Skip to main content
SpringerLink
Log in

Long-term intensive training induced brain structural changes in world class gymnasts

  • Original Article
  • Published:
Brain Structure and Function Aims and scope Submit manuscript

Abstract

Many previous studies suggested that both short-term and long-term motor training can modulate brain structures. However, little evidence exists for such brain anatomical changes in top-level gymnasts. Using diffusion-weighted and structural magnetic resonance images of the human brain, we applied voxel-based morphometry (VBM) and tract-based spatial statistics (TBSS) as well as FA-VBA (voxel-based analysis of fractional anisotropy, a VBM-style analysis) methods to quantitatively compare the brain structural differences between the world class gymnasts (WCG) and the non-athlete groups. In order to reduce the rate of false positive findings, we first determined that the clusters defined at a threshold of t > 2.3 and a cluster significance of p < 0.05 (FWE-corrected) across all subjects were the brain regions that showed significant differences in a between-group comparison. We then constructed several between-group comparisons based on the repeated diffusion or structural MRI data and created the intersecting regions from multiple between-group comparisons. Thus, we found significantly decreased fractional anisotropy (FA) not only in the white matter of the WCG in areas that included the bilateral superior longitudinal fasciculus, inferior longitudinal fasciculus, and inferior occipito-frontal fascicle, but also in the gray matter of the WCG in areas that included the bilateral middle cingulum, bilateral postcentral gyri, and bilateral motor regions. We also identified significantly increased gray matter density in the WCG, especially in the left inferior frontal gyrus, bilateral inferior and superior parietal lobule, bilateral superior lateral occipital cortex, left cuneus, left angular gyrus, and right postcentral gyrus. We speculate that the brain changes of the WCG may reflect the gymnasts’ extraordinary ability to estimate the direction of their movements, their speed of execution, and their identification of their own and surrounding objects’ locations. Our findings suggest that our method of constructing intersecting regions from multiple between-group comparison can considerably reduce the false positives, and our results provide new insights into the brain structure changes induced by long-term intensive gymnastic training.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

Abbreviations

DTI:

Diffusion tensor imaging

FA:

Fractional anisotropy

GM:

Gray matter

WM:

White matter

FA-VBA:

Voxel-based analysis of FA

WCG:

World class gymnasts (Gymnastic World Champions or Olympics Champions)

MRI:

Magnetic resonance imaging

TBSS:

Tract-based spatial statistics

VBM:

Voxel-based morphometry

GLM:

General linear model

BA:

Brodmann’s area

References

  • Amunts K (2013) Microstructural maps at multiple scales? JuBrain atlas and BigBrain. Frontiers in Neuroinformatics

  • Amunts K, Jäncke L, Mohlberg H, Steinmetz H, Zilles K (2000) Interhemispheric asymmetry of the human motor cortex related to handedness and gender. Neuropsychologia 38(3):304–312

    CAS  PubMed  Google Scholar 

  • Amunts K, Schleicher A, Zilles K (2007) Cytoarchitecture of the cerebral cortex–more than localization. Neuroimage 37(4):1061–1065 discussion 1066–1068

    CAS  PubMed  Google Scholar 

  • Amunts K, Lepage C, Borgeat L, Mohlberg H, Dickscheid T, Rousseau ME, Bludau S, Bazin PL, Lewis LB, Oros-Peusquens AM, Shah NJ, Lippert T, Zilles K, Evans AC (2013) BigBrain: an ultrahigh-resolution 3D human brain model. Science 340(6139):1472–1475

    CAS  PubMed  Google Scholar 

  • Andersen RA, Snyder LH, Bradley DC, Xing J (1997) Multimodal representation of space in the posterior parietal cortex and its use in planning movements. Annu Rev Neurosci 20:303–330

    CAS  PubMed  Google Scholar 

  • Ansari D (2008) Effects of development and enculturation on number representation in the brain. Nat Rev Neurosci 9(4):278–291

    CAS  PubMed  Google Scholar 

  • Ashburner J, Friston KJ (2000) Voxel-based morphometry—the methods. NeuroImage 11(6):805–821

    CAS  PubMed  Google Scholar 

  • Assmus A, Marshall JC, Ritzl A, Noth J, Zilles K, Fink GR (2003) Left inferior parietal cortex integrates time and space during collision judgments. NeuroImage 20(Suppl 1):S82–S88

