Purkinje cell complex and simple spike changes during a voluntary arm movement learning task in the monkey

C. L. Ojakangas, T. J. Ebner

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102 Scopus citations

Abstract

To evaluate the role of the cerebellum during improvement of voluntary motor performance over time, the discharge of 88 Purkinje cells in the intermediate and lateral cerebellum of two primates (Macaca mulatta) was investigated during a motor learning task involving visually guided arm movements. The animals were trained to move a draftsman's style manipulandum over a horizontally placed video screen. The animals were required to move a cursor from the start box to one of four target boxes by movement of the manipulandum. Errors were introduced into the movement by altering the visual feedback loop, changing the gain between the cursor movement and the hand movement. When a novel gain was presented over 100-200 movement trials, the animals adapted the movements to the new gain. The animals used a strategy of scaling the amplitude and velocity of the initial phase of the movement while keeping the time to peak velocity constant. After implantation of chronic unit recording hardware, Purkinje cell simple and complex spike discharge was recorded extracellularly during the learning task. The cells were located primarily in the ipsilateral intermediate zone or nearby hemisphere of lobules V and VI. Simple and complex spike histograms, as well as averages of the hand displacement and velocity profiles, were calculated for each phase of the paradigm. Statistically significant but transient changes occurred in complex spike discharge. During the learning paradigm, 43% (38/88) of the Purkinje cells exhibited a statistically significant change in complex spike activity. For 76% (29/38), the changes were transient, the complex spike discharge returning to control levels in the testing phase. The changes in complex spike responses were before or during the early phase of the movement (average 35 ms before movement onset to 238 ms after). For cells with a transient increase in complex spike discharge, the phase of maximum activity was almost equally likely to occur during the first, second, or third subperiod of the total learning phase. Using the distance control to account for the different amplitude movements before and after learning, the simple spike response changed during the movement in 34% (22/65) of Purkinje cells in a manner that could not be attributed to alterations in movement distance. Of the 31 cells with a significant change in complex spike discharge during learning in which a distance control was obtained, 10 (32%) exhibited this type of simple spike change. Simple spike background firing rate changed during the learning paradigm. In 65% (42/65) of the Purkinje cells studied, progressive changes occurred in the background simple spike discharge that could not be accounted for by movement distance. The timing of the complex spike and simple spike changes were examined in relation to the learning process using total movement duration as a measure of the adaptation. Adaptation occurred in different subperiods of the learning trials. The majority of complex spike and simple spike responses during movement and simple spike background changes occurred before or in the same phase in which total movement time stabilized. A similar analysis based on the scaling of peak velocity yielded comparable results. From these data, we conclude that the climbing fiber system is transiently activated during the process of learning to scale arm movements.

Original languageEnglish (US)
Pages (from-to)2222-2236
Number of pages15
JournalJournal of neurophysiology
Volume68
Issue number6
DOIs
StatePublished - 1992

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