SUMMARY Laboratory-reared Lymnaea are capable of detecting and responding to the scent of a crayfish predator. The present investigation is a first attempt to characterize multiple stress-related behavioural responses resulting from predator detection and to depict the neurophysiological correlates of one of these illustrated behaviours. Snails respond to crayfish effluent (CE) by increasing the following behaviours: aerial respiration,exploratory/searching phase and sensitivity to the shadow-elicited full-body withdrawal response. In contrast, when snails detect CE they decrease both their righting response time when dislodged from the substratum and their basal cutaneous oxygen consumption. Interestingly, basal heart rate does not change in response to CE exposure. Finally, we directly measured the activity of the neuron that initiates aerial respiratory behaviour, RPeD1, in semi-intact preparations. Naïve snails exposed to CE prior to recording demonstrated both a significantly reduced spontaneous firing rate and fewer bouts of bursting activity compared with non-exposed snails. These data show that laboratory-reared Lymnaea that have never experienced a natural predator are still capable of detecting and responding to the presence of a historically sympatric predator. These data open a new avenue of research,which may allow a direct investigation from the behavioural to the neuronal level as to how an ecologically relevant stressful stimulus alters behaviour.

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Stress has been shown to both impair and enhance learning, long-term memory (LTM) formation, and/or its recall. The pond snail, Lymnaea stagnalis, both detects and responds to the scent of a crayfish predator with multiple stress-related behavioral responses. Using both behavioral and electrophysiological evidence, this investigation is a first attempt to characterize how an environmentally relevant stressor (scent of a predator) enhances LTM formation in Lymnaea. Using a training procedure that, in "standard" pond water (PW), results in an intermediate-term memory that persists for only 3 h, we found that training snails in "crayfish effluent" (CE) induces a memory that persists for 48 h (i.e., its now an LTM). In addition, if we use a training procedure that in PW produces an LTM that persists for 1 d, we find that snails trained in CE have an LTM that persists for at least 8 d. Furthermore, we describe how a single neuron (RPeD1), which has been shown to be a necessary site for LTM formation, reflects the behavioral changes in its firing properties that persist for the duration of the LTM. Finally, Lymnaea exhibit context-specific memory, that is, when a memory is formed in a specific context (food odorant), it is only recalled in that context. Here, we found that snails trained in CE demonstrate context generalization, that is, memory is recalled in multiple contexts. All data are consistent with the hypothesis that learning in a stressful, yet biologically relevant, environment enhances LTM and prolongs its retention.

SUMMARYGaining insight into how natural trait variation is manifest in populations shaped by differential environmental factors is crucial to understanding the evolution, ecology and sensory biology of natural populations. We have demonstrated that lab-reared Lymnaea detect and respond to the scent of a crayfish predator with specific, appropriate anti-predator behavioral responses, including enhanced long-term memory (LTM) formation, and that such predator detection significantly alters the electrophysiological activity of RPeD1, a neuron that is a necessary site for LTM formation. Here we ask: (1) do distinct populations of wild Lymnaea stagnalis respond only to sympatric predators and if so, can these traits be quantified at both the behavioral and neurophysiological levels, and (2) does the presence of a non-sympatric predator elicit anti-predator behaviors including augmentation of LTM? We tested three different populations of wild (i.e. not lab-reared) snails freshly collected from their natural habitat: (1) polders near Utrecht in The Netherlands, (2) six seasonally isolated ponds in the Belly River drainage in southern Alberta, Canada and (3) a 20-year-old human-made dugout pond in southern Alberta. We found strain-specific variations in the ability to form LTM and that only a sympatric predator evoked anti-predatory behaviors, including enhanced LTM formation and changes in RPeD1 activity.

The ability to learn and form a memory enables organisms to adapt to a changing environment so as to be better able to survive. Learning and memory are behavioural manifestations of activity within individual neurons and neuronal circuits. While learning and memory are interrelated, they are separate processes each with different underlying molecular mechanisms and forms of expression. Learning can be broadly defined as the acquisition of a new behaviour, while memory is defined as the ability to both store and recall the new information.Learning and memory (or their correlates) have been studied at behavioural, systems, neuronal, and sub-cellular levels in organisms ranging from humans to worms. In this short review we will focus on research in an invertebrate model system that has provided insight into the underlying mechanisms of memory formation. While an understanding of the causal mechanisms of learning and memory formation in snails is of heuristic interest, our main reason for employing such a molluscan model system is to gain insight as to how learning and memory occur in us. It appears that the 'substrates' for learning and memory have been fairly conserved in all organisms throughout evolution.ABSTRACT: 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.RÉSUMÉ: L'apprentissage au pas d'escargot. Bien que l'apprentissage et la mémoire soient deux fonctions connexes, leurs processus sont distincts et chacun a des formes d'expression différentes et des mécanismes moléculaires sous-jacents différents. Nous utilisons un système dans un modèle invertébré, la Lymnaea stagnalis, pour étudier comment se forme une mémoire non déclarative. Nous avons utilisé ce modèle parce que : 1) Nous avons découvert un circuit neural qui assure la médiation d'un comportement intéressant et observable; 2) Ce comportement peut être conditionné en cours d'étude et la mémoire à moyen et à long terme peut être démontrée; 3) Il est possible de démontrer dans ce modèle qu'un seul neurone est nécessaire pour la formation de la mémoire. Cet article revoit comment la Lymnaea a été utilisée pour étudier les mécanismes comportementaux et moléculaires sous-jacents à la consolidation, à la reconsolidation, à l'extinction et à l'oubli. REVIEW ARTICLEMoreover, there are many experimental advantages (see below) to using invertebra...