Initial tracking conditions modulate the gain of visuo-motor transmission for smooth pursuit eye movements in monkeys

Abstract

Smooth pursuit eye movements allow primates to keep gaze pointed at small objects moving across stationary surroundings. In monkeys trained to track a small moving target, we have injected brief perturbations of target motion under different initial conditions as probes to read out the state of the visuo-motor pathways that guide pursuit. A large eye movement response was evoked if the perturbation was applied to a moving target the monkey was tracking. A small response was evoked if the same perturbation was applied to a stationary target the monkey was fixating. The gain of the response to the perturbation increased as a function of the initial speed of target motion and as a function of the interval from the onset of target motion to the time of the perturbation. The response to the perturbation also was direction selective. Gain was largest if the perturbation was along the axis of ongoing target motion and smallest if the perturbation was orthogonal to the axis of target motion. We suggest that two parallel sets of visual motion pathways through the extrastriate visual cortex may mediate, respectively, the visuo-motor processing for pursuit and the modulation of the gain of transmission through those pathways.

The Role of the Frontal Pursuit Area in Learning in Smooth Pursuit Eye Movements

“…In the absence of stimulation in the FPA, responses to the perturbation (Fig. 5B, gray traces) had gains of 0.2-0.5, consistent with previous observations (Schwartz and Lisberger, 1994). If the brief target motion was paired with microstimulation in the FPA, then the response to the perturbations was increased (Fig.…”

“…conditions alter the size of the motor response to a given visual stimulus (Schwartz and Lisberger, 1994;Tanaka and Lisberger, 2000;Missal and Heinen, 2001;Churchland and Lisberger, 2002). The output from the structure that we have studied here, the FPA, appears both to provide commands that drive smooth eye velocity and to play an important role in controlling the setting of the gain control Lisberger 2001, 2002a).…”

“…One process derives information about the direction and speed of image motion across the retina from the middle temporal (MT) and medial superior temporal (MST) areas of the extrastriate cortex and generates commands for changes in horizontal and vertical smooth eye velocity (Dursteler and Wurtz, 1988;Komatsu and Wurtz, 1988). The other process acts as a "gain control" that determines how strongly pursuit will respond to a given visual motion stimulus (Schwartz and Lisberger, 1994). Recent experiments from our laboratory have shown that output from the frontal pursuit area (FPA) in the arcuate sulcus can modulate the gain control: stimulation of the FPA increases the gain of smooth eye movements evoked by a given visual motion stimulus Lisberger, 2001, 2002a).…”

Inactivation and stimulation of the frontal pursuit area change pursuit metrics without affecting pursuit target selection

“…Stimulation during pursuit or fixation also increases the eye velocity response to perturbations of the tracked or fixated target stimulus (Tanaka and Lisberger 2001). These effects are analogous to the increase in the gain of the response to target perturbations during ongoing pursuit (Schwartz and Lisberger 1994) and demonstrate that activity in the FPA exerts a powerful influence over the gain of eye movement responses to visual motion inputs.…”

How Do Primates Anticipate Uncertain Future Events?

“…However, the same perturbation will induce a larger eye velocity response if injected during smooth pursuit (Schwartz and Lisberger, 1994;Churchland and Lisberger, 2002). This internal gain modulation depends of the context of the task (Keating and Pierre, 1996;Krauzlis and Miles, 1996;Tanaka and Lisberger, 2000) and the behavioral conditions (Churchland and Lisberger, 2002).…”