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Brain Structure and Function

, Volume 220, Issue 1, pp 273–290 | Cite as

Bimanual motor deficits in older adults predicted by diffusion tensor imaging metrics of corpus callosum subregions

  • L. Serbruyns
  • J. Gooijers
  • K. Caeyenberghs
  • R. L. Meesen
  • K. Cuypers
  • H. M. Sisti
  • A. Leemans
  • Stephan P. Swinnen
Original Article

Abstract

Age-related changes in the microstructural organization of the corpus callosum (CC) may explain declines in bimanual motor performance associated with normal aging. We used diffusion tensor imaging in young (n = 33) and older (n = 33) adults to investigate the microstructural organization of seven specific CC subregions (prefrontal, premotor, primary motor, primary sensory, parietal, temporal and occipital). A set of bimanual tasks was used to assess various aspects of bimanual motor functioning: the Purdue Pegboard test, simultaneous and alternating finger tapping, a choice reaction time test and a complex visuomotor tracking task. The older adults showed age-related deficits on all measures of bimanual motor performance. Correlation analyses within the older group showed that white matter fractional anisotropy of the CC occipital region was associated with bimanual fine manipulation skills (Purdue Pegboard test), whereas better performance on the other bimanual tasks was related to higher fractional anisotropy in the more anterior premotor, primary motor and primary sensory CC subregions. Such associations were less prominent in the younger group. Our findings suggest that structural alterations of subregional callosal fibers may account for bimanual motor declines in normal aging.

Keywords

Aging Bimanual coordination Corpus callosum DTI Fractional anisotropy 

Abbreviations

AD

Axial diffusivity

CC

Corpus callosum

DTI

Diffusion tensor imaging

FA

Fractional anisotropy

ISO

Isofrequency ratios

N-ISO

Non-isofrequency ratios

OA

Older adults

RD

Radial diffusivity

YA

Young adults

Notes

Acknowledgments

This work was supported by grants from the Research Fund of KU Leuven, Belgium (OT/11/071), the Flanders Fund for Scientific Research (G0483.10, G0721.12) and Grant P7/11 from the Inter-university Attraction Poles program of the Belgian federal government. J. Gooijers is funded by a Ph.D. fellowship of the Research Foundation—Flanders (FWO). K. Cuypers is supported by the Special Research Fund UHasselt.

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical standard

Participants were informed about the experimental procedures and provided written informed consent. The study was approved by the local Ethics Committee of KU Leuven and was performed in accordance with the 1964 Declaration of Helsinki.

Supplementary material

429_2013_654_MOESM1_ESM.pdf (125 kb)
Supplementary material 1 (PDF 125 kb)

