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Prediction error signaling explains neuronal mismatch responses in the medial prefrontal cortex

The mismatch negativity (MMN) is a key biomarker of automatic deviance detection thought to emerge from 2 cortical sources. First, the auditory cortex (AC) encodes spectral regularities and reports frequency-specific deviances. Then, more abstract representations in the prefrontal cortex (PFC) allow...

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Autores principales: Casado-Román, Lorena, Carbajal, Guillermo V., Pérez-González, David, Malmierca, Manuel S.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7785337/
https://www.ncbi.nlm.nih.gov/pubmed/33347436
http://dx.doi.org/10.1371/journal.pbio.3001019
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author Casado-Román, Lorena
Carbajal, Guillermo V.
Pérez-González, David
Malmierca, Manuel S.
author_facet Casado-Román, Lorena
Carbajal, Guillermo V.
Pérez-González, David
Malmierca, Manuel S.
author_sort Casado-Román, Lorena
collection PubMed
description The mismatch negativity (MMN) is a key biomarker of automatic deviance detection thought to emerge from 2 cortical sources. First, the auditory cortex (AC) encodes spectral regularities and reports frequency-specific deviances. Then, more abstract representations in the prefrontal cortex (PFC) allow to detect contextual changes of potential behavioral relevance. However, the precise location and time asynchronies between neuronal correlates underlying this frontotemporal network remain unclear and elusive. Our study presented auditory oddball paradigms along with “no-repetition” controls to record mismatch responses in neuronal spiking activity and local field potentials at the rat medial PFC. Whereas mismatch responses in the auditory system are mainly induced by stimulus-dependent effects, we found that auditory responsiveness in the PFC was driven by unpredictability, yielding context-dependent, comparatively delayed, more robust and longer-lasting mismatch responses mostly comprised of prediction error signaling activity. This characteristically different composition discarded that mismatch responses in the PFC could be simply inherited or amplified downstream from the auditory system. Conversely, it is more plausible for the PFC to exert top-down influences on the AC, since the PFC exhibited flexible and potent predictive processing, capable of suppressing redundant input more efficiently than the AC. Remarkably, the time course of the mismatch responses we observed in the spiking activity and local field potentials of the AC and the PFC combined coincided with the time course of the large-scale MMN-like signals reported in the rat brain, thereby linking the microscopic, mesoscopic, and macroscopic levels of automatic deviance detection.
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spelling pubmed-77853372021-01-13 Prediction error signaling explains neuronal mismatch responses in the medial prefrontal cortex Casado-Román, Lorena Carbajal, Guillermo V. Pérez-González, David Malmierca, Manuel S. PLoS Biol Research Article The mismatch negativity (MMN) is a key biomarker of automatic deviance detection thought to emerge from 2 cortical sources. First, the auditory cortex (AC) encodes spectral regularities and reports frequency-specific deviances. Then, more abstract representations in the prefrontal cortex (PFC) allow to detect contextual changes of potential behavioral relevance. However, the precise location and time asynchronies between neuronal correlates underlying this frontotemporal network remain unclear and elusive. Our study presented auditory oddball paradigms along with “no-repetition” controls to record mismatch responses in neuronal spiking activity and local field potentials at the rat medial PFC. Whereas mismatch responses in the auditory system are mainly induced by stimulus-dependent effects, we found that auditory responsiveness in the PFC was driven by unpredictability, yielding context-dependent, comparatively delayed, more robust and longer-lasting mismatch responses mostly comprised of prediction error signaling activity. This characteristically different composition discarded that mismatch responses in the PFC could be simply inherited or amplified downstream from the auditory system. Conversely, it is more plausible for the PFC to exert top-down influences on the AC, since the PFC exhibited flexible and potent predictive processing, capable of suppressing redundant input more efficiently than the AC. Remarkably, the time course of the mismatch responses we observed in the spiking activity and local field potentials of the AC and the PFC combined coincided with the time course of the large-scale MMN-like signals reported in the rat brain, thereby linking the microscopic, mesoscopic, and macroscopic levels of automatic deviance detection. Public Library of Science 2020-12-21 /pmc/articles/PMC7785337/ /pubmed/33347436 http://dx.doi.org/10.1371/journal.pbio.3001019 Text en © 2020 Casado-Román 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
Casado-Román, Lorena
Carbajal, Guillermo V.
Pérez-González, David
Malmierca, Manuel S.
Prediction error signaling explains neuronal mismatch responses in the medial prefrontal cortex
title Prediction error signaling explains neuronal mismatch responses in the medial prefrontal cortex
title_full Prediction error signaling explains neuronal mismatch responses in the medial prefrontal cortex
title_fullStr Prediction error signaling explains neuronal mismatch responses in the medial prefrontal cortex
title_full_unstemmed Prediction error signaling explains neuronal mismatch responses in the medial prefrontal cortex
title_short Prediction error signaling explains neuronal mismatch responses in the medial prefrontal cortex
title_sort prediction error signaling explains neuronal mismatch responses in the medial prefrontal cortex
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7785337/
https://www.ncbi.nlm.nih.gov/pubmed/33347436
http://dx.doi.org/10.1371/journal.pbio.3001019
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