Contextual conditioning and reinstatement of extinguished instrumental responding

In three experiments we studied the relationship between contextual conditioning and the reinstatement of extinguished lever pressing that occurs when noncontingent food is introduced following extinction. In all three experiments the non-contingent food was presented off-baseline (with the response levers not present). On subsequent tests, with the response levers present, animals that had been exposed to food showed more reinstatement of lever pressing than control animals. This finding rules out alternative mechanisms for the reinstated responding that rely on the interaction of non-contingent food and responding, such as superstitious reinforcement or the discriminative after-effects of food. In addition, in each experiment we demonstrated that manipulations known to affect contextual conditioning (signalling the food in Experiment 1, context extinction in Experiment 2, and switching contexts in Experiment 3) reduced the reinstatement. These results are consistent with the claim that contextual conditioning is important in controlling instrumental conditioning and closely parallel findings concerning the reinstatement of Pavlovian responsing following extinction.     

Overshadowing of a stimulus-reinforcer association by an instrumental response

In two experiments, rats were first exposed to pairings of a clicker and food; they were subsequently, in order to measure the effectiveness of the clicker as a conditioned reinforcer, given the opportunity to press a lever which turned the clicker on. For one group of animals the food originally delivered in the presence of the clicker had been contingent on their performance of an instrumental response (running in a running wheel); for a second the contingency between clicker and food had been purely classical. Although the actual correlation between clicker and food was identical for the two groups, the clicker was a less effective conditioned reinforcer for the first group than for the second. In a third experiment, all animals were initially required to run to obtain food in the presence of the clicker, but one group received additional trials on which food was delivered contingent on running in the absence of the clicker. This group showed less tendency to lever press for the clicker than a second group that had received free food on trials when the clicker was not presented. The results of all three experiments suggest that conditioning to the clicker could be overshadowed if the occurrence of food was more reliably predicted by the execution of an instrumental running response; they thus support the view that instrumental conditioning depends on the establishment of an association between response and reinforcer similar to the association between stimulus and reinforcer underlying classical conditioning.     

The role of response-contingent incentives in lithium chloride-mediated suppression of an operant response

Three experiments investigated what role a novel incentive plays in the development of operant response suppression mediated by lithium chloride. In all experiments animals were trained to press two levers under concurrent schedules of reinforcement. In Experiment 1 responding on one lever delivered a familiar incentive (food pellets), whereas responding on an alternative lever delivered a novel incentive (sucrose solution) prior to lithium chloride injections. If lithium was administered immediately after the instrumental session, the action associated with the novel, but not with the familiar, incentive was suppressed. By comparison, in a control group for which responding on both levers led to the familiar incentive, both actions were suppressed. Experiment 2 examined whether the novelty, rather than the sensory properties, of the incentive is crucial for observing performance suppression. It was found that animals familiarized with the “target” incentive were insensitive to aversion conditioning by lithium, in that there was no difference in response rates between the action that delivered the familiar incentive from that which earned the “target”. In contrast, if animals were unfamiliar with the “target” incentive at the time of aversion conditioning, they suppressed responding on the lever that was associated with the novel incentive but did not suppress responding on the lever associated with the familiar incentive. Experiment 3 investigated the mechanism underlying instrumental performance suppression. After the completion of concurrent lever press training, novel sucrose was introduced in conjunction with the pellets for responding on one lever; responding on the other lever continued to deliver only familiar pellets. Lithium injections were then administered either immediately following the sessions or several hours after the sessions. It was found that the rate of responding on the lever associated with the contingent delivery of sucrose was suppressed below that of the pellet-alone action. By comparison, if lithium injections were administered several hours following the session, an elevation in responding on the sucrose-plus-pellet lever was observed. The outcomes of all three experiments demonstrate not only that the novelty of an incentive is important in obtaining performance suppression, but also that a novel incentive can punish instrumental responding if it has been associated with toxicosis.     