References

  1. Abe O, Aoki S, Hayashi N, Yamada H, Kunimatsu A, Mori H, Yoshikawa T, Okubo T, Ohtomo K (2002) Normal aging in the central nervous system: quantitative MR diffusion-tensor analysis. Neurobiol Aging 23(3):433–441PubMedGoogle Scholar
  2. Aboitiz F, Montiel J (2003) One hundred million years of interhemispheric communication: the history of the corpus callosum. Braz J Med Biol Res 36(4):409–420PubMedGoogle Scholar
  3. Aboitiz F, Scheibel AB, Fisher RS, Zaidel E (1992) Fiber composition of the human corpus callosum. Brain Res 598(1–2):143–153PubMedGoogle Scholar
  4. Adamo DE, Martin BJ, Brown SH (2007) Age-related differences in upper limb proprioceptive acuity. Percept Mot Skills 104(3 Pt 2):1297–1309PubMedGoogle Scholar
  5. Anstey KJ, Mack HA, Christensen H, Li SC, Reglade-Meslin C, Maller J, Kumar R, Dear K, Easteal S, Sachdev P (2007) Corpus callosum size, reaction time speed and variability in mild cognitive disorders and in a normative sample. Neuropsychologia 45(8):1911–1920PubMedGoogle Scholar
  6. Bangert AS, Reuter-Lorenz PA, Walsh CM, Schachter AB, Seidler RD (2010) Bimanual coordination and aging: neurobehavioral implications. Neuropsychologia 48(4):1165–1170PubMedCentralPubMedGoogle Scholar
  7. Basser PJ, Pierpaoli C (1996) Microstructural and physiological features of tissues elucidated by quantitative-diffusion-tensor MRI. J Magn Reson B 111(3):209–219PubMedGoogle Scholar
  8. Basser PJ, Pajevic S, Pierpaoli C, Duda J, Aldroubi A (2000) In vivo fiber tractography using DT-MRI data. Magn Reson Med 44(4):625–632PubMedGoogle Scholar
  9. Beaulieu C, Allen PS (1994) Determinants of anisotropic water diffusion in nerves. Magn Reson Med 31(4):394–400PubMedGoogle Scholar
  10. Bennett IJ, Madden DJ, Vaidya CJ, Howard DV, Howard JH Jr (2010) Age-related differences in multiple measures of white matter integrity: a diffusion tensor imaging study of healthy aging. Hum Brain Mapp 31(3):378–390PubMedCentralPubMedGoogle Scholar
  11. Berlucchi G (2012) Frontal callosal disconnection syndromes. Cortex 48(1):36–45PubMedGoogle Scholar
  12. Bernard JA, Seidler RD (2012) Hand dominance and age have interactive effects on motor cortical representations. PLoS One 7(9):e45443Google Scholar
  13. Bhagat YA, Beaulieu C (2004) Diffusion anisotropy in subcortical white matter and cortical gray matter: changes with aging and the role of CSF-suppression. J Magn Reson Imaging 20(2):216–227PubMedGoogle Scholar
  14. Bloom JS, Hynd GW (2005) The role of the corpus callosum in interhemispheric transfer of information: excitation or inhibition? Neuropsychol Rev 15(2):59–71PubMedGoogle Scholar
  15. Bonzano L, Tacchino A, Roccatagliata L, Abbruzzese G, Mancardi GL, Bove M (2008) Callosal contributions to simultaneous bimanual finger movements. J Neurosci 28(12):3227–3233PubMedGoogle Scholar
  16. Buddenberg LA, Davis C (2000) Test-retest reliability of the Purdue Pegboard test. Am J Occup Ther 54(5):555–558PubMedGoogle Scholar
  17. Burzynska AZ, Preuschhof C, Backman L, Nyberg L, Li SC, Lindenberger U, Heekeren HR (2010) Age-related differences in white matter microstructure: region-specific patterns of diffusivity. Neuroimage 49(3):2104–2112PubMedGoogle Scholar
  18. Caeyenberghs K, Leemans A, Coxon J, Leunissen I, Drijkoningen D, Geurts M, Gooijers J, Michiels K, Sunaert S, Swinnen SP (2011) Bimanual coordination and corpus callosum microstructure in young adults with traumatic brain injury: a diffusion tensor imaging study. J Neurotrauma 28(6):897–913PubMedGoogle Scholar
  19. Camara E, Bodammer N, Rodriguez-Fornells A, Tempelmann C (2007) Age-related water diffusion changes in human brain: a voxel-based approach. Neuroimage 34(4):1588–1599PubMedGoogle Scholar
