Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Article
  • Published:

Superior colliculus encodes distance to target, not saccade amplitude, in multi-step gaze shifts

Nature Neuroscience volume 6, pages 404–413 (2003)Cite this article

Abstract

The superior colliculus (SC) is important for generating coordinated eye–head gaze saccades. Its deeper layers contain a retinotopically organized motor map in which each site is thought to encode a specific gaze saccade vector. Here we show that this fundamental assumption in current models of collicular function does not hold true during horizontal multi-step gaze shifts in darkness that are directed to a goal and composed of a sequence of gaze saccades separated by periods of steady fixation. At the start of a multi-step gaze shift in cats, neural activity on the SC's map was located caudally to encode the overall amplitude of the gaze displacement, not the first saccade in the sequence. As the gaze shift progressed, the locus of activity moved to encode the error between the goal and the current gaze position. Contrary to common belief, the locus of activity never encoded gaze saccade amplitude, except for the last saccade in the sequence.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on SpringerLink
  • Instant access to the full article PDF.

USD 39.95

Prices may be subject to local taxes which are calculated during checkout

Figure 1: Typical discharge pattern of a neuron in caudal SC during large, coordinated eye–head gaze shifts.
Figure 2: Comparative discharges of two neurons located on the motor map at different rostro–caudal positions during multi-step gaze shifts of different amplitudes.
Figure 3: Mean firing frequency of example cells K7 and K5 during gaze position plateaus (dark circles) at different GPEs.
Figure 4: Dependence of firing frequency on GPE for groups of cells located in different zones on the SC's map.
Figure 5: Relationships showing that GPE at peak discharge corresponds to the GPE encoded by the cell's location on the SC motor map.
Figure 6: Firing frequency during gaze saccades of different amplitudes.
Figure 7: Factors affecting differences between firing frequency profiles during first and last saccades.

Similar content being viewed by others

References

  1. Moschovakis, A.K., Scudder, C.A. & Highstein, S.M. The microscopic anatomy and physiology of the mammalian saccadic system. Prog. Neurobiol. 50, 133–254 (1996).

    Article  CAS  Google Scholar 

  2. Scudder, C.A., Kaneko, C.S. & Fuchs, A.F. The brainstem burst generator for saccadic eye movements: a modern synthesis. Exp. Brain Res. 142, 439–462 (2002).

    Article  Google Scholar 

  3. Freedman, E.G., Stanford, T.R. & Sparks, D.L. Combined eye head gaze shifts produced by electrical stimulation of the superior colliculus in rhesus monkeys. J. Neurophysiol. 76, 927–952 (1996).

    Article  CAS  Google Scholar 

  4. Paré, M., Crommelinck, M. & Guitton, D. Gaze shifts evoked by stimulation of the superior colliculus in the head-free cat conform to the motor map but also depend on stimulus strength and fixation activity. Exp. Brain Res. 101, 123–139 (1994).

    PubMed  Google Scholar 

  5. Roucoux, A., Guitton, D. & Crommelinck, M. Stimulation of the superior colliculus in the alert cat. II. Eye and head movements evoked when the head is unrestrained. Exp. Brain Res. 39, 75–85 (1980).

    Article  CAS  Google Scholar 

  6. Munoz, D.P. & Guitton, D. Control of orienting gaze shifts by the tectoreticulospinal system in the head-free cat. II. Sustained discharges during motor preparation and fixation. J. Neurophysiol. 66, 1624–1641 (1991).

    Article  CAS  Google Scholar 

  7. Munoz, D.P., Guitton, D. & Pelisson, D. Control of orienting gaze shifts by the tectoreticulospinal system in the head-free cat. III. Spatiotemporal characteristics of phasic motor discharges. J. Neurophysiol. 66, 1642–1666 (1991).

    Article  CAS  Google Scholar 

  8. Freedman, E.G. & Sparks, D.L. Activity of cells in the deeper layers of the superior colliculus of the rhesus monkey: evidence for a gaze displacement command. J. Neurophysiol. 78, 1669–1690 (1997).

    Article  CAS  Google Scholar 

  9. Aizawa, H. & Wurtz, R.H. Reversible inactivation of monkey superior colliculus. I. Curvature of saccadic trajectory. J. Neurophysiol. 79, 2082–2096 (1998).

    Article  CAS  Google Scholar 

  10. Quaia, C., Aizawa, H., Optican, L.M. & Wurtz, R.H. Reversible inactivation of monkey superior colliculus. I. Curvature of saccadic trajectory. J. Neurophysiol. 79, 2097–2110 (1998).

