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Cerebellar Motor Function in Spina Bifida Meningomyelocele

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Abstract

Spina bifida meningomyelocele (SBM), a congenital neurodevelopmental disorder, involves dysmorphology of the cerebellum, and its most obvious manifestations are motor deficits. This paper reviews cerebellar neuropathology and motor function across several motor systems well studied in SBM in relation to current models of cerebellar motor and timing function. Children and adults with SBM have widespread motor deficits in trunk, upper limbs, eyes, and speech articulators that are broadly congruent with those observed in adults with cerebellar lesions. The structure and function of the cerebellum are correlated with a range of motor functions. While motor learning is generally preserved in SBM, those motor functions requiring predictive signals and precise calibration of the temporal features of movement are impaired, resulting in deficits in smooth movement coordination as well as in the classical cerebellar triad of dysmetria, ataxia, and dysarthria. That motor function in individuals with SBM is disordered in a manner phenotypically similar to that in adult cerebellar lesions, and appears to involve similar deficits in predictive cerebellar motor control, suggests that age-based cerebellar motor plasticity is limited in individuals with this neurodevelopmental disorder.

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References

  1. Boulet SL, Gambrell D, Shin M, Honein MA, Mathews TJ. Racial/ethnic differences in the birth prevalence of spina bifida—United States, 1995–2005. JAMA. 2009;301(21):2203–4.

    CAS  Google Scholar 

  2. Koehler PJ, De Wever Z, Heerlen G. Neurology in Tulp’s observationes medicae. J Hist Neurosci. 1996;5:143–51.

    CAS  PubMed  Google Scholar 

  3. Lendon RG. Neuron population in the lumbosacral cord of myelomeningocele children. Dev Med Child Neurol Suppl. 1969;20:82–5.

    CAS  PubMed  Google Scholar 

  4. Lendon RG. Neuron population in the spinal cord of children with spina bifida and hydrocephalus. Dev Med Child Neurol. 1968;10(s15):50–4.

    Google Scholar 

  5. McEnery G, Borzyskowski M, Cox TC, Neville BG. The spinal cord in neurologically stable spina bifida: a clinical and MRI study. Dev Med Child Neurol. 1992;34(4):342–7.

    Article  CAS  PubMed  Google Scholar 

  6. Cleland J. Contributions to the study of spina bifida, encephalocoele, and anencephalus. J Anat Physiol. 1883;17:257–91.

    CAS  PubMed  Google Scholar 

  7. Arnett B. Arnold–Chiari malformation. Arch Neurol. 2003;60(6):898–900.

    Article  PubMed  Google Scholar 

  8. Pearce JMS. Arnold Chiari, or “Cruveilhier Cleland Chiari” malformation. J Neurol Neurosurg Psychiatry. 2000;68(1):8–13.

    Article  Google Scholar 

  9. Wagner WA, Schwarz MA, Perneczky AB. Primary myelomeningocele closure and consequences. Curr Opin Urol. 2002;12(6):465–8.

    Article  PubMed  Google Scholar 

  10. Barkovich AJ. Pediatric neuroimaging. 3rd ed. New York: Raven; 2000.

    Google Scholar 

  11. Harding B, Copp A. Malformations. In: Graham D, Lantos P, editors. Greenfield's neuropathology. London: Edward Arnold; 2002. p. 376–86.

    Google Scholar 

  12. Gilbert J, Jones K, Rorke L, Chemoff G, James H. Central nervous system anomalies associated with meningomyelocele, hydrocephalus, and the Arnold–Chiari malformation: reappraisal of theories regarding the pathogenesis of posterior neural tube closure defects. Neurosurgery. 1986;18:559–64.

    Article  CAS  PubMed  Google Scholar 

  13. Hannay HJ, Dennis M, Kramer L, Blaser S, Fletcher JM. Partial agenesis of the corpus callosum in spina bifida meningomyelocele and potential compensatory mechanisms. J Clin Exp Neuropsychol. 2009;31(2):180–94.

    Article  PubMed  Google Scholar 

  14. McLone DG, Dias MS. The Chiari II malformation: cause and impact. Childs Nerv Syst. 2003;19(7):540–50.

    Article  PubMed  Google Scholar 

  15. McLone DG, Knepper PA. The cause of Chiari II malformation: a unified theory. Pediatr Neurosci. 1989;15:1–12.

    Article  CAS  PubMed  Google Scholar 

  16. Bruner JP, Tulipan N, Paschall RL, Boehm FH, Walsh WF, Silva SR, et al. Fetal surgery for myelomeningocele and the incidence of shunt-dependent hydrocephalus. JAMA. 1999;282(19):1819–25.

    Article  CAS  PubMed  Google Scholar 

  17. Danzer E, Johnson M, Bebbington M, Simon E, Wilson R, Bilaniuk L, et al. Fetal head biometry assessed by fetal magnetic resonance imaging following in utero myelomeningocele repair. Fetal Diagn Ther. 2007;22(1):1–6.

    Article  PubMed  Google Scholar 

  18. Sutton LN, Adzick NS, Bilaniuk LT, Johnson MP, Crombleholme TM, Flake AW. Improvement in hindbrain herniation demonstrated by serial fetal magnetic resonance imaging following fetal surgery for myelomeningocele. JAMA. 1999;282(19):1826–31.

    Article  CAS  PubMed  Google Scholar 

  19. Danzer E, Finkel RS, Rintoul NE, Bebbington MW, Schwartz ES, Zarnow DM, et al. Reversal of hindbrain herniation after maternal–fetal surgery for myelomeningocele subsequently impacts on brain stem function. Neuropediatrics. 2008;39(06):359–62.

