Contribution of auditory nerve fibers to compound action potential of the auditory nerve.
Sound-evoked compound action potential (CAP), which captures the synchronous activation of the auditory nerve fibers (ANFs), is commonly used to probe deafness in experimental and clinical settings. All ANFs are believed to contribute to CAP threshold and amplitude: low sound pressure levels activate the high-spontaneous rate (SR) fibers, and increasing levels gradually recruit medium- and then low-SR fibers. In this study, we quantitatively analyze the contribution of the ANFs to CAP 6 days after 30-min infusion of ouabain into the round window niche. Anatomic examination showed a progressive ablation of ANFs following increasing concentration of ouabain. CAP amplitude and threshold plotted against loss of ANFs revealed three ANF pools: 1) a highly ouabain-sensitive pool, which does not participate in either CAP threshold or amplitude, 2) a less sensitive pool, which only encoded CAP amplitude, and 3) a ouabain-resistant pool, required for CAP threshold and amplitude. Remarkably, distribution of the three pools was similar to the SR-based ANF distribution (low-, medium-, and high-SR fibers), suggesting that the low-SR fiber loss leaves the CAP unaffected. Single-unit recordings from the auditory nerve confirmed this hypothesis and further showed that it is due to the delayed and broad first spike latency distribution of low-SR fibers. In addition to unraveling the neural mechanisms that encode CAP, our computational simulation of an assembly of guinea pig ANFs generalizes and extends our experimental findings to different species of mammals. Altogether, our data demonstrate that substantial ANF loss can coexist with normal hearing threshold and even unchanged CAP amplitude.
Institut National de la Santé et de la Recherche Médicale UMR 1051, Institute for Neurosciences of Montpellier, Montpellier, France; University of Montpellier 1 and 2, Montpellier, France; and.
Jérôme
J
Bourien
Institut National de la Santé et de la Recherche Médicale UMR 1051, Institute for Neurosciences of Montpellier, Montpellier, France; University of Montpellier 1 and 2, Montpellier, France; and Department of Otolaryngology, First Affiliated Hospital of Kunming Medical University, Kunming, China.
Yong
Y
Tang
Institut National de la Santé et de la Recherche Médicale UMR 1051, Institute for Neurosciences of Montpellier, Montpellier, France; University of Montpellier 1 and 2, Montpellier, France; and.
Charlène
C
Batrel
Institut National de la Santé et de la Recherche Médicale UMR 1051, Institute for Neurosciences of Montpellier, Montpellier, France; University of Montpellier 1 and 2, Montpellier, France; and.
Antoine
A
Huet
Institut National de la Santé et de la Recherche Médicale UMR 1051, Institute for Neurosciences of Montpellier, Montpellier, France; University of Montpellier 1 and 2, Montpellier, France; and.
Marc
M
Lenoir
Institut National de la Santé et de la Recherche Médicale UMR 1051, Institute for Neurosciences of Montpellier, Montpellier, France; University of Montpellier 1 and 2, Montpellier, France; and.
Sabine
S
Ladrech
Institut National de la Santé et de la Recherche Médicale UMR 1051, Institute for Neurosciences of Montpellier, Montpellier, France; University of Montpellier 1 and 2, Montpellier, France; and.
Gilles
G
Desmadryl
Institut National de la Santé et de la Recherche Médicale UMR 1051, Institute for Neurosciences of Montpellier, Montpellier, France; University of Montpellier 1 and 2, Montpellier, France; and.
Régis
R
Nouvian
Institut National de la Santé et de la Recherche Médicale UMR 1051, Institute for Neurosciences of Montpellier, Montpellier, France; University of Montpellier 1 and 2, Montpellier, France; and jean-luc.puel@inserm.fr.
Jean-Luc
JL
Puel
Institut National de la Santé et de la Recherche Médicale UMR 1051, Institute for Neurosciences of Montpellier, Montpellier, France; University of Montpellier 1 and 2, Montpellier, France; and.
Jing
J
Wang
D000161:Acoustic Stimulation; D000200:Action Potentials / Q000187:drug effects / Q000502:physiology*; D000818:Animals; D003051:Cochlea / Q000187:drug effects / Q000294:innervation* / Q000648:ultrastructure; D003056:Cochlear Nerve / Q000187:drug effects / Q000503:physiopathology* / Q000648:ultrastructure; D005849:Gerbillinae; D006168:Guinea Pigs; D008959:Models, Neurological; D009474:Neurons / Q000187:drug effects / Q000648:ultrastructure; D010042:Ouabain / Q000633:toxicity
D010042:Ouabain
auditory nerve fibers; compound action potential; computational modeling; first spike latency; ouabain