Analysis of the frequency response of the saccadic circuit: system behavior.

To more thoroughly describe the system dynamics for the saccadic circuit in monkeys, we have determined the frequency response by applying a frequency modulated train of microstimulation pulses in the superior colliculus. The resulting eye movements reflect the transfer function of the saccadic circuit. Below input modulations of 5 cycles/s, the saccadic circuit increasingly oscillates with multiple high-frequency, low-amplitude movements reminiscent of the "staircase saccades" evoked during the sustained step response. Between 5 and 20 cycles/s, the circuit entrains well to the input, exhibiting one saccadic response to each sinusoidal input. Within this range there are systematic frequency-dependent changes in movement amplitudes, including super-normal saccades at some input frequencies. Above 20 cycles/s, the saccadic circuit increasingly exhibits periodic failures at rates of 1:2 or higher. In addition, the circuit exhibits predictable amplitude-modulated interference patterns in response to a combined step and frequency-modulated input. These experimental results provide insight into several biological mechanisms and serve as benchmark tests of viable models of the saccadic system. The data are consistent with negative feedback models of the saccadic system that operate as a displacement controller and inconsistent with theories that put the superior colliculus within the lowest-order, local feedback loop. The data support theories that the circuit feedback operates with dynamics that simulate a "leaky integrator." In addition, the results demonstrate how the temporal output of the superior colliculus interacts with recurrent inhibition to influence the eye movement dynamics.