Learning to play badminton altered resting-state activity and functional connectivity of the cerebellar sub-regions in adults
Autoři:
Mengling Shao aff001; Huiyan Lin aff002; Desheng Yin aff001; Yongjie Li aff001; Yifan Wang aff001; Junpeng Ma aff001; Jianzhong Yin aff003; Hua Jin aff001
Působiště autorů:
Key Research Base of Humanities and Social Sciences of the Ministry of Education, Center of Cooperative Innovation for Assessment and Promotion of National Mental Health, Academy of Psychology and Behavior, Tianjin Normal University, Tianjin, China
aff001; Institute of Applied Psychology, School of Public Administration, Guangdong University of Finance, Guangzhou, China
aff002; Department of Radiology, Tianjin First Center Hospital, Tianjin, China
aff003
Vyšlo v časopise:
PLoS ONE 14(10)
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pone.0223234
Souhrn
Previous studies have shown that sport experts are different from novices in functions and structures of the cerebellar sub-regions and the functional connectivity (FC) associated with the cerebellum, suggesting the role of the cerebellum on motor skill learning (MSL). However, the manipulation of individuals with different motor skills fails to exclude the effects of innate talents. In addition, individuals with higher motor skills often start with the MSL in their young ages. It is still unclear whether the effects regarding the cerebellum would be shown at one’s adult age. The present study was to directly alter individuals’ motor skills to investigate whether MSL (taking learning to play badminton as an example) in adulthood influences resting-state activity in the cerebellum. To this end, young adults without ball training experience were recruited as participants and were assigned randomly into the experimental group and the control group. Participants in the experimental group were asked to attend a badminton training course for 12 weeks, while the control group did not regularly attend any ball sports during this period. Resting-state functional magnetic resonance imaging (fMRI) was recorded before and after the training. Results showed that compared to the control group, the experimental group had smaller amplitude of low-frequency fluctuation (ALFF) in right cerebellar hemispheric VI and left VIII after training. For the experimental group, right hemispheric VIII had a stronger FC with left hemispheric IV-V, cerebellar vermal IX, left middle cingulate gyrus and right hippocampus after training. Taken together, these findings suggested that MSL, at least learning to play badminton in adulthood, reduces resting-state activity in different sub-regions in the cerebellum but increases FC between sub-regions of the cerebellum as well as between sub-regions of the cerebellum and cerebral cortices (e.g., middle cingulate cortex and hippocampus).
Klíčová slova:
Learning – Cognition – Functional magnetic resonance imaging – Sports – Hippocampus – Brainstem – Eye movements – Cerebellum
Zdroje
1. Schmahmann JD, Doyon J, McDonald D, Holmes C, Lavoie K, Hurwitz AS, et al. Three-dimensional MRI atlas of the human cerebellum in proportional stereotaxic space. Neuroimage. 1999; 10: 233–260. https://doi.org/10.1006/nimg.1999.0459 10458940
2. Imamizu H, Miyauchi S, Tamada T, Sasaki Y, Takino R, PuÈtz B, et al. Human cerebellar activity reflecting an acquired internal model of a new tool. Nature. 2000; 403: 192–195. http://doi.org/10.1038/35003194 10646603
3. Ito M. Mechanisms of motor learning in the cerebellum. Brain research. 2000; 886: 237–245. https://doi.org/10.1016/S0006-8993(00)03142-5 11119699
4. Miall RC, Reckess GZ, Imamizu H. The cerebellum coordinates eye and hand tracking movements. Nature neuroscience. 2001; 4: 638–644. https://doi.org/10.1038/88465 11369946
