How aerobic exercise improves executive function in ADHD children: A resting-state fMRI study.

Kaihua Jiang, Yue Xu, Yamin Li, Lin Li, Mingmei Yang, Peng Xue
Author Information
  1. Kaihua Jiang: Department of Pediatrics, Changzhou Children's Hospital of Nantong University, Changzhou, China. ORCID
  2. Yue Xu: Department of Pediatrics, Changzhou Children's Hospital of Nantong University, Changzhou, China.
  3. Yamin Li: Department of Pediatrics, Changzhou Children's Hospital of Nantong University, Changzhou, China.
  4. Lin Li: Department of Pediatrics, Changzhou Children's Hospital of Nantong University, Changzhou, China.
  5. Mingmei Yang: Department of Pediatrics, Changzhou Children's Hospital of Nantong University, Changzhou, China.
  6. Peng Xue: Department of Pediatrics, Changzhou Children's Hospital of Nantong University, Changzhou, China.

Abstract

The aim of the study is to explore the functional magnetic resonance imaging (fMRI) characteristics of the improvement in executive function by aerobic exercise in children with attention deficit hyperactivity disorder (ADHD). Seventeen children with ADHD were selected for 8 weeks of rope skipping aerobic training, and fMRI findings and executive function were examined before and after training. Regional homogeneity (ReHo) and degree centrality (DC) indexes were used in fMRI analysis, whereas the flanker task was used to test executive function. A paired t test was used to compare the fMRI indexes and response time of executive function before and after training. After aerobic exercise, the brain regions in which the ReHo value of ADHD children significantly increased included the left middle frontal gyrus and the right superior frontal gyrus; the brain region in which the DC value increased was the right posterior cingulate cortex. The flanker task response time decreased significantly (P < 0.05, after correction) after aerobic exercise. The study findings support the hypothesis that aerobic exercise can improve the executive function of ADHD children, and the brain mechanism involved is mainly related to the enhancement of spontaneous prefrontal lobe activity.

