Conditioned Inhibition Produced by Extinction of a Conditioned Stimulus

Four experiments used a conditioned taste aversion procedure to examine the potential for CS-alone extinction treatment to produce a conditioned stimulus that possesses inhibitory properties. In Experiment 1, saccharin was paired with LiCl, and then saccharin was presented alone for several trials to produce extensive behavioral extinction. Animals receiving this treatment were retarded in reacquiring conditioned responding to saccharin relative to control subjects receiving conditioning to the flavor for the first time. In Experiment 2, the extinguished saccharin stimulus was shown to decrease conditioned responding to a known excitor when the two stimuli were presented in compound as a summation test. Experiments 3A and 3B replicated the findings of Experiments 1 and 2 while providing evidence that the effects were not due to the differential effects of neophobia during testing. These three experiments revealed that an extinguished conditioned excitor passes retardation and summation tests for conditioned inhibition. Experiment 4 found that extinction of a known excitor was slowed when the excitor was extinguished in compound with a previously extinguished conditioned stimulus. That is, an extinguished CS provided protection from extinction to another CS, a finding also consistent with the view that extinction produces conditioned inhibition.     

Retention of Conditioned Inhibition Produced by Extinction

Rats in a flavor aversion procedure were used to examine the extent to which an extinguished CS can pass a retardation and summation test for conditioned inhibition after either a short or a long retention interval. Rats were given a single pairing of a flavored solution with LiCl, and then received a large number of CS-alone extinction trials. Following extinction, some subjects received a 3-week retention interval following extinction while others did not. Extinction produced evidence of conditioned inhibition on both tests when a short retention interval occurred following extinction. However, conditioned inhibition was attenuated by the long retention interval when assessed with a retardation test, but no effect of the long retention interval was observed when inhibition was evaluated with a summation test.     

Mechanisms underlying retarded emergence of conditioned responding following inhibitory training: evidence for the comparator hypothesis

The comparator hypothesis posits that conditioned responding is determined by a comparison at the time of testing between the associative strengths of the conditioned stimulus (CS) and stimuli proximal to the CS at the time of conditioning. The hypothesis treats all associations as being excitatory and treats conditioned inhibition as the behavioral consequence of a CS that is less excitatory than its comparator stimuli. Conditioned lick suppression by rats was used to differentiate four possible sources of retarded responding to an inhibitory CS. These include habituation to the unconditioned stimulus (US), latent inhibition to the CS, blocking of the CS-US association by the conditioning context, and enhanced excitatory associations to the comparator stimuli. Prior research has demonstrated the first three phenomena. Therefore, we employed parameters expected to highlight the fourth one--the comparator process. In Experiment 1, our negative contingency training was shown to produce a conditioned inhibitor that passed inhibitory summation and retardation tests. In Experiment 2 we found transfer of retardation from an inhibitory CS to a novel stimulus when the location where retardation-test training occurred was excitatory, which is indicative of contextual blocking and/or comparator effects. In Experiment 3, extinction of the conditioning context was found to attenuate retardation regardless of whether extinction occurred before or after the CS-US pairings of the retardation test. This indicates that much of the present retardation was due to the comparator process rather than to contextual blocking. Experiment 4 demonstrated that habituation to the US did not contribute to retardation in the present case. Collectively, these studies suggest that retardation following inhibitory training can be explained without recourse to any of the traditional mechanisms of conditioned inhibition.     

Acquisition of a conditioned taste aversion becomes context dependent when it is learned after extinction

A conditioned taste aversion experiment tested context-switch effects on retrieval of conditioned stimulus (CS)–unconditioned stimulus (US) acquisition performance in rats. A context switch impaired performance when the target flavour was trained in a context where a different flavour underwent extinction. Conditioned taste aversion in the absence of previous extinction of the alternate flavour was not context dependent. It is suggested that the ambiguity in the meaning of the extinguished cue leads animals to pay attention to the context, so that the information learned in that context becomes context dependent.     

