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The Journal of Neuroscience, November 11, 2009, 29(45):14352-14362; doi:10.1523/JNEUROSCI.3498-09.2009

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Behavioral/Systems/Cognitive
Local Changes in the Excitability of the Cerebellar Cortex Produce Spatially Restricted Changes in Complex Spike Synchrony

Sarah P. Marshall and Eric J. Lang

Department of Physiology and Neuroscience, New York University School of Medicine, New York, New York 10016

Correspondence should be addressed to Dr. Eric J. Lang, Department of Physiology and Neuroscience, New York University School of Medicine, 550 First Avenue, New York, NY 10016. Email: eric.lang{at}nyumc.org

Complex spike (CS) synchrony patterns are modulated by the release of GABA within the inferior olive (IO). The GABAergic projection to most of the IO arises from the cerebellar nuclei, which are themselves subject to strong inhibitory control by Purkinje cells in the overlying cortex. Moreover, the connections between the IO and cerebellum are precisely aligned, raising the possibility that each cortical region controls its own CS synchrony distribution. This possibility was tested using multielectrode recordings of CSs and simple spikes (SSs) in crus 2a of anesthetized rats. Picrotoxin or muscimol was applied to the cerebellar cortex at the borders of the recording array. These drugs induced significant changes in CS synchrony and in CS and SS firing rates and changes in post-CS pauses and modulation of SS activity. The level of CS synchrony was correlated with SS firing rate in control, and application of picrotoxin increased both. In contrast, muscimol decreased CS synchrony. Furthermore, when picrotoxin was applied only at the lateral edge of the array, changes in CS synchrony occurred sequentially across the recording array, with cells located in the lateral half of the array having earlier and larger changes in CS synchrony than cells in the medial half. The results indicate that a double-inhibitory feedback circuit from Purkinje cells to the IO provides a mechanism by which SS activity may regulate CS synchrony. Thus, CS synchrony may be a physiologically controlled parameter of cerebellar activity, with the cerebellum and IO comprising a series of self-updating circuits.

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Received May 27, 2009; revised Oct. 1, 2009; accepted Oct. 2, 2009.

Correspondence should be addressed to Dr. Eric J. Lang, Department of Physiology and Neuroscience, New York University School of Medicine, 550 First Avenue, New York, NY 10016. Email: eric.lang{at}nyumc.org

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