How to Build a Fast and Highly Sensitive Sound Detector That Remains Robust to Temperature Shifts

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Abstract

Frogs must have sharp hearing abilities during the warm summer months to successfully find mating partners. This study aims to understand how frog hair cell ribbon-type synapses preserve both sensitivity and temporal precision during temperature changes. Under room (∼24°C) and high (∼32°C) temperature, we performed in vitro patch-clamp recordings of hair cells and their afferent fibers in amphibian papillae of either male or female bullfrogs. Afferent fibers exhibited a wide heterogeneity in membrane input resistance (Rin) from 100 mΩ to 1000 mΩ, which may contribute to variations in spike threshold and firing frequency. At higher temperatures, most fibers increased their frequency of spike firing due to an increase in spontaneous EPSC frequencies. Hair cell resting membrane potential (Vrest) remained surprisingly stable during temperature increases, because Ca2+ influx and K+ outflux increased simultaneously. This increase in Ca2+ current likely enhanced spontaneous EPSC frequencies. These larger "leak currents" at Vrest also lowered Rin and produced higher electrical resonant frequencies. Lowering Rin will reduce the hair cells receptor potential and presumably moderate the systems sensitivity. Using membrane capacitance measurements, we suggest that hair cells can partially compensate for this reduced sensitivity by increasing exocytosis efficiency and the size of the readily releasable pool of synaptic vesicles. Furthermore, paired recordings of hair cells and their afferent fibers showed that synaptic delays shortened and multivesicular release becomes more synchronous at higher temperatures, which should improve temporal precision. Together, our results explain many previous in vivo observations on the temperature dependence of spikes in auditory nerves.SIGNIFICANCE STATEMENT The vertebrate inner ear detects and transmits auditory information over a broad dynamic range of sound frequency and intensity. It achieves remarkable sensitivity to soft sounds and precise frequency selectivity. How does the ear of cold-blooded vertebrates maintain its performance level as temperature changes? More specifically, how does the hair cell to afferent fiber synapse in bullfrog amphibian papilla adjust to a wide range of physiological temperatures without losing its sensitivity and temporal fidelity to sound signals? This study uses in vitro experiments to reveal the biophysical mechanisms that explain many observations made from in vivo auditory nerve fiber recordings. We find that higher temperature facilitates vesicle exocytosis and electrical tuning to higher sound frequencies, which benefits sensitivity and selectivity.

Original languageEnglish (US)
Pages (from-to)7260-7276
Number of pages17
JournalThe Journal of neuroscience : the official journal of the Society for Neuroscience
Volume39
Issue number37
DOIs
StatePublished - Sep 11 2019

Fingerprint

Temperature
Rana catesbeiana
Cochlear Nerve
Exocytosis
Amphibians
Anura
Synapses
Vertebrates
Aptitude
Membranes
Synaptic Vesicles
Inner Ear
Nerve Fibers
Membrane Potentials
Hearing
Ear
Cell Membrane
Efficiency
In Vitro Techniques

Keywords

  • auditory nerve
  • Ca2+ current
  • EPSP
  • exocytosis
  • hair cell synapse
  • membrane resistance

ASJC Scopus subject areas

  • Neuroscience(all)