    Article  CAS  PubMed  Google Scholar 

  20. Boltshauser E, Schneider J, Kollias S, Waibel P, Weissert M. Vanishing cerebellum in myelomeningocoele. Eur J Paediatr Neurol. 2002;6(2):109–13.

    Article  PubMed  Google Scholar 

  21. Emery JL, Gadsdon DR. A quantitative study of the cell population of the cerebellum in children with myelomeningocele. Dev Med Child Neurol Suppl. 1975;35:20–5.

    PubMed  Google Scholar 

  22. Salman MS, Blaser SE, Sharpe JA, Dennis M. Cerebellar vermis morphology in children with spina bifida and Chiari type II malformation. Childs Nerv Syst. 2006;22(4):385–93.

    Article  PubMed  Google Scholar 

  23. Tsai T, Bookstein FL, Levey E, Kinsman SL. Chiari-II malformation: a biometric analysis. Eur J Pediatr Surg. 2002;12(S1):12–8.

    Article  Google Scholar 

  24. Juranek J, Dennis M, Cirino PT, El-Messidi L, Fletcher JM. The cerebellum in children with spina bifida and Chiari II malformation: quantitative volumetrics by region. Cerebellum. 2010;9(2):240–8.

    Article  PubMed  Google Scholar 

  25. Herweh C, Akbar M, Wengenroth M, Heiland S, Bendszus M, Stippich C. Reduced anisotropy in the middle cerebellar peduncle in Chiari-II malformation. Cerebellum. 2010 (in press).

  26. Harding BN, Copp AJ, editors. Malformations. 8th ed. London: Hodder Arnold; 2008.

    Google Scholar 

  27. Sav A. Pathological anatomy of spina bifida. In: Ozek MM, Cinalli G, Maixner W, editors. The spina bifida management and outcome. Milan: Springer; 2008.

    Google Scholar 

  28. Variend S, Emery JL. The pathology of the central lobes of the cerebellum in children with myelomeningocele. Dev Med Child Neurol. 1974;16(6 Suppl 32):99–106.

    CAS  PubMed  Google Scholar 

  29. Kuchukhidze G, Rauchenzauner M, Gotwald T, Janecke A, Trinka E. Hypoplasia of deep cerebellar nuclei in Joubert Syndrome. Pediatr Neurol. 2009;40(6):474–6.

    Article  PubMed  Google Scholar 

  30. Baumel Y, Jacobson GA, Cohen D. Implications of functional anatomy on information processing in the deep cerebellar nuclei. Frontiers in Cellular Neuroscience. 2009;3:14. doi:10.3389/neuro.03.014.2009.

    Article  PubMed  Google Scholar 

  31. Griffiths P, Wilkinson I, Variend S, Jones A, Paley M, Whitby E. Differential growth rates of the cerebellum and posterior fossa assessed by post mortem magnetic resonance imaging of the fetus: implications for the pathogenesis of the Chiari 2 deformity. Acta Radiol. 2004;45(2):236–42.

    Article  CAS  PubMed  Google Scholar 

  32. Raybaud C, Miller E. Radiological evaluation of myelomeningocele—Chiari II malformation. In: Ozek M, Cinalli G, Maixner W, editors. Spina bifida: management and outcome. Milan: Springer; 2008. p. 111–42.

    Chapter  Google Scholar 

  33. Juranek J, Salman MS. Anomalous development of brain structure and function in spina bifida myelomeningocele. Developmental Disorders and Research Reviews. 2010;16:23–30.

    Article  Google Scholar 

  34. Dennis M, Fitz C, Netley C, Sugar J, Harwood-Nash D, Hendrick E, et al. The intelligence of hydrocephalic children. Arch Neurol. 1981;38(10):607–15.

    CAS  PubMed  Google Scholar 

  35. Juranek J, Fletcher JM, Hasan KM, Breier JI, Cirino PT, Pazo-Alvarez P, et al. Neocortical reorganization in spina bifida. Neuroimage. 2008;40(4):1516–22.

    Article  PubMed  Google Scholar 

  36. Dennis M, Barnes MA. The cognitive phenotype of spina bifida meningomyelocele. Dev Disabil Res Rev. 2010;16(1):31–9.

    Article  PubMed  Google Scholar 

  37. Del Bigio MR. Neuropathology and structural changes in hydrocephalus. Dev Disabil Res Rev. 2010;16(1):16–22.

    Article  PubMed  Google Scholar 

  38. Warrington WB, Monsarrat K. A case of arrested development of the cerebellum and its peduncles with spina bifida and other developmental peculiarities in the cord. Brain. 1902;25:444–78.

    Article  Google Scholar 

  39. Turnbull FA. Syringomyelic complications of spina bifida. Brain. 1933;56:304–17.

    Article  Google Scholar 

  40. Schwartz ER. Characteristics of speech and language development in the child with myelomeningocele and hydrocephalus. J Speech Hear Disord. 1974;39:465–8.

    Google Scholar 

  41. Magnus JA. Congenital paralysis of both external recti treated by transplantation of eye muscles. Br J Ophthalmol. 1944;28(5):241–5.

    Article  CAS  PubMed  Google Scholar 

  42. Ivry RB, Richardson TC. Temporal control and coordination: the multiple timer model. Brain Cogn. 2002;48(1):117–32.

    Article  PubMed  Google Scholar 

  43. Combe G. On the functions of the cerebellum. London: Maclachlan & Stewart; 1838.

    Google Scholar 

  44. Babinski J. Sur le role du cervelet dans les actes volitionnels necessitant une succession rapide de mouvements. Revue Neurologique. 1902;10:1013–5.

    Google Scholar 

  45. Holmes G. The cerebellum of man. Brain. 1939;62:1–30.

    Article  Google Scholar 

  46. Williams EN, Broughton NS, Menelaus MB. Age-related walking in children with spina bifida. Dev Med Child Neurol. 1999;41(7):446–9.

