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Audible pain squeaks can mediate emotional contagion across pre-exposed rats with a potential effect of auto-conditioning

Footshock self-experience enhances rodents’ reactions to the distress of others. Here, we tested one potential mechanism supporting this phenomenon, namely that animals auto-condition to their own pain squeaks during shock pre-exposure. In Experiment 1, shock pre-exposure increased freezing and 22 k...

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Autores principales: Packheiser, Julian, Soyman, Efe, Paradiso, Enrica, Michon, Frédéric, Ramaaker, Eline, Sahin, Neslihan, Muralidharan, Sharmistha, Wöhr, Markus, Gazzola, Valeria, Keysers, Christian
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10600148/
https://www.ncbi.nlm.nih.gov/pubmed/37880354
http://dx.doi.org/10.1038/s42003-023-05474-x
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author Packheiser, Julian
Soyman, Efe
Paradiso, Enrica
Michon, Frédéric
Ramaaker, Eline
Sahin, Neslihan
Muralidharan, Sharmistha
Wöhr, Markus
Gazzola, Valeria
Keysers, Christian
author_facet Packheiser, Julian
Soyman, Efe
Paradiso, Enrica
Michon, Frédéric
Ramaaker, Eline
Sahin, Neslihan
Muralidharan, Sharmistha
Wöhr, Markus
Gazzola, Valeria
Keysers, Christian
author_sort Packheiser, Julian
collection PubMed
description Footshock self-experience enhances rodents’ reactions to the distress of others. Here, we tested one potential mechanism supporting this phenomenon, namely that animals auto-condition to their own pain squeaks during shock pre-exposure. In Experiment 1, shock pre-exposure increased freezing and 22 kHz distress vocalizations while animals listened to the audible pain-squeaks of others. In Experiment 2 and 3, to test the auto-conditioning theory, we weakened the noxious pre-exposure stimulus not to trigger pain squeaks, and compared pre-exposure protocols in which we paired it with squeak playback against unpaired control conditions. Although all animals later showed fear responses to squeak playbacks, these were weaker than following typical pre-exposure (Experiment 1) and not stronger following paired than unpaired pre-exposure. Experiment 1 thus demonstrates the relevance of audible pain squeaks in the transmission of distress but Experiment 2 and 3 highlight the difficulty to test auto-conditioning: stimuli weak enough to decouple pain experience from hearing self-emitted squeaks are too weak to trigger the experience-dependent increase in fear transmission that we aimed to study. Although our results do not contradict the auto-conditioning hypothesis, they fail to disentangle it from sensitization effects. Future studies could temporarily deafen animals during pre-exposure to further test this hypothesis.
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spelling pubmed-106001482023-10-27 Audible pain squeaks can mediate emotional contagion across pre-exposed rats with a potential effect of auto-conditioning Packheiser, Julian Soyman, Efe Paradiso, Enrica Michon, Frédéric Ramaaker, Eline Sahin, Neslihan Muralidharan, Sharmistha Wöhr, Markus Gazzola, Valeria Keysers, Christian Commun Biol Article Footshock self-experience enhances rodents’ reactions to the distress of others. Here, we tested one potential mechanism supporting this phenomenon, namely that animals auto-condition to their own pain squeaks during shock pre-exposure. In Experiment 1, shock pre-exposure increased freezing and 22 kHz distress vocalizations while animals listened to the audible pain-squeaks of others. In Experiment 2 and 3, to test the auto-conditioning theory, we weakened the noxious pre-exposure stimulus not to trigger pain squeaks, and compared pre-exposure protocols in which we paired it with squeak playback against unpaired control conditions. Although all animals later showed fear responses to squeak playbacks, these were weaker than following typical pre-exposure (Experiment 1) and not stronger following paired than unpaired pre-exposure. Experiment 1 thus demonstrates the relevance of audible pain squeaks in the transmission of distress but Experiment 2 and 3 highlight the difficulty to test auto-conditioning: stimuli weak enough to decouple pain experience from hearing self-emitted squeaks are too weak to trigger the experience-dependent increase in fear transmission that we aimed to study. Although our results do not contradict the auto-conditioning hypothesis, they fail to disentangle it from sensitization effects. Future studies could temporarily deafen animals during pre-exposure to further test this hypothesis. Nature Publishing Group UK 2023-10-25 /pmc/articles/PMC10600148/ /pubmed/37880354 http://dx.doi.org/10.1038/s42003-023-05474-x Text en © The Author(s) 2023 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
Packheiser, Julian
Soyman, Efe
Paradiso, Enrica
Michon, Frédéric
Ramaaker, Eline
Sahin, Neslihan
Muralidharan, Sharmistha
Wöhr, Markus
Gazzola, Valeria
Keysers, Christian
Audible pain squeaks can mediate emotional contagion across pre-exposed rats with a potential effect of auto-conditioning
title Audible pain squeaks can mediate emotional contagion across pre-exposed rats with a potential effect of auto-conditioning
title_full Audible pain squeaks can mediate emotional contagion across pre-exposed rats with a potential effect of auto-conditioning
title_fullStr Audible pain squeaks can mediate emotional contagion across pre-exposed rats with a potential effect of auto-conditioning
title_full_unstemmed Audible pain squeaks can mediate emotional contagion across pre-exposed rats with a potential effect of auto-conditioning
title_short Audible pain squeaks can mediate emotional contagion across pre-exposed rats with a potential effect of auto-conditioning
title_sort audible pain squeaks can mediate emotional contagion across pre-exposed rats with a potential effect of auto-conditioning
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10600148/
https://www.ncbi.nlm.nih.gov/pubmed/37880354
http://dx.doi.org/10.1038/s42003-023-05474-x
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