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Effects of Degrees of Degeneration on the Electrical Excitation of Human Spiral Ganglion Neurons Based on a High-Resolution Computer Model

After hearing loss retrograde degeneration of spiral ganglion neurons (SGNs) has been described. Studies modeling the effects of degeneration mostly omitted peripheral processes (dendrites). Recent experimental observations indicated that degenerating SGNs manifested also a reduced diameter of their...

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Autores principales: Croner, Albert M., Heshmat, Amirreza, Schrott-Fischer, Anneliese, Glueckert, Rudolf, Hemmert, Werner, Bai, Siwei
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9298973/
https://www.ncbi.nlm.nih.gov/pubmed/35873813
http://dx.doi.org/10.3389/fnins.2022.914876
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author Croner, Albert M.
Heshmat, Amirreza
Schrott-Fischer, Anneliese
Glueckert, Rudolf
Hemmert, Werner
Bai, Siwei
author_facet Croner, Albert M.
Heshmat, Amirreza
Schrott-Fischer, Anneliese
Glueckert, Rudolf
Hemmert, Werner
Bai, Siwei
author_sort Croner, Albert M.
collection PubMed
description After hearing loss retrograde degeneration of spiral ganglion neurons (SGNs) has been described. Studies modeling the effects of degeneration mostly omitted peripheral processes (dendrites). Recent experimental observations indicated that degenerating SGNs manifested also a reduced diameter of their dendrites. We simulated populations of 400 SGNs inside a high resolution cochlear model with a cochlear implant, based on μCT scans of a human temporal bone. Cochlear implant stimuli were delivered as biphasic pulses in a monopolar configuration. Three SGN situations were simulated, based on our previous measurements of human SGN dendrites: (A) SGNs with intact dendrites (before degeneration), (B) degenerating SGNs, dendrites with a smaller diameter but original length, (C) degenerating SGNs, dendrites omitted. SGN fibers were mapped to characteristic frequency, and place pitch was estimated from excitation profiles. Results from degenerating SGNs (B, C) were similar. Most action potentials were initiated in the somatic area for all cases (A, B, C), except for areas near stimulating electrodes in the apex with intact SGNs (A), where action potentials were initiated in the distal dendrite. In most cases, degenerating SGNs had lower thresholds than intact SGNs (A) (down to –2 dB). Excitation profiles showed increased ectopic activation, i.e., activation of unintended neuronal regions, as well as similar neuronal regions excited by different apical electrodes, for degenerating SGNs (B, C). The estimated pitch showed cases of pitch reversals in apical electrodes for intact SGNs (A), as well as mostly identical pitches evoked by the four most apical electrodes for degenerating SGNs (B, C). In conclusion, neuronal excitation profiles to electrical stimulation exhibited similar traits in both ways of modeling SGN degeneration. Models showed degeneration of dendrites caused increased ectopic activation, as well as similar excitation profiles and pitch evoked by different apical electrodes. Therefore, insertion of electrodes beyond approximately 450° may not provide any benefit if SGN dendrites are degenerated.
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spelling pubmed-92989732022-07-21 Effects of Degrees of Degeneration on the Electrical Excitation of Human Spiral Ganglion Neurons Based on a High-Resolution Computer Model Croner, Albert M. Heshmat, Amirreza Schrott-Fischer, Anneliese Glueckert, Rudolf Hemmert, Werner Bai, Siwei Front Neurosci Neuroscience After hearing loss retrograde degeneration of spiral ganglion neurons (SGNs) has been described. Studies modeling the effects of degeneration mostly omitted peripheral processes (dendrites). Recent experimental observations indicated that degenerating SGNs manifested also a reduced diameter of their dendrites. We simulated populations of 400 SGNs inside a high resolution cochlear model with a cochlear implant, based on μCT scans of a human temporal bone. Cochlear implant stimuli were delivered as biphasic pulses in a monopolar configuration. Three SGN situations were simulated, based on our previous measurements of human SGN dendrites: (A) SGNs with intact dendrites (before degeneration), (B) degenerating SGNs, dendrites with a smaller diameter but original length, (C) degenerating SGNs, dendrites omitted. SGN fibers were mapped to characteristic frequency, and place pitch was estimated from excitation profiles. Results from degenerating SGNs (B, C) were similar. Most action potentials were initiated in the somatic area for all cases (A, B, C), except for areas near stimulating electrodes in the apex with intact SGNs (A), where action potentials were initiated in the distal dendrite. In most cases, degenerating SGNs had lower thresholds than intact SGNs (A) (down to –2 dB). Excitation profiles showed increased ectopic activation, i.e., activation of unintended neuronal regions, as well as similar neuronal regions excited by different apical electrodes, for degenerating SGNs (B, C). The estimated pitch showed cases of pitch reversals in apical electrodes for intact SGNs (A), as well as mostly identical pitches evoked by the four most apical electrodes for degenerating SGNs (B, C). In conclusion, neuronal excitation profiles to electrical stimulation exhibited similar traits in both ways of modeling SGN degeneration. Models showed degeneration of dendrites caused increased ectopic activation, as well as similar excitation profiles and pitch evoked by different apical electrodes. Therefore, insertion of electrodes beyond approximately 450° may not provide any benefit if SGN dendrites are degenerated. Frontiers Media S.A. 2022-07-06 /pmc/articles/PMC9298973/ /pubmed/35873813 http://dx.doi.org/10.3389/fnins.2022.914876 Text en Copyright © 2022 Croner, Heshmat, Schrott-Fischer, Glueckert, Hemmert and Bai. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Neuroscience
Croner, Albert M.
Heshmat, Amirreza
Schrott-Fischer, Anneliese
Glueckert, Rudolf
Hemmert, Werner
Bai, Siwei
Effects of Degrees of Degeneration on the Electrical Excitation of Human Spiral Ganglion Neurons Based on a High-Resolution Computer Model
title Effects of Degrees of Degeneration on the Electrical Excitation of Human Spiral Ganglion Neurons Based on a High-Resolution Computer Model
title_full Effects of Degrees of Degeneration on the Electrical Excitation of Human Spiral Ganglion Neurons Based on a High-Resolution Computer Model
title_fullStr Effects of Degrees of Degeneration on the Electrical Excitation of Human Spiral Ganglion Neurons Based on a High-Resolution Computer Model
title_full_unstemmed Effects of Degrees of Degeneration on the Electrical Excitation of Human Spiral Ganglion Neurons Based on a High-Resolution Computer Model
title_short Effects of Degrees of Degeneration on the Electrical Excitation of Human Spiral Ganglion Neurons Based on a High-Resolution Computer Model
title_sort effects of degrees of degeneration on the electrical excitation of human spiral ganglion neurons based on a high-resolution computer model
topic Neuroscience
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9298973/
https://www.ncbi.nlm.nih.gov/pubmed/35873813
http://dx.doi.org/10.3389/fnins.2022.914876
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