Abstract
Long-term motor skill learning can induce plastic structural and functional reorganization of the brain. Our previous studies detected brain structural plasticity related to long-term intensive gymnastic training in world class gymnasts (WCGs). The goal of this study was to investigate brain functional plasticity in WCGs by using network measures of brain functional networks. Specifically, we acquired resting-state fMRI data from 13 WCGs and 14 controls, constructed their brain functional networks, and compared the differences in their network parameters. At the whole brain level, we detected significantly decreased overall functional connectivity (FC) and decreased local and global efficiency in the WCGs compared to the controls. At the modular level, we found intra- and inter-modular reorganization in three modules, the cerebellum, the cingulo-opercular and fronto-parietal networks, in the WCGs. On the nodal level, we revealed significantly decreased nodal strength and efficiency in several non-rich club regions of these three modules in the WCGs. These results suggested that functional plasticity can be detected in the brain functional networks of WCGs, especially in the cerebellum, fronto-parietal network, and cingulo-opercular network. In addition, we found that the FC between the fronto-parietal network and the sensorimotor network was significantly negatively correlated with the number of years of training in the WCGs. These findings may help us to understand the outstanding gymnastic performance of the gymnasts and to reveal the neural mechanisms that distinguish WCGs from controls.
Similar content being viewed by others
References
Albert NB, Robertson EM, Miall RC (2009) The resting human brain and motor learning. Curr Biol 19(12):1023–1027
Aoki Y, Cortese S, Tansella M (2015) Neural bases of atypical emotional face processing in autism: a meta-analysis of fMRI studies. World J Biol Psychiatry 16(5):291–300
Ashby FG, Turner BO, Horvitz JC (2010) Cortical and basal ganglia contributions to habit learning and automaticity. Trends Cogn Sci 14(5):208–215
Bernardi G, Ricciardi E, Sani L, Gaglianese A, Papasogli A, Ceccarelli R, Franzoni F, Galetta F, Santoro G, Goebel R, Pietrini P (2013) How skill expertise shapes the brain functional architecture: an fMRI study of visuo-spatial and motor processing in professional racing-car and naive drivers. Plos One 8(10):e77764
Braun U, Plichta MM, Esslinger C, Sauer C, Haddad L, Grimm O, Mier D, Mohnke S, Heinz A, Erk S, Walter H, Seiferth N, Kirsch P, Meyer-Lindenberg A (2012) Test-retest reliability of resting-state connectivity network characteristics using fMRI and graph theoretical measures. Neuroimage 59(2):1404–1412
Charlesworth JD, Warren TL, Brainard MS (2012) Covert skill learning in a cortical-basal ganglia circuit. Nature 486(7402):251–255
Cohen J (1992) A power primer. Psychol Bull 112(1):155–159
Cole MW, Reynolds JR, Power JD, Repovs G, Anticevic A, Braver TS (2013) Multi-task connectivity reveals flexible hubs for adaptive task control. Nat Neurosci 16(9):1348–1355
Collin G, Kahn RS, de Reus MA, Cahn W, van den Heuvel MP (2014a) Impaired rich club connectivity in unaffected siblings of schizophrenia patients. Schizophr Bull 40(2):438–448
Collin G, Sporns O, Mandl RC, van den Heuvel MP (2014b) Structural and functional aspects relating to cost and benefit of rich club organization in the human cerebral cortex. Cereb Cortex 24(9):2258–2267
Corbetta M, Shulman GL (2002) Control of goal-directed and stimulus-driven attention in the brain. Nat Rev Neurosci 3(3):201–215
