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Evidence for the utricular origin of the vestibular short-latency-evoked potential (VsEP) to bone-conducted vibration in guinea pig

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Abstract

Previous studies have shown that the vestibular short-latency-evoked potential (VsEP) in response to the brief head acceleration stimulus is a compound action potential of neurons innervating the otolith organs. However, due to the lack of direct evidence, it is currently unclear whether the VsEP is primarily generated by the activity of utricular or saccular afferent neurons, or some mixture of the two. Here, we investigated the origin of the VsEP evoked by brief bone-conducted vibration pulses in guinea pigs, using selective destruction of the cochlea, semicircular canals (SCCs), saccule, or utricle, along with neural blockade with tetrodotoxin (TTX) application, and mechanical displacements of the surgically exposed utricular macula. To access each end organ, either a dorsal or a ventral surgical approach was used. TTX application abolished the VsEP, supporting the neurogenic origin of the response. Selective cochlear, SCCs, or saccular destruction had no significant effect on VsEP amplitude, whereas utricular destruction abolished the VsEP completely. Displacement of the utricular membrane changed the VsEP amplitude in a non-monotonic fashion. These results suggest that the VsEP evoked by BCV in guinea pigs represents almost entirely a utricular response. Furthermore, it suggests that displacements of the utricular macula may alter its response to bone-conduction stimuli.

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Abbreviations

VsEP:

Vestibular short-latency-evoked response

RW:

Round window

SCC:

Semicircular canal

CAP:

Compound action potential

MD:

Ménière’s disease

BCV:

Bone-conducted vibration

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Acknowledgments

This study was supported through funds raised by the Ménière’s Research Fund Inc.—a charity organization, with funds maintained by The University of Sydney Medical Foundation. We would also like to acknowledge Em. Prof. Ian Curthoys’ support and advice throughout this study, in particular with issues relating to evoking and monitoring bone-conduction vibration stimulation in guinea pigs.

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Authors and Affiliations

  1. The Brain and Mind Research Institute, Sydney Medical School, The University of Sydney, 100 Mallett Street, Camperdown, NSW, 2050, Australia

    Yasuhiro Chihara, Vivian Wang & Daniel J. Brown

  2. National Institute of Sensory Organs, National Tokyo Medical Center, Tokyo, Japan

    Yasuhiro Chihara

  3. Raffles Japanese Clinic, Raffles Hospital, Singapore, Singapore

    Yasuhiro Chihara

Authors
  1. Yasuhiro Chihara
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  2. Vivian Wang
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  3. Daniel J. Brown
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Corresponding author

Correspondence to Daniel J. Brown.

Additional information

Y. Chihara and D. J. Brown contributed equally to this work.

Electronic supplementary material

Below is the link to the electronic supplementary material.

221_2013_3602_MOESM1_ESM.pdf

Figure S1: Example of a guinea pig skull bone. A. Surgical view of the dorsolateral approach for accessing the cochlea where the tympanic bulla has been opened just caudal to the ear canal. A recording wire has been inserted into the stylomastoid foramen leading to facial canal. B. Surgical view of dorsolateral approach exposing the semicircular canals. A small hole was made just rostral to the dorsolateral hole. C. Surgical view of the ventral approach for accessing whole cochlea and vestibule. (PDF 80 kb)

221_2013_3602_MOESM2_ESM.pdf

Figure S2: Schematic representation of the technique for correcting the skull vibration. A. An initial 1 ms test impulse BCV stimulus was delivered to the B71. The acceleration of the animal’s skull was then measured in response to this impulse stimulus. By comparing the difference between the FFT of the BCV impulse and the FFT of the measured skull acceleration, we could derive a calibration curve in the frequency and time domain that could be used to correct the BCV impulse. This calibration curve could then be used to create a corrected BCV impulse-like stimulus which generated an impulse acceleration of the animal’s skull. FFT: Fast Fourier Transform, IFFT: Inverse FFT, LPF: Low-pass filter. B. Example waveforms of skull acceleration and jerk before and after the correction technique. We could get an impulse-like stimulus by using B71 bone vibrator. (PDF 275 kb)

Supplemental video 1: Cochlear destruction via a ventral approach. This procedure did not alter the VsEP waveform. (MPG 4902 kb)

Supplemental video 2: Saccular destruction via a ventral approach (after removing the cochlear and exposing the vestibule). This procedure did not alter the VsEP waveform. (MPG 3480 kb)

Supplemental video 3: Utricular destruction via a ventral approach (after destroying the cochlear and saccule). Destroying the posterior part of the utricle decreased the VsEP to the half its initial amplitude. Subsequent destruction of the anterior part of the utricle abolished VsEP completely. (MPG 6976 kb)

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Chihara, Y., Wang, V. & Brown, D.J. Evidence for the utricular origin of the vestibular short-latency-evoked potential (VsEP) to bone-conducted vibration in guinea pig. Exp Brain Res 229, 157–170 (2013). https://doi.org/10.1007/s00221-013-3602-5

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