Omission Learning after Instrumental Pretraining

Hungry rats were pretrained to press two levers on a concurrent schedule for food pellets. Following either limited or extended pretraining, presentations of a sucrose solution were programmed on a random time schedule while the animals continued pressing on a concurrent schedule for food pellets. Presses on one of the levers-the omission lever-postponed deliveries of the sucrose solution scheduled to occur within a fixed period of time following the press, whereas presses on the other, control lever had no effect on the random time contingency. The animals pressed less frequently on the omission lever than on the control lever following limited pretraining but failed to discriminate between the two levers following extended pretraining. The insensitivity to the omission contingency produced by extended pretraining was due to either the number of presses performed during the initial training or the number of reinforced presses, rather than the number of reinforcers received. Finally, the insensitivity of performance on the omission lever to sucrose devaluation suggests that adaptation tothis negative contingency was mediated by an inhibitory stimulus-response association.     

Instrumental conditioning of scratching in the laboratory rat

Experiment 1 demonstrates that scratching in the laboratory rat can be instrumentally conditioned with food reinforcement. However, the asymptotic rate of performance of this response is shown to be low, as compared with an instrumental lever press response. It is suggested that one reason for this low rate of responding is that the scratch response can only be performed in the presence of an infrequently occurring itch stimulus. In support of this account the remaining experiments demonstrate that the rate of instrumental scratching can be increased relative to that shown by control groups by using a technique which might be supposed to increase the frequency at which an itch stimulus occurs.     

Alcohol seeking by rats: Action or habit?

In two experiments, we examined the relative susceptibility to outcome devaluation of lever pressing by rats for either a 10% ethanol solution or food pellets. The rats were trained to press different levers for these two reinforcers using a sucrose-substitution procedure. An aversion was then conditioned from either the ethanol solution or the food pellets by pairing consumption with illness induced by lithium chloride. When instrumental performance was subsequently tested in extinction, the rats pressed less on the pellet lever if the pellets, rather than the ethanol, had been devalued by aversion conditioning. By contrast, performance on the ethanol lever was unaffected by whether the ethanol or pellets were devalued. Moreover, noncontingent presentations of the devalued reinforcer had no impact on test performance. The differential resistance to outcome devaluation suggests that, in contrast to food seeking, alcohol seeking is a stimulus-response habit rather than a goal-directed action mediated by a representation of the action-outcome contingency.     

Lever attacking and pressing as a function of conditioning and extinguishing a lever-press avoidance response in rats

Six experimental rats were conditioned to press one of two available levers to avoid shock. The levers registered bites as well as presses. For four of these rats, shock was contingent on lever bites when a specified time period had elapsed after the previous shock. An extinction period, in which only periodic noncontingent shocks were presented, followed avoidance training. Six yoked-control rats received the same sequence of shocks as did the corresponding experimental rats in both the conditioning and extinction phases. All six experimental rats repeatedly bit the avoidance lever. Four bit it more than the nonavoidance lever during conditioning, and five bit it more during extinction. Five of the six experimental rats consistently bit the levers many more times during each session than did their respective control rats, suggesting that avoidance conditioning facilitated lever biting. Rates of lever biting and pressing by all of the experimental rats and by some of the control rats were highest immediately following shock throughout both phases. During later portions of the intervals following shock, characteristic effects of conditioning and extinction were observed. This finding suggests that extinction of avoidance behavior by unavoidable shock presentations can be demonstrated more readily when shock-elicited responding is extricated from the data.     

Orbital prefrontal cortex and guidance of instrumental behavior of rats by visuospatial stimuli predicting reward magnitude

The orbital prefrontal cortex (OPFC) is part of a circuitry mediating the perception of reward and the initiation of adaptive behavioral responses. We investigated whether the OPFC is involved in guidance of the speed of instrumental behavior by visuospatial stimuli predictive of different reward magnitudes. Unoperated rats, sham-lesioned rats, and rats with bilateral lesions of the OPFC by N-methyl-D-aspartate (NMDA) were trained in a visuospatial discrimination task. The task required a lever press on the illuminated lever of two available to obtain a food reward. Different reward magnitudes were permanently assigned to lever presses to respective sides of the operant chamber; that is, responses to one lever (e.g., the left one) were always rewarded with one pellet and responses to the other lever with five pellets. On each trial, the position of the illuminated lever was pseudorandomly determined in advance. Results revealed that OPFC lesions did not impair acquisition of the task, as the speed of conditioned responses was significantly shorter with expectancy of a high reward magnitude. In addition, during reversal, shift and reshift of lever position–reward magnitude contingencies and under extinction conditions, performance of the OPFC-lesioned and control groups did not differ. It is concluded that the OPFC in rats might not be critical for adapting behavioral responses to changes of stimulus–reward magnitude contingencies signaled by visuospatial cues.     

