Locus of the effect of a surprising reinforcer in the attenuation of blocking

Previous experiments on conditioned suppression in rats have shown that prior conditioning to one element of a compound conditioned stimulus paired with shock may block or prevent conditioning to the other element. Reliable conditioning may, however, occur to the added element (blocking may be attenuated), if a surprising second shock is added shortly after each compound trial. Experiment I confirmed this finding, and further showed that blocking was attenuated only when the second shock occurred 10 s after the compound trial, not when it occurred 100 s later. Experiment II showed that the surprising omission of an expected second shock 10 s after each compound trial would also attenuate blocking, thus implying that the surprising event does not itself act to reinforce conditioning to the added element, but rather permits the unconditioned stimulus (the first shock) to play its normal role as an effective reinforcer. This conclusion was confirmed by Experiment III, which showed that a surprising second shock does not produce any increase in conditioning to the added element on the trial on which it occurs; rather it serves to ensure adequate conditioning to that element on a subsequent compound trial. The implication is that the surprising event acts proactively to prevent subjects learning to ignore an otherwise redundant stimulus.     

Conditioned inhibition of fear: Evidence for a competing response mechanism

In two experiments, inhibitory conditioning was attempted by presenting a discrete CS in a neutral stimulus environment shortly following the termination of either shock (Experiment 1) or a second discrete CS which had been paired in a forward manner with shock (Experiment 2). Evidence of successful inhibitory conditioning was mixed in Experiment 1, where the properties of the CS were assessed within an escape-from-fear procedure. Postresponse presentations of the CS enhanced performance, whereas the presentation of the CS prior to responding did not have the expected degrading effect on performance. In Experiment 2, the inhibitory properties of the CS were assessed by combining this stimulus with an excitatory CS and presenting the compound to rats engaged in a water-reinforced licking response. Less response suppression was found in reaction to this compound relative to three separate comparison conditions, thus witnessing the success of the inhibitory-conditioning procedure used. The common assumption that inhibitory conditioning results from the nonreinforcement of a CS in a situation where reinforcement is expected, i.e., one which contains previously reinforced cues, is not supported by these data, for no previously reinforced cues were simultaneously presented with the CS during inhibitory training. The data are in agreement with a conditioned antagonistic-response interpretation of inhibitory conditioning.     

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.     

Contextual control of the extinction of conditioned fear

Rats received 15 pairings of a CS and shock in one context, and then a series of CS-alone trials in a second context. Even though this extinction procedure produced a complete loss of conditioned suppression, when the animals were returned to the site of original conditioning, suppression was renewed to a level comparable to that of animals that had not undergone extinction. Controls indicated that the renewed suppression was not due solely to pseudoconditioning, suggesting that the CS-US association had survived extinction. Renewed suppression was also demonstrated in a third context that was never associated with shock. Loss of suppression did not necessarily depend upon inhibitory conditioning of the extinction context. The data suggest that extinction of conditioned fear is specific to the context in which it occurs. They also suggest the possibility that animals might discriminate episodes in which a CS is reinforced and nonreinforced independently of the excitatory or inhibitory status of cues, like contextual stimuli, that are coincidentally present during those episodes.     

Transfer of conditioned appetitive stimuli to conditioned aversive excitatory and inhibitory stimuli

The transfer of Pavlovian appetitive stimuli to Pavlovian aversive stimuli was examined in three experiments. In Experiment 1, rats received appetitive (Ap) conditioning designed to establish a flashing-light stimulus as either a CS+, CSo, or CS? for food, or to maintain it as a novel stimulus for US-alone subjects. Then, the stimulus was employed as a signal for weak shock in conditioned-emotional-response (CER) training. Both acquisition and extinction results showed that the ApCS+ facilitated and the ApCS? retarded aversive excitatory conditioning relative to the ApCSo and US-alone controls. Experiment 2 replicated the findings of Experiment 1 with both a moderate and a severe shock in CER training. In Experiment 3, different groups received the same appetitive conditioning as before, but to a flashing-light stimulus which was then employed as a signal for no shock in CER training. The ApCS? facilitated and the ApCS+ retarded aversive inhibitory conditioning relative to ApCSo and US-alone controls. Collectively, these findings establish that, in Pavlovian conditioning, transfer of an appetitive CS to an aversive excitor or inhibitor is facilitated by maintaining the initial conditioning contingency.     