    Google Scholar 

  • Aydin K, Ucar A, Oguz KK, Okur OO, Agayev A, Unal Z, Yilmaz S, Ozturk C (2007) Increased gray matter density in the parietal cortex of mathematicians: a voxel-based morphometry study. AJNR Am J Neuroradiol 28(10):1859–1864

    CAS  PubMed  Google Scholar 

  • Bartlett JW, Frost C (2008) Reliability, repeatability and reproducibility: analysis of measurement errors in continuous variables. Ultrasound Obstet Gynecol 31(4):466–475

    CAS  PubMed  Google Scholar 

  • Basser PJ, Pierpaoli C (1996) Microstructural and physiological features of tissues elucidated by quantitative-diffusion-tensor MRI. J Magn Reson B 111(3):209–219

    CAS  PubMed  Google Scholar 

  • Beaulieu C (2002) The basis of anisotropic water diffusion in the nervous system-a technical review. NMR Biomed 15(7–8):435–455

    PubMed  Google Scholar 

  • Benedetta B, Zhaleh K, Mara C, David HM, Alan JT, Olga C (2009) Exploring the relationship between white matter and gray matter damage in early primary progressive multiple sclerosis: an in vivo study with TBSS and VBM. Hum Brain Mapp 30(9):2852–2861

    Google Scholar 

  • Bengtsson SL, Nagy Z, Skare S, Forsman L, Forssberg H, Ullen F (2005) Extensive piano practicing has regionally specific effects on white matter development. Nat Neurosci 8(9):1148–1150

    CAS  PubMed  Google Scholar 

  • Bennett CM, Miller MB (2010) How reliable are the results from functional magnetic resonance imaging? Ann N Y Acad Sci 1191:133–155

    PubMed  Google Scholar 

  • Breckel TPK, Giessing C, Thiel CM (2011) Impact of brain networks involved in vigilance on processing irrelevant visual motion. NeuroImage 55(4):1754–1762

    PubMed  Google Scholar 

  • Brinkman C (1981) Lesions in supplementary motor area interfere with a monkey’s performance of a bimanual coordination task. Neurosci Lett 27(3):267–270

    CAS  PubMed  Google Scholar 

  • Buonomano DV, Merzenich MM (1998) Cortical plasticity: from synapses to maps. Ann Rev Neurosci 21(1):149–186

    CAS  PubMed  Google Scholar 

  • Bush G, Vogt BA, Holmes J, Dale AM, Greve D, Jenike MA, Rosen BR (2002) Dorsal anterior cingulate cortex: a role in reward-based decision making. Proc Natl Acad Sci USA 99(1):523–528

    PubMed Central  CAS  PubMed  Google Scholar 

  • Cannonieri GC, Bonilha L, Fernandes PT, Cendes F, Li LM (2007) Practice and perfect: length of training and structural brain changes in experienced typists. NeuroReport 18(10):1063–1066

    PubMed  Google Scholar 

  • Colby CL, Goldberg ME (1999) Space and attention in parietal cortex. Annu Rev Neurosci 22:319–349

    CAS  PubMed  Google Scholar 

  • Coull JT, Frith CD, Frackowiak RS, Grasby PM (1996) A fronto-parietal network for rapid visual information processing: a PET study of sustained attention and working memory. Neuropsychologia 34(11):1085–1095

    CAS  PubMed  Google Scholar 

  • de Groot M, Vernooij MW, Klein S, Ikram MA, Vos FM, Smith SM, Niessen WJ, Andersson JLR (2013) Improving alignment in Tract-based spatial statistics: evaluation and optimization of image registration. NeuroImage 76:400–411

    PubMed  Google Scholar 

  • Draganski B, Kherif F (2013) In vivo assessment of use-dependent brain plasticity-Beyond the “one trick pony” imaging strategy. NeuroImage 73:255–259

    PubMed  Google Scholar 

  • Draganski B, Gaser C, Busch V, Schuierer G, Bogdahn U, May A (2004) Neuroplasticity: changes in grey matter induced by training. Nature 427(6972):311–312

