How Stress Alters Memory in ‘Smart’ Snails

Sarah Dalesman,Ken Lukowiak,Manabu Sakakibara

doi:10.1371/journal.pone.0032334

Abstract

Cognitive ability varies within species, but whether this variation alters the manner in which memory formation is affected by environmental stress is unclear. The great pond snail, Lymnaea stagnalis, is commonly used as model species in studies of learning and memory. The majority of those studies used a single laboratory strain (i.e. the Dutch strain) originating from a wild population in the Netherlands. However, our recent work has identified natural populations that demonstrate significantly enhanced long-term memory (LTM) formation relative to the Dutch strain following operant conditioning of aerial respiratory behaviour. Here we assess how two populations with enhanced memory formation (i.e. ‘smart’ snails), one from Canada (Trans Canada 1: TC1) and one from the U.K. (Chilton Moor: CM) respond to ecologically relevant stressors. In control conditions the Dutch strain forms memory lasting 1–3 h following a single 0.5 h training session in our standard calcium pond water (80 mg/l [Ca2+]), whereas the TC1 and CM populations formed LTM lasting 5+ days following this training regime. Exposure to low environmental calcium pond water (20 mg/l [Ca2+]), which blocks LTM in the Dutch strain, reduced LTM retention to 24 h in the TC1 and CM populations. Crowding (20 snails in 100 ml) immediately prior to training blocks LTM in the Dutch strain, and also did so in TC1 and CM populations. Therefore, snails with enhanced cognitive ability respond to these ecologically relevant stressors in a similar manner to the Dutch strain, but are more robust at forming LTM in a low calcium environment. Despite the two populations (CM and TC1) originating from different continents, LTM formation was indistinguishable in both control and stressed conditions. This indicates that the underlying mechanisms controlling cognitive differences among populations may be highly conserved in L. stagnalis.

Highlights

The ability of animals to learn and remember during their lifetime enables them to adapt to changes in predator threat [1,2], food availability [3] or food quality [4,5], as well as remembering conspecific interactions that may alter social status or mate preference [6,7,8], all of which will directly affect an animal’s fitness
Memory retention at 24 h in control conditions There was no significant difference between the two populations (Chilton Moor, U.K.: CM vs. Trans Canada 1, Canada: TC1) within each training group, independent of the training regime
Following operant conditioning snails from both populations demonstrated a significant decline in breathing attempts between training (TR) and the test at 24 h (CM: t = 5.49, P,0.001, N = 16; TC1: t = 3.38, P = 0.005, N = 14)

Summary

Introduction

The ability of animals to learn and remember during their lifetime enables them to adapt to changes in predator threat [1,2], food availability [3] or food quality [4,5], as well as remembering conspecific interactions that may alter social status or mate preference [6,7,8], all of which will directly affect an animal’s fitness. In the natural environment sub-optimal conditions can act as a stressor, considered here as changes in the environment that perturb normal physiological, psychological or behavioural function [9,10] This stress may significantly alter the ability of an animal to learn and form memory, dependent on the nature of the stress and timing relative to a period of learning [11,12]. Populations within a species can differ considerably in their response to a variety of environmental stimuli demonstrating local adaptation, for example in predator recognition and antipredator behaviour [17,18,19] Their perception of, or response to, environmental stressors that alter memory formation may differ. Populations or individuals may be differentially affected by the environment in terms of how stress alters memory forming potential

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