How stress alters memory in 'smart' snails

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 [Ca(2+)]), 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 [Ca(2+)]), 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

The participation of NMDA receptors, PKC, and MAPK in the formation of memory following operant conditioning in Lymnaea

<p>Abstract</p> <p>Background</p> <p>Memory is the ability to store, retain, and later retrieve information that has been learned. Intermediate term memory (ITM) that persists for up to 3 h requires new protein synthesis. Long term memory (LTM) that persists for at least 24 h requires: DNA transcription, RNA translation, and the trafficking of newly synthesized proteins. It has been shown in a number of different model systems that NMDA receptors, protein kinase C (PKC) and mitogen activated protein kinase (MAPK) are all involved in the memory formation process.</p> <p>Results</p> <p>Here we show that snails trained in control conditions are capable of forming, depending on the training procedure used, either ITM or LTM. However, blockage of NMDA receptors (MK 801), inhibition of PKC (GF109203X hydrochloride) and MAPK activity (UO126) prevent the formation of both ITM and LTM.</p> <p>Conclusions</p> <p>The injection of either U0126 or GF109203X, which inhibit MAPK and PKC activity respectively, 1 hour prior to training results in the inhibition of both ITM and LTM formation. We further found that NMDA receptor activity was necessary in order for both ITM and LTM formation.</p

Environmentally relevant stressors alter memory formation in the pond snail Lymnaea

Stress alters adaptive behaviours such as learning and memory. Stressors can either enhance or diminish learning, memory formation and/or memory recall. We focus attention here on how environmentally relevant stressors alter learning, memory and forgetting in the pond snail, Lymnaea stagnalis. Operant conditioning of aerial respiration causes associative learning that may lead to long-term memory (LTM) formation. However, individual ecologically relevant stressors, combinations of stressors, and bio-active substances can alter whether or not learning occurs or memory forms. While the behavioural memory phenotype may be similar as a result of exposure to different stressors, how each stressor alters memory formation may occur differently. In addition, when a combination of stressors are presented it is difficult to predict ahead of time what the outcome will be regarding memory formation. Thus, how combinations of stressors act is an emergent property of how the snail perceives the stressors.</jats:p

A quantitative proteomic analysis of long-term memory

BACKGROUND: Memory is the ability to store, retain, and later retrieve learned information. Long-term memory (LTM) formation requires: DNA transcription, RNA translation, and the trafficking of newly synthesized proteins. Several components of these processes have already been identified. However, due to the complexity of the memory formation process, there likely remain many yet to be identified proteins involved in memory formation and persistence. RESULTS: Here we use a quantitative proteomic method to identify novel memory-associated proteins in neural tissue taken from animals that were trained in vivo to form a long-term memory. We identified 8 proteins that were significantly up-regulated, and 13 that were significantly down-regulated in the LTM trained animals as compared to two different control groups. In addition we found 19 proteins unique to the trained animals, and 12 unique proteins found only in the control animals. CONCLUSIONS: These results both confirm the involvement of previously identified memory proteins such as: protein kinase C (PKC), adenylate cyclase (AC), and proteins in the mitogen-activated protein kinase (MAPK) pathway. In addition these results provide novel protein candidates (e.g. UHRF1 binding protein) on which to base future studies

Combining stressors that individually impede long-term memory blocks all memory processes

The effects of stress on memory are typically assessed individually; however, in reality different stressors are often experienced simultaneously. Here we determined the effect that two environmentally relevant stressors, crowding and low calcium availability, have on memory and neural activity following operant conditioning of aerial respiration in the pond snail, Lymnaea stagnalis. We measured aerial breathing behaviour and activity of a neuron necessary for memory formation, right pedal dorsal 1 (RPeD1), in the central pattern generator (CPG) that drives aerial respiration in untrained animals, and assessed how these traits changed following training. In naïve animals both crowding and combined stressors significantly depressed burst activity in RPeD1 which correlated with a depression in aerial breathing behaviour, whereas low calcium availability had no effect on RPeD1 activity. Following training, changes in burst activity in RPeD1 correlated with behavioural changes, decreasing relative to their naïve state at 3 h and 24 h in control conditions when both intermediate-term memory (ITM: 3 h) and long-term memory (LTM: 24 h) are formed, at 3 h but not 24 h when exposed to individual stressors when only ITM is formed, and did not change in combined stressors (i.e. when no memory is formed). Additionally, we also found that Lymnaea formed short-term memory (STM: 10 min) in the presence of individual stressors or under control conditions, but failed to do so in the presence of combined stressors. Our data demonstrate that by combining stressors that individually block LTM only we can block all memory processes. Therefore the effects of two stressors with similar individual affects on memory phenotype may be additive when experienced in combination

Monoamines, Insulin and the Roles They Play in Associative Learning in Pond Snails

Molluscan gastropods have long been used for studying the cellular and molecular mechanisms underlying learning and memory. One such gastropod, the pond snail Lymnaea stagnalis, exhibits long-term memory (LTM) following both classical and operant conditioning. Using Lymnaea, we have successfully elucidated cellular mechanisms of learning and memory utilizing an aversive classical conditioning procedure, conditioned taste aversion (CTA). Here, we present the behavioral changes following CTA training and show that the memory score depends on the duration of food deprivation. Then, we describe the relationship between the memory scores and the monoamine contents of the central nervous system (CNS). A comparison of learning capability in two different strains of Lymnaea, as well as the filial 1 (F1) cross from the two strains, presents how the memory scores are correlated in these populations with monoamine contents. Overall, when the memory scores are better, the monoamine contents of the CNS are lower. We also found that as the insulin content of the CNS decreases so does the monoamine contents which are correlated with higher memory scores. The present review deepens the relationship between monoamine and insulin contents with the memory score

Context Learning and the Effect of Context on Memory Retrieval in Lymnaea

Aerial respiratory behavior in Lymnaea was operantly conditioned so that the animals perform aerial respiration significantly less often. Using the standard training procedure (pond water made hypoxic by bubbling N(2) through it) both food-deprived and fed animals learned and exhibited long-term memory (LTM). However, food-deprived animals exhibited neither learning nor memory when trained under a condition in which the hypoxic pond water also contained a food odorant (carrot, the food-odorant procedure). Fed animals, however, learned and exhibited LTM with the food-odorant procedure. Thus, the presence of the food odorant per se did not prevent learning or the establishment of LTM. Further experimentation, however, revealed that the ability of the snails to have recall (i.e., memory) for the learned behavior was dependent on the context in which memory was tested. That is, if animals were trained with the food-odorant procedure they could only exhibit recall if tested in the food-odorant context and vice versa with the standard training procedure. Thus, although fed animals could learn and show LTM with either training and testing procedure, LTM could only be seen when they were tested in the context in which they were trained