  20. Catani M, Thiebaut de Schotten M (2008) A diffusion tensor imaging tractography atlas for virtual in vivo dissections. Cortex 44(8):1105–1132PubMedGoogle Scholar
  21. Cercignani M (2010) Strategies for patient–control comparison of diffusion MR data. In: Jones DK (ed) Diffusion MRI. Oxford University Press, Oxford, pp 485–499Google Scholar
  22. Chepuri NB, Yen YF, Burdette JH, Li H, Moody DM, Maldjian JA (2002) Diffusion anisotropy in the corpus callosum. AJNR Am J Neuroradiol 23(5):803–808PubMedGoogle Scholar
  23. Cole KJ, Rotella DL (2001) Old age affects fingertip forces when restraining an unpredictably loaded object. Exp Brain Res 136(4):535–542PubMedGoogle Scholar
  24. Coxon JP, Van Impe A, Wenderoth N, Swinnen SP (2012) Aging and inhibitory control of action: cortico-subthalamic connection strength predicts stopping performance. J Neurosci 32(24):8401–8412PubMedGoogle Scholar
  25. Davis SW, Dennis NA, Buchler NG, White LE, Madden DJ, Cabeza R (2009) Assessing the effects of age on long white matter tracts using diffusion tensor tractography. Neuroimage 46(2):530–541PubMedCentralPubMedGoogle Scholar
  26. Desrosiers J, Hebert R, Bravo G, Dutil E (1995) The Purdue Pegboard test: normative data for people aged 60 and over. Disabil Rehabil 17(5):217–224PubMedGoogle Scholar
  27. Desrosiers J, Hebert R, Bravo G, Rochette A (1999) Age-related changes in upper extremity performance of elderly people: a longitudinal study. Exp Gerontol 34(3):393–405PubMedGoogle Scholar
  28. Doherty TJ (2003) Aging and sarcopenia. J Appl Physiol 95(4):1717–1727PubMedGoogle Scholar
  29. Dougherty RF, Ben-Shachar M, Bammer R, Brewer AA, Wandell BA (2005) Functional organization of human occipital-callosal fiber tracts. Proc Natl Acad Sci USA 102(20):7350–7355PubMedCentralPubMedGoogle Scholar
  30. Fling BW, Seidler RD (2012) Fundamental differences in callosal structure, neurophysiologic function, and bimanual control in young and older adults. Cereb Cortex 22(11):2643–2652PubMedCentralPubMedGoogle Scholar
  31. Fling BW, Peltier SJ, Bo J, Welsh RC, Seidler RD (2011a) Age differences in interhemispheric interactions: callosal structure, physiological function, and behavior. Front Neurosci 5:38PubMedCentralPubMedGoogle Scholar
  32. Fling BW, Walsh CM, Bangert AS, Reuter-Lorenz PA, Welsh RC, Seidler RD (2011b) Differential callosal contributions to bimanual control in young and older adults. J Cogn Neurosci 23(9):2171–2185PubMedGoogle Scholar
  33. Gazzaniga MS (2005) Forty-five years of split-brain research and still going strong. Nat Rev Neurosci 6(8):653–659PubMedGoogle Scholar
  34. Gerloff C, Andres FG (2002) Bimanual coordination and interhemispheric interaction. Acta Psychol 110(2–3):161–186Google Scholar
  35. Goble DJ, Coxon JP, Wenderoth N, Van Impe A, Swinnen SP (2009) Proprioceptive sensibility in the elderly: degeneration, functional consequences and plastic-adaptive processes. Neurosci Biobehav Rev 33(3):271–278PubMedGoogle Scholar
  36. Goble DJ, Coxon JP, Van Impe A, Geurts M, Van Hecke W, Sunaert S, Wenderoth N, Swinnen SP (2012) The neural basis of central proprioceptive processing in older versus younger adults: an important sensory role for right putamen. Hum Brain Mapp 33(4):895–908PubMedGoogle Scholar
  37. Goodpaster BH, Park SW, Harris TB, Kritchevsky SB, Nevitt M, Schwartz AV, Simonsick EM, Tylavsky FA, Visser M, Newman AB (2006) The loss of skeletal muscle strength, mass, and quality in older adults: the health, aging and body composition study. J Gerontol Ser A Biol Sci Med Sci 61(10):1059–1064Google Scholar
  38. Gooijers J, Caeyenberghs K, Sisti HM, Geurts M, Heitger MH, Leemans A, Swinnen SP (2013) Diffusion tensor imaging metrics of the corpus callosum in relation to bimanual coordination: effect of task complexity and sensory feedback. Hum Brain Mapp 34(1):241–252PubMedGoogle Scholar
