Hostname: page-component-6d856f89d9-sp8b6 Total loading time: 0 Render date: 2024-07-16T05:57:52.673Z Has data issue: false hasContentIssue false

The Cerebellar Dysplasia of Chiari II Malformation as Revealed by Eye Movements

Published online by Cambridge University Press:  02 December 2014

Michael S. Salman*
Affiliation:
Section of Pediatric Neurology, Children's Hospital, University of Manitoba, Winnipeg, Manitoba
Maureen Dennis
Affiliation:
Program in Neurosciences and Mental Health, The Hospital for Sick Children University of Toronto, Toronto, Ontario, Canada
James A. Sharpe
Affiliation:
Division of Neurology, University Health Network University of Toronto, Toronto, Ontario, Canada
*
Section of Pediatric Neurology, Children's Hospital, AE 308, 820 Sherbrook Street, 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.
Introduction:

Chiari type II malformation (CII) is a developmental deformity of the hindbrain. We have previously reported that many patients with CII have impaired smooth pursuit, while few make inaccurate saccades or have an abnormal vestibuloocular reflex. In contrast, saccadic adaptation and visual fixation are normal. In this report, we correlate results from several eye movement studies with neuroimaging in CII. We present a model for structural changes within the cerebellum in CII.

Methods:

Saccades, smooth pursuit, the vestibulo-ocular reflex, and visual fixation were recorded in 21 patients with CII, aged 8-19 years and 39 age-matched controls, using an infrared eye tracker. Qualitative and quantitative MRI data were correlated with eye movements in 19 CII patients and 28 controls.

Results:

Nine patients with CII had abnormal eye movements. Smooth pursuit gain was subnormal in eight, saccadic accuracy abnormal in four, and vestibulo-ocular reflex gain abnormal in three. None had fixation instability. Patients with CII had a significantly smaller cerebellar volume than controls, and those with normal eye motion had an expanded midsagittal vermis compared to controls. However, patients with abnormal eye movements had a smaller (non-expanded) midsagittal vermis area, posterior fossa area and medial cerebellar volumes than CII patients with normal eye movements.

Conclusions:

The deformity of CII affects the structure and function of the cerebellum selectively and differently in those with abnormal eye movements. We propose that the vermis can expand when compressed within a small posterior fossa in some CII patients, thus sparing its ocular motor functions.

