Drosophila reward system - A summary of current knowledge

Dvořáček, Jiří; Kodrı́k, Dalibor

doi:10.1016/j.neubiorev.2020.12.032

Cited by 13 publications

(5 citation statements)

References 197 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

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“…Even if one rejects outright the premise that subjective experience requires the hierarchical forward models algorithm, it remains to be explained how insects could possibly generate subjective experience given that there is nothing in their known feedforward-feedback neural circuits, designed as they are to execute motor behaviors, that presupposes consciousness. It is becoming increasingly clear that the more we understand about the neural pathways underlying flexible behaviors in insects, the less likely it is that these behaviors depend on subjective experience ( Dvořáček and Kodrík, 2021 ). Flexible behaviors are readily explained by simple algorithmic rules that transform sensory inputs into motor outputs ( Hein et al, 2020 ; Lee and Wu, 2020 ).…”

Section: Discussionmentioning

confidence: 99%

Neural Design Principles for Subjective Experience: Implications for Insects

Key

Zalucki

Brown

2021

Front. Behav. Neurosci.

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How subjective experience is realized in nervous systems remains one of the great challenges in the natural sciences. An answer to this question should resolve debate about which animals are capable of subjective experience. We contend that subjective experience of sensory stimuli is dependent on the brain’s awareness of its internal neural processing of these stimuli. This premise is supported by empirical evidence demonstrating that disruption to either processing streams or awareness states perturb subjective experience. Given that the brain must predict the nature of sensory stimuli, we reason that conscious awareness is itself dependent on predictions generated by hierarchically organized forward models of the organism’s internal sensory processing. The operation of these forward models requires a specialized neural architecture and hence any nervous system lacking this architecture is unable to subjectively experience sensory stimuli. This approach removes difficulties associated with extrapolations from behavioral and brain homologies typically employed in addressing whether an animal can feel. Using nociception as a model sensation, we show here that the Drosophila brain lacks the required internal neural connectivity to implement the computations required of hierarchical forward models. Consequently, we conclude that Drosophila, and those insects with similar neuroanatomy, do not subjectively experience noxious stimuli and therefore cannot feel pain.

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“…Several studies have shown that a subset of dopaminergic (i.e. DPN-PAM neurons) and octopaminergic neurons are required for learning and retrieval of appetitive memories (Dvořáček and Kodrík;Huetteroth et al, 2015). A recent study reported the presence of octopaminergic, mPNs with inputs in the AL and outputs in the LH (Bates et al, 2020).…”

Section: Mpns Are Sufficient and Required For Appetitive Learningmentioning

confidence: 99%

Olfactory learning modulates a neural circuit mediating innate odor-guided behavior inDrosophila

Campetella,

Huber,

Klappenbach

et al. 2023

Preprint

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Behavior is often categorized as being innate or learned, with the specific circuits being assigned to one of these categories. In Drosophila, neural circuits mediating an innate behavioral response are considered as being 'hard-wired', as activation of these neuronal pathways leads to stereotyped behaviors. However, only a limited number of studies assessed whether innate behaviors and their underlying neural circuits are plastic or show experience-dependent modulation. Here, we show that experience modulates second- order olfactory neurons involved in innate behavioral responses. We focus on the neural circuit defined by multiglomerular projection neurons (mPNs) that target the lateral horn, a structure relevant in the genesis of innate behavior. We show that mPNs, coding for odor attraction, are bidirectionally modulated after olfactory associative learning: when an olfactory stimulus is paired with an aversive electric shock, the activity of these neurons is decreased, while when the odor is paired with a sucrose-reward they are potentiated. We further show that this modulation requires glutamate and serotonin signaling, and that downstream third-order neurons are consequently affected. The bidirectional nature of the plasticity in these neurons is reflected in behavior: silencing mPN activity leads to odor avoidance, while artificial activation induces approach. While output from the mPNs is not required in aversive olfactory conditioning, silencing these neurons during retrieval of appetitive memories leads to a significant memory impairment. Artificially activating these neurons during odor presentation is sufficient to generate a 3 h appetitive memory. Our study in flies shows that a neural circuit coding for innate odor attraction can contribute to learned behavior, is modulated by olfactory learning and can provide reward-like reinforcement.

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Drosophila reward system - A summary of current knowledge

Cited by 13 publications

References 197 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

Neural Design Principles for Subjective Experience: Implications for Insects

Olfactory learning modulates a neural circuit mediating innate odor-guided behavior inDrosophila

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