Coynel D, Marrelec G, Perlbarg V, Pélégrini-Issac M, Van de Moortele PF, Ugurbil K, Doyon J, Benali H, Lehéricy S (2010) Dynamics of motor-related functional integration during motor sequence learning. Neuroimage 49(1):759–776
Cruse D, Chennu S, Chatelle C, Bekinschtein TA, Fernandez-Espejo D, Pickard JD, Laureys S, Owen AM (2011) Bedside detection of awareness in the vegetative state: a cohort study. Lancet 378(9809):2088–2094
Dayan E, Cohen LG (2011) Neuroplasticity subserving motor skill learning. Neuron 72(3):443–454
de Reus MA, van den Heuvel MP (2013a) The parcellation-based connectome: limitations and extensions. Neuroimage 80:397–404
de Reus MA, van den Heuvel MP (2013b) Rich club organization and intermodule communication in the cat connectome. J Neurosci 33(32):12929–12939
Desco M, Hernandez JA, Santos A, Brammer M (2001) Multiresolution analysis in fMRI: sensitivity and specificity in the detection of brain activation. Hum Brain Mapp 14(1):16–27
Deuker L, Bullmore ET, Smith M, Christensen S, Nathan PJ, Rockstroh B, Bassett DS (2009) Reproducibility of graph metrics of human brain functional networks. Neuroimage 47(4):1460–1468
Di Paola M, Caltagirone C, Petrosini L (2013) Prolonged rock climbing activity induces structural changes in cerebellum and parietal lobe. Hum Brain Mapp 34(10):2707–2714
Di X, Zhu S, Jin H, Wang P, Ye Z, Zhou K, Zhuo Y, Rao H (2012) Altered resting brain function and structure in professional badminton players. Brain Connect 2(4):225–233
Dosenbach NU, Fair DA, Miezin FM, Cohen AL, Wenger KK, Dosenbach RA, Fox MD, Snyder AZ, Vincent JL, Raichle ME, Schlaggar BL, Petersen SE (2007) Distinct brain networks for adaptive and stable task control in humans. Proc Natl Acad Sci USA 104(26):11073–11078
Dosenbach NUF, Fair DA, Cohen AL, Schlaggar BL, Petersen SE (2008) A dual-networks architecture of top-down control. Trends Cogn Sci 12(3):99–105
Dosenbach NUF, Nardos B, Cohen AL, Fair DA, Power JD, Church JA, Nelson SM, Wig GS, Vogel AC, Lessov-Schlaggar CN, Barnes KA, Dubis JW, Feczko E, Coalson RS, Pruett JR, Barch DM, Petersen SE, Schlaggar BL (2010) Prediction of individual brain maturity using fMRI. Science 329(5997):1358–1361
Doyon J, Benali H (2005) Reorganization and plasticity in the adult brain during learning of motor skills. Curr Opin Neurobiol 15(2):161–167
Doyon J, Ungerleider LG, Squire L, Schacter D (2002) Functional anatomy of motor skill learning. Neuropsychol Mem 3:225–238
Doyon J, Bellec P, Amsel R, Penhune V, Monchi O, Carrier J, Lehericy S, Benali H (2009) Contributions of the basal ganglia and functionally related brain structures to motor learning. Behav Brain Res 199(1):61–75
Duan X, He S, Liao W, Liang D, Qiu L, Wei L, Li Y, Liu C, Gong Q, Chen H (2012) Reduced caudate volume and enhanced striatal-DMN integration in chess experts. Neuroimage 60(2):1280–1286
Fine EJ, Ionita CC, Lohr L (2002) The history of the development of the cerebellar examination. Semin Neurol 22(4):375–384
Floyer-Lea A, Matthews PM (2005) Distinguishable brain activation networks for short- and long-term motor skill learning. J Neurophysiol 94(1):512–518
Fox MD, Zhang D, Snyder AZ, Raichle ME (2009) The global signal and observed anticorrelated resting state brain networks. J Neurophysiol 101(6):3270–3283
Garrison KA, Scheinost D, Finn ES, Shen X, Constable RT (2015) The (in)stability of functional brain network measures across thresholds. Neuroimage 118:651–661
Greicius MD, Supekar K, Menon V, Dougherty RF (2009) Resting-state functional connectivity reflects structural connectivity in the default mode network. Cereb Cortex 19(1):72–78
