Brain, Yangzhou University, Yangzhou 225127, China

School of Physical Education and Sports Science, Beijing Normal University, Beijing 100000, China

Chinese–Polish Laboratory of Sport and Brain Science, Yangzhou University, Yangzhou 225127, China

Funding

National Natural Science Foundation of China · Fok Ying Tung Education Foundation

References (99)

Show source-provided references
1. Neurobiology of exercise10.1038/oby.2006.46 ↗
2. Neurocognitive Contributions to Motor Skill Learning: The Role of Working Memory10.1080/00222895.2012.672348 ↗
3. Neuroplasticity subserving motor skill learning10.1016/j.neuron.2011.10.008 ↗
4. A neuropsychological theory of motor skill learning10.1037/0033-295X.105.3.558 ↗
5. Chaddock-Heyman, L., Erickson, K.I., Voss, M.W., Powers, J.P., Knecht, A.M., Pontifex, M.B., Drollette, E.S., Moore, R.D., Raine, L.B., and Scudder, M.R. (2013). White matter microstructure is associated with cognitive control in children. Biol. Psychol.10.1016/j.biopsycho.2013.05.008 ↗
6. Physical fitness, but not acute exercise modulates event-related potential indices for executive control in healthy adolescents10.1016/j.brainres.2009.02.073 ↗
7. Contributions of Spatial Working Memory to Visuomotor Learning10.1162/jocn.2009.21351 ↗
8. Dual-task training on cognition and resistance training improved both balance and working memory in older people10.1080/00913847.2019.1623996 ↗
9. Niederer, I., Kriemler, S., Gut, J., Hartmann, T., and Puder, J.J. (2011). Relationship of aerobic fitness and motor skills with memory and attention in preschoolers (Ballabeina): A cross-sectional and longitudinal study. BMC Pediatr., 11.10.1186/1471-2431-11-34 ↗
10. Exercise, ageing and cognitive function—Effects of a personalized physical exercise program in the cognitive function of older adults10.1016/j.physbeh.2019.01.018 ↗
11. Nouchi, R., Taki, Y., Takeuchi, H., Hashizume, H., Nozawa, T., Kambara, T., Sekiguchi, A., Miyauchi, C.M., Kotozaki, Y., and Nouchi, H. (2013). Brain Training Game Boosts Executive Functions, Working Memory and Processing Speed in the Young Adults: A Randomized Controlled Trial. PLoS ONE, 8.10.1371/journal.pone.0055518 ↗
12. Balance training improves memory and spatial cognition in healthy adults10.1038/s41598-017-06071-9 ↗
13. Relationship of tennis play to executive function in children and adolescents10.1080/17461391.2017.1334831 ↗
14. The Relationship Between Cognitive Functions and Sport-Specific Motor Skills in Elite Youth Soccer Players10.3389/fpsyg.2019.00817 ↗
15. Grassi, M., Meneghetti, C., Toffalini, E., and Borella, E. (2017). Auditory and cognitive performance in elderly musicians and nonmusicians. PLoS ONE, 12.10.1371/journal.pone.0187881 ↗
16. Geertsen, S.S., Thomas, R., Larsen, M.N., Dahn, I.M., Andersen, J.N., Krause-Jensen, M., Korup, V., Nielsen, C.M., Wienecke, J., and Ritz, C. (2016). Motor Skills and Exercise Capacity Are Associated with Objective Measures of Cognitive Functions and Academic Performance in Preadolescent Children. PLoS ONE, 11.10.1371/journal.pone.0161960 ↗
17. Verburgh, L., Scherder, E.J., Van Lange, P.A., and Oosterlaan, J. (2016). Do Elite and Amateur Soccer Players Outperform Non-Athletes on Neurocognitive Functioning? A Study Among 8–12 Year Old Children. PLoS ONE, 11.10.1371/journal.pone.0165741 ↗
18. Wouters, H., Aalbers, T., Maessen, M., Verbeek, A., Olde Rikkert, M., Kessels, R., Hopman, M., and Eijsvogels, T. (2017). Physical activity and cognitive function of long distance walkers: Studying four days marches participants. Rejuvenation Res., 20.10.1089/rej.2016.1876 ↗
