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Neuronal population model of globular bushy cells covering unit-to-unit variability

Computations of acoustic information along the central auditory pathways start in the cochlear nucleus. Bushy cells in the anteroventral cochlear nucleus, which innervate monaural and binaural stations in the superior olivary complex, process and transfer temporal cues relevant for sound localizatio...

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Autores principales: Ashida, Go, Heinermann, Helen T., Kretzberg, Jutta
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6934273/
https://www.ncbi.nlm.nih.gov/pubmed/31881018
http://dx.doi.org/10.1371/journal.pcbi.1007563
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author Ashida, Go
Heinermann, Helen T.
Kretzberg, Jutta
author_facet Ashida, Go
Heinermann, Helen T.
Kretzberg, Jutta
author_sort Ashida, Go
collection PubMed
description Computations of acoustic information along the central auditory pathways start in the cochlear nucleus. Bushy cells in the anteroventral cochlear nucleus, which innervate monaural and binaural stations in the superior olivary complex, process and transfer temporal cues relevant for sound localization. These cells are categorized into two groups: spherical and globular bushy cells (SBCs/GBCs). Spontaneous rates of GBCs innervated by multiple auditory nerve (AN) fibers are generally lower than those of SBCs that receive a small number of large AN synapses. In response to low-frequency tonal stimulation, both types of bushy cells show improved phase-locking and entrainment compared to AN fibers. When driven by high-frequency tones, GBCs show primary-like-with-notch or onset-L peristimulus time histograms and relatively irregular spiking. However, previous in vivo physiological studies of bushy cells also found considerable unit-to-unit variability in these response patterns. Here we present a population of models that can simulate the observed variation in GBCs. We used a simple coincidence detection model with an adaptive threshold and systematically varied its six parameters. Out of 567000 parameter combinations tested, 7520 primary-like-with-notch models and 4094 onset-L models were selected that satisfied a set of physiological criteria for a GBC unit. Analyses of the model parameters and output measures revealed that the parameters of the accepted model population are weakly correlated with each other to retain major GBC properties, and that the output spiking patterns of the model are affected by a combination of multiple parameters. Simulations of frequency-dependent temporal properties of the model GBCs showed a reasonable fit to empirical data, supporting the validity of our population modeling. The computational simplicity and efficiency of the model structure makes our approach suitable for future large-scale simulations of binaural information processing that may involve thousands of GBC units.
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spelling pubmed-69342732020-01-07 Neuronal population model of globular bushy cells covering unit-to-unit variability Ashida, Go Heinermann, Helen T. Kretzberg, Jutta PLoS Comput Biol Research Article Computations of acoustic information along the central auditory pathways start in the cochlear nucleus. Bushy cells in the anteroventral cochlear nucleus, which innervate monaural and binaural stations in the superior olivary complex, process and transfer temporal cues relevant for sound localization. These cells are categorized into two groups: spherical and globular bushy cells (SBCs/GBCs). Spontaneous rates of GBCs innervated by multiple auditory nerve (AN) fibers are generally lower than those of SBCs that receive a small number of large AN synapses. In response to low-frequency tonal stimulation, both types of bushy cells show improved phase-locking and entrainment compared to AN fibers. When driven by high-frequency tones, GBCs show primary-like-with-notch or onset-L peristimulus time histograms and relatively irregular spiking. However, previous in vivo physiological studies of bushy cells also found considerable unit-to-unit variability in these response patterns. Here we present a population of models that can simulate the observed variation in GBCs. We used a simple coincidence detection model with an adaptive threshold and systematically varied its six parameters. Out of 567000 parameter combinations tested, 7520 primary-like-with-notch models and 4094 onset-L models were selected that satisfied a set of physiological criteria for a GBC unit. Analyses of the model parameters and output measures revealed that the parameters of the accepted model population are weakly correlated with each other to retain major GBC properties, and that the output spiking patterns of the model are affected by a combination of multiple parameters. Simulations of frequency-dependent temporal properties of the model GBCs showed a reasonable fit to empirical data, supporting the validity of our population modeling. The computational simplicity and efficiency of the model structure makes our approach suitable for future large-scale simulations of binaural information processing that may involve thousands of GBC units. Public Library of Science 2019-12-27 /pmc/articles/PMC6934273/ /pubmed/31881018 http://dx.doi.org/10.1371/journal.pcbi.1007563 Text en © 2019 Ashida et al http://creativecommons.org/licenses/by/4.0/ This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Ashida, Go
Heinermann, Helen T.
Kretzberg, Jutta
Neuronal population model of globular bushy cells covering unit-to-unit variability
title Neuronal population model of globular bushy cells covering unit-to-unit variability
title_full Neuronal population model of globular bushy cells covering unit-to-unit variability
title_fullStr Neuronal population model of globular bushy cells covering unit-to-unit variability
title_full_unstemmed Neuronal population model of globular bushy cells covering unit-to-unit variability
title_short Neuronal population model of globular bushy cells covering unit-to-unit variability
title_sort neuronal population model of globular bushy cells covering unit-to-unit variability
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6934273/
https://www.ncbi.nlm.nih.gov/pubmed/31881018
http://dx.doi.org/10.1371/journal.pcbi.1007563
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