Skip to main content
Log in

A novel interpretation for the collicular role in saccade generation

  • Original Papers
  • Published:
Biological Cybernetics Aims and scope Submit manuscript

Abstract

Recently, we found evidence that the activity of neurons in the deep layers of the monkey superior colliculus (SC) is modulated by initial eye position (gain fields). In this paper, we propose a quantitative model of the motor SC which incorporates these new findings. Inputs to the motor map represent the desired eye displacement vector (motor error), as well as initial eye position. A unit's activity in the motor map is described by multiplying a weak linear eye position sensitivity with a gaussian tuning to motor error. The motor map projects to several sets of output neurons, representing the coordinates of the desired eye displacement vector, the desired eye position in the head, and the three-dimensional ocular rotation axis for saccades in Listing's plane, respectively. All these signals have been hypothesized in the literature to drive the saccade burst generator. We show that these signals can be extracted from the motor map by a linear weighting of the population activity. The saccadic system may employ all coding strategies in parallel to ensure high spatial accuracy in many complex sensorimotor tasks, such as orienting to multimodal stimuli.

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.

Institutional subscriptions

Similar content being viewed by others

References

  • Albano JE, Wurtz RH (1982) Deficits in eye position following ablation of monkey superior colliculus, pretectum, and posterior-medial thalamus. J Neurophysiol 48:318–337

    PubMed  Google Scholar 

  • Andersen RA, Essick GK, Siegel RM (1985) Encoding of spatial location by posterior parietal neurons. Science 230:456–458

    PubMed  Google Scholar 

  • Andersen RA, Bracewell RM, Barash S, Gnadt JW, Fogassi L (1990) Eye position effects on visual, memory, and saccade-related activity in areas LIP and 7a of macaque. J Neurosci 10:1176–1196

    PubMed  Google Scholar 

  • Duhamel J-R, Colby CL, Goldberg ME (1992) The updating of the representation of visual space in parietal cortex by intended eye movements. Science 255:90–92

    PubMed  Google Scholar 

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

    PubMed  Google Scholar 

  • Hartwich-Young R, Nelson JS, Sparks DL (1990) The perihypoglossal projection to the superior colliculus in the rhesus monkey. Visual Neurosci 4:29–42

    Google Scholar 

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

    Google Scholar 

  • Hepp K, Van Opstal AJ, Straumann D, Hess BJM, Henn V (1993) Monkey superior colliculus represents rapid eye movements in a two-dimensional motor map. J Neurophysiol 69:965–979

    PubMed  Google Scholar 

  • Jay MF, Sparks DL (1987) Sensorimotor integration in the primate superior colliculus. II. Coordinates of auditory signals. J Neurophysiol 57:35–55

    PubMed  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

    Article  PubMed  Google Scholar 

  • Keating EG, Kenney DV, Gooley SG, Pratt SE, McGillis SL (1986) Targeting errors and reduced oculomotor range following ablations of the superior colliculus or pretectum/thalamus. Behav Brain Res 22:191–210

    Article  PubMed  Google Scholar 

  • Lee C, Rohrer WH, Sparks DL (1988) Population coding of saccadic eye movements by neurons in the superior colliculus. Nature 332:357–360

    Article  PubMed  Google Scholar 

  • McIlwain JT (1982) Lateral spread of neural excitation during microstimulation in the intermediate gray layer of cat's superior colliculus. J Neurophysiol 47:167–178

    PubMed  Google Scholar 

  • McIlwain JT (1986) Effects of eye position of saccades evoked electrically from superior colliculus of alert cats. J Neurophysiol 55:97–112

    PubMed  Google Scholar 

  • Ottes FP, Van Gisbergen JAM, Eggermont JJ (1986) Visuomotor fields of the superior colliculus: a quantitative model. Vision Res 26:857–873

    Article  PubMed  Google Scholar 

  • Peck CK (1986) Eye position signals in cat superior colliculus. Exp Brain Res 61:447–450

    Article  PubMed  Google Scholar 

  • Peck CK, Baro JA, Warder SM (1995) Effects of eye position on saccadic eye movements and on the neuronal responses to auditory and visual stimuli in cat superior colliculus. Exp Brain Res (in press)

  • Poggio T (1990) A theory of how the brain might work. Cold Spring Harbor Symp Quant Biol 55:899–910

    PubMed  Google Scholar 

  • Poggio T, Girosy F (1990) Regularization algorithms for learning that are equivalent to multilayer networks. Science 247:978–982