19. Working Memory: How Important Is White Matter?10.1177/1073858416634298 ↗
20. The cognitive neuroscience of working memory10.1146/annurev-psych-010814-015031 ↗
21. Miller, E.K., Lundqvist, M., and Bastos, A.M. (2018). Working Memory 2.0. Neuron.10.1016/j.neuron.2018.09.023 ↗
22. Motor skill learning induces changes in white matter microstructure and myelination10.1523/JNEUROSCI.3048-13.2013 ↗
23. Training induces changes in white-matter architecture10.1038/nn.2412 ↗
24. Badea, A., Ng, K.L., Anderson, R.J., Zhang, J., Miller, M.I., and O’Brien, R.J. (2019). Magnetic resonance imaging of mouse brain networks plasticity following motor learning. PLoS ONE, 14.10.1371/journal.pone.0216596 ↗
25. Neuroplasticity: Changes in grey matter induced by training10.1038/427311a ↗
26. Pi, Y.L., Wu, X.H., Wang, F.J., Liu, K., Wu, Y., Zhu, H., and Zhang, J. (2019). Motor skill learning induces brain network plasticity: A diffusion-tensor imaging study. PLoS ONE, 14.10.1371/journal.pone.0210015 ↗
27. Lehmann, N., Tolentino-Castro, J.W., Kaminski, E., Ragert, P., and Taubert, M. (2019). Interindividual differences in gray and white matter properties are associated with early complex motor skill acquisition. Hum. Brain Mapp., 40.10.1002/hbm.24704 ↗
28. Plasticity in deep and superficial white matter: A DTI study in world class gymnasts
29. Differences in white matter architecture between musicians and non-musicians: A diffusion tensor imaging study10.1016/S0304-3940(02)00054-X ↗
30. White Matter Microstructural Changes Following Quadrato Motor Training: A Longitudinal Study10.3389/fnhum.2017.00590 ↗
31. Short-Term Learning Induces White Matter Plasticity in the Fornix10.1523/JNEUROSCI.4520-12.2013 ↗
32. Weber, B., Koschutnig, K., Schwerdtfeger, A., Rominger, C., Papousek, I., Weiss, E.M., Tilp, M., and Fink, A. (2019). Learning Unicycling Evokes Manifold Changes in Gray and White Matter Networks Related to Motor and Cognitive Functions. Sci. Rep., 9.10.1038/s41598-019-40533-6 ↗
33. Altered structural plasticity in early adulthood after badminton training10.3724/SP.J.1041.2020.00173 ↗
34. Brain changes following four weeks of unimanual motor training: Evidence from fMRI-guided diffusion MRI tractography10.1002/hbm.23514 ↗
35. The adolescent brain10.1196/annals.1440.010 ↗
36. White matter connectivity and aerobic fitness in male adolescents10.1016/j.dcn.2013.11.003 ↗
37. Diffusion tensor imaging detects and differentiates axon and myelin degeneration in mouse optic nerve after retinal ischemia10.1016/j.neuroimage.2003.07.005 ↗
38. The relationship between BOLD fMRI response and the underlying white matter as measured by fractional anisotropy (FA): A systematic review10.1016/j.neuroimage.2016.12.075 ↗
39. Sex and Diffusion Tensor Imaging of White Matter in Schizophrenia: A Systematic Review Plus Meta-analysis of the Corpus Callosum10.1093/schbul/sbx049 ↗
40. Relationship between white matter integrity and post-traumatic cognitive deficits: A systematic review and meta-analysis10.1136/jnnp-2017-317691 ↗
41. Constrained by Our Connections: White Matter’s Key Role in Interindividual Variability in Visual Working Memory Capacity10.1523/JNEUROSCI.2317-14.2014 ↗
42. Maturation of white matter is associated with the development of cognitive functions during childhood10.1162/0898929041920441 ↗
43. Working Memory And Brain Tissue Microstructure: White Matter Tract Integrity Based On Multi-Shell Diffusion MRI10.1038/s41598-018-21428-4 ↗
