Upregulated energy metabolism in the Drosophila mushroom body is the trigger for long-term memory

Pierre-Yves Plaçais,Thomas Preat,Séverine Trannoy,Lisa Scheunemann,Guillaume Isabel,Kyung-An Han,Éloïse De Tredern,Valérie Goguel

doi:10.1038/ncomms15510

Abstract

Efficient energy use has constrained the evolution of nervous systems. However, it is unresolved whether energy metabolism may resultantly regulate major brain functions. Our observation that Drosophila flies double their sucrose intake at an early stage of long-term memory formation initiated the investigation of how energy metabolism intervenes in this process. Cellular-resolution imaging of energy metabolism reveals a concurrent elevation of energy consumption in neurons of the mushroom body, the fly’s major memory centre. Strikingly, upregulation of mushroom body energy flux is both necessary and sufficient to drive long-term memory formation. This effect is triggered by a specific pair of dopaminergic neurons afferent to the mushroom bodies, via the D5-like DAMB dopamine receptor. Hence, dopamine signalling mediates an energy switch in the mushroom body that controls long-term memory encoding. Our data thus point to an instructional role for energy flux in the execution of demanding higher brain functions.

Highlights

Efficient energy use has constrained the evolution of nervous systems
We previously showed that the trigger for long-term memory (LTM) formation involves rhythmic signalling on mushroom body (MB) neurons from specific dopaminergic neurons, which occurs during and immediately after spaced training[18]
Flies were subjected to a spaced training protocol, and their subsequent intake of a sucrose solution was measured using two distinct methods: a dye-feeding assay and a Capillary Feeding (CAFE) assay

Summary

Introduction

Efficient energy use has constrained the evolution of nervous systems. it is unresolved whether energy metabolism may resultantly regulate major brain functions. Upregulation of mushroom body energy flux is both necessary and sufficient to drive long-term memory formation This effect is triggered by a specific pair of dopaminergic neurons afferent to the mushroom bodies, via the D5-like DAMB dopamine receptor. Our results establish that following spaced training, flies strongly increase their energy intake This reflects an elevation of energy flux in MB neurons, which we show is a necessary, and a sufficient condition to consolidate memory into LTM. This upregulation is initiated by dopamine signalling through a specific receptor, the D5-like DAMB receptor.

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