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The Journal of Neuroscience, January 30, 2008, 28(5):1140-1152; doi:10.1523/JNEUROSCI.3942-07.2008

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Behavioral/Systems/Cognitive
Functions of Interneurons in Mouse Cerebellum

Neal H. Barmack and Vadim Yakhnitsa

Neurological Sciences Institute, Oregon Health & Science University, Beaverton, Oregon 97006

Correspondence should be addressed to Dr. Neal H. Barmack, Neurological Sciences Institute, Oregon Health & Science University, 505 Northwest 185th Avenue, Beaverton, OR 97006. Email: barmackn{at}ohsu.edu

The output signal of Purkinje cells is conveyed by the modulated discharge of simple spikes (SSs) often ascribed to mossy fiber–granule cell–parallel fiber inputs to Purkinje cell dendrites. Although generally accepted, this view lacks experimental support. We can address this view by controlling afferent signals that reach the cerebellum over climbing and mossy fiber pathways. Vestibular primary afferents constitute the largest mossy fiber projection to the uvula-nodulus. The discharge of vestibular primary afferent mossy fibers increases during ipsilateral roll tilt. The discharge of SSs decreases during ipsilateral roll tilt. Climbing fiber discharge [complex spikes (CSs)] increases during ipsilateral roll tilt. These observations suggest that the modulation of SSs during vestibular stimulation cannot be attributed directly to vestibular mossy fiber afferents. Rather we suggest that interneurons driven by vestibular climbing fibers may determine SS modulation. We recorded from cerebellar interneurons (granule, unipolar brush, Golgi, stellate, basket, and Lugaro cells) and Purkinje cells in the uvula-nodulus of anesthetized mice during vestibular stimulation. We identified all neuronal types by juxtacellular labeling with neurobiotin. Granule, unipolar brush, stellate, and basket cells discharge in phase with ipsilateral roll tilt and in phase with CSs. Golgi cells discharge out of phase with ipsilateral roll tilt and out of phase with CSs. The phases of stellate and basket cell discharge suggests that their activity could account for the antiphasic behavior of CSs and SSs. Because Golgi cells discharge in phase with SSs, Golgi cell activity cannot account for SS modulation. The sagittal array of Golgi cell axon terminals suggests that they contribute to the organization of discrete parasagittal vestibular zones.

Key words: mossy fiber; climbing fiber; inferior olive; nodulus; uvula; Golgi cell; stellate cell; granule cell; unipolar brush cell

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Received Aug. 28, 2007; revised Dec. 14, 2007; accepted Dec. 17, 2007.

Correspondence should be addressed to Dr. Neal H. Barmack, Neurological Sciences Institute, Oregon Health & Science University, 505 Northwest 185th Avenue, Beaverton, OR 97006. Email: barmackn{at}ohsu.edu

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