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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...
Autores principales: | , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
Nature Publishing Group UK
2020
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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 |
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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 |
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