Guerra-Carrillo B, Mackey AP, Bunge SA (2014) Resting-state fMRI a window into human brain plasticity. Neuroscientist. http://nro.sagepub.com/content/early/2014/02/21/1073858414524442.full.pdf+html
Hamzei F, Glauche V, Schwarzwald R, May A (2012) Dynamic gray matter changes within cortex and striatum after short motor skill training are associated with their increased functional interaction. Neuroimage 59(4):3364-3372
Hardwick RM, Rottschy C, Miall RC, Eickhoff SB (2013) A quantitative meta-analysis and review of motor learning in the human brain. Neuroimage 67:283–297
Harriger L, van den Heuvel MP, Sporns O (2012) Rich club organization of macaque cerebral cortex and its role in network communication. Plos One 7(9):e46497
Haslinger B, Erhard P, Altenmuller E, Hennenlotter A, Schwaiger M, Grafin von Einsiedel H, Rummeny E, Conrad B, Ceballos-Baumann AO (2004) Reduced recruitment of motor association areas during bimanual coordination in concert pianists. Hum Brain Mapp 22(3):206–215
He Y, Wang J, Wang L, Chen ZJ, Yan C, Yang H, Tang H, Zhu C, Gong Q, Zang Y, Evans AC (2009) Uncovering intrinsic modular organization of spontaneous brain activity in humans. Plos One 4(4):e5226
Hikosaka O, Nakamura K, Sakai K, Nakahara H (2002) Central mechanisms of motor skill learning. Curr Opin Neurobiol 12(2):217–222
Huang R, Lu M, Song Z, Wang J (2013) Long-term intensive training induced brain structural changes in world class gymnasts. Brain Struct Funct 220(2):625–644
Jancke L, Koeneke S, Hoppe A, Rominger C, Hanggi J (2009) The architecture of the golfer’s brain. Plos One 4(3):e4785
Jiang G, Wen X, Qiu Y, Zhang R, Wang J, Li M, Ma X, Tian J, Huang R (2013) Disrupted topological organization in whole-brain functional networks of heroin-dependent individuals: a resting-state FMRI study. Plos One 8(12):e82715
Kim J, Lee HM, Kim WJ, Park HJ, Kim SW, Moon DH, Woo M, Tennant LK (2008) Neural correlates of pre-performance routines in expert and novice archers. Neurosci Lett 445(3):236–241
Krakauer JW, Mazzoni P (2011) Human sensorimotor learning: adaptation, skill, and beyond. Curr Opin Neurobiol 21(4):636–644
Kurata K (2005) Activity properties and location of neurons in the motor thalamus that project to the cortical motor areas in monkeys. J Neurophysiol 94(1):550–566
Leiguarda RC, Marsden CD (2000) Limb apraxias—higher-order disorders of sensorimotor integration. Brain 123:860–879
Liang X, Wang J, Yan C, Shu N, Xu K, Gong G, He Y (2012) Effects of different correlation metrics and preprocessing factors on small-world brain functional networks: a resting-state functional MRI study. Plos One 7(3):e32766
Luo C, Guo ZW, Lai YX, Liao W, Liu Q, Kendrick KM, Yao DZ, Li H (2012) Musical training induces functional plasticity in perceptual and motor networks: insights from resting-state FMRI. Plos One 7(5):e36568
Lynall ME, Bassett DS, Kerwin R, McKenna PJ, Kitzbichler M, Muller U, Bullmore E (2010) Functional connectivity and brain networks in schizophrenia. J Neurosci 30(28):9477–9487 Ma L, Wang B, Narayana S, Hazeltine E, Chen X, Robin DA, Fox PT, Xiong J (2010) Changes in regional activity are accompanied with changes in inter-regional connectivity during 4 weeks motor learning. Brain research 1318:64-76
Ma L, Narayana S, Robin DA, Fox PT, Xiong J (2011) Changes occur in resting state network of motor system during 4weeks of motor skill learning. Neuroimage 58(1):226–233
Ma L, Wang B, Narayana S, Hazeltine E, Chen X, Robin DA, Fox PT, Xiong J (2010) Changes in regional activity are accompanied with changes in inter-regional connectivity during 4 weeks motor learning. Brain research 1318:64–76