    Article  CAS  PubMed  Google Scholar 

  47. Wallace SJ. The effect of upper-limb function on mobility of children with myelomeningocele. Dev Med Child Neurol Suppl. 1973;Suppl 29:84–91.

    Google Scholar 

  48. Karlsson A, Norrlin S, Silander HC, Dahl M, Lanshammar H. Amplitude and frequency analysis of force plate data in sitting children with and without MMC. Clin Biomech (Bristol, Avon). 2000;7:541–5.

    Article  Google Scholar 

  49. Norrlin S, Karlsson A, Ahlsten G, Lanshammar H, Silander HC, Dahl M. Force measurements of postural sway and rapid arm lift in seated children with and without MMC. Clin Biomech (Bristol, Avon). 2002;3:197–202.

    Article  Google Scholar 

  50. Dennis M, Salman MS, Jewell D, Hetherington R, Spiegler BJ, MacGregor DL, et al. Upper limb motor function in young adults with spina bifida and hydrocephalus. Childs Nerv Syst. 2009;25(11):1447–53.

    Article  CAS  PubMed  Google Scholar 

  51. Hoglund A, Norrlin S. Influence of dual tasks on sitting postural sway in children and adolescents with myelomeningocele. Gait Posture. 2009;30(4):424–30.

    Article  PubMed  Google Scholar 

  52. Jewell D, Fletcher JM, Mahy CE, Hetherington R, MacGregor D, Drake JM, et al. Upper limb cerebellar motor function in children with spina bifida. Childs Nerv Syst. 2010;26(1):67–73.

    Article  PubMed  Google Scholar 

  53. Grimm RA. Hand function and tactile perception in a sample of children with myelomeningocele. Am J Occup Ther. 1976;30(4):234–40.

    CAS  PubMed  Google Scholar 

  54. Muen WJ, Bannister CM. Hand function in subjects with spina bifida. Eur J Pediatr Surg. 1997;7 Suppl 1:18–22.

    Article  PubMed  Google Scholar 

  55. Norrlin S, Dahl M, Rosblad B. Control of reaching movements in children and young adults with myelomeningocele. Dev Med Child Neurol. 2004;46(1):28–33.

    Article  PubMed  Google Scholar 

  56. Fletcher J, Brookshire B, Bohan T, Brandt M, Davidson K. Early hydrocephalus. In: Rourke B, editor. Syndrome of nonverbal learning disabilities: neurodevelopmental manifestations. New York: Guilford; 1995. p. 206–38.

    Google Scholar 

  57. Hetherington R, Dennis M. Motor function profile in children with early onset hydrocephalus. Dev Neuropsychol. 1999;15(1):25–51.

    Article  Google Scholar 

  58. Lomax-Bream LE, Barnes M, Copeland K, Taylor HB, Landry SH. The impact of spina bifida on development across the first 3 years. Dev Neuropsychol. 2007;31(1):1–20.

    Article  PubMed  Google Scholar 

  59. Vinck A, Nijhuis-van der Sanden MW, Roeleveld NJ, Mullaart RA, Rotteveel JJ, Maassen BA. Motor profile and cognitive functioning in children with spina bifida. Eur J Paediatr Neurol. 2010;14(1):86–92.

    Article  PubMed  Google Scholar 

  60. Wills K. Neuropsychological functioning in children with spina bifida and/or hydrocephalus. J Clin Child Psychol. 1993;22(2):247–65.

    Article  Google Scholar 

  61. Zeiner HK, Prigatano GP, Pollay M, Biscoe CB, Smith RV. Ocular motility, visual acuity and dysfunction of neuropsychological impairment in children with shunted uncomplicated hydrocephalus. Childs Nerv Syst. 1985;1(2):115–22.

    Article  CAS  PubMed  Google Scholar 

  62. Anderson EM, Plewis I. Impairment of a motor skill in children with spina bifida cystica and hydrocephalus: an exploratory study. Br J Psychol. 1977;68(1):61–70.

    CAS  PubMed  Google Scholar 

  63. Hamilton A, Shah A. Physical hand function of the child with spina bifida-myelomeningocele. British Journal of Occupational Therapy. 1984;147–50.

  64. Turner A. Hand function in children with myelomeningocele. J Bone Joint Surg Br. 1985;67(2):268–72.

    CAS  PubMed  Google Scholar 

  65. Turner A. Upper-limb function of children with myelomeningocele. Dev Med Child Neurol. 1986;28(6):790–8.

    Article  CAS  PubMed  Google Scholar 

  66. Brunt D. Characteristics of upper limb movements in a sample of meningomyelocele children. Percept Mot Skills. 1980;51(2):431–7.

    CAS  PubMed  Google Scholar 

  67. Sandler AD, Macias M, Brown TT. The drawings of children with spina bifida: developmental correlations and interpretations. Eur J Pediatr Surg. 1993;3 Suppl 1:25–7.

    PubMed  Google Scholar 

  68. Soare P, Raimondi A. Intellectual and perceptual-motor characteristics of treated myelomeningocele children. Am J Dis Child. 1977;131(2):199–204.

    CAS  PubMed  Google Scholar 

  69. Pearson A, Carr J, Hallwell M. The handwriting of children with spina bifida. Z Kinderchir. 1988;43(S2):40–2.

    PubMed  Google Scholar 

  70. Ziviani J, Hayes A, Chant D. Handwriting: a perceptual-motor disturbance in children with myelomeningocele. Occup Ther J Res. 1990;10:12–26.

