Feeding behavior of Aplysia: a model system for comparing cellular mechanisms of classical and operant conditioning

Feeding behavior of Aplysia provides an excellent model system for analyzing and comparing mechanisms underlying appetitive classical conditioning and reward operant conditioning. Behavioral protocols have been developed for both forms of associative learning, both of which increase the occurrence of biting following training. Because the neural circuitry that mediates the behavior is well characterized and amenable to detailed cellular analyses, substantial progress has been made toward a comparative analysis of the cellular mechanisms underlying these two forms of associative learning. Both forms of associative learning use the same reinforcement pathway (the esophageal nerve, En) and the same reinforcement transmitter (dopamine, DA). In addition, at least one cellular locus of plasticity (cell B51) is modified by both forms of associative learning. However, the two forms of associative learning have opposite effects on B51. Classical conditioning decreases the excitability of B51, whereas operant conditioning increases the excitability of B51. Thus, the approach of using two forms of associative learning to modify a single behavior, which is mediated by an analytically tractable neural circuit, is revealing similarities and differences in the mechanisms that underlie classical and operant conditioning.     

Identification of a reinforcement pathway necessary for operant conditioning of head waving in Aplysia californica

The marine mollusc Aplysia californica exhibits a wide range of nonassociative and associative forms of learning. Recently, we found that the learning repertoire of Aplysia includes operant conditioning (Cook & Carew, 1986, 1989b). The behavior we examined is a naturally occurring, side-to-side head-waving response used by Aplysia in seeking food, obtaining a foothold, and egg laying. Aplysia can be operantly conditioned to reduce head-waving to one side of their body if such a response results in exposure to bright uniform-field illumination, which the animals find aversive. An essential step toward achieving a mechanistic understanding of operant conditioning is to identify and characterize the reinforcement pathway used during the learning. Toward this end, we wished to determine which of the peripheral visual pathways in Aplysia are critical for performance of the operant task. Previous experiments indicated that photic input from the optic and rhinophore nerves functionally inhibited motor neurons that participate in the operant response (head-waving), while photic input from the oral veil nerves excited these same motor neurons (Cook & Carew, 1989c). These findings suggested the hypothesis that one or both of these pathways could play an important role in mediating reinforcement during training. To explore this possibility we operantly trained animals that had received chronic bilateral transections of either the optic and rhinophore nerves or the oral veil nerves C1-C3 (in conjunction with transection of the optic and rhinophore nerves). We found that operant conditioning was not disrupted by ablation of input from the eyes and rhinophores. By contrast, ablation of input from the oral veil (together with that from the eyes and rhinophores) abolished operant conditioning. Thus, the oral veil nerves play a critical modulatory role in operant conditioning of head-waving. This observation further suggested that photic input from the oral veil is conveyed to the CNS via the oral veil nerves. In a final experiment we confirmed that stimulation of the oral veil with light evokes increased afferent activity in the oral veil nerves C1-C2. These results support the idea that the oral veil nerves contain processes that are critical components of the reinforcement pathway for operant conditioning of head-waving.     

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

In a recently developed in vitro analog of appetitive classical conditioning of feeding in Aplysia, the unconditioned stimulus (US) was electrical stimulation of the esophageal nerve (En). This nerve is rich in dopamine (DA)-containing processes, which suggests that DA mediates reinforcement during appetitive conditioning. To test this possibility, methylergonovine was used to antagonize DA receptors. 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.     

Discriminated response and incentive processes in operant conditioning: a two-factor model of stimulus control

Understanding stimulus control generated in instrumental learning requires the direct investigation of discriminated response and reinforcer (incentive) processes acquired exclusively through the response-reinforcer contingencies operating on complex (multicomponent) baselines. Two series of stimulus-compounding studies accomplished this direct investigation. In one series, the independent variable was the relative reinforcement between schedule components; in the second series, it was relative response rate between components. Stimulus-compounding tests revealed that response and incentive processes enhanced each other when in agreement, counteracted each other when in opposition, and produced intermediate results when only one factor was operating. This pattern of results led to the conclusion that these factors were algebraically combining and to the development of a response/incentive matrix reflecting these dynamics. This two-factor analysis was extended to the peak-shift effect in stimulus generalization experiments and to the generation of inhibitory control. Two decades of stimulus compounding and peak-shift research were organized within this two-factor framework, extending this traditional approach to learning to active research areas heretofore not systematically considered in these terms.     

