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A prefrontal-bed nucleus of the stria terminalis circuit limits fear to uncertain threat

In many cases of trauma, the same environmental stimuli that become associated with aversive events are experienced on other occasions without adverse consequence. We examined neural circuits underlying partially reinforced fear (PRF), whereby mice received tone-shock pairings on half of conditionin...

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Autores principales: Glover, Lucas R, McFadden, Kerry M, Bjorni, Max, Smith, Sawyer R, Rovero, Natalie G, Oreizi-Esfahani, Sarvar, Yoshida, Takayuki, Postle, Abagail F, Nonaka, Mio, Halladay, Lindsay R, Holmes, Andrew
Formato: Online Artículo Texto
Lenguaje:English
Publicado: eLife Sciences Publications, Ltd 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7899651/
https://www.ncbi.nlm.nih.gov/pubmed/33319747
http://dx.doi.org/10.7554/eLife.60812
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author Glover, Lucas R
McFadden, Kerry M
Bjorni, Max
Smith, Sawyer R
Rovero, Natalie G
Oreizi-Esfahani, Sarvar
Yoshida, Takayuki
Postle, Abagail F
Nonaka, Mio
Halladay, Lindsay R
Holmes, Andrew
author_facet Glover, Lucas R
McFadden, Kerry M
Bjorni, Max
Smith, Sawyer R
Rovero, Natalie G
Oreizi-Esfahani, Sarvar
Yoshida, Takayuki
Postle, Abagail F
Nonaka, Mio
Halladay, Lindsay R
Holmes, Andrew
author_sort Glover, Lucas R
collection PubMed
description In many cases of trauma, the same environmental stimuli that become associated with aversive events are experienced on other occasions without adverse consequence. We examined neural circuits underlying partially reinforced fear (PRF), whereby mice received tone-shock pairings on half of conditioning trials. Tone-elicited freezing was lower after PRF conditioning than fully reinforced fear (FRF) conditioning, despite an equivalent number of tone-shock pairings. PRF preferentially activated medial prefrontal cortex (mPFC) and bed nucleus of the stria terminalis (BNST). Chemogenetic inhibition of BNST-projecting mPFC neurons increased PRF, not FRF, freezing. Multiplexing chemogenetics with in vivo neuronal recordings showed elevated infralimbic cortex (IL) neuronal activity during CS onset and freezing cessation; these neural correlates were abolished by chemogenetic mPFC→BNST inhibition. These data suggest that mPFC→BNST neurons limit fear to threats with a history of partial association with an aversive stimulus, with potential implications for understanding the neural basis of trauma-related disorders.
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spelling pubmed-78996512021-02-24 A prefrontal-bed nucleus of the stria terminalis circuit limits fear to uncertain threat Glover, Lucas R McFadden, Kerry M Bjorni, Max Smith, Sawyer R Rovero, Natalie G Oreizi-Esfahani, Sarvar Yoshida, Takayuki Postle, Abagail F Nonaka, Mio Halladay, Lindsay R Holmes, Andrew eLife Neuroscience In many cases of trauma, the same environmental stimuli that become associated with aversive events are experienced on other occasions without adverse consequence. We examined neural circuits underlying partially reinforced fear (PRF), whereby mice received tone-shock pairings on half of conditioning trials. Tone-elicited freezing was lower after PRF conditioning than fully reinforced fear (FRF) conditioning, despite an equivalent number of tone-shock pairings. PRF preferentially activated medial prefrontal cortex (mPFC) and bed nucleus of the stria terminalis (BNST). Chemogenetic inhibition of BNST-projecting mPFC neurons increased PRF, not FRF, freezing. Multiplexing chemogenetics with in vivo neuronal recordings showed elevated infralimbic cortex (IL) neuronal activity during CS onset and freezing cessation; these neural correlates were abolished by chemogenetic mPFC→BNST inhibition. These data suggest that mPFC→BNST neurons limit fear to threats with a history of partial association with an aversive stimulus, with potential implications for understanding the neural basis of trauma-related disorders. eLife Sciences Publications, Ltd 2020-12-15 /pmc/articles/PMC7899651/ /pubmed/33319747 http://dx.doi.org/10.7554/eLife.60812 Text en http://creativecommons.org/publicdomain/zero/1.0/ http://creativecommons.org/publicdomain/zero/1.0/This is an open-access article, free of all copyright, and may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. The work is made available under the Creative Commons CC0 public domain dedication (http://creativecommons.org/publicdomain/zero/1.0/) .
spellingShingle Neuroscience
Glover, Lucas R
McFadden, Kerry M
Bjorni, Max
Smith, Sawyer R
Rovero, Natalie G
Oreizi-Esfahani, Sarvar
Yoshida, Takayuki
Postle, Abagail F
Nonaka, Mio
Halladay, Lindsay R
Holmes, Andrew
A prefrontal-bed nucleus of the stria terminalis circuit limits fear to uncertain threat
title A prefrontal-bed nucleus of the stria terminalis circuit limits fear to uncertain threat
title_full A prefrontal-bed nucleus of the stria terminalis circuit limits fear to uncertain threat
title_fullStr A prefrontal-bed nucleus of the stria terminalis circuit limits fear to uncertain threat
title_full_unstemmed A prefrontal-bed nucleus of the stria terminalis circuit limits fear to uncertain threat
title_short A prefrontal-bed nucleus of the stria terminalis circuit limits fear to uncertain threat
title_sort prefrontal-bed nucleus of the stria terminalis circuit limits fear to uncertain threat
topic Neuroscience
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7899651/
https://www.ncbi.nlm.nih.gov/pubmed/33319747
http://dx.doi.org/10.7554/eLife.60812
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