Learning on Multiple Timescales in Smooth Pursuit Eye Movements

Abstract

We commonly think of motor learning as a gradual process that makes small, adaptive steps in a consistent direction. We now report evidence that learning in pursuit eye movements could start with large, transient short-term alterations that stoke a more gradual long-term process. Monkeys tracked a target that started moving horizontally or vertically. After 250 ms of motion had produced a preinstruction eye velocity close to target velocity, an orthogonal component of target motion created an instructive change in target direction that was randomly in one of the two directions along the orthogonal axis. The preinstruction eye velocity in each trial expressed single-trial learning as a bias toward the direction of the instruction in the prior trial. The single-trial learning was forgotten within 4 to 10 s. Two observations implied that single-trial learning was not simply cognitive anticipation. First, the magnitude of the trial-over-trial change in eye velocity depended on the ongoing eye velocity at the time of the instruction in the prior trial. Single-trial learning was negligible if the prior trial had provided a well-timed cue without evoking any preinstruction eye velocity. Second, regular alternation of the direction of the instructive target motion caused reactive rather than anticipatory trial-over-trial changes in eye velocity. Humans showed very different responses that appeared to be based on cognitive anticipation rather than learning. We suggest that single-trial learning results from a low-level learning mechanism and may be a necessary prerequisite for longer-term modifications that are more permanent.

Timing Rules for Synaptic Plasticity Matched to Behavioral Function

“…During oculomotor learning, a spike in a climbing fiber on one trial is associated with a suppression of firing in its Purkinje cell target on the next trial (Kimpo et al, 2014; Medina and Lisberger, 2008; Yang and Lisberger, 2010, 2014). The temporal precision of this single-trial plasticity reported in vivo had appeared to be significantly less than what we found at the PF-to-PC synapses in vitro (hundreds of milliseconds vs. tens of milliseconds).…”

Reward Action in the Initiation of Smooth Pursuit Eye Movements

“…We subjected monkeys to tracking conditions that cause a learned change in the direction of pursuit eye movements (Medina et al, 2005; Yang and Lisberger, 2010) under different reward conditions. The schematic at the top of Figure 8 illustrates the configuration of the “learning” and “probe” trials used for these experiments.…”

Learned Timing of Motor Behavior in the Smooth Eye Movement Region of the Frontal Eye Fields

“…Previous studies have suggested that motor learning occurs on multiple time scales (Lee and Schweighofer, 2009; Ethier et al, 2008; Smith et al, 2006), including situations where the behavior on a given trial reflects the instruction provided on the previous trial (Yang and Lisberger, 2010). To measure the relative contributions of single-trial versus longer-term learning processes to the behavioral and neural changes reported here, we sorted learning trials based on the identity of the immediately preceding trial.…”

“…Thus, the cerebellum could act independently in learning motor timing, or inputs from the FEF SEM could contribute to the temporal sparseness of the granule cell population in a way that is enhanced by learning in the FEF SEM . Recent work also has highlighted the possibility that learning occurs on different time scales (Lee and Schweighofer, 2009; Ethier et al, 2008; Smith et al, 2006; Yang and Lisberger, 2010) with the possibility of very rapid short term learning in the cerebellar cortex as a prelude to slower, longer-term changes in the FEF SEM .…”