Skip to main content
Log in

Three-dimensional analysis of strongly curved saccades elicited by double-step stimuli

  • Published:
Experimental Brain Research Aims and scope Submit manuscript

Abstract

Earlier recordings of eye position in three dimensions have revealed that Listing's law is obeyed in reasonable approximation, both statically and dynamically. This implies that all eye positions are confined to a plane when using a rotation vector or quaternion representation. The orientation of the angular velocity axis is crucial in order to preserve the law. For a single-axis rotation, the eye's angular velocity axis has to tilt out of Listing's plane, otherwise the law cannot be preserved in eccentric saccades. Experimental work has confirmed that normal, visually-guided saccades resemble single-axis rotations whose angular velocity axis tilts by the right amount. We investigated how well the saccadic system implements Listing's law when the trajectory of the eyes is more complicated, as in a non-single-axis rotation where the angular velocity vector depends on instantaneous eye position. Eye position was measured in three dimensions using the magnetic scleral search coil method for five subjects. Non-single-axis rotations of the eye were evoked with a double-step paradigm. We found that Listing's law is obeyed equally well during fixations, single-axis saccades and in non-single-axis saccades. Some deviations from the law were found in both curved and single-axis eye movements, but we demonstrated that the net torsional component of eye position of these saccades is negligible compared to that expected if the angular velocity axis did not tilt at all. In addition, analysis of the angular velocity signals in the curved movements showed strong similarity to the computed signal required for implementing Listing's law. Our results show that the observed deviations from Listing's law reflect only minor failures in the mechanism underlying its dynamic implementation. We conclude that single-axis rotations are not a necessary condition for the implementation of Listing's law in saccades. Our results are compatible with the notion that the implementation of Listing's law relies upon internal feedback. Various suggestions of how models can be reconciled with recent data on the three-dimensional control of saccades are discussed.

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

Access this article

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

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Crawford JD, Vilis T (1991) Axes of eye rotation and Listing's law during rotations of the head. J Neurophysiol 65: 407–423

    CAS  PubMed  Google Scholar 

  • Droulez J, Berthoz A (1991) A neural network model of sensoritopic maps with predictive short term memory properties. Proc Natl Acad Sci USA 88: 9653–9657

    Google Scholar 

  • Ferman L, Collewijn H, Jansen TC, Van den Berg AV (1987a) Human gaze stability in the horizontal, vertical and torsional direction during voluntary head movements, evaluated with a three-dimensional sceral induction coil technique. Vision Res 27: 811–828

    Google Scholar 

  • Ferman L, Collewijn H, Jansen TC, Van den Berg AV (1987b) A direct test of Listing's law. I. Human ocular torsion measured in static tertiary positions. Vision Res 27: 929–938

    Google Scholar 

  • Ferman L, Collewijn H, Jansen TC, Van den Berg AV (1987c) A direct test of Listing's law. II. Human ocular torsion measured under dynamic conditions. Vision Res 27: 939–951

    Google Scholar 

  • Goldberg ME, Bruce CJ (1990) Primate frontal eye fields. III. Maintenance of a spatially accurate saccade signal. J Neurophysiol 64: 489–508

    Google Scholar 

  • Grossman GE, Robinson DA (1988) Ambivalence in modelling oblique saccades. Biol Cybern 58: 13–18

    Google Scholar 

  • Haustein W (1989) Considerations on Listing's law and the primary position by means of a matrix description of eye position control. Biol Cybern 60: 411–420

    Google Scholar 

  • Helmholtz H von (1867) Handbuch der Physiologischen Optik. Vol 3 Voss Verlag, Hamburg

    Google Scholar 

  • Henis E, Flash T (1991) A mechanism for arm trajectory modification induced by stimuli presented in quick succession. Eur J Neurosci [Suppl 14] 178

  • Hepp K (1990) On Listing's law. Comm Math Phys 132: 285–292

    Google Scholar 

  • Hepp K, Henn V (1987) Nonabelian neurodynamics. In: Baeriswyl D, Droz M, Malaspinas A, Martinoli P (eds) Physics in living matter. (Lecture Notes in Physics, vol 284) Springer, Berlin Heidelberg New York, pp 163–177

    Google Scholar 

  • Hepp K, Van Opstal AJ, Henn V (1990a) Role of superior colliculus in 3D eye movement generation II. Visual saccades and 3D fast phases of nystagmus after reversible inactivation with muscimol. Eur J Neurosci [Suppl 13] 164

  • Hepp K, Van Opstal AJ, Hess BJM, Straumann D, Henn V (1990b) On the central implementation of saccades in Listing's plane. Soc Neurosci Abstr 16:pp 1064

    Google Scholar 

  • Hess BJM (1990) Dual-search coil for measuring 3-dimensional eye movements in experimental animals. Vision Res 30: 597–602

    Google Scholar 

  • Hess BJM, Van Opstal AJ, Straumann D, Hepp K (1992) Calibration of three-dimensional eye position using search coil signals in the Rhesus monkey. Vision Res 32: 1647–1654

    Google Scholar 

  • Jürgens R, Becker W, Kornhuber HH (1981) Natural and drug-induced variations of velocity and duration of human saccadic eye movements: evidence for a control of the neural pulse generator by local feedback. Biol Cybern 39: 87–96

