Hostname: page-component-76fb5796d-vfjqv Total loading time: 0 Render date: 2024-04-26T08:34:49.528Z Has data issue: false hasContentIssue false

Saccadic Adaptation in Chiari Type II Malformation

Published online by Cambridge University Press:  02 December 2014

Michael S. Salman*
Affiliation:
Division of Neurology, The Hospital for Sick Children, Toronto, ON and the Divisions of Neurology, Vision Science, Research Program, University Health Network, University of Toronto, Toronto, ON and the Section of Pediatric Neurology, Children's Hospital, University of Manitoba, Winnipeg, MB, Canada
James A. Sharpe
Affiliation:
Divisions of Neurology, Vision Science, Research Program, University Health Network, University of Toronto, Toronto, ON
Moshe Eizenman
Affiliation:
Department of Biomedical Engineering, University of Toronto, Toronto, ON
Linda Lillakas
Affiliation:
Division of Vision Science, Research Program, University Health Network, University of Toronto, Toronto, ON
Teresa To
Affiliation:
Division of Population Health Sciences, The Hospital for Sick Children, Toronto, ON
Carol Westall
Affiliation:
Divisions of Opthalmology and Vision Sciences, The Hospital for Sick Children, Toronto, ON
Martin J. Steinbach
Affiliation:
Divisions of Vision Science, Research Program, University Health Network, University of Toronto, Toronto, ON
Maureen Dennis
Affiliation:
Division of Psychology, The Hospital for Sick Children, Toronto, ON
*
Section of Pediatric Neurology, AE 108, Harry Medovy House, Children’s Hosptial, 820 Sherbrook St., Winnipeg, Manitoba, R3A 1R9, Canada
Rights & Permissions [Opens in a new window]

Abstract

Core share and HTML view are not available for this content. However, as you have access to this content, a full PDF is available via the ‘Save PDF’ action button.
Background:

Saccadic adaptation corrects errors in saccadic amplitude. Experimentally-induced saccadic adaptation provides a method for studying motor learning. The cerebellum is a major participant in saccadic adaptation. Chiari type II malformation (CII) is a developmental deformity of the cerebellum and brainstem that is associated with spina bifida. We investigated the effects of CII on saccadic adaptation.

Method:

We measured eye movements using an infrared eye tracker in 21 subjects with CII (CII group) and 39 typically developing children (control group), aged 8-19 years. Saccadic adaptation was induced experimentally using targets that stepped horizontally 12º to the right and then stepped backward 3º during saccades.

Results:

Saccadic adaptation was achieved at the end of the adaptation phase in participants in each group. Saccadic amplitude gain decreased by 6.9% in the CII group and 9.3% in the control group. The groups did not differ significantly (p = 0.27). Amplitude gain reduction was significantly less in the CII participants who had multiple shunt revisions. Regression analyses revealed no effects of spinal lesion level, presence of nystagmus, or cerebellar vermis dysmorphology on saccadic adaptation.

Conclusion:

The neural circuits involved in saccadic adaptation appear to be functionally intact in CII.

Résumé:

RÉSUMÉ:Contexte:

L’adaptation saccadique corrige les erreurs de l’amplitude saccadique. L’adaptation saccadique induite expérimentalement peut être utilisée pour étudier l’apprentissage moteur. Le cervelet participe de façon importante à l’adaptation saccadique. La malformation de Chiari de type II (CII) est une malformation du cervelet et du tronc cérébral qui est associée au spina bifida. Nous avons évalué les effets du CII sur l’adaptation saccadique.

Méthodes:

Nous avons mesuré les mouvements oculaires au moyen d’un oculomètre à infrarouge chez 21 sujets atteints de CII (groupe CII) et chez 39 enfants de 8 et 19 ans qui avaient un développement normal (groupe témoin). L’adaptation saccadique était induite expérimentalement au moyen de cibles qui se déplaçaient horizontalement de 12º vers la droite avec retour de 3º pendant les saccades.

