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Negative energy balance hinders prosocial helping behavior

The internal state of an animal, including homeostatic requirements, modulates its behavior. Negative energy balance stimulates hunger, thus promoting a range of actions aimed at obtaining food. While these survival actions are well established, the influence of the energy status on prosocial behavi...

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Autores principales: Pozo, Macarena, Milà-Guasch, Maria, Haddad-Tóvolli, Roberta, Boudjadja, Mehdi Boutagouga, Chivite, Iñigo, Toledo, Miriam, Gómez-Valadés, Alicia G., Eyre, Elena, Ramírez, Sara, Obri, Arnaud, Ben-Ami Bartal, Inbal, D'Agostino, Giuseppe, Costa-Font, Joan, Claret, Marc
Formato: Online Artículo Texto
Lenguaje:English
Publicado: National Academy of Sciences 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10104524/
https://www.ncbi.nlm.nih.gov/pubmed/37023123
http://dx.doi.org/10.1073/pnas.2218142120
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author Pozo, Macarena
Milà-Guasch, Maria
Haddad-Tóvolli, Roberta
Boudjadja, Mehdi Boutagouga
Chivite, Iñigo
Toledo, Miriam
Gómez-Valadés, Alicia G.
Eyre, Elena
Ramírez, Sara
Obri, Arnaud
Ben-Ami Bartal, Inbal
D'Agostino, Giuseppe
Costa-Font, Joan
Claret, Marc
author_facet Pozo, Macarena
Milà-Guasch, Maria
Haddad-Tóvolli, Roberta
Boudjadja, Mehdi Boutagouga
Chivite, Iñigo
Toledo, Miriam
Gómez-Valadés, Alicia G.
Eyre, Elena
Ramírez, Sara
Obri, Arnaud
Ben-Ami Bartal, Inbal
D'Agostino, Giuseppe
Costa-Font, Joan
Claret, Marc
author_sort Pozo, Macarena
collection PubMed
description The internal state of an animal, including homeostatic requirements, modulates its behavior. Negative energy balance stimulates hunger, thus promoting a range of actions aimed at obtaining food. While these survival actions are well established, the influence of the energy status on prosocial behavior remains unexplored. We developed a paradigm to assess helping behavior in which a free mouse was faced with a conspecific trapped in a restrainer. We measured the willingness of the free mouse to liberate the confined mouse under diverse metabolic conditions. Around 42% of ad libitum–fed mice exhibited a helping behavior, as evidenced by the reduction in the latencies to release the trapped cagemate. This behavior was independent of subsequent social contact reward and was associated with changes in corticosterone indicative of emotional contagion. This decision-making process was coupled with reduced blood glucose excursions and higher Adenosine triphosphate (ATP):Adenosine diphosphate (ADP) ratios in the forebrain of helper mice, suggesting that it was a highly energy-demanding process. Interestingly, chronic (food restriction and type 2 diabetes) and acute (chemogenetic activation of hunger-promoting AgRP neurons) situations mimicking organismal negative energy balance and enhanced appetite attenuated helping behavior toward a distressed conspecific. To investigate similar effects in humans, we estimated the influence of glycated hemoglobin (a surrogate of long-term glycemic control) on prosocial behavior (namely charity donation) using the Understanding Society dataset. Our results evidenced that organismal energy status markedly influences helping behavior and that hypothalamic AgRP neurons are at the interface of metabolism and prosocial behavior.
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spelling pubmed-101045242023-10-06 Negative energy balance hinders prosocial helping behavior Pozo, Macarena Milà-Guasch, Maria Haddad-Tóvolli, Roberta Boudjadja, Mehdi Boutagouga Chivite, Iñigo Toledo, Miriam Gómez-Valadés, Alicia G. Eyre, Elena Ramírez, Sara Obri, Arnaud Ben-Ami Bartal, Inbal D'Agostino, Giuseppe Costa-Font, Joan Claret, Marc Proc Natl Acad Sci U S A Biological Sciences The internal state of an animal, including homeostatic requirements, modulates its behavior. Negative energy balance stimulates hunger, thus promoting a range of actions aimed at obtaining food. While these survival actions are well established, the influence of the energy status on prosocial behavior remains unexplored. We developed a paradigm to assess helping behavior in which a free mouse was faced with a conspecific trapped in a restrainer. We measured the willingness of the free mouse to liberate the confined mouse under diverse metabolic conditions. Around 42% of ad libitum–fed mice exhibited a helping behavior, as evidenced by the reduction in the latencies to release the trapped cagemate. This behavior was independent of subsequent social contact reward and was associated with changes in corticosterone indicative of emotional contagion. This decision-making process was coupled with reduced blood glucose excursions and higher Adenosine triphosphate (ATP):Adenosine diphosphate (ADP) ratios in the forebrain of helper mice, suggesting that it was a highly energy-demanding process. Interestingly, chronic (food restriction and type 2 diabetes) and acute (chemogenetic activation of hunger-promoting AgRP neurons) situations mimicking organismal negative energy balance and enhanced appetite attenuated helping behavior toward a distressed conspecific. To investigate similar effects in humans, we estimated the influence of glycated hemoglobin (a surrogate of long-term glycemic control) on prosocial behavior (namely charity donation) using the Understanding Society dataset. Our results evidenced that organismal energy status markedly influences helping behavior and that hypothalamic AgRP neurons are at the interface of metabolism and prosocial behavior. National Academy of Sciences 2023-04-06 2023-04-11 /pmc/articles/PMC10104524/ /pubmed/37023123 http://dx.doi.org/10.1073/pnas.2218142120 Text en Copyright © 2023 the Author(s). Published by PNAS. https://creativecommons.org/licenses/by-nc-nd/4.0/This 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
Pozo, Macarena
Milà-Guasch, Maria
Haddad-Tóvolli, Roberta
Boudjadja, Mehdi Boutagouga
Chivite, Iñigo
Toledo, Miriam
Gómez-Valadés, Alicia G.
Eyre, Elena
Ramírez, Sara
Obri, Arnaud
Ben-Ami Bartal, Inbal
D'Agostino, Giuseppe
Costa-Font, Joan
Claret, Marc
Negative energy balance hinders prosocial helping behavior
title Negative energy balance hinders prosocial helping behavior
title_full Negative energy balance hinders prosocial helping behavior
title_fullStr Negative energy balance hinders prosocial helping behavior
title_full_unstemmed Negative energy balance hinders prosocial helping behavior
title_short Negative energy balance hinders prosocial helping behavior
title_sort negative energy balance hinders prosocial helping behavior
topic Biological Sciences
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10104524/
https://www.ncbi.nlm.nih.gov/pubmed/37023123
http://dx.doi.org/10.1073/pnas.2218142120
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