Rapid, nonaversive conditioning in a freshwater gastropod

Audesirk, Teresa; Alexander, James Edward; Audesirk, Gerald; Moyer, Carol M.

doi:10.1016/s0163-1047(82)90782-8

Cited by 63 publications

(42 citation statements)

References 30 publications

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“…In conditioning of feeding behavior, amyl acetate (the CS) is paired with sucrose, [the unconditioned stimulus (US)], resulting in the formation of an associative long-term memory (Alexander et al, 1984). Although the CS has been reported to be neutral with respect to feeding Audesirk et al, 1982), we show here that, before conditioning, amyl acetate can both excite and inhibit feeding behavior depending on its concentration. Our knowledge of the Lymnaea feeding system (Benjamin and Elliott, 1989;Benjamin et al, 2000;Kemenes et al, 2001;Straub et al, 2002) allowed us to identify the neural pathways serving the excitatory and inhibitory effects on feeding in naive animals.…”

Section: Introductioncontrasting

confidence: 64%

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

Straub

Kemenes²,

O’Shea³

et al. 2006

J. Neurosci.

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Associative conditioning involves changes in the processing pathways activated by sensory information to link the conditioned stimulus (CS) to the conditioned behavior. Thus, conditioning can recruit neuronal elements to form new pathways for the processing of the CS and/or can change the strength of existing pathways. Using a behavioral and systems level electrophysiological approach on a tractable invertebrate circuit generating feeding in the mollusk Lymnaea stagnalis, we identified three independent pathways for the processing of the CS amyl acetate used in appetitive conditioning. Two of these pathways, one suppressing and the other stimulating feeding, mediate responses to the CS in naive animals. The effects of these two pathways on feeding behavior are unaltered by conditioning. In contrast, the CS response of a third stimulatory pathway is significantly enhanced after conditioning, becoming an important contributor to the overall CS response. This is unusual because, in most of the previous examples in which naive animals already respond to the CS, memory formation results from changes in the strength of pathways that mediate the existing response. Here, we show that, in the molluscan feeding system, both modified and unmodified pathways are activated in parallel by the CS after conditioning, and it is their integration that results in the conditioned response.

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Section: Introductioncontrasting

confidence: 64%

“…Amyl acetate has been described previously as a neutral feeding stimulus Audesirk et al, 1982). However, by applying different concentrations of the CS, we identified excitatory and inhibitory feeding responses in naive snails.…”

Section: Identification Of Cs Pathways In Naive Snailsmentioning

confidence: 98%

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

Straub

Kemenes²,

O’Shea³

et al. 2006

J. Neurosci.

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“…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.…”

Section: Discussionmentioning

confidence: 99%

“…Food-satiated Hermissenda exhibit large elevations in feeding thresholds and frequently show an active aversion to food (Ram, Noirot, Waddell, & Anderson, 1988). In other molluscs (e.g., Lymnaea), satiation has also been shown to disrupt both the acquisition (Audesirk, Alexander, Audesirk, & Moyer, 1982;Kemenes & Benjamin, 1994) and the expression (Audesirk et al, 1982) of conditioned feeding responses. It seems likely that similar interference effects occurred here with Hermissenda.…”

Section: Nonassociative Sources Of Feeding Suppression In Hermissendamentioning

confidence: 99%

Chemosensory conditioning in molluscs: II. A critical review

Farley

Jin

Huang

et al. 2004

Learning & Behavior

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We critically review chemosensory conditioning studies with molluscs and find that, in many studies, the influence of nonassociative processes complicates, obscures, and renders ambiguous the unique contribution of associative learning. These nonassociative processes include sensory adaptation, habituation, sensitization, and changes in feeding motivation. They arise from both the food extracts that have often been used as conditioned stimuli and the aversive stimuli that have been used as unconditioned stimuli.

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“…This is particularly true for the identification of potential food sources, initiation of feeding, and the detection of predators and noxious stimuli (Audesirk & Audesirk, 1985;Croll, 1983;Kohn, 196I;Kupfermann, 1974;Preston & Lee, 1973). Furthermore, the capacity ofchemosensory systems to participate in the conditioning of invertebrates is well established (Audesirk, Alexander, Audesirk, & Moyer, 1982;Farley et aI., 1990;Sahley et aI., 1990;Sahley et aI., 198 I;Walters, Carew, & Kandel, 1981).…”

Section: Methodsmentioning

confidence: 99%

Chemosensory-based contextual conditioning inHermissenda crassicornis

Rogers

Schiller

Matzel

1996

Animal Learning & Behavior

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In two experiments, the marine mollusk Hermissenda crassicornis was exposed to context discrimination training. In one context, defined by the presence of a diffuse chemosensory stimulus (shellfish extract A), brief, unsignaled, unconditioned stimuli (USs; high-speed rotation) were presented; in a second context, defined by the presence of shellfish extract B, no USs were presented. Animals were then tested (at both 1.5 and 24 h) by exposing them to small pieces of the shellfish meat used to define the two contexts. The latency to strike at the meat served as an index of the context-US association. In Experiment 1, the latency to strike at the cue associated with rotation was reduced relative to both preconditioning strike latencies and the associatively neutral cue. However, in a two-choice test where the animals could approach the conditioned or neutral stimulus, the animals regularly avoided the stimulus paired with rotation. Moreover, if, following conditioning, the animals were presented with an unsignaled rotation in the conditioned context or the neutral context, the animals exhibited more effective defensive clinging (an unconditioned reflex normally elicited by rotation) in the conditioned context, suggesting that it "prepared" the animal for the aversive US. In total, these results demonstrate that Hermissenda is capable of making associations to diffuse background (contextual) stimuli. Moreover, the results suggest that pairing the chemosensory cue with an aversive USelicits a strike response in Hermissenda when the animal is placed in forced contact with the cue and an active avoidance response when the animal can choose between that cue and a neutral cue.

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Rapid, nonaversive conditioning in a freshwater gastropod

Cited by 63 publications

References 30 publications

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

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

Chemosensory conditioning in molluscs: II. A critical review

Chemosensory-based contextual conditioning inHermissenda crassicornis

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