Skip to main content
SpringerLink
Log in

Functional Consequences of Oculomotor Disorders in Hereditary Cerebellar Ataxias

  • Original Paper
  • Published:
The Cerebellum Aims and scope Submit manuscript

Abstract

Saccadic eye movements are traditionally cited as an especially successful combination of accuracy and velocity, such high level of performances being believed to be crucial for optimal vision. Although the structures subtending these properties are now well recognized, very little is known about the functional consequences on visually guided behaviors of reduced saccade performances, i.e., slowness and/or inaccuracy. We therefore investigated the impact of such impairments in patients with spino-cerebellar and Friedreich ataxia, i.e., diseases known to affect both saccade parameters. Subjects performed a classical eye movement task, in order to quantify saccade inaccuracy and/or slowness, a visually search task and a reading task and completed a questionnaire designed to evaluate their perceived visual discomfort in daily activities. The first main result was that saccade impairments did have an impact on visually guided behaviors, resulting in an increased time for target detection, especially when accurate foveation was needed, and in an increased reading time. The main responsible oculomotor factor was increased variability of saccade accuracy, and the least responsible factor was reduced saccade velocity. The second main result was that saccade disorders did not induce significant subjective discomfort, since no correlations were found between the results of the questionnaire and saccade parameters. These results emphasize the functional impact of increased variable error of saccade accuracy and question the rationale of high saccade velocities. The discrepancy between objective and subjective measures underlines the largely unconscious aspect of saccade control and leads us to consider the need for an adapted therapy.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  1. Leigh RJ, Zee DS. The neurology of eye movements. New York: Oxford University Press; 2006.

    Google Scholar 

  2. Spieker S, Schulz JB, Petersen D, et al. Fixation instability and oculomotor abnormalities in Friedreich’s ataxia. J Neurol. 1995;242:517–21.

    Article  PubMed  CAS  Google Scholar 

  3. Klostermann W, Zühlke C, Heide W, et al. Slow saccades and other eye movement disorders in spinocerebellar atrophy type 1. J Neurol. 1997;244:105–11.

    Article  PubMed  CAS  Google Scholar 

  4. Buttner N, Geschwind D, Jen JC, et al. Oculomotor phenotypes in autosomal dominant ataxias. Arch Neurol. 1998;55:1353–7.

    Article  PubMed  CAS  Google Scholar 

  5. Rivaud-Pechoux S, Dürr A, Gaymard B, et al. Eye movement abnormalities correlate with genotype in autosomal dominant cerebellar ataxia type I. Ann Neurol. 1998;43:297–302.

    Article  PubMed  CAS  Google Scholar 

  6. Bürk K, Fetter M, Abele M, et al. Autosomal dominant cerebellar ataxia type I: oculomotor abnormalities in families with SCA1, SCA2, and SCA3. J Neurol. 1999;246:789–97.

    Article  PubMed  Google Scholar 

  7. Schmitz-Hübsch T, du Montcel ST, Baliko L, et al. Scale for the assessment and rating of ataxia: development of a new clinical scale. Neurology. 2006;66:1717–20.

    Article  PubMed  Google Scholar 

  8. Schulz JB, Borkert J, Wolf S, et al. Visualization, quantification and correlation of brain atrophy with clinical symptoms in spinocerebellar ataxia types 1, 3 and 6. NeuroImage. 2010;49:158–68.

    Article  PubMed  Google Scholar 

  9. Mangione CM, Lee PP, Gutierrez PR, et al. Development of the 25-item National Eye Institute Visual Function Questionnaire. Arch Ophthalmol. 2001;119:1050–8.

    Article  PubMed  CAS  Google Scholar 

  10. Nyström M, Holmqvist K. An adaptive algorithm for fixation, saccade, and glissade detection in eyetracking data. Behav Res Methods. 2010;42:188–204.

    Article  PubMed  Google Scholar 

  11. White M, Lalonde R, Botez-Marquard T. Neuropsychologic and neuropsychiatric characteristics of patients with Friedreich’s ataxia. Acta Neurol Scand. 2000;102:222–6.

