Social facilitation of long-lasting memory is mediated by CO2 in Drosophila

Muria, Aurélie; Musso, Pierre-Yves; Durrieu, Matthias; Portugal, Felipe Ramón; Ronsin, Brice; Gordon, Michael D.; Jeanson, Raphaël; Isabel, Guillaume

doi:10.1016/j.cub.2021.02.044

Cited by 15 publications

(8 citation statements)

References 53 publications

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“…We hypothesized blocking KC synaptic output could alter PKA activity signaling measured by PKA-SPARK::GFP puncta localization. To test effects of output connectivity on PKA activity, we used the temperature-sensitive shibire ts allele ( Koenig et al, 1983 ; Kitamoto, 2001 ), which is frequently employed to block neurotransmission ( Jacob et al, 2021 ; Muria et al, 2021 ). At restrictive temperatures (>29°C), shibire ts is defective in SV recycling, and semi-dominant over wild type ( Koenig et al, 1983 ; Kitamoto, 2001 ).…”

Section: Resultsmentioning

confidence: 99%

Temporally and Spatially Localized PKA Activity within Learning and Memory Circuitry Regulated by Network Feedback

Sears

Broadie

2022

eNeuro

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Dynamic functional connectivity within brain circuits requires coordination of intercellular signaling and intracellular signal transduction. Critical roles for cAMP-dependent protein kinase A (PKA) signaling are well established in the Drosophila mushroom body (MB) learning and memory circuitry, but local PKA activity within this well-mapped neuronal network is uncharacterized. Here, we use an in vivo PKA activity sensor (PKA-SPARK) to test spatiotemporal regulatory requirements in the MB axon lobes. We find immature animals have little detectable PKA activity, whereas postcritical period adults show high field-selective activation primarily in just 3/16 defined output regions. In addition to the age-dependent PKA activity in distinct α’/β’ lobe nodes, females show sex-dependent elevation compared with males in these same restricted regions. Loss of neural cell body Fragile X mental retardation protein (FMRP) and Rugose [human Neurobeachin (NBEA)] suppresses localized PKA activity, whereas overexpression (OE) of MB lobe PKA-synergist Meng-Po (human SBK1) promotes PKA activity. Elevated Meng-Po subverts the PKA age-dependence, with elevated activity in immature animals, and spatial-restriction, with striking γ lobe activity. Testing circuit signaling requirements with temperature-sensitive shibire (human Dynamin) blockade, we find broadly expanded PKA activity within the MB lobes. Using transgenic tetanus toxin to block MB synaptic output, we find greatly heightened PKA activity in virtually all MB lobe fields, although the age-dependence is maintained. We conclude spatiotemporally restricted PKA activity signaling within this well-mapped learning/memory circuit is age-dependent and sex-dependent, driven by FMRP-Rugose pathway activation, temporally promoted by Meng-Po kinase function, and restricted by output neurotransmission providing network feedback.

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Section: Resultsmentioning

confidence: 99%

Temporally and Spatially Localized PKA Activity within Learning and Memory Circuitry Regulated by Network Feedback

Sears

Broadie

2022

eNeuro

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“…It is likely that additional social factors modulate oviposition site selection once flies have arrived at an oviposition site. For example, flies physically present at the oviposition site may modify oviposition behavior through visual input 71 , physical interaction between individuals 72 , or the release of stress pheromones 73 , 74 .…”

Section: Discussionmentioning

confidence: 99%

Aggregation pheromones have a non-linear effect on oviposition behavior in Drosophila melanogaster

Verschut

Doubovetzky

et al. 2023

Nat Commun

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Female fruit flies (Drosophila melanogaster) oviposit at communal sites where the larvae may cooperate or compete for resources depending on group size. This offers a model system to determine how females assess quantitative social information. We show that the concentration of pheromones found on a substrate increases linearly with the number of adult flies that have visited that site. Females prefer oviposition sites with pheromone concentrations corresponding to an intermediate number of previous visitors, whereas sites with low or high concentrations are unattractive. This dose-dependent decision is based on a blend of 11-cis-Vaccenyl Acetate (cVA) indicating the number of previous visitors and heptanal (a novel pheromone deriving from the oxidation of 7-Tricosene), which acts as a dose-independent co-factor. This response is mediated by detection of cVA by odorant receptor neurons Or67d and Or65a, and at least five different odorant receptor neurons for heptanal. Our results identify a mechanism allowing individuals to transform a linear increase of pheromones into a non-linear behavioral response.

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“…Indeed, Drosophila shows approach behavior to other individuals and a natural tendency to aggregate ( Jiang et al 2020 ; Sun et al 2020 ). This moderate degree of sociability seems to be beneficial for flies, as it facilitates the spread of relevant information about their surroundings, learning, and avoidance of dangers within a group ( Kacsoh et al 2015 ; Ramdya et al 2015 ; Muria et al 2021 ; Wu et al 2023 ).…”

Section: The Social Brainmentioning

confidence: 99%

An integrative sensor of body states: how the mushroom body modulates behavior depending on physiological context

Suárez-Grimalt,

Grunwald Kadow,

Scheunemann

2024

Learn. Mem.

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The brain constantly compares past and present experiences to predict the future, thereby enabling instantaneous and future behavioral adjustments. Integration of external information with the animal's current internal needs and behavioral state represents a key challenge of the nervous system. Recent advancements in dissecting the function of theDrosophilamushroom body (MB) at the single-cell level have uncovered its three-layered logic and parallel systems conveying positive and negative values during associative learning. This review explores a lesser-known role of the MB in detecting and integrating body states such as hunger, thirst, and sleep, ultimately modulating motivation and sensory-driven decisions based on the physiological state of the fly. State-dependent signals predominantly affect the activity of modulatory MB input neurons (dopaminergic, serotoninergic, and octopaminergic), but also induce plastic changes directly at the level of the MB intrinsic and output neurons. Thus, the MB emerges as a tightly regulated relay station in the insect brain, orchestrating neuroadaptations due to current internal and behavioral states leading to short- but also long-lasting changes in behavior. While these adaptations are crucial to ensure fitness and survival, recent findings also underscore how circuit motifs in the MB may reflect fundamental design principles that contribute to maladaptive behaviors such as addiction or depression-like symptoms.

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Social facilitation of long-lasting memory is mediated by CO2 in Drosophila

Cited by 15 publications

References 53 publications

Temporally and Spatially Localized PKA Activity within Learning and Memory Circuitry Regulated by Network Feedback

Temporally and Spatially Localized PKA Activity within Learning and Memory Circuitry Regulated by Network Feedback

Aggregation pheromones have a non-linear effect on oviposition behavior in Drosophila melanogaster

An integrative sensor of body states: how the mushroom body modulates behavior depending on physiological context

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