    Google Scholar 

  71. Blumenfeld H. Neuroanatomy through clinical cases. Sunderland: Sinauer; 2002.

    Google Scholar 

  72. Brown JR, Darley FL, Aronson AE. Ataxic dysarhria. Int J Neurol. 1970;7(2):302–18.

    CAS  PubMed  Google Scholar 

  73. Darley FL, Aronson AE, Brown JR. Differential diagnostic patterns of dysarthria. J Speech Hear Res. 1969;12(2):246–69.

    CAS  PubMed  Google Scholar 

  74. Dennis M, Hendrick EB, Hoffman HJ, Humphreys RP. Language of hydrocephalic children and adolescents. J Clin Exp Neuropsychol. 1987;9(5):593–621.

    Article  CAS  PubMed  Google Scholar 

  75. Huber-Okrainec J, Dennis M, Brettschneider J, Spiegler BJ. Neuromotor speech deficits in children and adults with spina bifida and hydrocephalus. Brain Lang. 2002;80(3):592–602.

    Article  PubMed  Google Scholar 

  76. Kent RD, Netsell R, Abbs JH. Acoustic characteristics of dysarthria associated with cerebellar disease. J Speech Hear Res. 1979;22(3):627–48.

    CAS  PubMed  Google Scholar 

  77. Ackermann H, Mathiak K, Ivry RB. Temporal organization of “internal speech” as a basis for cerebellar modulation of cognitive functions. Behav Cogn Neurosci Rev. 2004;3(1):14–22.

    Article  PubMed  Google Scholar 

  78. Caines E, Dahl M, Holmstrom G. Longterm oculomotor and visual function in spina bifida cystica: a population-based study. Acta Ophthalmol Scand. 2007;85(6):662–6.

    Article  PubMed  Google Scholar 

  79. Nishizaki T, Tamaki N, Nishida Y, Matsumoto S. Bilateral internuclear ophthalmoplegia due to hydrocephalus: a case report. Neurosurgery. 1985;17(5):822–5.

    Article  CAS  PubMed  Google Scholar 

  80. Arnold AC, Baloh RW, Yee RD, Hepler RS. Internuclear ophthalmoplegia in the Chiari type II malformation. Neurology. 1990;40(12):1850–4.

    CAS  PubMed  Google Scholar 

  81. Biglan AW. Ophthalmologic complications of meningomyelocele: a longitudinal study. Trans Am Ophthalmol Soc. 1990;88:389–462.

    CAS  PubMed  Google Scholar 

  82. Collard M, Strubel-Streicher D, Eber AM, Remy C. Oculomotor disorders associated with Arnold–Chiari malformations (author's transl). Rev Neurol (Paris). 1980;136(8–9):531–8.

    CAS  Google Scholar 

  83. Leigh R, Zee D. The neurology of eye movements. 4th ed. New York: Oxford University Press; 2006.

    Google Scholar 

  84. Lennerstrand G, Gallo J, Samuelsson L. Neuro-ophthalmological findings in relation to CNS lesions in patients with myelomeningocele. Dev Med Child Neurol. 1990;32(5):423–31.

    Article  CAS  PubMed  Google Scholar 

  85. Lennerstrand G, Gallo J. Neuro-ophthalmological evaluation of patients with myelomeningocele and Chiari malformations. Dev Med Child Neurol. 1990;32(5):415–22.

    Article  CAS  PubMed  Google Scholar 

  86. Longridge NS, Mallinson AI. Arnold–Chiari malformation and the otolaryngologist: place of magnetic resonance imaging and electronystagmography. Laryngoscope. 1985;95(3):335–9.

    CAS  PubMed  Google Scholar 

  87. Mossman SS, Bronstein AM, Gresty MA, Kendall B, Rudge P. Convergence nystagmus associated with Arnold–Chiari malformation. Arch Neurol. 1990;47(3):357–9.

    CAS  PubMed  Google Scholar 

  88. Spooner JW, Baloh RW. Arnold–Chiari malformation: improvement in eye movements after surgical treatment. Brain. 1981;104(Pt 1):51–60.

    Article  CAS  PubMed  Google Scholar 

  89. Salman MS, Sharpe JA, Eizenman M, Lillakas L, To T, Westall C, et al. Saccades in children with spina bifida and Chiari type II malformation. Neurology. 2005;64(12):2098–101.

    Article  CAS  PubMed  Google Scholar 

  90. Salman MS, Sharpe JA, Lillakas L, Dennis M, Steinbach MJ. The vestibulo-ocular reflex during active head motion in Chiari II malformation. Can J Neurol Sci. 2008;35(4):495–500.

    PubMed  Google Scholar 

  91. Salman MS, Sharpe JA, Lillakas L, Dennis M, Steinbach MJ. Visual fixation in Chiari type II malformation. J Child Neurol. 2009;24(2):161–5.

    Article  PubMed  Google Scholar 

  92. Salman MS, Sharpe JA, Lillakas L, Steinbach MJ, Dennis M. Smooth ocular pursuit in Chiari type II malformation. Dev Med Child Neurol. 2007;49(4):289–93.

    Article  PubMed  Google Scholar 

  93. Takagi M, Zee DS, Tamargo RJ. Effects of lesions of the oculomotor vermis on eye movements in primate: saccades. J Neurophysiol. 1998;80(4):1911–31.

    CAS  PubMed  Google Scholar 

  94. Fukushima K, Buharin EV, Fukushima J. Responses of floccular Purkinje cells to sinusoidal vertical rotation and effects of muscimol infusion into the flocculus in alert cats. Neurosci Res. 1993;17(4):297–305.

    Article  CAS  PubMed  Google Scholar 

  95. Yakusheva TA, Shaikh AG, Green AM, Blazquez PM, Dickman JD, Angelaki DE. Purkinje cells in posterior cerebellar vermis encode motion in an inertial reference frame. Neuron. 2007;54(6):973–85.

