Architecture of a gain controller in the pursuit system.

A monkey can pursue faster target oscillations if they appear during ongoing smooth pursuit than if they appear while the monkey is fixating a stationary target. Others have proposed a switch in the pursuit circuit to account for this bistable sensitivity to high frequency targets. It is hypothesized that the switch is closed only during pursuit, permitting the retinal motion signal to pass through the circuit at full gain. Losses in pursuit gain caused by certain cortical lesions do mimic the effect of a switch jammed open. To explore this gain adjustment mechanism further, we measured in monkeys the smooth eye movements in response to a high frequency sinusoidal target (called 'humm') presented under a variety of testing conditions. Pursuit gain measured in response to this humm was not merely bistable. Rather, a graded gain modulation of the pursuit system was possible. Furthermore, the gain adjustment had some directional sensitivity to it, enhancing the response to humm along one axis more than the other. In exploring the factors which gated the gain adjustment, it appeared that the movement of the eyes and not the image motion that occurs during pursuit was paramount for enhancing pursuit gain. Gain was not enhanced by saccadic but only by smooth pursuit tracking movements. Finally, gain could be modulated somewhat by covert signals such as the expectation of future smooth pursuit movements.