Critical Period of Memory Enhancement during Taste Avoidance Conditioning in Lymnaea stagnalis

Tomoyo Takahashi,Manabu Sakakibara,Ken Lukowiak,Satoshi Takigami,Hiroshi Sunada,Efthimios M C Skoulakis

doi:10.1371/journal.pone.0075276

Tomoyo Takahashi, Manabu Sakakibara + Show 4 more

Open Access

https://doi.org/10.1371/journal.pone.0075276

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Journal: PLoS ONE	Publication Date: Oct 3, 2013
Citations: 80	License type: CC BY 4.0

Affiliation: Tokai University, University of Calgary

Abstract

The present study investigated the optimal training procedure leading to long-lasting taste avoidance behavior in Lymnaea. A training procedure comprising 5 repeated pairings of a conditional stimulus (CS, sucrose), with an unconditional stimulus (US, a tactile stimulation to the animal’s head), over a 4-day period resulted in an enhanced memory formation than 10 CS-US repeated pairings over a 2-day period or 20 CS-US repeated pairings on a single day. Backward conditioning (US-CS) pairings did not result in conditioning. Thus, this taste avoidance conditioning was CS-US pairing specific. Food avoidance behavior was not observed following training, however, if snails were immediately subjected to a cold-block (4°C for 10 min). It was critical that the cold-block be applied within 10 min to block long-term memory (LTM) formation. Further, exposure to the cold-block 180 min after training also blocked both STM and LTM formation. The effects of the cold-block on subsequent learning and memory formation were also examined. We found no long lasting effects of the cold-block on subsequent memory formation. If protein kinase C was activated before the conditioning paradigm, snails could still acquire STM despite exposure to the cold-block.

Highlights

Our understanding of the causal neuronal mechanisms that underlie learning and the subsequent formation of long-lasting memory has been greatly advanced by studies of simpler invertebrate model systems
We evaluated whether the effect of cooling is really reversible, i.e., does application of the coldblock prevent snails from learning and forming memory? we examined whether protein kinase C (PKC)mediated phosphorylation is required to form short-term memory (STM)
We previously demonstrated that 20 paired CS-US presentations was the minimum number of pairings required for long-term memory (LTM) formation [1]

Summary

Introduction

Our understanding of the causal neuronal mechanisms that underlie learning and the subsequent formation of long-lasting memory has been greatly advanced by studies of simpler invertebrate model systems. We investigated the critical time periods following classical conditioning training during which memory formation can be interrupted using a reversible cold-block technique (cooling-induced amnesia). Knowledge of the critical time periods for consolidation is crucial to elucidate the molecular events that underlie memory. To establish taste avoidance conditioning (TAC), we paired sucrose application (conditional stimulus, CS), which elicits a feeding response, with a tactile stimulus to the head (unconditional stimulus, US), which evokes a withdrawal response. The withdrawal response is incompatible with feeding, and the feeding response elicited by the CS is immediately terminated. After a number of CS-US pairings, the CS no longer elicits feeding. If the order of the pairing is reversed (i.e., US-CS; backward conditioning), the CS continues to elicit feeding behavior [1]

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