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Downstream changes in firing regularity following damage to the early auditory system

Downstream changes in firing regularity following damage to the early auditory system Goodman et al. BMC Neuroscience 2015, 16(Suppl 1):O11 http://www.biomedcentral.com/1471-2202/16/S1/O11 ORAL PRESENTATION Open Access Downstream changes in firing regularity following damage to the early auditory system 1* 2 3 2 Dan FM Goodman , Alain de Cheveigné , Ian M Winter , Christian Lorenzi From 24th Annual Computational Neuroscience Meeting: CNS*2015 Prague, Czech Republic. 18-23 July 2015 We demonstrate how an abstract mathematical model One simple prediction of this model is that when the that approximates a wide range of more detailed models intensity of a stimulus changes, leading to a change in can be used to make predictions about hearing loss- the average firing rate of the ANF inputs, there will be a related changes in neural behaviour. corresponding change in the regularity of the chopper One consequence of neurosensory hearing loss (noise- cell spike train. This prediction poses problems for the induced and aging-related) is a reduced ability to under- widely used scheme for classifying chopper cells as sus- tained or transient based on their ongoing CVs as it stand speech, particularly in noisy environments, and sometimes beyond what would be predicted from implies that the classification could be level-dependent. reduced audibility. Indeed, this type of speech deficit can We present a re-analysis of an existing experimental data occur in listeners with near-normal hearing thresholds set that demonstrates that ongoing CV is indeed level- [1]. A promising avenue of investigation to explain this dependent in the majority of chopper cells, and that in comes from experimental results in mice showing that some cells (>7%) this leads to a level-dependence in their there can be a permanent loss of auditory nerve fibres classification. (ANFs) following “temporary” noise-induced hearing loss Assuming a homeostatic regulation of long term firing (i.e. when thresholds return to normal after a few weeks) rates, a loss of ANFs will lead to an increase in the stan- [2]. The downstream consequences of this loss of fibres dard deviation of the stochastic process and a consequent has not yet been systematically investigated (although see increase in the CV of the chopper cell. Some choppers that [3]). We predict, using a theoretical analysis that applies were previously classified as sustained will become transi- to a wide range of neural models, that the regularity of ent, a substantial change in their behaviour that is highly the spike trains of many neurons in the cochlear nucleus likely to disrupt auditory processing. While the function of (the next structure after the auditory nerve) will decrease chopper cells is still debated, one suggested role is in the following a reduction in the number of input cells. coding of temporal envelope [4], which is widely agreed to We present a mathematical analysis of the stationary be essential for understanding speech. Loss of ANFs could behaviour of “chopper” cells in the ventral cochlear therefore lead to a disruption of the processing of temporal nucleus, approximating them by a stochastic process that envelope, and consequently degrade speech intelligibility. is entirely characterised by its mean, standard deviation We briefly conclude by discussing the challenges of testing and time constants. Furthermore, these constants can be this hypothesis experimentally. straightforwardly related to physiologically significant parameters including the number of inputs and their Authors’ details average firing rates. From this approximation, we can 1 Department of Electrical and Electronic Engineering, Imperial College compute the regularity of the chopper cell spike trains London, London, UK. Laboratoire des Systèmes Perceptifs, Centre National de la Recherche Scientifique and École Normale Supérieure, Paris, France. measured as the coefficient of variation of their interspike Centre for the Neural Basis of Hearing, The Physiological Laboratory, intervals (CV). Department of Physiology, Development and Neuroscience, University of Cambridge, Cambridge, UK. * Correspondence: d.goodman@imperial.ac.uk Published: 18 December 2015 Department of Electrical and Electronic Engineering, Imperial College London, London, UK Full list of author information is available at the end of the article © 2015 Goodman et al. 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 work is properly cited. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/ publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Goodman et al. BMC Neuroscience 2015, 16(Suppl 1):O11 Page 2 of 2 http://www.biomedcentral.com/1471-2202/16/S1/O11 References 1. Leger AC, Moore BCJ, Lorenzi C: Temporal and spectral masking release in low-and mid-frequency regions for normal-hearing and hearing- impaired listeners. J Acoust Soc Am 2012, 131(2):1502-1514. 2. Kujawa SG, Liberman MC: Adding insult to injury: cochlear nerve degeneration after “temporary” noise-induced hearing loss. J Neurosci 2009, 29(45):14077-14085. 3. Lopez-Poveda EA, Barrios P: Perception of stochastically undersampled sound waveforms: a model of auditory deafferentation. Front Neurosci 2013, 7:124. 4. Lorenzi C, Micheyl C, Berthommier F: Neuronal correlates of perceptual amplitude-modulation detection. Hearing Research 1995, 90(1-2):, 219-227. doi:10.1186/1471-2202-16-S1-O11 Cite this article as: Goodman et al.: Downstream changes in firing regularity following damage to the early auditory system. BMC Neuroscience 2015 16(Suppl 1):O11. Submit your next manuscript to BioMed Central and take full advantage of: • Convenient online submission • Thorough peer review • No space constraints or color figure charges • Immediate publication on acceptance • Inclusion in PubMed, CAS, Scopus and Google Scholar • Research which is freely available for redistribution Submit your manuscript at www.biomedcentral.com/submit http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png BMC Neuroscience Springer Journals

Downstream changes in firing regularity following damage to the early auditory system

