PUBLICATION

Mechanism of spontaneous activity in afferent neurons of the zebrafish lateral-line organ

Authors
Trapani, J.G., and Nicolson, T.
ID
ZDB-PUB-110207-27
Date
2011
Source
The Journal of neuroscience : the official journal of the Society for Neuroscience   31(5): 1614-1623 (Journal)
Registered Authors
Nicolson, Teresa, Trapani, Josef
Keywords
none
MeSH Terms
  • Action Potentials/physiology
  • Animals
  • Benzazepines/pharmacology
  • Calcium Channels, L-Type/physiology*
  • Cyclic Nucleotide-Gated Cation Channels/physiology*
  • Electric Stimulation/methods
  • Electrophysiology
  • Hair Cells, Auditory/physiology
  • Hyperpolarization-Activated Cyclic Nucleotide-Gated Channels
  • Lateral Line System/drug effects
  • Lateral Line System/physiology*
  • Mechanotransduction, Cellular/drug effects
  • Mechanotransduction, Cellular/physiology*
  • Membrane Potentials/drug effects
  • Membrane Potentials/physiology*
  • Neurons, Afferent/drug effects
  • Neurons, Afferent/physiology*
  • Physical Stimulation/methods
  • Potassium Channels/physiology*
  • Pyrimidines/pharmacology
  • Reverse Transcriptase Polymerase Chain Reaction
  • Vesicular Glutamate Transport Proteins/deficiency
  • Vesicular Glutamate Transport Proteins/genetics
  • Zebrafish
PubMed
21289170 Full text @ J. Neurosci.
Abstract
Many auditory, vestibular, and lateral-line afferent neurons display spontaneous action potentials. This spontaneous spiking is thought to result from hair-cell glutamate release in the absence of stimuli. Spontaneous release at hair-cell resting potentials presumably results from Ca(V)1.3 L-type calcium channel activity. Here, using intact zebrafish larvae, we recorded robust spontaneous spiking from lateral-line afferent neurons in the absence of external stimuli. Consistent with the above assumptions, spiking was absent in mutants that lacked either Vesicular glutamate transporter 3 (Vglut3) or Ca(V)1.3. We then tested the hypothesis that spontaneous spiking resulted from sustained Ca(V)1.3 activity due to depolarizing currents that are active at rest. Mechanotransduction currents (I(MET)) provide a depolarizing influence to the resting potential. However, following block of I(MET), spontaneous spiking persisted and was characterized by longer interspike intervals and increased periods of inactivity. These results suggest that an additional depolarizing influence maintains the resting potential within the activation range of Ca(V)1.3. To test whether the hyperpolarization-activated cation current, I(h) participates in setting the resting potential, we applied I(h) antagonists. Both ZD7288 and DK-AH 269 reduced spontaneous activity. Finally, concomitant block of I(MET) and I(h) essentially abolished spontaneous activity, ostensibly by hyperpolarization outside of the activation range for Ca(V)1.3. Together, our data support a mechanism for spontaneous spiking that results from Ca(2+)-dependent neurotransmitter release at hair-cell resting potentials that are maintained within the activation range of Ca(V)1.3 channels through active I(MET) and I(h).
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