5. Doyon J, Penhune V, Ungerleider LG. Distinct contribution of the cortico-striatal and cortico-cerebellar systems to motor skill learning. Neuropsychologia. 2003; 41: 252–262. https://doi.org/10.1016/S0028-3932(02)00158-6 12457751
6. Doyon J, Song AW, Karni A, Lalonde F, Adams MM, Ungerleider LG. Experience-dependent changes in cerebellar contributions to motor sequence learning. Proceedings of the National Academy of Sciences. 2002; 99: 1017–1022. https://doi.org/10.1073/pnas.022615199 11805340
7. Grodd W, Hülsmann E, Lotze M, Wildgruber D, Erb M. Sensorimotor mapping of the human cerebellum: fMRI evidence of somatotopic organization. Human brain mapping. 2001; 13: 55–73. https://doi.org/10.1002/hbm.1025 11346886
8. Stoodley CJ, Valera EM, Schmahmann JD. Functional topography of the cerebellum for motor and cognitive tasks: an fMRI study. Neuroimage. 2012; 59: 1560–1570. https://doi.org/10.1016/j.neuroimage.2011.08.065 21907811
9. Wang C, Kipping J, Bao C, Ji H, Qiu A. Cerebellar functional parcellation using sparse dictionary learning clustering. Frontiers in neuroscience. 2016; 10: 188. https://doi.org/10.3389/fnins.2016.00188 27199650
10. Sang L, Qin W, Liu Y, Han W, Zhang Y, Jiang T, et al. Resting-state functional connectivity of the vermal and hemispheric subregions of the cerebellum with both the cerebral cortical networks and subcortical structures. Neuroimage. 2012; 61: 1213–1225. https://doi.org/10.1016/j.neuroimage.2012.04.011 22525876
11. Habas C, Kamdar N, Nguyen D, Prater K, Beckmann CF, Menon V, et al. Distinct cerebellar contributions to intrinsic connectivity networks. Journal of neuroscience. 2009; 29: 8586–8594. https://doi.org/10.1523/JNEUROSCI.1868-09.2009 19571149
12. Schlerf JE, Verstynen TD, Ivry RB, Spencer RM. Evidence of a novel somatopic map in the human neocerebellum during complex actions. Journal of neurophysiology. 2010; 103: 3330–3336. https://doi.org/10.1152/jn.01117.2009 20393055
13. Alahmadi AA, Pardini M, Samson RS, Friston KJ, Toosy AT, D’angelo E, et al. Cerebellar lobules and dentate nuclei mirror cortical force‐related‐BOLD responses: Beyond all (linear) expectations. Human brain mapping. 2017; 38: 2566–2579. https://doi.org/10.1002/hbm.23541 28240422
14. Vahedi K, Rivaud S, Amarenco P, Pierrot-Deseilligny C. Horizontal eye movement disorders after posterior vermis infarctions. Journal of Neurology Neurosurgery & Psychiatry. 1995; 58: 91–94.
15. Grimaldi G, Manto M. Topography of cerebellar deficits in humans. The Cerebellum. 2012; 11: 336–351. https://doi.org/10.1007/s12311-011-0247-4 21240580
16. Park IS, Lee NJ, Rhyu IJ. Roles of the Declive, Folium, and Tuber Cerebellar Vermian Lobules in Sportspeople. Journal of Clinical Neurology. 2018; 14: 1–7. https://doi.org/10.3988/jcn.2018.14.1.1 29141275
17. Jacini WF, Cannonieri GC, Fernandes PT, Bonilha L, Cendes F, Li LM. Can exercise shape your brain? cortical differences associated with judo practice. Journal of Science and Medicine in Sport. 2009; 12: 688–690. https://doi.org/10.1016/j.jsams.2008.11.004 19147406
18. Di X, Zhu S, Jin H, Wang P, Ye Z, Zhou K, et al. Altered resting brain function and structure in professional badminton players. Brain Connectivity. 2012; 2: 225–233. https://doi.org/10.1089/brain.2011.0050 22840241
19. Park IS, Lee KJ, Han JW, Lee NJ, Lee WT, Park KA, et al. Experience-dependent plasticity of cerebellar vermis in basketball players. The Cerebellum. 2009; 8: 334–339. doi: 10.1007/s12311-009-0100-1 19259755
20. Park IS, Ye NL, Kwon S, Lee NJ, Rhyu IJ. White matter plasticity in the cerebellum of elite basketball athletes. Anatomy and Cell Biology. 2016; 48: 262–267. https://doi.org/10.5115/abc.2015.48.4.262 26770877
21. Kim W, Chang Y, Kim J, Seo J, Ryu K, Lee E, et al. An fMRI study of differences in brain activity among elite, expert, and novice archers at the moment of optimal aiming. Cognitive and Behavioral Neurology. 2014; 27: 173–182. doi: 10.1097/WNN.0000000000000042 25539036