    Google Scholar 

  • Pouget A, Sejnowski TJ (1995) Spatial representations in the parietal cortex may use basis functions. NIPS Conf Proc, Vol 7 (in press)

  • Robinson DA (1972) Eye movements evoked by collicular stimulation in the alert monkey. Vision Res 12:1795–1808

    Article  PubMed  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 

  • Roucoux A, Crommelinck M (1976) Eye movements evoked by superior colliculus stimulation in the alert cat. Brain Res 106:349–363

    Article  PubMed  Google Scholar 

  • Schiller PH, Stryker M (1972) Single-unit recordings and stimulation in superior colliculus of the alert rhesus monkey. J Neurophysiol. 35:915–924

    PubMed  Google Scholar 

  • Schnabolk C, Raphan T (1994) Modelling three-dimensional velocityto-position transformation in oculomotor control. J Neurophysiol 71:623–638

    PubMed  Google Scholar 

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

    PubMed  Google Scholar 

  • Segraves MA, Goldberg ME (1984) Initial orbital position affects the trajectories of large saccades evoked by electrical stimulation of the monkey superior coolliculus. Soc Neuorsci Abstr 10:389

    Google Scholar 

  • Sparks DL, Mays LE (1980) Movement fields of saccade-related burst neurons in the monkey superior colliculus. Brain Res 190:39–50

    Article  PubMed  Google Scholar 

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

    Google Scholar 

  • Sparks DL, Mays LE (1990) Signal transformations required for the generation of saccadic eye movements. Annu Rev Neurosci 13:309–336

    Article  PubMed  Google Scholar 

  • Stein BE, Meredith MA (1993) The merging of the senses. MIT Press, Cambridge, Mass

    Google Scholar 

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

    PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Tweed D, Misslisch H, Fetter M (1994) Testing models of the oculomotor velocity-to-position transformation. J Neurophysiol 72:1425–1429

    PubMed  Google Scholar 

  • Van Gisbergen JAM, Van Opstal AJ, Tax AAM (1987) A model of the ollicular motor map based on vector summation. Neuroscience 7:555–567

    Google Scholar 

  • Van Opstal AJ (1993a) Representation of eye position in three dimensions. In: Berthoz A (ed) Multisensory control of movement. Oxford University Press, Oxford, pp 27–41

    Google Scholar 

  • Van Opstal AJ (1993b) Experimental test of two models for the role of monkey superior colliculus in 3D saccade generation. In: Berthoz A (eds) Multisensory control of movement. Oxford University Press, Oxford, pp 240–254

    Google Scholar 

  • Van Opstal AJ (1994) Nonlinearities in the saccadic system and efferent feedback to the collicular motor map. In: Delgado-García J-M, Vidal P, Godeaux E (eds) Information processing underlying gaze control. Pergamon Press, Oxford, pp 139–149

    Google Scholar 

  • Van Opstal AJ, Hepp K (1995) Motor map of monkey superior colliculus may encode eye motor error, target position relative to the head, or both. Fourth IBRD World Conf Neurosci Abstr, pp. 49

  • Van Opstal AJ, Kappen H (1993) A two-dimensional ensemble coding model of spatial-temporal transformation of saccades in monkey superior colliculus. Network 4:19–38

    Google Scholar 

  • Van Opstal AJ, Hepp K, Suzuki Y, Henn V (1995) Influence of eye position on activity in monkey superior colliculus. J Neurophysiol (in press)

  • Van Opstal AJ, Van Gisbergen JAM, Smit AC (1990) Comparison of saccades evoked by visual stimulation and collicular electrical stimulation in the alert monkey. Exp Brain Res 79:299–312

    Article  PubMed  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

    PubMed  Google Scholar 

  • Waitzman DM, Ma TP, Optican LM, Wurtz RH (1991) Superior colliculus neurons mediate the dynamic characteristics of saccades. J Neurophysiol 66:1716–1737

    PubMed  Google Scholar 

  • Zipser D, Andersen RA (1988) A back-propagation programmed network that simulates response properties of a subset of posterior parietal neurons. Nature 331:679–684

    Article  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Van Opstal, A.J., Hepp, K. A novel interpretation for the collicular role in saccade generation. Biol. Cybern. 73, 431–445 (1995). https://doi.org/10.1007/BF00201478

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00201478

Keywords

Navigation