    CAS  PubMed  Google Scholar 

  • Eickhoff SB, Stephan KE, Mohlberg H, Grefkes C, Fink GR, Amunts K, Zilles K (2005) A new SPM toolbox for combining probabilistic cytoarchitectonic maps and functional imaging data. NeuroImage 25(4):1325–1335

    PubMed  Google Scholar 

  • Erickson KI (2013) Evidence for structural plasticity in humans: comment on Thomas and Baker (2012). NeuroImage 73:237–238

    PubMed  Google Scholar 

  • Evarts EV (1968) Relation of pyramidal tract activity to force exerted during voluntary movement. J Neurophysiol 31(1):14–27

    CAS  PubMed  Google Scholar 

  • Fields RD (2013) Changes in brain structure during learning: fact or artifact? Reply to Thomas and Baker. NeuroImage 73:260–264

    PubMed  Google Scholar 

  • Fieremans E, De Deene Y, Delputte S, Ozdemir MS, D’Asseler Y, Vlassenbroeck J, Deblaere K, Achten E, Lemahieu I (2008) Simulation and experimental verification of the diffusion in an anisotropic fiber phantom. J Magn Reson 190(2):189–199

    CAS  PubMed  Google Scholar 

  • Fieremans E, Deene YD, Baete S, Lemahieu I (2009) Design of anisotropic diffusion hardware fiber phantoms. Diffus Fundam 10:1–3

    Google Scholar 

  • Gaser C, Schlaug G (2003) Brain structures differ between musicians and non-musicians. J Neurosci 23(27):9240–9245

    CAS  PubMed  Google Scholar 

  • Georgopoulos AP, Schwartz AB, Kettner RE (1986) Neuronal population coding of movement direction. Science 233(4771):1416–1419

    CAS  PubMed  Google Scholar 

  • Georgopoulos AP, Merchant H, Naselaris T, Amirikian B (2007) Mapping of the preferred direction in the motor cortex. Proc Natl Acad Sci USA 104(26):11068–11072

    PubMed Central  CAS  PubMed  Google Scholar 

  • Goldberg G (1985) Supplementary motor area structure and function: review and hypotheses. Behav Brain Sci 8(04):567–588

    Google Scholar 

  • Good CD, Johnsrude IS, Ashburner J, Henson RN, Friston KJ, Frackowiak RS (2001) A voxel-based morphometric study of ageing in 465 normal adult human brains. NeuroImage 14(1 Pt 1):21–36

    CAS  PubMed  Google Scholar 

  • Grabner RH, Ansari D, Koschutnig K, Reishofer G, Ebner F, Neuper C (2009) To retrieve or to calculate? Left angular gyrus mediates the retrieval of arithmetic facts during problem solving. Neuropsychologia 47(2):604–608

    PubMed  Google Scholar 

  • Grabner RH, Ansari D, Koschutnig K, Reishofer G, Ebner F (2013) The function of the left angular gyrus in mental arithmetic: evidence from the associative confusion effect. Hum Brain Mapp 34(5):1013–1024

    PubMed  Google Scholar 

  • Grill-Spector K, Kourtzi Z, Kanwisher N (2001) The lateral occipital complex and its role in object recognition. Vision Res 41(10–11):1409–1422

    CAS  PubMed  Google Scholar 

  • Griswold MA, Jakob PM, Heidemann RM, Nittka M, Jellus V, Wang J, Kiefer B, Haase A (2002) Generalized autocalibrating partially parallel acquisitions (GRAPPA). Magn Reson Med 47:1202–1210

    PubMed  Google Scholar 

  • Hahn B, Ross TJ, Stein EA (2006) Neuroanatomical dissociation between bottom–up and top–down processes of visuospatial selective attention. NeuroImage 32(2):842–853

    PubMed Central  PubMed  Google Scholar 

  • Han Y, Yang H, Lv Y-T, Zhu C-Z, He Y, Tang H-H, Gong Q-Y, Luo Y-J, Zang Y-F, Dong Q (2009) Gray matter density and white matter integrity in pianists’ brain: a combined structural and diffusion tensor MRI study. Neurosci Lett 459(1):3–6

    CAS  PubMed  Google Scholar 

  • Hänggi J, Koeneke S, Bezzola L, Jäncke L (2010) Structural neuroplasticity in the sensorimotor network of professional female ballet dancers. Hum Brain Mapp 31(8):1196–1206

