Cerebellar climbing fibers modulate simple spikes in Purkinje cells

Neal H. Barmack, Vadim Yakhnitsa

Research output: Contribution to journalArticle

47 Citations (Scopus)

Abstract

Purkinje cells have two action potentials: Climbing fiber responses (CFRs) and simple spikes (SSs). CFRs reflect the discharge of a single climbing fiber at multiple synaptic sites on the proximal dendrite of the Purkinje cell. SSs reflect the summed action of a subset of parallel fiber synapses on Purkinje cell dendritic spines. Because mossy fiber afferents terminate on granule cells, the ascending axons of which bifurcate, giving rise to parallel fibers, the modulation of SSs has been attributed to mossy fiber afferent signals. This inference has never been tested. Conversely, the low discharge frequency of CFRs has led many to conclude that they have a unique and intermittent role in cerebellar signal processing. We examine the relative potency of vestibularly modulated mossy fiber and climbing fiber signals in evoking CFRs and SSs in Purkinje cells of the uvula-nodulus in chloralose- urethane-anesthetized rabbits. Vestibular primary afferents were blocked by unilateral labyrinthectomy (UL). A UL destroys the vestibular primary afferent signal to the ipsilateral uvula-nodulus, while leaving intact the vestibular climbing fiber signal from the contralateral inferior olive. After UL, vestibular stimulation modulated CFRs and SSs in ipsilateral uvula-nodular Purkinje cells, demonstrating that the primary vestibular afferent mossy fiber input to the ipsilateral uvula-nodulus was not necessary for SS modulation. Unilateral microlesions of the caudal half of the β-nucleus of the inferior olive reduced a modulated climbing fiber signal to the contralateral uvula-nodulus, causing loss of both vestibularly modulated CFRs and SSs in contralateral Purkinje cells. Vestibular climbing fibers not only evoke low-frequency CFRs, but also indirectly modulate higher-frequency SSs. This modulation must be attributed to cerebellar interneurons. Golgi cell inhibition of granule cells may provide the interneuronal mechanism for CFR-induced SS modulation.

Original languageEnglish (US)
Pages (from-to)7904-7916
Number of pages13
JournalJournal of Neuroscience
Volume23
Issue number21
StatePublished - Aug 27 2003

Fingerprint

Uvula
Purkinje Cells
Dendritic Spines
Chloralose
Urethane
Interneurons
Dendrites
Synapses
Action Potentials
Axons
Rabbits

Keywords

  • Cerebellum
  • Climbing fiber response
  • Golgi cell
  • Nodulus
  • Parallel fiber
  • Uvula
  • Vestibular primary afferents

ASJC Scopus subject areas

  • Neuroscience(all)

Cite this

Barmack, N. H., & Yakhnitsa, V. (2003). Cerebellar climbing fibers modulate simple spikes in Purkinje cells. Journal of Neuroscience, 23(21), 7904-7916.

Cerebellar climbing fibers modulate simple spikes in Purkinje cells. / Barmack, Neal H.; Yakhnitsa, Vadim.

In: Journal of Neuroscience, Vol. 23, No. 21, 27.08.2003, p. 7904-7916.

Research output: Contribution to journalArticle

Barmack, NH & Yakhnitsa, V 2003, 'Cerebellar climbing fibers modulate simple spikes in Purkinje cells', Journal of Neuroscience, vol. 23, no. 21, pp. 7904-7916.
Barmack, Neal H. ; Yakhnitsa, Vadim. / Cerebellar climbing fibers modulate simple spikes in Purkinje cells. In: Journal of Neuroscience. 2003 ; Vol. 23, No. 21. pp. 7904-7916.
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AB - Purkinje cells have two action potentials: Climbing fiber responses (CFRs) and simple spikes (SSs). CFRs reflect the discharge of a single climbing fiber at multiple synaptic sites on the proximal dendrite of the Purkinje cell. SSs reflect the summed action of a subset of parallel fiber synapses on Purkinje cell dendritic spines. Because mossy fiber afferents terminate on granule cells, the ascending axons of which bifurcate, giving rise to parallel fibers, the modulation of SSs has been attributed to mossy fiber afferent signals. This inference has never been tested. Conversely, the low discharge frequency of CFRs has led many to conclude that they have a unique and intermittent role in cerebellar signal processing. We examine the relative potency of vestibularly modulated mossy fiber and climbing fiber signals in evoking CFRs and SSs in Purkinje cells of the uvula-nodulus in chloralose- urethane-anesthetized rabbits. Vestibular primary afferents were blocked by unilateral labyrinthectomy (UL). A UL destroys the vestibular primary afferent signal to the ipsilateral uvula-nodulus, while leaving intact the vestibular climbing fiber signal from the contralateral inferior olive. After UL, vestibular stimulation modulated CFRs and SSs in ipsilateral uvula-nodular Purkinje cells, demonstrating that the primary vestibular afferent mossy fiber input to the ipsilateral uvula-nodulus was not necessary for SS modulation. Unilateral microlesions of the caudal half of the β-nucleus of the inferior olive reduced a modulated climbing fiber signal to the contralateral uvula-nodulus, causing loss of both vestibularly modulated CFRs and SSs in contralateral Purkinje cells. Vestibular climbing fibers not only evoke low-frequency CFRs, but also indirectly modulate higher-frequency SSs. This modulation must be attributed to cerebellar interneurons. Golgi cell inhibition of granule cells may provide the interneuronal mechanism for CFR-induced SS modulation.

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