Pavlovian Conditioning ofHermissenda: Current Cellular, Molecular, and Circuit Perspectives

Abstract

The less-complex central nervous system of many invertebrates make them attractive for not only the molecular analysis of the associative learning and memory, but also in determining how neural circuits are modified by learning to generate changes in behavior. The nudibranch mollusk Hermissenda crassicornis is a preparation that has contributed to an understanding of cellular and molecular mechanisms of Pavlovian conditioning. Identified neurons in the conditioned stimulus (CS) pathway have been studied in detail using biophysical, biochemical, and molecular techniques. These studies have resulted in the identification and characterization of specific membrane conductances contributing to enhanced excitability and synaptic facilitation in the CS pathway of conditioned animals. Second-messenger systems activated by the CS and US have been examined, and proteins that are regulated by one-trial and multi-trial Pavlovian conditioning have been identified in the CS pathway. The recent progress that has been made in the identification of the neural circuitry supporting the unconditioned response (UR) and conditioned response (CR) now provides for the opportunity to understand how Pavlovian conditioning is expressed in behavior.The analysis of learning in several vertebrate and invertebrate nervous systems has generated a number of candidate mechanisms of Pavlovian conditioning involving changes in both cellular excitability and synaptic strength. In general, studies of associative learning in these model systems have been dominated by the search for mechanisms of Pavlovian conditioning that provide an explanation for temporal contiguity between the conditioned stimulus (CS) and unconditioned stimulus (US). However, a comprehensive analysis of associative learning requires an understanding of all aspects of the associative process, including the generation of behavior, in addition to providing insights into mechanisms of temporal contiguity. The issue of how learning is expressed in behavior may be effectively addressed by studying conditioning from a cellular and synaptic perspective in the relatively simple nervous system of invertebrates. The analyses of learning in several model systems have used a combination of cellular and synaptic physiology in conjunction with a neural circuit analysis to examine how Pavlovian conditioning is expressed in behavior, or how learning results in the generation of a conditioned response (CR). Some invertebrate preparations are especially attractive for this type of analysis, as the neural circuitry supporting behaviors involving muscular contraction, respiration, locomotion, and feeding is known in considerable detail (for review, see Sahley and Crow 1998).One animal that has contributed to an understanding of the physiology of learning and memory at a cellular, synaptic, and systems level of analysis is the nudibranch mollusk Hermissenda crassicornis. Associative learning in Hermissenda has been extensively examined using a Pavlovian conditioning procedure. The Hermissenda central...

Operant Conditioning of Gill Withdrawal inAplysia

“…A good deal is known about the cellular mechanisms of an associative form of learning, classical conditioning, as well as nonassociative forms of learning of several invertebrate behaviors (Hawkins et al, 1987;Benjamin et al, 2000;Burrell and Sahley, 2001;Menzel, 2001;Roman and Davis, 2001;Crow, 2004), including the gill-and siphon-withdrawal reflex in Aplysia (Hawkins et al, 1993;Antonov et al, 2001Antonov et al, , 2003Roberts and Glanzman, 2003). In recent years, there also has been progress in understanding mechanisms of another associative form of learning, operant conditioning, in invertebrates (Brembs, 2003), allowing comparisons with mechanisms of both classical conditioning and nonassociative forms of learning.…”

Cognition in Invertebrates

“…The conditioning procedure consists of pairing light CS with high-speed rotation, or orbital shaking (US) which are aversive stimuli for the snail (Crow, 2004). Two responses are elicited by rotation, a reduced rate of forward locomotion and foot shortening.…”

Associative Memory Stored by Functional Novel Pathway rather than Modifications of Preexisting Neuronal Pathways

“…Alternatively, existing synapses may be nonfunctional or too weak to mediate a strong effect on feeding activity in naive animals before conditioning. Strengthening of weak synapses has been demonstrated to underlie various conditioning paradigms (Kandel and Schwartz, 1982;Glanzman, 1995;Hawkins et al, 1998;Antonov et al, 2003;Roberts and Glanzman, 2003;Wickens et al, 2003;Crow, 2004), whereas the activation of silent synapses has been suggested to contribute to long-term potentiation (Montgomery et al, 2001;Voronin and Cherubini, 2004). Regardless of the underlying mechanism, our results suggest that conditioning leads to the creation of a functionally new pathway, probably attributable to the enhanced recruitment of CBIs to the CS processing pathway, which enables the CS to activate feeding after conditioning.…”