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Active Dendrites and Differential Distribution of Calcium Channels Enable Functional Compartmentalization of Golgi Cells.

Publication ,  Journal Article
Rudolph, S; Hull, C; Regehr, WG
Published in: J Neurosci
November 25, 2015

UNLABELLED: Interneurons are essential to controlling excitability, timing, and synaptic integration in neuronal networks. Golgi cells (GoCs) serve these roles at the input layer of the cerebellar cortex by releasing GABA to inhibit granule cells (grcs). GoCs are excited by mossy fibers (MFs) and grcs and provide feedforward and feedback inhibition to grcs. Here we investigate two important aspects of GoC physiology: the properties of GoC dendrites and the role of calcium signaling in regulating GoC spontaneous activity. Although GoC dendrites are extensive, previous studies concluded they are devoid of voltage-gated ion channels. Hence, the current view holds that somatic voltage signals decay passively within GoC dendrites, and grc synapses onto distal dendrites are not amplified and are therefore ineffective at firing GoCs because of strong passive attenuation. Using whole-cell recording and calcium imaging in rat slices, we find that dendritic voltage-gated sodium channels allow somatic action potentials to activate voltage-gated calcium channels (VGCCs) along the entire dendritic length, with R-type and T-type VGCCs preferentially located distally. We show that R- and T-type VGCCs located in the dendrites can boost distal synaptic inputs and promote burst firing. Active dendrites are thus critical to the regulation of GoC activity, and consequently, to the processing of input to the cerebellar cortex. In contrast, we find that N-type channels are preferentially located near the soma, and control the frequency and pattern of spontaneous firing through their close association with calcium-activated potassium (KCa) channels. Thus, VGCC types are differentially distributed and serve specialized functions within GoCs. SIGNIFICANCE STATEMENT: Interneurons are essential to neural processing because they modulate excitability, timing, and synaptic integration within circuits. At the input layer of the cerebellar cortex, a single type of interneuron, the Golgi cell (GoC), carries these functions. The extent of inhibition depends on both spontaneous activity of GoCs and the excitatory synaptic input they receive. In this study, we find that different types of calcium channels are differentially distributed, with dendritic calcium channels being activated by somatic activity, boosting synaptic inputs and enabling bursting, and somatic calcium cannels promoting regular firing. We therefore challenge the current view that GoC dendrites are passive and identify the mechanisms that contribute to GoCs regulating the flow of sensory information in the cerebellar cortex.

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Published In

J Neurosci

DOI

EISSN

1529-2401

Publication Date

November 25, 2015

Volume

35

Issue

47

Start / End Page

15492 / 15504

Location

United States

Related Subject Headings

  • Rats, Sprague-Dawley
  • Rats
  • Neurology & Neurosurgery
  • Male
  • Golgi Apparatus
  • Female
  • Excitatory Postsynaptic Potentials
  • Dendrites
  • Cerebellar Cortex
  • Calcium Channels
 

Citation

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Rudolph, S., Hull, C., & Regehr, W. G. (2015). Active Dendrites and Differential Distribution of Calcium Channels Enable Functional Compartmentalization of Golgi Cells. J Neurosci, 35(47), 15492–15504. https://doi.org/10.1523/JNEUROSCI.3132-15.2015
Rudolph, Stephanie, Court Hull, and Wade G. Regehr. “Active Dendrites and Differential Distribution of Calcium Channels Enable Functional Compartmentalization of Golgi Cells.J Neurosci 35, no. 47 (November 25, 2015): 15492–504. https://doi.org/10.1523/JNEUROSCI.3132-15.2015.
Rudolph, Stephanie, et al. “Active Dendrites and Differential Distribution of Calcium Channels Enable Functional Compartmentalization of Golgi Cells.J Neurosci, vol. 35, no. 47, Nov. 2015, pp. 15492–504. Pubmed, doi:10.1523/JNEUROSCI.3132-15.2015.

Published In

J Neurosci

DOI

EISSN

1529-2401

Publication Date

November 25, 2015

Volume

35

Issue

47

Start / End Page

15492 / 15504

Location

United States

Related Subject Headings

  • Rats, Sprague-Dawley
  • Rats
  • Neurology & Neurosurgery
  • Male
  • Golgi Apparatus
  • Female
  • Excitatory Postsynaptic Potentials
  • Dendrites
  • Cerebellar Cortex
  • Calcium Channels