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Cited by 160Hearing, Cochlea, Tinnitus, GeneticsHearing Loss and RehabilitationVestibular and auditory disorders

The postsynaptic function of type II cochlear afferents

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Weisz, Catherine, Glowatzki, Elisabeth, Fuchs, Paul·2009·Nature
DOI 10.1038/nature08487PMC PMC2785502
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Abstract

The mammalian cochlea is innervated by two classes of sensory neurons. Type I neurons make up 90-95% of the cochlear nerve and contact single inner hair cells to provide acoustic analysis as we know it. In contrast, the far less numerous type II neurons arborize extensively among outer hair cells (OHCs) and supporting cells. Their scarcity and smaller calibre axons have made them the subject of much speculation, but little experimental progress for the past 50 years. Here we record from type II fibres near their terminal arbors under OHCs to show that they receive excitatory glutamatergic synaptic input. The type II peripheral arbor conducts action potentials, but the small and infrequent glutamatergic excitation indicates a requirement for strong acoustic stimulation. Furthermore, we show that type II neurons are excited by ATP. Exogenous ATP depolarized type II neurons, both directly and by evoking glutamatergic synaptic input. These results prove that type II neurons function as cochlear afferents, and can be modulated by ATP. The lesser magnitude of synaptic drive dictates a fundamentally different role in auditory signalling from that of type I afferents.

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  • Type II afferents are strongly depolarized by direct application of ATP.

    “But in addition, type II afferents are strongly depolarized by direct application of ATP (4), a known algogenic mediator in skin (35).”

    From Damage-evoked signals in cochlear neurons and supporting cells (2024) · cites this paper as [4]

    The results passage (section labeled Abstract) reports that applied ATP directly depolarized young (P5–9) Type II fibers by 31.3 ± 10.1 mV. The same section says the effect was significantly smaller at P12–13 and smaller or absent in some P17–19 recordings, so the unqualified claim of strong depolarization overstates the age-dependent result. (LLM, conf=0.84)

    Experimental — accuracy not yet measured

  • Intracellular tight-seal recordings from type II afferents in cochlear explants revealed that glutamatergic transmission from one OHC was orders of magnitude weaker than that provided by each IHC to type I afferent ribbon synapse.

    “Intracellular tight-seal recordings from type II afferents in cochlear explants revealed that glutamatergic transmission from one OHC was orders of magnitude weaker than that provided by each IHC to type I afferent ribbon synapse (4, 33, 34).”

    From Damage-evoked signals in cochlear neurons and supporting cells (2024) · cites this paper as [4]

    The Methods Summary describes gigaohm-seal recordings from type II fibers in dissected rat cochleas. The paper reports smaller, much less frequent glutamatergic EPSCs than at type I afferent boutons and contrasts input from more than a dozen OHCs with release from a single IHC ribbon synapse (Abstract section; page unavailable). It does not quantify the difference as orders of magnitude or directly measure transmission from one OHC. (LLM, conf=0.84)

    Experimental — accuracy not yet measured

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Authors
Weisz, C., Glowatzki, E., & Fuchs, P.
Affiliations
Johns Hopkins University (US)
Corresponding author
Fuchs, Paul
ORCID
Venue
Nature
Publisher
Springer Science and Business Media LLC
Published
2009-10
Volume
461
Issue
7267
Pages
1126-1129
ISSN
  • 0028-0836 (ISSN-L)
  • 1476-4687
DOI
10.1038/nature08487
PMC
PMC2785502
OpenAlex
W2035657815
Cited by
160
References
33
Citations by year
2026: 7 · 2025: 5 · 2024: 7 · 2023: 1 · 2022: 10 · 2021: 12 · 2020: 16 · 2019: 5 · 2018: 14 · 2017: 4 · 2016: 7 · 2015: 22 · 2014: 8 · 2013: 12 · 2012: 10
FWCI
4.87
Type
journal article
Language
en
Open access
Licence
www.springer.com/tdm (tdm)
Locations
  • Nature (publishedVersion)
  • PubMed (publishedVersion)
  • PubMed Central (acceptedVersion)
  • RePEc: Research Papers in Economics (submittedVersion)
Funders
  • Johns Hopkins University
  • National Institute on Deafness and Other Communication Disorders (R01DC006476, P30DC005211, R01DC000276, T32DC000023)
Topics
  • Life Sciences › Neuroscience › Sensory Systems › Hearing, Cochlea, Tinnitus, Genetics
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Hearing Loss and Rehabilitation
  • Life Sciences › Neuroscience › Neurology › Vestibular and auditory disorders
Keywords
hyperacusis, acoustic trauma, ATP, outer hair cells, glutamatergic synaptic input, auditory nerve, postsynaptic function, rat cochlea
MeSH terms
Acoustic Stimulation, Adenosine Triphosphate, Afferent Pathways, Animals, Auditory Perception, Cochlea, Sensory Receptor Cells, Synapses, Rats, Sprague-Dawley, Hair Cells, Auditory, Outer, Glutamic Acid, Excitatory Postsynaptic Potentials, Rats, Neuronal Tract-Tracers

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