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Motor learning in children with spina bifida: Intact learning and performance on a ballistic task

Published online by Cambridge University Press:  08 September 2006

MAUREEN DENNIS
Affiliation:
Brain and Behaviour Program, The Hospital for Sick Children, Toronto, Ontario, Canada Department of Surgery, University of Toronto, Toronto, Ontario, Canada Department of Psychology, University of Toronto, Toronto, Ontario, Canada
DERRYN JEWELL
Affiliation:
Brain and Behaviour Program, The Hospital for Sick Children, Toronto, Ontario, Canada
KIM EDELSTEIN
Affiliation:
Brain and Behaviour Program, The Hospital for Sick Children, Toronto, Ontario, Canada
MICHAEL E. BRANDT
Affiliation:
Center for Computational Biomedicine, University of Texas Health Science Center, Houston, Texas
ROSS HETHERINGTON
Affiliation:
Department of Psychology, University of Toronto, Toronto, Ontario, Canada Community Health Systems Resource Group, The Hospital for Sick Children, Toronto, Ontario, Canada
SUSAN E. BLASER
Affiliation:
Department of Radiology, The Hospital for Sick Children, Toronto, Ontario, Canada
JACK M. FLETCHER
Affiliation:
Department of Psychology, University of Houston, Houston, Texas

Abstract

Learning and performance on a ballistic task were investigated in children with spina bifida meningomyelocele (SBM), with either upper level spinal lesions (n = 21) or lower level spinal lesions (n = 81), and in typically developing controls (n = 35). Participants completed three phases (20 trials each) of an elbow goniometer task that required a ballistic arm movement to move a cursor to one of two target positions on a screen, including (1) an initial learning phase, (2) an adaptation phase with a gain change such that recalibration of the ballistic arm movement was required, and (3) a learning reactivation phase under the original gain condition. Initial error rate, asymptotic error rate, and learning rate did not differ significantly between the SBM and control groups. Relative to controls, the SBM group had reduced volumes in the cerebellar hemispheres and pericallosal gray matter (the region including the basal ganglia), although only the pericallosal gray matter was significantly correlated with motor adaptation. Congenital cerebellar dysmorphology is associated with preserved motor skill learning on voluntary, nonreflexive tasks in children with SBM, in whom the relative roles of the cerebellum and basal ganglia may differ from those in the adult brain. (JINS, 2006, 12, 598–608.)

Type
Research Article
Copyright
© 2006 The International Neuropsychological Society