    PubMed  Google Scholar 

  • Hasan MT, Hernández-González S, Dogbevia G, Treviño M, Bertocchi I, Gruart A, Delgado-García JM (2013) Role of motor cortex NMDA receptors in learning-dependent synaptic plasticity of behaving mice. Nat Commun 4. doi:10.1038/ncomms3258

  • Hayasaka S, Phan KL, Liberzon I, Worsley KJ, Nichols TE (2004) Nonstationary cluster-size inference with random field and permutation methods. NeuroImage 22(2):676–687

    PubMed  Google Scholar 

  • Hoeft F, Barnea-Goraly N, Haas BW, Golarai G, Ng D, Mills D, Korenberg J, Bellugi U, Galaburda A, Reiss AL (2007) More is not always better: increased fractional anisotropy of superior longitudinal fasciculus associated with poor visuospatial abilities in Williams Syndrome. J Neurosci 27(44):11960–11965

    CAS  PubMed  Google Scholar 

  • Iwamura Y, Tanaka M (1996) Representation of reaching and grasping in the monkey postcentral gyrus. Neurosci Lett 214(2–3):147–150

    CAS  PubMed  Google Scholar 

  • Jäncke L, Beeli G, Eulig C, Hanggi J (2009a) The neuroanatomy of grapheme-color synesthesia. Eur J Neurosci 29(6):1287–1293

    PubMed  Google Scholar 

  • Jäncke L, Koeneke S, Hoppe A, Rominger C, Hänggi J (2009b) The architecture of the Golfer’s brain. PLoS One 4(3):e4785

    PubMed Central  PubMed  Google Scholar 

  • Jones DK, Symms MR, Cercignani M, Howard RJ (2005) The effect of filter size on VBM analyses of DT-MRI data. NeuroImage 26(2):546–554

    PubMed  Google Scholar 

  • Jordan K, Wüstenberg T, Heinze H-J, Peters M, Jäncke L (2002) Women and men exhibit different cortical activation patterns during mental rotation tasks. Neuropsychologia 40(13):2397–2408

    PubMed  Google Scholar 

  • Keller TA, Just MA (2009) Altering cortical connectivity: remediation-induced changes in the white matter of poor readers. Neuron 64(5):624–631

    PubMed Central  CAS  PubMed  Google Scholar 

  • Kennerley SW, Walton ME, Behrens TEJ, Buckley MJ, Rushworth MFS (2006) Optimal decision making and the anterior cingulate cortex. Nat Neurosci 9(7):940–947

    CAS  PubMed  Google Scholar 

  • Klein A, Andersson J, Ardekani BA, Ashburner J, Avants B, Chiang M-C, Christensen GE, Collins DL, Gee J, Hellier P, Song JH, Jenkinson M, Lepage C, Rueckert D, Thompson P, Vercauteren T, Woods RP, Mann JJ, Parsey RV (2009) Evaluation of 14 nonlinear deformation algorithms applied to human brain MRI registration. NeuroImage 46(3):786–802

    PubMed Central  PubMed  Google Scholar 

  • Koechlin E, Ody C, Kouneiher F (2003) The architecture of cognitive control in the human prefrontal cortex. Science 302(5648):1181–1185

    CAS  PubMed  Google Scholar 

  • Kourtzi Z, Kanwisher N (2001) Representation of perceived object shape by the human lateral occipital complex. Science 293(5534):1506–1509

    CAS  PubMed  Google Scholar 

  • Kung C–C, Peissig JJ, Tarr MJ (2007) Is region-of-interest overlap comparison a reliable measure of category specificity? J Cogn Neurosci 19(12):2019–2034

    PubMed  Google Scholar 

  • Lee D, Quessy S (2003) Activity in the supplementary motor area related to learning and performance during a sequential visuomotor task. J Neurophysiol 89(2):1039–1056

    PubMed  Google Scholar 

  • Leemans A, Jones DK (2009) The B1-matrix must be rotated when correcting for subject motion in DTI data. Magn Reson Med 61(6):1336–1349

