Failure to mate enhances investment in behaviors that may promote mating reward and impairs the ability to cope with stressors via a subpopulation of Neuropeptide F receptor neurons
Living in dynamic environments such as the social domain, where interaction with others determines the reproductive success of individuals, requires the ability to recognize opportunities to obtain natural rewards and cope with challenges that are associated with achieving them. As such, actions tha...
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| Published in: | PLoS genetics Vol. 20; no. 1; p. e1011054 |
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| Main Authors: | , , , , , , , , , , , , |
| Format: | Journal Article |
| Language: | English |
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18-01-2024
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| Abstract | Living in dynamic environments such as the social domain, where interaction with others determines the reproductive success of individuals, requires the ability to recognize opportunities to obtain natural rewards and cope with challenges that are associated with achieving them. As such, actions that promote survival and reproduction are reinforced by the brain reward system, whereas coping with the challenges associated with obtaining these rewards is mediated by stress-response pathways, the activation of which can impair health and shorten lifespan. While much research has been devoted to understanding mechanisms underlying the way by which natural rewards are processed by the reward system, less attention has been given to the consequences of failure to obtain a desirable reward. As a model system to study the impact of failure to obtain a natural reward, we used the well-established courtship suppression paradigm in Drosophila melanogaster as means to induce repeated failures to obtain sexual reward in male flies. We discovered that beyond the known reduction in courtship actions caused by interaction with non-receptive females, repeated failures to mate induce a stress response characterized by persistent motivation to obtain the sexual reward, reduced male-male social interaction, and enhanced aggression. This frustrative-like state caused by the conflict between high motivation to obtain sexual reward and the inability to fulfill their mating drive impairs the capacity of rejected males to tolerate stressors such as starvation and oxidative stress. We further show that sensitivity to starvation and enhanced social arousal is mediated by the disinhibition of a small population of neurons that express receptors for the fly homologue of neuropeptide Y. Our findings demonstrate for the first time the existence of social stress in flies and offers a framework to study mechanisms underlying the crosstalk between reward, stress, and reproduction in a simple nervous system that is highly amenable to genetic manipulation. |
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| AbstractList | Living in dynamic environments such as the social domain, where interaction with others determines the reproductive success of individuals, requires the ability to recognize opportunities to obtain natural rewards and cope with challenges that are associated with achieving them. As such, actions that promote survival and reproduction are reinforced by the brain reward system, whereas coping with the challenges associated with obtaining these rewards is mediated by stress-response pathways, the activation of which can impair health and shorten lifespan. While much research has been devoted to understanding mechanisms underlying the way by which natural rewards are processed by the reward system, less attention has been given to the consequences of failure to obtain a desirable reward. As a model system to study the impact of failure to obtain a natural reward, we used the well-established courtship suppression paradigm in Drosophila melanogaster as means to induce repeated failures to obtain sexual reward in male flies. We discovered that beyond the known reduction in courtship actions caused by interaction with non-receptive females, repeated failures to mate induce a stress response characterized by persistent motivation to obtain the sexual reward, reduced male-male social interaction, and enhanced aggression. This frustrative-like state caused by the conflict between high motivation to obtain sexual reward and the inability to fulfill their mating drive impairs the capacity of rejected males to tolerate stressors such as starvation and oxidative stress. We further show that sensitivity to starvation and enhanced social arousal is mediated by the disinhibition of a small population of neurons that express receptors for the fly homologue of neuropeptide Y. Our findings demonstrate for the first time the existence of social stress in flies and offers a framework to study mechanisms underlying the crosstalk between reward, stress, and reproduction in a simple nervous system that is highly