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Encoding of Natural Sounds at Multiple Spectral and Temporal Resolutions in the Human Auditory Cortex

Functional neuroimaging research provides detailed observations of the response patterns that natural sounds (e.g. human voices and speech, animal cries, environmental sounds) evoke in the human brain. The computational and representational mechanisms underlying these observations, however, remain l...

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Autores principales: Santoro, Roberta, Moerel, Michelle, De Martino, Federico, Goebel, Rainer, Ugurbil, Kamil, Yacoub, Essa, Formisano, Elia
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2014
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3879146/
https://www.ncbi.nlm.nih.gov/pubmed/24391486
http://dx.doi.org/10.1371/journal.pcbi.1003412
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author Santoro, Roberta
Moerel, Michelle
De Martino, Federico
Goebel, Rainer
Ugurbil, Kamil
Yacoub, Essa
Formisano, Elia
author_facet Santoro, Roberta
Moerel, Michelle
De Martino, Federico
Goebel, Rainer
Ugurbil, Kamil
Yacoub, Essa
Formisano, Elia
author_sort Santoro, Roberta
collection PubMed
description Functional neuroimaging research provides detailed observations of the response patterns that natural sounds (e.g. human voices and speech, animal cries, environmental sounds) evoke in the human brain. The computational and representational mechanisms underlying these observations, however, remain largely unknown. Here we combine high spatial resolution (3 and 7 Tesla) functional magnetic resonance imaging (fMRI) with computational modeling to reveal how natural sounds are represented in the human brain. We compare competing models of sound representations and select the model that most accurately predicts fMRI response patterns to natural sounds. Our results show that the cortical encoding of natural sounds entails the formation of multiple representations of sound spectrograms with different degrees of spectral and temporal resolution. The cortex derives these multi-resolution representations through frequency-specific neural processing channels and through the combined analysis of the spectral and temporal modulations in the spectrogram. Furthermore, our findings suggest that a spectral-temporal resolution trade-off may govern the modulation tuning of neuronal populations throughout the auditory cortex. Specifically, our fMRI results suggest that neuronal populations in posterior/dorsal auditory regions preferably encode coarse spectral information with high temporal precision. Vice-versa, neuronal populations in anterior/ventral auditory regions preferably encode fine-grained spectral information with low temporal precision. We propose that such a multi-resolution analysis may be crucially relevant for flexible and behaviorally-relevant sound processing and may constitute one of the computational underpinnings of functional specialization in auditory cortex.
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spelling pubmed-38791462014-01-03 Encoding of Natural Sounds at Multiple Spectral and Temporal Resolutions in the Human Auditory Cortex Santoro, Roberta Moerel, Michelle De Martino, Federico Goebel, Rainer Ugurbil, Kamil Yacoub, Essa Formisano, Elia PLoS Comput Biol Research Article Functional neuroimaging research provides detailed observations of the response patterns that natural sounds (e.g. human voices and speech, animal cries, environmental sounds) evoke in the human brain. The computational and representational mechanisms underlying these observations, however, remain largely unknown. Here we combine high spatial resolution (3 and 7 Tesla) functional magnetic resonance imaging (fMRI) with computational modeling to reveal how natural sounds are represented in the human brain. We compare competing models of sound representations and select the model that most accurately predicts fMRI response patterns to natural sounds. Our results show that the cortical encoding of natural sounds entails the formation of multiple representations of sound spectrograms with different degrees of spectral and temporal resolution. The cortex derives these multi-resolution representations through frequency-specific neural processing channels and through the combined analysis of the spectral and temporal modulations in the spectrogram. Furthermore, our findings suggest that a spectral-temporal resolution trade-off may govern the modulation tuning of neuronal populations throughout the auditory cortex. Specifically, our fMRI results suggest that neuronal populations in posterior/dorsal auditory regions preferably encode coarse spectral information with high temporal precision. Vice-versa, neuronal populations in anterior/ventral auditory regions preferably encode fine-grained spectral information with low temporal precision. We propose that such a multi-resolution analysis may be crucially relevant for flexible and behaviorally-relevant sound processing and may constitute one of the computational underpinnings of functional specialization in auditory cortex. Public Library of Science 2014-01-02 /pmc/articles/PMC3879146/ /pubmed/24391486 http://dx.doi.org/10.1371/journal.pcbi.1003412 Text en 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
Santoro, Roberta
Moerel, Michelle
De Martino, Federico
Goebel, Rainer
Ugurbil, Kamil
Yacoub, Essa
Formisano, Elia
Encoding of Natural Sounds at Multiple Spectral and Temporal Resolutions in the Human Auditory Cortex
title Encoding of Natural Sounds at Multiple Spectral and Temporal Resolutions in the Human Auditory Cortex
title_full Encoding of Natural Sounds at Multiple Spectral and Temporal Resolutions in the Human Auditory Cortex
title_fullStr Encoding of Natural Sounds at Multiple Spectral and Temporal Resolutions in the Human Auditory Cortex
title_full_unstemmed Encoding of Natural Sounds at Multiple Spectral and Temporal Resolutions in the Human Auditory Cortex
title_short Encoding of Natural Sounds at Multiple Spectral and Temporal Resolutions in the Human Auditory Cortex
title_sort encoding of natural sounds at multiple spectral and temporal resolutions in the human auditory cortex
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3879146/
https://www.ncbi.nlm.nih.gov/pubmed/24391486
http://dx.doi.org/10.1371/journal.pcbi.1003412
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