Enlargement of ribbons in zebrafish hair cells increases calcium currents but disrupts afferent spontaneous activity and timing of stimulus onset

Lavinia Sheets, Xinyi J. He, Jennifer Olt, Mary Schreck, Ronald S. Petralia, Ya Xian Wang, Qiuxiang Zhang, Alisha Beirl, Teresa Nicolson, Walter Marcotti, Josef G. Trapani, Katie S. Kindt

Research output: Contribution to journalArticle

12 Citations (Scopus)

Abstract

In sensory hair cells of auditory and vestibular organs, the ribbon synapse is required for the precise encoding of a wide range of complex stimuli. Hair cells have a unique presynaptic structure, the synaptic ribbon, which organizes both synaptic vesicles and calcium channels at the active zone. Previous work has shown that hair-cell ribbon size is correlated with differences in postsynaptic activity. However, additional variability in postsynapse size presents a challenge to determining the specific role of ribbon size in sensory encoding. To selectively assess the impact of ribbon size on synapse function, we examined hair cells in transgenic zebrafish that have enlarged ribbons, without postsynaptic alterations. Morphologically, we found that enlarged ribbons had more associated vesicles and reduced presynaptic calcium-channel clustering. Functionally, hair cells with enlarged ribbons had larger global and ribbon-localized calcium currents. Afferent neuron recordings revealed that hair cells with enlarged ribbons resulted in reduced spontaneous spike rates. Additionally, despite larger presynaptic calcium signals, we observed fewer evoked spikes with longer latencies from stimulus onset. Together, our work indicates that hair-cell ribbon size influences the spontaneous spiking and the precise encoding of stimulus onset in afferent neurons.

Original languageEnglish (US)
Pages (from-to)6299-6313
Number of pages15
JournalJournal of Neuroscience
Volume37
Issue number26
DOIs
StatePublished - 2017

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Zebrafish
Calcium
Afferent Neurons
Calcium Channels
Cell Size
Synapses
Auditory Hair Cells
Vestibular Hair Cells
Synaptic Vesicles
Cluster Analysis

Keywords

  • Calcium channels
  • Hair cell
  • Ribbon synapse
  • Sensory
  • Synapse
  • Zebrafish

ASJC Scopus subject areas

  • Neuroscience(all)

Cite this

Enlargement of ribbons in zebrafish hair cells increases calcium currents but disrupts afferent spontaneous activity and timing of stimulus onset. / Sheets, Lavinia; He, Xinyi J.; Olt, Jennifer; Schreck, Mary; Petralia, Ronald S.; Wang, Ya Xian; Zhang, Qiuxiang; Beirl, Alisha; Nicolson, Teresa; Marcotti, Walter; Trapani, Josef G.; Kindt, Katie S.

In: Journal of Neuroscience, Vol. 37, No. 26, 2017, p. 6299-6313.

Research output: Contribution to journalArticle

Sheets, L, He, XJ, Olt, J, Schreck, M, Petralia, RS, Wang, YX, Zhang, Q, Beirl, A, Nicolson, T, Marcotti, W, Trapani, JG & Kindt, KS 2017, 'Enlargement of ribbons in zebrafish hair cells increases calcium currents but disrupts afferent spontaneous activity and timing of stimulus onset', Journal of Neuroscience, vol. 37, no. 26, pp. 6299-6313. https://doi.org/10.1523/JNEUROSCI.2878-16.2017
Sheets, Lavinia ; He, Xinyi J. ; Olt, Jennifer ; Schreck, Mary ; Petralia, Ronald S. ; Wang, Ya Xian ; Zhang, Qiuxiang ; Beirl, Alisha ; Nicolson, Teresa ; Marcotti, Walter ; Trapani, Josef G. ; Kindt, Katie S. / Enlargement of ribbons in zebrafish hair cells increases calcium currents but disrupts afferent spontaneous activity and timing of stimulus onset. In: Journal of Neuroscience. 2017 ; Vol. 37, No. 26. pp. 6299-6313.
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AU - Sheets, Lavinia

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AU - Schreck, Mary

AU - Petralia, Ronald S.

AU - Wang, Ya Xian

AU - Zhang, Qiuxiang

AU - Beirl, Alisha

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AU - Marcotti, Walter

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AU - Kindt, Katie S.

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