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Two stages of bandwidth scaling drives efficient neural coding of natural sounds

Theories of efficient coding propose that the auditory system is optimized for the statistical structure of natural sounds, yet the transformations underlying optimal acoustic representations are not well understood. Using a database of natural sounds including human speech and a physiologically-ins...

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Autores principales: He, Fengrong, Stevenson, Ian H., Escabí, Monty A.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9970106/
https://www.ncbi.nlm.nih.gov/pubmed/36787338
http://dx.doi.org/10.1371/journal.pcbi.1010862
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author He, Fengrong
Stevenson, Ian H.
Escabí, Monty A.
author_facet He, Fengrong
Stevenson, Ian H.
Escabí, Monty A.
author_sort He, Fengrong
collection PubMed
description Theories of efficient coding propose that the auditory system is optimized for the statistical structure of natural sounds, yet the transformations underlying optimal acoustic representations are not well understood. Using a database of natural sounds including human speech and a physiologically-inspired auditory model, we explore the consequences of peripheral (cochlear) and mid-level (auditory midbrain) filter tuning transformations on the representation of natural sound spectra and modulation statistics. Whereas Fourier-based sound decompositions have constant time-frequency resolution at all frequencies, cochlear and auditory midbrain filters bandwidths increase proportional to the filter center frequency. This form of bandwidth scaling produces a systematic decrease in spectral resolution and increase in temporal resolution with increasing frequency. Here we demonstrate that cochlear bandwidth scaling produces a frequency-dependent gain that counteracts the tendency of natural sound power to decrease with frequency, resulting in a whitened output representation. Similarly, bandwidth scaling in mid-level auditory filters further enhances the representation of natural sounds by producing a whitened modulation power spectrum (MPS) with higher modulation entropy than both the cochlear outputs and the conventional Fourier MPS. These findings suggest that the tuning characteristics of the peripheral and mid-level auditory system together produce a whitened output representation in three dimensions (frequency, temporal and spectral modulation) that reduces redundancies and allows for a more efficient use of neural resources. This hierarchical multi-stage tuning strategy is thus likely optimized to extract available information and may underlies perceptual sensitivity to natural sounds.
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spelling pubmed-99701062023-02-28 Two stages of bandwidth scaling drives efficient neural coding of natural sounds He, Fengrong Stevenson, Ian H. Escabí, Monty A. PLoS Comput Biol Research Article Theories of efficient coding propose that the auditory system is optimized for the statistical structure of natural sounds, yet the transformations underlying optimal acoustic representations are not well understood. Using a database of natural sounds including human speech and a physiologically-inspired auditory model, we explore the consequences of peripheral (cochlear) and mid-level (auditory midbrain) filter tuning transformations on the representation of natural sound spectra and modulation statistics. Whereas Fourier-based sound decompositions have constant time-frequency resolution at all frequencies, cochlear and auditory midbrain filters bandwidths increase proportional to the filter center frequency. This form of bandwidth scaling produces a systematic decrease in spectral resolution and increase in temporal resolution with increasing frequency. Here we demonstrate that cochlear bandwidth scaling produces a frequency-dependent gain that counteracts the tendency of natural sound power to decrease with frequency, resulting in a whitened output representation. Similarly, bandwidth scaling in mid-level auditory filters further enhances the representation of natural sounds by producing a whitened modulation power spectrum (MPS) with higher modulation entropy than both the cochlear outputs and the conventional Fourier MPS. These findings suggest that the tuning characteristics of the peripheral and mid-level auditory system together produce a whitened output representation in three dimensions (frequency, temporal and spectral modulation) that reduces redundancies and allows for a more efficient use of neural resources. This hierarchical multi-stage tuning strategy is thus likely optimized to extract available information and may underlies perceptual sensitivity to natural sounds. Public Library of Science 2023-02-14 /pmc/articles/PMC9970106/ /pubmed/36787338 http://dx.doi.org/10.1371/journal.pcbi.1010862 Text en © 2023 He et al https://creativecommons.org/licenses/by/4.0/This is an open access article distributed under the terms of the Creative Commons Attribution License (https://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
He, Fengrong
Stevenson, Ian H.
Escabí, Monty A.
Two stages of bandwidth scaling drives efficient neural coding of natural sounds
title Two stages of bandwidth scaling drives efficient neural coding of natural sounds
title_full Two stages of bandwidth scaling drives efficient neural coding of natural sounds
title_fullStr Two stages of bandwidth scaling drives efficient neural coding of natural sounds
title_full_unstemmed Two stages of bandwidth scaling drives efficient neural coding of natural sounds
title_short Two stages of bandwidth scaling drives efficient neural coding of natural sounds
title_sort two stages of bandwidth scaling drives efficient neural coding of natural sounds
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9970106/
https://www.ncbi.nlm.nih.gov/pubmed/36787338
http://dx.doi.org/10.1371/journal.pcbi.1010862
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