Abstract
A visual scene is scrutinized during sequential periods of steady fixation, connected by saccades that shift the visual axis (gaze) to new positions. During such exploratory scan paths, gaze frequently strays from and then returns to salient features. How the brain keeps track of major end-goals and intermediate subgoals is not understood. We studied the discharge of fixation neurons of the brainstem's superior colliculus during multiple-step gaze shifts composed of a sequence of saccades made in the dark and separated by short periods of steady fixation. Cells were initially silent. As sequential gaze saccades approached the goal, firing began; its frequency increased progressively and peaked when gaze was on the remembered target location. We conclude that these fixation neurons encode the error between desired and actual gaze positions, irrespective of trajectory characteristics.
This is a preview of subscription content, access via your institution
Access options
Subscribe to this journal
Receive 12 print issues and online access
$209.00 per year
only $17.42 per issue
Buy this article
- Purchase on Springer Link
- Instant access to full article PDF
Prices may be subject to local taxes which are calculated during checkout
Similar content being viewed by others
References
Munoz, D. P. & Wurtz, R. H. Fixation cells in monkey superior colliculus. I. Characteristics of cell discharge. J. Neurophysiol. 70, 559–575 (1993).
Hanes, D. P., Patterson, W. F. & Schall J. D. Role of frontal eye fields in countermanding saccades: visual, movement, and fixation activity. J. Neurophysiol. 79, 817–834 (1998).
Munoz, D. P. & Guitton, D. Fixation and orientation control by the tecto-reticulo-spinal system in the cat whose head is unrestrained . Rev. Neurol. (Paris) 145, 567– 579 (1989).
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).
Paré, M. & Guitton, D. The fixation area of the cat superior colliculus: effects of electrical stimulation and direct connection with brainstem omnipause neurons. Exp. Brain Res. 101, 109–122 (1994).
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).
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).
Everling, S., Paré, M., Dorris, M. C. & Munoz, D. P. Comparison of the discharge characteristics of brain stem omnipause neurons and superior colliculus fixation neurons in monkey: implications for control of fixation and saccade behavior. J. Neurophysiol. 79, 511–528 (1998).
Munoz, D. P. & Wurtz, R. H. Fixation cells in monkey superior colliculus. II. Reversible activation and deactivation. J. Neurophysiol. 70, 576–589 (1993).
Munoz, D. P. & Wurtz, R. H. Saccade-related activity in monkey superior colliculus. II. Spread of activity during saccades. J. Neurophysiol. 73, 2334–2348 (1995).
Gandhi, N. J. & Keller, E. L. Spatial distribution and discharge characteristics of superior colliculus neurons antidromically activated from the omnipause region in monkey. J. Neurophysiol. 78 , 2221–2225 (1997).
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).
Grantyn, A. & Berthoz, A. Burst activity of identified tecto-reticulo-spinal neurons in the alert cat. Exp. Brain Res. 57, 417–421 (1985).
Grantyn, A. & Grantyn, R. Axonal patterns and sites of termination of cat superior colliculus neurons projecting in the tecto-bulbo-spinal tract . Exp. Brain Res. 46, 243– 256 (1982).
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).
Munoz, D. P. & Istvan, P. J. Lateral inhibitory interactions in the intermediate layers of the monkey superior colliculus. J. Neurophysiol. 79, 1193–1209 (1998).
Büttner-Ennever, J. A., Horn, A. K. E., Henn, V. & Cohen, B. Projections from the superior colliculus motor map to omnipause neurons. J. Comp. Neurol. 413, 55–67 (1999).
Evinger, C., Kaneko, C. R. & Fuchs, A. F. Activity of omnipause neurons in alert cats during saccadic eye movements and visual stimuli. J. Neurophysiol. 47, 827–844 (1982).
Guitton, D., Douglas, R. M. & Volle, M. Coordinated eye head movements in the cat. J. Neurophysiol. 52, 1030–1050 (1984).
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).
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).
Krauzlis, R. J., Basso, M. A. & Wurtz, R. H. Shared motor error for multiple eye movements. Science 276, 1693–1695 (1997).
Petit, J., Klam, F., Grantyn, A. & Berthoz, A. Saccades and multisaccadic gaze shifts are gated by different pontine omnipause neurons in head-fixed cats. Exp. Brain Res. 125, 287– 301 (1999).
Jeannerod, M., Gerin, P. & Pernier, J. Déplacement et fixations du regard dans l'exploration libre d'une scène visuelle. Vision Res. 8, 81–97 (1968).
Yarbus, A.L. Eye Movement and Vision (Plenum, New York, 1967).
Zusne, L. & Michels, K. M. Nonrepresentational shapes and eye movements. Perceptual Motor Skills 18, 11–20 (1964).
Robinson, D. A. A method of measuring eye movements using a scleral search coil in a magnetic field. IEEE Trans. Biomed. Eng. 10, 137– 145 (1963).
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).
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).
Acknowledgements
Funded by the Medical Research Council of Canada. We thank J. Murphy for developing some of the electrode technology and W.Y. Choi, D. Crawford, K. Cullen and T. Herter for reading earlier versions of the manuscript.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Bergeron, A., Guitton, D. Fixation neurons in the superior colliculus encode distance between current and desired gaze positions. Nat Neurosci 3, 932–939 (2000). https://doi.org/10.1038/78847
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1038/78847
This article is cited by
-
Retinal sensitivity and gaze fixation evaluated by microperimetry in subjects with type 2 diabetes: two independent parameters that explore different neuronal circuits
Journal of Endocrinological Investigation (2023)
-
Activation of superior colliculi in humans during visual exploration
BMC Neuroscience (2007)
-
Superior colliculus encodes distance to target, not saccade amplitude, in multi-step gaze shifts
Nature Neuroscience (2003)