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Rats respond to aversive emotional arousal of human handlers with the activation of the basolateral and central amygdala

Reading danger signals may save an animal’s life, and learning about threats from others allows avoiding first-hand aversive and often fatal experiences. Fear expressed by other individuals, including those belonging to other species, may indicate the presence of a threat in the environment and is a...

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Autores principales: Kaźmierowska, Anna M., Kostecki, Mateusz, Szczepanik, Michał, Nikolaev, Tomasz, Hamed, Adam, Michałowski, Jarosław M., Wypych, Marek, Marchewka, Artur, Knapska, Ewelina
Formato: Online Artículo Texto
Lenguaje:English
Publicado: National Academy of Sciences 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10655214/
https://www.ncbi.nlm.nih.gov/pubmed/37934822
http://dx.doi.org/10.1073/pnas.2302655120
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author Kaźmierowska, Anna M.
Kostecki, Mateusz
Szczepanik, Michał
Nikolaev, Tomasz
Hamed, Adam
Michałowski, Jarosław M.
Wypych, Marek
Marchewka, Artur
Knapska, Ewelina
author_facet Kaźmierowska, Anna M.
Kostecki, Mateusz
Szczepanik, Michał
Nikolaev, Tomasz
Hamed, Adam
Michałowski, Jarosław M.
Wypych, Marek
Marchewka, Artur
Knapska, Ewelina
author_sort Kaźmierowska, Anna M.
collection PubMed
description Reading danger signals may save an animal’s life, and learning about threats from others allows avoiding first-hand aversive and often fatal experiences. Fear expressed by other individuals, including those belonging to other species, may indicate the presence of a threat in the environment and is an important social cue. Humans and other animals respond to conspecifics’ fear with increased activity of the amygdala, the brain structure crucial for detecting threats and mounting an appropriate response to them. It is unclear, however, whether the cross-species transmission of threat information involves similar mechanisms, e.g., whether animals respond to the aversively induced emotional arousal of humans with activation of fear-processing circuits in the brain. Here, we report that when rats interact with a human caregiver who had recently undergone fear conditioning, they show risk assessment behavior and enhanced amygdala activation. The amygdala response involves its two major parts, the basolateral and central, which detect a threat and orchestrate defensive responses. Further, we show that humans who learn about a threat by observing another aversively aroused human, similar to rats, activate the basolateral and centromedial parts of the amygdala. Our results demonstrate that rats detect the emotional arousal of recently aversively stimulated caregivers and suggest that cross-species social transmission of threat information may involve similar neural circuits in the amygdala as the within-species transmission.
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spelling pubmed-106552142023-11-07 Rats respond to aversive emotional arousal of human handlers with the activation of the basolateral and central amygdala Kaźmierowska, Anna M. Kostecki, Mateusz Szczepanik, Michał Nikolaev, Tomasz Hamed, Adam Michałowski, Jarosław M. Wypych, Marek Marchewka, Artur Knapska, Ewelina Proc Natl Acad Sci U S A Biological Sciences Reading danger signals may save an animal’s life, and learning about threats from others allows avoiding first-hand aversive and often fatal experiences. Fear expressed by other individuals, including those belonging to other species, may indicate the presence of a threat in the environment and is an important social cue. Humans and other animals respond to conspecifics’ fear with increased activity of the amygdala, the brain structure crucial for detecting threats and mounting an appropriate response to them. It is unclear, however, whether the cross-species transmission of threat information involves similar mechanisms, e.g., whether animals respond to the aversively induced emotional arousal of humans with activation of fear-processing circuits in the brain. Here, we report that when rats interact with a human caregiver who had recently undergone fear conditioning, they show risk assessment behavior and enhanced amygdala activation. The amygdala response involves its two major parts, the basolateral and central, which detect a threat and orchestrate defensive responses. Further, we show that humans who learn about a threat by observing another aversively aroused human, similar to rats, activate the basolateral and centromedial parts of the amygdala. Our results demonstrate that rats detect the emotional arousal of recently aversively stimulated caregivers and suggest that cross-species social transmission of threat information may involve similar neural circuits in the amygdala as the within-species transmission. National Academy of Sciences 2023-11-07 2023-11-14 /pmc/articles/PMC10655214/ /pubmed/37934822 http://dx.doi.org/10.1073/pnas.2302655120 Text en Copyright © 2023 the Author(s). Published by PNAS. https://creativecommons.org/licenses/by-nc-nd/4.0/This open access article is distributed under Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND) (https://creativecommons.org/licenses/by-nc-nd/4.0/) .
spellingShingle Biological Sciences
Kaźmierowska, Anna M.
Kostecki, Mateusz
Szczepanik, Michał
Nikolaev, Tomasz
Hamed, Adam
Michałowski, Jarosław M.
Wypych, Marek
Marchewka, Artur
Knapska, Ewelina
Rats respond to aversive emotional arousal of human handlers with the activation of the basolateral and central amygdala
title Rats respond to aversive emotional arousal of human handlers with the activation of the basolateral and central amygdala
title_full Rats respond to aversive emotional arousal of human handlers with the activation of the basolateral and central amygdala
title_fullStr Rats respond to aversive emotional arousal of human handlers with the activation of the basolateral and central amygdala
title_full_unstemmed Rats respond to aversive emotional arousal of human handlers with the activation of the basolateral and central amygdala
title_short Rats respond to aversive emotional arousal of human handlers with the activation of the basolateral and central amygdala
title_sort rats respond to aversive emotional arousal of human handlers with the activation of the basolateral and central amygdala
topic Biological Sciences
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10655214/
https://www.ncbi.nlm.nih.gov/pubmed/37934822
http://dx.doi.org/10.1073/pnas.2302655120
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