Type
Other
Copyright
Copyright © The Canadian Journal of Neurological 2009

References

1.Fletcher, JM, McCauley, SR, Brandt, ME, Bohan, TP, Kramer, LA, Francis, DJ, et al.Regional brain tissue composition in children with hydrocephalus: relationships with cognitive development. Arch Neurol. 1996;53:54957.Google Scholar
2.McLone, DG, Knepper, PA.The cause of Chiari II malformation: Aaunified theory. Pediatr Neurosci. 1989;15:112.Google Scholar
3.Sarnat, HB.Molecular genetic classification of central nervous system malformations. J Child Neurol. 2000;15(10):67587.CrossRefGoogle ScholarPubMed
4.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.Google Scholar
5.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
6.Wagner, W, Schwarz, M, Perneczky, A.Primary myelomeningocele closure and consequences. Curr Opin Urol. 2002;12:4658.Google Scholar
7.Barkovich, AJ.Congenital malformations of the brain and skull / Congenital anomalies of the spine. In: Barkovich, AJ, editor. Pediatric neuroimaging. Philadelphia, PA: Lippincott Williams & Wilkins; 2000. p. 3307.Google Scholar
8.Hori, A.Chiari anomaly type II without cerebellar herniation. Acta Neuropathol. 2002;105:1934.CrossRefGoogle ScholarPubMed
9.Brocklehurst, G.A quantitative study of a spina bifida foetus. J Pathol. 1969;99:20511.CrossRefGoogle ScholarPubMed
10.Pilu, G, Romero, R, Reece, EA, Goldstein, I, Hobbins, JC, Bovicelli, L.Subnormal cerebellum in fetuses with spina bifida. Am J Obstet Gynecol. 1988;158:10526.Google Scholar
11.Sener, RN.Cerebellar agenesis versus vanishing cerebellum in Chiari II malformation. Comput Med Imaging Graph. 1995;19:4914.Google Scholar
12.Boltshauser, E, Schneider, J, Kollias, S, Waibel, P, Weissert, M.Vanishing cerebellum in myelomeningocele. Eur J Paediatr Neurol. 2002;6:10913.CrossRefGoogle Scholar
13.Emery, JL, Gadsdon, DR.A quantitative study of the cell population of the cerebellum in children with myelomeningocele. Dev Med Child Neurol. 1975;15 Suppl 29:205.Google Scholar
14.Variend, S, Emery, JL.The weight of the cerebellum in children with myelomeningocele. Dev Med Child Neurol. 1973:15(Suppl 29): 7783.Google Scholar
15.Harding, BN, Copp, AJ.Malformations. In: Graham, DI, Lantos, PL, editors. Greenfield’s neuropathology. London: Edward Arnold; 2002. p. 37686.Google Scholar
16.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
17.Salman, MS.The cerebellum: it’s about time! But timing is not everything: new insights into the role of the cerebellum in timing motor and cognitive tasks. J Child Neurol. 2002;17:19.Google Scholar
18.Ivry, RB, Keele, SW, Diener, HC.Dissociation of the lateral and medial cerebellum in movement timing and movement execution. Exp Brain Res. 1988;73:16780.Google Scholar
19.Mauk, MD, Medina, JF, Nores, WL, Ohyama, T.Cerebellar function: coordination, learning or timing? Curr Biol. 2000;10:R5225.Google Scholar
20.Bloedel, JR, Bracha, V, Larson, PS.Real time operations of the cerebellar cortex. Can J Neurol Sci. 1993;20 Suppl 3:S718.Google ScholarPubMed
21.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.Google Scholar
22.Wallace, SJ.The effect of upper-limb function on mobility of children with myelomeningocele. Dev Med Child Neurol. 1973;15 Suppl 29:8491.Google Scholar
23.Lennerstrand, G, Gallo, JE.Neuro-ophthalmological evaluation of patients with myelomeningocele and Chiari malformations. Dev Med Child Neurol. 1990;32:41522.CrossRefGoogle ScholarPubMed
24.Lennerstrand, G, Gallo, JE, Samuelsson, L.Neuro-ophthalmological findings in relation to CNS lesions in patients with myelomeningocele. Dev Med Child Neurol. 1990;32:42331.Google Scholar
25.Biglan, AW.Ophthalmological complications of meningomyelocele: A longitudinal study. Trans Am Ophthalmol Soc. 1990;88:389462.Google Scholar
26.Leigh, RJ, Zee, DS.The neurology of eye movements, 4th ed. New York: Oxford University Press; 2006. p. 2053.Google Scholar
27.Wills, KE.Neuropsychological functioning in children with spina bifida and/ or hydrocephalus. J Clin Child Psychol. 1993;22:24765.Google Scholar
28.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.CrossRefGoogle ScholarPubMed
29.Salman, MS.The cerebellum in Chiari type II malformation. Neuroembryol Aging. 2008;5:1422.Google Scholar