Involvement of the rat anterior cingulate cortex in control of instrumental responses guided by reward expectancy

The anterior cingulate cortex (ACC) plays a critical role in stimulus-reinforcement learning and reward-guided selection of actions. Here we conducted a series of experiments to further elucidate the role of the ACC in instrumental behavior involving effort-based decision-making and instrumental learning guided by reward-predictive stimuli. In Experiment 1, rats were trained on a cost-benefit T-maze task in which they could either choose to climb a barrier to obtain a high reward (four pellets) in one arm or a low reward (two pellets) in the other with no barrier present. In line with previous studies, our data reveal that rats with quinolinic acid lesions of the ACC selected the response involving less work and smaller reward. Experiment 2 demonstrates that breaking points of instrumental performance under a progressive ratio schedule were similar in sham-lesioned and ACC-lesioned rats. Thus, lesions of the ACC did not interfere with the effort a rat is willing to expend to obtain a specific reward in this test. In a subsequent task, we examined effort-based decision-making in a lever-press task where rats had the choice between pressing a lever to receive preferred food pellets under a progressive ratio schedule, or free feeding on a less preferred food, i.e. lab chow. Results show that sham- and ACC-lesioned animals had similar breaking points and ingested comparable amounts of less-preferred food. Together, the results of Experiment 1 and 2 suggest that the ACC plays a role in evaluating how much effort to expend for reward; however, the ACC is not necessary in all situations requiring an assessment of costs and benefits. In Experiment 3 we investigated learning and reversal learning of instrumental responses guided by reward predictive stimuli. A reaction time (RT) task demanding conditioned lever release was used in which the upcoming reward magnitude (five vs. one food pellet) was signalled in advance by discriminative visual stimuli. Results revealed that rats with ACC lesions were able to discriminate reward magnitude-predictive stimuli and to adapt instrumental behavior to reversed stimulus-reward magnitude contingencies. Thus, in a simple discrimination task as used here, the ACC appears not to be required to discriminate reward magnitude-predictive stimuli and to use the learned significance of the stimuli to guide instrumental behavior.     

The conditioned reinforcement of repeated acquisition

Three monkeys were trained to emit a chain of three responses on three separate levers in a set of six levers to obtain food. The chain producing food (correct chain) was changed each day. During a trial, a press on any lever produced a feedback stimulus; a press on a correct lever produced an additional distinctive stimulus; the third correct press produced a food pellet. Test sessions in which either the food or the distinctive stimuli were removed were interspersed with baseline sessions. In tests without food presentations, the subjects acquired the correct chain rapidly, with a level of accuracy comparable to baseline. Removing the distintive stimuli for either the first or second member of the correct chain greatly retarded acquisition of that member of the chain. Removing all distinctive stimuli often reduced accuracy throughout the chain to chance level, even though food was presented following each correct chain. These results were interpreted as evidence that the distinctive stimuli presented after correct responses functioned as conditioned reinforcers. Reductions in accuracy following an omitted distinctive stimulus indicated that they were also discriminative stimuli for correct responding in their presence.     

Contingency effects with maintained instrumental reinforcement

In three experiments we investigated the effect on the performance of thirsty rats of varying the instrumental contingency between lever pressing and the delivery of a saccharin reinforcer. In Experiment 1, the subjects performed more slowly in a non-contingent condition, in which the momentary probability of reinforcement was unaffected by whether or not the animals pressed, than in a contingent condition in which the reinforcer was never presented except following a lever press. This was true of performance under both random ratio and interval schedules in which the function determining the probability of reinforcement following a lever press remained the same across the contingent and non-contingent conditions. Experiment 2 demonstrated that instrumental performance was less affected when the contingency was degraded by the introduction of free reinforcers if these reinforcers were signalled. In Experiment 3, lever pressing was reinstated to some degree after non-contingent training by giving non-reinforced exposure to the operant chamber in the absence of the lever. These results suggest that free reinforcers depress instrumental behaviour through a performance mechanism engaged by their ability to support conditioning of the contextual cues.     