    Article  PubMed  CAS  Google Scholar 

  12. Wollmann T, Nieto-Barco A, Montón-Alvarez F, et al. Friedreich’s ataxia: analysis of magnetic resonance imaging parameters and their correlates with cognitive and motor slowing. Rev Neurol. 2004;38:217–22.

    PubMed  CAS  Google Scholar 

  13. Fahey MC, Cremer PD, Aw ST, et al. Vestibular, saccadic and fixation abnormalities in genetically confirmed Friedreich ataxia. Brain. 2008;131:1035–45.

    Article  PubMed  Google Scholar 

  14. Thier P, Haarmeier T, Treue S, et al. Absence of a common functional denominator of visual disturbances in cerebellar disease. Brain. 1999;122:2133–46.

    Article  PubMed  Google Scholar 

  15. Machner B, Sprenger A, Kömpf D, et al. Cerebellar infarction affects visual search. NeuroReport. 2005;16:1507–11.

    Article  PubMed  Google Scholar 

  16. Dale RT, Kirby AW, Jampel RS. Square wave jerks in Friedreich’s ataxia. Am J Ophthalmol. 1978;85:400–6.

    PubMed  CAS  Google Scholar 

  17. Kirkham TH, Guitton D, Katsarkas A, et al. Oculomotor abnormalities in Friedreich’s ataxia. Can J Neurol Sci. 1979;6:167–72.

    PubMed  CAS  Google Scholar 

  18. Furman JM, Perlman S, Baloh RW. Eye movements in Friedreich’s ataxia. Arch Neurol. 1983;40:343–6.

    Article  PubMed  CAS  Google Scholar 

  19. Schöls L, Linnemann C, Globas C. Electrophysiology in spinocerebellar ataxias: spread of disease and characteristic findings. Cerebellum. 2008;7:198–203.

    Article  PubMed  Google Scholar 

  20. Donato SD, Mariotti C, Taroni F. Spinocerebellar ataxia type 1. Handb Clin Neurol. 2012;103:399–421.

    Article  PubMed  Google Scholar 

  21. Quaia C, Lefèvre P, Optican LM. Model of the control of saccades by superior colliculus and cerebellum. J Neurophysiol. 1999;82:999–1018.

    PubMed  CAS  Google Scholar 

  22. Averbuch-Heller L, Stahl JS, Hlavin ML, et al. Square-wave jerks induced by pallidotomy in parkinsonian patients. Neurology. 1999;52:185–8.

    Article  PubMed  CAS  Google Scholar 

  23. Salman MS, Sharpe JA, Lillakas L, et al. Visual fixation in Chiari type II malformation. J Child Neurol. 2009;24:161–5.

    Article  PubMed  Google Scholar 

  24. Velázquez-Pérez L, Seifried C, Santos-Falcón N, et al. Saccade velocity is controlled by polyglutamine size in spinocerebellar ataxia 2. Ann Neurol. 2004;56:444–7.

    Article  PubMed  Google Scholar 

  25. Rüb U, Brunt ER, Gierga K, et al. The nucleus raphe interpositus in spinocerebellar ataxia type 3 (Machado-Joseph disease). J Chem Neuroanat. 2003;25:115–27.

    Article  PubMed  Google Scholar 

  26. Geiner S, Horn AK, Wadia NH, et al. The neuroanatomical basis of slow saccades in spinocerebellar ataxia type 2 (Wadia-subtype). Prog Brain Res. 2008;171:575–81.

    Article  PubMed  CAS  Google Scholar 

  27. Quinet J, Goffart L. Head-unrestrained gaze shifts after muscimol injection in the caudal fastigial nucleus of the monkey. J Neurophysiol. 2007;98:3269–83.

    Article  PubMed  Google Scholar 

  28. Von Noorden GK, Mackensen G. Phenomenology of eccentric fixation. Am J Ophthalmol. 1962;53:642–60.

    Google Scholar 

  29. Pélisson D, Alahyane N, Panouillères M, et al. Sensorimotor adaptation of saccadic eye movements. Neurosci Biobehav Rev. 2010;34:1103–20.

    Article  PubMed  Google Scholar 

  30. Desmurget M, Pélisson D, Urquizar C, et al. Functional anatomy of saccadic adaptation in humans. Nat Neurosci. 1998;1:524–8.

