Abstract
SummaryForming long-term memory (LTM) often requires repetitive experience spread over time. Studies in Drosophila suggest aversive olfactory LTM is optimal after spaced training, multiple trials of differential odor conditioning with rest intervals. Memory after spaced training is frequently compared to that after the same number of trials without intervals. Here we show that, after spaced training, flies acquire additional information and form an aversive memory for the shock-paired odor and a slowly emerging and more persistent “safety-memory” for the explicitly unpaired odor. Safety-memory acquisition requires repetition, order, and spacing of the training trials and relies on triggering specific rewarding dopaminergic neurons. Co-existence of aversive and safety memories is evident as depression of odor-specific responses at different combinations of junctions in the mushroom body output network; combining two outputs appears to signal relative safety. Having complementary aversive and safety memories augments LTM performance after spaced training by making the odor preference more certain.
Highlights
Memory allows animals to anticipate forthcoming meaningful events and use learned predictive sensory cues to guide preemptive behavior
In Drosophila, studies frequently compare differences in memory formed after a number of training trials with or without intertrial intervals (ITIs)
We conditioned flies using a spaced training protocol of six differential training trials separated by 15 min intervals (Figure 1A)
Summary
Memory allows animals to anticipate forthcoming meaningful events and use learned predictive sensory cues to guide preemptive behavior. Across the animal kingdom, forming longterm memory (LTM) often requires multiple training trials with intervening rest periods, or intertrial intervals (ITIs) (Ebbinghaus, 1913; Carew et al, 1972; Tully et al, 1994; Kogan et al, 1997; Hermitte et al, 1999; Menzel et al, 2001). Acquisition of aversive LTM in Drosophila is considered to require five to ten spaced training trials with a 15 min ITI, where an individual trial pairs one of two odors with an electric-shock reinforcement. Flies mutant for the radish (rad) gene, which encodes a putative Rap GTPase activating protein (Folkers et al, 2006), lack aversive ARM, whereas pharmacological and genetic blockers of new transcription and protein synthesis only disrupt LTM (Tully et al, 1994; Yin et al, 1994; Dubnau et al, 2003; Chen et al, 2012; Miyashita et al, 2012)
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