  39. Gunning-Dixon FM, Brickman AM, Cheng JC, Alexopoulos GS (2009) Aging of cerebral white matter: a review of MRI findings. Int J Geriatr Psychiatry 24(2):109–117PubMedCentralPubMedGoogle Scholar
  40. Hairi NN, Cumming RG, Naganathan V, Handelsman DJ, Le Couteur DG, Creasey H, Waite LM, Seibel MJ, Sambrook PN (2010) Loss of muscle strength, mass (sarcopenia), and quality (specific force) and its relationship with functional limitation and physical disability: the concord health and ageing in men project. J Am Geriatr Soc 58(11):2055–2062PubMedGoogle Scholar
  41. Halsband U, Lange RK (2006) Motor learning in man: a review of functional and clinical studies. J Physiol Paris 99(4–6):414–424PubMedGoogle Scholar
  42. Harris T (1997) Muscle mass and strength: relation to function in population studies. J Nutr 127(5 Suppl):1004S–1006SPubMedGoogle Scholar
  43. Hasan KM, Kamali A, Kramer LA, Papnicolaou AC, Fletcher JM, Ewing-Cobbs L (2008) Diffusion tensor quantification of the human midsagittal corpus callosum subdivisions across the lifespan. Brain Res 1227:52–67PubMedCentralPubMedGoogle Scholar
  44. Hofer S, Frahm J (2006) Topography of the human corpus callosum revisited–comprehensive fiber tractography using diffusion tensor magnetic resonance imaging. Neuroimage 32(3):989–994PubMedGoogle Scholar
  45. Hsu JL, Van Hecke W, Bai CH, Lee CH, Tsai YF, Chiu HC, Jaw FS, Hsu CY, Leu JG, Chen WH et al (2010) Microstructural white matter changes in normal aging: a diffusion tensor imaging study with higher-order polynomial regression models. Neuroimage 49(1):32–43PubMedGoogle Scholar
  46. Huang H, Zhang JY, Jiang HY, Wakana S, Poetscher L, Miller MI, van Zijl PCM, Hillis AE, Wytik R, Mori S (2005) DTI tractography based parcellation of white matter: application to the mid-sagittal morphology of corpus callosum. Neuroimage 26(1):195–205PubMedGoogle Scholar
  47. Hugenschmidt CE, Peiffer AM, Kraft RA, Casanova R, Deibler AR, Burdette JH, Maldjian JA, Laurienti PJ (2008) Relating imaging indices of white matter integrity and volume in healthy older adults. Cereb Cortex 18(2):433–442PubMedGoogle Scholar
  48. Inano S, Takao H, Hayashi N, Abe O, Ohtomo K (2011) Effects of age and gender on white matter integrity. Am J Neuroradiol 32(11):2103–2109PubMedGoogle Scholar
  49. Janve VA, Zu ZL, Yao SY, Li K, Zhang FL, Wilson KJ, Ou XW, Does MD, Subramaniam S, Gochberg DF (2013) The radial diffusivity and magnetization transfer pool size ratio are sensitive markers for demyelination in a rat model of type III multiple sclerosis (MS) lesions. Neuroimage 74:298–305PubMedCentralPubMedGoogle Scholar
  50. Jarbo K, Verstynen T, Schneider W (2012) In vivo quantification of global connectivity in the human corpus callosum. Neuroimage 59(3):1988–1996PubMedGoogle Scholar
  51. Jeurissen B, Leemans A, Tournier JD, Jones DK, Sijbers J (2012) Investigating the prevalence of complex fiber configurations in white matter tissue with diffusion magnetic resonance imaging. Hum Brain Mapp. doi: 10.1002/hbm.22099 PubMedGoogle Scholar
  52. Johansen-Berg H, Della-Maggiore V, Behrens TE, Smith SM, Paus T (2007) Integrity of white matter in the corpus callosum correlates with bimanual co-ordination skills. Neuroimage 36(Suppl 2):T16–T21PubMedCentralPubMedGoogle Scholar
  53. Klein S, Staring M, Murphy K, Viergever MA, Pluim JP (2010) Elastix: a toolbox for intensity-based medical image registration. IEEE Trans Med Imaging 29(1):196–205PubMedGoogle Scholar
  54. Langan J, Peltier SJ, Bo J, Fling BW, Welsh RC, Seidler RD (2010) Functional implications of age differences in motor system connectivity. Front Syst Neurosci 4:17PubMedCentralPubMedGoogle Scholar
  55. Lebel C, Caverhill-Godkewitsch S, Beaulieu C (2010) Age-related regional variations of the corpus callosum identified by diffusion tensor tractography. Neuroimage 52(1):20–31PubMedGoogle Scholar
