Three-Dimensional Properties of Saccadic Eye Movements in Patients with Cerebellar Ataxia

  • M. Fetter
  • D. Anastasopoulos
  • T. Haslwanter
Chapter

Abstract

Eye muscles in humans are arranged such that, by appropriate activation, they allow for eye rotations with three degrees of freedom. Yet it has been known for more than a century that during fixation, while the head is stationary, the eyes do only utilize the horizontal and vertical degrees of rotational freedom while the torsional position of the line of sight is kept constant, i.e., during fixation, the eye is restricted to a two-dimensional (2-D) subspace of the three-dimensional (3-D) space of all possible orientations. This has been first described qualitatively by Donders (1847) who stated that the amount of torsion is fixed for all eye positions, independent of from where the eye has reached a particular position. The geometric consequence of this statement is that all eye positions lie in a 2-D surface. By observing the systematic tilt of afterimages in different gaze directions, Helmholtz was able to determine which 2-D subspace the eye is restricted to. He found, according to what Listing suggested, that the eye positions are not only confined to a surface but to a plane called Listing’s plane. This result, cited as Listing’s law (LL) by Helmholtz (1863), is most simply described if eye positions are expressed in terms of the axes of their rotational displacements from a particular eye position known as primary position and represented by angular position vectors. Then LL states that the eye assumes only those positions that can be reached from primary position by a single rotation about an axis in Listing’s plane, which lies orthogonal to the gaze direction in primary position.

Keywords

Multiple System Atrophy Smooth Pursuit Cerebellar Ataxia Search Coil Torsional Position 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Bechert K, Koenig E (1996) A search coil system with automatic field stabilization, calibration, and geometric processing for eye movement recording in humans. Neuro-ophthalmology 16: 163–170CrossRefGoogle Scholar
  2. Crawford JD, Vilis T (1991) Axes of eye rotation and Listing’s law during rotations of the head. J Neurophysiol 65: 407–423PubMedGoogle Scholar
  3. Demer JL, Miller JM, Poukens V, Vinters HV, Glasgow BJ (1995) Evidence for fibromuscular pulleys of the recti extraocular muscles. Invest Ophthalmol Visual Sci 36: 1125–1136Google Scholar
  4. Donders FC (1847), Beitrag zur Lehre von den Bewegungen des menschlichen Auges. In: Holland Beitr Anat Physiol Wiss 1: 104–145Google Scholar
  5. Ferman L, Collewijn H, Hansen TC, van den Berg AV (1987) Human gaze stability in the horizontal, vertical and torsional direction during voluntary head movements, evaluated with a three-dimensional scleral induction coil technique. Vis Res 27: 811–828PubMedCrossRefGoogle Scholar
  6. Fetter M, Tweed D, Misslisch H, Koenig E (1994) Three-dimensional human eye movements are organized differently for the different oculomotor subsystems. Neuro-ophthalmology 14: 147–152CrossRefGoogle Scholar
  7. Haslwanter T, Straumann D, Hepp K, Hess BJM, Henn V (1991) Smooth pursuit eye movements obey Listing’s law in monkey. Exp Brain Res 87: 470–472PubMedCrossRefGoogle Scholar
  8. Helmchen C, Glasauer S, Büttner U (1997) Pathological torsional eye deviation during voluntary saccades: a violation of Lisitng’s law. J Neurol Neurosurg Psychiatry 62: 253–260PubMedCrossRefGoogle Scholar
  9. Helmholtz H von (1863) Üeber die normalen Bewegungen des menschlichen Auges. Arch Ophthalmol IX (2): 153–214CrossRefGoogle Scholar
  10. Henn V, Straumann D, Hess BJM, Haslwanter T, Kawachi N (1992) Three-dimensional transformation from vestibular and visual input to oculomotor output. Ann NY Acad Sci 656: 166–180PubMedCrossRefGoogle Scholar
  11. Klockgether T, Wüllner U, Dichgans J, Grodd W, Nägele T, Petersen D, Schroth G, Schmidt O, Voigt K (1993) Clinical and imaging correlations in inherited ataxias. Adv Neurol 61: 77–96PubMedGoogle Scholar
  12. Klockgether T, Zühlke C, Schulz JB, Bürk K, Fetter M, Dittman H, Skalej M, Dichgans J (1996) Friedreich’s ataxia with retained tendon reflexes: Molecular genetics, clinical neurophysiology, and magnetic resonance imaging. Neurology 46: 118–121PubMedCrossRefGoogle Scholar
  13. Leigh RJ, Zee DS (1991) The neurology of eye movements. 2nd ed. FA Davis, Philadelphia, pp 424–428Google Scholar
  14. Nakayama K (1975) Coordination of extraocular muscles. In: Lennerstrand G, Bachy-Rita P (eds) Basic mechanisms of ocular motility and their clinical implications. Pergamon, Oxford, pp 193–207Google Scholar
  15. Schnabolk C, Raphan T (1994) Modeling three-dimensional velocity-to-position transformation in oculomotor control. J Neurophysiol 71: 623–638PubMedGoogle Scholar
  16. Tweed D, Vilis T (1990) Geometric relations of eye position and velocity vectors during saccades. Vis Res 30: 111–127PubMedCrossRefGoogle Scholar
  17. Tweed D, Cadera W, Vilis T (1990) Computing three-dimensional eye position quaternions and eye velocity from search coil signals. Vis Res 30: 97–110PubMedCrossRefGoogle Scholar
  18. Tweed D, Fetter M, Andreadaki S, Koenig E, Dichgans J (1992) Three-dimensional properties of human pursuit eye movements. Vis Res 32: 1225–1238PubMedCrossRefGoogle Scholar
  19. Tweed D, Fischer D, Misslisch H, Fetter M, Zee DS, Koenig E (1994a) Rotational kinematics of the human vestibuloocular reflex I: gain matrices. J Neurophys 72: 2467–2479Google Scholar
  20. Tweed D, Fetter M, Fischer D, Misslisch H, Koenig E (1994b) Rotational kinematics of the human vestibuloocular reflex II: velocity steps. J Neurophys 72: 2480–2489Google Scholar
  21. Tweed D, Misslisch H, Fetter M (1994c) Testing models of the oculomotor velocity to position transformation. J Neurophys 72: 1425–1429Google Scholar
  22. Wessel K, Zeffiro T, Lou J-S, Toro C, Hallett M (1995) Regional cerebral blood flow during self-paced sequential finger opposition task in patients with cerebellar degeneration. Brain 118: 379–393PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 1999

Authors and Affiliations

  • M. Fetter
    • 1
  • D. Anastasopoulos
    • 2
  • T. Haslwanter
    • 1
  1. 1.Department of NeurologyEberhard-Karls-UniversityTübingenGermany
  2. 2.Department of NeurologyUniversity of IoanninaIoanninaGreece

Personalised recommendations