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Basal and Stress-Induced Network Activity in the Adrenal Medulla In Vivo

The adrenal medulla plays a critical role in mammalian homeostasis and the stress response. It is populated by clustered chromaffin cells that secrete epinephrine or norepinephrine along with peptides into the bloodstream affecting distant target organs. Despite been heavily studied, the central con...

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Autores principales: Lopez Ruiz, Jose R., Ernst, Stephen A., Holz, Ronald W., Stuenkel, Edward L.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9250985/
https://www.ncbi.nlm.nih.gov/pubmed/35795145
http://dx.doi.org/10.3389/fendo.2022.875865
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author Lopez Ruiz, Jose R.
Ernst, Stephen A.
Holz, Ronald W.
Stuenkel, Edward L.
author_facet Lopez Ruiz, Jose R.
Ernst, Stephen A.
Holz, Ronald W.
Stuenkel, Edward L.
author_sort Lopez Ruiz, Jose R.
collection PubMed
description The adrenal medulla plays a critical role in mammalian homeostasis and the stress response. It is populated by clustered chromaffin cells that secrete epinephrine or norepinephrine along with peptides into the bloodstream affecting distant target organs. Despite been heavily studied, the central control of adrenal medulla and in-situ spatiotemporal responsiveness remains poorly understood. For this work, we continuously monitored the electrical activity of individual adrenomedullary chromaffin cells in the living anesthetized rat using multielectrode arrays. We measured the chromaffin cell activity under basal and physiological stress conditions and characterized the functional micro-architecture of the adrenal medulla. Under basal conditions, chromaffin cells fired action potentials with frequencies between ~0.2 and 4 Hz. Activity was almost completely driven by sympathetic inputs coming through the splanchnic nerve. Chromaffin cells were organized into independent local networks in which cells fired in a specific order, with latencies from hundreds of microseconds to a few milliseconds. Electrical stimulation of the splanchnic nerve evoked almost exactly the same spatiotemporal firing patterns that occurred spontaneously. Hypoglycemic stress, induced by insulin administration resulted in increased activity of a subset of the chromaffin cells. In contrast, respiratory arrest induced by lethal anesthesia resulted in an increase in the activity of virtually all chromaffin cells before cessation of all activity. These results suggest a stressor-specific activation of adrenomedullary chromaffin cell networks and revealed a surprisingly complex electrical organization that likely reflects the dynamic nature of the adrenal medulla’s neuroendocrine output during basal conditions and during different types of physiological stress.
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spelling pubmed-92509852022-07-05 Basal and Stress-Induced Network Activity in the Adrenal Medulla In Vivo Lopez Ruiz, Jose R. Ernst, Stephen A. Holz, Ronald W. Stuenkel, Edward L. Front Endocrinol (Lausanne) Endocrinology The adrenal medulla plays a critical role in mammalian homeostasis and the stress response. It is populated by clustered chromaffin cells that secrete epinephrine or norepinephrine along with peptides into the bloodstream affecting distant target organs. Despite been heavily studied, the central control of adrenal medulla and in-situ spatiotemporal responsiveness remains poorly understood. For this work, we continuously monitored the electrical activity of individual adrenomedullary chromaffin cells in the living anesthetized rat using multielectrode arrays. We measured the chromaffin cell activity under basal and physiological stress conditions and characterized the functional micro-architecture of the adrenal medulla. Under basal conditions, chromaffin cells fired action potentials with frequencies between ~0.2 and 4 Hz. Activity was almost completely driven by sympathetic inputs coming through the splanchnic nerve. Chromaffin cells were organized into independent local networks in which cells fired in a specific order, with latencies from hundreds of microseconds to a few milliseconds. Electrical stimulation of the splanchnic nerve evoked almost exactly the same spatiotemporal firing patterns that occurred spontaneously. Hypoglycemic stress, induced by insulin administration resulted in increased activity of a subset of the chromaffin cells. In contrast, respiratory arrest induced by lethal anesthesia resulted in an increase in the activity of virtually all chromaffin cells before cessation of all activity. These results suggest a stressor-specific activation of adrenomedullary chromaffin cell networks and revealed a surprisingly complex electrical organization that likely reflects the dynamic nature of the adrenal medulla’s neuroendocrine output during basal conditions and during different types of physiological stress. Frontiers Media S.A. 2022-06-20 /pmc/articles/PMC9250985/ /pubmed/35795145 http://dx.doi.org/10.3389/fendo.2022.875865 Text en Copyright © 2022 Lopez Ruiz, Ernst, Holz and Stuenkel 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 Endocrinology
Lopez Ruiz, Jose R.
Ernst, Stephen A.
Holz, Ronald W.
Stuenkel, Edward L.
Basal and Stress-Induced Network Activity in the Adrenal Medulla In Vivo
title Basal and Stress-Induced Network Activity in the Adrenal Medulla In Vivo
title_full Basal and Stress-Induced Network Activity in the Adrenal Medulla In Vivo
title_fullStr Basal and Stress-Induced Network Activity in the Adrenal Medulla In Vivo
title_full_unstemmed Basal and Stress-Induced Network Activity in the Adrenal Medulla In Vivo
title_short Basal and Stress-Induced Network Activity in the Adrenal Medulla In Vivo
title_sort basal and stress-induced network activity in the adrenal medulla in vivo
topic Endocrinology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9250985/
https://www.ncbi.nlm.nih.gov/pubmed/35795145
http://dx.doi.org/10.3389/fendo.2022.875865
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