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Springer Journals
Copyright
Copyright © 2015 by Goodman et al.
Subject
Biomedicine; Neurosciences; Neurobiology; Animal Models
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1471-2202
DOI
10.1186/1471-2202-16-S1-O11
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Abstract

Goodman et al. BMC Neuroscience 2015, 16(Suppl 1):O11 http://www.biomedcentral.com/1471-2202/16/S1/O11 ORAL PRESENTATION Open Access Downstream changes in firing regularity following damage to the early auditory system 1* 2 3 2 Dan FM Goodman , Alain de Cheveigné , Ian M Winter , Christian Lorenzi From 24th Annual Computational Neuroscience Meeting: CNS*2015 Prague, Czech Republic. 18-23 July 2015 We demonstrate how an abstract mathematical model One simple prediction of this model is that when the that approximates a wide range of more detailed models intensity of a stimulus changes, leading to a change in can be used to make predictions about hearing loss- the average firing rate of the ANF inputs, there will be a related changes in neural behaviour. corresponding change in the regularity of the chopper One consequence of neurosensory hearing loss (noise- cell spike train. This prediction poses problems for the induced and aging-related) is a reduced ability to under- widely used scheme for classifying chopper cells as sus- tained or transient based on their ongoing CVs as it stand speech, particularly in noisy environments, and sometimes beyond what would be predicted from implies that the classification could be level-dependent. reduced audibility. Indeed, this type of speech deficit can We present a re-analysis of an existing experimental data occur in listeners with near-normal hearing thresholds set that demonstrates that ongoing CV is indeed level- [1]. A promising avenue of investigation to explain this dependent in the majority of chopper cells, and that in comes from experimental results in mice showing that some cells (>7%) this leads to a level-dependence in their there can be a permanent loss of auditory nerve fibres classification. (ANFs) following “temporary” noise-induced hearing loss Assuming a homeostatic regulation of long term firing (i.e. when thresholds return to normal after a few weeks) rates, a loss of ANFs will lead to an increase in the stan- [2]. The downstream consequences of this loss of fibres dard deviation of the stochastic process and a consequent has not yet been systematically investigated (although see increase in the CV of the chopper cell. Some choppers that [3]). We predict, using a theoretical analysis that applies were previously classified as sustained will become transi- to a wide range of neural models, that the regularity of ent, a substantial change in their behaviour that is highly the spike trains of many neurons in the cochlear nucleus likely to disrupt auditory processing. While the function of (the next structure after the auditory nerve) will decrease chopper cells is still debated, one suggested role is in the following a reduction in the number of input cells. coding of temporal envelope [4], which is widely agreed to We present a mathematical analysis of the stationary be essential for understanding speech. Loss of ANFs could behaviour of “chopper” cells in the ventral cochlear therefore lead to a disruption of the processing of temporal nucleus, approximating them by a stochastic process that envelope, and consequently degrade speech intelligibility. is entirely characterised by its mean, standard deviation We briefly conclude by discussing the challenges of testing and time constants. Furthermore, these constants can be this hypothesis experimentally. straightforwardly related to physiologically significant parameters including the number of inputs and their Authors’ details average firing rates. From this approximation, we can 1 Department of Electrical and Electronic Engineering, Imperial College compute the regularity of the chopper cell spike trains London, London, UK. Laboratoire des Systèmes Perceptifs, Centre National de la Recherche Scientifique and École Normale Supérieure, Paris, France. measured as the coefficient of variation of their interspike Centre for the Neural Basis of Hearing, The Physiological Laboratory, intervals (CV). Department of Physiology, Development and Neuroscience, University of Cambridge, Cambridge, UK. * Correspondence: d.goodman@imperial.ac.uk Published: 18 December 2015 Department of Electrical and Electronic Engineering, Imperial College London, London, UK Full list of author information is available at the end of the article © 2015 Goodman et al. 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 work is properly cited. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/ publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Goodman et al. BMC Neuroscience 2015, 16(Suppl 1):O11 Page 2 of 2 http://www.biomedcentral.com/1471-2202/16/S1/O11 References 1. Leger AC, Moore BCJ, Lorenzi C: Temporal and spectral masking release in low-and mid-frequency regions for normal-hearing and hearing- impaired listeners. J Acoust Soc Am 2012, 131(2):1502-1514. 2. Kujawa SG, Liberman MC: Adding insult to injury: cochlear nerve degeneration after “temporary” noise-induced hearing loss. J Neurosci 2009, 29(45):14077-14085. 3. Lopez-Poveda EA, Barrios P: Perception of stochastically undersampled sound waveforms: a model of auditory deafferentation. Front Neurosci 2013, 7:124. 4. Lorenzi C, Micheyl C, Berthommier F: Neuronal correlates of perceptual amplitude-modulation detection. Hearing Research 1995, 90(1-2):, 219-227. doi:10.1186/1471-2202-16-S1-O11 Cite this article as: Goodman et al.: Downstream changes in firing regularity following damage to the early auditory system. BMC Neuroscience 2015 16(Suppl 1):O11. Submit your next manuscript to BioMed Central and take full advantage of: • Convenient online submission • Thorough peer review • No space constraints or color figure charges • Immediate publication on acceptance • Inclusion in PubMed, CAS, Scopus and Google Scholar • Research which is freely available for redistribution Submit your manuscript at www.biomedcentral.com/submit

Journal

BMC Neuroscience – Springer Journals

Published: Dec 4, 2015

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