Résultats:

L’adaptation saccadique était réussie à la fin de la phase d’adaptation chez les sujets des deux groupes. Le gain d’amplitude saccadique diminuait de 6,9% dans le groupe CII et de 9,3% dans le groupe témoin. Les groupes n’étaient pas significativement différents (p = 0,27). La diminution du gain d’amplitude était significativement moindre chez les sujets CII qui avaient eu de multiples reprises chirurgicales de leur dérivation. Les analyses de régression n’ont pas montré d’effet du niveau de la lésion spinale, de la présence de nystagmus ou de la dysmorphologie du vermis cérébelleux sur l’adaptation saccadique.

Conclusion:

Les circuits nerveux impliqués dans l’adaptation saccadique semblent intacts au point de vue fonctionnel dans le CII

Type
Original Articles
Copyright
Copyright © The Canadian Journal of Neurological 2006

References

1. Gilbert, JN, Jones, KL, Rorke, LB, Chernoff, GF, James, HE. 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;18:55964.CrossRefGoogle ScholarPubMed
2. 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;22:38593.Google Scholar
3. 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;282:182631.Google Scholar
4. Wagner, W, Schwarz, M, Perneczky, A. Primary myelomeningocele closure and consequences. Curr Opin Urol. 2002;12:4658.Google Scholar
5. Scudder, CA, Batourina, EY, Tunder, GS. Comparison of two methods of producing adaptation of saccade size and implications for the site of plasticity. J Neurophysiol. 1998;79:70415.Google Scholar
6. 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;19:109319.Google Scholar
7. Scudder, CA, McGee, DM. Adaptive modification of saccade size produces correlated changes in the discharges of fastigial nucleus neurons. J Neurophysiol. 2003;90:101126.Google Scholar
8. Desmurget, M, Pelisson, D, Urquizar, C, Prablanc, C, Alexander, GE, Grafton, ST. Functional anatomy of saccadic adaptation in humans. Nat Neurosci. 1998;1:5248.Google Scholar
9. Straube, A, Fuchs, AF, Usher, S, Robinson, FR. Characteristics of saccadic gain adaptation in rhesus macaques. J Neurophysiol. 1997;77:87495.Google Scholar
10. Waespe, W, Baumgartner, R. Enduring dysmetria and impaired gain adaptivity of saccade eye movements in Wallenberg’s lateral medullary syndrome. Brain. 1992;115:112546.Google Scholar
11. 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;127:110.Google Scholar
12. Thier, P, Dicke, PW, Haas, R, Barash, S. Encoding of movement time by populations of cerebellar Purkinje cells. Nature. 2000;405:726.Google Scholar
13. Thier, P, Dicke, PW, Haas, R, Thielert, CD, Catz, N. The role of the oculomotor vermis in the control of saccadic eye movements. Ann NY Acad Sci. 2002;978:5062.Google Scholar
14. Mclaughlin, SC. Parametric adjustment in saccadic eye movements. Percept Psychophys. 1967;2:35962.Google Scholar
15. Schweighofer, N, Arbib, MA, Dominey, PF. A model of the cerebellum in adaptive control of saccadic gain. I. The model and its biological substrate. Biol Cybern. 1996;75:1928.Google Scholar
16. Albano, JE, King, WM. Rapid adaptation of saccadic amplitude in humans and monkeys. Invest Ophthalmol Vis Sci. 1989;30:188393.Google Scholar
17. Deubel, H. Separate adaptive mechanisms for the control of reactive and volitional saccadic eye movements. Vision Res. 1995;35:352940.CrossRefGoogle ScholarPubMed
18. Salman, MS, Sharpe, JA, Eizenman, M, Lillakas, L, To, T, Westall, C, et al. Saccadic adaptation in children. J Child Neurol. (in press).Google Scholar
19. Salman, MS, Sharpe, JA, Eizenman, M, Lillakas, L, To, T, Westall, C, et al. Saccades in Children with Chiari type II malformation. Neurology. 2005;64:2098101.Google Scholar
