Cargando…

Dual mechanisms of opioid-induced respiratory depression in the inspiratory rhythm-generating network

The analgesic utility of opioid-based drugs is limited by the life-threatening risk of respiratory depression. Opioid-induced respiratory depression (OIRD), mediated by the μ-opioid receptor (MOR), is characterized by a pronounced decrease in the frequency and regularity of the inspiratory rhythm, w...

Descripción completa

Detalles Bibliográficos
Autores principales: Baertsch, Nathan A, Bush, Nicholas E, Burgraff, Nicholas J, Ramirez, Jan-Marino
Formato: Online Artículo Texto
Lenguaje:English
Publicado: eLife Sciences Publications, Ltd 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8390004/
https://www.ncbi.nlm.nih.gov/pubmed/34402425
http://dx.doi.org/10.7554/eLife.67523
_version_ 1783742996476329984
author Baertsch, Nathan A
Bush, Nicholas E
Burgraff, Nicholas J
Ramirez, Jan-Marino
author_facet Baertsch, Nathan A
Bush, Nicholas E
Burgraff, Nicholas J
Ramirez, Jan-Marino
author_sort Baertsch, Nathan A
collection PubMed
description The analgesic utility of opioid-based drugs is limited by the life-threatening risk of respiratory depression. Opioid-induced respiratory depression (OIRD), mediated by the μ-opioid receptor (MOR), is characterized by a pronounced decrease in the frequency and regularity of the inspiratory rhythm, which originates from the medullary preBötzinger Complex (preBötC). To unravel the cellular- and network-level consequences of MOR activation in the preBötC, MOR-expressing neurons were optogenetically identified and manipulated in transgenic mice in vitro and in vivo. Based on these results, a model of OIRD was developed in silico. We conclude that hyperpolarization of MOR-expressing preBötC neurons alone does not phenocopy OIRD. Instead, the effects of MOR activation are twofold: (1) pre-inspiratory spiking is reduced and (2) excitatory synaptic transmission is suppressed, thereby disrupting network-driven rhythmogenesis. These dual mechanisms of opioid action act synergistically to make the normally robust inspiratory rhythm-generating network particularly prone to collapse when challenged with exogenous opioids.
format Online
Article
Text
id pubmed-8390004
institution National Center for Biotechnology Information
language English
publishDate 2021
publisher eLife Sciences Publications, Ltd
record_format MEDLINE/PubMed
spelling pubmed-83900042021-08-27 Dual mechanisms of opioid-induced respiratory depression in the inspiratory rhythm-generating network Baertsch, Nathan A Bush, Nicholas E Burgraff, Nicholas J Ramirez, Jan-Marino eLife Neuroscience The analgesic utility of opioid-based drugs is limited by the life-threatening risk of respiratory depression. Opioid-induced respiratory depression (OIRD), mediated by the μ-opioid receptor (MOR), is characterized by a pronounced decrease in the frequency and regularity of the inspiratory rhythm, which originates from the medullary preBötzinger Complex (preBötC). To unravel the cellular- and network-level consequences of MOR activation in the preBötC, MOR-expressing neurons were optogenetically identified and manipulated in transgenic mice in vitro and in vivo. Based on these results, a model of OIRD was developed in silico. We conclude that hyperpolarization of MOR-expressing preBötC neurons alone does not phenocopy OIRD. Instead, the effects of MOR activation are twofold: (1) pre-inspiratory spiking is reduced and (2) excitatory synaptic transmission is suppressed, thereby disrupting network-driven rhythmogenesis. These dual mechanisms of opioid action act synergistically to make the normally robust inspiratory rhythm-generating network particularly prone to collapse when challenged with exogenous opioids. eLife Sciences Publications, Ltd 2021-08-17 /pmc/articles/PMC8390004/ /pubmed/34402425 http://dx.doi.org/10.7554/eLife.67523 Text en © 2021, Baertsch et al https://creativecommons.org/licenses/by/4.0/This article is distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use and redistribution provided that the original author and source are credited.
spellingShingle Neuroscience
Baertsch, Nathan A
Bush, Nicholas E
Burgraff, Nicholas J
Ramirez, Jan-Marino
Dual mechanisms of opioid-induced respiratory depression in the inspiratory rhythm-generating network
title Dual mechanisms of opioid-induced respiratory depression in the inspiratory rhythm-generating network
title_full Dual mechanisms of opioid-induced respiratory depression in the inspiratory rhythm-generating network
title_fullStr Dual mechanisms of opioid-induced respiratory depression in the inspiratory rhythm-generating network
title_full_unstemmed Dual mechanisms of opioid-induced respiratory depression in the inspiratory rhythm-generating network
title_short Dual mechanisms of opioid-induced respiratory depression in the inspiratory rhythm-generating network
title_sort dual mechanisms of opioid-induced respiratory depression in the inspiratory rhythm-generating network
topic Neuroscience
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8390004/
https://www.ncbi.nlm.nih.gov/pubmed/34402425
http://dx.doi.org/10.7554/eLife.67523
work_keys_str_mv AT baertschnathana dualmechanismsofopioidinducedrespiratorydepressionintheinspiratoryrhythmgeneratingnetwork
AT bushnicholase dualmechanismsofopioidinducedrespiratorydepressionintheinspiratoryrhythmgeneratingnetwork
AT burgraffnicholasj dualmechanismsofopioidinducedrespiratorydepressionintheinspiratoryrhythmgeneratingnetwork
AT ramirezjanmarino dualmechanismsofopioidinducedrespiratorydepressionintheinspiratoryrhythmgeneratingnetwork