Serial linkage of target selection for orienting and tracking eye movements

Abstract

Many natural actions require the coordination of two different kinds of movements. How are targets chosen under these circumstances: do central commands instruct different movement systems in parallel, or does the execution of one movement activate a serial chain that automatically chooses targets for the other movement? We examined a natural eye tracking action that consists of orienting saccades and tracking smooth pursuit eye movements, and found strong physiological evidence for a serial strategy. Monkeys chose freely between two identical spots that appeared at different sites in the visual field and moved in orthogonal directions. If a saccade was evoked to one of the moving targets by microstimulation in either the frontal eye field (FEF) or the superior colliculus (SC), then the same target was automatically chosen for pursuit. Our results imply that the neural signals responsible for saccade execution can also act as an internal command of target choice for other movement systems.

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Figure 1: Example of saccade-induced target choice for pursuit at a single stimulation site.
Figure 2: Saccade-induced target choice for pursuit is selective for the direction of motion of the target and not the direction of the saccade.
Figure 3: Trial-by-trial analysis of target choice for pursuit by saccades.
Figure 4: Target choice for pursuit by saccades, averaged across all trials.
Figure 5: Target choice for pursuit by saccades is not a transient phenomenon.
Figure 6: Subthreshold stimulation of the FEF does not enhance pursuit.
Figure 7: Saccades elicited from the SC also cause target selection for pursuit.

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Acknowledgements

We are grateful to P. Glimcher, M. Shadlen and the Lisberger lab for helpful discussions, and to A. Doupe and I. Chou for comments on an earlier version of the paper. We also thank J. Horton for surgical assistance, K. MacLeod, E. Montgomery and S. Tokiyama for surgical, animal and technical assistance, M. Meneses for animal husbandry, K. McGary for electronics, L. Bocskai for machining, S. Ruffner for computer programming, D. Kleinhesselink for network management and E. Molyneaux for administrative support. Research was supported by the Howard Hughes Medical Institute, National Eye Institute grant EY03878, and a Burroughs Welcome Fund training grant in Quantitative Biology (J.L.G.).

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Correspondence to Justin L. Gardner.

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Gardner, J., Lisberger, S. Serial linkage of target selection for orienting and tracking eye movements. Nat Neurosci 5, 892–899 (2002). https://doi.org/10.1038/nn897

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