Multimodal cues displayed by submissive rats promote prosocial choices by dominants

Animals often display prosocial behaviors, performing actions that benefit others. Although prosociality is essential for social bonding and cooperation, we still know little about how animals integrate behavioral cues from those in need to make decisions that increase their well-being. To address t...

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Autores: Munyua Gachomba, Michael Joe, Esteve-Agraz, Joan, Caref, Kevin, Sanz Maroto, Aroa, Bortolozzo-Gleich, Maria Helena, Laplagne, Diego Andrés, Márquez, Cristina
Tipo de recurso: artículo
Estado:Versión publicada
Fecha de publicación:2022
País:España
Institución:Consejo Superior de Investigaciones Científicas (CSIC)
Repositorio:DIGITAL.CSIC. Repositorio Institucional del CSIC
OAI Identifier:oai:digital.csic.es:10261/306785
Acceso en línea:http://hdl.handle.net/10261/306785
Access Level:acceso abierto
Palabra clave:Social behavior
Social decision-making
Social hierarchies
Prosociality
Empathy
Behavioral synchrony
Ultrasonic vocalizations
Body language
Other-regarding
Sex differences
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spelling Multimodal cues displayed by submissive rats promote prosocial choices by dominantsMunyua Gachomba, Michael JoeEsteve-Agraz, JoanCaref, KevinSanz Maroto, AroaBortolozzo-Gleich, Maria HelenaLaplagne, Diego AndrésMárquez, CristinaSocial behaviorSocial decision-makingSocial hierarchiesProsocialityEmpathyBehavioral synchronyUltrasonic vocalizationsBody languageOther-regardingSex differencesAnimals often display prosocial behaviors, performing actions that benefit others. Although prosociality is essential for social bonding and cooperation, we still know little about how animals integrate behavioral cues from those in need to make decisions that increase their well-being. To address this question, we used a two-choice task where rats can provide rewards to a conspecific in the absence of self-benefit and investigated which conditions promote prosociality by manipulating the social context of the interacting animals. Although sex or degree of familiarity did not affect prosocial choices in rats, social hierarchy revealed to be a potent modulator, with dominant decision-makers showing faster emergence and higher levels of prosocial choices toward their submissive cage mates. Leveraging quantitative analysis of multimodal social dynamics prior to choice, we identified that pairs with dominant decision-makers exhibited more proximal interactions. Interestingly, these closer interactions were driven by submissive animals that modulated their position and movement following their dominants and whose 50-kHz vocalization rate correlated with dominants’ prosociality. Moreover, Granger causality revealed stronger bidirectional influences in pairs with dominant focals and submissive recipients, indicating increased behavioral coordination. Finally, multivariate analysis highlighted body language as the main information dominants use on a trial-by-trial basis to learn that their actions have effects on others. Our results provide a refined understanding of the behavioral dynamics that rats use for action-selection upon perception of socially relevant cues and navigate social decision-making.This work was supported by the NARSAD Young Investigator Grant from the Brain & Behavior Research Foundation (grant 26478 to C.M.), Fundaçao Bial (250/16 to C.M.), and the Spanish Agency of Research (grant RTI2018-097843-B-100 to C.M.). M.J.M.G. was supported by “la Caixa” Foundation (ID 100010434), under the agreement LCF/BQ/DI17/11620002, and by Fondazione Ing. Aldo Gini. D.A.L. received a travel grant from the Carolina Foundation in the context of this collaboration.Peer reviewedElsevierBrain and Behavior Research FoundationBIAL FoundationMinisterio de Ciencia, Innovación y Universidades (España)Agencia Estatal de Investigación (España)Fundación CarolinaFundación la CaixaConsejo Superior de Investigaciones Científicas [https://ror.org/02gfc7t72]202320232022info:eu-repo/semantics/articlehttp://purl.org/coar/resource_type/c_6501Publisher's versioninfo:eu-repo/semantics/publishedVersionapplication/pdfhttp://hdl.handle.net/10261/306785reponame:DIGITAL.CSIC. Repositorio Institucional del CSICinstname:Consejo Superior de Investigaciones Científicas (CSIC)Inglés#PLACEHOLDER_PARENT_METADATA_VALUE#info:eu-repo/grantAgreement/AEI/Plan Estatal de Investigación Científica y Técnica y de Innovación 2017-2020/RTI2018-097843-B-I00Current BiologyThe underlying dataset has been published as supplementary material of the article in the publisher platform at DOI 10.1016/j.cub.2022.06.026https://doi.org/10.1016/j.cub.2022.06.026Síinfo:eu-repo/semantics/openAccessoai:digital.csic.es:10261/3067852026-05-22T06:33:51Z
dc.title.none.fl_str_mv Multimodal cues displayed by submissive rats promote prosocial choices by dominants
title Multimodal cues displayed by submissive rats promote prosocial choices by dominants
