Relationship Between Extraretinal Component of Firing Rate and Eye Speed in Area MST of Macaque Monkeys

We have isolated extraretinal and retinal components of firing during smooth pursuit eye movements in the medial-superior-temporal area (MST) in the extrastriate visual cortex. Awake macaque monkeys tracked spots in total darkness to eliminate image motion inputs from the background. For 300 ms during sustained tracking at different speeds, the target was stabilized on the moving eye, practically eliminating image motion inputs from the tracking target. The extraretinal component of firing rate during image stabilization was direction selective and related to eye speed but sometimes showed a different preferred speed from the retinal component of the same neuron's responses. The highly variable firing rate of individual MST neurons allowed an ideal observer to predict target speed correctly on 25% of trials. Pooling the data from 71 MST neurons improved the correct response rate to 50%. Behavioral experiments imposed brief perturbations of target velocity to assess the gain of visual-motor transmission for pursuit. The average response to perturbations increased as a function of target speed. However, the size of the responses to individual perturbations allowed an ideal observer to predict target speed correctly on only 35% of the trials. The imprecision of MST responses argues that the output of MST may be a poor candidate to drive eye velocity and so may instead regulate another component of pursuit. The good agreement between the eye velocity precision of the behavioral responses to perturbations of target motion and the firing of MST neurons raises regulation of the visual-motor gain of pursuit as one candidate component.