Learning and Memory in<i>Drosophila</i>Larvae

Weber, Denise; Richter, Vincent; Rohwedder, Astrid; Großjohann, Alexandra; Thum, Andreas S.

doi:10.1101/pdb.top107863

Cited by 5 publications

(4 citation statements)

References 41 publications

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“…Overall these appetitive results are consistent with the model of associative memory of other stimuli in Drosophila [6, 9, 11, 63], and more generally across other taxa [3, 4, 18].…”

Section: Discussionsupporting

confidence: 86%

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Drosophilalarvae demonstrate associative learning and memory in response to thermal conditioning

Polizos,

Dancausse,

Rios

et al. 2024

Preprint

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Organisms have evolved the ability to detect, process, and respond to many different surrounding stimuli in order to successfully navigate their environments. Sensory experiences can also be stored and referenced in the form of memory. The Drosophila larva is a simple model organism that can store associative memories during classical conditioning, and is well-suited for studying learning and memory at a fundamental level. Much progress has been made in understanding larval learning behavior and the associated neural circuitry for olfactory conditioning, but other sensory systems are relatively unexplored. Here, we investigate memory formation in larvae treated with a temperature-based associative conditioning protocol, pairing normally neutral temperatures with appetitive (fructose, FRU) or aversive (salt, NaCl) stimuli. Associative memory is tested using thermal gradient geometries, and we quantify navigation strength towards or away from conditioned temperatures. We find that larvae demonstrate short-term associative learning. They navigate towards warmer or colder temperatures paired with FRU, and away from warmer temperatures paired with NaCl. These results, especially when combined with future investigations of thermal memory circuitry in larvae, should provide broader insight into how sensory stimuli are encoded and retrieved in insects and more complex systems.

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“…Overall these appetitive results are consistent with the model of associative memory of other stimuli in Drosophila [6, 9, 11, 63], and more generally across other taxa [3, 4, 18].…”

Section: Discussionsupporting

confidence: 86%

“…Overall these appetitive results are consistent with the model of associative memory of other stimuli in Drosophila [6,9,11,63], and more generally across other taxa [3,4,18]. Conditioned IR25a 2 larvae showed no directed movement to conditioned temperatures (Fig.…”

Section: Discussionsupporting

confidence: 86%

Drosophilalarvae demonstrate associative learning and memory in response to thermal conditioning

Polizos,

Dancausse,

Rios

et al. 2024

Preprint

View full text Add to dashboard Cite

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“…First, we preformed detailed analyses of larval locomotion and its modulations in response to previous associative odour-sugar training. Such associative learning experiments are established for about two decades and used in many laboratories [39][40][41][45][46][47]. In brief, groups of larvae were trained to associate an odour with a sugar reward by repeated pairings and subsequently tested with the odour source on one side of the Petri dish.…”

Section: Previous Training Modulates Hc Behaviourmentioning

confidence: 99%

High-resolution analysis of individual Drosophila melanogaster larvae uncovers individual variability in locomotion and its neurogenetic modulation

et al. 2023

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Neuronally orchestrated muscular movement and locomotion are defining faculties of multicellular animals. Due to its simple brain and genetic accessibility, the larva of the fruit fly Drosophila melanogaster allows one to study these processes at tractable levels of complexity. However, although the faculty of locomotion clearly pertains to the individual, most studies of locomotion in larvae use measurements aggregated across animals, or animals tested one by one, an extravagance for larger-scale analyses. This prevents grasping the inter- and intra-individual variability in locomotion and its neurogenetic determinants. Here, we present the IMBA (individual maggot behaviour analyser) for analysing the behaviour of individual larvae within groups, reliably resolving individual identity across collisions. We use the IMBA to systematically describe the inter- and intra-individual variability in locomotion of wild-type animals, and how the variability is reduced by associative learning. We then report a novel locomotion phenotype of an adhesion GPCR mutant. We further investigated the modulation of locomotion across repeated activations of dopamine neurons in individual animals, and the transient backward locomotion induced by brief optogenetic activation of the brain-descending ‘mooncrawler’ neurons. In summary, the IMBA is an easy-to-use toolbox allowing an unprecedentedly rich view of the behaviour and its variability of individual larvae, with utility in multiple biomedical research contexts.

