A non-canonical pathway from cochlea to brain signals tissue-damaging noise

Emma N. Flores, Anne Duggan, Thomas Madathany, Ann K. Hogan, Freddie G. Márquez, Gagan Kumar, Rebecca P. Seal, Robert H. Edwards, M. Charles Liberman, Jaime Garcia-Anoveros*

*Corresponding author for this work

Research output: Contribution to journalArticle

44 Citations (Scopus)

Abstract

Intense noise damages the cochlear organ of Corti, particularly the outer hair cells (OHCs) [1]; however, this epithelium is not innervated by nociceptors of somatosensory ganglia, which detect damage elsewhere in the body. The only sensory neurons innervating the organ of Corti originate from the spiral ganglion, roughly 95% of which innervate exclusively inner hair cells (IHCs) [2-4]. Upon sound stimulation, IHCs release glutamate to activate AMPA-type receptors on these myelinated type-I neurons, which carry the neuronal signals to the cochlear nucleus. The remaining spiral ganglion cells (type IIs) are unmyelinated and contact OHCs [2-4]. Their function is unknown. Using immunoreactivity to cFos, we documented neuronal activation in the brainstem of Vglut3-/- mice, in which the canonical auditory pathway (activation of type-I afferents by glutamate released from inner hair cells) is silenced [5, 6]. In these deaf mice, we found responses to noxious noise, which damages hair cells, but not to innocuous noise, in neurons of the cochlear nucleus, but not in the vestibular or trigeminal nuclei. This response originates in the cochlea and not in other areas also stimulated by intense noise (middle ear and vestibule) as it was absent in CD1 mice with selective cochlear degeneration but normal vestibular and somatosensory function. These data imply the existence of an alternative neuronal pathway from cochlea to brainstem that is activated by tissue-damaging noise and does not require glutamate release from IHCs. This detection of noise-induced tissue damage, possibly by type-II cochlear afferents, represents a novel form of sensation that we term auditory nociception.

Original languageEnglish (US)
Pages (from-to)606-612
Number of pages7
JournalCurrent Biology
Volume25
Issue number5
DOIs
StatePublished - Mar 2 2015

Fingerprint

Inner Auditory Hair Cells
Cochlea
Noise
Brain
hairs
Cells
Tissue
Neurons
brain
Outer Auditory Hair Cells
Glutamic Acid
Spiral Ganglion
Cochlear Nucleus
Organ of Corti
Chemical activation
glutamates
cells
Brain Stem
AMPA Receptors
brain stem

ASJC Scopus subject areas

  • Biochemistry, Genetics and Molecular Biology(all)
  • Agricultural and Biological Sciences(all)

Cite this

Flores, Emma N. ; Duggan, Anne ; Madathany, Thomas ; Hogan, Ann K. ; Márquez, Freddie G. ; Kumar, Gagan ; Seal, Rebecca P. ; Edwards, Robert H. ; Liberman, M. Charles ; Garcia-Anoveros, Jaime. / A non-canonical pathway from cochlea to brain signals tissue-damaging noise. In: Current Biology. 2015 ; Vol. 25, No. 5. pp. 606-612.
@article{1d19975615114ecebc835832ad732828,
title = "A non-canonical pathway from cochlea to brain signals tissue-damaging noise",
abstract = "Intense noise damages the cochlear organ of Corti, particularly the outer hair cells (OHCs) [1]; however, this epithelium is not innervated by nociceptors of somatosensory ganglia, which detect damage elsewhere in the body. The only sensory neurons innervating the organ of Corti originate from the spiral ganglion, roughly 95{\%} of which innervate exclusively inner hair cells (IHCs) [2-4]. Upon sound stimulation, IHCs release glutamate to activate AMPA-type receptors on these myelinated type-I neurons, which carry the neuronal signals to the cochlear nucleus. The remaining spiral ganglion cells (type IIs) are unmyelinated and contact OHCs [2-4]. Their function is unknown. Using immunoreactivity to cFos, we documented neuronal activation in the brainstem of Vglut3-/- mice, in which the canonical auditory pathway (activation of type-I afferents by glutamate released from inner hair cells) is silenced [5, 6]. In these deaf mice, we found responses to noxious noise, which damages hair cells, but not to innocuous noise, in neurons of the cochlear nucleus, but not in the vestibular or trigeminal nuclei. This response originates in the cochlea and not in other areas also stimulated by intense noise (middle ear and vestibule) as it was absent in CD1 mice with selective cochlear degeneration but normal vestibular and somatosensory function. These data imply the existence of an alternative neuronal pathway from cochlea to brainstem that is activated by tissue-damaging noise and does not require glutamate release from IHCs. This detection of noise-induced tissue damage, possibly by type-II cochlear afferents, represents a novel form of sensation that we term auditory nociception.",
author = "Flores, {Emma N.} and Anne Duggan and Thomas Madathany and Hogan, {Ann K.} and M{\'a}rquez, {Freddie G.} and Gagan Kumar and Seal, {Rebecca P.} and Edwards, {Robert H.} and Liberman, {M. Charles} and Jaime Garcia-Anoveros",
year = "2015",
month = "3",
day = "2",
doi = "10.1016/j.cub.2015.01.009",
language = "English (US)",
volume = "25",
pages = "606--612",
journal = "Current Biology",
issn = "0960-9822",
publisher = "Cell Press",
number = "5",

