Biological Bulletin Virtual Symposium: Marine Invertebrate Models of Learning and Memory (original) (raw)

Associative learning and memory inLymnaea stagnalis: how well do they remember?

The Journal of Experimental Biology, 2003

Molluscan model systems for the study of learning and memory This is not by any means an exhaustive review of invertebrate model systems that have been used to study the neuronal and molecular mechanisms of learning and memory; the interested reader is directed to two recent excellent reviews on this subject (Sahley and Crow, 1998; Chase, 2002). We have also restricted our discussion to gastropod molluscs, but this should in no way be taken to mean that the truly groundbreaking work on the mechanisms of learning and memory using 'worms' (e.g. Caenorhabditis elegans) or insects such as Drosophila is not worth mentioning or pursuing but rather that space limitations preclude their inclusion. For much the same reason, the fascinating studies using cephalopod molluscs (e.g. octopus), which exhibit very sophisticated learning and memory capabilities, will also not be reviewed here. Some of the first studies in the 'modern' search for the engram took the comparative physiological and psychological approach. For example, in the early 1900s, Piéron (1911), Dawson (1911) and Thompson (1917) used snails in attempts to discover how learning occurred. However, these studies were, by and large, forgotten, and it really was not until tests that were more natural and meaningful to the organisms were used that a full appreciation of the learning capabilities of gastropods became apparent. The 1960s saw a burst of activity that is still evident today to study how the nervous system is 'wired-up' to mediate specific behaviours and how changes in the behaviour brought about by training procedures are reflected or caused (the real goal) by changes in the activity of specific neurons. Thus, preparations such as Aplysia, Hermissenda, Pleurobranchaea and Tritonia gained popularity. Eric Kandel, with his share of the Nobel Prize for Medicine and Physiology in 2000, attained one of the pinnacles of science in part by using Aplysia. All the species mentioned above are marine creatures, and, with few exceptions (e.g. the land slug Limax and the land snail Helix), conventional wisdom from the 1970s through to the early 1990s was that the freshwater gastropods just did not have the 'right stuff' to be used in the quest for the Holy Grail. This review will focus on why that conventional wisdom was incorrect and why using Lymnaea might just be a very useful path to take to grasp the Grail in hand. Lymnaea as a model system for neurobiology Until the Dutch, under the inspired leadership of Professors Lever and Joose in The Department of Biology at Vrije Universeit in Amsterdam, adopted Lymnaea as their animal of choice for study in the early 1970s, Lymnaea was not often used in neurobiological research. The natural history of the 2097

Learning and memory in the Port Jackson shark, Heterodontus portusjacksoni

Animal Cognition, 2014

Basic understanding of the fundamental principles and mechanisms involved in learning is lacking for elasmobranch fishes. Our aim in this study was to experimentally investigate the learning and memory capacity of juvenile Port Jackson sharks, Heterodontus portusjacksoni. Sharks (N = 30) were conditioned over a 19-day period to associate an underwater LED light or stream of air-bubbles [conditioned stimulus (CS)] with a food reward [unconditioned stimulus (US)], using three procedures (delay, trace and control). During experiments, the CS signalled at a random time between 180 and 300 s for 30 s (six times per day). For the delay the US overlapped in time with the CS, for the trace the US delivered 10 s after the CS and for our control the US was delivered at random time between 180 and 300 s after the CS. H. portusjacksoni sharks trained in all procedures improved consistently in their time to obtain food, indicative of Pavlovian learning. Importantly, the number of sharks in the feeding area 5 s prior to CS onset did not change over time for any procedures. However, significantly more sharks were present 5 s after CS onset for delay for both air-bubble and light CS. Sharks trained in the delay and trace procedures using air-bubbles as the CS also displayed significantly more anticipatory behaviours, such as turning towards the CS and biting. Sharks trained with the light CS did not exhibit such behaviours; however, trace procedural sharks did show a significant improvement in moving towards the CS at its onset. At 20 and 40 days after the end of the conditioning experiments, some sharks were presented the CS without reward. Two sharks trained in the delay procedure using air-bubbles as the CS exhibited biting behaviours: one at 20 and the other at 40 days. This study demonstrates that H. portusjacksoni have the capacity to learn a classical conditioning procedure relatively quickly (30 trials during 5 days) and associate two time-separated events and retention of learnt associations for at least 24 h and possibly up to 40 days.

A learning and memory area in the octopus brain manifests a vertebrate-like long-term potentiation

Journal of …, 2003

Cellular mechanisms underlying learning and memory were investigated in the octopus using a brain slice preparation of the vertical lobe, an area of the octopus brain involved in learning and memory. Field potential recordings revealed long-term potentiation (LTP) of glutamatergic synaptic field potentials similar to that in vertebrates. These findings suggest that convergent evolution has led to the selection of similar activity-dependent synaptic processes that mediat e complex forms of learning and memory in vertebrates and invertebrates. Martin SJ, Grimwood PD, Morris RG. Synaptic plasticity and memory: an evaluation of the hypothesis. Annu Rev Neurosci 23: 649-711, 2000. Matzner H, Gutfreund Y, Hochner B. Neuromuscular system of the flexible arm of the octopus: physiological characterization.

Learning in fishes: from three-second memory to culture

2003

Learning plays a pivotal role in the behavioural development of all vertebrates, and fish are no exception. This collection of essays on learning in fishes is timely for at least two reasons. First, it is now over 10 years since the last substantive survey of the role of learning in fish behaviour (Kieffer and Colgan 1992) had been conducted, and the intervening period has witnessed a relative explosion of interest in this topic.

Neuromodulatory pathways in learning and memory: Lessons from invertebrates

Journal of Neuroendocrinology, 2020

In an ever-changing environment, animals have to continuously adapt behavior. The ability to learn from experience is crucial for animals to increase their chances of survival. It is therefore not surprising that learning and memory evolved early in evolution and are mediated by conserved molecular mechanisms. A broad range of neuromodulators, in particular monoamines and neuropeptides, have been found to influence learning and memory, but our knowledge on their modulatory functions in learning circuits remains fragmentary. Many neuromodulatory systems are evolutionarily ancient and well-conserved between vertebrates and invertebrates. Here, we highlight general principles and mechanistic insights on the actions of monoamines and neuropeptides in learning circuits that have emerged from invertebrate studies. Diverse neuromodulators have been shown to influence learning and memory in invertebrates, which can have divergent or convergent actions at different spatiotemporal scales. In addition, neuromodulators can regulate learning dependent on internal and external states, such as food and social context. The strong conservation of neuromodulatory systems, the extensive toolkit and compact learning circuits in invertebrate models makes these powerful systems to further deepen our understanding of neuromodulatory pathways involved in learning and memory.