Acquisition of a conditioned taste aversion becomes context dependent when it is learned after extinction

A conditioned taste aversion experiment tested context-switch effects on retrieval of conditioned stimulus (CS)-unconditioned stimulus (US) acquisition performance in rats. A context switch impaired performance when the target flavour was trained in a context where a different flavour underwent extinction. Conditioned taste aversion in the absence of previous extinction of the alternate flavour was not context dependent. It is suggested that the ambiguity in the meaning of the extinguished cue leads animals to pay attention to the context, so that the information learned in that context becomes context dependent.     

Temporal coding in conditioned inhibition: analysis of associative structure of inhibition

Two experiments with rats as subjects were conducted to investigate the associative structure of temporal control of conditioned inhibition through posttraining manipulation of the training excitor-unconditioned stimulus (US) temporal relationship. Experiment 1 found that following simultaneous Pavlovian inhibition training (i.e., A --> US/XA-no US) in which a conditioned stimulus (CS A) was established as a delay excitor, maximal inhibition was observed on a summation test when CS X was compounded with a delay transfer CS. Furthermore, posttraining shifts in the A-US temporal relationship from delay to trace resulted in maximal inhibition of a trace transfer CS. Experiment 2 found complementary results to Experiment 1 with an A-US posttraining shift from serial to simultaneous. These results suggest that temporal control of inhibition is mediated by the training excitor-US temporal relationship.     

Spontaneous recovery of extinguished fear responses deepens their extinction: a role for error-correction mechanisms

A series of experiments used a within-subject design to study spontaneous recovery of fear responses (freezing) to an extinguished conditioned stimulus (CS) in rats. Experiments 1, 2, 3, and 4 demonstrated that: a remotely extinguished CS elicited more freezing than a recently extinguished one on a common test; that the CS showing recovery underwent greater response loss across additional extinction than the one lacking recovery; and that spontaneous recovery and deepening of response loss survived reconditioning. Experiment 5 demonstrated that an excitor extinguished in compound with a CS showing recovery suffered greater loss than an excitor extinguished in compound with a CS not showing recovery, implying that the differential change is regulated by a common error term. Experiments 6 and 7 demonstrated that extinction of a compound composed of two CSs, one showing recovery and a second lacking recovery, produced greater loss to the CS that showed recovery, implying that the change is also regulated by individual error term.     

Enhancement of Pavlovian conditioned inhibition achieved by posttraining inflation of the training excitor

In two conditioned lick suppression experiments using water-deprived rats, we examined the effects of following Pavlovian conditioned inhibition training (i.e., A–US/AX-NoUS) with pairings of the training excitor (A) and the unconditioned stimulus (US). Experiments 1 and 2 assessed the effects of this posttraining inflation treatment on Pavlovian conditioned inhibition using a summation test and a retardation test, respectively. Both experiments revealed that subjects exposed to inflation treatment demonstrated behavior indicative of enhanced conditioned inhibition compared to subjects that did not receive inflation treatment. The results in conjunction with other recent findings suggest that posttraining associative deflation (i.e., extinction of A) and inflation effects are more symmetrical than has previously been realized.     

Context specificity of latent inhibition in taste aversion learning

In three experiments rats were given injections of LiCl after consuming distinctively flavoured water. The rats developed an aversion to the flavour and in all experiments the magnitude of the aversion was found to be reduced in subjects that had received pre-exposure to the flavour without aversive consequences. Experiment 1 demonstrated this pre-exposure effect to be a case of latent inhibition. The remaining experiments investigated the effects of pre-exposing the flavour in a context different from that used for conditioning. It was found (Experiment 2) diat latent inhibition transferred perfectly when the context change consisted of a move from one home cage to another. Context specificity of latent inhibition was found (Experiment 3) only when the subjects were given daily sessions in die experimental contexts, these being cages different from the home cage.     

