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The Journal of Neuroscience, May 15, 2003, 23(10):4288-4298
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Rapid Motor Learning in the Translational Vestibulo-Ocular Reflex
Wu Zhou,1,2,3 Patrick Weldon,2 Bingfeng Tang,2 andW. M. King2,3,4 1Department of Otolaryngology and Communicative Sciences, University of Mississippi Medical Center, Jackson, Mississippi 39216, 2Department of Neurology, University of Mississippi Medical Center, Jackson, Mississippi 39216, 3Department of Anatomy, University of Mississippi Medical Center, Jackson, Mississippi 39216, and 4Department of Otolaryngology, University of Michigan, Ann Arbor, Michigan 48109
Motor learning was induced in the translational vestibulo-ocular reflex (TVOR) when monkeys were repeatedly subjected to a brief (0.5 sec) head translation while they tried to maintain binocular fixation on a visual target for juice rewards. If the target was world-fixed, the initial eye speed of the TVOR gradually increased; if the target was head-fixed, the initial eye speed of the TVOR gradually decreased. The rate of learning acquisition was very rapid, with a time constant of
100 trials, which was equivalent to <1 min of accumulated stimulation. These learned changes were consolidated over
1 d without any reinforcement, indicating induction of long-term synaptic plasticity. Although the learning generalized to targets with different viewing distances and to head translations with different accelerations, it was highly specific for the particular combination of head motion and evoked eye movement associated with the training. For example, it was specific to the modality of the stimulus (translation vs rotation) and the direction of the evoked eye movement in the training. Furthermore, when one eye was aligned with the heading direction so that it remained motionless during training, learning was not expressed in this eye, but only in the other nonaligned eye. These specificities show that the learning sites are neither in the sensory nor the motor limb of the reflex but in the sensory-motor transformation stage of the reflex. The dependence of the learning on both head motion and evoked eye movement suggests that Hebbian learning may be one of the underlying cellular mechanisms.
Key words: motor learning; VOR; monkey; sensory-motor transformation; synaptic plasticity; Hebbian learning; otolith
Received Oct. 3, 2002; revised Feb. 20, 2003; accepted Feb. 28, 2003.
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