22. Olsson CJ, Jonsson B, Larsson A, Nyberg L. Motor representations and practice affect brain systems underlying imagery: an fMRI study of internal imagery in novices and active high jumpers. Open Neuroimaging Journal. 2008; 2: 5–13. https://doi.org/10.2174/1874440000802010005 19018312
23. Wang J, Lu M, Fan Y, Wen X, Zhang R, Wang B, et al. Exploring brain functional plasticity in world class gymnasts: a network analysis. Brain Structure and Function. 2016; 221: 3503–3519. https://doi.org/10.1007/s00429-015-1116-6 26420277
24. Kim JH, Han JK, Kim BN, Han DH. Brain networks governing the golf swing in professional golfers. Journal of Sports Sciences. 2015; 33: 1980–1987. https://doi.org/10.1080/02640414.2015.1022570 25761601
25. Ma L, Narayana S, Robin DA, Fox PT, Xiong J. Changes occur in resting state network of motor system during 4 weeks of motor skill learning. Neuroimage. 2011; 58(1): 226–33. https://dor.org/10.1016/j.neuroimage.2011.06.014 21689765
26. Meylan C, Cronin J, Oliver J, Hughes M. Talent identification in soccer: The role of maturity status on physical, physiological and technical characteristics. International Journal of Sports Science & Coaching. 2010; 5: 571–592. https://doi.org/10.1260/1747-9541.5.4.571
27. Werkiani ME, Zakizadeh B, Feizabadi MS, Golsefidi FN, Rahimi M. Review of the effective talent identification factors of badminton for better teaching to success. Procedia—Social and Behavioral Sciences. 2012; 31: 834–836. https://doi.org/10.1016/j.sbspro.2011.12.151
28. Woods CT, Banyard HG, McKeown I, Fransen J, Robertson S. Discriminating talent identified junior Australian footballers using a fundamental gross athletic movement assessment. Journal of sports science & medicine. 2016; 15: 548. 27803635
29. Müller RA, Behen ME, Rothermel RD, Muzik O, Chakraborty PK, Chugani HT. Brain organization for language in children, adolescents, and adults with left hemisphere lesion: a PET study. Progress in Neuro-Psychopharmacology and Biological Psychiatry. 1999; 23: 657–668. https://doi.org/10.1016/S0278-5846(99)00024-X 10390724
30. Haslinger B, Erhard P, Altenmüller E, Hennenlotter A, Schwaiger M, Gräfin von Einsiedel H, et al. Reduced recruitment of motor association areas during bimanual coordination in concert pianists. Human brain mapping. 2004; 22: 206–215. https://doi.org/10.1002/hbm.20028 15195287
31. Sacco K, Cauda F, Cerliani L, Mate D, Duca S, Geminiani GC. Motor imagery of walking following training in locomotor attention. The effect of ‘the tango lesson’. Neuroimage. 2006; 32: 1441–1449. https://doi.org/10.1016/j.neuroimage.2006.05.018 16861008
32. Bernardi G, Ricciardi E, Sani L, Gaglianese A, Papasogli A, Ceccarelli R, et al. How skill expertise shapes the brain functional architecture: an fMRI study of visuo-spatial and motor processing in professional racing-car and naïve drivers. Plos One. 2013; 8: e77764. https://doi.org/10.1371/journal.pone.0077764 24204955
33. Logothetis NK, Pauls J, Augath M, Trinath T, Oeltermann A. Neurophysiological investigation of the basis of the fMRI signal. Nature. 2001; 412: 150. https://doi.org/10.1038/35084005 11449264
34. Zang Y, He Y, Zhu C, Cao Q, Sui M, Liang M. Altered baseline brain activity in children with ADHD revealed by resting-state functional MRI. Brain and Development. 2007; 29: 83–91. https://doi.org/10.1016/j.BRAINDEV.2006.07.002 16919409
35. Biswal B, Yetkin FZ, Haughton VM, Hyde JS. Functional connectivity in the motor cortex of resting human brain using echo‐planar MRI. Magnetic resonance in medicine. 1995; 34: 537–541. doi: 10.1002/mrm.1910340409 8524021
36. Damoiseaux JS, Rombouts SARB, Barkhof F, Scheltens P, Stam CJ, Smith SM, et al. Consistent resting-state networks across healthy subjects. Proceedings of the national academy of sciences. 2006; 103: 13848–13853. https://doi.org/10.1073/pnas.0601417103 16945915