  56. Lebel C, Gee M, Camicioli R, Wieler M, Martin W, Beaulieu C (2012) Diffusion tensor imaging of white matter tract evolution over the lifespan. Neuroimage 60(1):340–352PubMedGoogle Scholar
  57. Leemans A, Jones DK (2009) The B-matrix must be rotated when correcting for subject motion in DTI data. Magn Reson Med 61(6):1336–1349PubMedGoogle Scholar
  58. Leemans A, Sijbers J, De Backer S, Vandervliet E, Parizel PM (2005) Affine coregistration of diffusion tensor magnetic resonance images using mutual information. Adv Concepts Intell Vis Syst Proc 3708:523–530Google Scholar
  59. Leemans A, Jeurissen B, Sijbers J, Jones D (2009) ExploreDTI: a graphical toolbox for processing, analyzing, and visualizing diffusion MR data. In: 17th Annual Meeting of International Society of Magnetic Resonance Medicine. Hawaii, USA, p 3537Google Scholar
  60. Leibowitz HM, Krueger DE, Maunder LR, Milton RC, Kini MM, Kahn HA, Nickerson RJ, Pool J, Colton TL, Ganley JP et al (1980) The Framingham eye study monograph: an ophthalmological and epidemiological study of cataract, glaucoma, diabetic retinopathy, macular degeneration, and visual acuity in a general population of 2631 adults 1973–1975. Surv Ophthalmol 24(Suppl):335–610PubMedGoogle Scholar
  61. Madden DJ, Whiting WL, Huettel SA, White LE, MacFall JR, Provenzale JM (2004) Diffusion tensor imaging of adult age differences in cerebral white matter: relation to response time. Neuroimage 21(3):1174–1181PubMedGoogle Scholar
  62. Madden DJ, Spaniol J, Costello MC, Bucur B, White LE, Cabeza R, Davis SW, Dennis NA, Provenzale JM, Huettel SA (2009) Cerebral white matter integrity mediates adult age differences in cognitive performance. J Cogn Neurosci 21(2):289–302PubMedCentralPubMedGoogle Scholar
  63. Madden DJ, Bennett IJ, Burzynska A, Potter GG, Chen NK, Song AW (2012) Diffusion tensor imaging of cerebral white matter integrity in cognitive aging. Biochim Biophys Acta 1822(3):386–400PubMedCentralPubMedGoogle Scholar
  64. Marneweck M, Loftus A, Hammond G (2011) Short-interval intracortical inhibition and manual dexterity in healthy aging. Neurosci Res 70(4):408–414PubMedGoogle Scholar
  65. Marquardt DW (1963) An algorithm for least-squares estimation of nonlinear parameters. J Soc Ind Appl Math 11(2):431–441Google Scholar
  66. McLaughlin NC, Paul RH, Grieve SM, Williams LM, Laidlaw D, DiCarlo M, Clark CR, Whelihan W, Cohen RA, Whitford TJ et al (2007) Diffusion tensor imaging of the corpus callosum: a cross-sectional study across the lifespan. Int J Dev Neurosci 25(4):215–221PubMedGoogle Scholar
  67. Michielse S, Coupland N, Camicioli R, Carter R, Seres P, Sabino J, Malykhin N (2010) Selective effects of aging on brain white matter microstructure: a diffusion tensor imaging tractography study. Neuroimage 52(4):1190–1201PubMedGoogle Scholar
  68. Mueller KL, Marion SD, Paul LK, Brown WS (2009) Bimanual motor coordination in agenesis of the corpus callosum. Behav Neurosci 123(5):1000–1011PubMedGoogle Scholar
  69. Muetzel RL, Collins PF, Mueller BA, M Schissel A, Lim KO, Luciana M (2008) The development of corpus callosum microstructure and associations with bimanual task performance in healthy adolescents. Neuroimage 39(4):1918–1925PubMedCentralPubMedGoogle Scholar
  70. Nasreddine ZS, Phillips NA, Bedirian V, Charbonneau S, Whitehead V, Collin I, Cummings JL, Chertkow H (2005) The montreal cognitive assessment, MoCA: a brief screening tool for mild cognitive impairment. J Am Geriatr Soc 53(4):695–699PubMedGoogle Scholar
  71. Njiokiktjien C, De Sonneville L, Hessels M, Kurgansky A, Vildavsky V, Vranken M (1997) Unimanual and bimanual simultaneous fingertapping in schoolchildren: developmental aspects and hand preference-related asymmetries. Laterality 2(2):117–135PubMedGoogle Scholar