Manto M, Bower JM, Conforto AB, Delgado-Garcia JM, da Guarda SNF, Gerwig M, Habas C, Hagura N, Ivry RB, Marien P, Molinari M, Naito E, Nowak DA, Ben Taib NO, Pelisson D, Tesche CD, Tilikete C, Timmann D (2012) Consensus Paper: roles of the cerebellum in motor control-the diversity of ideas on cerebellar involvement in movement. Cerebellum 11(2):457–487
Mauk MD, Medina JF, Nores WL, Ohyama T (2000) Cerebellar function: coordination, learning or timing? Curr Biol 10(14):R522–R525
Meng C, Brandl F, Tahmasian M, Shao JM, Manoliu A, Scherr M, Schwerthoffer D, Bauml J, Forstl H, Zimmer C, Wohlschlager AM, Riedl V, Sorg C (2014) Aberrant topology of striatum’s connectivity is associated with the number of episodes in depression. Brain 137:598–609
Miller EK, Cohen JD (2001) An integrative theory of prefrontal cortex function. Annu Rev Neurosci 24:167–202
Mowinckel AM, Espeseth T, Westlye LT (2012) Network-specific effects of age and in-scanner subject motion: a resting-state fMRI study of 238 healthy adults. Neuroimage 63(3):1364–1373
Murphy K, Birn RM, Handwerker DA, Jones TB, Bandettini PA (2009) The impact of global signal regression on resting state correlations: are anti-correlated networks introduced? Neuroimage 44(3):893–905
Nakao T, Radua J, Rubia K, Mataix-Cols D (2011) Gray matter volume abnormalities in ADHD: voxel-based meta-analysis exploring the effects of age and stimulant medication. Am J Psychiatry 168(11):1154–1163
Nakata H, Yoshie M, Miura A, Kudo K (2010) Characteristics of the athletes’ brain: evidence from neurophysiology and neuroimaging. Brain Res Rev 62(2):197–211
Newman ME (2006) Modularity and community structure in networks. Proc Natl Acad Sci USA 103(23):8577–8582
Newman MEJ (2012) Communities, modules and large-scale structure in networks. Nat Phys 8(1):25–31
Nichols TE, Holmes AP (2002) Nonparametric permutation tests for functional neuroimaging: a primer with examples. Hum Brain Mapp 15(1):1–25
Pencina MJ, D’Agostino RB Sr, D’Agostino RB Jr, Vasan RS (2008) Evaluating the added predictive ability of a new marker: from area under the ROC curve to reclassification and beyond. Stat Med 27(2):157–172
Penhune VB, Steele CJ (2012) Parallel contributions of cerebellar, striatal and M1 mechanisms to motor sequence learning. Behav Brain Res 226(2):579–591
Picard N, Strick PL (1996) Motor areas of the medial wall: a review of their location and functional activation. Cereb Cortex 6(3):342–353
Power JD, Cohen AL, Nelson SM, Wig GS, Barnes KA, Church JA, Vogel AC, Laumann TO, Miezin FM, Schlaggar BL, Petersen SE (2011) Functional network organization of the human brain. Neuron 72(4):665–678
Ray S, Miller M, Karalunas S, Robertson C, Grayson DS, Cary RP, Hawkey E, Painter JG, Kriz D, Fombonne E, Nigg JT, Fair DA (2014) Structural and functional connectivity of the human brain in autism spectrum disorders and attention-deficit/hyperactivity disorder: a rich club-organization study. Hum Brain Mapp 35(12):6032–6048
Rizzolatti G, Luppino G (2001) The cortical motor system. Neuron 31(6):889–901
Rubinov M, Sporns O (2010) Complex network measures of brain connectivity: uses and interpretations. NeuroImage 52(3):1059–1069
Sakai ST, Inase M, Tanji J (2002) The relationship between MI and SMA afferents and cerebellar and pallidal efferents in the macaque monkey. Somatosens Mot Res 19(2):139–148
Sampaio-Baptista C, Scholz J, Jenkinson M, Thomas AG, Filippini N, Smit G, Douaud G, Johansen-Berg H (2014) Gray matter volume is associated with rate of subsequent skill learning after a long term training intervention. Neuroimage 96:158–166
