What can we teach Lymnaea and what can Lymnaea teach us?

Abstract

This review describes the advantages of adopting a molluscan complementary model, the freshwater snail Lymnaea stagnalis, to study the neural basis of learning and memory in appetitive and avoidance classical conditioning; as well as operant conditioning of its aerial respiratory and escape behaviour. We firstly explored ‘what we can teach Lymnaea’ by discussing a variety of sensitive, solid, easily reproducible and simple behavioural tests that have been used to uncover the memory abilities of this model system. Answering this question will allow us to open new frontiers in neuroscience and behavioural research to enhance our understanding of how the nervous system mediates learning and memory. In fact, from a translational perspective, Lymnaea and its nervous system can help to understand the neural transformation pathways from behavioural output to sensory coding in more complex systems like the mammalian brain. Moving on to the second question: ‘what can Lymnaea teach us?’, it is now known that Lymnaea shares important associative learning characteristics with vertebrates, including stimulus generalization, generalization of extinction and discriminative learning, opening the possibility to use snails as animal models for neuroscience translational research.

Oiling the gears of memory: quercetin exposure during memory formation, consolidation, and recall enhances memory in Lymnaea stagnalis

“…Our current data provides the first support for Q-modulated enhancement of cognitive function in an invertebrate model after an operant conditioning procedure. Thus, strengthening the case for Lymnaea as a model for translational neuroscience (Rivi et al, 2021b, Fodor et al, 2020).…”

“…Finally, the data also illustrate the advantages of using our model system in gaining an understanding of how substances, such as Q, alter cognition. Q, as well as many other compounds (e.g., epicatechin), easily penetrate through the integument of the snail and, because snails have an open circulatory system, can easily and quickly reach the CNS (Fruson et al, 2012; Rivi et al, 2021b, Rivi et al, 2020).…”

Insulin and Memory in Invertebrates

“…For example, Aplysia and Limax are well-known to be capable of associative learning (Yamanaka et al, 2021 ; Momohara et al, 2022 ). Furthermore, the pond snail Lymnaea stagnalis can be classically or operantly conditioned for many different types of behaviors (e.g., feeding and aerial respiratory behaviors; Sunada et al, 2017a ; Crossley et al, 2019 ; Fodor et al, 2020 ; Itoh et al, 2021 ; Pirger et al, 2021 ; Rivi et al, 2021a , b ). As described in the “Introduction” Section, ILP in Lymnaea was recognized as the first ILP with its DNA sequence revealed in invertebrates (Smit et al, 1988 ; Thorpe and Duve, 1988 ), leading to extensive studies of the relationship between insulin function and memory formation in Lymnaea (Pirger et al, 2014 ; Kojima et al, 2015 ; Benjamin and Kemenes, 2020 ).…”

A circuit mechanism linking past and future learning through shifts in perception

“…Simple invertebrate models have been extensively exploited to elucidate fundamental neural mechanisms for learning and action selection (6)(7)(8)(9)(10)(11)(12)(13)(14). Here, we used Lymnaea, an established molluscan system (15)(16)(17)(18)(19)(20)(21)(22), to directly probe the relationship between past memory, perception, and new learning. This animal can rapidly form associations between stimuli after a single training session with the resulting memory lasting for several weeks (23,24).…”