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Brief Communications

Gating of Acoustic Transducer Channels Is Shaped by Biomechanical Filter Processes

Jennifer Hummel, Stefan Schöneich, Manfred Kössl, Jan Scherberich, Berthold Hedwig, Simone Prinz and Manuela Nowotny
Journal of Neuroscience 24 February 2016, 36 (8) 2377-2382; DOI: https://doi.org/10.1523/JNEUROSCI.3948-15.2016
Jennifer Hummel
1Institute of Cell Biology and Neuroscience, Goethe University, 60438 Frankfurt am Main, Germany,
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Stefan Schöneich
2Department of Zoology, University of Cambridge, CB2 3EJ Cambridge, United Kingdom, and
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Manfred Kössl
1Institute of Cell Biology and Neuroscience, Goethe University, 60438 Frankfurt am Main, Germany,
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Jan Scherberich
1Institute of Cell Biology and Neuroscience, Goethe University, 60438 Frankfurt am Main, Germany,
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Berthold Hedwig
2Department of Zoology, University of Cambridge, CB2 3EJ Cambridge, United Kingdom, and
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Simone Prinz
3Max-Planck-Institute for Biophysics, 60438 Frankfurt am Main, Germany
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Manuela Nowotny
1Institute of Cell Biology and Neuroscience, Goethe University, 60438 Frankfurt am Main, Germany,
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Abstract

Mechanoelectrical transduction of acoustic signals is the fundamental process for hearing in all ears across the animal kingdom. Here, we performed in vivo laser-vibrometric and electrophysiological measurements at the transduction site in an insect ear (Mecopoda elongata) to relate the biomechanical tonotopy along the hearing organ to the frequency tuning of the corresponding sensory cells. Our mechanical and electrophysiological map revealed a biomechanical filter process that considerably sharpens the neuronal response. We demonstrate that the channel gating, which acts on chordotonal stretch receptor neurons, is based on a mechanical directionality of the sound-induced motion. Further, anatomical studies of the transduction site support our finding of a stimulus-relevant tilt. In conclusion, we were able to show, in an insect ear, that directionality of channel gating considerably sharpens the neuronal frequency selectivity at the peripheral level and have identified a mechanism that enhances frequency discrimination in tonotopically organized ears.

SIGNIFICANCE STATEMENT The evolutionarily conserved ability of sensory cells to sense sound-induced mechanical forces is a fundamental process that still need investigating. In ears, the transduction process of acoustic signals from sound to frequency-specific neuronal responses of sensory cells is based on the opening of mechanosensitive ion channels. Here, we investigated mechanotransduction in the katydid's hearing organ with in vivo measurements of the sound-induced mechanical stimulus and of the electrical responses of the sensory cell at the transduction site. By combining anatomical, biophysical, and neurophysiological data, we present for the first time evidence of a crucial frequency-filter mechanism integral to the channel gating process. This filter takes effect at the first step of the signal transduction chain and shapes behavior-relevant hearing information.

  • acoustic signal transduction
  • frequency tuning
  • insects
  • transduction channel
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The Journal of Neuroscience: 36 (8)
Journal of Neuroscience
Vol. 36, Issue 8
24 Feb 2016
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Gating of Acoustic Transducer Channels Is Shaped by Biomechanical Filter Processes
Jennifer Hummel, Stefan Schöneich, Manfred Kössl, Jan Scherberich, Berthold Hedwig, Simone Prinz, Manuela Nowotny
Journal of Neuroscience 24 February 2016, 36 (8) 2377-2382; DOI: 10.1523/JNEUROSCI.3948-15.2016

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Gating of Acoustic Transducer Channels Is Shaped by Biomechanical Filter Processes
Jennifer Hummel, Stefan Schöneich, Manfred Kössl, Jan Scherberich, Berthold Hedwig, Simone Prinz, Manuela Nowotny
Journal of Neuroscience 24 February 2016, 36 (8) 2377-2382; DOI: 10.1523/JNEUROSCI.3948-15.2016
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Keywords

  • acoustic signal transduction
  • frequency tuning
  • insects
  • transduction channel

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