37. Smith SM, Fox PT, Miller KL, Glahn DC, Fox PM, Mackay CE, et al. Correspondence of the brain’s functional architecture during activation and rest. Proceedings of the National Academy of Sciences. 2009; 106: 13040–13045. https://doi.org/10.1073/pnas.0905267106 19620724
38. Oldfield RC. The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia. 1971; 9: 97–113. https://doi.org/10.1016/0028-3932(71)90067-4c 5146491
39. Chapman SB, Aslan S, Spence JS, DeFina LF, Keebler MW, Didehbani N, et al. Shorter term aerobic exercise improves brain, cognition, and cardiovascular fitness in aging. Frontiers in Aging Neuroscience. 2013; 5: 1–9. https://doi.org/10.3389/fnagi.2013.00075
40. Nishiguchi S, Yamada M, Tanigawa T, Sekiyama K, Kawagoe T, Suzuki M, et al. A 12-Week Physical and Cognitive Exercise Program Can Improve Cognitive Function and Neural Efficiency in Community-Dwelling Older Adults: A Randomized Controlled Trial. The American Geriatrics Society. 2015; 63(7): 1355–63. http://doi.wiley.com/10.1111/jgs.13481
41. Yan CG, Wang XD, Zuo XN, Zang YF. Dpabi: data processing & analysis for (resting-state) brain imaging. Neuroinformatics. 2016; 14: 339–351. doi: 10.1007/s12021-016-9299-4 27075850
42. Tzourio-Mazoyer N, Landeau B, Papathanassiou D, Crivello F, Etard O, Delcroix N, et al. Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain. Neuroimage. 2002; 15: 273–289. https://doi.org/10.1006/nimg.2001.0978 11771995
43. Friston KJ, Frith CD, Liddle PF, Frackowiak RS. Functional connectivity: the principal-component analysis of large (PET) data sets. Journal of Cerebral Blood Flow & Metabolism Official Journal of the International Society of Cerebral Blood Flow & Metabolism. 1993; 13: 5–14. https://doi.org/10.1038/jcbfm.1993.4
44. Kumaran D, Maguire EA. The human hippocampus: cognitive maps or relational memory?. Journal of Neuroscience. 2005; 25: 7254–7259. https://doi.org/10.1523/JNEUROSCI.1103-05.2005 16079407
45. Wright MJ, Bishop DT, Jackson RC, Abernethy B. Cortical fMRI activation to opponents’ body kinematics in sport-related anticipation: expert-novice differences with normal and point-light video. Neuroscience letters. 2011; 500: 216–221. https://doi.org/10.1016/j.neulet.2011.06.045 21741450
46. Abreu AM, Macaluso E, Azevedo RT, Cesari P, Urgesi C, Aglioti SM. Action anticipation beyond the action observation network: a functional magnetic resonance imaging study in expert basketball players. European Journal of Neuroscience. 2012; 35: 1646–1654. https://doi.org/10.1111/j.1460-9568.2012.08104.x 22541026
47. Bishop DT, Wright MJ, Jackson RC, Abernethy B. Neural bases for anticipation skill in soccer: an fMRI study. Journal of Sport and Exercise Psychology. 2013; 35: 98–109. https://doi.org/10.1123/jsep.35.1.98 23404883
48. Wimshurst ZL, Sowden PT, Wright M. Expert–novice differences in brain function of field hockey players. Neuroscience. 2016; 315: 31–44. https://dor.org/10.1016/j.neuroscience.2015.11.064 26674059
Článok vyšiel v časopise
PLOS One
2019 Číslo 10
- Metamizol jako analgetikum první volby: kdy, pro koho, jak a proč?
- Nejasný stín na plicích – kazuistika
- Masturbační chování žen v ČR − dotazníková studie
- Těžké menstruační krvácení může značit poruchu krevní srážlivosti. Jaký management vyšetření a léčby je v takovém případě vhodný?
- Fixní kombinace paracetamol/kodein nabízí synergické analgetické účinky
Najčítanejšie v tomto čísle
- Correction: Low dose naltrexone: Effects on medication in rheumatoid and seropositive arthritis. A nationwide register-based controlled quasi-experimental before-after study
- Combining CDK4/6 inhibitors ribociclib and palbociclib with cytotoxic agents does not enhance cytotoxicity
- Experimentally validated simulation of coronary stents considering different dogboning ratios and asymmetric stent positioning
- Risk factors associated with IgA vasculitis with nephritis (Henoch–Schönlein purpura nephritis) progressing to unfavorable outcomes: A meta-analysis