30.Daroff, RB.A personal introduction to eye movements. Ann NY Acad Sci. 2002;956:16.Google Scholar
31.Takagi, M, Zee, DS, Tamargo, RJ.Effects of lesions of the oculomotor vermis on eye movements in primate: saccades. J Neurophysiol. 1998;80:191131.CrossRefGoogle ScholarPubMed
32.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;17:297305.CrossRefGoogle ScholarPubMed
33.Yakusheva, T, Shaikh, A, Green, A, Blazquez, P, Dickman, J, Angelaki, D.Purkinje cells in posterior cerebellar vermis encode motion in an inertial reference frame. Neuron. 2007;54:97385.CrossRefGoogle Scholar
34.Mossman, SS, Bronstein, AM, Gresty, MA, Kendall, B, Rudge, P.Convergence nystagmus associated with Arnold-Chiari malformation. Arch Neurol. 1990;47:3579.CrossRefGoogle ScholarPubMed
35.Collard, M, Strubel-Streicher, D, Eber, AM, Remy, C.Les troubles oculomoteurs dans les malformations d’Arnold-Chiari. Rev Neurol. 1980;136:5318.Google Scholar
36.Nishizaki, T, Tamaki, N, Nishida, Y, Matsumoto, S.Bilateral internuclear ophthalmoplegia due to hydrocephalus: a case report. Neurosurgery. 1985;17:8225.CrossRefGoogle ScholarPubMed
37.Arnold, AC, Baloh, RW, Yee, RD, Hepler, RS.Internuclear ophthalmoplegia in the Chiari type II malformation. Neurology. 1990;40:18504.Google Scholar
38.Spooner, JW, Baloh, RW.Arnold-Chiari malformation: improvement in eye movements after surgical treatment. Brain. 1981;104:5160.CrossRefGoogle ScholarPubMed
39.Longridge, NS, Mallinson, AI.Arnold-Chiari malformation and the otolaryngologist: Place of magnetic resonance imaging and electronystagmography. Laryngoscope. 1985;95:3359.Google Scholar
40.Pieh, C, Gottlob, I.Arnold-Chiari malformation and nystagmus of skew. J Neurol Neurosurg Psychiatry. 2000;69:1246.Google Scholar
41.Lewis, AR, Kline, LB, Sharpe, JA.Acquired esotropia in Arnold Chiari I malformation. J Neuroophthalmol. 1996;16:4954.Google Scholar
42.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;64:2098101.Google Scholar
43.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;33:3728.Google Scholar
44.Salman, MS, Sharpe, JA, Lillakas, L, Steinbach, MJ, Dennis, M.Smooth ocular pursuit in Chiari type II malformation. Dev Med Child Neurol. 2007;49:28993.Google Scholar
45.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):495500.CrossRefGoogle ScholarPubMed
46.Salman, MS, Sharpe, JA, Lillakas, L, Dennis, M, Steinbach, MJ.Visual fixation in Chiari type II malformation. J Child Neurol. 2009;24:1615.Google Scholar
47.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
48.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.Google Scholar
49.Altman, DG.Practical statistics for medical research. New York: Chapman and Hall London; 1995.Google Scholar
50.Salman, MS, Blaser, S, Sharpe, JA, Dennis, M.Cerebellar vermis morphology in children with spina bifida and Chiari type II malformation. Childs Nerv Syst. 2006;22(4):38593.Google Scholar
51.Tsai, T, Bookstein, FL, Levey, E, Kinsman, SL.Chiari-II malformation: a biometric analysis. Eur J Pediatr Surg. 2002;12 Suppl 1:S128.Google Scholar
52.Nitschke, MF, Binkofski, F, Buccino, G, Posse, S, Erdmann, C, Köpf, D, et al.Activation of cerebellar hemispheres in spatial memorization of saccadic eye movements: an fMRI study. Hum Brain Mapp. 2004;22(2):15564.CrossRefGoogle ScholarPubMed
53.Straube, A, Scheuerer, W, Eggert, T.Unilateral cerebellar lesions affect initiation of ipsilateral smooth pursuit eye movements in humans. Ann Neurol. 1997;42(6):8918.Google Scholar
54.Dieterich, M, Bucher, SF, Seelos, KC, Brandt, T.Cerebellar activation during optokinetic stimulation and saccades. Neurology. 2000;54(1):14855.Google Scholar
55.Ohki, M, Kitazawa, H, Hiramatsu, T, Kaga, K, Kitamura, T, Yamada, J, et al.J Neurophysiol. 2009;101(2):93447.Google Scholar
56.Takagi, M, Zee, DS, Tamargo, RJ.Effects of lesions of the oculomotor cerebellar vermis on eye movements in primate: smooth pursuit. J Neurophysiol. 2000;83:204762.Google Scholar
57.Fletcher, JM, Dennis, M, Northrup, H, Barnes, MA.Hannay, HJ, Landry, S, et al.Spina bifida: genes, brain, and development. Int Rev Res Ment Retard. 2004;29:63117.Google Scholar
58.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
59.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
60.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):598608.Google Scholar