    Article  CAS  Google Scholar 

  11. Lee, C., Rohrer, W.H. & Sparks, D.L. Population coding of saccadic eye movements by neurons in the superior colliculus. Nature 332, 357–360 (1988).

    Article  CAS  Google Scholar 

  12. Bergeron, A. & Guitton, D. Fixation neurons in superior colliculus encode gaze position error, the distance between current and desired gaze positions. Nat. Neurosci. 3, 932–939 (2000).

    Article  CAS  Google Scholar 

  13. Bergeron, A. & Guitton, D. The superior colliculus and its control of fixation behavior via projections to brainstem omnipause neurons. Progr. Brain Res. 134, 97–107 (2001).

    Article  CAS  Google Scholar 

  14. Bergeron, A. & Guitton, D. In multiple-step gaze shifts: omnipause (OPNs) and collicular fixation neurons encode gaze position error; OPNs gate saccades. J. Neurophysiol. 88, 1726–1742 (2002).

    Article  Google Scholar 

  15. Munoz, D.P. & Guitton, D. Fixation and orientation control by the tecto-reticulo-spinal system in the cat whose head is unrestrained. Revue Neurol. (Paris) 145, 567–579 (1989).

    CAS  Google Scholar 

  16. Munoz, D.P. & Wurtz, R.H. Fixation cells in monkey superior colliculus. I. Characteristics of cell discharge. J. Neurophysiol. 70, 559–575 (1993).

    Article  CAS  Google Scholar 

  17. Peck, C.K.A. Visual responses of neurones in cat superior colliculus in relation to fixation of targets. J. Physiol. 414, 301–315 (1989).

    Article  CAS  Google Scholar 

  18. Peck, C.K. & Baro, J.A. Discharge patterns of neurons in the rostral superior colliculus of cat: activity related to fixation of visual and auditory targets. Exp. Brain Res. 113, 291–302 (1997).

    Article  CAS  Google Scholar 

  19. Munoz, D.P. & Istvan, P.J. Lateral inhibitory interactions in the intermediate layers of the monkey superior colliculus. J. Neurophysiol. 79, 1193–1209 (1998).

    Article  CAS  Google Scholar 

  20. Krauzlis, R.J., Basso, M.A. & Wurtz, R.H. Shared motor error for multiple eye movements. Science 276, 1693–1695 (1997).

    Article  CAS  Google Scholar 

  21. Krauzlis, R.J., Basso, M.A. & Wurtz, R.H. Discharge properties of neurons in the rostral superior colliculus of the monkey during smooth pursuit eye movements. J. Neurophysiol. 84, 876–891 (2000).

    Article  CAS  Google Scholar 

  22. Guitton, D., Douglas, R.M. & Volle, M. Coordinated eye head movements in the cat. J. Neurophysiol. 52, 1030–1050 (1984).

    Article  CAS  Google Scholar 

  23. Guitton, D. & Munoz, D.P. Control of orienting gaze shifts by the tecto reticulo spinal system in the heat-free cat. I. Identification, localization and effects of behavior on sensory responses. J. Neurophysiol. 66, 1605–1623 (1991).

    Article  CAS  Google Scholar 

  24. Edelman, J.A. & Goldberg, M.E. Dependence of saccade-related activity in the primate superior colliculus on visual target presence. J. Neurophysiol. 86, 676–691 (2001).

    Article  CAS  Google Scholar 

  25. Goossens, H.H. & Van Opstal, A.J. Blink-perturbed saccades in monkey. II. Superior colliculus activity. J. Neurophysiol. 83, 3430–3452 (2000).

    Article  CAS  Google Scholar 

  26. Anderson, R.W., Keller, E.L., Gandhi, N.J. & Das, S. Two dimensional saccade related population activity in superior colliculus in monkey. J. Neurophysiol. 80, 798–817 (1998).

    Article  CAS  Google Scholar 

  27. Gandhi, N.J. & Keller, E.L. Comparison of saccades perturbed by stimulation of the rostral superior colliculus, the caudal superior colliculus, and the omnipause neuron region. J. Neurophysiol. 82, 3236–3253 (1999).

    Article  CAS  Google Scholar 

  28. Munoz, D.P., Pelisson, D. & Guitton, D. Movement of neural activity on the superior colliculus motor map during gaze shifts. Science 251, 1358–1360 (1991).

    Article  CAS  Google Scholar 

  29. Quaia, C., Lefevre, P. & Optican, L.M. Model of the control of saccades by superior colliculus and cerebellum. J. Neurophysiol. 82, 999–1018 (1999).

    Article  CAS  Google Scholar 

  30. Klier, E.M., Wang, H. & Crawford, J.D. The superior colliculus encodes gaze commands in retinal coordinates. Nat. Neurosci. 4, 627–632 (2001).