Perirhinal cortex lesions impair feature-negative discrimination

The role of the perirhinal cortex in inhibitory eyeblink conditioning was examined. In Experiment 1, rats were given lesions of the perirhinal cortex or control surgery and subsequently trained with a feature-negative discrimination procedure followed by summation and retardation tests for conditioned inhibition. Perirhinal cortex lesions impaired, but did not prevent acquisition of feature-negative discrimination. Results from the summation test showed that rats with perirhinal cortex lesions could not generalize feature-negative discrimination to a new stimulus. There were no group differences during the retardation test. Experiment 2 showed that lesions of the perirhinal cortex did not impair simple excitatory conditioning. Experiment 3 showed that perirhinal cortex lesions had no effect on acquisition of a simple tone-light discrimination. The results suggest that the perirhinal cortex plays a role in eyeblink conditioning when using discrimination procedures involving overlapping stimuli.     

Associative status of the training context determines the effectiveness of compound extinction

Studies of extinction of a target cue in compound with another excitor have produced evidence of both deepened and attenuated extinction relative to elemental extinction. The present experiments sought to resolve this discrepancy by assessing the effect of the extinction context-unconditioned stimulus (US) association on compound extinction. In an ABC renewal situation with rats, Experiment 1 replicated the observation that enhanced extinction (i.e., reduced conditioned suppression) occurs as a result of nonreinforcement in compound with a concurrent excitor. In Experiment 2, inflation of the extinction context-US association through unsignaled, intertrial US presentations reversed the effect of a concurrent excitor (i.e., extinction with a concurrent excitor was less effective than elemental extinction). Experiment 3 compared compound extinction and second-order conditioning with respect to the effect of context inflation, and produced results incompatible with the view that second-order conditioning contributed to the results of Experiment 2. In Experiment 4, a concurrent excitor enhanced extinction in ABC renewal and attenuated extinction in AAC renewal. The present results suggest that the effect of a concurrent excitor during extinction depends on the strength of the extinction context-US association, thereby confirming predictions of the sometimes -competing retrieval model of associative acquisition and extinction.     

Constraints on enhanced extinction resulting from extinction treatment in the presence of an added excitor

Three Pavlovian fear conditioning experiments with rats as subjects explored the effect of extinction in the presence of a concurrent excitor. Our aim was to explore this particular treatment, documented in previous studies to deepen extinction, with novel control groups to shed light on the processes involved in extinction. Relative to subjects extinguished on the target CS alone, Experiments 1 and 2 found across a range of parameters that any appreciable effect of facilitated extinction due to the concurrent excitor was submerged by generalization decrement going from extinction to testing. In Experiment 3 we used different durations for the target and concurrent stimuli in order to discourage configuring and an ABC renewal design to increase sensitivity, and observed diminished renewal resulting from extinction in the presence of a second excitor. Our findings suggest that there are distinct limits to the observation of enhanced extinction in the presence of an excitor and identifies some of the sources of these limitations.     

Inhibition as a "slave" process: deactivation of conditioned inhibition through extinction of conditioned excitation

Rats were used in a conditioned-suppression paradigm to investigate why a conditioned inhibition (CS-) does not extinguish when presented alone. Experiment 1 assessed the role of blocking by excitatory contextual cues and/or an evoked representation of the conditioned excitor (CS+), which had been nonreinforced in compound with the CS-. When the CS+ and context were extinguished prior to presentations of the CS- alone, the CS- showed a retardation effect, evidently reflecting latent inhibition, because no inhibition was detected in controls for which presentations of the CS- alone had been omitted. Experiment 2 showed that the loss of conditioned inhibition (CI) was due to excitatory extinction and not to time since conditioning. Furthermore, when excitation was reconditioned to the extinguished CS+ (Experiment 1), or to a novel CS in the same context (Experiment 2), CI was restored. Two other experiments evaluated whether the maintenance of CI depended upon excitation that was generic in form or associatively tied to the training context. They showed no loss of CI when groups received CS+ extinction in that context, along with concomitant presentations in a different context of the US by itself, for a novel CS, or correlated either positively or negatively with the original CS+. Collectively, the findings argue that CI is a "slave" to excitation, for when excitation is extinguished, CI is deactivated; and yet when excitation is reconditioned to the original or a new CS+ in the same or a different context, CI is restored.     