Extraversion and reinforcement in verbal operant conditioning.

The present investigation was designed to study the relationship between extraversion and modes of reinforcement in verbal operant conditioning. A 4 X 3 randomized block design was replicated ten times. Eighty graduate and post-graduate male students were individually subjected to the standard Taffel conditioning procedure. When the numbers of conditioned responses produced by introverts and extraverts were compared, it was found that: (1) under negative reinforcement ('bad' and electric shock), with both the female and male experimenters, and under positive reinforcement ('good') with the male experimenter, the introverts' score was the higher of the two; (2) under positive reinforcement ('good') with the female experimenter, the extraverts' score was higher than that of the introverts.     

In vitro analog of classical conditioning of feeding behavior in aplysia

The feeding behavior of Aplysia californica can be classically conditioned using tactile stimulation of the lips as a conditioned stimulus (CS) and food as an unconditioned stimulus (US). Moreover, several neural correlates of classical conditioning have been identified. The present study extended previous work by developing an in vitro analog of classical conditioning and by investigating pairing-specific changes in neuronal and synaptic properties. The preparation consisted of the isolated cerebral and buccal ganglia. Electrical stimulation of a lip nerve (AT4) and a branch of the esophageal nerve (En2) served as the CS and US, respectively. Three protocols were used: paired, unpaired, and US alone. Only the paired protocol produced a significant increase in CS-evoked fictive feeding. At the cellular level, classical conditioning enhanced the magnitude of the CS-evoked synaptic input to pattern-initiating neuron B31/32. In addition, paired training enhanced both the magnitude of the CS-evoked synaptic input and the CS-evoked spike activity in command-like neuron CBI-2. The in vitro analog of classical conditioning reproduced all of the cellular changes that previously were identified following behavioral conditioning and has led to the identification of several new learning-related neural changes. In addition, the pairing-specific enhancement of the CS response in CBI-2 indicates that some aspects of associative plasticity may occur at the level of the cerebral sensory neurons.     

Operant conditioning of epileptic neurons in monkeys and its theoretical application to EEG operant conditioning in humans

This paper reviews a series of previous reports which summarize the physiology of chronic experimental epileptic foci in monkeys. It is shown that such monkeys can be trained to bidirectionally control the firing rates of normal and epileptic neurons which comprise the epileptic focus. As a result of this acquired operant performance, the monkeys show both a decrease in clinical seizures as well as a decrease in single unit epileptic activity. The EEC correlate of this change in single unit epileptic actvity is generalized EEG desynchronization. The conclusion from these data would indicate epileptic neurons can be operantly controlled and this control is not correlated with any specific EEG pattern. This brings to question the specificity of the SMR in EEG biofeedback paradigms which treat human epilepsy. This author feels that the result from such biofeedback studies are the result of the patient learning to manipulate electrical events within the CNS pathways through which the seizure propagates and is not contingent upon specific EEG frequencies.     

A comparison of the effects of vicariously instigated classical conditioning and direct classical conditioning procedures

Two groups of Ss received either two or 16 paired classical conditioning trials beyond the peak CR. A third group received the same stimuli as in the 16 postpeak condition but in an unpaired and random order. The stimuli in all three groups were delivered directly to S. Subsequently, all three groups, including a fourth which was not given any prior direct classical conditioning, were exposed to vicariously instigated classical conditioning. This consisted of havingS observe someone (model) employed byE who received the same CS as was delivered during direct conditioning. The CS was paired with the feigned arm movement of the model, simulating a reaction to shock. This vicarious classical conditioning procedure when compared to direct classical conditioning resulted in smaller GSR magnitudes for both the CRs and UCRs. Previous experience with direct classical conditioning seems to have had an attenuating effect on GSR magnitude during the vicarious situation. A postexperimental questionnaire tended to support the results, and the relationship between the present study and current classical conditioning theory is discussed.     

