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.     

A search for context-stimulus associations in latent inhibition

Six experiments investigated the effects of pre-exposure to a tone on the subsequent acquisition of conditioned suppression by rats. In Experiments 1-3 the response suppressed was drinking; in Experiments 4-6 it was food-rewarded lever pressing. Repeated exposure to the tone resulted in latent inhibition, i.e., a retardation in the acquisition of suppression. The size of the latent inhibition effect was reduced when a different context was used for conditioning from that used for pre-exposure (Experiment 2). When the context remained the same throughout, a phase of exposure to the context alone, interposed between pre-exposure and conditioning, had no influence on the size of the latent inhibition effect ultimately observed. This last result casts doubt upon Wagner's (1976, 1979) theory of the role of contextual factors in latent inhibition, and alternative accounts are considered.     

Contextual Control of Latent Inhibition by the Reinforcer

Three experiments examined the contextual control of latent inhibition (LI) by the unconditioned stimulus (US) using a within-subjects conditioned suppression procedure with rats. The effect of reducing the context change produced by the introduction of the shock US was investigated by presenting this US during preexposure to the conditioned stimulus (CS). Although limited CS preexposure in the absence of the US had no impact on subsequent conditioning, preexposure in the presence of the shock retarded both excitatory and inhibitory conditioning. We conclude that the introduction of the US during the conditioning phase of a normal LI experiment can produce a contextual change that reduces the observed magnitude of LI.     

Contextual control of extinguished conditioned performance in humans

Animal research has shown that extinguished conditioned performance is modulated by the environmental context in which extinction treatment has occurred. When the conditioned stimulus is presented outside the extinction context, conditioned responding is renewed. In two experiments, whether a renewal effect can also be found in humans was investigated. In Experiment 1, a renewal effect was observed, although the effect was small and far from complete. In Experiment 2, a more substantial renewal effect was observed. The extent to which this effect occurred depended on the degree to which context was manipulated. In a third experiment, the exact nature of the observed renewal effect was examined. Results indicated that, as opposed to animals, the extinction context does not modulate extinguished conditioned responding in humans.     

Kappa opioid receptors mediate where fear is expressed following extinction training

Six experiments used a within-subjects renewal design to examine the involvement of kappa opioid receptors (KORs) in regulating the expression and recovery of extinguished fear. Rats were trained to fear a tone conditioned stimulus (CS) via pairings with foot shock in a distinctive context (A). This was followed by extinction training of the CS in a second context (B). Finally, all rats were tested for fear to the tone in the extinction context (ABB) and the training (ABA) or a novel (ABC) context. Intracerebroventricular (ICV) infusion of the KOR antagonist nor-binaltorphimine dihydrochloride (nor-BNI) dose-dependently prevented ABA renewal of fear, but had no effect on the expression of ABC renewal, the expression of extinction, or the expression of nonextinguished fear. Conversely, pretest infusion of the KOR agonist U50,488 hydrochloride (U50,488) selectively facilitated the expression of ABA renewal and had no effect on the expression of extinction. Pretest infusion of nor-BNI had no effect on the expression of context-specific latent inhibition. Collectively, these results suggest that KORs gate the expression of fear following extinction training and may comprise a critical neuropeptide component of the circuitry underlying context-dependent expression of fear.     

Unpaired shocks during extinction weaken the contextual renewal of a conditioned discrimination

Extinction is generally more fragile than conditioning, as illustrated by the contextual renewal effect. The traditional extinction procedure entails isolated presentations of the conditioned stimulus. Extinction may be boosted by adding isolated presentations of the unconditioned stimulus, as this should augment breaking the contingency between the two stimuli. In a human conditioning experiment with on-line expectancy ratings and electrodermal responding as dependent variables, 32 participants were differentially conditioned to two neutral figures using electric shock. After a change of context, one group received normal extinction treatment whereas another group received explicitly unpaired presentations of the figures and shock. At test, the two figures were presented in the original context again. For both measures, only the group that received normal extinction showed renewal of the conditioned discrimination. These results suggest that unpaired shocks during extinction strengthen the extinction learning.     

