Switch-like and persistent memory formation in individual Drosophila larvae.

Amanda Lesar,Marc Gershow,Javan Tahir,Jason Wolk

doi:10.7554/elife.70317

Amanda Lesar, Marc Gershow + Show 2 more

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https://doi.org/10.7554/elife.70317

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Abstract

Associative learning allows animals to use past experience to predict future events. The circuits underlying memory formation support immediate and sustained changes in function, often in response to a single example. Larval Drosophila is a genetic model for memory formation that can be accessed at molecular, synaptic, cellular, and circuit levels, often simultaneously, but existing behavioral assays for larval learning and memory do not address individual animals, and it has been difficult to form long-lasting memories, especially those requiring synaptic reorganization. We demonstrate a new assay for learning and memory capable of tracking the changing preferences of individual larvae. We use this assay to explore how activation of a pair of reward neurons changes the response to the innately aversive gas carbon dioxide (CO2). We confirm that when coupled to CO2 presentation in appropriate temporal sequence, optogenetic reward reduces avoidance of CO2. We find that learning is switch-like: all-or-none and quantized in two states. Memories can be extinguished by repeated unrewarded exposure to CO2 but are stabilized against extinction by repeated training or overnight consolidation. Finally, we demonstrate long-lasting protein synthesis dependent and independent memory formation.

Highlights

Associative learning allows animals to use past experience to predict important future events, such as the appearance of food or predators, or changes in their environmental conditions (Pavlov, 1927; Kandel et al, 2014)
Larval Drosophila has long been a model for the study of memory formation, with a well-established paradigm developed to study associative memory formation through classical conditioning (Gerber et al, 2013; Widmann et al, 2018; Schleyer et al, 2018; Scherer et al, 2003; Neuser et al, 2005; Gerber and Stocker, 2007; Apostolopoulou et al, 2013; Saumweber et al, 2018; Weiglein et al, 2019)
To verify that spacing the trials was essential to forming a protein-synthesis dependent memory, we duplicated the experiments exactly, except we presented 10 cycles of training en masse, rather than spacing them

Summary

Introduction

Associative learning allows animals to use past experience to predict important future events, such as the appearance of food or predators, or changes in their environmental conditions (Pavlov, 1927; Kandel et al, 2014). Larval Drosophila has long been a model for the study of memory formation, with a well-established paradigm developed to study associative memory formation through classical conditioning (Gerber et al, 2013; Widmann et al, 2018; Schleyer et al, 2018; Scherer et al, 2003; Neuser et al, 2005; Gerber and Stocker, 2007; Apostolopoulou et al, 2013; Saumweber et al, 2018; Weiglein et al, 2019) In this paradigm, larvae are trained and tested in groups, and learning is quantified by the difference in the olfactory

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