Coordinate System for Learning in the Smooth Pursuit Eye Movements of Monkeys

Abstract

Learning was induced in smooth pursuit eye movements by repeated presentation of targets that moved at one speed for 100 msec and then changed to a second, higher or lower, speed. The learned changes, measured as eye acceleration for the first 100 msec of pursuit, were largest in a "late" interval from 50 to 80 msec after the onset of pursuit and were smaller and less consistent in the earliest 30 msec of pursuit. In each experiment, target motion in one direction consisted of learning trials, whereas target motion in the opposite (control) direction consisted of trials in which targets moved at a constant speed for the entire duration of the trial. Under these conditions, the learning did not generalize to the control direction. For target motion in the learning direction, the changes in pursuit generalized to responses evoked by targets moving at speeds ranging from 15 to 45 degrees/sec as well as to targets of different colors and sizes. Although learning was induced at the initiation of pursuit, it generalized to the response to image motion in the learning direction when it was presented during pursuit in the learning direction. However, learning did not generalize to the response to image motion in the learning direction when it was presented during pursuit in the control direction. The results suggest that the learning does not occur in purely sensory or motor coordinates but in an intermediate reference frame at least partly defined by the direction of eye movement. The selectivity of learning provides new evidence for a previously hypothesized neural "switch" that gates visual information on the basis of movement direction. This selectivity also suggests that the locus of pursuit learning is in pathways related to the operation of the switch.

A Population Decoding Framework for Motion Aftereffects on Smooth Pursuit Eye Movements

“…Thus, adaptation cannot be caused by a residual smooth eye movement left over from a larger response generated to suppress smooth tracking during presentation of the adapting stimulus. Furthermore, our results are distinct from those for pursuit motor learning, which shows partial generalization to targets presented even in the opposite hemifield (Chou and Lisberger, 2002) and is specific for the direction of target/eye motion rather than the direction of visual motion (Kahlon and Lisberger, 1996). Thus, motion adaptation in pursuit occurs in a sensory coordinate system, whereas pursuit learning occurs in an intermediate, sensory-motor coordinate system.…”

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

“…The graphs in Figure 1 B show the directional specificity of the behavioral learning across all experiments by plotting the change in mean pursuit velocity in the first 200 msec of the response for target motion in the control direction (ordinate) as a function of that for target motion in the learning direction (abscissa). Figure 1 B shows a small negative regression slope of Ϫ0.16 that was significantly different from zero ( p Ͻ 0.01), indicating that the pursuit in the control direction showed weak changes in the opposite direction from those for the learning direction, in agreement with the data of Kahlon and Lisberger (1996). In subsequent graphs, we use the change in eye velocity in the learning direction, in degrees per second, as our independent variable, and we call it the "magnitude of learning."…”

“…Previous examinations of patterns of learning generalization have suggested that learning occurs in a representation that is intermediate between purely sensory and purely motor, and that it is specific to the sensory-motor combination that is being altered (Kahlon and Lisberger, 1996;Chou and Lisberger, 2002). In addition, available evidence suggests that cortical and subcortical circuits generate pursuit through the interaction of two separate processes, either or both of which could be modified by learning.…”

Changes in motion perception following oculomotor smooth pursuit adaptation

“…On the basis of previous research using similar SP adaptation procedures (Carl & Gellman, 1986;Kahlon & Lisberger, 1996), we expected the most consistent effects to be observed for the steady-state eye velocity measure only.…”

“…The use of a double velocity step has recently been shown to be a simple and effective means of adapting SP output (Kahlon & Lisberger, 1996). The motion ofthe target in relation to the SP response is analogous to that occurring when a percentage of eye motion is added onto target motion (Carl & Gellman, 1986;van Donkelaar et aI., 1994;van Donkelaar et aI., 1997;van Donkelaar et aI., 1996).…”