Behavioral features of motivated response to alcohol in<i>Drosophila</i>

Jl, Catalano; N, Mei; Azanchi, Reza; Song, Sophia; Blackwater, Tyler; Heberlein, Ulrike; Kr, Kaun

doi:10.1101/2020.02.17.953026

Cited by 3 publications

(2 citation statements)

References 28 publications

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“…Similar responses to social stress and reward-seeking behaviors can be seen in a variety of animals, suggesting that the central systems facilitating survival and reproduction originated early in evolution and that similar ancient basic building blocks mediate these processes [ 41 , 42 ]. In agreement with this concept, we and others showed that Drosophila melanogaster can adjust its behavior and physiology to various social conditions [ 43 – 55 ] and that the brains of mammals and fruit flies share similar principles in encoding stress and reward [ 43 , 56 – 58 ]. For example, the fly homologue of the NPY signaling system (i.e., NPY and its receptor) functions in processing natural and drug rewards, decreases aggressive behaviors and suppresses responses to aversive stimuli such as harsh physical environments [ 43 , 59 – 69 ].…”

Section: Introductionsupporting

confidence: 71%

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

Ryvkin,

Omesi,

Kim

et al. 2024

PLoS Genet

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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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Section: Introductionsupporting

confidence: 71%

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

Ryvkin,

Omesi,

Kim

et al. 2024

PLoS Genet

Self Cite

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“…In agreement with this concept, we and others showed that Drosophila melanogaster display the ability to adjust their behavior and physiology to various changes in their social environment [40][41][42][43][44][45][46][47][48][49][50][51][52] . Moreover, recent studies provided evidence that the brains of mammals and fruit flies share similar principles when it comes to encoding stress and reward 40,[53][54][55] . The homologs for NPY and CRF in Drosophila are Neuropeptide F (NPF) and Diuretic hormone 44 (Dh44), respectively [56][57][58] .…”

Section: Introductionmentioning

confidence: 99%

Sexual deprivation induces a CRF independent stress response and decreases resistance to stressors inDrosophilavia a subpopulation of Neuropeptide F receptor-expressing neurons

Ryvkin

Shmueli

Levi

et al. 2022

Preprint

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Living in a changing environment composed of other behaving animals entails both opportunities and challenges to obtain resources and mating partners. Actions that promote survival and reproduction are reinforced by the brain reward systems, whereas coping with the challenges associated with obtaining these rewards are mediated by stress response pathways. The activation of the latter can impair health and shorten lifespan. Although similar responses to social opportunity and challenge exist across the animal kingdom, little is known about the mechanisms that process reward and stress under different social conditions. Here, we studied the interplay between deprivation of sexual reward and stress response in Drosophila melanogaster and discovered that repeated failures to obtain sexual reward induces a frustration-like state that is characterized by increased arousal, persistent sexual motivation, and impaired ability to cope with starvation and oxidative stressors. We show that this increased arousal and sensitivity to starvation is mediated by disinhibition of neurons that express receptors for the fly homologue of neuropeptide Y (neuropeptide F, NPF). We furthermore demonstrate the existence of an anatomical overlap between stress and reward systems in the fly brain in the form of neurons that co-express receptors for NPF (NPFR) and the corticotropin-releasing factor (CRF)-like homologue Diuretic hormone 44 (Dh44), and that deprivation of sexual reward leads to translocation of forkhead box-subgroup O (FoxO) to the cytoplasm in these neurons. Nevertheless, the activity of Dh44 neurons alone does not mediate sensitivity to starvation and aroused behavior following sexual deprivation, instead, these responses are mediated by disinhibition of ~12-16 NPFR-expressing neurons via a dynamin-independent synaptic signaling mechanism, suggesting the existence of a NPFR mediated stress pathway which is Dh44-independent. This paves the path for using simple model organisms to dissect mechanisms behind anticipation of reward, and more specifically, to determine what happens when expectations to obtain natural and drug rewards are not met.

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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

Omesi

Levi

Bentzur³

et al. 2021

Preprint

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In highly polyandrous species, where females mate with multiple males within a single fertility period, there is typically a high level of sperm competition. To cope with this challenge, males apply various behavioral and physiological strategies to maximize their paternity rates. Previous studies in Drosophila melanogaster established a link between the composition of the social environment and the reproductive success of individual male flies. While most studies until now focused on the adaptive responses of male flies to the presence of rival males, little is known about whether the outcomes of sexual interactions with female partners affect male-male social interactions in a competitive environment such as the social group. Here we show that repeated failures to mate promote a coordinated physiological and behavioral responses that can serve to increase paternity chances over mating rivals. We exposed male flies to sexual deprivation or successful mating and analyzed the behavioral repertoires of individuals within groups and the structure of their emerging social networks. We discovered that failures to mate and successful mating generate distinct emergent group interactions and structures, where sexually deprived males form low density social networks and actively minimize their encounters with other group members, while increasing their aggressive behavior. In addition, sexually deprived male flies elevate the production of seminal fluid proteins (known to facilitate post-mating responses in females) and extend mating duration upon mating with receptive females, altogether leading to reduced re-mating rates. Our results demonstrate the existence of a flexible mating strategy that may provide a short-term fitness advantage over competing rivals and pave the path for using simple model organisms to dissect the neurobiology of social plasticity as coping strategy to living in a highly dynamic environment as the social domain.

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Behavioral features of motivated response to alcohol inDrosophila

Cited by 3 publications

References 28 publications

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

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

Sexual deprivation induces a CRF independent stress response and decreases resistance to stressors inDrosophilavia a subpopulation of Neuropeptide F receptor-expressing neurons

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

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