  72. Oldfield RC (1971) The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 9(1):97–113PubMedGoogle Scholar
  73. Olejnik S, Li JM, Supattathum S, Huberty CJ (1997) Multiple testing and statistical power with modified Bonferroni procedures. J Educ Behav Stat 22(4):389–406Google Scholar
  74. Ota M, Obata T, Akine Y, Ito H, Ikehira H, Asada T, Suhara T (2006) Age-related degeneration of corpus callosum measured with diffusion tensor imaging. Neuroimage 31(4):1445–1452PubMedGoogle Scholar
  75. Pelletier J, Habib M, Lyoncaen O, Salamon G, Poncet M, Khalil R (1993) Functional and magnetic-resonance-imaging correlates of callosal involvement in multiple-sclerosis. Arch Neurol 50(10):1077–1082PubMedGoogle Scholar
  76. Picard N, Strick PL (2001) Imaging the premotor areas. Curr Opin Neurobiol 11(6):663–672PubMedGoogle Scholar
  77. Porciatti V, Fiorentini A, Morrone MC, Burr DC (1999) The effects of ageing on reaction times to motion onset. Vis Res 39(12):2157–2164PubMedGoogle Scholar
  78. Preilowski BF (1972) Possible contribution of the anterior forebrain commissures to bilateral motor coordination. Neuropsychologia 10(3):267–277PubMedGoogle Scholar
  79. Raz N, Rodrigue KM (2006) Differential aging of the brain: patterns, cognitive correlates and modifiers. Neurosci Biobehav Rev 30(6):730–748PubMedGoogle Scholar
  80. Sage CA, Van Hecke W, Peeters R, Sijbers J, Robberecht W, Parizel P, Marchal G, Leemans A, Sunaert S (2009) Quantitative diffusion tensor imaging in amyotrophic lateral sclerosis: revisited. Hum Brain Mapp 30(11):3657–3675PubMedGoogle Scholar
  81. Sala S, Agosta F, Pagani E, Copetti M, Comi G, Filippi M (2012) Microstructural changes and atrophy in brain white matter tracts with aging. Neurobiol Aging 33(3):488–498 e482PubMedGoogle Scholar
  82. Salat DH, Tuch DS, Greve DN, van der Kouwe AJW, Hevelone ND, Zaleta AK, Rosen BR, Fischl B, Corkin S, Rosas HD et al (2005) Age-related alterations in white matter microstructure measured by diffusion tensor imaging. Neurobiol Aging 26(8):1215–1227PubMedGoogle Scholar
  83. Salthouse TA, Czaja SJ (2000) Structural constraints on process explanations in cognitive aging. Psychol Aging 15(1):44–55PubMedGoogle Scholar
  84. Schluter ND, Rushworth MF, Passingham RE, Mills KR (1998) Temporary interference in human lateral premotor cortex suggests dominance for the selection of movements. A study using transcranial magnetic stimulation. Brain 121(5):785–799PubMedGoogle Scholar
  85. Serrien DJ, Swinnen SP, Stelmach GE (2000) Age-related deterioration of coordinated interlimb behavior. J Gerontol B Psychol Sci Soc Sci 55(5):P295–P303PubMedGoogle Scholar
  86. Serrien DJ, Strens LH, Oliviero A, Brown P (2002) Repetitive transcranial magnetic stimulation of the supplementary motor area (SMA) degrades bimanual movement control in humans. Neurosci Lett 328(2):89–92PubMedGoogle Scholar
  87. Sisti HM, Geurts M, Clerckx R, Gooijers J, Coxon JP, Heitger MH, Caeyenberghs K, Beets IA, Serbruyns L, Swinnen SP (2011) Testing multiple coordination constraints with a novel bimanual visuomotor task. PLoS One 6(8):e23619PubMedCentralPubMedGoogle Scholar
  88. Sisti HM, Geurts M, Gooijers J, Heitger MH, Caeyenberghs K, Beets IA, Serbruyns L, Leemans A, Swinnen SP (2012) Microstructural organization of corpus callosum projections to prefrontal cortex predicts bimanual motor learning. Learn Mem 19(8):351–357PubMedGoogle Scholar
  89. Smith EE (1968) Choice reaction time: an analysis of the major theoretical positions. Psychol Bull 69(2):77–110PubMedGoogle Scholar
  90. Snodgras JG, Luce RD, Galanter E (1967) Some experiments on simple and choice reaction time. J Exp Psychol 75(1):1–17Google Scholar