    Article  CAS  PubMed  Google Scholar 

  96. Desmurget M, Pelisson D, Grethe JS, Alexander GE, Urquizar C, Prablanc C, et al. Functional adaptation of reactive saccades in humans: a PET study. Exp Brain Res. 2000;132(2):243–59.

    Article  CAS  PubMed  Google Scholar 

  97. Barash S, Melikyan A, Sivakov A, Zhang M, Glickstein M, Thier P. Saccadic dysmetria and adaptation after lesions of the cerebellar cortex. J Neurosci. 1999;19(24):10931–9.

    CAS  PubMed  Google Scholar 

  98. Vaziri S, Diedrichsen J, Shadmehr R. Why does the brain predict sensory consequences of oculomotor commands? Optimal integration of the predicted and the actual sensory feedback. J Neurosci. 2006;26(16):4188–97.

    Article  CAS  PubMed  Google Scholar 

  99. Baier B, Stoeter P, Dieterich M. Anatomical correlates of ocular motor deficits in cerebellar lesions. Brain. 2009;132(Pt 8):2114–24.

    Article  CAS  PubMed  Google Scholar 

  100. Salman MS, Dennis M, Sharpe JA. The cerebellar dysplasia of Chiari II malformation as revealed by eye movements. Can J Neurol Sci. 2009;36(6):713–24.

    PubMed  Google Scholar 

  101. Salman MS, Sharpe JA, Eizenman M, Lillakas L, To T, Westall C, et al. Saccadic adaptation in Chiari type II malformation. Can J Neurol Sci. 2006;33(4):372–8.

    PubMed  Google Scholar 

  102. Colvin AN, Yeates KO, Enrile BG, Coury DL. Motor adaptation in children with myelomeningocele: comparison to children with ADHD and healthy siblings. J Int Neuropsychol Soc. 2003;9(04):642–52.

    Article  PubMed  Google Scholar 

  103. Edelstein K, Dennis M, Copeland K, Frederick J, Francis D, Hetherington R, et al. Motor learning in children with spina bifida: dissociation between performance level and acquisition rate. J Int Neuropsychol Soc. 2004;10(6):877–87.

    Article  PubMed  Google Scholar 

  104. Wiedenbauer G, Jansen-Osmann P. Mental rotation ability of children with spina bifida: what influence does manual rotation training have? Dev Neuropsychol. 2007;32(3):809–24.

    PubMed  Google Scholar 

  105. Dennis M, Jewell D, Edelstein K, Brandt ME, Hetherington R, Blaser SE, et al. Motor learning in children with spina bifida: intact learning and performance on a ballistic task. J Int Neuropsychol Soc. 2006;12(5):598–608.

    Article  PubMed  Google Scholar 

  106. Albus JS. A theory of cerebellar function. Math Biosci. 1971;10:25–61.

    Article  Google Scholar 

  107. Marr D. A theory of cerebellar cortex. J Physiol. 1969;202(2):437–70.

    CAS  PubMed  Google Scholar 

  108. Weiner MJ, Hallett M, Funkenstein HH. Adaptation to lateral displacement of vision in patients with lesions of the central nervous system. Neurology. 1983;33(6):766–72.

    CAS  PubMed  Google Scholar 

  109. Deuschl G, Toro C, Zeffiro T, Massaquoi S, Hallett M. Adaptation motor learning of arm movements in patients with cerebellar disease. J Neurol Neurosurg Psychiatry. 1996;60(5):515–9.

    Article  CAS  PubMed  Google Scholar 

  110. Doyon J, Benali H. Reorganization and plasticity in the adult brain during learning of motor skills. Curr Opin Neurobiol. 2005;15(2):161–7.

    Article  CAS  PubMed  Google Scholar 

  111. Doyon J, Penhune V, Ungerleider LG. Distinct contribution of the cortico-striatal and cortico-cerebellar systems to motor skill learning. Neuropsychologia. 2003;41(3):252–62.

    Article  PubMed  Google Scholar 

  112. Doyon J, Ungerleider LG. Functional anatomy of motor skill learning. In: Squire LR, Schacter DL, editors. The neuropsychology of memory. 3rd ed. New York: Guilford; 2002. p. 225–38.

    Google Scholar 

  113. Park J-W, Kim Y-H, Jang SH, Chang WH, C-h P, Kim ST. Dynamic changes in the cortico-subcortical network during early motor learning. NeuroRehabilitation. 2010;26(2):95–103.

    PubMed  Google Scholar 

  114. Orban P, Peigneux P, Lungu O, Albouy G, Breton E, Laberenne F, et al. The multifaceted nature of the relationship between performance and brain activity in motor sequence learning. Neuroimage. 2010;49(1):694–702.

    Article  PubMed  Google Scholar 

  115. Hasan KM, Sankar A, Halphen C, Kramer LA, Ewing-Cobbs L, Dennis M, et al. Quantitative diffusion tensor imaging and intellectual outcomes in spina bifida: laboratory investigation. J Neurosurg Pediatr. 2008;2(1):75–82.

    Article  PubMed  Google Scholar 

  116. Werner S, Bock O, Gizewski ER, Schoch B, Timmann D. Visuomotor adaptive improvement and aftereffects are impaired differentially following cerebellar lesions in SCA and PICA territory. Exp Brain Res. 2010;201(3):429–39.

    Article  PubMed  Google Scholar 

  117. Lewis PA, Miall RC. Distinct systems for automatic and cognitively controlled time measurement: evidence from neuroimaging. Curr Opin Neurobiol. 2003;13(2):250–5.

