Experience modulates vicarious freezing in rats: a model for empathy.

The study of the neural basis of emotional empathy has received a surge of interest in recent years but mostly employing human neuroimaging. A simpler animal model would pave the way for systematic single cell recordings and invasive manipulations of the brain regions implicated in empathy. Recent e...

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Autores principales:	Piray Atsak, Marie Orre, Petra Bakker, Leonardo Cerliani, Benno Roozendaal, Valeria Gazzola, Marta Moita, Christian Keysers
Formato:	article
Lenguaje:	EN
Publicado:	Public Library of Science (PLoS) 2011
Materias:	Medicine R Science Q
Acceso en línea:	https://doaj.org/article/6ce8dbe361024a929850cc4a3d077725
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spelling	oai:doaj.org-article:6ce8dbe361024a929850cc4a3d0777252021-11-18T06:50:22ZExperience modulates vicarious freezing in rats: a model for empathy.1932-620310.1371/journal.pone.0021855https://doaj.org/article/6ce8dbe361024a929850cc4a3d0777252011-01-01T00:00:00Zhttps://www.ncbi.nlm.nih.gov/pmc/articles/pmid/21765921/?tool=EBIhttps://doaj.org/toc/1932-6203The study of the neural basis of emotional empathy has received a surge of interest in recent years but mostly employing human neuroimaging. A simpler animal model would pave the way for systematic single cell recordings and invasive manipulations of the brain regions implicated in empathy. Recent evidence has been put forward for the existence of empathy in rodents. In this study, we describe a potential model of empathy in female rats, in which we studied interactions between two rats: a witness observes a demonstrator experiencing a series of footshocks. By comparing the reaction of witnesses with or without previous footshock experience, we examine the role of prior experience as a modulator of empathy. We show that witnesses having previously experienced footshocks, but not naïve ones, display vicarious freezing behavior upon witnessing a cage-mate experiencing footshocks. Strikingly, the demonstrator's behavior was in turn modulated by the behavior of the witness: demonstrators froze more following footshocks if their witness froze more. Previous experiments have shown that rats emit ultrasonic vocalizations (USVs) when receiving footshocks. Thus, the role of USV in triggering vicarious freezing in our paradigm is examined. We found that experienced witness-demonstrator pairs emitted more USVs than naïve witness-demonstrator pairs, but the number of USVs was correlated with freezing in demonstrators, not in witnesses. Furthermore, playing back the USVs, recorded from witness-demonstrator pairs during the empathy test, did not induce vicarious freezing behavior in experienced witnesses. Thus, our findings confirm that vicarious freezing can be triggered in rats, and moreover it can be modulated by prior experience. Additionally, our result suggests that vicarious freezing is not triggered by USVs per se and it influences back onto the behavior of the demonstrator that had elicited the vicarious freezing in witnesses, introducing a paradigm to study empathy as a social loop.Piray AtsakMarie OrrePetra BakkerLeonardo CerlianiBenno RoozendaalValeria GazzolaMarta MoitaChristian KeysersPublic Library of Science (PLoS)articleMedicineRScienceQENPLoS ONE, Vol 6, Iss 7, p e21855 (2011)
institution	DOAJ
collection	DOAJ
language	EN
topic	Medicine R Science Q
spellingShingle	Medicine R Science Q Piray Atsak Marie Orre Petra Bakker Leonardo Cerliani Benno Roozendaal Valeria Gazzola Marta Moita Christian Keysers Experience modulates vicarious freezing in rats: a model for empathy.
description	The study of the neural basis of emotional empathy has received a surge of interest in recent years but mostly employing human neuroimaging. A simpler animal model would pave the way for systematic single cell recordings and invasive manipulations of the brain regions implicated in empathy. Recent evidence has been put forward for the existence of empathy in rodents. In this study, we describe a potential model of empathy in female rats, in which we studied interactions between two rats: a witness observes a demonstrator experiencing a series of footshocks. By comparing the reaction of witnesses with or without previous footshock experience, we examine the role of prior experience as a modulator of empathy. We show that witnesses having previously experienced footshocks, but not naïve ones, display vicarious freezing behavior upon witnessing a cage-mate experiencing footshocks. Strikingly, the demonstrator's behavior was in turn modulated by the behavior of the witness: demonstrators froze more following footshocks if their witness froze more. Previous experiments have shown that rats emit ultrasonic vocalizations (USVs) when receiving footshocks. Thus, the role of USV in triggering vicarious freezing in our paradigm is examined. We found that experienced witness-demonstrator pairs emitted more USVs than naïve witness-demonstrator pairs, but the number of USVs was correlated with freezing in demonstrators, not in witnesses. Furthermore, playing back the USVs, recorded from witness-demonstrator pairs during the empathy test, did not induce vicarious freezing behavior in experienced witnesses. Thus, our findings confirm that vicarious freezing can be triggered in rats, and moreover it can be modulated by prior experience. Additionally, our result suggests that vicarious freezing is not triggered by USVs per se and it influences back onto the behavior of the demonstrator that had elicited the vicarious freezing in witnesses, introducing a paradigm to study empathy as a social loop.
format	article
author	Piray Atsak Marie Orre Petra Bakker Leonardo Cerliani Benno Roozendaal Valeria Gazzola Marta Moita Christian Keysers
author_facet	Piray Atsak Marie Orre Petra Bakker Leonardo Cerliani Benno Roozendaal Valeria Gazzola Marta Moita Christian Keysers
author_sort	Piray Atsak
title	Experience modulates vicarious freezing in rats: a model for empathy.
title_short	Experience modulates vicarious freezing in rats: a model for empathy.
title_full	Experience modulates vicarious freezing in rats: a model for empathy.
title_fullStr	Experience modulates vicarious freezing in rats: a model for empathy.
title_full_unstemmed	Experience modulates vicarious freezing in rats: a model for empathy.
title_sort	experience modulates vicarious freezing in rats: a model for empathy.
publisher	Public Library of Science (PLoS)
publishDate	2011
url	https://doaj.org/article/6ce8dbe361024a929850cc4a3d077725
work_keys_str_mv	AT pirayatsak experiencemodulatesvicariousfreezinginratsamodelforempathy AT marieorre experiencemodulatesvicariousfreezinginratsamodelforempathy AT petrabakker experiencemodulatesvicariousfreezinginratsamodelforempathy AT leonardocerliani experiencemodulatesvicariousfreezinginratsamodelforempathy AT bennoroozendaal experiencemodulatesvicariousfreezinginratsamodelforempathy AT valeriagazzola experiencemodulatesvicariousfreezinginratsamodelforempathy AT martamoita experiencemodulatesvicariousfreezinginratsamodelforempathy AT christiankeysers experiencemodulatesvicariousfreezinginratsamodelforempathy
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Experience modulates vicarious freezing in rats: a model for empathy.

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