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Metabolic regulations and neuron-glia interactions underlying long-term memory formation in Drosophila melanogaster

Abstract : In flies, long-term memory (LTM) formation is an energetically costly mechanism that is tightly controlled by both external parameters and the internal state (Plaçais and Preat, 2013), which questions the role and the regulation of energy metabolism during memory formation. In vertebrates, several studies already described that specific metabolic pathways support LTM, such as glycogen hydrolysis (Gibbs et al., 2006; Suzuki et al., 2011) in astrocytic glia, which then provide glycogen-derived lactate to the active neurons (Gao et al., 2016). The involvement of glial cells in LTM is, for the time being, poorly documented in flies (Matsuno et al., 2015). Still, Drosophila melanogaster is a well-suited model organism to study molecular mechanisms in precise cell types, or even at the subcellular level. In this thesis, we studied if and how glial cells were involved in the formation of aversive LTM following an association between odors and electric shocks in flies. Thanks to the use of several powerful genetic tools that are available in this model, we demonstrated that glial cells were early involved in the consolidation of memory, specifically for LTM. Drosophila, as mammals, possess various glial subtypes. We dissected which glial subtype was involved, and surprisingly, we found that the glial cells enwrapping the neuronal soma, named cortex glia, were involved in LTM consolidation. This was highly unexpected, as the work conducted until now focused on neuron-glia interactions at the level of the synapse, leaving glia-neuronal soma interactions understudied, in particular during memory formation.By using cell type specific gene knockdown restricted to adulthood associated to behavioral and in vivo imaging experiments, we investigated the signaling pathway occurring in cortex glia during LTM formation. Our data evidence a model of cortex glia – mushroom body neurons interactions that occur specifically during LTM formation. During and/or early after the spaced conditioning, cholinergic neurons, probably mushroom body neurons, release acetylcholine that activates the cholinergic receptor nAChRα7 expressed in cortex glia. This triggers a calcium elevation in cortex glia that induces the release of the insulin-like peptide Ilp4, which function was unknown until now. Ilp4 autocrinally activates the insulin receptor expressed in cortex glia, increasing glucose synthesis from trehalose in these cells, and glucose export towards the mushroom body neuronal soma to support their increased glucose demand.
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Eloise de Tredern. Metabolic regulations and neuron-glia interactions underlying long-term memory formation in Drosophila melanogaster. Neurons and Cognition [q-bio.NC]. Université Paris sciences et lettres, 2019. English. ⟨NNT : 2019PSLET009⟩. ⟨tel-03331628⟩

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