Canadian Association of Neurosciences Review: Learning at a Snail's Pace

Hotchkiss Brain Institute, University of Calgary, Calgary, AB, Canada.
The Canadian journal of neurological sciences. Le journal canadien des sciences neurologiques (Impact Factor: 1.53). 12/2006; 33(4):347-56. DOI: 10.1017/S0317167100005291
Source: PubMed


While learning and memory are related, they are distinct processes each with different forms of expression and underlying molecular mechanisms. An invertebrate model system, Lymnaea stagnalis, is used to study memory formation of a non-declarative memory. We have done so because: (1) We have discovered the neural circuit that mediates an interesting and tractable behaviour; (2) This behaviour can be operantly conditioned and intermediate-term and long-term memory can be demonstrated; and (3) It is possible to demonstrate that a single neuron in the model system is a necessary site of memory formation. This article reviews how Lymnaea has been used in the study of behavioural and molecular mechanisms underlying consolidation, reconsolidation, extinction and forgetting.

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Available from: Ken Lukowiak, Dec 26, 2013
    • "These studies all suggest that retinoic acid activity in the CNS is important in vertebrate learning and memory. Molluscs such as Lymnaea and Aplysia (Byrne et al., 1991;Benjamin, Staras, & Kemenes, 2000;Parvez, Rosenegger, Orr, Martens, & Lukowiak, 2006) have long been utilized to study cellular and molecular mechanisms underlying non-associative and associative learning, but to date, there has been no evidence supporting a role for retinoid signaling in implicit memory formation in invertebrates. Although there is evidence that the ecdysone receptor of Drosophila, which heterodimerizes with the Drosophila homologue of RXR (ultraspiracle) plays a role in LTM formation in response to an edcysone metabolite (Ishimoto, Sakai, & Kitamoto, 2009), experimental evidence suggests that ultraspiracle does not bind retinoic acid (Mangelsdorf et al., 1992). "
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    ABSTRACT: Retinoic acid, a metabolite of vitamin A, is proposed to play an important role in vertebrate learning and memory, as well as hippocampal-dependent synaptic plasticity. However, it has not yet been determined whether retinoic acid plays a similar role in learning and memory in invertebrates. In this study, we report that retinoid signaling in the mollusc Lymnaea stagnalis, is required for long-term memory formation following operant conditioning of its aerial respiratory behaviour. Animals were exposed to inhibitors of the RALDH enzyme (which synthesizes retinoic acid), or various retinoid receptor antagonists. Following exposure to these inhibitors, neither learning nor intermediate-term memory (lasting 2 hours) was affected, but long-term memory formation (tested at either 24 or 72 hours) was inhibited. We next demonstrated that various retinoid receptor agonists promoted long-term memory formation. Using a training paradigm shown only to produce intermediate-term memory (lasting 2 hours, but not 24 hours) we found that exposure of animals to synthetic retinoids promoted memory formation that lasted up to 30 hours. These findings suggest that the role of retinoids in memory formation is ancient in origin, and that retinoid signaling is also important for the formation of implicit memories, in addition to its previously demonstrated role in hippocampal-dependent memories.
    No preview · Article · Jun 2014 · Neurobiology of Learning and Memory
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    • "The great pond snail, Lymnaea stagnalis, has been used extensively as a model organism to study the mechanisms of learning and memory [20], [21], [22], [23]. Much of this work has been carried out using individuals that have been reared in the laboratory over many generations, derived from a population originally collected in the 1950s from canals in a polder in Utrecht province in the Netherlands (i.e. the Dutch laboratory strain). "
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    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 [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.
    Full-text · Article · Feb 2012 · PLoS ONE
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    • "Therefore, it is important to consider changes in multiple behavioural traits if we are to accurately assess whether an animal has responded to a particular stimulus. The great pond snail L. stagnalis is frequently used as a model species to study learning and memory, due to a simple set of behaviours that are easily observable and altered through experience, and a relatively simple nervous system that allows the neural correlates for these behavioural changes to be determined (Parvez et al. 2006; Benjamin and Kemenes 2008; Lukowiak et al. 2003). "
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    ABSTRACT: Frequently studies of learning and memory measure a single focal behaviour; however it is likely that any learning paradigm will alter multiple behavioural traits in the same animal. We used video footage of the great pond snail (Lymnaea stagnalis), collected immediately prior to both training and testing for memory in response to operant conditioning to reduce aerial respiration, to measure two additional alternate behavioural traits: reducing the size of the pneumostome (breathing orifice) opening and shell tilt to cover the pneumostome. Typically, the training regime used here results in memory to reduce the number of breathing attempts lasting 24 h but not 72 h. However, memory duration when measured using the two additional behavioural traits differed significantly; shell tilt was short-lived lasting less than 1 h following training, whereas the reduction in pneumostome size was still apparent 72 h following training. Therefore, conclusions about the ability of L. stagnalis to retain memory in response to a single type of training regime will differ significantly depending on the focal behavioural trait measured. A significant correlation between the reduction in opening attempts and visible pneumostome area indicated that these behavioural traits are co-specialised, whereas pneumostome opening and shell tilt behaviour varied independently.
    Full-text · Article · Feb 2012 · Animal Cognition
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