    Article  CAS  Google Scholar 

  31. Keller, E.L. & Edelman, J.A. Use of interrupted saccade paradigm to study spatial and temporal dynamics of saccadic burst cells in superior colliculus in monkey. J. Neurophysiol. 72, 2754–2770 (1994).

    Article  CAS  Google Scholar 

  32. Munoz, D.P., Waitzman, D.M. & Wurtz, R.H. Activity of neurons in monkey superior colliculus during interrupted saccades. J. Neurophysiol. 75, 2562–2580 (1996).

    Article  CAS  Google Scholar 

  33. Keller, E.L., Gandhi, N.J. & Weir, P.T. Discharge of superior collicular neurons during saccades made to moving targets. J. Neurophysiol. 76, 3573–3577 (1996).

    Article  CAS  Google Scholar 

  34. Stanford, T.R. & Sparks, D.L. Systematic errors for saccades to remembered targets: evidence for a dissociation between saccade metrics and activity in the superior colliculus. Vision Res. 34, 93–106 (1994).

    Article  CAS  Google Scholar 

  35. Goffart, L. & Pelisson, D. Orienting gaze shifts during muscimol inactivation of caudal fastigial nucleus in the cat. I. Gaze dysmetria. J. Neurophysiol. 79, 1942–1958 (1998).

    Article  CAS  Google Scholar 

  36. Goffart, L., Pelisson, D. & Guillaume, A. Orienting gaze shifts during muscimol inactivation of caudal fastigial nucleus in the cat. II. Dynamics and eye–head coupling. J. Neurophysiol. 79, 1959–1976 (1998).

    Article  CAS  Google Scholar 

  37. Pelisson, D., Goffart, L. & Guillaume, A. Contribution of the rostral fastigial nucleus to the control of orienting gaze shifts in the head-unrestrained cat. J. Neurophysiol. 80, 1180–1196 (1998).

    Article  CAS  Google Scholar 

  38. Fakhri, S., Pélisson, D. & Guitton, D. Compensation for perturbations of gaze and role of vestibular signals in gaze control. in Information Processing Underlying Gaze Control. (eds. Delgado-Garcia, J.M., Godaux, E. & Vidal, P.P.) 53–63 (Elsevier, New York, 1994).

    Chapter  Google Scholar 

  39. Chun, K.S. & Robinson, D.A. A model of quick phase generation in the vestibulo-ocular reflex. Biol. Cybern. 28, 209–221 (1978).

    Article  CAS  Google Scholar 

  40. Galiana H.L. A nystagmus strategy to linearize the vestibulo-ocular reflex. IEEE Trans. Biomed. Eng. 38, 532–543 (1991).

    Article  CAS  Google Scholar 

  41. Paré, M. & Guitton, D. Brain stem omnipause neurons and the control of combined eye–head gaze saccades in the alert cat. J. Neurophysiol. 79, 3060–3076 (1998).

    Article  Google Scholar 

  42. MacPherson, J.M. & Aldridge, J.W. A quantitative method of computer analysis of spike train data collected from behaving animals. Brain Res. 175, 183–187 (1979).

    Article  CAS  Google Scholar 

  43. Richmond, B.J., Optican, L.M., Podell, M. & Spitzer H. Temporal encoding of two-dimensional patterns by single units in primate inferior temporal cortex. I. Response characteristics. J. Neurophysiol. 57, 132–146 (1987)

    Article  CAS  Google Scholar 

Download references

Acknowledgements

Funded by the Canadian Institutes of Health Research (CIHR). A.B. held a CIHR studentship. S.M. was supported by a Grant-in-Aid for Scientific Research from the Japanese Ministry of Education, Science and Culture. We thank W.Y. Choi.

Author information

Authors and Affiliations

  1. Department of Neurology and Neurosurgery and Montreal Neurological Institute, McGill University, 3801 University St., Montreal, H3A2B4, Quebec, Canada

    André Bergeron, Satoshi Matsuo & Daniel Guitton

Authors
  1. André Bergeron
    View author publications

    Search author on:PubMed Google Scholar

  2. Satoshi Matsuo
    View author publications

    Search author on:PubMed Google Scholar

  3. Daniel Guitton
    View author publications

    Search author on:PubMed Google Scholar

Corresponding author

Correspondence to Daniel Guitton.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Bergeron, A., Matsuo, S. & Guitton, D. Superior colliculus encodes distance to target, not saccade amplitude, in multi-step gaze shifts. Nat Neurosci 6, 404–413 (2003). https://doi.org/10.1038/nn1027

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue date:

  • DOI: https://doi.org/10.1038/nn1027

This article is cited by

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing