Cargando…

Interoceptive insular cortex participates in sensory processing of gastrointestinal malaise and associated behaviors

The insular cortex plays a central role in the perception and regulation of bodily needs and emotions. Its modular arrangement, corresponding with different sensory modalities, denotes a complex organization, and reveals it to be a hub that is able to coordinate autonomic and behavioral responses to...

Descripción completa

Detalles Bibliográficos
Autores principales: Aguilar-Rivera, Marcelo, Kim, Sanggyun, Coleman, Todd P., Maldonado, Pedro E., Torrealba, Fernando
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7730439/
https://www.ncbi.nlm.nih.gov/pubmed/33303809
http://dx.doi.org/10.1038/s41598-020-78200-w
_version_ 1783621684694089728
author Aguilar-Rivera, Marcelo
Kim, Sanggyun
Coleman, Todd P.
Maldonado, Pedro E.
Torrealba, Fernando
author_facet Aguilar-Rivera, Marcelo
Kim, Sanggyun
Coleman, Todd P.
Maldonado, Pedro E.
Torrealba, Fernando
author_sort Aguilar-Rivera, Marcelo
collection PubMed
description The insular cortex plays a central role in the perception and regulation of bodily needs and emotions. Its modular arrangement, corresponding with different sensory modalities, denotes a complex organization, and reveals it to be a hub that is able to coordinate autonomic and behavioral responses to many types of stimuli. Yet, little is known about the dynamics of its electrical activity at the neuronal level. We recorded single neurons in behaving rats from the posterior insula cortex (pIC), a subdivision considered as a primary interoceptive cortex, during gastrointestinal (GI) malaise, a state akin to the emotion of disgust in humans. We found that a large proportion of pIC neurons were modulated during the rodent compensatory behaviors of lying on belly (LOB) and Pica. Furthermore, we demonstrated that LOB was correlated with low-frequency oscillations in the field potentials and spikes at the theta (8 Hz) band, and that low-frequency electrical microstimulation of pIC elicited LOB and Pica. These findings demonstrate that pIC neurons play a critical role in GI malaise perception, and that the pIC influences the expression of behaviors that alleviate GI malaise. Our model provides an accessible approach at the single cell level to study innate emotional behaviors, currently elusive in humans.
format Online
Article
Text
id pubmed-7730439
institution National Center for Biotechnology Information
language English
publishDate 2020
publisher Nature Publishing Group UK
record_format MEDLINE/PubMed
spelling pubmed-77304392020-12-14 Interoceptive insular cortex participates in sensory processing of gastrointestinal malaise and associated behaviors Aguilar-Rivera, Marcelo Kim, Sanggyun Coleman, Todd P. Maldonado, Pedro E. Torrealba, Fernando Sci Rep Article The insular cortex plays a central role in the perception and regulation of bodily needs and emotions. Its modular arrangement, corresponding with different sensory modalities, denotes a complex organization, and reveals it to be a hub that is able to coordinate autonomic and behavioral responses to many types of stimuli. Yet, little is known about the dynamics of its electrical activity at the neuronal level. We recorded single neurons in behaving rats from the posterior insula cortex (pIC), a subdivision considered as a primary interoceptive cortex, during gastrointestinal (GI) malaise, a state akin to the emotion of disgust in humans. We found that a large proportion of pIC neurons were modulated during the rodent compensatory behaviors of lying on belly (LOB) and Pica. Furthermore, we demonstrated that LOB was correlated with low-frequency oscillations in the field potentials and spikes at the theta (8 Hz) band, and that low-frequency electrical microstimulation of pIC elicited LOB and Pica. These findings demonstrate that pIC neurons play a critical role in GI malaise perception, and that the pIC influences the expression of behaviors that alleviate GI malaise. Our model provides an accessible approach at the single cell level to study innate emotional behaviors, currently elusive in humans. Nature Publishing Group UK 2020-12-10 /pmc/articles/PMC7730439/ /pubmed/33303809 http://dx.doi.org/10.1038/s41598-020-78200-w Text en © The Author(s) 2020 Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/.
spellingShingle Article
Aguilar-Rivera, Marcelo
Kim, Sanggyun
Coleman, Todd P.
Maldonado, Pedro E.
Torrealba, Fernando
Interoceptive insular cortex participates in sensory processing of gastrointestinal malaise and associated behaviors
title Interoceptive insular cortex participates in sensory processing of gastrointestinal malaise and associated behaviors
title_full Interoceptive insular cortex participates in sensory processing of gastrointestinal malaise and associated behaviors
title_fullStr Interoceptive insular cortex participates in sensory processing of gastrointestinal malaise and associated behaviors
title_full_unstemmed Interoceptive insular cortex participates in sensory processing of gastrointestinal malaise and associated behaviors
title_short Interoceptive insular cortex participates in sensory processing of gastrointestinal malaise and associated behaviors
title_sort interoceptive insular cortex participates in sensory processing of gastrointestinal malaise and associated behaviors
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7730439/
https://www.ncbi.nlm.nih.gov/pubmed/33303809
http://dx.doi.org/10.1038/s41598-020-78200-w
work_keys_str_mv AT aguilarriveramarcelo interoceptiveinsularcortexparticipatesinsensoryprocessingofgastrointestinalmalaiseandassociatedbehaviors
AT kimsanggyun interoceptiveinsularcortexparticipatesinsensoryprocessingofgastrointestinalmalaiseandassociatedbehaviors
AT colemantoddp interoceptiveinsularcortexparticipatesinsensoryprocessingofgastrointestinalmalaiseandassociatedbehaviors
AT maldonadopedroe interoceptiveinsularcortexparticipatesinsensoryprocessingofgastrointestinalmalaiseandassociatedbehaviors
AT torrealbafernando interoceptiveinsularcortexparticipatesinsensoryprocessingofgastrointestinalmalaiseandassociatedbehaviors