    Article  CAS  PubMed  Google Scholar 

  118. Krumhansl CL. Rhythm and pitch in music recognition. Psychol Bull. 2000;126(1):159–79.

    Article  CAS  PubMed  Google Scholar 

  119. Griffiths TD. The neural processing of complex sounds. Ann NY Acad Sci. 2001;930:133–42.

    Article  CAS  PubMed  Google Scholar 

  120. Dennis M, Edelstein K, Hetherington R, Copeland K, Frederick J, Blaser SE, et al. Neurobiology of perceptual and motor timing in children with spina bifida in relation to cerebellar volume. Brain. 2004;127(6):1292–301.

    Article  PubMed  Google Scholar 

  121. Dennis M, Hopyan T, Juranek J, Cirino PT, Hasan KM, Fletcher J. Strong-meter and weak-meter rhythm identification in spina bifida meningomyelocele and volumetric parcellation of rhythm-relevant cerebellar regions. Ann NY Acad Sci. 2009;1169:84–8.

    Article  PubMed  Google Scholar 

  122. Hopyan T, Schellenberg EG, Dennis M. Perception of strong-meter and weak-meter rhythms in children with spina bifida meningomyelocele. J Int Neuropsychol Soc. 2009;15(4):521–8.

    Article  PubMed  Google Scholar 

  123. Kotani S, Kawahara S, Kirino Y. Purkinje cell activity during learning a new timing in classical eyeblink conditioning. Brain Res. 2003;994(2):193–202.

    Article  CAS  PubMed  Google Scholar 

  124. Koekkoek SK, Hulscher HC, Dortland BR, Hensbroek RA, Elgersma Y, Ruigrok TJ, et al. Cerebellar LTD and learning-dependent timing of conditioned eyelid responses. Science. 2003;301(5640):1736–9.

    Article  CAS  PubMed  Google Scholar 

  125. Braitenberg V. Is the cerebellar cortex a biological clock in the millisecond range? Prog Brain Res. 1967;25:334–46.

    Article  CAS  PubMed  Google Scholar 

  126. Ivry RB. The representation of temporal information in perception and motor control. Curr Opin Neurobiol. 1996;6(6):851–7.

    Article  CAS  PubMed  Google Scholar 

  127. Molinari M, Leggio MG, Thaut MH. The cerebellum and neural networks for rhythmic sensorimotor synchronization in the human brain. Cerebellum. 2007;6(1):18–23.

    Article  PubMed  Google Scholar 

  128. Ivry RB, Keele SW. Timing functions of the cerebellum. J Cogn Neurosci. 1989;1:136–52.

    Article  Google Scholar 

  129. Ivry RB, Keele SW, Diener HC. Dissociation of the lateral and medial cerebellum in movement timing and movement execution. Exp Brain Res. 1988;73(1):167–80.

    Article  CAS  PubMed  Google Scholar 

  130. Mostofsky SH, Kunze JC, Cutting LE, Lederman HM, Denckla MB. Judgment of duration in individuals with ataxia-telangiectasia. Dev Neuropsychol. 2000;17(1):63–74.

    Article  CAS  PubMed  Google Scholar 

  131. Hetherington R, Dennis M, Spiegler B. Perception and estimation of time in long-term survivors of childhood posterior fossa tumors. J Int Neuropsychol Soc. 2000;6(6):682–92.

    Article  CAS  PubMed  Google Scholar 

  132. Lebrun-Guillaud G, Tillmann B, Justus T. Perception of tonal and temporal structures in chord sequences by patients with cerebellar damage. Music Percept. 2008;25:271–83.

    Article  Google Scholar 

  133. Schlerf JE, Spencer RM, Zelaznik HN, Ivry RB. Timing of rhythmic movements in patients with cerebellar degeneration. Cerebellum. 2007;6(3):221–31.

    Article  CAS  PubMed  Google Scholar 

  134. Bubic A, von Cramon DY, Schubotz RI. Prediction, cognition and the brain. Frontiers in Human Neuroscience. 2010;4:1–15.

    Google Scholar 

  135. Raichle ME. Two views of brain function. Trends Cogn Sci. 2010;14(4):180–90.

    Article  PubMed  Google Scholar 

  136. Blakemore SJ, Wolpert DM, Frith CD. Central cancellation of self-produced tickle sensation. Nat Neurosci. 1998;1(7):635–40.

    Article  CAS  PubMed  Google Scholar 

  137. Wolpert DM, Miall RC. Forward nodels for physiological motor control. Neural Netw. 1996;9(8):1265–79.

    Article  PubMed  Google Scholar 

  138. Gross L. Self-generated touch: a neural perspective. PLoS Biol. 2006;4(2):e48.

    Article  PubMed  Google Scholar 

  139. Sperry RW. Neural basis of the spontaneous optokinetic response produced by visual inversion. J Comp Physiol Psychol. 1950;43(6):482–9.

    Article  CAS  PubMed  Google Scholar 

  140. Kawato M, Kuroda T, Imamizu H, Nakano E, Miyauchi S, Yoshioka T. Internal forward models in the cerebellum: fMRI study on grip force and load force coupling. Prog Brain Res. 2003;142:171–88.

    Article  PubMed  Google Scholar 

  141. Mauk MD, Medina JF, Nores WL, Ohyama T. Cerebellar function: coordination, learning or timing? Curr Biol. 2000;10(14):R522–5.

    Article  CAS  PubMed  Google Scholar 

  142. Pollok B, Gross J, Kamp D, Schnitzler A. Evidence for anticipatory motor control within a cerebello-diencephalic-parietal network. J Cogn Neurosci. 2008;20(5):828–40.

    Article  PubMed  Google Scholar 

  143. Wolpert DM, Miall RC, Kawato M. Internal models in the cerebellum. Trends Cogn Sci. 1998;2(9):338–47.

    Article  CAS  PubMed  Google Scholar 

  144. Molinari M, Restuccia D, Leggio MG. State estimation, response prediction, and cerebellar sensory processing for behavioral control. Cerebellum. 2009;8(3):399–402.