20. Dennis, M, Fletcher, JM, Rogers, T, Hetherington, R, Francis, DJ. Object-based and action-based visual perception in children with spina bifida and hydrocephalus. J Int Neuropsychol Soc. 2002;8:95106.CrossRefGoogle ScholarPubMed
21. Van Allen, MI, Kalousek, DK, Chernoff, GF, Juriloff, D, Harris, M, McGillivray, BC, et al. Evidence for multi-site closure of the neural tube in humans. Am J Med Genet. 1993;47:72343.Google Scholar
22. Fletcher, JM, Dennis, M, Northrup, H, Barnes, MA, Hannay, HJ, Landry, SH, et al. Spina bifida: genes, brain, and development. Int Rev Res Ment Retard. 2004;29:63117.Google Scholar
23. Wills, KE. Neuropsychological functioning in children with spina bifida and/ or hydrocephalus. J Clin Child Psychol. 1993;22: 24765.Google Scholar
24. Dennis, M, Fitz, CR, Netley, CT, Sugar, J, Harwood-Nash, DC, Hendrick, EB, et al. The intelligence of hydrocephalic children. Arch Neurol. 1981;38:60715.Google Scholar
25. Hunt, GM. The Casey Holter lecture. Non-selective intervention in newborn babies with open spina bifida: the outcome 30 years on for the complete cohort. Eur J Pediatr Surg. 1999;9 Suppl 1:S58.Google Scholar
26. Mazur, JM, Aylward, GP, Colliver, J, Stacey, J, Menelaus, M. Impaired mental capabilities and hand function in myelomeningocele patients. Z Kinderchir. 1988;43 Suppl 2 :S247.Google Scholar
27. DiScenna, AO, Das, VE, Zivotofsky, AZ, Seidman, SH, Leigh, RJ. Evaluation of a video tracking device for measurement of horizontal and vertical eye rotations during locomotion. J Neurosci Meth. 1995;58:8994.Google Scholar
28. SPSS Inc. SPSS (Statistical Package for the Social Sciences) for windows: Chicago, IL, 2001.Google Scholar
29. Altman, DG. Practical statistics for medical research. London; New York: Chapman and Hall; 1995.Google Scholar
30. Hopp, JJ, Fuchs, AF. Investigating the site of human saccadic adaptation with express and targeting saccades. Exp Brain Res. 2002;144:53848.Google Scholar
31. Mezey, LE, Harris, CM. Adaptive control of saccades in children with dancing eye syndrome. Ann NY Acad Sci. 2002;956:44952.CrossRefGoogle ScholarPubMed
32. Robinson, FR. Role of the cerebellum in movement control and adaptation. Curr Opin Neurobiol. 1995;5:75562.Google Scholar
33. Straube, A, Deubel, H, Ditterich, J, Eggert, T. Cerebellar lesions impair rapid saccade amplitude adaptation. Neurology. 2001;57:21058.Google Scholar
34. Dennis, M, Edelstein, K, Frederick, J, Copeland, K, Francis, DJ, 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; 43:200010.Google Scholar
35. Hashimoto, M, Ohtsuka, K. Transcranial magnetic stimulation over the posterior cerebellum during visually guided saccades in man. Brain. 1995;118:118593.Google Scholar
36. Robinson, FR, Fuchs, AF, Noto, CT. Cerebellar influences on saccade plasticity. Ann NY Acad Sci. 2002;956:15563.CrossRefGoogle ScholarPubMed
37. Coesmans, M, Smitt, PA, Linden, DJ, Shigemoto, R, Hirano, T, Yamakawa, Y, et al. Mechanisms underlying cerebellar motor deficits due to mGluR1-autoantibodies. Ann Neurol. 2003;53:32536.Google Scholar
38. Huber-Okrainec, J, Dennis, M, Brettschneider, J, Spiegler, BJ. Neuromotor speech deficits in children and adults with spina bifida and hydrocephalus. Brain Lang. 2002;80:592602.CrossRefGoogle ScholarPubMed
39. 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;9:64252.Google Scholar
40. Edelstein, K, Dennis, M, Copeland, K, Frederick, J, Francis, DJ, Hetherington, CR, et al. Motor learning in children with spina bifida: Dissociation between performance level and acquisition rate. J Int Neuropsychol Soc. 2004;10:111.Google Scholar