Keywords

References

  1. Benzing, V., & Schmidt, M. (2019). The effect of exergaming on executive functions in children with ADHD: A randomized clinical trial. Scandinavian Journal of Medicine & Science in Sports, 29(8), 1243-1253. https://doi.org/10.1111/sms.13446
  2. Cará, V. M., Esper, N. B., de Azeredo, L. A., Iochpe, V., Dalfovo, N. P., Santos, R. C., Sanvicente-Vieira, B., Grassi-Oliveira, R., Franco, A. R., & Buchweitz, A. (2019). An fMRI study of inhibitory control and the effects of exposure to violence in Latin-American early adolescents: Alterations in frontoparietal activation and performance. Social Cognitive and Affective Neuroscience, 14(10), 1097-1107. https://doi.org/10.1093/scan/nsz092
  3. Caye, A., Swanson, J. M., Coghill, D., & Rohde, L. A. (2019). Treatment strategies for ADHD: An evidence-based guide to select optimal treatment. Molecular Psychiatry, 24(3), 390-408. https://doi.org/10.1038/s41380-018-0116-3
  4. Chang, Y. K., Chen, F. T., Kuan, G., Wei, G. X., Chu, C. H., Yan, J., Chen, A. G., & Hung, T. M. (2019). Effects of acute exercise duration on the inhibition aspect of executive function in late middle-aged adults. Frontiers in Aging Neuroscience, 11, 227. https://doi.org/10.3389/fnagi.2019.00227
  5. Chen, A. G., Yan, J., Yin, H. C., Pan, C. Y., & Chang, Y. K. (2014). Effects of acute aerobic exercise on multiple aspects of executive function in preadolescent children. Psychology of Sport and Exercise, 15, 627-636. https://doi.org/10.1016/j.psychsport.2014.06.004
  6. Choi, J. W., Han, D. H., Kang, K. D., Jung, H. Y., & Renshaw, P. F. (2015). Aerobic exercise and attention deficit hyperactivity disorder: Brain research. Medicine and Science in Sports and Exercise, 47(1), 33-39. https://doi.org/10.1249/MSS.0000000000000373
  7. Collette, F., & Van der Linden, M. (2002). Brain imaging of the central executive component of working memory. Neuroscience and Biobehavioral Reviews, 26(2), 105-125. https://doi.org/10.1016/S0149-7634(01)00063-X
  8. Diamond, A. (2020). Executive functions. Handbook of Clinical Neurology, 173, 225-240. https://doi.org/10.1016/B978-0-444-64150-2.00020-4
  9. Fuster, J. M. (2019). The prefrontal cortex in the neurology clinic. Handbook of Clinical Neurology, 163, 3-15. https://doi.org/10.1016/B978-0-12-804281-6.00001-X
  10. Golestani, A. M., Kwinta, J. B., Khatamian, Y. B., & Chen, J. J. (2017). The effect of low-frequency physiological correction on the reproducibility and specificity of resting-state fMRI metrics: Functional connectivity, ALFF, and ReHo. Frontiers in Neuroscience, 11, 546. https://doi.org/10.3389/fnins.2017.00546
  11. Huang, C. J., Huang, C. W., Tsai, Y. J., Tsai, C. L., Chang, Y. K., & Hung, T. M. (2017). A preliminary examination of aerobic exercise effects on resting EEG in children with ADHD. Journal of Attention Disorders, 21(11), 898-903. https://doi.org/10.1177/1087054714554611
  12. Hung, C. L., Huang, C. J., Tsai, Y. J., Chang, Y. K., & Hung, T. M. (2016). Neuroelectric and behavioral effects of acute exercise on task switching in children with attention-deficit/hyperactivity disorder. Frontiers in Psychology, 7, 1589. https://doi.org/10.3389/fpsyg.2016.01589
  13. Jiang, X., Liu, L., Ji, H., & Zhu, Y. (2018). Association of affected neurocircuitry with deficit of response inhibition and delayed gratification in attention deficit hyperactivity disorder: A narrative review. Frontiers in Human Neuroscience, 12, 506. https://doi.org/10.3389/fnhum.2018.00506
  14. Kuss, D. J., Pontes, H. M., & Griffiths, M. D. (2018). Neurobiological correlates in internet gaming disorder: A systematic literature review. Frontiers in Psychiatry, 9, 166. https://doi.org/10.3389/fpsyt.2018.00166
  15. Li, L., Su, Y. A., Wu, Y. K., Castellanos, F. X., Li, K., Li, J. T., Si, T. M., & Yan, C. G. (2021). Eight-week antidepressant treatment reduces functional connectivity in first-episode drug-naïve patients with major depressive disorder. Human Brain Mapping, 42(8), 2593-2605. https://doi.org/10.1002/hbm.25391
  16. Li, L., Zhang, S., Cui, J., Chen, L. Z., Wang, X., Fan, M., & Wei, G. X. (2019). Fitness-dependent effect of acute aerobic exercise on executive function. Frontiers in Physiology, 10, 902. https://doi.org/10.3389/fphys.2019.00902
  17. McGrath, J. (2020). ADHD and Covid-19: Current roadblocks and future opportunities. Irish Journal of Psychological Medicine, 37(3), 204-211. https://doi.org/10.1017/ipm.2020.53
