Avoidance of Heat and Attraction to Optogenetically Induced Sugar Sensation as Operant Behavior in Adult<i>Drosophila</i>

Nuwal, Nidhi; Stock, Patrick; Hiemeyer, Jochen; Schmid, Benjamin; Fiala, André; Buchner, Erich

doi:10.3109/01677063.2012.700266

Cited by 13 publications

(11 citation statements)

References 42 publications

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“…Previous work has demonstrated that the PER can be elicited with ChR2-wt when high light intensities are used (6.5 mW/mm 2 at 480 nm) and flies are starved before the experiment (30). Both ChR2-T159C and ChR2-XXL triggered a PER in satiated flies using considerably lower light intensities (Fig.…”

Section: Significancementioning

confidence: 99%

Channelrhodopsin-2–XXL, a powerful optogenetic tool for low-light applications

Dawydow

Gueta

Ljaschenko

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

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Channelrhodopsin-2 (ChR2) has provided a breakthrough for the optogenetic control of neuronal activity. In adult Drosophila melanogaster, however, its applications are severely constrained. This limitation in a powerful model system has curtailed unfolding the full potential of ChR2 for behavioral neuroscience. Here, we describe the D156C mutant, termed ChR2-XXL (extra high expression and long open state), which displays increased expression, improved subcellular localization, elevated retinal affinity, an extended open-state lifetime, and photocurrent amplitudes greatly exceeding those of all heretofore published ChR variants. As a result, neuronal activity could be efficiently evoked with ambient light and even without retinal supplementation. We validated the benefits of the variant in intact flies by eliciting simple and complex behaviors. We demonstrate efficient and prolonged photostimulation of monosynaptic transmission at the neuromuscular junction and reliable activation of a gustatory reflex pathway. Innate male courtship was triggered in male and female flies, and olfactory memories were written through light-induced associative training.

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Section: Significancementioning

confidence: 99%

Channelrhodopsin-2–XXL, a powerful optogenetic tool for low-light applications

Dawydow

Gueta

Ljaschenko

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

Self Cite

185

235

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“…Although visual place learning has been demonstrated in freely walking flies in 2D environments [43], studies of visual conditioning in head-fixed flies have relied on 1D environments in which flies are trained to avoid aversive heat by orienting toward certain visual cues [61]. Our paradigm relied on optogenetically stimulating heat sensing neurons, but the detailed knowledge of —and genetic access to— sensory and reinforcement pathways in Drosophila should permit the generation of other “virtual” sensory stimuli using optogenetics [35, 62, 63]. Using optogenetically-generated virtual stimuli offers significant advantages for experimental design by enabling the creation of sensations in flies that might otherwise affect their state of health (for example, heat, which can physically damage a fly’s body, or sugar, which might satiate it).…”

Section: Discussionmentioning

confidence: 99%

On the adaptive behavior of head-fixed flies navigating in two-dimensional, visual virtual reality

Haberkern

Basnak

Ahanonu

et al. 2018

Preprint

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A navigating animal’s sensory experience is shaped not just by its surroundings, but by its movements within them, which in turn are influenced by its past experiences. Studying the intertwined roles of sensation, experience and directed action in navigation has been made easier by the development of virtual reality (VR) environments for head-fixed animals, which allow for quantitative measurements of behavior in well-controlled sensory conditions. VR has long featured in studies of Drosophila melanogaster, but these experiments have typically relied on one-dimensional (1D) VR, effectively allowing the fly to change only its heading in a visual scene, and not its position. Here we explore how flies navigate in a two-dimensional (2D) visual VR environment that more closely resembles their experience during free behavior. We show that flies’ interaction with landmarks in 2D environments cannot be automatically derived from their behavior in simpler 1D environments. Using a novel paradigm, we then demonstrate that flies in 2D VR adapt their behavior in a visual environment in response to optogenetically delivered appetitive and aversive stimuli. Much like free-walking flies after encounters with food, head-fixed flies respond to optogenetic activation of sugar-sensing neurons by initiating a local search behavior. Finally, by pairing optogenetic activation of heat-sensing cells to the flies’ presence near visual landmarks of specific shapes, we elicit selective learned avoidance of landmarks associated with aversive “virtual heat”. These head-fixed paradigms set the stage for an interrogation of fly brain circuitry underlying flexible navigation in complex visual environments.

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“…Surprisingly, in the fruit fly behavioural field probabilistic reward foraging decision making tasks are missing. Although pavlovian and operant tasks have been extensively used in the fruit fly learning field [48][49][50], these studies do not typically control the value on a continuous scale. Different from learning paradigms, the manipulation of value is necessary to understand what decision variables drive animals' choices on a trial by trial basis.…”

Section: Plos Onementioning

confidence: 99%

Reward foraging task and model-based analysis reveal how fruit flies learn value of available options

et al. 2020

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Foraging animals have to evaluate, compare and select food patches in order to increase their fitness. Understanding what drives foraging decisions requires careful manipulation of the value of alternative options while monitoring animals choices. Value-based decisionmaking tasks in combination with formal learning models have provided both an experimental and theoretical framework to study foraging decisions in lab settings. While these approaches were successfully used in the past to understand what drives choices in mammals, very little work has been done on fruit flies. This is despite the fact that fruit flies have served as model organism for many complex behavioural paradigms. To fill this gap we developed a single-animal, trial-based decision making task, where freely walking flies experienced optogenetic sugar-receptor neuron stimulation. We controlled the value of available options by manipulating the probabilities of optogenetic stimulation. We show that flies integrate reward history of chosen options and forget value of unchosen options. We further discover that flies assign higher values to rewards experienced early in the behavioural session, consistent with formal reinforcement learning models. Finally, we also show that the probabilistic rewards affect walking trajectories of flies, suggesting that accumulated value is controlling the navigation vector of flies in a graded fashion. These findings establish the fruit fly as a model organism to explore the genetic and circuit basis of reward foraging decisions.

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Avoidance of Heat and Attraction to Optogenetically Induced Sugar Sensation as Operant Behavior in AdultDrosophila

Cited by 13 publications

References 42 publications

Channelrhodopsin-2–XXL, a powerful optogenetic tool for low-light applications

Channelrhodopsin-2–XXL, a powerful optogenetic tool for low-light applications

On the adaptive behavior of head-fixed flies navigating in two-dimensional, visual virtual reality

Reward foraging task and model-based analysis reveal how fruit flies learn value of available options

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