    PubMed  Google Scholar 

  • Lloyd DM, Shore DI, Spence C, Calvert GA (2003) Multisensory representation of limb position in human premotor cortex. Nat Neurosci 6(1):17–18

    CAS  PubMed  Google Scholar 

  • MacEvoy SP (2013) “What?” and “where?” versus “what is where?”: the impact of task on coding of object form and position in the lateral occipital complex. J Vis 13(8)

  • MacEvoy SP, Epstein RA (2011) Constructing scenes from objects in human occipitotemporal cortex. Nat Neurosci 14(10):1323–1329

    CAS  PubMed  Google Scholar 

  • Maguire EA, Gadian DG, Johnsrude IS, Good CD, Ashburner J, Frackowiak RSJ, Frith CD (2000) Navigation-related structural change in the hippocampi of taxi drivers. PNAS 97(8):4398–4403

    PubMed Central  CAS  PubMed  Google Scholar 

  • Maitra R (2010) A re-defined and generalized percent-overlap-of-activation measure for studies of fMRI reproducibility and its use in identifying outlier activation maps. NeuroImage 50(1):124–135

    PubMed  Google Scholar 

  • May A, Gaser C (2012) Response to Thomas and Baker: the structural adaptation of the brain to training. Trends Cogn Sci 16(2):97–98

    Google Scholar 

  • Mechelli A, Crinion JT, Noppeney U, O’Doherty J, Ashburner J, Frackowiak RS, Price CJ (2004) Neurolinguistics: structural plasticity in the bilingual brain. Nature 431(7010):757

    CAS  PubMed  Google Scholar 

  • Mechelli A, Price CJ, Friston KJ, Ashburner J (2005) Voxel-based morphometry of the human brain: methods and applications. Curr Med Imag Rev 1(2):105–113

    Google Scholar 

  • Mori S, van Zijl PC (2002) Fiber tracking: principles and strategies-a technical review. NMR Biomed 15(7–8):468–480

    PubMed  Google Scholar 

  • Muellbacher W, Ziemann U, Wissel J, Dang N, Kofler M, Facchini S, Boroojerdi B, Poewe W, Hallett M (2002) Early consolidation in human primary motor cortex. Nature 415(6872):640–644

    CAS  PubMed  Google Scholar 

  • Nachev P, Kennard C, Husain M (2008) Functional role of the supplementary and pre-supplementary motor areas. Nat Rev Neurosci 9(11):856–869

    CAS  PubMed  Google Scholar 

  • Naito E, Ehrsson HH (2006) Somatic sensation of hand-object interactive movement is associated with activity in the left inferior parietal cortex. J Neurosci 26(14):3783–3790

    CAS  PubMed  Google Scholar 

  • Nichols TE, Holmes AP (2002) Nonparametric permutation tests for functional neuroimaging: a primer with examples. Hum Brain Mapp 15(1):1–25

    PubMed  Google Scholar 

  • Oechslin MS, Imfeld A, Loenneker T, Meyer M, Jäncke L (2009) The plasticity of the superior longitudinal fasciculus as a function of musical expertise: a diffusion tensor imaging study. Front Human Neurosci 3

  • Oh JS, Kubicki M, Rosenberger G, Bouix S, Levitt JJ, McCarley RW, Westin CF, Shenton ME (2009) Thalamo-frontal white matter alterations in chronic schizophrenia: a quantitative diffusion tractography study. Hum Brain Mapp 30(11):3812–3825

    PubMed Central  PubMed  Google Scholar 

  • Oishi K, Zilles K, Amunts K, Faria A, Jiang H, Li X, Akhter K, Hua K, Woods R, Toga AW, Pike GB, Rosa-Neto P, Evans A, Zhang J, Huang H, Miller MI, van Zijl PCM, Mazziotta J, Mori S (2008) Human brain white matter atlas: identification and assignment of common anatomical structures in superficial white matter. NeuroImage 43(3):447–457

    PubMed Central  PubMed  Google Scholar 

  • Pascual-Leone A, Amedi A, Fregni F, Merabet LB (2005) The plastic human brain cortex. Annu Rev Neurosci 28(1):377–401

    CAS  PubMed  Google Scholar 

  • Peelen MV, Kastner S (2011) Is that a bathtub in your kitchen? Nat Neurosci 14(10):1224–1226