    Article  PubMed  Google Scholar 

  145. McKinstry JL, Edelman GM, Krichmar JL. A cerebellar model for predictive motor control tested in a brain-based device. Proc Natl Acad Sci USA. 2006;103(9):3387–92.

    Article  CAS  PubMed  Google Scholar 

  146. Iacoboni M. Playing tennis with the cerebellum. Nat Neurosci. 2001;4(6):555–6.

    Article  CAS  PubMed  Google Scholar 

  147. Bastian AJ. Learning to predict the future: the cerebellum adapts feedforward movement control. Curr Opin Neurobiol. 2006;16(6):645–9.

    Article  CAS  PubMed  Google Scholar 

  148. Nowak DA, Timmann D, Hermsdorfer J. Dexterity in cerebellar agenesis. Neuropsychologia. 2007;45(4):696–703.

    Article  PubMed  Google Scholar 

  149. Bares M, Lungu OV, Husarova I, Gescheidt T. Predictive motor timing performance dissociates between early diseases of the cerebellum and Parkinson's disease. Cerebellum. 2010;9(1):124–35.

    Article  PubMed  Google Scholar 

  150. Torres E, Andersen R. Space-time separation during obstacle-avoidance learning in monkeys. J Neurophysiol. 2006;96(5):2613–32.

    Article  PubMed  Google Scholar 

  151. Thaut MH, Demartin M, Sanes JN. Brain networks for integrative rhythm formation. PLoS ONE. 2008;3(5):e2312.

    Article  PubMed  CAS  Google Scholar 

  152. Aziz-Zadeh L, Wilson SM, Rizzolatti G, Iacoboni M. Congruent embodied representations for visually presented actions and linguistic phrases describing actions. Curr Biol. 2006;16(18):1818–23.

    Article  CAS  PubMed  Google Scholar 

  153. Fischer MH, Zwaan RA. Embodied language: a review of the role of the motor system in language comprehension. Q J Exp Psychol. 2008;61(6):825–50.

    Article  Google Scholar 

  154. Glenberg AM, Kaschak MP. Grounding language in action. Psychon Bull Rev. 2002;9(3):558–65.

    PubMed  Google Scholar 

  155. Gallistel CR. The organization of action: a new synthesis. Hillsdale: Lawrence Erlbaum; 1980.

    Google Scholar 

  156. Poulet JF, Hedwig B. The cellular basis of a corollary discharge. Science. 2006;311(5760):518–22.

    Article  CAS  PubMed  Google Scholar 

  157. Blakemore SJ, Wolpert D, Frith C. Why can't you tickle yourself? NeuroReport. 2000;11(11):R11–6.

    Article  CAS  PubMed  Google Scholar 

  158. Hesse MD, Nishitani N, Fink GR, Jousmaki V, Hari R. Attenuation of somatosensory responses to self-produced tactile stimulation. Cereb Cortex. 2010;20(2):425–32.

    Article  PubMed  Google Scholar 

  159. Bays PM, Flanagan JR, Wolpert DM. Attenuation of self-generated tactile sensations is predictive, not postdictive. PLoS Biol. 2006;4(2):e28.

    Article  PubMed  Google Scholar 

  160. Bays PM, Wolpert DM, Flanagan JR. Perception of the consequences of self-action is temporally tuned and event driven. Curr Biol. 2005;15(12):1125–8.

    Article  CAS  PubMed  Google Scholar 

  161. Diedrichsen J, Hashambhoy Y, Rane T, Shadmehr R. Neural correlates of reach errors. J Neurosci. 2005;25(43):9919–31.

    Article  CAS  PubMed  Google Scholar 

  162. Isope P, Dieudonne S, Barbour B. Temporal organization of activity in the cerebellar cortex: a manifesto for synchrony. Ann NY Acad Sci. 2002;978:164–74.

    Article  PubMed  Google Scholar 

  163. Jacobson GA, Rokni D, Yarom Y. A model of the olivo-cerebellar system as a temporal pattern generator. Trends Neurosci. 2008;31(12):617–25.

    Article  CAS  PubMed  Google Scholar 

  164. Llinas R, Leznik E, Makarenko VI. On the amazing olivocerebellar system. Ann NY Acad Sci. 2002;978:258–72.

    Article  CAS  PubMed  Google Scholar 

  165. Peach B. Arnold–Chiari malformation: anatomic features of 20 cases. Arch Neurol. 1965;12:613–21.

    CAS  PubMed  Google Scholar 

  166. Bastian AJ. Understanding sensorimotor adaptation and learning for rehabilitation. Curr Opin Neurol. 2008;21(6):628–33.

    Article  PubMed  Google Scholar 

  167. Imamizu H, Miyauchi S, Tamada T, Sasaki Y, Takino R, Putz B, et al. Human cerebellar activity reflecting an acquired internal model of a new tool. Nature. 2000;403(6766):192–5.

    Article  CAS  PubMed  Google Scholar 

  168. Clower DM, West RA, Lynch JC, Strick PL. The inferior parietal lobule is the target of output from the superior colliculus, hippocampus, and cerebellum. J Neurosci. 2001;21(16):6283–91.

    CAS  PubMed  Google Scholar 

  169. Dennis M, Jewell D, Hetherington R, Burton C, Brandt ME, Blaser SE, et al. Verb generation in children with spina bifida. J Int Neuropsychol Soc. 2008;14(2):181–91.

    Article  PubMed  Google Scholar 

  170. Diedrichsen J, Criscimagna-Hemminger SE, Shadmehr R. Dissociating timing and coordination as functions of the cerebellum. J Neurosci. 2007;27(23):6291–301.

