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Research Articles, Cellular/Molecular

Graded Coexpression of Ion Channel, Neurofilament, and Synaptic Genes in Fast-Spiking Vestibular Nucleus Neurons

Takashi Kodama, Aryn H. Gittis, Minyoung Shin, Keith Kelleher, Kristine E. Kolkman, Lauren McElvain, Minh Lam and Sascha du Lac
Journal of Neuroscience 15 January 2020, 40 (3) 496-508; DOI: https://doi.org/10.1523/JNEUROSCI.1500-19.2019
Takashi Kodama
1Johns Hopkins University School of Medicine, Baltimore, Maryland 21205, 2Howard Hughes Medical Institute, La Jolla, California, 92037, 3Salk Institute for Biological Studies, La Jolla, California, 92037,
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Aryn H. Gittis
3Salk Institute for Biological Studies, La Jolla, California, 92037, 4Neurosciences Graduate Program, University of California San Diego, La Jolla, California 92037, 5Carnegie Mellon University, Pittsburgh, Pennsylvania 15213, and
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Minyoung Shin
2Howard Hughes Medical Institute, La Jolla, California, 92037,
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Keith Kelleher
2Howard Hughes Medical Institute, La Jolla, California, 92037, 3Salk Institute for Biological Studies, La Jolla, California, 92037,
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Kristine E. Kolkman
3Salk Institute for Biological Studies, La Jolla, California, 92037, 4Neurosciences Graduate Program, University of California San Diego, La Jolla, California 92037, 6Cornell University, Ithaca, NY 14853
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Lauren McElvain
3Salk Institute for Biological Studies, La Jolla, California, 92037, 4Neurosciences Graduate Program, University of California San Diego, La Jolla, California 92037,
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Minh Lam
1Johns Hopkins University School of Medicine, Baltimore, Maryland 21205,
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Sascha du Lac
1Johns Hopkins University School of Medicine, Baltimore, Maryland 21205, 2Howard Hughes Medical Institute, La Jolla, California, 92037, 3Salk Institute for Biological Studies, La Jolla, California, 92037,
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Abstract

Computations that require speed and temporal precision are implemented throughout the nervous system by neurons capable of firing at very high rates, rapidly encoding and transmitting a rich amount of information, but with substantial metabolic and physical costs. For economical fast spiking and high throughput information processing, neurons need to optimize multiple biophysical properties in parallel, but the mechanisms of this coordination remain unknown. We hypothesized that coordinated gene expression may underlie the coordinated tuning of the biophysical properties required for rapid firing and signal transmission. Taking advantage of the diversity of fast-spiking cell types in the medial vestibular nucleus of mice of both sexes, we examined the relationship between gene expression, ionic currents, and neuronal firing capacity. Across excitatory and inhibitory cell types, genes encoding voltage-gated ion channels responsible for depolarizing and repolarizing the action potential were tightly coexpressed, and their absolute expression levels increased with maximal firing rate. Remarkably, this coordinated gene expression extended to neurofilaments and specific presynaptic molecules, providing a mechanism for coregulating axon caliber and transmitter release to match firing capacity. These findings suggest the presence of a module of genes, which is coexpressed in a graded manner and jointly tunes multiple biophysical properties for economical differentiation of firing capacity. The graded tuning of fast-spiking capacity by the absolute expression levels of specific ion channels provides a counterexample to the widely held assumption that cell-type-specific firing patterns can be achieved via a vast combination of different ion channels.

SIGNIFICANCE STATEMENT Although essential roles of fast-spiking neurons in various neural circuits have been widely recognized, it remains unclear how neurons efficiently coordinate the multiple biophysical properties required to maintain high rates of action potential firing and transmitter release. Taking advantage of diverse fast-firing capacities among medial vestibular nucleus neurons of mice, we identify a group of ion channel, synaptic, and structural genes that exhibit mutually correlated expression levels, which covary with firing capacity. Coexpression of this fast-spiking gene module may be a basic strategy for neurons to efficiently and coordinately tune the speed of action potential generation and propagation and transmitter release at presynaptic terminals.

  • flocculus
  • high-frequency firing
  • ion channel genes
  • Kv3
  • pre-cerebellar
  • sodium channel
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The Journal of Neuroscience: 40 (3)
Journal of Neuroscience
Vol. 40, Issue 3
15 Jan 2020
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Graded Coexpression of Ion Channel, Neurofilament, and Synaptic Genes in Fast-Spiking Vestibular Nucleus Neurons
Takashi Kodama, Aryn H. Gittis, Minyoung Shin, Keith Kelleher, Kristine E. Kolkman, Lauren McElvain, Minh Lam, Sascha du Lac
Journal of Neuroscience 15 January 2020, 40 (3) 496-508; DOI: 10.1523/JNEUROSCI.1500-19.2019

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Graded Coexpression of Ion Channel, Neurofilament, and Synaptic Genes in Fast-Spiking Vestibular Nucleus Neurons
Takashi Kodama, Aryn H. Gittis, Minyoung Shin, Keith Kelleher, Kristine E. Kolkman, Lauren McElvain, Minh Lam, Sascha du Lac
Journal of Neuroscience 15 January 2020, 40 (3) 496-508; DOI: 10.1523/JNEUROSCI.1500-19.2019
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Keywords

  • flocculus
  • high-frequency firing
  • ion channel genes
  • Kv3
  • pre-cerebellar
  • sodium channel

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