amenable to genetic manipulation. Living in dynamic environments such as the social domain, where interaction with others determines the reproductive success of individuals, requires the ability to recognize opportunities to obtain natural rewards and cope with challenges that are associated with achieving them. As such, actions that promote survival and reproduction are reinforced by the brain reward system, whereas coping with the challenges associated with obtaining these rewards is mediated by stress-response pathways, the activation of which can impair health and shorten lifespan. While much research has been devoted to understanding mechanisms underlying the way by which natural rewards are processed by the reward system, less attention has been given to the consequences of failure to obtain a desirable reward. As a model system to study the impact of failure to obtain a natural reward, we used the well-established courtship suppression paradigm in Drosophila melanogaster as means to induce repeated failures to obtain sexual reward in male flies. We discovered that beyond the known reduction in courtship actions caused by interaction with non-receptive females, repeated failures to mate induce a stress response characterized by persistent motivation to obtain the sexual reward, reduced male-male social interaction, and enhanced aggression. This frustrative-like state caused by the conflict between high motivation to obtain sexual reward and the inability to fulfill their mating drive impairs the capacity of rejected males to tolerate stressors such as starvation and oxidative stress. We further show that sensitivity to starvation and enhanced social arousal is mediated by the disinhibition of a small population of neurons that express receptors for the fly homologue of neuropeptide Y. Our findings demonstrate for the first time the existence of social stress in flies and offers a framework to study mechanisms underlying the crosstalk between reward, stress, and reproduction in a simple nervous system that is highly amenable to genetic manipulation. In this study we investigated the effects of failure to obtain reward on the behavioral actions and physiology of male flies. We exposed Drosophila males to repeated sexual encounters with non-receptive females that rejected their courtship efforts and tested the effect on their behavioral responses using a collection of behavioral paradigms. These responses encompass alterations in social behavior, increased aggression, heightened motivation to mate, and a reduced capacity to cope with stressors. We further show that the high motivational state and sensitivity to stress is mediated by the disinhibition of a small population of neurons that express receptors for the fly homologue of neuropeptide Y. Living in dynamic environments such as the social domain, where interaction with others determines the reproductive success of individuals, requires the ability to recognize opportunities to obtain natural rewards and cope with challenges that are associated with achieving them. As such, actions that promote survival and reproduction are reinforced by the brain reward system, whereas coping with the challenges associated with obtaining these rewards is mediated by stress-response pathways, the activation of which can impair health and shorten lifespan. While much research has been devoted to understanding mechanisms underlying the way by which natural rewards are processed by the reward system, less attention has been given to the consequences of failure to obtain a desirable reward. As a model system to study the impact of failure to obtain a natural reward, we used the well-established courtship suppression paradigm in Drosophila melanogaster as means to induce repeated failures to obtain sexual reward in male flies. We discovered that beyond the known reduction in courtship actions caused by interaction with non-receptive females, repeated failures to mate induce a stress response characterized by persistent motivation to obtain the sexual reward, reduced male-male social interaction, and enhanced aggression. This frustrative-like state caused by the conflict between high motivation to obtain sexual reward and the inability to fulfill their mating drive impairs the capacity of rejected males to tolerate stressors such as starvation and oxidative stress. We further show that sensitivity to starvation and enhanced social arousal is mediated by the disinhibition of a small population of neurons that express receptors for the fly homologue of neuropeptide Y. Our findings demonstrate for the first time the existence of social stress in flies and offers a framework to study mechanisms underlying the crosstalk between reward, stress, and reproduction in a simple nervous system that is highly amenable to genetic manipulation. In this study we investigated the effects of failure to obtain reward on the behavioral actions and physiology of male flies. We exposed Drosophila males to repeated sexual encounters