  18. Mehren, A., Özyurt, J., Lam, A. P., Brandes, M., Müller, H., Thiel, C. M., & Philipsen, A. (2019). Acute effects of aerobic exercise on executive function and attention in adult patients with ADHD. Frontiers in Psychiatry, 10, 132. https://doi.org/10.3389/fpsyt.2019.00132
  19. Miklós, M., Futó, J., Komáromy, D., & Balázs, J. (2019). Executive function and attention performance in children with ADHD: Effects of medication and comparison with typically developing children. International Journal of Environmental Research and Public Health, 16(20), 3822. https://doi.org/10.3390/ijerph16203822
  20. Moehlman, T. M., de Zwart, J. A., Chappel-Farley, M. G., Liu, X., McClain, I. B., Chang, C., Mandelkow, H., Özbay, P. S., Johnson, N. L., Bieber, R. E., Fernandez, K. A., King, K. A., Zalewski, C. K., Brewer, C. C., van Gelderen, P., Duyn, J. H., & Picchioni, D. (2019). All-night functional magnetic resonance imaging sleep studies. Journal of Neuroscience Methods, 316, 83-98. https://doi.org/10.1016/j.jneumeth.2018.09.019
  21. Pineda-Alhucema, W., Aristizabal, E., Escudero-Cabarcas, J., Acosta-López, J. E., & Vélez, J. I. (2018). Executive function and theory of mind in children with ADHD: A systematic review. Neuropsychology Review, 28(3), 341-358. https://doi.org/10.1007/s11065-018-9381-9
  22. Shaw, P., Greenstein, D., Lerch, J., Clasen, L., Lenroot, R., Gogtay, N., Evans, A., Rapoport, J., & Giedd, J. (2006). Intellectual ability and cortical development in children and adolescents. Nature, 440(7084), 676-679. https://doi.org/10.1038/nature04513
  23. Shuai, L., Daley, D., Wang, Y. F., Zhang, J. S., Kong, Y. T., Tan, X., & Ji, N. (2017). Executive function training for children with attention deficit hyperactivity disorder. Chinese Medical Journal, 130(5), 549-558. https://doi.org/10.4103/0366-6999.200541
  24. Shum, K. K., Zheng, Q., Chak, G. S., Kei, K. T., Lam, C. W., Lam, I. K., Lok, C., & Tang, J. W. (2021). Dimensional structure of the BRIEF2 and its relations with ADHD symptoms and task performance on executive functions in Chinese children. Child Neuropsychology: A Journal on Normal and Abnormal Development in Childhood and Adolescence, 27(2), 165-189. https://doi.org/10.1080/09297049.2020.1817355
  25. Tsujii, N., Mikawa, W., Tsujimoto, E., Adachi, T., Niwa, A., Ono, H., & Shirakawa, O. (2017). Reduced left precentral regional responses in patients with major depressive disorder and history of suicide attempts. PLoS ONE, 12(4), e0175249. https://doi.org/10.1371/journal.pone.0175249
  26. Wang, L. J., Yang, C. Y., Chou, W. J., Lee, M. J., Chou, M. C., Kuo, H. C., Yeh, Y. M., Lee, S. Y., Huang, L. H., & Li, S. C. (2020). Gut microbiota and dietary patterns in children with attention-deficit/hyperactivity disorder. European Child & Adolescent Psychiatry, 29(3), 287-297. https://doi.org/10.1007/s00787-019-01352-2
  27. Wang, J. B., Zheng, L. J., Cao, Q. J., Wang, Y. F., Sun, L., Zang, Y. F., & Zhang, H. (2017). Inconsistency in abnormal brain activity across cohorts of ADHD-200 in children with attention deficit hyperactivity disorder. Frontiers in Neuroscience, 11, 320. https://doi.org/10.3389/fnins.2017.00320
  28. Wu, K., Liu, M., He, L., & Tan, Y. (2020). Abnormal degree centrality in delayed encephalopathy after carbon monoxide poisoning: A resting-state fMRI study. Neuroradiology, 62(5), 609-616. https://doi.org/10.1007/s00234-020-02369-0
  29. Xiong, X., Zhu, L. N., Dong, X. X., Wang, W., Yan, J., & Chen, A. G. (2018). Aerobic exercise intervention alters executive function and white matter integrity in deaf children: A randomized controlled study. Neural Plasticity, 2018, 1-8, 3735208. https://doi.org/10.1155/2018/3735208
  30. Yan, C. G., Wang, X. D., Zuo, X. N., & Zang, Y. F. (2016). DPABI: Data processing & analysis for (resting-state) brain imaging. Neuroinformatics, 14, 339-351. https://doi.org/10.1007/s12021-016-9299-4
  31. Yuan, B. K., Zang, Y. F., & Liu, D. Q. (2016). Influences of head motion regression on high-frequency oscillation amplitudes of resting-state fMRI signals. Frontiers in Human Neuroscience, 10, 243. https://doi.org/10.3389/fnhum.2016.00243

Grants

  1. CJ20200081/Science and Technology Program of Basic Applying of Changzhou

MeSH Term

Attention Deficit Disorder with Hyperactivity
Brain
Brain Mapping
Child
Executive Function
Exercise
Humans
Magnetic Resonance Imaging

Word Cloud

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