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Climbing Fibers Mediate Vestibular Modulation of Both “Complex” and “Simple Spikes” in Purkinje Cells

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Abstract

Climbing and mossy fibers comprise two distinct afferent paths to the cerebellum. Climbing fibers directly evoke a large multispiked action potential in Purkinje cells termed a “complex spike” (CS). By logical exclusion, the other class of Purkinje cell action potential, termed “simple spike” (SS), has often been attributed to activity conveyed by mossy fibers and relayed to Purkinje cells through granule cells. Here, we investigate the relative importance of climbing and mossy fiber pathways in modulating neuronal activity by recording extracellularly from Purkinje cells, as well as from mossy fiber terminals and interneurons in folia 8–10. Sinusoidal roll-tilt vestibular stimulation vigorously modulates the discharge of climbing and mossy fiber afferents, Purkinje cells, and interneurons in folia 9–10 in anesthetized mice. Roll-tilt onto the side ipsilateral to the recording site increases the discharge of both climbing fibers (CSs) and mossy fibers. However, the discharges of SSs decrease during ipsilateral roll-tilt. Unilateral microlesions of the beta nucleus (β-nucleus) of the inferior olive blocks vestibular modulation of both CSs and SSs in contralateral Purkinje cells. The blockage of SSs occurs even though primary and secondary vestibular mossy fibers remain intact. When mossy fiber afferents are damaged by a unilateral labyrinthectomy (UL), vestibular modulation of SSs in Purkinje cells ipsilateral to the UL remains intact. Two inhibitory interneurons, Golgi and stellate cells, could potentially contribute to climbing fiber-induced modulation of SSs. However, during sinusoidal roll-tilt, only stellate cells discharge appropriately out of phase with the discharge of SSs. Golgi cells discharge in phase with SSs. When the vestibularly modulated discharge is blocked by a microlesion of the inferior olive, the modulated discharge of CSs and SSs is also blocked. When the vestibular mossy fiber pathway is destroyed, vestibular modulation of ipsilateral CSs and SSs persists. We conclude that climbing fibers are primarily responsible for the vestibularly modulated discharge of both CSs and SSs. Modulation of the discharge of SSs is likely caused by climbing fiber-evoked stellate cell inhibition.

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Acknowledgments

This research was supported by DC006668 from the National Institute of Deafness and Communicative Disorders and EY018561 from the National Eye Institute.

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The authors declare that they have no competing interests.

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  1. Department of Physiology and Pharmacology, Oregon Health & Science University, 3181 SW Sam Jackson Park Road, Portland, OR, 97239, USA

    N. H. Barmack & V. Yakhnitsa

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  1. N. H. Barmack
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Correspondence to N. H. Barmack.

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I first encountered Enrico Mugnaini when I was beginning and he was ending a postdoctoral fellowship in Oslo in the fall of 1969. I most remember Enrico speaking with enthusiasm as he described his most recent electron micrographs demonstrating cerebellar circuitry. Our paths crossed at several meetings during the next 10 years. Each time, he not only had new and interesting findings but was keen to learn how the circuitry fit together functionally. In 1980, I was recruited by the Department of Biological Sciences at the University of Connecticut. So Enrico and I became colleagues and collaborators. We worked together in unraveling the GABAergic pathways to the inferior olive.

Anyone who visited Enrico’s laboratory could only describe it as an adventure. While most of the campus buildings at UCONN were clustered together, Enrico’s lab was set apart on the side of a hill in a farm meadow. Descending to his lab felt like falling off the edge of the earth. A rusted-out tractor marked the entrance to his lab. When we co-examined immunohistochemical preparations he engaged in an anthropomorphic narrative of each histological detail.

Both of us eventually left UCONN. Enrico had a very productive period at Northwestern, scientifically and administratively. I knew that he would become an excellent chairman, because he had the ability to engage informal and humorous conversation with me in his laboratory while simultaneously feigning anger and insult on the telephone with an administrator who had done him wrong. This volume to honor his work and career is more than justified.

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Barmack, N.H., Yakhnitsa, V. Climbing Fibers Mediate Vestibular Modulation of Both “Complex” and “Simple Spikes” in Purkinje Cells. Cerebellum 14, 597–612 (2015). https://doi.org/10.1007/s12311-015-0725-1

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