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Research Articles, Cellular/Molecular

Muscarinic Acetylcholine Receptors Modulate HCN Channel Properties in Vestibular Ganglion Neurons

Daniel Bronson and Radha Kalluri
Journal of Neuroscience 8 February 2023, 43 (6) 902-917; DOI: https://doi.org/10.1523/JNEUROSCI.2552-21.2022
Daniel Bronson
1Hearing and Communications Neuroscience Training Program, University of Southern California, Los Angeles, California 90057
2Department of Otolaryngology-Head and Neck Surgery, Keck School of Medicine, University of Southern California, Los Angeles, California 90057
3Zilkha Neurogenetic Institute, Keck School of Medicine, University of Southern California, Los Angeles, California 90057
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Radha Kalluri
1Hearing and Communications Neuroscience Training Program, University of Southern California, Los Angeles, California 90057
2Department of Otolaryngology-Head and Neck Surgery, Keck School of Medicine, University of Southern California, Los Angeles, California 90057
3Zilkha Neurogenetic Institute, Keck School of Medicine, University of Southern California, Los Angeles, California 90057
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Abstract

Efferent modulation of vestibular afferent excitability is linked to muscarinic signaling cascades that close low-voltage-gated potassium channels (i.e., KCNQ). Here, we show that muscarinic signaling cascades also depolarize the activation range of hyperpolarization-activated cyclic-nucleotide gated (HCN) channels. We compared the voltage activation range and kinetics of HCN channels and induced firing patterns before and after administering the muscarinic acetylcholine receptor (mAChR) agonist oxotremorine-M (Oxo-M) in dissociated vestibular ganglion neurons (VGNs) from rats of either sex using perforated whole-cell patch-clamp methods. Oxo-M depolarized HCN channels' half-activation voltage (V1/2) and sped up the rate of activation near resting potential twofold. HCN channels in large-diameter and/or transient firing VGN (putative cell bodies of irregular firing neuron from central epithelial zones) had relatively depolarized V1/2 in control solution and were less sensitive to mAChR activation than those found in small-diameter VGN with sustained firing patterns (putatively belonging to regular firing afferents). The impact of mAChR on HCN channels is not a direct consequence of closing KCNQ channels since pretreating the cells with Linopirdine, a KCNQ channel blocker, did not prevent HCN channel depolarization by Oxo-M. Efferent signaling promoted ion channel configurations that were favorable to highly regular spiking in some VGN, but not others. This is consistent with previous observations that low-voltage gated potassium currents in VGN are conducted by mAChR agonist-sensitive and -insensitive channels. Connecting efferent signaling to HCN channels is significant because of the channel's impact on spike-timing regularity and nonchemical transmission between Type I hair cells and vestibular afferents.

SIGNIFICANCE STATEMENT Vestibular afferents express a diverse complement of ion channels. In vitro studies identified low-voltage activated potassium channels and hyperpolarization-activated cyclic-nucleotide gated (HCN) channels as crucial for shaping the timing and sensitivity of afferent responses. Moreover, a network of acetylcholine-releasing efferent neurons controls afferent excitability by closing a subgroup of low-voltage activated potassium channels on the afferent neuron. This work shows that these efferent signaling cascades also enhance the activation of HCN channels by depolarizing their voltage activation range. The size of this effect varies depending on the endogenous properties of the HCN channel and on cell type (as determined by discharge patterns and cell size). Simultaneously controlling two ion-channel groups gives the vestibular efferent system exquisite control over afferent neuron activity.

  • efferent neurons
  • HCN channels
  • KCNQ channels
  • modulation
  • muscarinic acetylcholine receptors
  • vestibular ganglion

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The Journal of Neuroscience: 43 (6)
Journal of Neuroscience
Vol. 43, Issue 6
8 Feb 2023
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Muscarinic Acetylcholine Receptors Modulate HCN Channel Properties in Vestibular Ganglion Neurons
Daniel Bronson, Radha Kalluri
Journal of Neuroscience 8 February 2023, 43 (6) 902-917; DOI: 10.1523/JNEUROSCI.2552-21.2022

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Muscarinic Acetylcholine Receptors Modulate HCN Channel Properties in Vestibular Ganglion Neurons
Daniel Bronson, Radha Kalluri
Journal of Neuroscience 8 February 2023, 43 (6) 902-917; DOI: 10.1523/JNEUROSCI.2552-21.2022
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Keywords

  • efferent neurons
  • HCN channels
  • KCNQ channels
  • modulation
  • muscarinic acetylcholine receptors
  • vestibular ganglion

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