with non-receptive females that rejected their courtship efforts and tested the effect on their behavioral responses using a collection of behavioral paradigms. These responses encompass alterations in social behavior, increased aggression, heightened motivation to mate, and a reduced capacity to cope with stressors. We further show that the high motivational state and sensitivity to stress is mediated by the disinhibition of a small population of neurons that express receptors for the fly homologue of neuropeptide Y. Living in dynamic environments such as the social domain, where interaction with others determines the reproductive success of individuals, requires the ability to recognize opportunities to obtain natural rewards and cope with challenges that are associated with achieving them. As such, actions that promote survival and reproduction are reinforced by the brain reward system, whereas coping with the challenges associated with obtaining these rewards is mediated by stress-response pathways, the activation of which can impair health and shorten lifespan. While much research has been devoted to understanding mechanisms underlying the way by which natural rewards are processed by the reward system, less attention has been given to the consequences of failure to obtain a desirable reward. As a model system to study the impact of failure to obtain a natural reward, we used the well-established courtship suppression paradigm in Drosophila melanogaster as means to induce repeated failures to obtain sexual reward in male flies. We discovered that beyond the known reduction in courtship actions caused by interaction with non-receptive females, repeated failures to mate induce a stress response characterized by persistent motivation to obtain the sexual reward, reduced male-male social interaction, and enhanced aggression. This frustrative-like state caused by the conflict between high motivation to obtain sexual reward and the inability to fulfill their mating drive impairs the capacity of rejected males to tolerate stressors such as starvation and oxidative stress. We further show that sensitivity to starvation and enhanced social arousal is mediated by the disinhibition of a small population of neurons that express receptors for the fly homologue of neuropeptide Y. Our findings demonstrate for the first time the existence of social stress in flies and offers a framework to study mechanisms underlying the crosstalk between reward, stress, and reproduction in a simple nervous system that is highly amenable to genetic manipulation. |
| Audience | Academic |
| Author | Pozeilov, Hadar Heberlein, Ulrike Agranovich, Bella Omesi, Liora Shohat-Ophir, Galit Jacob, Avi Gottlieb, Eyal Abramovich, Ifat Ryvkin, Julia Barak-Buchris, Lital Levi, Mali Nässel, Dick R Kim, Yong-Kyu |
| AuthorAffiliation | 4 The Kanbar scientific equipment center. The Mina & Everard Goodman Faculty of Life Sciences, Bar-Ilan University, Ramat Gan, Israel Geisel School of Medicine at Dartmouth, UNITED STATES 2 Janelia Research Campus, Howard Hughes Medical Institute, Ashburn, Virginia, United States of America 5 Department of Zoology, Stockholm University, Stockholm, Sweden 3 Ruth and Bruce Rappaport Faculty of Medicine, Technion—Israel Institute of Technology, Haifa, Israel 1 The Mina & Everard Goodman Faculty of Life Sciences, The Leslie and Susan Gonda Multidisciplinary Brain Research Center and the Nanotechnology Institute, Bar-Ilan University, Ramat Gan, Israel |
| AuthorAffiliation_xml | – name: 2 Janelia Research Campus, Howard Hughes Medical Institute, Ashburn, Virginia, United States of America – name: 1 The Mina & Everard Goodman Faculty of Life Sciences, The Leslie and Susan Gonda Multidisciplinary Brain Research Center and the Nanotechnology Institute, Bar-Ilan University, Ramat Gan, Israel – name: Geisel School of Medicine at Dartmouth, UNITED STATES – name: 3 Ruth and Bruce Rappaport Faculty of Medicine, Technion—Israel Institute of Technology, Haifa, Israel – name: 4 The Kanbar scientific equipment center. The Mina & Everard Goodman Faculty of Life Sciences, Bar-Ilan University, Ramat Gan, Israel – name: 5 Department of Zoology, Stockholm University, Stockholm, Sweden |
| Author_xml | – sequence: 1 givenname: Julia orcidid: 0000-0002-1172-8350 surname: Ryvkin fullname: Ryvkin, Julia organization: The Mina & Everard Goodman Faculty of Life Sciences, The Leslie and Susan Gonda Multidisciplinary Brain Research Center and the Nanotechnology Institute, Bar-Ilan University, Ramat Gan, Israel – sequence: 2 givenname: Liora surname: Omesi fullname: Omesi, Liora organization: The Mina & Everard Goodman Faculty of Life Sciences, The Leslie and Susan Gonda Multidisciplinary Brain Research Center and the Nanotechnology Institute, Bar-Ilan University, Ramat Gan, Israel – sequence: 3 givenname: Yong-Kyu surname: Kim fullname: Kim, Yong-Kyu organization: Janelia Research Campus, Howard Hughes Medical Institute, Ashburn, Virginia, United States of America – sequence: 4 