A neural circuit linking learning and sleep in Drosophila long-term memory

Zhengchang Lei,Krystyna Keleman,Kristin Henderson

doi:10.1038/s41467-022-28256-1

Abstract

Animals retain some but not all experiences in long-term memory (LTM). Sleep supports LTM retention across animal species. It is well established that learning experiences enhance post-learning sleep. However, the underlying mechanisms of how learning mediates sleep for memory retention are not clear. Drosophila males display increased amounts of sleep after courtship learning. Courtship learning depends on Mushroom Body (MB) neurons, and post-learning sleep is mediated by the sleep-promoting ventral Fan-Shaped Body neurons (vFBs). We show that post-learning sleep is regulated by two opposing output neurons (MBONs) from the MB, which encode a measure of learning. Excitatory MBONs-γ2α’1 becomes increasingly active upon increasing time of learning, whereas inhibitory MBONs-β’2mp is activated only by a short learning experience. These MB outputs are integrated by SFS neurons, which excite vFBs to promote sleep after prolonged but not short training. This circuit may ensure that only longer or more intense learning experiences induce sleep and are thereby consolidated into LTM.

Highlights

Animals retain some but not all experiences in long-term memory (LTM)
We hypothesized that this selectivity is reflected in the activity of ventral Fan-Shaped Body neurons (vFBs), such that they would be selectively activated in time period between 1–3 h (TP1-3) after a learning experience that induces LTM but not short-term memory (STM)
VFBs activity was significantly higher after training for 4 h in comparison to the control naïve males and males that were trained for 1 or 2 h (Fig. 1a, b). This effect was specific to vFBs, as training with mated females for 6 h did not lead to increased activity of the dorsal FB neurons, which are involved in sleep homeostasis[5,9,10,26] (Supplementary Fig. 2a)

Summary

Introduction

Animals retain some but not all experiences in long-term memory (LTM). Sleep supports LTM retention across animal species. Excitatory MBONs-γ2α’1 becomes increasingly active upon increasing time of learning, whereas inhibitory MBONs-β’2mp is activated only by a short learning experience These MB outputs are integrated by SFS neurons, which excite vFBs to promote sleep after prolonged but not short training. This circuit may ensure that only longer or more intense learning experiences induce sleep and are thereby consolidated into LTM. 1234567890():,; Post-learning sleep supports LTM retention across animal species[1,2,3,4,5] It mediates consolidation of spatial and courtship LTM in rodents and fruit flies, respectively, by the reactivation of the neural pathways previously engaged during memory acquisition[6,7,8].

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