}

Flores, EN, Duggan, A, Madathany, T, Hogan, AK, Márquez, FG, Kumar, G, Seal, RP, Edwards, RH, Liberman, MC & Garcia-Anoveros, J 2015, 'A non-canonical pathway from cochlea to brain signals tissue-damaging noise', Current Biology, vol. 25, no. 5, pp. 606-612. https://doi.org/10.1016/j.cub.2015.01.009

A non-canonical pathway from cochlea to brain signals tissue-damaging noise. / Flores, Emma N.; Duggan, Anne; Madathany, Thomas; Hogan, Ann K.; Márquez, Freddie G.; Kumar, Gagan; Seal, Rebecca P.; Edwards, Robert H.; Liberman, M. Charles; Garcia-Anoveros, Jaime.

In: Current Biology, Vol. 25, No. 5, 02.03.2015, p. 606-612.

Research output: Contribution to journalArticle

TY - JOUR

T1 - A non-canonical pathway from cochlea to brain signals tissue-damaging noise

AU - Flores, Emma N.

AU - Duggan, Anne

AU - Madathany, Thomas

AU - Hogan, Ann K.

AU - Márquez, Freddie G.

AU - Kumar, Gagan

AU - Seal, Rebecca P.

AU - Edwards, Robert H.

AU - Liberman, M. Charles

AU - Garcia-Anoveros, Jaime

PY - 2015/3/2

Y1 - 2015/3/2

N2 - Intense noise damages the cochlear organ of Corti, particularly the outer hair cells (OHCs) [1]; however, this epithelium is not innervated by nociceptors of somatosensory ganglia, which detect damage elsewhere in the body. The only sensory neurons innervating the organ of Corti originate from the spiral ganglion, roughly 95% of which innervate exclusively inner hair cells (IHCs) [2-4]. Upon sound stimulation, IHCs release glutamate to activate AMPA-type receptors on these myelinated type-I neurons, which carry the neuronal signals to the cochlear nucleus. The remaining spiral ganglion cells (type IIs) are unmyelinated and contact OHCs [2-4]. Their function is unknown. Using immunoreactivity to cFos, we documented neuronal activation in the brainstem of Vglut3-/- mice, in which the canonical auditory pathway (activation of type-I afferents by glutamate released from inner hair cells) is silenced [5, 6]. In these deaf mice, we found responses to noxious noise, which damages hair cells, but not to innocuous noise, in neurons of the cochlear nucleus, but not in the vestibular or trigeminal nuclei. This response originates in the cochlea and not in other areas also stimulated by intense noise (middle ear and vestibule) as it was absent in CD1 mice with selective cochlear degeneration but normal vestibular and somatosensory function. These data imply the existence of an alternative neuronal pathway from cochlea to brainstem that is activated by tissue-damaging noise and does not require glutamate release from IHCs. This detection of noise-induced tissue damage, possibly by type-II cochlear afferents, represents a novel form of sensation that we term auditory nociception.

AB - Intense noise damages the cochlear organ of Corti, particularly the outer hair cells (OHCs) [1]; however, this epithelium is not innervated by nociceptors of somatosensory ganglia, which detect damage elsewhere in the body. The only sensory neurons innervating the organ of Corti originate from the spiral ganglion, roughly 95% of which innervate exclusively inner hair cells (IHCs) [2-4]. Upon sound stimulation, IHCs release glutamate to activate AMPA-type receptors on these myelinated type-I neurons, which carry the neuronal signals to the cochlear nucleus. The remaining spiral ganglion cells (type IIs) are unmyelinated and contact OHCs [2-4]. Their function is unknown. Using immunoreactivity to cFos, we documented neuronal activation in the brainstem of Vglut3-/- mice, in which the canonical auditory pathway (activation of type-I afferents by glutamate released from inner hair cells) is silenced [5, 6]. In these deaf mice, we found responses to noxious noise, which damages hair cells, but not to innocuous noise, in neurons of the cochlear nucleus, but not in the vestibular or trigeminal nuclei. This response originates in the cochlea and not in other areas also stimulated by intense noise (middle ear and vestibule) as it was absent in CD1 mice with selective cochlear degeneration but normal vestibular and somatosensory function. These data imply the existence of an alternative neuronal pathway from cochlea to brainstem that is activated by tissue-damaging noise and does not require glutamate release from IHCs. This detection of noise-induced tissue damage, possibly by type-II cochlear afferents, represents a novel form of sensation that we term auditory nociception.

UR - http://www.scopus.com/inward/record.url?scp=84923632653&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=84923632653&partnerID=8YFLogxK

U2 - 10.1016/j.cub.2015.01.009

DO - 10.1016/j.cub.2015.01.009

M3 - Article

VL - 25

SP - 606

EP - 612

JO - Current Biology

JF - Current Biology

SN - 0960-9822

IS - 5

ER -