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References

REFERENCES

Albus, J.S. (1971). A theory of cerebellar function. Mathematical Biosciences, 10, 2561.CrossRefGoogle Scholar
Barkovich, A.J. (2000). Pediatric neuroimaging (3rd ed.). New York: Raven Press.
Beery, K.E. (1989). The developmental test of visual-motor integration (3rd Rev.). Cleveland, OH: Modern Curriculum Press.
Brandt, M.E., Bohan, T.P., Kramer, L.A., & Fletcher, J.M. (1994). Estimation of CSF, white and gray matter volumes in hydrocephalic children using fuzzy clustering of MR images. Computerized Medical Imaging and Graphics, 18, 2534.CrossRefGoogle Scholar
Brandt, M.E., Bohan, T.P., Thorstad, K., Beaver, S.R., Davidson, K.C., Francis, D.J., Kramer, L.A., & Fletcher, J.M. (1996). Reliability of brain structure morphometry in hydrocephalic children using MR images. Magnetic Resonance Imaging, 14, 649655.CrossRefGoogle Scholar
Brandt, M.E., Fletcher, J.M., & Bohan, T.P. (1992). Estimation of CSF, white, and gray matter volumes from MRIs of hydrocephalic and HIV-positive subjects. Proceedings of SimTec/WNN, 643650.
Colvin, A.N., Yeates, K.O., Enrile, B.G., & Coury, D.L. (2003). Motor adaptation in children with myelomeningocele: Comparison to children with ADHD and healthy siblings. Journal of the International Neuropsychological Society, 9, 642652.Google Scholar
del Bigio, M. (1993). Neuropathological changes caused by hydrocephalus. Acta Neuropathologica, 18, 573585.CrossRefGoogle Scholar
Dennis, M., Edelstein, K., Hetherington, R., Copeland, K., Frederick, J., Blaser, S.E., Kramer, L.A., Drake, J.M., Brandt, M., & Fletcher, J.M. (2004). Neurobiology of perceptual and motor timing in children with spina bifida in relation to cerebellar volume. Brain, 127, 12921301.Google Scholar
Dennis, M., Landry, S.H., Barnes, M., & Fletcher, J.M. (2006). A model of neurocognitive function in spina bifida over the life span. Journal of the International Neuropsychological Society, 12, 285296.Google Scholar
Desmurget, M., Grafton, S.T., Vindras, P., Gréa, H., & Turner, R.S. (2004). The basal ganglia network mediates the planning of movement amplitude. European Journal of Neuroscience, 19, 28712880.Google Scholar
Deuschl, G., Toro, C., Zeffiro, T., Massaquoi, S., & Hallett, M. (1996). Adaptation motor learning of arm movements in patients with cerebellar disease. Journal of Neurology, Neurosurgery, and Psychiatry, 60, 515519.Google Scholar
Doyon, J. & Benali, H. (2005). Reorganization and plasticity in the adult brain during learning of motor skills. Current Opinion in Neurobiology, 15, 161167.CrossRefGoogle Scholar
Doyon, J., Penhune, V., & Ungerleider, L.G. (2003). Distinct contribution of the cortico-striatal and cortico-cerebellar systems to motor skill learning. Neuropsychologia, 41, 252262.Google Scholar
Doyon, J. & Ungerleider, L.G. (2002). Functional anatomy of motor skill learning. In L.R. Squire & D.L. Schacter (Eds.), Neuropsychology of memory (3rd ed.). (pp. 225238). New York: Guilford Press.
Edelstein, K., Dennis, M., Copeland, K., Frederick, J., Francis, D., Hetherington, R., Brandt, M.E., & Fletcher, J.M. (2004). Motor learning in children with spina bifida: Dissociation between performance level and acquisition rate. Journal of the International Neuropsychological Society, 10, 111.Google Scholar
Filipek, P., Richelme, C., Kennedy, D., Rademacher, J., Pitcher, D., Zidel, S., & Caviness, V.S. (1992). Morphometric analysis of the brain in developmental language disorders and autism. Annals of Neurology, 32, 475.Google Scholar
Fletcher, J.M., Copeland, K., Frederick, J.A., Blaser, S.E., Kramer, L.A., Northrup, H., Hannay, H.J., Brandt, M.E., Francis, D.J., Villareal, G., Drake, J., Laurent, J.P., Townsend, I., Inwood, S., Boudousquie, A., & Dennis, M. (2005). Spinal lesion level in spina bifida: A source of neural and cognitive heterogeneity. Journal of Neurosurgery: Pediatrics, 102, 268279.Google Scholar
Graybiel, A.M. (2005). The basal ganglia: Learning new tricks and loving it. Current Opinion in Neurobiology, 15, 638644.CrossRefGoogle Scholar