Context Conditioning and Free operant Acquisition under Delayed Reinforcement

Three experiments examined the effect of context conditioning on the acquisition of freeoperant lever pressing by hungry rats when the presentation of the food reinforcer was delayed for 32 sec. The first study replicated the preexposure effect reported by Dickinson, Watt, and Griffiths (1992): Exposure to the contextual cues with the lever withdrawn prior to each instrumental training session enhanced acquisition, an effect that was attenuated by the presentation of non-contingent reinforcement during the preexposure periods. Signalling the non-contingent reinforcers during the preexposure periods with a brief auditory stimulus enhanced acquisition in a second study, suggesting that the non-contingent reinforcement interferes with acquisition through context conditioning. The final study confirmed this conclusion using a within-subject procedure in which pressing different levers was reinforced in two contexts, one of which was also associated with non-contingent reinforcers.     

Instrumental Outcome Devaluation Is Attenuated by the Anti-emetic Ondansetron

In three experiments we assessed the effect of an anti-emetic, the selective S-HT antagonist ondansetron, on (1) the conditioning of a taste aversion using lithium chloride (LiCl); (2) the expression of that aversion; and (3) instrumental outcome-devaluation effects. In Experiment 1 it was found that ondansetron reduced the aversion induced by LiCl when administered prior to the LiCl injection and also attenuated the expression of that aversion when administered prior to test sessions. In Experiments 2 and 3, thirsty rats were trained, in a single session, to lever press and chain pull for sucrose and saline solutions concurrently before being injected with LiCl. They were then re-exposed to both solutions, one after injection of vehicle and the other after injection of ondansetron. In a choice extinction test on the levers and chains, animals performed more of the action whose training outcome was re-exposed under ondansetron than the other action, whether the test was conducted after an injection of vehicle or after one of ondansetron.     

An experimental analysis of optimal foraging behaviour in patchy environments

A series of experiments was designed to explore the cognitive mechanisms involved in optimal foraging models by using the behavioural controls of operant methodology. Rats were trained to press one of two levers to obtain reinforcement on a progressive variable-interval schedule, which modelled food patch depletion; the schedule was reset by pressing the other lever. Thus both duration (residence time in a patch) and rate-related (interval before and after the final reward) measures were obtained. Experiment 1, which manipulated environmental stability and quality, and Experiment 2, which varied travel time between patches, found results that supported the marginal value theorem (Charnov, 1976) and suggested that rats adjust capture rate to the environment average by monitoring the length of the interval between rewards. Experiment 3 modelled the clumping of food items and found that capture rate was now adjusted by adoption of a fixed giving-up time. Finally, Experiments 4a and 4b ruled out a time expectancy hypothesis by manipulating the number of food clumps and the series of inter-reinforcement intervals. Overall the experiments demonstrate the value of modelling foraging strategies in operant apparatus, and suggest that rats adopt rate predictive strategies when deciding to switch patches.     

The role of response-reward correlation in stimulus-response overshadowing

Rats pressed levers for food reward which was delivered, when appropriate, 0·4 s after the response. For one group, the delay interval was filled by a light cue; for the other group, the same number of lights was given but they were not correlated with food delivery. In Experiment I, all lever presses were reinforced and there were no differences in response rate between groups. In Experiments II and III, lever pressing was rewarded according to a VI and VR schedule respectively. Group differences were observed in Experiment II but they disappeared in Experiment III. The results of Experiments I and II show that a reward-related stimulus does not overshadow a lever response unless the stimulus is a better predictor of reward. Differences in salience or competition from sign-tracking behaviors were ruled out as causes of this phenomenon. Experiment III demonstrated, however, that a weak response-reward correlation is not a sufficient condition for the overshadowing effect. A fourth experiment replicated the results of Experiment III using naive animals. The results of these last two experiments are not consistent with an information theory approach unless (a) a response-units concept is adopted or (b) the cue involved in overshadowing is not the pre-food light but the end of a temporal interval, whose salience is enhanced by the light.     

An assessment of factors contributing to instrumental performance for sexual reward in the rat

Male and female rats were gonadectomized, implanted in adulthood with capsules containing either testosterone propionate (TP) or cholesterol, and were trained to lever press for access to an oestrous female. When lever press performance was tested in extinction, only the male rats implanted with TP displayed significantly higher levels of responding than controls, demonstrating that lever pressing for oestrous females as a reward is sexually dimorphic. Ejaculation patterns from a separate assessment of these rats' copulatory ability were significantly correlated with their instrumental performance. In a second experiment, "masculinized" females exposed to TP postnatally and given TP implants responded in extinction at mean levels equivalent to those exhibited by adult males that were either intact or castrated with androgen replacement. These data suggest that organizational steroid exposure perinatally affects the actual reward value assigned to oestrous females inadulthood, in combination withconsummatory sexual experience.     

