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

Josef G. Trapani, Teresa Nicolson

Research output: Contribution to journalArticle

41 Scopus citations

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 CaV1.3 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 V1.3. We then tested the hypothesis that spontaneous spiking resulted from sustained CaV1.3 activity due to depolarizing currents that are active at rest. Mechanotransduction currents (IMET) provide a depolarizing influence to the resting potential. However, following block of IMET, 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 CaV1.3. To test whether the hyperpolarization-activated cation current, Ih participates in setting the resting potential, we applied Ih antagonists. Both ZD7288 and DK-AH 269 reduced spontaneous activity. Finally, concomitant block of IMET and Ih essentially abolished spontaneous activity, ostensibly by hyperpolarization outside of the activation range for Ca V1.3. Together, our data support a mechanism for spontaneous spiking that results from Ca2+-dependent neurotransmitter release at hair-cell resting potentials that are maintained within the activation range of CaV1.3 channels through active IMET and Ih.

Original languageEnglish (US)
Pages (from-to)1614-1623
Number of pages10
JournalJournal of Neuroscience
Volume31
Issue number5
DOIs
StatePublished - Feb 2 2011

ASJC Scopus subject areas

  • Neuroscience(all)

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