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Maternal separation modifies spontaneous synaptic activity in the infralimbic cortex of stress-resilient male rats

Glutamate and GABA signaling systems are necessary to maintain proper function of the central nervous system through excitation/inhibition (E/I) balance. Alteration of this balance in the medial prefrontal cortex (mPFC), as an effect of early-life stress, may lead to the development of anxiety and d...

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Autores principales: Ayala-Rodríguez, Jesús David, García-Colunga, Jesús
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10635473/
https://www.ncbi.nlm.nih.gov/pubmed/37943747
http://dx.doi.org/10.1371/journal.pone.0294151
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author Ayala-Rodríguez, Jesús David
García-Colunga, Jesús
author_facet Ayala-Rodríguez, Jesús David
García-Colunga, Jesús
author_sort Ayala-Rodríguez, Jesús David
collection PubMed
description Glutamate and GABA signaling systems are necessary to maintain proper function of the central nervous system through excitation/inhibition (E/I) balance. Alteration of this balance in the medial prefrontal cortex (mPFC), as an effect of early-life stress, may lead to the development of anxiety and depressive disorders. Few studies exist in the infralimbic division of the mPFC to understand the effect of early-life stress at different ages, which is the purpose of the present work. Newborn Sprague Dawley male rats were subjected to maternal separation (MS) for two weeks. First, tests measuring anxiety- and depression-like behaviors were performed on adolescent and adult rats subjected to MS (MS-rats). Then, to establish a relationship with behavioral results, electrophysiological recordings were performed in neurons of the infralimbic cortex in acute brain slices of infant, adolescent, and adult rats. In the behavioral tests, there were no significant differences in MS-rats compared to control rats at any age. Moreover, MS had no effect on the passive membrane properties nor neuronal excitability in the infralimbic cortex, whereas spontaneous synaptic activity in infralimbic neurons was altered. The frequency of spontaneous glutamatergic synaptic events increased in infant MS-rats, whereas in adolescent MS-rats both the frequency and the amplitude of spontaneous GABAergic events increased without any effect on glutamatergic synaptic responses. In adult MS-rats, these two parameters decreased in spontaneous GABAergic synaptic events, whereas only the frequency of glutamatergic events decreased. These data suggest that rats subjected to MS did not exhibit behavioral changes and presented an age-dependent E/I imbalance in the infralimbic cortex, possibly due to differential changes in neurotransmitter release and/or receptor expression.
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spelling pubmed-106354732023-11-10 Maternal separation modifies spontaneous synaptic activity in the infralimbic cortex of stress-resilient male rats Ayala-Rodríguez, Jesús David García-Colunga, Jesús PLoS One Research Article Glutamate and GABA signaling systems are necessary to maintain proper function of the central nervous system through excitation/inhibition (E/I) balance. Alteration of this balance in the medial prefrontal cortex (mPFC), as an effect of early-life stress, may lead to the development of anxiety and depressive disorders. Few studies exist in the infralimbic division of the mPFC to understand the effect of early-life stress at different ages, which is the purpose of the present work. Newborn Sprague Dawley male rats were subjected to maternal separation (MS) for two weeks. First, tests measuring anxiety- and depression-like behaviors were performed on adolescent and adult rats subjected to MS (MS-rats). Then, to establish a relationship with behavioral results, electrophysiological recordings were performed in neurons of the infralimbic cortex in acute brain slices of infant, adolescent, and adult rats. In the behavioral tests, there were no significant differences in MS-rats compared to control rats at any age. Moreover, MS had no effect on the passive membrane properties nor neuronal excitability in the infralimbic cortex, whereas spontaneous synaptic activity in infralimbic neurons was altered. The frequency of spontaneous glutamatergic synaptic events increased in infant MS-rats, whereas in adolescent MS-rats both the frequency and the amplitude of spontaneous GABAergic events increased without any effect on glutamatergic synaptic responses. In adult MS-rats, these two parameters decreased in spontaneous GABAergic synaptic events, whereas only the frequency of glutamatergic events decreased. These data suggest that rats subjected to MS did not exhibit behavioral changes and presented an age-dependent E/I imbalance in the infralimbic cortex, possibly due to differential changes in neurotransmitter release and/or receptor expression. Public Library of Science 2023-11-09 /pmc/articles/PMC10635473/ /pubmed/37943747 http://dx.doi.org/10.1371/journal.pone.0294151 Text en © 2023 Ayala-Rodríguez, García-Colunga 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
Ayala-Rodríguez, Jesús David
García-Colunga, Jesús
Maternal separation modifies spontaneous synaptic activity in the infralimbic cortex of stress-resilient male rats
title Maternal separation modifies spontaneous synaptic activity in the infralimbic cortex of stress-resilient male rats
title_full Maternal separation modifies spontaneous synaptic activity in the infralimbic cortex of stress-resilient male rats
title_fullStr Maternal separation modifies spontaneous synaptic activity in the infralimbic cortex of stress-resilient male rats
title_full_unstemmed Maternal separation modifies spontaneous synaptic activity in the infralimbic cortex of stress-resilient male rats
title_short Maternal separation modifies spontaneous synaptic activity in the infralimbic cortex of stress-resilient male rats
title_sort maternal separation modifies spontaneous synaptic activity in the infralimbic cortex of stress-resilient male rats
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10635473/
https://www.ncbi.nlm.nih.gov/pubmed/37943747
http://dx.doi.org/10.1371/journal.pone.0294151
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