    Article  PubMed  CAS  Google Scholar 

  31. Suzuki Y, Kase M, Hashimoto M, et al. Leaky neural integration observed in square-wave jerks. Jpn J Ophthalmol. 2003;47:535–6.

    Article  PubMed  Google Scholar 

  32. Kawai Y, Suenaga M, Watanabe H, et al. Cognitive impairment in spinocerebellar degeneration. Eur Neurol. 2009;61:257–68.

    Article  PubMed  CAS  Google Scholar 

  33. Nieto A, Correia R, de Nobrega E, Monton F, Hess S, Barroso J. Cognition in Freidreich ataxia. Cerebellum 2012;11:834–44.

    Google Scholar 

  34. Rayner K, Slattery TJ, Bélanger NN. Eye movements, the perceptual span, and reading speed. Psychon Bull Rev. 2010;17:834–9.

    Article  PubMed  Google Scholar 

  35. Clausi S, De Luca M, Chiricozzi FR, Tedesco AM, Casali C, Molinari M, Leggio MG. Oculomotor deficits affect neuropsychological performance in oculomotor apraxia type 2. Cortex 2012 [Epub ahead of print]

  36. Hyönä J, Bertram R, Pollatsek A. Are long compound words identified serially via their constituents? Evidence from an eye-movement-contingent display change study. Mem Cognit. 2004;32:523–32.

    Article  PubMed  Google Scholar 

  37. McAskill MR, Anderson TJ, Jones RD. Suppression of displacement in severely slowed saccades. Vision Res. 2000;40:3405–13.

    Article  Google Scholar 

  38. Grunfeld EA, Shallo-Hoffmann JA, Cassidy L, et al. Vestibular perception in patients with acquired ophthalmoplegia. Neurology. 2003;60:1993–5.

    Article  PubMed  CAS  Google Scholar 

  39. McLaughlin SC. Parametric adjustment in saccadic eye movements. Perception and Psychophysics. 1967;2:359–62.

    Article  Google Scholar 

  40. Guerraz M, Yardley L, Bertholon P, et al. Visual vertigo: symptom assessment, spatial orientation and postural control. Brain. 2001;124:1646–56.

    Article  PubMed  CAS  Google Scholar 

Download references

Conflict of Interest

The authors declare no conflict of interest.

Author information

Authors and Affiliations

  1. Service d’Ophtalmologie, AP-HP, Hôpital Pitié Salpêtrière, 75013, Paris, France

    M. F. Alexandre & G. Challe

  2. Centre de Recherche de l’Institut du Cerveau et de la Moelle épinière, Université Pierre et Marie Curie-Paris6, UMR-S975, Paris, France

    S. Rivaud-Péchoux, A. Durr & B. Gaymard

  3. INSERM, U975, Paris, France

    S. Rivaud-Péchoux, A. Durr & B. Gaymard

  4. CNRS, UMR 7225, Paris, France

    S. Rivaud-Péchoux, A. Durr & B. Gaymard

  5. Département de Génétique et Cytogénétique, AP-HP, Hôpital Pitié Salpêtrière, 75013, Paris, France

    A. Durr

  6. Département de Neurophysiologie Clinique, AP-HP, Hôpital Pitié Salpêtrière, 75013, Paris, France

    B. Gaymard

  7. Centre de Recherche de l’Institut du Cerveau et de la Moelle Epinière, Hôpital de la Salpêtrière, 47 boulevard de l’Hôpital, 75651, Paris CEDEX 13, France

    B. Gaymard

Authors
  1. M. F. Alexandre
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. S. Rivaud-Péchoux
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. G. Challe
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. A. Durr
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. B. Gaymard
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to B. Gaymard.

Additional information

Alexandre MF: Deceased July 17, 2012

Electronic supplementary material

Below is the link to the electronic supplementary material.

ESM 1

(DOCX 31 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Alexandre, M.F., Rivaud-Péchoux, S., Challe, G. et al. Functional Consequences of Oculomotor Disorders in Hereditary Cerebellar Ataxias. Cerebellum 12, 396–405 (2013). https://doi.org/10.1007/s12311-012-0433-z

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12311-012-0433-z

Keywords

Search

Navigation