    CAS  PubMed  Google Scholar 

  • King WM, Lisberger SG, Fuchs AF (1986) Oblique saccadic eye movements of primates. J Neurophysiol 56: 769–784

    Google Scholar 

  • Minken AWH, Van Opstal AJ, Van Gisbergen JAM (1991) Validity of Listing's law in strongly curved saccades. Eur J Neurosci [Suppl 14] 306

  • Nakayama K (1975) Coordination of extraocular muscles. In: Lennerstrand G, Bach-y-Rita P (eds) Basic mechanisms of ocular motility and their clinical implications. Pergamon Press, Oxford, pp 193–209

    Google Scholar 

  • Robinson DA (1975) Oculomotor control signals. In: Lennerstrand G, Bach-y-Rita P (eds) Basic mechanisms of ocular motility and their clinical implications. Pergamon Press, Oxford, pp 337–374

    Google Scholar 

  • Scudder CA (1988) A new local feedback model of the saccadic burst generator. J Neurophysiol 59: 1455–1475

    CAS  PubMed  Google Scholar 

  • Smit AC, Van Gisbergen JAM (1990) An analysis of curvature in fast and slow human saccades. Exp Brain Res 81: 335–345

    Google Scholar 

  • Smit AC, Van Opstal AJ, Van Gisbergen JAM (1990) Component stretching in fast and slow oblique saccades in the human. Exp Brain Res 81: 325–334

    Google Scholar 

  • Sparks DL, Mays LE (1983) Spatial localization of saccade targets. I. Compensation for stimulation-induced perturbations in eye positions. J Neurophysiol 49: 45–63

    Google Scholar 

  • Sparks DL, Porter D (1983) Spatial localization of saccade targets. II. Activity of superior colliculus neurons preceding compensatory saccades. J Neurophysiol 49: 64–74

    Google Scholar 

  • Straumann D, Haslwanter T, Hepp-Reymond M-C, Hepp K (1991) Listing's law for eye, head and arm movements and their synergestic control. Exp Brain Res 86: 209–215

    CAS  PubMed  Google Scholar 

  • Tweed D, Vilis T (1985) A two-dimensional model for saccade generation. Biol Cybern 52: 219–227

    Google Scholar 

  • Tweed D, Vilis T (1987) Implications of rotational kinematics for the oculomotor system in three dimensions. J Neurophysiol 58: 832–849

    CAS  PubMed  Google Scholar 

  • Tweed D, Vilis T (1990a) The superior colliculus and spatiotemporal translation in the saccadic system. Neural Networks 3: 75–86

    Google Scholar 

  • Tweed D, Vilis T (1990b) Geometric relations of eye positions and velocity vectors during saccades. Vision Res 30: 111–127

    Article  CAS  PubMed  Google Scholar 

  • Tweed D, Cadera W, Vilis T (1990) Computing three-dimensional eye position quaternions and eye velocity from search coil signals. Vision Res 30: 97–110

    Article  CAS  PubMed  Google Scholar 

  • Van Gisbergen JAM, Minken AWH (1991) Rapid and slow mechanisms for the control of ocular torsion during voluntary gaze shifts. Soc Neurosci Abstr 17:p 862

    Google Scholar 

  • Van Gisbergen JAM, Robinson DA, Gielen S (1981) A quantitative analysis of generation of saccadic eye movements by burst neurons. J Neurophysiol 21: 541–555

    Google Scholar 

  • Van Gisbergen JAM, Van Opstal AJ, Schoenmakers JJM (1985) Experimental test of two models for the generation of oblique saccades. Exp Brain Res 57: 321–336

    Google Scholar 

  • Van Gisbergen JAM, Van Opstal AJ, Roebroek JGH (1987) Stimulus-induced midflight modification of saccades. In O'Regan JK, Levy-Schoen A (eds) Eye Movements: from physiology to cognition. Elsevier, Amsterdam, 27–36

    Google Scholar 

  • Van Gisbergen JAM, Van Opstal AJ, Minken AWH (1991) Current views on the visuomotor interface of the saccadic system. In: Gorea A (ed) Representations of vision, Cambridge University Press, Cambridge, pp 201–215

    Google Scholar 

  • Van Opstal AJ, Hepp K, Straumann D, Hess BJM (1990a) Role of superior colliculus in 3D eye movement generation. I. Results of electrical stimulation. Eur J Neurosci [Suppl 13] 164

  • Van Opstal AJ, Henn V, Hess BJM, Straumann D, Hepp K (1990b) Two-dimensional versus three-dimensional rapid eye movement generation in the superior colliculus and the rostral interstitial nucleus of the MLF in the monkey. Soc Neurosci Abstr 16:p 1084

    Google Scholar 

  • Van Opstal AJ, Hepp K, Hess BJM, Straumann D, Henn V (1991) Two-rather than three-dimensional representation of saccades in monkey superior colliculus. Science 252: 1313–1315

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Minken, A.W.H., Van Opstal, A.J. & Van Gisbergen, J.A.M. Three-dimensional analysis of strongly curved saccades elicited by double-step stimuli. Exp Brain Res 93, 521–533 (1993). https://doi.org/10.1007/BF00229367

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00229367

Key words

Navigation