Sampaio-Baptista C, Filippini N, Stagg CJ, Near J, Scholz J, Johansen-Berg H (2015) Changes in functional connectivity and GABA levels with long-term motor learning. Neuroimage 106:15–20
Schendan HE, Searl MM, Melrose RJ, Stern CE (2003) An FMRI study of the role of the medial temporal lobe in implicit and explicit sequence learning. Neuron 37(6):1013–1025
Seeley WW, Menon V, Schatzberg AF, Keller J, Glover GH, Kenna H, Reiss AL, Greicius MD (2007) Dissociable intrinsic connectivity networks for salience processing and executive control. J Neurosci 27(9):2349–2356
Skudlarski P, Jagannathan K, Anderson K, Stevens MC, Calhoun VD, Skudlarska BA, Pearlson G (2010) Brain connectivity is not only lower but different in schizophrenia: a combined anatomical and functional approach. Biol Psychiat 68(1):61–69
Sporns O (2013) Network attributes for segregation and integration in the human brain. Curr Opin Neurobiol 23(2):162–171
Sridharan D, Levitin DJ, Menon V (2008) A critical role for the right fronto-insular cortex in switching between central-executive and default-mode networks. Proc Natl Acad Sci USA 105(34):12569–12574
Tanji J (1996) New concepts of the supplementary motor area. Curr Opin Neurobiol 6(6):782–787
Taubert M, Lohmann G, Margulies DS, Villringer A, Ragert P (2011) Long-term effects of motor training on resting-state networks and underlying brain structure. Neuroimage 57(4):1492–1498
Telesford QK, Burdette JH, Laurienti PJ (2013) An exploration of graph metric reproducibility in complex brain networks. Front Neurosci 7:67
Tian L, Wang J, Yan C, He Y (2011) Hemisphere- and gender-related differences in small-world brain networks: a resting-state functional MRI study. NeuroImage 54(1):191–202
Tzourio-Mazoyer N, Landeau B, Papathanassiou D, Crivello F, Etard O, Delcroix N, Mazoyer B, Joliot M (2002) Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain. NeuroImage 15(1):273–289
Uehara T, Yamasaki T, Okamoto T, Koike T, Kan S, Miyauchi S, Kira J, Tobimatsu S (2014) Efficiency of a “small-world” brain network depends on consciousness level: a resting-state FMRI study. Cereb Cortex 24(6):1529–1539
van den Heuvel MP, Sporns O (2011) Rich-club organization of the human connectome. J Neurosci 31(44):15775–15786
van den Heuvel M, Mandl R, Luigjes J, Pol HH (2008) Microstructural organization of the cingulum tract and the level of default mode functional connectivity. J Neurosci 28(43):10844–10851
van den Heuvel MP, Mandl RCW, Kahn RS, Pol HEH (2009) Functionally linked resting-state networks reflect the underlying structural connectivity architecture of the human brain. Hum Brain Mapp 30(10):3127–3141
van den Heuvel MP, Mandl RC, Stam CJ, Kahn RS, Hulshoff Pol HE (2010) Aberrant frontal and temporal complex network structure in schizophrenia: a graph theoretical analysis. J Neurosci 30(47):15915–15926
van den Heuvel MP, Sporns O, Collin G, Scheewe T, Mandl RCW, Cahn W, Goni J, Pol HEH, Kahn RS (2013) Abnormal rich club organization and functional brain dynamics in Schizophrenia. Jama Psychiat 70(8):783–792
Walz AD, Doppl K, Kaza E, Roschka S, Platz T, Lotze M (2015) Changes in cortical, cerebellar and basal ganglia representation after comprehensive long term unilateral hand motor training. Behav Brain Res 278:393–403
Wang J, Wang L, Zang Y, Yang H, Tang H, Gong Q, Chen Z, Zhu C, He Y (2009) Parcellation-dependent small-world brain functional networks: a resting-state fMRI study. Hum Brain Mapp 30(5):1511–1523
