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Arousal State-Dependence of Interactions Between Short- and Long-Term Auditory Novelty Responses in Human Subjects

In everyday life, predictable sensory stimuli are generally not ecologically informative. By contrast, novel or unexpected stimuli signal ecologically salient changes in the environment. This idea forms the basis of the predictive coding hypothesis: efficient sensory encoding minimizes neural activi...

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Autores principales: Nourski, Kirill V., Steinschneider, Mitchell, Rhone, Ariane E., Mueller, Rashmi N., Kawasaki, Hiroto, Banks, Matthew I.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8517406/
https://www.ncbi.nlm.nih.gov/pubmed/34658820
http://dx.doi.org/10.3389/fnhum.2021.737230
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author Nourski, Kirill V.
Steinschneider, Mitchell
Rhone, Ariane E.
Mueller, Rashmi N.
Kawasaki, Hiroto
Banks, Matthew I.
author_facet Nourski, Kirill V.
Steinschneider, Mitchell
Rhone, Ariane E.
Mueller, Rashmi N.
Kawasaki, Hiroto
Banks, Matthew I.
author_sort Nourski, Kirill V.
collection PubMed
description In everyday life, predictable sensory stimuli are generally not ecologically informative. By contrast, novel or unexpected stimuli signal ecologically salient changes in the environment. This idea forms the basis of the predictive coding hypothesis: efficient sensory encoding minimizes neural activity associated with predictable backgrounds and emphasizes detection of changes in the environment. In real life, the brain must resolve multiple unexpected sensory events occurring over different time scales. The local/global deviant experimental paradigm examines auditory predictive coding over multiple time scales. For short-term novelty [hundreds of milliseconds; local deviance (LD)], sequences of identical sounds (/xxxxx/) are interspersed with sequences that contain deviants (/xxxxy/). Long-term novelty [several seconds; global deviance (GD)] is created using either (a) frequent /xxxxx/ and infrequent /xxxxy/ sequences, or (b) frequent /xxxxy/ and infrequent /xxxxx/ sequences. In scenario (a), there is both an LD and a GD effect (LDGD, “double surprise”). In (b), the global deviant is a local standard, i.e., sequence of identical sounds (LSGD). Cortical responses reflecting LD and GD originate in different brain areas, have a different time course, and are differentially sensitive to general anesthesia. Neural processes underlying LD and GD have been shown to interact, reflecting overlapping networks subserving the detection of novel auditory stimuli. This study examined these interactions using intracranial electroencephalography in neurosurgical patients. Subjects performed a GD target detection task before and during induction of anesthesia with propofol. Recordings were made from the auditory cortex, surrounding auditory-related and prefrontal cortex in awake, sedated, and unresponsive states. High gamma activity was used to measure the neural basis of local-by-global novelty interactions. Positive interaction was defined as a greater response to the double surprise LDGD condition compared to LSGD. Negative interaction was defined as a weaker response to LDGD. Positive interaction was more frequent than negative interaction and was primarily found in auditory cortex. Negative interaction typically occurred in prefrontal cortex and was more sensitive to general anesthesia. Temporo-parietal auditory-related areas exhibited both types of interaction. These interactions may have relevance in a clinical setting as biomarkers of conscious perception in the assessment of depth of anesthesia and disorders of consciousness.
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spelling pubmed-85174062021-10-16 Arousal State-Dependence of Interactions Between Short- and Long-Term Auditory Novelty Responses in Human Subjects Nourski, Kirill V. Steinschneider, Mitchell Rhone, Ariane E. Mueller, Rashmi N. Kawasaki, Hiroto Banks, Matthew I. Front Hum Neurosci Neuroscience In everyday life, predictable sensory stimuli are generally not ecologically informative. By contrast, novel or unexpected stimuli signal ecologically salient changes in the environment. This idea forms the basis of the predictive coding hypothesis: efficient sensory encoding minimizes neural activity associated with predictable backgrounds and emphasizes detection of changes in the environment. In real life, the brain must resolve multiple unexpected sensory events occurring over different time scales. The local/global deviant experimental paradigm examines auditory predictive coding over multiple time scales. For short-term novelty [hundreds of milliseconds; local deviance (LD)], sequences of identical sounds (/xxxxx/) are interspersed with sequences that contain deviants (/xxxxy/). Long-term novelty [several seconds; global deviance (GD)] is created using either (a) frequent /xxxxx/ and infrequent /xxxxy/ sequences, or (b) frequent /xxxxy/ and infrequent /xxxxx/ sequences. In scenario (a), there is both an LD and a GD effect (LDGD, “double surprise”). In (b), the global deviant is a local standard, i.e., sequence of identical sounds (LSGD). Cortical responses reflecting LD and GD originate in different brain areas, have a different time course, and are differentially sensitive to general anesthesia. Neural processes underlying LD and GD have been shown to interact, reflecting overlapping networks subserving the detection of novel auditory stimuli. This study examined these interactions using intracranial electroencephalography in neurosurgical patients. Subjects performed a GD target detection task before and during induction of anesthesia with propofol. Recordings were made from the auditory cortex, surrounding auditory-related and prefrontal cortex in awake, sedated, and unresponsive states. High gamma activity was used to measure the neural basis of local-by-global novelty interactions. Positive interaction was defined as a greater response to the double surprise LDGD condition compared to LSGD. Negative interaction was defined as a weaker response to LDGD. Positive interaction was more frequent than negative interaction and was primarily found in auditory cortex. Negative interaction typically occurred in prefrontal cortex and was more sensitive to general anesthesia. Temporo-parietal auditory-related areas exhibited both types of interaction. These interactions may have relevance in a clinical setting as biomarkers of conscious perception in the assessment of depth of anesthesia and disorders of consciousness. Frontiers Media S.A. 2021-10-01 /pmc/articles/PMC8517406/ /pubmed/34658820 http://dx.doi.org/10.3389/fnhum.2021.737230 Text en Copyright © 2021 Nourski, Steinschneider, Rhone, Mueller, Kawasaki and Banks. 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
Nourski, Kirill V.
Steinschneider, Mitchell
Rhone, Ariane E.
Mueller, Rashmi N.
Kawasaki, Hiroto
Banks, Matthew I.
Arousal State-Dependence of Interactions Between Short- and Long-Term Auditory Novelty Responses in Human Subjects
title Arousal State-Dependence of Interactions Between Short- and Long-Term Auditory Novelty Responses in Human Subjects
title_full Arousal State-Dependence of Interactions Between Short- and Long-Term Auditory Novelty Responses in Human Subjects
title_fullStr Arousal State-Dependence of Interactions Between Short- and Long-Term Auditory Novelty Responses in Human Subjects
title_full_unstemmed Arousal State-Dependence of Interactions Between Short- and Long-Term Auditory Novelty Responses in Human Subjects
title_short Arousal State-Dependence of Interactions Between Short- and Long-Term Auditory Novelty Responses in Human Subjects
title_sort arousal state-dependence of interactions between short- and long-term auditory novelty responses in human subjects
topic Neuroscience
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8517406/
https://www.ncbi.nlm.nih.gov/pubmed/34658820
http://dx.doi.org/10.3389/fnhum.2021.737230
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