Cargando…

Information theoretic evidence for layer- and frequency-specific changes in cortical information processing under anesthesia

Nature relies on highly distributed computation for the processing of information in nervous systems across the entire animal kingdom. Such distributed computation can be more easily understood if decomposed into the three elementary components of information processing, i.e. storage, transfer and m...

Descripción completa

Detalles Bibliográficos
Autores principales: Pinzuti, Edoardo, Wollstadt, Patricia, Tüscher, Oliver, Wibral, Michael
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9904504/
https://www.ncbi.nlm.nih.gov/pubmed/36701388
http://dx.doi.org/10.1371/journal.pcbi.1010380
_version_ 1784883629082542080
author Pinzuti, Edoardo
Wollstadt, Patricia
Tüscher, Oliver
Wibral, Michael
author_facet Pinzuti, Edoardo
Wollstadt, Patricia
Tüscher, Oliver
Wibral, Michael
author_sort Pinzuti, Edoardo
collection PubMed
description Nature relies on highly distributed computation for the processing of information in nervous systems across the entire animal kingdom. Such distributed computation can be more easily understood if decomposed into the three elementary components of information processing, i.e. storage, transfer and modification, and rigorous information theoretic measures for these components exist. However, the distributed computation is often also linked to neural dynamics exhibiting distinct rhythms. Thus, it would be beneficial to associate the above components of information processing with distinct rhythmic processes where possible. Here we focus on the storage of information in neural dynamics and introduce a novel spectrally-resolved measure of active information storage (AIS). Drawing on intracortical recordings of neural activity in ferrets under anesthesia before and after loss of consciousness (LOC) we show that anesthesia- related modulation of AIS is highly specific to different frequency bands and that these frequency-specific effects differ across cortical layers and brain regions. We found that in the high/low gamma band the effects of anesthesia result in AIS modulation only in the supergranular layers, while in the alpha/beta band the strongest decrease in AIS can be seen at infragranular layers. Finally, we show that the increase of spectral power at multiple frequencies, in particular at alpha and delta bands in frontal areas, that is often observed during LOC (’anteriorization’) also impacts local information processing—but in a frequency specific way: Increases in isoflurane concentration induced a decrease in AIS in the alpha frequencies, while they increased AIS in the delta frequency range < 2Hz. Thus, the analysis of spectrally-resolved AIS provides valuable additional insights into changes in cortical information processing under anaesthesia.
format Online
Article
Text
id pubmed-9904504
institution National Center for Biotechnology Information
language English
publishDate 2023
publisher Public Library of Science
record_format MEDLINE/PubMed
spelling pubmed-99045042023-02-08 Information theoretic evidence for layer- and frequency-specific changes in cortical information processing under anesthesia Pinzuti, Edoardo Wollstadt, Patricia Tüscher, Oliver Wibral, Michael PLoS Comput Biol Research Article Nature relies on highly distributed computation for the processing of information in nervous systems across the entire animal kingdom. Such distributed computation can be more easily understood if decomposed into the three elementary components of information processing, i.e. storage, transfer and modification, and rigorous information theoretic measures for these components exist. However, the distributed computation is often also linked to neural dynamics exhibiting distinct rhythms. Thus, it would be beneficial to associate the above components of information processing with distinct rhythmic processes where possible. Here we focus on the storage of information in neural dynamics and introduce a novel spectrally-resolved measure of active information storage (AIS). Drawing on intracortical recordings of neural activity in ferrets under anesthesia before and after loss of consciousness (LOC) we show that anesthesia- related modulation of AIS is highly specific to different frequency bands and that these frequency-specific effects differ across cortical layers and brain regions. We found that in the high/low gamma band the effects of anesthesia result in AIS modulation only in the supergranular layers, while in the alpha/beta band the strongest decrease in AIS can be seen at infragranular layers. Finally, we show that the increase of spectral power at multiple frequencies, in particular at alpha and delta bands in frontal areas, that is often observed during LOC (’anteriorization’) also impacts local information processing—but in a frequency specific way: Increases in isoflurane concentration induced a decrease in AIS in the alpha frequencies, while they increased AIS in the delta frequency range < 2Hz. Thus, the analysis of spectrally-resolved AIS provides valuable additional insights into changes in cortical information processing under anaesthesia. Public Library of Science 2023-01-26 /pmc/articles/PMC9904504/ /pubmed/36701388 http://dx.doi.org/10.1371/journal.pcbi.1010380 Text en © 2023 Pinzuti 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
Pinzuti, Edoardo
Wollstadt, Patricia
Tüscher, Oliver
Wibral, Michael
Information theoretic evidence for layer- and frequency-specific changes in cortical information processing under anesthesia
title Information theoretic evidence for layer- and frequency-specific changes in cortical information processing under anesthesia
title_full Information theoretic evidence for layer- and frequency-specific changes in cortical information processing under anesthesia
title_fullStr Information theoretic evidence for layer- and frequency-specific changes in cortical information processing under anesthesia
title_full_unstemmed Information theoretic evidence for layer- and frequency-specific changes in cortical information processing under anesthesia
title_short Information theoretic evidence for layer- and frequency-specific changes in cortical information processing under anesthesia
title_sort information theoretic evidence for layer- and frequency-specific changes in cortical information processing under anesthesia
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9904504/
https://www.ncbi.nlm.nih.gov/pubmed/36701388
http://dx.doi.org/10.1371/journal.pcbi.1010380
work_keys_str_mv AT pinzutiedoardo informationtheoreticevidenceforlayerandfrequencyspecificchangesincorticalinformationprocessingunderanesthesia
AT wollstadtpatricia informationtheoreticevidenceforlayerandfrequencyspecificchangesincorticalinformationprocessingunderanesthesia
AT tuscheroliver informationtheoreticevidenceforlayerandfrequencyspecificchangesincorticalinformationprocessingunderanesthesia
AT wibralmichael informationtheoreticevidenceforlayerandfrequencyspecificchangesincorticalinformationprocessingunderanesthesia