To press or not to press? Differential receptor expression and response to novelty in rats learning an operant response for reward

Learning to perform instrumental tasks is an ability of all animals. In a population of rats, not all individuals will acquire an operant response for reward. We hypothesized that there could be a genetic explanation for differences between High Consumers (those that acquired the lever press response) and Low Consumers (lever press response is low). Additionally, we proposed that this genetic difference could produce measurable changes in response to novelty. Wistar rats were trained to lever press for a 0.2% saccharin reward and on the 10th day they were placed in a novel open field for 30 min to record locomotor activity. The prefrontal cortex and hippocampus were dissected and qPCR was used to measure mRNA expression. A significant difference (p=.048; 2-way ANOVA) in gene expression was observed between Low and High Consumers. A principal component analysis (PCA), to cluster which genes represent this difference, identified 4 genes; 5-HT2A and mGlu1 in the hippocampus and AMPA GluR1 and adrenergic alpha2A in the prefrontal cortex. Response to a novel open field also differed since Low Consumers displayed a higher Total Distance in comparison to High Consumers. Additionally, Low Consumers could be subdivided into Low-Lever (with lever press response only when water deprived) and Low-Non-Lever (lever press response is low throughout training). PCA with this subdivision identified an additional nine genes differing within the divisions; NMDA NR2B and GABAAalpha3 in the prefrontal cortex and adrenergic alpha2B and alpha2A, AMPA GluR1, GluR2 and GluR3, 5-HT1B and GABAAalpha5 in the hippocampus.     

The role of the instrumental contingency in the motivational control of performance

In four experiments we investigated an irrelevant incentive effect based upon a transition from hunger to thirst. Hungry rats were trained to lever press either for sucrose solution or for food pellets before performance was tested in extinction while they were thirsty. Reinforcer-specific motivational control was found in the first experiment in that the animals pressed the lever more on tests following training with the sucrose solution rather than with food pellets. Moreover, this effect was seen only when testing was conducted following water, but not following food deprivation. The outcome of the remaining experiments suggests that this motivational control is not mediated by the instrumental contingency between lever pressing and the sucrose reinforcer during training. In these studies lever pressing and chain pulling were reinforced concurrently, one with sucrose and the other with food pellets, in order to equate the noninstrumental functions of the incentives. Following this training, lever pressing in extinction under thirst was unaffected by the type of incentive used as its reinforcer during training.     

The effect of rearing environments on the contrafreeloading phenomenon in rats

Eight naive rats were reared in enriched or impoverished environments for 39 days after weaning and then lived in operant chambers, in which they could obtain food pellets freely or by lever pressing, for 25 or 30 days. The animals raised in an impoverished environment acquired the bar-press response quickly when placed in the operant chambers and maintained a preference for obtaining food via bar pressing. Animals raised in an enriched environment did not learn to lever press, as demonstrated by low levels of responding and the lack of bar pressing when free food was subsequently removed. It was concluded that restricting animals' postweaning environments facilitated learning in a choice situation, probably because of increased activity levels. The results are interpreted in relation to previous studies on rearing environments and on contrafreeloading.     

The interaction between discriminative stimuli and outcomes during instrumental learning

Rats were trained on a biconditional discrimination in which the delivery of a food pellet stimulus signalled that pressing on one of two levers would be reinforced, whereas the delivery of a sucrose solution stimulus signalled that the reward was contingent on pressing the other lever. The outcome was the same food type as the discriminative stimulus in the congruent group but the other food type in the incongruent group. Both responses were rewarded with the same outcome in the same group. All the three groups learned the discrimination at statistically indistinguishable rates. Prefeeding one of the outcomes selectively reduced the associated response thereby demonstrating that responding was mediated by a representation of the outcome. Moreover, the outcome of one trial controlled responding on the next trial in accord with the stimulus function of the food type. These results are discussed in relation to the associative structures mediating the discriminative control of instrumental performance.