44. Improving Children’s Coordinative Skills and Executive Functions: The Effects of a Football Exercise Program10.1177/0031512515627527 ↗
45. Motor and cognitive growth following a Football Training Program
46. Lind, R.R., Geertsen, S.S., Ørntoft, C., Madsen, M., Larsen, M.N., Dvorak, J., Ritz, C., and Krustrup, P. (2018). Improved cognitive performance in preadolescent Danish children after the school-based physical activity programme “FIFA 11 for Health” for Europe—A cluster-randomised controlled trial. Eur. J. Sport Sci.10.1080/17461391.2017.1394369 ↗
47. Chia-Liang, T., Pan, C.Y., Chen, F.C., and Yu-Ting, T. (2017). Open- and Closed-Skill Exercise Interventions Produce Different Neurocognitive Effects on Executive Functions in the Elderly: A 6-Month Randomized, Controlled Trial. Front. Aging Neurosci., 9.10.3389/fnagi.2017.00294 ↗
48. Zhu, H., Chen, A., Guo, W., Zhu, F., and Wang, B. (2020). Which Type of Exercise Is More Beneficial for Cognitive Function? A Meta-Analysis of the Effects of Open-Skill Exercise versus Closed-Skill Exercise among Children, Adults, and Elderly Populations. Appl. Sci., 10.10.3390/app10082737 ↗
49. Kai, P., Hkkinen, K., Santtila, M., Raitanen, J., and Kyrlinen, H. (2020). Differences in Training Adaptations of Endurance Performance during Combined Strength and Endurance Training in a 6-Month Crisis Management Operation. Int. J. Environ. Res. Public Health, 17.10.3390/ijerph17051688 ↗
50. Reliability of health-related physical fitness tests in European adolescents. The HELENA Study10.1038/ijo.2008.183 ↗
51. Hsu, C.C., Gu, M., Lee, T.S., and Lu, C.J. (2020). The Effects of Daily Sleep Condition on Performances of Physical Fitness among Taiwanese Adults: A Cross-Sectional Study. Int. J. Environ. Res. Public Health, 17.10.3390/ijerph17061907 ↗
52. The assessment and analysis of handedness: The Edinburgh inventory10.1016/0028-3932(71)90067-4 ↗
53. Raven, J., Court, J., and Raven, J. (1988). Raven’s Standard Progressive Matrices, Oxford Pyschologists Press Oxford.
54. Arrindell, W.A., and Ettema, J.H.M. (1986). SCL-90: Handleiding bij een Multidimensionele Psychopathologieindicator, Swets en Zeitlinger.
55. (2019, December 20). Notice of the General Office of the Ministry of Education on the Issuance of the “National Youth Campus Football Teaching Guide (Trial)” and the “Students Football Sports Skilled Grade Assessment Standard (Trial)”, Available online: http://www.moe.gov.cn/srcsite/A17/s7059/201607/t20160718_272137.html.
56. Effects of acute aerobic exercise on multiple aspects of executive function in preadolescent children10.1016/j.psychsport.2014.06.004 ↗
57. Neural Basis of Working Memory Enhancement after Acute Aerobic Exercise: fMRI Study of Preadolescent Children10.3389/fpsyg.2016.01804 ↗
58. Normative data on the n-back task for children and young adolescents10.3389/fpsyg.2015.01544 ↗
59. Fitness-Dependent Effect of Acute Aerobic Exercise on Executive Function
60. The Effects of Transcranial Direct Current Stimulation Versus Electroacupuncture on Working Memory in Healthy Subjects10.1089/acm.2018.0532 ↗
61. PANDA: A pipeline toolbox for analyzing brain diffusion images10.3389/fnhum.2013.00042 ↗
62. Tract probability maps in stereotaxic spaces: Analyses of white matter anatomy and tract-specific quantification10.1016/j.neuroimage.2007.07.053 ↗
63. Stereotaxic white matter atlas based on diffusion tensor imaging in an ICBM template10.1016/j.neuroimage.2007.12.035 ↗