  91. Song SK, Sun SW, Ramsbottom MJ, Chang C, Russell J, Cross AH (2002) Dysmyelination revealed through MRI as increased radial (but unchanged axial) diffusion of water. Neuroimage 17(3):1429–1436PubMedGoogle Scholar
  92. Song SK, Sun SW, Ju WK, Lin SJ, Cross AH, Neufeld AH (2003) Diffusion tensor imaging detects and differentiates axon and myelin degeneration in mouse optic nerve after retinal ischemia. Neuroimage 20(3):1714–1722PubMedGoogle Scholar
  93. Song SK, Yoshino J, Le TQ, Lin SJ, Sun SW, Cross AH, Armstrong RC (2005) Demyelination increases radial diffusivity in corpus callosum of mouse brain. Neuroimage 26(1):132–140PubMedGoogle Scholar
  94. Stelmach GE, Sirica A (1986) Aging and proprioception. Age 9(4):99–103Google Scholar
  95. Stinear JW, Byblow WD (2002) Disinhibition in the human motor cortex is enhanced by synchronous upper limb movements. J Physiol Lond 543(1):307–316PubMedCentralPubMedGoogle Scholar
  96. Sullivan EV, Pfefferbaum A (2006) Diffusion tensor imaging and aging. Neurosci Biobehav Rev 30(6):749–761PubMedGoogle Scholar
  97. Sullivan EV, Adalsteinsson E, Hedehus M, Ju C, Moseley M, Lim KO, Pfefferbaum A (2001) Equivalent disruption of regional white matter microstructure in ageing healthy men and women. Neuroreport 12(1):99–104PubMedGoogle Scholar
  98. Sullivan EV, Adalsteinsson E, Pfefferbaum A (2006) Selective age-related degradation of anterior callosal fiber bundles quantified in vivo with fiber tracking. Cereb Cortex 16(7):1030–1039PubMedGoogle Scholar
  99. Sullivan EV, Rohlfing T, Pfefferbaum A (2010) Quantitative fiber tracking of lateral and interhemispheric white matter systems in normal aging: relations to timed performance. Neurobiol Aging 31(3):464–481PubMedCentralPubMedGoogle Scholar
  100. Summers JJ, Lewis J, Fujiyama H (2010) Aging effects on event and emergent timing in bimanual coordination. Hum Mov Sci 29(5):820–830PubMedGoogle Scholar
  101. Sun SW, Liang HF, Trinkaus K, Cross AH, Armstrong RC, Song SK (2006) Noninvasive detection of cuprizone induced axonal damage and demyelination in the mouse corpus callosum. Magn Reson Med 55(2):302–308PubMedGoogle Scholar
  102. Sun SW, Liang HF, Schmidt RE, Cross AH, Song SK (2007) Selective vulnerability of cerebral white matter in a murine model of multiple sclerosis detected using diffusion tensor imaging. Neurobiol Dis 28(1):30–38PubMedCentralPubMedGoogle Scholar
  103. Swinnen SP, Wenderoth N (2004) Two hands, one brain: cognitive neuroscience of bimanual skill. Trends Cogn Sci 8(1):18–25PubMedGoogle Scholar
  104. Swinnen SP, Verschueren SMP, Bogaerts H, Dounskaia N, Lee TD, Stelmach GE, Serrien DJ (1998) Age-related deficits in motor learning and differences in feedback processing during the production of a bimanual coordination pattern. Cogn Neuropsychol 15(5):439–466Google Scholar
  105. Takser L, Dellatolas G, Bowler R, Laplante N (2002) Predictive factors of manual dexterity and cognitive performance at 17 years: a 10-year longitudinal study in a rural area of France. Percept Mot Skills 95(1):15–26PubMedGoogle Scholar
  106. Tiffin J, Asher EJ (1948) The Purdue pegboard; norms and studies of reliability and validity. J Appl Psychol 32(3):234–247PubMedGoogle Scholar
  107. Tournier JD, Mori S, Leemans A (2011) Diffusion tensor imaging and beyond. Magn Reson Med 65(6):1532–1556PubMedCentralPubMedGoogle Scholar
  108. Tuch DS, Salat DH, Wisco JJ, Zaleta AK, Hevelone ND, Rosas HD (2005) Choice reaction time performance correlates with diffusion anisotropy in white matter pathways supporting visuospatial attention. Proc Natl Acad Sci USA 102(34):12212–12217PubMedCentralPubMedGoogle Scholar
  109. Van Hecke W, Leemans A, D’Agostino E, De Backer S, Vandervliet E, Parizel PM, Sijbers J (2007) Nonrigid coregistration of diffusion tensor images using a viscous fluid model and mutual information. IEEE Trans Med Imaging 26(11):1598–1612PubMedGoogle Scholar