    Article  CAS  PubMed  Google Scholar 

  171. Sakai K, Hikosaka O, Nakamura K. Emergence of rhythm during motor learning. Trends Cogn Sci. 2004;8(12):547–53.

    Article  PubMed  Google Scholar 

  172. D'Angelo E, De Zeeuw CI. Timing and plasticity in the cerebellum: focus on the granular layer. Trends Neurosci. 2009;32(1):30–40.

    Article  PubMed  CAS  Google Scholar 

  173. Halligan PW, Fink GR, Marshall JC, Vallar G. Spatial cognition: evidence from visual neglect. Trends Cogn Sci. 2003;7(3):125–33.

    Article  PubMed  Google Scholar 

  174. Brozzoli C, Cardinali L, Pavani F, Farne A. Action-specific remapping of peripersonal space. Neuropsychologia. 2010;48(3):796–802.

    Article  CAS  PubMed  Google Scholar 

  175. Dennis M, Edelstein K, Frederick J, Copeland K, Francis D, Blaser SE, et al. Peripersonal spatial attention in children with spina bifida: associations between horizontal and vertical line bisection and congenital malformations of the corpus callosum, midbrain, and posterior cortex. Neuropsychologia. 2005;43(14):2000–10.

    Article  PubMed  Google Scholar 

  176. Poretti A, Prayer D, Boltshauser E. Morphological spectrum of prenatal cerebellar disruptions. Eur J Paediatr Neurol. 2009;13(5):397–407.

    Article  PubMed  Google Scholar 

  177. Baillieux H, De Smet HJ, Dobbeleir A, Paquier PF, De Deyn PP, Mariën P. Cognitive and affective disturbances following focal cerebellar damage in adults: a neuropsychological and SPECT study. Cortex. 2010;46(7):869–79.

    Article  PubMed  Google Scholar 

  178. Dennis M, Edelstein K, Copeland K, Frederick JA, Francis DJ, Hetherington R, et al. Space-based inhibition of return in children with spina bifida. Neuropsychology. 2005;19(4):456–65.

    Article  PubMed  Google Scholar 

  179. Huber-Okrainec J, Blaser SE, Dennis M. Idiom comprehension deficits in relation to corpus callosum agenesis and hypoplasia in children with spina bifida meningomyelocele. Brain Lang. 2005;93(3):349–68.

    Article  PubMed  Google Scholar 

  180. Fletcher JM, Copeland K, Frederick JA, Blaser SE, Kramer LA, Northrup H, et al. Spinal lesion level in spina bifida: a source of neural and cognitive heterogeneity. J Neurosurg Pediatr. 2005;102(3):268–79.

    Article  Google Scholar 

  181. Hasan K, Eluvathingal T, Kramer L, Ewing-Cobbs L, Dennis M, Fletcher J. White matter microstructural abnormalities in children with spina bifida myelomeningocele and hydrocephalus: a diffusion tensor tractography study of the association pathways. J Magn Reson Imaging. 2008;27(4):700–9.

    Article  PubMed  Google Scholar 

  182. Stoodley CJ, Schmahmann JD. Evidence for topographic organization in the cerebellum of motor control versus cognitive and affective processing. Cortex. 2010;46(7):831–44.

    Article  PubMed  Google Scholar 

  183. Fuentes CT, Bastian AJ. ‘Motor cognition’—what is it and is the cerebellum involved? Cerebellum. 2007;6(3):232–6.

    Article  PubMed  Google Scholar 

  184. Umilta C, Priftis K, Zorzi M. The spatial representation of numbers: evidence from neglect and pseudoneglect. Exp Brain Res. 2009;192(3):561–9.

    Article  PubMed  Google Scholar 

  185. Rizzolatti G, Sinigaglia C. The functional role of the parieto-frontal mirror circuit: interpretations and misinterpretations. Nat Rev Neurosci. 2010;11(4):264–74.

    Article  CAS  PubMed  Google Scholar 

  186. Ackermann H, Wildgruber D, Daum I, Grodd W. Does the cerebellum contribute to cognitive aspects of speech production? A functional magnetic resonance imaging (fMRI) study in humans. Neurosci Lett. 1998;247(2–3):187–90.

    Article  CAS  PubMed  Google Scholar 

  187. James KH. Sensori-motor experience leads to changes in visual processing in the developing brain. Dev Sci. 2010;13(2):279–88.

    Article  PubMed  Google Scholar 

  188. Dennis M, Landry SH, Barnes M, Fletcher JM. A model of neurocognitive function in spina bifida over the life span. J Int Neuropsychol Soc. 2006;12(02):285–96.

    Article  PubMed  Google Scholar 

  189. Barnes MA, Huber J, Johnston AM, Dennis M. A model of comprehension in spina bifida meningomyelocele: meaning activation, integration, and revision. J Int Neuropsychol Soc. 2007;13(5):854–64.

    Article  PubMed  Google Scholar 

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Acknowledgement

Preparation of this paper was supported in part by grant P01-HD35946 awarded from the Eunice Kennedy Shriver National Institute of Child Health and Human Development (NICHD). The content is solely the responsibility of the authors and does not necessarily represent the official views of the NICHD or the National Institutes of Health. We thank Alexandra Basile for assistance with the preparation of the manuscript.

Conflict of interest statement

There are no financial or personal relationships that might bias this work (e.g., consultancies, stock ownership, equity interests, and patent-licensing arrangements). No conflicts of interest exist.

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Dennis, M., Salman, M.S., Juranek, J. et al. Cerebellar Motor Function in Spina Bifida Meningomyelocele. Cerebellum 9, 484–498 (2010). https://doi.org/10.1007/s12311-010-0191-8

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