64. Neurosurgery, and Radiology (2005). MRI Atlas of Human White Matter, Elsevier.
65. Reproducibility of quantitative tractography methods applied to cerebral white matter10.1016/j.neuroimage.2007.02.049 ↗
66. Brain Regions Related to Impulsivity Mediate the Effects of Early Adversity on Antisocial Behavior10.1016/j.biopsych.2015.12.027 ↗
67. Prefrontal gray matter volume mediates genetic risks for obesity10.1038/mp.2017.51 ↗
68. Mediation of the influence of childhood maltreatment on depression relapse by cortical structure: A 2-year longitudinal observational study10.1016/S2215-0366(19)30044-6 ↗
69. Associations Between Physical Fitness and Brain Structure in Young Adulthood10.3389/fpsyg.2020.608049 ↗
70. Fernandes, R.M., Correa, M.G., Santos, M.A.R.D., Almeida, A.P.C.P.S.C., Fagundes, N.C.F., Maia, L.C., and Lima, R.R. (2018). The Effects of Moderate Physical Exercise on Adult Cognition: A Systematic Review. Front. Physiol., 9.10.3389/fphys.2018.00667 ↗
71. Williams, R.A., Cooper, S.B., Dring, K.J., Hatch, L., and Nevill, M.E. (2020). Effect of football activity and physical fitness on information processing, inhibitory control and working memory in adolescents. BMC Public Health, 20.10.1186/s12889-020-09484-w ↗
72. Brain Training Games Enhance Cognitive Function in Healthy Subjects10.12659/MSMBR.909022 ↗
73. Emotional and cognitive reinforcement of rat hippocampal long-term potentiation by different learning paradigms10.1017/S1740925X05000153 ↗
74. Information processing speed, neural efficiency, and working memory performance in multiple sclerosis: Differential relationships with structural magnetic resonance imaging10.1080/13803395.2011.614597 ↗
75. Temporal Aspects of Memory: A Comparison of Memory Performance, Processing Speed and Time Estimation Between Young and Older Adults10.3389/fnagi.2018.00352 ↗
76. Nouchi, R., Taki, Y., Takeuchi, H., Hashizume, H., Akitsuki, Y., Shigemune, Y., Sekiguchi, A., Kotozaki, Y., Tsukiura, T., and Yomogida, Y. (2012). Brain training game improves executive functions and processing speed in the elderly: A randomized controlled trial. PLoS ONE, 7.10.1371/journal.pone.0029676 ↗
77. Acute and chronic effect of physical activity on cognition and behaviour in young people with ADHD: A systematic review of intervention studies10.1016/j.ridd.2018.03.015 ↗
78. Rough-and-tumble play and the development of the social brain10.1111/j.1467-8721.2007.00483.x ↗
79. Diffusion tensor imaging of the brain10.1016/j.nurt.2007.05.011 ↗
80. Ruotsalainen, I., Gorbach, T., Perkola, J., Renvall, V., and Parviainen, T. (2020). Physical activity, aerobic fitness, and brain white matter: Their role for executive functions in adolescence. Dev. Cogn. Neurosci.10.1101/674846 ↗
81. Aerobic Exercise Intervention Alters Executive Function and White Matter Integrity in Deaf Children: A Randomized Controlled Study
82. White matter microstructure changes induced by motor skill learning utilizing a body machine interface10.1016/j.neuroimage.2013.10.066 ↗
83. White Matter Development in Adolescence: A DTI Study10.1093/cercor/bhp282 ↗
84. Life-Span Changes of the Human Brain White Matter: Diffusion Tensor Imaging (DTI) and Volumetry10.1093/cercor/bhp280 ↗
85. Lebel, C., Treit, S., and Beaulieu, C. (2017). A review of diffusion MRI of typical white matter development from early childhood to young adulthood. NMR Biomed., e3778.10.1002/nbm.3778 ↗
86. White matter microstructure mediates the association between physical fitness and cognition in healthy, young adults10.1038/s41598-019-49301-y ↗
88. Meta-analyses of the n-back working memory task: fMRI evidence of age-related changes in prefrontal cortex involvement across the adult lifespan10.1016/j.neuroimage.2019.03.074 ↗
89. Positive correlations between corpus callosum thickness and intelligence10.1016/j.neuroimage.2007.06.028 ↗
90. Cerebral white matter and cognition in hydrocephalic children10.1001/archneur.1992.00530320042010 ↗
91. General fluid-type intelligence is related to indices of white matter structure in middle-aged and old adults10.1016/j.neuroimage.2013.06.040 ↗
92. Brain white matter structure and information processing speed in healthy older age10.1007/s00429-015-1097-5 ↗
93. White matter microstructure mediates the relationship between cardiorespiratory fitness and spatial working memory in older adults10.1016/j.neuroimage.2015.09.053 ↗
94. Socioeconomic status is positively correlated with frontal white matter integrity in aging10.1007/s11357-012-9493-8 ↗
95. Aging white matter and cognition: Differential effects of regional variations in diffusion properties on memory, executive functions, and speed10.1016/j.neuropsychologia.2009.01.001 ↗
96. Krogsrud, S.K., Fjell, A.M., Tamnes, C.K., Grydeland, H., Due-Tonnessen, P., Bjornerud, A., Sampaio-Baptista, C., Andersson, J., Johansen-Berg, H., and Walhovd, K.B. (2018). Development of white matter microstructure in relation to verbal and visuospatial working memory-A longitudinal study. PLoS ONE, 13.10.1371/journal.pone.0195540 ↗
97. Morphometry and connectivity of the fronto-parietal verbal working memory network in development10.1016/j.neuropsychologia.2011.10.001 ↗
98. White matter microstructure in superior longitudinal fasciculus associated with spatial working memory performance in children10.1162/jocn.2010.21592 ↗
99. Object working memory performance depends on microstructure of the frontal-occipital fasciculus10.1089/brain.2011.0037 ↗