Differential coding of absolute and relative aversive value in the Drosophila brain

Villar, María Eugenia; Pavão-Delgado, Miguel; Amigo, Marie; Jacob, Pedro F.; Merabet, Nesrine; Pinot, Anthony; Perry, Sophie A; Waddell, Scott; Perisse, Emmanuel

doi:10.1016/j.cub.2022.08.058

Cited by 25 publications

(22 citation statements)

References 102 publications

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“…KCs synapse onto MBONs, which guide action by signaling the valence of an odor i.e. it’s attractive/repulsive quality, rather than a specific action(31, 56, 62). KC-MBON synapses are modified by a plasticity rule that depends on the coincident activity of odor-representing KCs and release of dopamine by reward-signaling DANs (33, 34, 51, 55–58, 60, 88, 94) (Fig.…”

Section: Resultsmentioning

confidence: 99%

“…Over the last half century, researchers have shown that flies can learn a wide variety of Pavlovian associations between cues and rewards(27–38). With the help of advances in functional and anatomical tools(39–45), they have identified the mushroom body (MB) as the neural substrate for these learning processes, including the assignment of value to sensory cues, and the underlying plasticity mechanisms have been extensively characterized(46–62). Recent theoretical work has also attempted to formalize the features of the learning rule that is mediated by these plasticity mechanisms(63–67).…”

Section: Introductionmentioning

confidence: 99%

“…Over the last half century, researchers have shown that flies can learn a wide variety of Pavlovian associations between cues and rewards (27)(28)(29)(30)(31)(32)(33)(34)(35)(36)(37)(38). With the help of advances in functional and anatomical tools (39)(40)(41)(42)(43)(44)(45), they have identified the mushroom body (MB) as the neural substrate for these learning processes, including the assignment of value to sensory cues, and the underlying plasticity mechanisms have been extensively characterized (46)(47)(48)(49)(50)(51)(52)(53)(54)(55)(56)(57)(58)(59)(60)(61)(62).…”

Section: Introductionmentioning

confidence: 99%

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Reward expectations direct learning and drive operant matching inDrosophila

Rajagopalan

Darshan

Fitzgerald

et al. 2022

Preprint

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Foraging animals must use decision-making strategies that dynamically account for uncertainty in the world. To cope with this uncertainty, animals have developed strikingly convergent strategies that use information about multiple past choices and reward to learn representations of the current state of the world. However, the underlying learning rules that drive the required learning have remained unclear. Here, working in the relatively simple nervous system of Drosophila, we combine behavioral measurements, mathematical modeling, and neural circuit perturbations to show that dynamic foraging depends on a learning rule incorporating reward expectation. Using a novel olfactory dynamic foraging task, we characterize the behavioral strategies used by individual flies when faced with unpredictable rewards and show, for the first time, that they perform operant matching. We build on past theoretical work and demonstrate that this strategy requires the existence of a covariance-based learning rule in the mushroom body - a hub for learning in the fly. In particular, the behavioral consequences of optogenetic perturbation experiments suggest that this learning rule incorporates reward expectation. Our results identify a key element of the algorithm underlying dynamic foraging in flies and suggest a comprehensive mechanism that could be fundamental to these behaviors across species.

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Section: Resultsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

See 1 more Smart Citation

Reward expectations direct learning and drive operant matching inDrosophila

Rajagopalan

Darshan

Fitzgerald

et al. 2022

Preprint

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“…Previous studies have shown that olfactory memory performance exhibits a ceiling effect when associated with a 1-minute odor and 12-time 60-volt electric shocks. 19 , 50 , 51 We further investigated whether the lack of significant differences in 3-minute and 1-hour memory enhancement between the mixed feeding and single strain feeding groups was due to the ceiling effect. We employed a milder training protocol for subsequent experiments in which flies were trained to associate a 1-minute odor with only three occurrences of 40-volt electric shocks.…”

Section: Resultsmentioning

confidence: 99%

Probiotic Lactobacillus spp. improves Drosophila memory by increasing lactate dehydrogenase levels in the brain mushroom body neurons

Ho,

Tsai,

Lai

et al. 2024

Gut Microbes

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Probiotics are live microorganisms that offer potential benefits to their hosts and can occasionally influence behavioral responses. However, the detailed mechanisms by which probiotics affect the behavior of their hosts and the underlying biogenic effects remain unclear. Lactic acid bacteria, specifically Lactobacillus spp. are known probiotics. Drosophila melanogaster , commonly known as the fruit fly, is a well-established model organism for investigating the interaction between the host and gut microbiota in translational research. Herein, we showed that 5-day administration of Lactobacillus acidophilus (termed GMNL-185) or Lacticaseibacillus rhamnosus (termed GMNL-680) enhances olfactory-associative memory in Drosophila . Moreover, a combined diet of GMNL-185 and GMNL-680 demonstrated synergistic effects on memory functions. Live brain imaging revealed a significant increase in calcium responses to the training odor in the mushroom body β and γ lobes of flies that underwent mixed feeding with GMNL-185 and GMNL-680. Quantitative reverse transcription polymerase chain reaction (qRT-PCR) and whole-mount brain immunohistochemistry revealed significant upregulation of lactate dehydrogenase (LDH) expression in the fly brain following the mixed feeding. Notably, the genetic knockdown of Ldh in neurons, specifically in mushroom body, ameliorated the beneficial effects of mixed feeding with GMNL-185 and GMNL-680 on memory improvement. Altogether, our results demonstrate that supplementation with L. acidophilus and L. rhamnosus enhances memory functions in flies by increasing brain LDH levels.

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“…These types of neurons respond to the presence of rewards [13][14][15][16][17][18] as well as punishments [18][19][20][21][22] in the environment and the electrical stimulation or optogenetic activation of DANs induces approach or avoidance both in vertebrates [23][24][25][26] and invertebrates [6,22,[27][28][29][30][31]. Ultimately DANs do not only signal the presence of rewards or punishments but have also been suggested to encode PE in various vertebrate species [19,[32][33][34][35] and might have a similar function in insects [3,18,22,[36][37][38].…”

Section: Introductionmentioning

confidence: 99%

Prediction error drives associative olfactory learning and conditioned behavior in a spiking model ofDrosophila larva

Jürgensen

Sakagiannis

Schleyer

et al. 2022

Preprint

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Predicting positive or negative reinforcement from environmental clues is essential to guide decision making and goal-directed behavior. In insect brains the mushroom body is a central structure for learning such valuable associations between sensory signals and reinforcement. We propose a biologically realistic spiking network model of the Drosophila larval olfactory pathway for the association of odors and reinforcement to bias behavior towards either approach or avoidance. We demonstrate that prediction error coding through integration of present and expected reinforcement in dopaminergic neurons can serve as a driving force in learning that can, combined with synaptic homeostasis, account for the experimentally observed features of acquisition and extinction of associations that depend on the intensity of odor and reward, as well as temporal features of the odor/reward pairing. To allow for a direct comparison of our simulation results with behavioral data we model learning-induced plasticity over the full time course of behavioral experiments and simulate locomotion of individual larvae towards or away from odor sources in a virtual environment.

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Differential coding of absolute and relative aversive value in the Drosophila brain

Cited by 25 publications

References 102 publications

Reward expectations direct learning and drive operant matching inDrosophila

Reward expectations direct learning and drive operant matching inDrosophila

Probiotic Lactobacillus spp. improves Drosophila memory by increasing lactate dehydrogenase levels in the brain mushroom body neurons

Prediction error drives associative olfactory learning and conditioned behavior in a spiking model ofDrosophila larva

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