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.

Fig. 1

Example of saccade-induced target choice for pursuit at a single stimulation site. (a) Eye position traces from trials in which microstimulation was applied during fixation show evoked saccadic eye movement. (b) Target configurations were specifically tailored for the evoked saccade from this site such that one target (stim target) crossed the endpoint of the evoked saccade (dashed circle), and the other target (non-stim target) moved in an orthogonal direction. Eye position (c) and velocity (d) are shown for the away configuration. Blue and green traces are stim target trajectory and non-stim target trajectory, respectively. Black and red traces are eye movement records from control and stimulation trials, respectively. Upward deflections indicate rightward (for horizontal traces) or upward (for vertical traces) eye position (c) or velocity (d).

Fig. 2

Saccade-induced target choice for pursuit is selective for the direction of motion of the target and not the direction of the saccade. At the same stimulation site as in Figure 1, we tested target motion towards the initial fixation position (a) in the opposite direction as the evoked saccade, thus disassociating the two directions. Eye and target position (b) and velocity (c) traces follow the same convention as in Fig. 1.

Fig. 3

Trial-by-trial analysis of target choice for pursuit by saccades. Each point shows the direction and speed of smooth eye velocity from a single trial. Different graphs plot data measured after evoked saccades (b), after natural saccades (c), and at the same time in control trials as after evoked saccades on stimulation trials (a). Points have been rotated and flipped as necessary so that the direction of pursuit to the stim target presented alone is rightward (0°, stim target dir) and the direction of the non-stim target is upward (non-stim target dir). Points have been colored according to how densely packed on the graph they are: 100% density refers to the maximum density for each graph. Two and thirteen points plotted off the axis of the graphs in (b) and (c), respectively, and were therefore omitted.

Fig. 4

Target choice for pursuit by saccades, averaged across all trials. Small ellipses mark the 95% confidence ellipses around the mean and large ellipses indicate the standard ellipse. Different colors indicate control eye velocity (black), eye velocity after stimulation evoked saccades (red), and eye velocity after natural targeting saccades (blue). Ellipses were computed after rotating and flipping the points as described in Fig. 3.

Fig. 5

Target choice for pursuit by saccades is not a transient phenomenon. Choice probability is plotted as a function of time after the end of stimulation evoked saccades (red) and natural targeting saccades (blue) and at the same time in control trials (black) as for stimulation evoked saccades. Bootstrapping was used to estimate 95% confidence intervals.

Fig. 6

Subthreshold stimulation of the FEF does not enhance pursuit. (a) Horizontal eye velocity is plotted for one site where suprathreshold stimulation (red traces) caused pursuit target selection. When stimulation frequency was reduced to just below the rate at which saccades are elicited (cyan traces), it did not change pursuit compared to control (black traces) trials. (b) Summary data for all seven subthreshold sites. Pursuit velocity in subthreshold trials (cyan) analyzed at the same time relative to target onset as suprathreshold trials (red) do not differ significantly from control non-stimulation trials (black).

Fig. 7

Saccades elicited from the SC also cause target selection for pursuit. (a) Horizontal eye velocity trace showing stimulation effect (red) as compared to controls (black). (b) Summary data, same conventions as Figs. 6 and 4.