Cite this

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title = "How to Build a Fast and Highly Sensitive Sound Detector That Remains Robust to Temperature Shifts",
abstract = "Frogs must have sharp hearing abilities during the warm summer months to successfully find mating partners. This study aims to understand how frog hair cell ribbon-type synapses preserve both sensitivity and temporal precision during temperature changes. Under room (∼24°C) and high (∼32°C) temperature, we performed in vitro patch-clamp recordings of hair cells and their afferent fibers in amphibian papillae of either male or female bullfrogs. Afferent fibers exhibited a wide heterogeneity in membrane input resistance (Rin) from 100 mΩ to 1000 mΩ, which may contribute to variations in spike threshold and firing frequency. At higher temperatures, most fibers increased their frequency of spike firing due to an increase in spontaneous EPSC frequencies. Hair cell resting membrane potential (Vrest) remained surprisingly stable during temperature increases, because Ca2+ influx and K+ outflux increased simultaneously. This increase in Ca2+ current likely enhanced spontaneous EPSC frequencies. These larger {"}leak currents{"} at Vrest also lowered Rin and produced higher electrical resonant frequencies. Lowering Rin will reduce the hair cells receptor potential and presumably moderate the systems sensitivity. Using membrane capacitance measurements, we suggest that hair cells can partially compensate for this reduced sensitivity by increasing exocytosis efficiency and the size of the readily releasable pool of synaptic vesicles. Furthermore, paired recordings of hair cells and their afferent fibers showed that synaptic delays shortened and multivesicular release becomes more synchronous at higher temperatures, which should improve temporal precision. Together, our results explain many previous in vivo observations on the temperature dependence of spikes in auditory nerves.SIGNIFICANCE STATEMENT The vertebrate inner ear detects and transmits auditory information over a broad dynamic range of sound frequency and intensity. It achieves remarkable sensitivity to soft sounds and precise frequency selectivity. How does the ear of cold-blooded vertebrates maintain its performance level as temperature changes? More specifically, how does the hair cell to afferent fiber synapse in bullfrog amphibian papilla adjust to a wide range of physiological temperatures without losing its sensitivity and temporal fidelity to sound signals? This study uses in vitro experiments to reveal the biophysical mechanisms that explain many observations made from in vivo auditory nerve fiber recordings. We find that higher temperature facilitates vesicle exocytosis and electrical tuning to higher sound frequencies, which benefits sensitivity and selectivity.",
keywords = "auditory nerve, Ca2+ current, EPSP, exocytosis, hair cell synapse, membrane resistance",
author = "Minghui Chen and {Von Gersdorff}, Henrique",
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T1 - How to Build a Fast and Highly Sensitive Sound Detector That Remains Robust to Temperature Shifts

AU - Chen, Minghui

AU - Von Gersdorff, Henrique

PY - 2019/9/11

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N2 - Frogs must have sharp hearing abilities during the warm summer months to successfully find mating partners. This study aims to understand how frog hair cell ribbon-type synapses preserve both sensitivity and temporal precision during temperature changes. Under room (∼24°C) and high (∼32°C) temperature, we performed in vitro patch-clamp recordings of hair cells and their afferent fibers in amphibian papillae of either male or female bullfrogs. Afferent fibers exhibited a wide heterogeneity in membrane input resistance (Rin) from 100 mΩ to 1000 mΩ, which may contribute to variations in spike threshold and firing frequency. At higher temperatures, most fibers increased their frequency of spike firing due to an increase in spontaneous EPSC frequencies. Hair cell resting membrane potential (Vrest) remained surprisingly stable during temperature increases, because Ca2+ influx and K+ outflux increased simultaneously. This increase in Ca2+ current likely enhanced spontaneous EPSC frequencies. These larger "leak currents" at Vrest also lowered Rin and produced higher electrical resonant frequencies. Lowering Rin will reduce the hair cells receptor potential and presumably moderate the systems sensitivity. Using membrane capacitance measurements, we suggest that hair cells can partially compensate for this reduced sensitivity by increasing exocytosis efficiency and the size of the readily releasable pool of synaptic vesicles. Furthermore, paired recordings of hair cells and their afferent fibers showed that synaptic delays shortened and multivesicular release becomes more synchronous at higher temperatures, which should improve temporal precision. Together, our results explain many previous in vivo observations on the temperature dependence of spikes in auditory nerves.SIGNIFICANCE STATEMENT The vertebrate inner ear detects and transmits auditory information over a broad dynamic range of sound frequency and intensity. It achieves remarkable sensitivity to soft sounds and precise frequency selectivity. How does the ear of cold-blooded vertebrates maintain its performance level as temperature changes? More specifically, how does the hair cell to afferent fiber synapse in bullfrog amphibian papilla adjust to a wide range of physiological temperatures without losing its sensitivity and temporal fidelity to sound signals? This study uses in vitro experiments to reveal the biophysical mechanisms that explain many observations made from in vivo auditory nerve fiber recordings. We find that higher temperature facilitates vesicle exocytosis and electrical tuning to higher sound frequencies, which benefits sensitivity and selectivity.

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