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.     

Interaction between preexposure and overshadowing: Further analysis of the extended comparator hypothesis

Three experiments with rats used conditioned suppression of barpress to test predictions of the extended comparator hypothesis, which assumes that the effectiveness of (first-order) comparator stimuli in modulating responding to a target conditioned stimulus (CS) is itself modulated by other (second-order) comparator stimuli. Experiment 1 demonstrated that both pretraining exposure to the target CS alone (i.e., CS-preexposure effect, also known as latent inhibition) and pretraining exposure to a compound of the target CS and nontarget CS (i.e., compound-CS-preexposure effect) counteract overshadowing, and that posttraining deflation (i.e., extinction) of the overshadowing stimulus attenuates responding to the target CS when overshadowing is preceded by a CS-preexposure treatment (i.e., yields a CS-preexposure effect), but not when overshadowing is preceded by a compound-CS-preexposure treatment. Experiment 2 examined the consequences of posttraining associative inflation of the overshadowing stimulus or the preexposure companion stimulus following conjoint compound-CS-preexposure and overshadowing treatment. Experiment 3 examined the consequences of posttraining inflation of the overshadowing stimulus or the context following conjoint CS-alone preexposure and overshadowing treatment. The results support the expression-focused comparator view in contrast to recent acquisition-focused models of retrospective revaluation.     

The effects of context changes on the reinstatement of extinguished conditioned behavior in a conditioned suppression task with humans

Reinstatement refers to the return of previously extinguished conditioned responses to test trials of a conditional stimulus (CS) when presentations of the unconditional stimulus (US) alone are given following extinction. Four experiments were conducted to determine whether reinstatement could be found in a conditioned suppression task with humans and whether contextual changes can abolish it. Experiment 1 demonstrated the reinstatement of conditioned suppression when acquisition, extinction, US alone, and test trials were all given in the same context. Experiments 2 and 3 suggested that the reinstatement effect was still present when the US alone presentations were given in a different context to the subsequent test trials. Experiment 4 replicated this effect using additional controls over the amount of exposure to the various contexts. The results suggest that reinstatement can be robust across changing contexts. Aspects of the conditioned suppression task that promote the transfer of learning across contexts or the establishment of configural context-CS stimuli may underlie the apparent lack of contextual control over reinstatement.     

Latent inhibition experiments with goldfish (Carassius auratus)

Evidence of latent inhibition was sought in a series of experiments with goldfish. In Experiment 1, goldfish were given nonreinforced preexposure to a color that subsequently predicted shock in an activity conditioning situation; their performance did not differ from that of control animals preexposed to a markedly different color. In Experiment 2, a group of goldfish given nonreinforced preexposure to a tone and an unstimulated control group were trained in an appetitive situation, with the tone serving either as a conditioned excitor or as a conditioned inhibitor. Preexposure had no significant effect in the conditioned excitation training, but it reduced the level of responding both to the positive stimulus and to the negative compound in the conditioned inhibition training. In Experiments 3 and 4, classical aversive conditioning was studied in the shuttle box. In Experiment 3, excitatory conditioning to a color was found to be impaired (relative to the performance of nonpreexposed control animals) as much by nonreinforced preexposure to the training color as by nonreinforced preexposure to a markedly different color; substantial variation in amount of preexposure was without significant effect. In the conditioned inhibition training of Experiment 4, animals with nonreinforced preexposure responded less than did unstimulated control animals both to the positive stimulus and to the negative compound. The results for goldfish can be understood on the assumption that the effect of preexposure in these animals is simply to reduce general responsiveness or level of arousal.     

Rapid reaquisition in conditioning of the rabbit's nictitating membrane response.