Grimm, R.A. (1976). Hand function and tactile perception in a sample of children with myelomeningocele. American Journal of Occupational Therapy, 30, 234240.Google Scholar
Hetherington, R. & Dennis, M. (1999). Motor function profile in children with early onset hydrocephalus. Developmental Neuropsychology, 15, 2551.CrossRefGoogle Scholar
Ivry, R. & Keele, S. (1989). Timing functions of the cerebellum. Journal of Cognitive Neuroscience, 1, 136151.CrossRefGoogle Scholar
Ivry, R.B., Keele, S.W., & Diener, H.C. (1988). Dissociation of the lateral and medial cerebellum in movement timing and movement execution. Experimental Brain Research, 73, 167180.Google Scholar
Keating, J.G. & Thach, W.T. (1990). Cerebellar motor learning: Quantitation of movement adaptation and performance in rhesus monkeys and humans implicates cortex as the site of adaptation. Society for Neuroscience Abstracts, 16, 762.Google Scholar
Keating, J.G. & Thach, W.T. (1991). The cerebellar cortical area required for the adaptation of the monkey's “JUMP” task is lateral, localized, and small. Society for Neuroscience Abstracts, 17, 1381.Google Scholar
Leigh, R.G. & Zee, D.S. (1999). The neurology of eye movements (3rd ed.). New York: Oxford University Press.
Madsen, J.R., Young Poussaint, T., & Barnes, P.D. (2002). Congenital malformations of the cerebellum and posterior fossa. In M-U. Manto & M. Pandolfo (Eds.), The cerebellum and its disorders (pp. 161177). Cambridge: Cambridge University Press.
Mangels, J.A., Ivry, R.B., & Shimizu, N. (1998). Dissociable contributions of the prefrontal and neocerebellar cortex to time perception. Cognitive Brain Research, 7, 1539.CrossRefGoogle Scholar
Marr, D. (1969). A theory of cerebellar cortex. Journal of Physiology, 202, 437470.CrossRefGoogle Scholar
Nichelli, P., Alway, D., & Grafman, J. (1996). Perceptual timing in cerebellar degeneration. Neuropsychologia, 34, 863871.CrossRefGoogle Scholar
Park, C.H., Stewart, W., Khoury, M.J., & Mulinare, J. (1992). Is there etiologic heterogeneity between upper and lower neural tube defects? American Journal of Epidemiology, 136, 14911493.Google Scholar
Pao, Y-H. (1989). Adaptive pattern recognition and neural networks. Reading, MA: Addison Wesley.
Penhune, V.B., Zattore, R.J., & Evans, A.C. (1998). Cerebellar contributions to motor timing: A PET study of auditory and visual rhythm reproduction. Journal of Cognitive Neuroscience, 10, 752765.Google Scholar
Rao, S.M., Harrington, D.L., Haaland, K.Y., Bobholz, J.A., Cox, R.W., & Binder, J.R. (1997). Distributed neural systems underlying the timing of movements. Journal of Neuroscience, 17, 55285535.Google Scholar
Salman, M.S., Blaser, S.E., Sharpe, J.A., & Dennis, M. (2006). Cerebellar vermis morphology in children with spina bifida and Chiari type II malformation. Child's Nervous System, 22, 385393.Google Scholar
Salman, M.S., Sharpe, J.A., Eizenman, M., Lillakas, L., To, T., Westall, C., Steinbach, M.J., & Dennis, M., (in press). Saccadic adaptation in Chiari type II malformation. Canadian Journal of Neurological Sciences.
Salman, M.S., Sharpe, J.A., Lillakas, L., Steinbach, M.J., & Dennis, M. (2005). Smooth pursuit in children with Chiari type II malformation and spina bifida. Annals of Neurology, 58(Suppl. 9), S130.Google Scholar
Seidler, R.D., Purushotham, A., Kim, S.-G., Uğurbil, K., Willingham, D., & Ashe, J. (2002). Cerebellum activation associated with performance change but not motor learning. Science, 296, 20432046.CrossRefGoogle Scholar
Swanson, J.M. (1992). School-based assessments and interventions for students with ADHD. Irvine, CA: KC Press.
Thach, W.T. (1998). A role for the cerebellum in learning movement coordination. Neurobiology of Learning and Memory, 70, 177188.Google Scholar
Thorndike, R.L., Hagen, E.P., & Sattler, J.M. (1986). The Stanford-Binet Intelligence Scale (4th ed.). Itasca, IL: Riverside.
Weiner, M.J., Hallett, M., & Funkenstein, H.H. (1983). Adaptation to lateral displacement of vision in patients with lesions of the central nervous system. Neurology, 33, 766772.Google Scholar
Willingham, D.B. (1998). A neuropsychological theory of motor skill learning. Psychological Review, 105, 558584.CrossRefGoogle Scholar