    CAS  PubMed  Google Scholar 

  • Penfield W, Welch K (1951) The supplementary motor area of the cerebral cortex: a clinical and experimental study. AMA Arch Neurol Psychiatry 66(3):289–317

    CAS  PubMed  Google Scholar 

  • Pierpaoli C, Basser PJ (1996) Toward a quantitative assessment of diffusion anisotropy. Magn Reson Med 36(6):893–906

    CAS  PubMed  Google Scholar 

  • Radua J, Canales-Rodríguez EJ, Pomarol-Clotet E, Salvador R (2013) Validity of modulation and optimal settings for advanced voxel-based morphometry. NeuroImage (0). doi:10.1016/j.neuroimage.2013.07.084

  • Reese TG, Heid O, Weisskoff RM, Wedeen VJ (2003) Reduction of eddy-current-induced distortion in diffusion MRI using a twice-refocused spin echo. Magn Reson Med 49(1):177–182

    CAS  PubMed  Google Scholar 

  • Ridgway GR, Henley SM, Rohrer JD, Scahill RI, Warren JD, Fox NC (2008) Ten simple rules for reporting voxel-based morphometry studies. NeuroImage 40(4):1429–1435

    PubMed  Google Scholar 

  • Rivera SM, Reiss AL, Eckert MA, Menon V (2005) Developmental changes in mental arithmetic: evidence for increased functional specialization in the left inferior parietal cortex. Cereb Cortex 15(11):1779–1790

    CAS  PubMed  Google Scholar 

  • Rizzolatti G, Luppino G (2001) The cortical motor system. Neuron 31(6):889–901

    CAS  PubMed  Google Scholar 

  • Rizzolatti G, Matelli M, Pavesi G (1983) Deficits in attention and movement following the removal of postarcuate (area 6) and prearcuate (area 8) cortex in macaque monkeys. Brain 106(3):655–673

    PubMed  Google Scholar 

  • Rohde GK, Barnett AS, Basser PJ, Marenco S, Pierpaoli C (2004) Comprehensive approach for correction of motion and distortion in diffusion-weighted MRI. Magn Reson Med 51(1):103–114

    CAS  PubMed  Google Scholar 

  • Roland PE, Larsen B, Lassen NA, Skinhoj E (1980) Supplementary motor area and other cortical areas in organization of voluntary movements in man. J Neurophysiol 43(1):118–136

    CAS  PubMed  Google Scholar 

  • Scarpazza C, Sartori G, De Simone MS, Mechelli A (2013) When the single matters more than the group: very high false positive rates in single case voxel based morphometry. NeuroImage 70:175–188

    CAS  PubMed  Google Scholar 

  • Schlaug G, Forgeard M, Zhu L, Norton A, Winner E (2009) Training-induced neuroplasticity in young children. Ann N Y Acad Sci 1169:205–208

    PubMed Central  PubMed  Google Scholar 

  • Schmahmann JD, Pandya DN, Wang R, Dai G, D’Arceuil HE, de Crespigny AJ, Wedeen VJ (2007) Association fibre pathways of the brain: parallel observations from diffusion spectrum imaging and autoradiography. Brain 130(Pt 3):630–653

    PubMed  Google Scholar 

  • Schmithorst VJ, Wilke M (2002) Differences in white matter architecture between musicians and non-musicians: a diffusion tensor imaging study. Neurosci Lett 321(1–2):57–60

    CAS  PubMed  Google Scholar 

  • Scholz J, Klein MC, Behrens TEJ, Johansen-Berg H (2009) Training induces changes in white-matter architecture. Nat Neurosci 12:1370–1371

    PubMed Central  CAS  PubMed  Google Scholar 

  • Seghier ML, Fagan E, Price CJ (2010) Functional subdivisions in the left angular gyrus where the semantic system meets and diverges from the default network. J Neurosci 30(50):16809–16817

    PubMed Central  CAS  PubMed  Google Scholar 

  • Shibasaki H, Sadato N, Lyshkow H, Yonekura Y, Honda M, Nagamine T, Suwazono S, Magata Y, Ikeda A, Miyazaki M, Fukuyama H, Asato R, Konishi J (1993) Both primary motor cortex and supplementary motor area play an important role in complex finger movement. Brain 116(6):1387–1398

