Proactive and retroactive interference with associative memory consolidation in the snail Lymnaea is time and circuit dependent

Paul R Benjamin,Ildikó Kemenes,Frederick D Lorenzetti,Souvik Naskar,György Kemenes,Michael Crossley,Michael O'Shea

doi:10.1038/s42003-019-0470-y

Paul R Benjamin, Ildikó Kemenes + Show 5 more

Open Access

https://doi.org/10.1038/s42003-019-0470-y

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Journal: Communications Biology	Publication Date: Jun 26, 2019
Citations: 17	License type: open-access

Affiliation: University of Sussex

Abstract

Interference-based forgetting occurs when new information acquired either before or after a learning event attenuates memory expression (proactive and retroactive interference, respectively). Multiple learning events often occur in rapid succession, leading to competition between consolidating memories. However, it is unknown what factors determine which memory is remembered or forgotten. Here, we challenge the snail, Lymnaea, to acquire two consecutive similar or different memories and identify learning-induced changes in neurons of its well-characterized motor circuits. We show that when new learning takes place during a stable period of the original memory, proactive interference only occurs if the two consolidating memories engage the same circuit mechanisms. If different circuits are used, both memories survive. However, any new learning during a labile period of consolidation promotes retroactive interference and the acquisition of the new memory. Therefore, the effect of interference depends both on the timing of new learning and the underlying neuronal mechanisms.

Highlights

Interference-based forgetting occurs when new information acquired either before or after a learning event attenuates memory expression
We tested the hypothesis that the direction of interference between a memory trace and new learning during its consolidation is dependent upon the timing of the interference in the consolidation sequence of the original memory
We examined whether the original and the new memory are encoded by plastic changes in the same or different circuits and whether it depended on the type of learning used for interference

Summary

Introduction

Interference-based forgetting occurs when new information acquired either before or after a learning event attenuates memory expression (proactive and retroactive interference, respectively). We examined whether the original and the new memory are encoded by plastic changes in the same or different circuits and whether it depended on the type of learning used for interference To address these questions, we used the pond snail, Lymnaea stagnalis, which can learn simple associations after a single pairing of a conditioned and unconditioned stimulus, leading to long-term memory that lasts up to 19 days[8,9]. We used the pond snail, Lymnaea stagnalis, which can learn simple associations after a single pairing of a conditioned and unconditioned stimulus, leading to long-term memory that lasts up to 19 days[8,9] Their neurons are large and re-identifiable, and the underlying circuitry of the conditioned behaviors studied here have been extensively characterized[10,11,12,13,14], aiding in the identification of learning-induced changes in neural activity responsible for encoding memories[9,15,16,17,18]. Our study reveals that the type of interference depends on the timing of the new learning as well as the underlying neural circuits by which the memories are encoded

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