givenname: Mali surname: Levi fullname: Levi, Mali organization: The Mina & Everard Goodman Faculty of Life Sciences, The Leslie and Susan Gonda Multidisciplinary Brain Research Center and the Nanotechnology Institute, Bar-Ilan University, Ramat Gan, Israel – sequence: 5 givenname: Hadar surname: Pozeilov fullname: Pozeilov, Hadar organization: The Mina & Everard Goodman Faculty of Life Sciences, The Leslie and Susan Gonda Multidisciplinary Brain Research Center and the Nanotechnology Institute, Bar-Ilan University, Ramat Gan, Israel – sequence: 6 givenname: Lital surname: Barak-Buchris fullname: Barak-Buchris, Lital organization: The Mina & Everard Goodman Faculty of Life Sciences, The Leslie and Susan Gonda Multidisciplinary Brain Research Center and the Nanotechnology Institute, Bar-Ilan University, Ramat Gan, Israel – sequence: 7 givenname: Bella surname: Agranovich fullname: Agranovich, Bella organization: Ruth and Bruce Rappaport Faculty of Medicine, Technion-Israel Institute of Technology, Haifa, Israel – sequence: 8 givenname: Ifat surname: Abramovich fullname: Abramovich, Ifat organization: Ruth and Bruce Rappaport Faculty of Medicine, Technion-Israel Institute of Technology, Haifa, Israel – sequence: 9 givenname: Eyal orcidid: 0000-0002-9770-0956 surname: Gottlieb fullname: Gottlieb, Eyal organization: Ruth and Bruce Rappaport Faculty of Medicine, Technion-Israel Institute of Technology, Haifa, Israel – sequence: 10 givenname: Avi orcidid: 0000-0002-0096-9888 surname: Jacob fullname: Jacob, Avi organization: The Kanbar scientific equipment center. The Mina & Everard Goodman Faculty of Life Sciences, Bar-Ilan University, Ramat Gan, Israel – sequence: 11 givenname: Dick R orcidid: 0000-0002-1147-7766 surname: Nässel fullname: Nässel, Dick R organization: Department of Zoology, Stockholm University, Stockholm, Sweden – sequence: 12 givenname: Ulrike surname: Heberlein fullname: Heberlein, Ulrike organization: Janelia Research Campus, Howard Hughes Medical Institute, Ashburn, Virginia, United States of America – sequence: 13 givenname: Galit orcidid: 0000-0003-1246-1827 surname: Shohat-Ophir fullname: Shohat-Ophir, Galit organization: The Mina & Everard Goodman Faculty of Life Sciences, The Leslie and Susan Gonda Multidisciplinary Brain Research Center and the Nanotechnology Institute, Bar-Ilan University, Ramat Gan, Israel |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/38236837$$D View this record in MEDLINE/PubMed https://urn.kb.se/resolve?urn=urn:nbn:se:su:diva-227753$$DView record from Swedish Publication Index |
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| ContentType | Journal Article |
| Copyright | Copyright: © 2024 Ryvkin et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. COPYRIGHT 2024 Public Library of Science 2024 Ryvkin et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License. 2024 Ryvkin et al 2024 Ryvkin et al 2024 Ryvkin et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License. |
| Copyright_xml | – notice: Copyright: © 2024 Ryvkin et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. – notice: COPYRIGHT 2024 Public Library of Science – notice: 2024 Ryvkin et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License. – notice: 2024 Ryvkin et al 2024 Ryvkin et al – notice: 2024 Ryvkin et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License. |
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| License | Copyright: © 2024 Ryvkin et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Creative Commons Attribution License |
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| MergedId | FETCHMERGED-LOGICAL-c713t-f388aa0448bdb294be4571ea20905788fc4be4b8d7d5852600c37fd5d485b94e3 |
| Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 The authors have declared that no competing interests exist. Current address: Department of Neurobiology, Northwestern University, Evanston, Illinois, United States of America |
| ORCID | 0000-0002-9770-0956 0000-0002-1172-8350 0000-0002-1147-7766 0000-0002-0096-9888 0000-0003-1246-1827 |
| OpenAccessLink | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10795991/ |
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| PublicationCentury | 2000 |
| PublicationDate | 2024-01-18 |
| PublicationDateYYYYMMDD | 2024-01-18 |
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| PublicationTitle | PLoS genetics |
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| Title | Failure to mate enhances investment in behaviors that may promote mating reward and impairs the ability to cope with stressors via a subpopulation of Neuropeptide F receptor neurons |
| URI | https://www.ncbi.nlm.nih.gov/pubmed/38236837 https://www.proquest.com/docview/3069179367 https://search.proquest.com/docview/2917559851 https://pubmed.ncbi.nlm.nih.gov/PMC10795991 https://urn.kb.se/resolve?urn=urn:nbn:se:su:diva-227753 https://doaj.org/article/6cf28e82284b4f6b94198bdc9d325c1e http://dx.doi.org/10.1371/journal.pgen.1011054 |
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