    PubMed  Google Scholar 

  • Shima K, Tanji J (1998) Both supplementary and presupplementary motor areas are crucial for the temporal organization of multiple movements. J Neurophysiol 80(6):3247–3260

    CAS  PubMed  Google Scholar 

  • Silver M, Montana G, Nichols TE (2011) False positives in neuroimaging genetics using voxel-based morphometry data. NeuroImage 54(2):992–1000

    PubMed Central  PubMed  Google Scholar 

  • Sluming V, Barrick T, Howard M, Cezayirli E, Mayes A, Roberts N (2002) Voxel-based morphometry reveals increased gray matter density in broca’s area in male symphony orchestra musicians. NeuroImage 17(3):1613–1622

    PubMed  Google Scholar 

  • Smith SM, Nichols TE (2009) Threshold-free cluster enhancement: addressing problems of smoothing, threshold dependence and localisation in cluster inference. NeuroImage 44(1):83–98

    PubMed  Google Scholar 

  • Smith SM, Jenkinson M, Johansen-Berg H, Rueckert D, Nichols TE, Mackay CE, Watkins KE, Ciccarelli O, Cader MZ, Matthews PM, Behrens TEJ (2006) Tract-based spatial statistics: voxelwise analysis of multi-subject diffusion data. NeuroImage 31(4):1487–1505

    PubMed  Google Scholar 

  • Song W, Francis JT (2013) Tactile information processing in primate hand somatosensory cortex (S1) during passive arm movement. J Neurophysiol

  • Swick D, Ashley V, Turken AU (2008) Left inferior frontal gyrus is critical for response inhibition. BMC Neurosci 9:102

    PubMed Central  PubMed  Google Scholar 

  • Takahashi M, Hackney DB, Zhang G, Wehrli SL, Wright AC, O’Brien WT, Uematsu H, Wehrli FW, Selzer ME (2002) Magnetic resonance microimaging of intraaxonal water diffusion in live excised lamprey spinal cord. Proc Natl Acad Sci USA 99(25):16192–16196

    PubMed Central  CAS  PubMed  Google Scholar 

  • Tanaka S, Honda M, Sadato N (2005) Modality-specific cognitive function of medial and lateral human Brodmann area 6. J Neurosci 25(2):496–501

    CAS  PubMed  Google Scholar 

  • Tanji J (1994) The supplementary motor area in the cerebral cortex. Neurosci Res 19(3):251–268

    CAS  PubMed  Google Scholar 

  • Tanji J (1996) New concepts of the supplementary motor area. Curr Opin Neurobiol 6(6):782–787

    CAS  PubMed  Google Scholar 

  • Tanji J (2001) Sequential organization of multiple movements: involvement of cortical motor areas. Annu Rev Neurosci 24:631–651

    CAS  PubMed  Google Scholar 

  • Thomas C, Baker CI (2013a) On evidence, biases and confounding factors: response to commentaries. NeuroImage 73:265–267

    PubMed Central  PubMed  Google Scholar 

  • Thomas C, Baker CI (2013b) Teaching an adult brain new tricks: a critical review of evidence for training-dependent structural plasticity in humans. NeuroImage 73:225–236

    PubMed  Google Scholar 

  • Thomas AG, Marrett S, Saad ZS, Ruff DA, Martin A, Bandettini PA (2009) Functional but not structural changes associated with learning: an exploration of longitudinal voxel-based morphometry (VBM). NeuroImage 48(1):117–125

    PubMed Central  PubMed  Google Scholar 

  • Uddin LQ, Supekar K, Amin H, Rykhlevskaia E, Nguyen DA, Greicius MD, Menon V (2010) Dissociable connectivity within human angular gyrus and intraparietal sulcus: evidence from functional and structural connectivity. Cereb Cortex 20(11):2636–2646

    PubMed Central  PubMed  Google Scholar 

  • Vaina LM, Solomon J, Chowdhury S, Sinha P, Belliveau JW (2001) Functional neuroanatomy of biological motion perception in humans. PNAS 98(20):11656–11661

    PubMed Central  CAS  PubMed  Google Scholar 

  • van Veen V, Cohen JD, Botvinick MM, Stenger VA, Carter CS (2001) Anterior cingulate cortex, conflict monitoring, and levels of processing. NeuroImage 14(6):1302–1308