  110. Van Hecke W, Sijbers J, De Backer S, Poot D, Parizel PM, Leemans A (2009) On the construction of a ground truth framework for evaluating voxel-based diffusion tensor MRI analysis methods. Neuroimage 46(3):692–707PubMedGoogle Scholar
  111. Van Hecke W, Nagels G, Leemans A, Vandervliet E, Sijbers J, Parizel PM (2010) Correlation of cognitive dysfunction and diffusion tensor MRI measures in patients with mild and moderate multiple sclerosis. J Magn Reson Imaging 31(6):1492–1498PubMedGoogle Scholar
  112. Verhoeven JS, Sage CA, Leemans A, Van Hecke W, Callaert D, Peeters R, De Cock P, Lagae L, Sunaert S (2010) Construction of a stereotaxic DTI atlas with full diffusion tensor information for studying white matter maturation from childhood to adolescence using tractography-based segmentations. Hum Brain Mapp 31(3):470–486PubMedGoogle Scholar
  113. Voineskos AN, Rajji TK, Lobaugh NJ, Miranda D, Shenton ME, Kennedy JL, Pollock BG, Mulsant BH (2012) Age-related decline in white matter tract integrity and cognitive performance: a DTI tractography and structural equation modeling study. Neurobiol Aging 33(1):21–34PubMedCentralPubMedGoogle Scholar
  114. Vos SB, Jones DK, Jeurissen B, Viergever MA, Leemans A (2012) The influence of complex white matter architecture on the mean diffusivity in diffusion tensor MRI of the human brain. Neuroimage 59(3):2208–2216PubMedGoogle Scholar
  115. Wang LE, Tittgemeyer M, Imperati D, Diekhoff S, Ameli M, Fink GR, Grefkes C (2012) Degeneration of corpus callosum and recovery of motor function after stroke: a multimodal magnetic resonance imaging study. Hum Brain Mapp 33(12):2941–2956PubMedGoogle Scholar
  116. Wedeen VJ, Wang RP, Schmahmann JD, Benner T, Tseng WY, Dai G, Pandya DN, Hagmann P, D’Arceuil H, de Crespigny AJ (2008) Diffusion spectrum magnetic resonance imaging (DSI) tractography of crossing fibers. Neuroimage 41(4):1267–1277PubMedGoogle Scholar
  117. Wiegell MR, Larsson HB, Wedeen VJ (2000) Fiber crossing in human brain depicted with diffusion tensor MR imaging. Radiology 217(3):897–903PubMedGoogle Scholar
  118. Wishart LR, Lee TD, Murdoch JE, Hodges NJ (2000) Effects of aging on automatic and effortful processes in bimanual coordination. J Gerontol B Psychol Sci Soc Sci 55(2):P85–P94PubMedGoogle Scholar
  119. Zahr NM, Rohlfing T, Pfefferbaum A, Sullivan EV (2009) Problem solving, working memory, and motor correlates of association and commissural fiber bundles in normal aging: a quantitative fiber tracking study. Neuroimage 44(3):1050–1062PubMedCentralPubMedGoogle Scholar
  120. Zhang Y, Du AT, Hayasaka S, Jahng GH, Hlavin J, Zhan W, Weiner MW, Schuff N (2010) Patterns of age-related water diffusion changes in human brain by concordance and discordance analysis. Neurobiol Aging 31(11):1991–2001PubMedCentralPubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  • L. Serbruyns
    • 1
  • J. Gooijers
    • 1
  • K. Caeyenberghs
    • 1
    • 2
  • R. L. Meesen
    • 1
    • 3
    • 4
  • K. Cuypers
    • 1
    • 3
    • 4
  • H. M. Sisti
    • 1
  • A. Leemans
    • 5
  • Stephan P. Swinnen
    • 1
    • 6
  1. 1.Motor Control Laboratory, Movement Control and Neuroplasticity Research Group, Biomedical Sciences GroupKU LeuvenHeverleeBelgium
  2. 2.Department of Physical Therapy and Motor Rehabilitation, Faculty of Medicine and Health SciencesUniversity of GhentGhentBelgium
  3. 3.REVAL Research Group, Department of Health Care SciencesPHL University CollegeHasseltBelgium
  4. 4.BIOMED, Biomedical Research InstituteHasselt UniversityDiepenbeekBelgium
  5. 5.Image Sciences InstituteUniversity Medical Center UtrechtUtrechtThe Netherlands
  6. 6.Leuven Research Institute for Neuroscience and Disease (LIND)KU LeuvenLeuvenBelgium

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