Learning on Multiple Timescales in Smooth Pursuit Eye Movements
- 1 November 2010
- journal article
- research article
- Published by American Physiological Society in Journal of Neurophysiology
- Vol. 104 (5), 2850-2862
- https://doi.org/10.1152/jn.00761.2010
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.Keywords
This publication has 48 references indexed in Scilit:
- Size of Error Affects Cerebellar Contributions to Motor LearningJournal of Neurophysiology, 2010
- Dual Adaptation Supports a Parallel Architecture of Motor MemoryJournal of Neuroscience, 2009
- Mechanisms of Potentiation of Mossy Fiber EPSCs in the Cerebellar Nuclei by Coincident Synaptic Excitation and InhibitionJournal of Neuroscience, 2008
- Links from complex spikes to local plasticity and motor learning in the cerebellum of awake-behaving monkeysNature Neuroscience, 2008
- Spontaneous Recovery of Motor Memory During Saccade AdaptationJournal of Neurophysiology, 2008
- Calibration of Visually Guided Reaching Is Driven by Error-Corrective Learning and Internal DynamicsJournal of Neurophysiology, 2007
- Interacting Adaptive Processes with Different Timescales Underlie Short-Term Motor LearningPLoS Biology, 2006
- CEREBELLUM-DEPENDENT LEARNING: The Role of Multiple Plasticity MechanismsAnnual Review of Neuroscience, 2004
- A long-term depression of AMPA currents in cultured cerebellar purkinje neuronsNeuron, 1991
- Neural design of the cerebellar motor control systemBrain Research, 1972