spellingShingle Multimodal cues displayed by submissive rats promote prosocial choices by dominants
Munyua Gachomba, Michael Joe
Social behavior
Social decision-making
Social hierarchies
Prosociality
Empathy
Behavioral synchrony
Ultrasonic vocalizations
Body language
Other-regarding
Sex differences
title_short Multimodal cues displayed by submissive rats promote prosocial choices by dominants
title_full Multimodal cues displayed by submissive rats promote prosocial choices by dominants
title_fullStr Multimodal cues displayed by submissive rats promote prosocial choices by dominants
title_full_unstemmed Multimodal cues displayed by submissive rats promote prosocial choices by dominants
title_sort Multimodal cues displayed by submissive rats promote prosocial choices by dominants
dc.creator.none.fl_str_mv Munyua Gachomba, Michael Joe
Esteve-Agraz, Joan
Caref, Kevin
Sanz Maroto, Aroa
Bortolozzo-Gleich, Maria Helena
Laplagne, Diego Andrés
Márquez, Cristina
author Munyua Gachomba, Michael Joe
author_facet Munyua Gachomba, Michael Joe
Esteve-Agraz, Joan
Caref, Kevin
Sanz Maroto, Aroa
Bortolozzo-Gleich, Maria Helena
Laplagne, Diego Andrés
Márquez, Cristina
author_role author
author2 Esteve-Agraz, Joan
Caref, Kevin
Sanz Maroto, Aroa
Bortolozzo-Gleich, Maria Helena
Laplagne, Diego Andrés
Márquez, Cristina
author2_role author
author
author
author
author
author
dc.contributor.none.fl_str_mv Brain and Behavior Research Foundation
BIAL Foundation
Ministerio de Ciencia, Innovación y Universidades (España)
Agencia Estatal de Investigación (España)
Fundación Carolina
Fundación la Caixa
Consejo Superior de Investigaciones Científicas [https://ror.org/02gfc7t72]
dc.subject.none.fl_str_mv Social behavior
Social decision-making
Social hierarchies
Prosociality
Empathy
Behavioral synchrony
Ultrasonic vocalizations
Body language
Other-regarding
Sex differences
topic Social behavior
Social decision-making
Social hierarchies
Prosociality
Empathy
Behavioral synchrony
Ultrasonic vocalizations
Body language
Other-regarding
Sex differences
description Animals often display prosocial behaviors, performing actions that benefit others. Although prosociality is essential for social bonding and cooperation, we still know little about how animals integrate behavioral cues from those in need to make decisions that increase their well-being. To address this question, we used a two-choice task where rats can provide rewards to a conspecific in the absence of self-benefit and investigated which conditions promote prosociality by manipulating the social context of the interacting animals. Although sex or degree of familiarity did not affect prosocial choices in rats, social hierarchy revealed to be a potent modulator, with dominant decision-makers showing faster emergence and higher levels of prosocial choices toward their submissive cage mates. Leveraging quantitative analysis of multimodal social dynamics prior to choice, we identified that pairs with dominant decision-makers exhibited more proximal interactions. Interestingly, these closer interactions were driven by submissive animals that modulated their position and movement following their dominants and whose 50-kHz vocalization rate correlated with dominants’ prosociality. Moreover, Granger causality revealed stronger bidirectional influences in pairs with dominant focals and submissive recipients, indicating increased behavioral coordination. Finally, multivariate analysis highlighted body language as the main information dominants use on a trial-by-trial basis to learn that their actions have effects on others. Our results provide a refined understanding of the behavioral dynamics that rats use for action-selection upon perception of socially relevant cues and navigate social decision-making.
publishDate 2022
dc.date.none.fl_str_mv 2022
2023
2023
dc.type.none.fl_str_mv info:eu-repo/semantics/article
http://purl.org/coar/resource_type/c_6501
Publisher's version
info:eu-repo/semantics/publishedVersion
format article
status_str publishedVersion
dc.identifier.none.fl_str_mv http://hdl.handle.net/10261/306785
url http://hdl.handle.net/10261/306785
dc.language.none.fl_str_mv Inglés
language_invalid_str_mv Inglés
dc.relation.none.fl_str_mv #PLACEHOLDER_PARENT_METADATA_VALUE#
info:eu-repo/grantAgreement/AEI/Plan Estatal de Investigación Científica y Técnica y de Innovación 2017-2020/RTI2018-097843-B-I00
Current Biology
The underlying dataset has been published as supplementary material of the article in the publisher platform at DOI 10.1016/j.cub.2022.06.026
https://doi.org/10.1016/j.cub.2022.06.026

dc.rights.none.fl_str_mv info:eu-repo/semantics/openAccess
eu_rights_str_mv openAccess
dc.format.none.fl_str_mv application/pdf
dc.publisher.none.fl_str_mv Elsevier
publisher.none.fl_str_mv Elsevier
dc.source.none.fl_str_mv reponame:DIGITAL.CSIC. Repositorio Institucional del CSIC
instname:Consejo Superior de Investigaciones Científicas (CSIC)
instname_str Consejo Superior de Investigaciones Científicas (CSIC)
reponame_str DIGITAL.CSIC. Repositorio Institucional del CSIC
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