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Fixation neurons in the superior colliculus encode distance between current and desired gaze positions

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.

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Figure 1: Overview of connectivity and discharge patterns of SCFNs.
Figure 2: Discharges of cell N40 (right superior colliculus) during 12 single-step gaze saccades of different amplitudes.
Figure 3: Discharges of two SCFNs during multiple-step gaze shifts of different amplitudes.
Figure 4: Calculation of minimum standard deviation (s.d.) of time of onset of first spike.
Figure 5: Timing of first spike referred to preferred GPE.
Figure 6: Comparison of timing of first spike between preferred GPE and end of gaze sequence.
Figure 7: Firing frequency during gaze plateaus depends on GPE.

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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.

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Correspondence to Daniel Guitton.

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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

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