Pavlovian appetitive discriminative conditioning inAplysia californica

Abstract

Three experiments demonstrated Pavlovian appetitive discrimination learning in the marine mollusc, Aplysia californica. In each experiment, subjects were exposed to two conditioned stimuli; one stimulus (CS+) was paired with food presentations and the other stimulus (CS-) was never followed by food. In Experiments 1 and 3 different chemosensory stimuli were used, and in Experiment 2 different tactile stimuli were used. For both types of conditioned stimuli, bite responses occurred significantly more often to the CS+ than to the CS-. Experiment 2 also showed that Aplysia could learn a reversal of this discrimination. Experiment 3 showed that nonreinforced presentations of CS+ resulted in a decline in the frequency of conditioned biting. The implications of these results for neurobiological analyses of learning are discussed.In a typical Pavlovian discriminative conditioning procedure, subjects are exposed to two conditioned stimuli (CSs) that differ in their temporal relation to an unconditioned stimulus (US). One of these stimuli (CS+) immediately precedes presentations of the US; the other stimulus (CS-) is never paired with that US. Differential responding to the CS+ and CS-is found to emerge over the course of discrimination training in various vertebrate (e.g., Hammond, 1967;Hoffman & Fitzgerald, 1982;Moore, 1972;Pavlov, 1927;Rescorla, 1980;Schneiderman, 1972) and invertebrate subjects (e.g., Bitterman, Menzel, Fietz, & Schafer, 1983;Block & McConnell, 1967;Fukushi, 1979;Nelson, 1971;Ricker, Brzorad, & Hirsch, 1986).Of particular interest are reports of Pavlovian discriminative conditioning in those invertebrates especially suited to a neurophysiological analysis of plasticity. Behavioral sensitivity to the differential treatments ofa CS+ and CS -has been found in several experiments using aversive USs with the marine mollusc Aplysia califomica , the leech Haemopis marmorata (Karrer & Sahley, 1988), and the terrestrial mollusc Limax maximus (Sahley, Gelperin, & Rudy, 1981). For example, in the leech, Karrer and Sahley (1988) paired one food (e.g., raw chicken) but not This research was supported by National Science Foundation Grant BNS-8922551 to R.M.C. and by funds from the Howard Hughes Medical Institute. K.G. and A.M. were supported by research fellowships awarded by Brown University's Early Identification Program. We thank Robin Absher and Emily Whitcomb for assistance with data collection. Experiment 1 was presented at the 65th Annual Meeting ofthe Eastern Psychological Association in Providence and at the Second Annual Summer Research Symposium at Brown University in August 1993. A brief description of Experiment 1 also appears in Colwill (1996). Reprint requests should be addressed to R. M. Colwill, Department of Psychology, Brown University, Box 1853, Providence, RI 02912 (e-mail: ruth_colwill@brown.edu).another food (e.g., raw liver) with a quinidine sulfate solution. On test trials, subjects were given a choice between raw beefand either the CS+ or the CS-foods. The preference for the CS+ relative ...

Chemosensory conditioning in molluscs: II. A critical review

“…Prior to any conditioning, these chemosensory stimuli elicit overt and conspicuous behaviors, such as feeding and disruption of escape locomotion (e.g., Figure 4C in Walters, Carew, & Kandel, 1979). Food (solid or extract) has been used as an US to condition feeding responses to other CSs-typically, novel chemical or tactile stimuli (Audesirk et al, 1982;Colwill et al, 1997;Kemenes & Benjamin, 1989;Mpitsos & Davis, 1973)-and to countercondition a preference for an innately aversive odor in Limax (Sahley et al, 1990). In short, food extracts are powerful stimuli that affect multiple sensory, motivational, and behavioral systems in gastropod molluscs.…”

“…Consider studies by Colwill and colleagues (Colwill et al, 1988;Colwill, Goodrum, & Martin, 1997), who have presented strong evidence for context discrimination learning by Aplysia. In an aversive context-conditioning study using two distinct environments that differed in substrate texture, shape, chemosensory composition, and other cues, Colwill et al (1988) administered a series of electric shocks in one context (CSϩ), but not in the other (CSϪ).…”

“…Using a Pavlovian appetitive discrimination-learning paradigm with Aplysia, Colwill et al (1997) obtained evidence for selective responding to discrete CSϩs. These experiments are noteworthy for two reasons.…”

Reinforcement in an in vitro analog of appetitive classical conditioning of feeding behavior in Aplysia: Blockade by a dopamine antagonist

“…Methylergonovine (1 nM) blocked the pairing-specific increase in fictive feeding that is usually induced by in vitro classical conditioning. The present results and previous observation that methylergonovine also blocks the effects of contingent reinforcement in an in vitro analog of appetitive operant conditioning suggest that DA mediates reinforcement for appetitive associative conditioning of feeding in Aplysia.The feeding behavior of Aplysia californica provides an attractive model system for investigating the cellular and molecular mechanisms underlying associative learning (see Susswein and Schwartz 1983;Colwill et al 1997; Elliot and Susswein 2002;Katzoff et al 2002;Brembs 2003;Brembs et al 2004;Cropper et al 2004). For example, aspects of feeding behavior (i.e., biting) can be modified by appetitive classical conditioning (Colwill et al 1997;Lechner et al 2000a); the isolated nervous system readily generates fictive feeding patterns (see Church and Lloyd 1994;Nargeot et al 1997); neural correlates of conditioning can be identified and studied in the isolated nervous system (Lechner et al 2000b;Lorenzetti et al 2004); and in vitro analogs, which are amenable to cellular and molecular analyses, recapitulate behavioral and neural changes that follow in vivo training (Mozzachiodi et al 2003;Brembs et al 2004;Lorenzetti et al 2004).…”

“…For example, aspects of feeding behavior (i.e., biting) can be modified by appetitive classical conditioning (Colwill et al 1997;Lechner et al 2000a); the isolated nervous system readily generates fictive feeding patterns (see Church and Lloyd 1994;Nargeot et al 1997); neural correlates of conditioning can be identified and studied in the isolated nervous system (Lechner et al 2000b;Lorenzetti et al 2004); and in vitro analogs, which are amenable to cellular and molecular analyses, recapitulate behavioral and neural changes that follow in vivo training (Mozzachiodi et al 2003;Brembs et al 2004;Lorenzetti et al 2004). Several lines of evidence indicate that the esophageal nerve (En) mediates the effects of the unconditioned stimulus (US) during appetitive classical conditioning.…”