Wang JH, Zuo XN, Gohel S, Milham MP, Biswal BB, He Y (2011) Graph theoretical analysis of functional brain networks: test-retest evaluation on short- and long-term resting-state functional MRI data. Plos One 6(7):e21976
Wang B, Fan Y, Lu M, Li S, Song Z, Peng X, Zhang R, Lin Q, He Y, Wang J, Huang R (2013a) Brain anatomical networks in world class gymnasts: a DTI tractography study. Neuroimage 65:476–487
Wang JH, Zuo XN, Dai ZJ, Xia MR, Zhao ZL, Zhao XL, Jia JP, Han Y, He Y (2013b) Disrupted functional brain connectome in individuals at risk for Alzheimer’s disease. Bio Psychiatry 73(5):472–481
Wang J, Qiu S, Xu Y, Liu Z, Wen X, Hu X, Zhang R, Li M, Wang W, Huang R (2014) Graph theoretical analysis reveals disrupted topological properties of whole brain functional networks in temporal lobe epilepsy. Clin Neurophysiol 125(9):1744–1756
Willingham DB (1998) A neuropsychological theory of motor skill learning. Psychol Rev 105(3):558–584
Wu T, Kansaku K, Hallett M (2004) How self-initiated memorized movements become automatic: a functional MRI study. J Neurophysiol 91(4):1690–1698
Yan C, Zang Y (2010) DPARSF: a MATLAB toolbox for “pipeline” data analysis of resting-state fMRI. Front Syst Neurosci 4:13
Yao Z, Hu B, Xie Y, Moore P, Zheng J (2015) A review of structural and functional brain networks: small world and atlas. Brain Informatics 2(1):45–52
Zalesky A, Fornito A, Bullmore ET (2010) Network-based statistic: identifying differences in brain networks. Neuroimage 53(4):1197–1207
Zanto TP, Gazzaley A (2013) Fronto-parietal network: flexible hub of cognitive control. Trends Cogn Sci 17(12):602–603
Zhang Z, Liao W, Chen H, Mantini D, Ding JR, Xu Q, Wang Z, Yuan C, Chen G, Jiao Q, Lu G (2011) Altered functional-structural coupling of large-scale brain networks in idiopathic generalized epilepsy. Brain 134(Pt 10):2912–2928
Zuo XN, Xing XX (2014) Test-retest reliabilities of resting-state FMRI measurements in human brain functional connectomics: a systems neuroscience perspective. Neurosci Biobehav R 45:100–118
Zuo XN, Anderson JS, Bellec P, Birn RM, Biswal BB, Blautzik J, Breitner JC, Buckner RL, Calhoun VD, Castellanos FX, Chen A, Chen B, Chen J, Chen X, Colcombe SJ, Courtney W, Craddock RC, Di Martino A, Dong HM, Fu X, Gong Q, Gorgolewski KJ, Han Y, He Y, Ho E, Holmes A, Hou XH, Huckins J, Jiang T, Jiang Y, Kelley W, Kelly C, King M, LaConte SM, Lainhart JE, Lei X, Li HJ, Li K, Lin Q, Liu D, Liu J, Liu X, Liu Y, Lu G, Lu J, Luna B, Luo J, Lurie D, Mao Y, Margulies DS, Mayer AR, Meindl T, Meyerand ME, Nan W, Nielsen JA, O’Connor D, Paulsen D, Prabhakaran V, Qi Z, Qiu J, Shao C, Shehzad Z, Tang W, Villringer A, Wang H, Wang K, Wei D, Wei GX, Weng XC, Wu X, Xu T, Yang N, Yang Z, Zang YF, Zhang L, Zhang Q, Zhang Z, Zhao K, Zhen Z, Zhou Y, Zhu XT, Milham MP (2014) An open science resource for establishing reliability and reproducibility in functional connectomics. Sci Data 1:140049
Acknowledgments
This work was supported by the funding from the National Natural Science Foundation of China (Grant numbers: 81071149, 81271548, 81371535, 81428013, and 81471654). The authors express appreciation to Drs. Rhoda E. and Edmund F. Perozzi for editing assistance.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Competing interest
The authors declare that they have no competing financial interests.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Wang, J., Lu, M., Fan, Y. et al. Exploring brain functional plasticity in world class gymnasts: a network analysis. Brain Struct Funct 221, 3503–3519 (2016). https://doi.org/10.1007/s00429-015-1116-6
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00429-015-1116-6