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Auditory, Visual, and Cross-Modal Mismatch Negativities in the Rat Auditory and Visual Cortices

When the brain tries to acquire an elaborate model of the world, multisensory integration should contribute to building predictions based on the various pieces of information, and deviance detection should repeatedly update these predictions by detecting “errors” from the actual sensory inputs. Accu...

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Autores principales: Shiramatsu, Tomoyo Isoguchi, Mori, Kanato, Ishizu, Kotaro, Takahashi, Hirokazu
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8484534/
https://www.ncbi.nlm.nih.gov/pubmed/34602996
http://dx.doi.org/10.3389/fnhum.2021.721476
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author Shiramatsu, Tomoyo Isoguchi
Mori, Kanato
Ishizu, Kotaro
Takahashi, Hirokazu
author_facet Shiramatsu, Tomoyo Isoguchi
Mori, Kanato
Ishizu, Kotaro
Takahashi, Hirokazu
author_sort Shiramatsu, Tomoyo Isoguchi
collection PubMed
description When the brain tries to acquire an elaborate model of the world, multisensory integration should contribute to building predictions based on the various pieces of information, and deviance detection should repeatedly update these predictions by detecting “errors” from the actual sensory inputs. Accumulating evidence such as a hierarchical organization of the deviance-detection system indicates that the deviance-detection system can be interpreted in the predictive coding framework. Herein, we targeted mismatch negativity (MMN) as a type of prediction-error signal and investigated the relationship between multisensory integration and MMN. In particular, we studied whether and how cross-modal information processing affected MMN in rodents. We designed a new surface microelectrode array and simultaneously recorded visual and auditory evoked potentials from the visual and auditory cortices of rats under anesthesia. Then, we mapped MMNs for five types of deviant stimuli: single-modal deviants in (i) the visual oddball and (ii) auditory oddball paradigms, eliciting single-modal MMN; (iii) congruent audio-visual deviants, (iv) incongruent visual deviants, and (v) incongruent auditory deviants in the audio-visual oddball paradigm, eliciting cross-modal MMN. First, we demonstrated that visual MMN exhibited deviance detection properties and that the first-generation focus of visual MMN was localized in the visual cortex, as previously reported in human studies. Second, a comparison of MMN amplitudes revealed a non-linear relationship between single-modal and cross-modal MMNs. Moreover, congruent audio-visual MMN exhibited characteristics of both visual and auditory MMNs—its latency was similar to that of auditory MMN, whereas local blockage of N-methyl-D-aspartic acid receptors in the visual cortex diminished it as well as visual MMN. These results indicate that cross-modal information processing affects MMN without involving strong top-down effects, such as those of prior knowledge and attention. The present study is the first electrophysiological evidence of cross-modal MMN in animal models, and future studies on the neural mechanisms combining multisensory integration and deviance detection are expected to provide electrophysiological evidence to confirm the links between MMN and predictive coding theory.
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spelling pubmed-84845342021-10-02 Auditory, Visual, and Cross-Modal Mismatch Negativities in the Rat Auditory and Visual Cortices Shiramatsu, Tomoyo Isoguchi Mori, Kanato Ishizu, Kotaro Takahashi, Hirokazu Front Hum Neurosci Neuroscience When the brain tries to acquire an elaborate model of the world, multisensory integration should contribute to building predictions based on the various pieces of information, and deviance detection should repeatedly update these predictions by detecting “errors” from the actual sensory inputs. Accumulating evidence such as a hierarchical organization of the deviance-detection system indicates that the deviance-detection system can be interpreted in the predictive coding framework. Herein, we targeted mismatch negativity (MMN) as a type of prediction-error signal and investigated the relationship between multisensory integration and MMN. In particular, we studied whether and how cross-modal information processing affected MMN in rodents. We designed a new surface microelectrode array and simultaneously recorded visual and auditory evoked potentials from the visual and auditory cortices of rats under anesthesia. Then, we mapped MMNs for five types of deviant stimuli: single-modal deviants in (i) the visual oddball and (ii) auditory oddball paradigms, eliciting single-modal MMN; (iii) congruent audio-visual deviants, (iv) incongruent visual deviants, and (v) incongruent auditory deviants in the audio-visual oddball paradigm, eliciting cross-modal MMN. First, we demonstrated that visual MMN exhibited deviance detection properties and that the first-generation focus of visual MMN was localized in the visual cortex, as previously reported in human studies. Second, a comparison of MMN amplitudes revealed a non-linear relationship between single-modal and cross-modal MMNs. Moreover, congruent audio-visual MMN exhibited characteristics of both visual and auditory MMNs—its latency was similar to that of auditory MMN, whereas local blockage of N-methyl-D-aspartic acid receptors in the visual cortex diminished it as well as visual MMN. These results indicate that cross-modal information processing affects MMN without involving strong top-down effects, such as those of prior knowledge and attention. The present study is the first electrophysiological evidence of cross-modal MMN in animal models, and future studies on the neural mechanisms combining multisensory integration and deviance detection are expected to provide electrophysiological evidence to confirm the links between MMN and predictive coding theory. Frontiers Media S.A. 2021-09-17 /pmc/articles/PMC8484534/ /pubmed/34602996 http://dx.doi.org/10.3389/fnhum.2021.721476 Text en Copyright © 2021 Shiramatsu, Mori, Ishizu and Takahashi. 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
Shiramatsu, Tomoyo Isoguchi
Mori, Kanato
Ishizu, Kotaro
Takahashi, Hirokazu
Auditory, Visual, and Cross-Modal Mismatch Negativities in the Rat Auditory and Visual Cortices
title Auditory, Visual, and Cross-Modal Mismatch Negativities in the Rat Auditory and Visual Cortices
title_full Auditory, Visual, and Cross-Modal Mismatch Negativities in the Rat Auditory and Visual Cortices
title_fullStr Auditory, Visual, and Cross-Modal Mismatch Negativities in the Rat Auditory and Visual Cortices
title_full_unstemmed Auditory, Visual, and Cross-Modal Mismatch Negativities in the Rat Auditory and Visual Cortices
title_short Auditory, Visual, and Cross-Modal Mismatch Negativities in the Rat Auditory and Visual Cortices
title_sort auditory, visual, and cross-modal mismatch negativities in the rat auditory and visual cortices
topic Neuroscience
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8484534/
https://www.ncbi.nlm.nih.gov/pubmed/34602996
http://dx.doi.org/10.3389/fnhum.2021.721476
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