Edgar T. Walters

Classical conditioning in a simple withdrawal reflex in Aplysia californica

The ability of Aplysia and other gastropod molluscs to exhibit complex behaviors that can be modified by associative learning has encouraged us to search for an elementary behavior controlled by a simple and well analyzed neural circuit that also can be modified by this type of learning. Toward that end, we have now produced classical conditioning in the defensive siphon and gill withdrawal reflex of Aplysia. We used as a conditioned stimulus (CS) a light tactile stimulus to the siphon, which produces weak siphon and gill withdrawal. As the unconditioned stimulus (US), we used a strong electric shock to the tail, which produces a massive withdrawal reflex. Specific temporal pairing of the CS and US endowed the CS with the ability of triggering enhanced withdrawal of both the siphon and the gill. Random or unpaired presentations of the CS and US, as well as presentations of the CS or US alone, produced either no enhancement or significantly less enhancement than paired presentations of the CS and US. The conditioning is acquired rapidly (within 15 trials) and is retained for several days. The conditioned response is abolished completely by removal of the abdominal ganglion and many of the neurons involved in the conditioning have been identified in this ganglion previously. These include the sensory neurons and several interneurons in the CS pathway and the siphon and gill motor neurons of the conditioned and unconditioned response pathways. Moreover, the sensory neurons of the US pathway have been identified in the pleural ganglia. As a result of its simplicity, it should be possible in this reflex to specify neurons that are causally related to the conditioned response. Since this reflex also exhibits nonassociative learning, it also may be possible to compare associative and nonassociative learning on a mechanistic level.

Motorneuronal control of locomotion in Aplysia.

We have carried out a combined behavioral and cellular analysis of escape locomotion in Aplysia. Using videotape recording we obtained a detailed description of the coordinated movements of the different regions of the foot and body during locomotion. Alternating waves of extension and longitudinal contraction begin at the head and propagate caudally through each pedal segment at a constant rate. Cobalt backfill of pedal nerves indicated that certain regions of the pedal ganglia were likely to contain motor neurons for the foot and body wall musculature. We examined these areas using intracellular techniques and identified three unique cells and three regional classes of neurons having clear motor effects on the foot and body wall. We also found that locomotion is driven by a central program. The basic locomotor pattern of the identified motor neurons and regional classes of motor neurons persists even after the circumesophageal ganglia have been isolated from the periphery. The motor neurons are not synaptically interconnected; patterned bursting during locomotor activity is produced by cyclic synaptic input. Because the locomotor system has large neurons favorable for cellular analysis and because locomotion is characterized by features of both stereotypy and flexibility, Aplysia promises to be useful for investigating the mechanisms underlying both the generation and modulation of a central program.

Classical Conditioning in Aplysia: Neuronal Circuits Involved in Associative Learning

Recent analyses of the neural control of learning and memory suggest that one needs to identify and examine the neuronal circuitry specific to the behavior that is modified by the learning in order to study the cellular mechanisms underlying these processes. In this paper we describe an example of a simple form of classical conditioning in the gastropod mollusk Aplysia californica. This example of associative learning offers considerable promise for a cellular analysis because it involves relatively simple and well-analyzed neuronal circuits. Knowledge of the neuronal circuits involved in the conditioning pathways is reviewed, and a preliminary hypothesis for the mechanisms of this form of classical conditioning is considered.

Habituation, Sensitization and Associative Learning in Aplysia

A central problem in the study of behavior is how various forms of learning are interrelated. Are they governed by separate mechanisms or by variations on a common mechanism? A particularly important question concerns the relationship between simple nonassociative learning and more complex associative forms. A comparison of the mechanisms underlying these different types of learning requires an experimentally advantageous animal in which both non associative and associative learning can be studied on the cellular level. Because of the relative simplicity of its nervous system, the marine snail Aplysia has been useful for cellular studies of the mechanisms of nonassociative learning. We have found recently that this animal is also capable of associative learning. This capability permits us to compare these two classes of learning.

BEHAVIORAL AND CELLULAR STUDIES OF ASSOCIATIVE LEARNING IN APLYSIA

Publisher Summary This chapter discusses the behavioral and cellular studies of associative learning in aplysia, which can form a classically conditioned association between a chemosensory conditioned stimulus (CS) and an aversive unconditioned stimulus (US). In the locomotor system, where the learned behavior is expressed as an increase in a recurrent motor sequence, the CS enhances the output of the central program, leading to an increase in the number of spike bursts in the motor neurons. However, in the inking and siphon withdrawal systems, where the learning is expressed as a decrease in threshold or an increase in response amplitude, the CS enhances afferent synaptic input directly onto the motor neurons. An identification of neuronal elements influencing each of the several defensive motor systems that express the associative learning should be useful for mapping the circuitry responsible for both the performance and acquisition of associative learning.