The use of operant conditioning to reinstate speech in mute schizophrenics

Eighteen schizophrenic patients who had been mute from 3 to 37 years were selected by means of a speech test. Nine of these were positively reinforced for speaking and nine were reinforced for staying silent. After 25 sessions the speech-reinforced group had improved significantly more than the silence-reinforced group.     

Ontogeny of classical and operant learning behaviors in zebrafish

The performance of developing zebrafish in both classical and operant conditioning assays was tested with a particular focus on the emergence of these learning behaviors during development. Strategically positioned visual cues paired with electroshocks were used in two fully automated assays to investigate both learning paradigms. These allow the evaluation of the behavioral performance of zebrafish continuously throughout development, from larva to adult. We found that learning improves throughout development, starts reliably around week 3, and reaches adult performance levels at week 6. Adult fish quickly learned to perform perfectly, and the expression of the learned behavior is manifestly controlled by vision. The memory is behaviorally expressed in adults for at least 6 h and retrievable for at least 12 h.     

Impulsivity/sociability and reinforcement in verbal operant conditioning

The present investigation was designed to study the relationship between impulsivity/sociability and modes of reinforcement in verbal operant conditioning. Two 2x3 randomized block designs, one each for impulsivity and sociability, were replicated ten times. One hundred and twenty undergraduate female students (60 for impulsivity and 60 for sociability) were individually subjected to Taffel's verbal conditioning procedure. When the conditioning scores of high and low scorers on the impulsivity and sociability scales were compared, it was found that under rewarding conditions ('good' and 'buzzer' in respect of sociability and 'good' in respect of impulsivity) the high scorers' score and under punishing conditions ('electric shock') the low scorers' score was the higher of the two. The study also revealed that the high scorers (on the impulsivity scale) conditioned more under rewarding conditions while the low scorers (both on the impulsivity and sociability scales) conditioned more under punishing ones.     

Operant conditioning of an in vitro CNS-pneumostome preparation of Lymnaea

Operant conditioning of aerial respiratory behaviour and its consolidation into long-term memory in Lymnaea has been previously studied in both intact, freely moving snails and in in vitro preparations made from previously trained snails. Here, we show in previously untrained semi-intact in vitro Lymnaea preparations that aerial respiratory behaviour can also be operantly conditioned. Neither yoked control nor 'run-down' control procedures in these in vitro preparations result in an alteration of aerial respiratory behaviour. Memory in the operantly trained semi-intact preparations persists for at least 1h after training. Intracellular recordings made from RPeD1, one of the 3-CPG neurons and the neuron that initiates CPG activity; show that there are specific changes in central excitatory input to this neuron concurrent with learning and its consolidation into memory. In addition following the acquisition of learning and its consolidation into memory the ability of RPeD1 and VI/J neurons when depolarized to cause a pneumostome opening is significantly decreased. Thus, previously untrained in vitro semi-intact preparations can be used to study changes in neuronal activity in a neuron known to be both necessary for the behaviour and for memory formation.     

Associative competition in operant conditioning: blocking the response-reinforcer association

Naive rats were trained to leverpress with a 30-sec delay-of-reinforcement contingency from the start of training. In Experiment 1, the delay interval for different groups of subjects included a signal in the first 5 sec, a signal in the last 5 sec, or no signal at any time. Rats with the signal at the start of the delay interval learned most rapidly. Rats with the signal at the end of the delay failed to learn. In Experiment 2, a choice procedure was used, in which each of two levers was associated with its own 30-sec delay of reinforcement. The delay for one lever included a 5-sec signal at the end of the delay. The delay for the second lever had no signal in its 30-sec delay. Preference was in favor of the lever without the signal in the delay interval. The results demonstrate that the acquisition of new response can be blocked in a manner analogous to the blocking of Pavlovian conditioning.