Flavour-odour compound conditioning: Odour-potentiation and flavour-attenuation

Five experiments employed a toxiphobia conditioning paradigm to examine the strengths of odour and flavour aversions when conditioned separately and in compound. When conditioned in compound, odour aversions were stronger than when conditioned separately, i.e., the flavour potentiated the odour (Experiment Ia), but flavour aversions were weaker than when conditioned separately, i.e., the odour attenuated the flavour (Experiment Ib). The duration of exposure to the reinforced compound governed the nature of the interaction between the components: at a brief exposure, the flavour overshadowed the odour; at a long exposure, the flavour potentiated the odour (Experiment II). The remaining experiments examined the mechanism subserving the potentiation effect. Experiment III demonstrated that extinction of the flavour associate of the odour attenuated the odour aversion but further conditioning of the flavour did not strengthen the odour aversion. Experiment IV confirmed this effect of extinction but also found a comparable attenuation of the odour aversion from extinction of a separately conditioned flavour. Experiment V examined the previous failure to influence the strength of the odour aversion by strengthening the flavour aversion. In this experiment, conditioning the flavour associate or a separately conditioned flavour with a more potent US augmented the strength of the odour aversion. The results did not provide support for the idea that the potentiation phenomenon reflects the formation of within-compound associations but did indicate that a potentiated odour aversion could be modulated by manipulations designed to alter the US representation.     

Predictive learning in nutrient-based flavor conditioning

This paper presents two experiments on nutrient-based flavor conditioning with rats as subjects and sucrose as the unconditioned stimulus (US). Experiment 1 was aimed at establishing an optimal control for conditioning, comparing simultaneous and serial presentations of a flavor and the US. The results showed that simultaneous, but not serial training, produced conditioning. Experiment 2 was designed to obtain evidence of summation as an index of both conditioned inhibition and predictive learning. Group Simultaneous received Pavlovian conditioned inhibition training during which flavor A was simultaneously paired with sucrose on excitatory trials (A+), and forming an unreinforced compound with flavor B on inhibitory trials (AB-). An independent excitor for the summation test was also trained by simultaneous pairings with sucrose (C+). In the control group (Blocked), the AB- trials were presented forming a block at the beginning of training to avoid a negative contingency-relationship with sucrose, and flavor A received serial rather than simultaneous pairing with sucrose (A --> +). On the summation test, only in group Simultaneous was consumption of the CB compound lower than that of flavor C alone, suggesting that, during training, flavor A activated an expectancy of the US occurrence.     

Distractor effect on the latent inhibition of conditioned flavor aversion in rats

Using a conditioned flavor aversion procedure with rats as subjects, the effect of the addition of a distractor stimulus on the magnitude of the latent inhibition effect was examined. Experiment 1 showed that latent inhibition to vinegar was attenuated by the addition of sucrose during preexposure. On the other hand, sucrose added during conditioning to vinegar did not attenuate latent inhibition. It was also found that the degree of latent inhibition to the vinegar-sucrose compound solution was less when vinegar alone was preexposed (i.e., when sucrose was added only during conditioning) than when the compound solution was preexposed (i.e., when sucrose was added both during preexposure and during conditioning). Experiment 2 gave similar results but with sucrose assigned as the target flavor and vinegar as the distractor. These findings are in full agreement with the generalization decrement account of latent inhibition.     