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“…To cope with a constantly changing environment, animals derive benefit from learning behavioral rules that need constant adaptation and updating. To test this ability, researchers often use Pavlovian or classical conditioning experiments (Pavlov 1927), which examine an organism's capacity to form associations between sensory cues, called conditioned stimuli (CS), and rewards or punishments, referred to as aversive and appetitive unconditioned stimuli (US) or teaching signals (Gerber et al 2009, Glanzman 1995, Heisenberg 2003, Menzel 2022, Waddell 2013, Weber et al 2023b, Widmann et al 2018. Dopaminergic neurons (DANs) and other modulatory neurons mediate teaching signals that allow animals to classify a given CS into positive or negative valence based on past experience (Cognigni et al 2018, Menzel 2001, Schultz 2015, Thum & Gerber 2019, Watabe-Uchida et al 2017.…”

Section: Introductionmentioning

confidence: 99%

Four Individually Identified Paired Dopamine Neurons Signal Taste Punishment in LarvalDrosophila

Weber

Vogt

Miroschnikow³

et al. 2023

Preprint

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Dopaminergic neurons (DANs) carry out multiple tasks in the brain, including the transmission of information related to rewards and punishments across various animal species. They are responsible for evaluating sensory input, storing resultant associations as memory, and continuously updating them based on their relevance and reliability. Accurate comprehension of the dopaminergic system's operation necessitates an understanding of the specific functions mediated by individual DANs. To this end, our research employs Drosophila larvae, which possess approximately 12,000 neurons in their brains, of which only around 1% (approximately 120) are DANs. The presynaptic projections to the mushroom body (MB) - a brain region pivotal for associative olfactory learning in insects - are limited to only eight larval dopaminergic neurons. These DANs are further subdivided into two clusters: the primary protocerebral anterior medial cluster (pPAM) comprises four cells, and the dorsolateral 1 cluster (DL1) comprises the remaining four cells. Our findings confirm previous research that demonstrates that the pPAM DANs innervating the MB's medial lobe encode for a gustatory sugar reward signal. Furthermore, we have identified four DANs in the DL1 cluster - DAN-c1, DAN-d1, DAN-f1, and DAN-g1 - each of which innervates distinct compartments of the MB peduncle, lateral appendix, and vertical lobe. Optogenetic activation of DAN-f1 and DAN-g1 alone suffices to substitute for salt punishment. Furthermore, optogenetic inhibition, calcium imaging results and electron microscopy-based reconstruction of all sensory input circuits to the four DL1 DANs demonstrate that each DAN encodes a different aspect of salt punishment, with DAN-g1 being of central importance. To summarize, our investigation has revealed the existence of a cellular division of labor among larval DANs concerning the transmission of dopaminergic reward (pPAM cluster) and punishment signals (DL1 cluster). Individual DANs in each cluster encode for distinct but partially overlapping aspects of the teaching signal. The striking resemblance in the organizing principle of larval DANs with that of its adult counterpart and the mammalian basal ganglion suggests that there may be a limited number of efficient neural circuit solutions available to address more complex cognitive challenges in nature.

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Learning and Memory inDrosophilaLarvae

Cited by 5 publications

References 41 publications

Drosophilalarvae demonstrate associative learning and memory in response to thermal conditioning

Drosophilalarvae demonstrate associative learning and memory in response to thermal conditioning

High-resolution analysis of individual Drosophila melanogaster larvae uncovers individual variability in locomotion and its neurogenetic modulation

Four Individually Identified Paired Dopamine Neurons Signal Taste Punishment in LarvalDrosophila

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