The role of the frontal pursuit area in learning in smooth pursuit eye movements.

The frontal pursuit area (FPA) in the cerebral cortex is part of the circuit for smooth pursuit eye movements. The present paper asks whether the FPA is upstream, downstream, or at the site of learning in pursuit eye movements. Learning was induced by having monkeys repeatedly pursue targets that moved at one speed for 150 msec before changing speed. Single-cell recording showed no consistent correlate of pursuit learning in the responses of FPA neurons. Some neurons showed changes in firing in the same direction as the learning, others showed changes in the opposite direction, and many showed no changes at all. In contrast, the eye movements evoked by electrical stimulation of the FPA showed clear correlates of learning. Learning effects were observed when microstimulation was delivered during the initiation of pursuit and during fixation of a stationary target. In addition, learning caused changes in the degree to which stimulation of the FPA enhanced the eye velocity evoked by brief perturbations of a stationary target. The magnitude of the change in the stimulation-evoked eye movement in each tracking condition was proportional to the size of the eye movement evoked under that condition before learning. We conclude that learning occurs downstream from the FPA, possibly within the cerebellum, and that learning may be related to mechanisms that also control the gain of visual-motor responses on a rapid time scale.

Evidence for object permanence in the smooth-pursuit eye movements of monkeys.

We recorded the smooth-pursuit eye movements of monkeys in response to targets that were extinguished (blinked) for 200 ms in mid-trajectory. Eye velocity declined considerably during the target blinks, even when the blinks were completely predictable in time and space. Eye velocity declined whether blinks were presented during steady-state pursuit of a constant-velocity target, during initiation of pursuit before target velocity was reached, or during eye accelerations induced by a change in target velocity. When a physical occluder covered the trajectory of the target during blinks, creating the impression that the target moved behind it, the decline in eye velocity was reduced or abolished. If the target was occluded once the eye had reached target velocity, pursuit was only slightly poorer than normal, uninterrupted pursuit. In contrast, if the target was occluded during the initiation of pursuit, while the eye was accelerating toward target velocity, pursuit during occlusion was very different from normal pursuit. Eye velocity remained relatively stable during target occlusion, showing much less acceleration than normal pursuit and much less of a decline than was produced by a target blink. Anticipatory or predictive eye acceleration was typically observed just prior to the reappearance of the target. Computer simulations show that these results are best understood by assuming that a mechanism of eye-velocity memory remains engaged during target occlusion but is disengaged during target blinks.

Directional anisotropies reveal a functional segregation of visual motion processing for perception and action.

Human exhibits an anisotropy in direction perception: discrimination is superior when motion is around horizontal or vertical rather than diagonal axes. In contrast to the consistent directional anisotropy in perception, we found only small idiosyncratic anisotropies in smooth pursuit eye movements, a motor action requiring accurate discrimination of visual motion direction. Both pursuit and perceptual direction discrimination rely on signals from the middle temporal visual area (MT), yet analysis of multiple measures of MT neuronal responses in the macaque failed to provide evidence of a directional anisotropy. We conclude that MT represents different motion directions uniformly, and subsequent processing creates a directional anisotropy in pathways unique to perception. Our data support the hypothesis that, at least for visual motion, perception and action are guided by inputs from separate sensory streams. The directional anisotropy of perception appears to originate after the two streams have segregated and downstream from area MT.

Spatial generalization of learning in smooth pursuit eye movements: implications for the coordinate frame and sites of learning.

We have examined the underlying coordinate frame for pursuit learning by testing how broadly learning generalizes to different retinal loci and directions of target motion. Learned changes in pursuit were induced using double steps of target speed. Monkeys tracked a target that stepped obliquely away from the point of fixation, then moved smoothly either leftward or rightward. In each experimental session, we adapted the response to targets moving in one direction across one locus of the visual field by changing target speed during the initial catch-up saccade. Learning occurred in both presaccadic and postsaccadic eye velocity. The changes were specific to the adapted direction and did not generalize to the opposite direction of pursuit. To test the spatial scale of learning, we examined the responses to targets that moved across different parts of the visual field at the same velocity as the learning targets. Learning generalized partially to motion presented at untrained locations in the visual field, even those across the vertical meridian. Experiments with two sets of learning trials showed interference between learning at different sites in the visual field, suggesting that pursuit learning is not capable of spatial specificity. Our findings are consistent with the previous suggestions that pursuit learning is encoded in an intermediate representation that is neither strictly sensory nor strictly motor. Our data add the constraint that the site or sites of pursuit learning must process visual information on a fairly large spatial scale that extends across the horizontal and vertical meridians.