Flavour aversion produced by running and attenuated by prior exposure to wheels

In two experiments hungry rats were given access to running wheels. When given the novel flavour, almond, prior to novel access to the wheels, a conditioned aversion to almond was revealed by a subsequent two-bottle test. No such aversion was found in rats with previous experience of wheel running, whether this prior running occurred in the absence of any novel flavour, as in Experiment 1, or following access to saccharin, as in Experiment 2. These results suggest that the failure of rats with prior experience of the running wheels to develop a flavour aversion (unconditioned stimulus, US, preexposure effect) is unlikely to be due to associative blocking. Instead it seems that increasing exposure to a wheel produces habituation of its nausea-inducing properties.     

Overshadowing and blocking procedures in latent inhibition

Three experiments used rats as subjects and a flavour-aversion procedure to examine the effect of compound flavour (AB) pre-exposure on the extent of latent inhibition to an element (A) of that compound. In Experiment 1 a group of rats exposed to AB exhibited less latent inhibition to stimulus A than a group for which A was presented in isolation or than a group that received A followed by a second stimulus, B, during the pre-exposure phase. Experiment 2 and Experiment 3 showed that the effectiveness of B during compound pre-exposure depended on its novelty. Thus a group that received exposure to stimulus B prior to AB pre-exposure showed more latent inhibition than a group that did not receive prior experience of the B stimulus. Two explanations for these effects were considered: that compound pre-exposure might reduce effective processing of the elements of that compound during the pre-exposure phase; alternatively, that exposure to an element as a part of a compound may modify the way in which that element is perceived.     

Effects of contingency violations on the extinction of a conditioned fear inhibitor and a conditioned fear excitor

Rats were used in a conditioned-suppression paradigm to assess the effects of contingency variations on responding to a conditioned inhibitor (CS-) and a conditioned excitor (CS+). In Experiment 1, various unconditioned stimulus (US) frequencies were equated across the presence and absence of a CS- in the context of either background cues (continuous-trial procedure) or an explicit neutral event (discrete-trial procedure). With both procedures, a CS-alone treatment enhanced inhibition, whereas treatments involving 50% or 100% reinforcement for the CS- eliminated inhibition without conditioning excitation to that CS. The latter outcome also occurred in Experiment 2, with discrete-trial training equating considerably reduced US frequencies for the presence and absence of the CS-. In further evidence that inhibition was eliminated without conditioning excitation to the CS-, Experiment 3 showed that a novel CS did not acquire excitation when 25%, 50%, or 100% reinforcement was equated across the presence and absence of that CS in the context of a discrete-trial event. Using the procedures of Experiment 1, Experiment 4 showed that a CS+ was extinguished by a CS-alone treatment but was substantially maintained by treatments involving 50% or 100% uncorrelated reinforcement. These effects for a CS+ and a CS- implicate CS-US contiguity, rather than contingency, as the factor determining the extinction of a CS.     

Extinction of the context and latent inhibition

The hypothesis that latent inhibition could be reduced by extinguishing the experimental context, that is, exposing the rats to the context between exposure to the conditional stimulus (CS) and conditioning, was tested. All experiments used the conditioned emotional response procedure. In Experiment 1, extinction was not effective when the animals were exposed to the clicker 40 times off the baseline of responding for food and when the clicker CS was partially reinforced with shocks during the test phase. In Experiments 2 and 3, latent inhibition could be reduced by extinction if the animals were exposed to the CS 24 or 16 times on-baseline, and if continuous reinforcement was used during the test. In Experiments 4, 5, and 6, we attempted to determine which variable was responsible for the discrepant results. In Experiment 4, extinction was effective with 20 or 40 on-baseline exposures to the CS, using continuous reinforcement during the test. In Experiment 5, extinction was not effective with exposure on- or off-baseline, using 24 exposures and partial reinforcement. Finally, in Experiment 6, extinction reduced latent inhibition using continuous, but not partial, reinforcement with 40 exposures off-baseline. From these results, we concluded that Wagner's model of habituation was not sufficient to account for latent inhibition and that a hybrid model, using both associative and cognitive representational processes, was necessary.