Review
Cellular mechanisms of behavioral plasticity in terrestrial snail

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Abstract

Functional organization of networks underlying withdrawal, feeding, and respiration in terrestrial gastropod snail Helix are described. Tracking the changes during non-associative and associative modifications of behavior, analysis of plasticity mechanisms in identified neurons involved in these networks allowed to formulate several conceptual principles which are not widely accepted. The review will present data underlying the following principles:

  • 1.

    Command neuron concept can be applied only to all-or-none behavior.

  • 2.

    Habituation is an active down-regulation process opposite to up-regulating sensitization. All long-term behavioral changes at least in part are associative.

  • 3.

    Reinforcement is a motivational state mediated by neuromodulatory neurons and can be produced by activity of a single modulatory neuron.

  • 4.

    Non-addressed (‘soft-wired’) neuromodulatory influences are necessary for acquisition of memory, while retention of memory depends mostly on ‘hard-wired’ local changes in synaptic connectivity.

  • 5.

    Retrieval of declarative (sensory) and procedural (motor) memory involves different functional classes of neurons.

Introduction

It is not necessary now to praise the usefulness of neurobiological investigations in invertebrates. A number of neuroscientists interested in cellular analysis of behavior are exploiting the unique properties of invertebrate nervous systems, relatively simple and stereotyped behavior. Investigations of cellular mechanisms of learning and memory in invertebrates became an important part of contemporary neuroscience.

Learning (as a part of behavior) is an emergent property of the nervous system. Pinsker [1] defined an emergent property as the one possessed by an entire system but not by its individual components. We consider the concept of emergence to be the main problem for anyone using reductionist strategy in his research. Since an emergent property is not possessed by the individual components, there is only one sequence to follow when analyzing underlying mechanisms. One should begin with characterization of the phenomenon as a whole and then isolate the components for analysis. Molluscans provide an extremely useful model in this respect taking into account that their behavior is relatively complex, and the nervous network is relatively accessible for the analysis. But is their behavioural repertoire relevant for the psychological problems? There have been a number of demonstrations of higher brain functions (including associative learning) in a variety of invertebrates including Helix [2], [3], [4], [5], [6]. Even a possibility for self-stimulation was shown in terrestrial snails by Balaban and Chase [7].

A detailed analysis of behavior is a necessary prerequisite of neurophysiological studies. Present work is a review (some results were published only in Russian) concerning the description of two types of memory in terrestrial snails (Helix sp.), and an investigation of the role of individual cells and neuromodulatory systems in learning. By analyzing the behavior and memory in snails, it was possible to distinguish declarative memory (which do not require any motor response to a certain stimuli, but can influence behavioral performance), and a procedural memory, which is manifested in changes in certain motor responses to a certain stimuli.

One of the most difficult problems in neurobiology is functional identification of neurons involved in network underlying certain behavior. Only primary sensory neurons and motor neurons can be easily identified due to their morphological connections to receptors and muscles. All other neurons involved in behavior interact with one another, and detecting their contribution to behavior constitutes an independent task.

Section snippets

Functional organization of Helix nervous system

Using relatively simple nervous system of terrestrial snail Helix we tried to formulate criteria for the identification of behavioral function of neurons and to describe the networks involved in withdrawal, feeding, and respiration.

Non-associative forms of behavioral plasticity

Usually, two simplest forms of behavioral plasticity—habituation (negative learning) and sensitization (facilitation, dehabituation, etc.) are considered as independent ones. In spite of the existence of independent mechanisms underlying habituation and sensitization, we will consider them as a cooperative system.

Most of our data concerning simple forms of behavioral plasticity conforms to the dual-process theory of habituation delineated in 1970 by Groves and Thompson [39], [40]. The main

Associative forms of behavioral plasticity

At the present time there is no doubt that associative modifications of behavior may be elaborated in gastropods. History of attempts of elaboration of conditioned response in snails starts with experiments of Thompson [72] in pond snail Physa gyrina. He associated tactile stimulation of foot with food presentation, and after 250 paired trials in 2 days the tactile CS elicited feeding responses in 39.6% of cases compared to 3.3% before conditioning. Unfortunately, no controls for associativity

Applicability of the reinforcement concept to studies in simple nervous systems

The reinforcement concept is widely used in studies of learning and memory mechanisms which have been performed in the last few decades, not only at the behavioral level, but also in model systems, such as brain slices, invertebrate isolated nervous systems and synaptically connected neurons in vitro and in vivo. In these studies the terminology elaborated for animal behavior has mainly been used. In this section analyzing the limitations and applicability of the behavioral concept of

Conclusions and perspectives: induction of learning and retention of changes, hardwired synaptic connections and modulation

Going by the reductionist way and studying more and more local events in the network, cell, synapse, membrane, ionic channel, we inevitably are losing the functioning of the brain as a whole entity, which may have emergent properties not attributable to its parts. Having in mind to locate the sites of plasticity, it is interesting to compare the behavioral learning and the local synaptic plasticity in order to explicitly delineate the limits of discussed phenomena.

During elaboration of the

Acknowledgements

Author thanks his coworkers N. Bravarenko, V. Ierusalimski, O. Maksimova, A. Malyshev, and I. Zakharov for help. The work was supported by grants of the Russian Foundation for Basic Research, INTAS grant 99-1481, and Howard Hughes Medical Institute grant #75195-544301.

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