    PubMed  Google Scholar 

  • Vidoni ED, Acerra NE, Dao E, Meehan SK, Boyd LA (2010) Role of the primary somatosensory cortex in motor learning: an rTMS study. Neurobiol Learn Mem 93(4):532–539

    CAS  PubMed  Google Scholar 

  • Vinberg J, Grill-Spector K (2008) Representation of shapes, edges, and surfaces across multiple cues in the human visual cortex. J Neurophysiol 99(3):1380–1393

    PubMed  Google Scholar 

  • Wang B, Fan Y, Lu M, Li S, Song Z, Peng X, Zhang R, Lin Q, He Y, Wang J, Huang R (2013) Brain anatomical networks in world class gymnasts: a DTI tractography study. NeuroImage 65:476–487

    PubMed  Google Scholar 

  • Ward NS, Newton JM, Swayne OB, Lee L, Thompson AJ, Greenwood RJ, Rothwell JC, Frackowiak RS (2006) Motor system activation after subcortical stroke depends on corticospinal system integrity. Brain 129(Pt 3):809–819

    PubMed Central  PubMed  Google Scholar 

  • Welberg L (2012) Visual system: How the brain distinguishes bugs from birds. Nat Rev Neurosci 11(1):223

    Google Scholar 

  • Wenderoth N, Debaere F, Sunaert S, Hecke PV, Swinnen SP (2004) Parieto-premotor areas mediate directional interference during bimanual movements. Cereb Cortex 14(10):1153–1163

    PubMed  Google Scholar 

  • Yarrow K, Brown P, Krakauer JW (2009) Inside the brain of an elite athlete: the neural processes that support high achievement in sports. Nat Rev Neurosci 10(8):585–596

    CAS  PubMed  Google Scholar 

  • Zalc B, Douglas Fields R (2000) Do action potentials regulate myelination? Neuroscientist 6(1):5–13

    PubMed Central  CAS  PubMed  Google Scholar 

  • Zalesky A (2011) Moderating registration misalignment in voxelwise comparisons of DTI data: a performance evaluation of skeleton projection. Magn Reson Imaging 29(1):111–125

    PubMed  Google Scholar 

  • Zatorre RJ, Fields RD, Johansen-Berg H (2012) Plasticity in gray and white: neuroimaging changes in brain structure during learning. Nat Neurosci 15(4):528–536

    PubMed Central  CAS  PubMed  Google Scholar 

  • Zilles K, Amunts K (2010) Centenary of Brodmann’s map—conception and fate. Nat Rev Neurosci 11(2):139–145

    CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported by the funding of Natural Science Foundation of China (Grant Numbers: 30800267, 81071149, 81271548, and 81371535) and the Scientific Research Foundation for the Returned Overseas Chinese Scholars (RH, JW), State Education Ministry of China. The authors thank Drs. Rhoda and Edmund Perozzi for English editing and comments. The authors also would like to thank the anonymous reviewers for their constructive comments and suggestions.

Conflict of interest

The authors declare that they have no competing financial interests.

Author information

Authors and Affiliations

  1. State Key Laboratory of Cognitive Neuroscience and Learning, Beijing Normal University, Beijing, 100875, People’s Republic of China

    Ruiwang Huang, Min Lu, Zheng Song & Jun Wang

  2. Brain Imaging Center, Center for Studies of Psychological Application, Key Laboratory of Mental Health and Cognitive Science of Guangdong Province, School of Psychology, South China Normal University, Guangzhou, 510631, People’s Republic of China

    Ruiwang Huang

  3. Key Laboratory of Mental Health, Institute of Psychology, Chinese Academy of Sciences, Beijing, 100101, People’s Republic of China

    Min Lu

Authors
  1. Ruiwang Huang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Min Lu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Zheng Song
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Jun Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Ruiwang Huang or Jun Wang.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOC 3301 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Huang, R., Lu, M., Song, Z. et al. Long-term intensive training induced brain structural changes in world class gymnasts. Brain Struct Funct 220, 625–644 (2015). https://doi.org/10.1007/s00429-013-0677-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00429-013-0677-5

Keywords

Search

Navigation