Reacquisition after extinction often appears faster than original acquisition. However, data from conditioned suppression studies indicate that this effect may arise from spontaneous recovery and reinstatement of unextinguished contextual stimuli related to the unconditioned stimulus (US). In the present experiments using the rabbit nictitating membrane preparation, spontaneous recovery was eradicated before reaquisition training. US contextual stimuli were controlled by retaining the US during extinction through explicit unpairings of the conditioned stimulus (CS) and US. Attempts were also made to drive the associative strength of the CS into the inhibitory region by differential conditioning and conditioned inhibition procedures. In all cases, reacquisition was very rapid in comparison with a rest control. The results are discussed with respect to their implications for CS and US processing models of conditioning.     

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.     

Latent inhibition and conditioning after preexposure to the training context

Experiment 1, using the conditioned suppression technique with rats, showed that the retardation of learning produced by prior exposure to a stimulus (latent inhibition) was more marked in subjects given an initial phase of preexposure to the training context. This effect was confirmed and extended in Experiment 2 in which an appetitive conditioning procedure was used. Experiments 3 and 4, again using conditioned suppression, found no effect of preexposure to the context on the acquisition of suppression when training was given with a novel stimulus, either immediately after preexposure or after a delay; but context preexposure was again found to be effective when exposure to the to-be-conditioned stimulus was given in the delay interval between context preexposure and conditioning. The implications of these findings for accounts of the role of contextual factors in latent inhibition are discussed.     

The role of contextual associations in producing the partial reinforcement acquisition deficit

Three conditioned suppression experiments with rats as subjects assessed the contributions of the conditioned stimulus (CS)-context and context-unconditioned stimulus (US) associations to the degraded stimulus control by the CS that is observed following partial reinforcement relative to continuous reinforcement training. In Experiment 1, posttraining associative deflation (i.e., extinction) of the training context after partial reinforcement restored responding to a level comparable to the one produced by continuous reinforcement. In Experiment 2, posttraining associative inflation of the context (achieved by administering unsignaled outcome presentations in the context) enhanced the detrimental effect of partial reinforcement. Experiment 3 found that the training context must be an effective competitor to produce the partial reinforcement acquisition deficit. When the context was down-modulated, the target regained behavioral control thereby demonstrating higher-order retrospective revaluation. The results are discussed in terms of retrospective revaluation, and are used to contrast the predictions of a performance-focused model with those of an acquisition-focused model.     

Blocking between occasion setters and contextual stimuli

Two appetitive conditioning experiments with rats used a blocking procedure to compare the mechanisms through which contexts and positive occasion setters control responding to conditioned stimuli (CSs) in discrimination learning. In Experiment 1, a light (L) initially set the occasion for food reinforcement of a tone CS (T). Then a compound of L and a novel context signaled reinforcement of T. Previous learning about L blocked contextual control of responding to T. Blocking was not due to simple excitation conditioned to L during discrimination training; comparable excitation to L in a control group did not result in blocking. Conversely, in Experiment 2, initial learning about the context blocked the acquisition of occasion setting to L. Excitation conditioned to the context could not account for the blocking. In general, the results suggest that contexts and occasion setters may control responding to CSs through similar mechanisms.     

Attenuation of latent inhibition after compound pre-exposure: Associative and perceptual explanations

Three experiments used rats as subjects and the conditioned emotional response (CER) paradigm to examine the effect of pre-exposure to a compound stimulus on the extent of latent inhibition to an element of that compound. In Experiment 1a a group of rats exposed to a compound that comprised a tone and a click exhibited less latent inhibition to the tone than did a group that had received pre-exposure to the tone in isolation. Experiment 1b showed that pre-exposure to the tone/click compound also resulted in an attenuation of latent inhibition to the click relative to a group that was pre-exposed to the click in isolation. Experiment 2 demonstrated that latent inhibition to the tone was left intact following pre-exposure to the tone in compound with a light. This pattern of results seems to be most plausibly explained in terms of the presence and absence of generalization decrement following compound pre-exposure.     

Contextual control over conditioned responding in a latent inhibition paradigm

We used 1-, 2-, and 3-context designs to study the control exerted by contexts over freezing in rats exposed to a conditioned stimulus (CS) in advance of its pairing with a shock unconditioned stimulus. The latent inhibition observed when preexposure, conditioning, and testing occurred in the same context was attenuated if preexposure occurred in a different context to conditioning and testing. Latent inhibition (i.e., attenuated performance) was restored in a CS-specific manner if preexposure and testing occurred in the same context and conditioning in a different one. Latent inhibition was also reduced by a long retention interval but remained specific for a particular context-CS relation. Finally, CS preexposure resulted in contextual control over the expression of excitatory conditioned performance. The results are discussed in terms of memory, associative, and associative-performance models of CS-preexposure effects.     

Occasional reinforced trials during extinction can slow the rate of rapid reacquisition

Two appetitive conditioning experiments with rats examined reacquisition after conditioned responding was eliminated by either extinction or by a partial reinforcement procedure in which reinforced trials were occasionally presented among many nonreinforced trials. In Experiment 1, reacquisition to a conditional stimulus (CS) that had been conditioned and extinguished was more rapid than acquisition in a group that had received no prior conditioning. However, the addition of occasional reinforced trials to extinction slowed this rapid reacquisition effect. Experiment 2 replicated the result and showed that a procedure in which the CS and the unconditional stimulus (US) were unpaired in extinction interfered even further with reacquisition. The results suggest that rapid reacquisition is ordinarily produced when reinforced trials provide a contextual cue that can renew responding by signaling other acquisition trials (Ricker & Bouton, 1996). The effects of partial reinforcement in extinction are surprising from several theoretical perspectives and have useful clinical implications.     

Latent Inhibition of Contextual Stimuli Reduces the US Preexposure Effect in Rats

Two experiments are reported which utilized latent inhibition of contextual stimuli prior to administering unsignaled presentations of the Us in an attempt to further assess the role of contextual stimuli in the US preexposure effect. Specifically in Experiment 1, rats received either 0-, 5-, 10-, or 15-minute exposure to the context in which the unsignaled Uss were to occur (latent inhibition). Following preexposure to the US, animals were trained in a CER paradigm with a tone CS. Measures of suppression to the tone indicated that the greatest US preexposure effect occurred in the 0 group and that no US preexposure effect was evident in the 15 group. Experiment 2 includec two important control groups which were omitted in Experiment 1 (no US preexposures) and an additional dependent variable (time to initiate licking) to measure fear to contextual stimuli. These results are discussed in terms of the role context conditioning may play in US preexposure.

     

Contextually Based Conditional Discrimination of the Rabbit Eyeblink Response

Rabbits received conditional discrimination training using contextual stimuli to set the occasion for stimulus pairings during eyelid conditioning. Specifically, animals were exposed to either the presence or the absence of an oscillating chamber light throughout the intertrial interval (50 ± 10 s). For half the animals, this light signaled paired presentations of a discrete tone conditioned stimulus (CS) and air puff unconditioned stimulus (US) while darkness signaled presentations of only the tone CS. The remaining animals experienced the opposite contextual relationship to the conditioning stimuli. These trial types occurred pseudo-randomly across a session, with all transitions between contextual settings (i.e., light or dark) taking place immediately at the CS–US offset. Under these conditions, animals successfully utilized the contextual stimuli as conditional cues for differential responding to the shared CS. Moreover, both light and dark were equally effective as discriminative stimuli. A subset of animals received further training in which the contextual contingency was removed by restricting all conditioning to the CS-alone context. Without the contingency in place, subsequent CS presentations (paired and CS-alone) evoked equivalent conditioned responding across three sessions of training. Following the reinstatement of the contextual contingencies, discriminatory responding was immediately observed and returned to previous levels within three sessions. Finally, animals appeared to use the static representation of the conditional cue, rather than the phasic transition between cues, for discriminatory responding. These findings are discussed in terms of current neurobiological models of eyelid conditioning.