Protection from extinction in human fear conditioning

Two experiments examined the ability of an added stimulus to interfere with extinction of a target excitatory fear stimulus (a predictor of shock) in human autonomic conditioning. Both experiments demonstrated disruption of extinction when the added stimulus was inhibitory (a predictor of no shock, or safety signal). Subjects showed a return of fear when the target stimulus was tested alone, on both self-reported shock expectancy and skin conductance measures. The second experiment also demonstrated disruption of extinction when the added stimulus was excitatory. This results suggests that protection from extinction may occur even when the added stimulus is not inhibitory. Additional factors that may contribute to protection from extinction include context-specificity, occasion-setting and external inhibition. The results highlight the role that concurrent stimuli play in extinction, and emphasise the need to keep concurrent stimuli as similar as possible to the desired transfer context in practical applications of extinction such as exposure therapy for anxiety.     

Summation of excitatory and inhibitory control produced by traditional tone-shock contingencies and autocontingencies

Previous research has demonstrated that rats can use unsignaled shock to predict subsequent periods free from shock. This shock-no shock stimulus arrangement, termed an autocontingency, has appeared less likely to exert behavioral control when a traditional tone-shock contingency was simultaneously available. The present research examined the generality of CS-US contingency dominance in a conditioned suppression paradigm by using a summation test in which “probe” stimuli derived from tone-shock contingencies were superimposed upon responding maintained by an autocontingency. In experiment 1, an inhibitory CS accelerated responding only when responding was normally suppressed by the autocontingency. In experiment 2, an excitatory CS failed to yield conditioned suppression during an inhibitory (accelerative) period produced by the autocontingency. Unlike our previous findings (e.g., Davis, Memmott & Hurwitz, 1975), these results do not support a general notion of tone-shock contingency dominance over autocontingencies. Behavioral control by autocontingencies appears robust and “holds its own” in summation with both excitatory and inhibitory CSs derived from traditional contingencies.     

Testing response generation rules

Robbins (1988) reported data that he viewed as inconsistent with Miller and Schachtman's (1985a) comparator hypothesis of conditioned response generation. Here we explain why we do not find his experiments a compelling test of the comparator hypothesis. We also briefly review other studies that tested the same predictions of the comparator hypothesis that Robbins examined. We conclude that there is considerable evidence that following excitatory or inhibitory conditioning with a target conditioned stimulus (CS) and unconditioned stimulus (US), extinction of other cues that were present during CS training ordinarily increases excitatory responding and decreases inhibitory responding to the CS. However, consistent with Robbins's conclusion, there is scant evidence that after CS-US training, enhancing the associative value of other cues that were present during CS training influences excitatory or inhibitory responding to the CS. The implications of these conclusions for the comparator hypothesis as an explanation of differences in acquired behavior and as a heuristic tool are considered.     

The comparator hypothesis of conditioned response generation: manifest conditioned excitation and inhibition as a function of relative excitatory strengths of CS and conditioning context at the time of testing

In the present research water-deprived rats were used in a conditioned lick suppression paradigm to test and further develop Rescorla's (1968) contingency theory, which posits that excitatory associations are formed when a conditioned stimulus (CS) signals an increase in unconditioned stimulus (US) likelihood and that inhibitory associations develop when the CS signals a decrease in US likelihood. In Experiment 1 we found that responding to a CS varied inversely with the associative status of the context in which the CS was trained and that this response was unaltered when testing occurred in a distinctively dissimilar context with a different conditioning history, provided associative summation with the test context was minimized. These results suggest that manifest excitatory and inhibitory conditioned responding is modulated by the associative value of the training context rather than that of the test context. In Experiment 2 it was demonstrated that postconditioning decreases in the associative value of the CS training context reduced the effective inhibitory value of the CS even when testing occurred outside of the training context. Moreover, this contextual deflation effect was specific to the CS training context as opposed to any other excitatory context. Collectively, these studies support the comparator hypothesis, which states that conditioned responding is determined by a comparison of the associative strengths of the CS and its training context that occurs at the time of testing rather than at the time of conditioning. This implies that all associations are excitatory and that responding indicative of conditioned inhibition reflects a CS-US association that is below (or near) the associative strength of its comparator stimulus. It is suggested that response rules which go beyond a monotonic relation between associative value and response strength can partially relieve learning theories of their explanatory burdens, thereby allowing for simpler models of acquisition.     

Analysis of the learned irrelevance effect in appetitive Pavlovian conditioning

In Experiments 1 and 2 rats received uncorrelated presentations of a light conditioned stimulus (CS) and a food unconditioned stimulus (US) on each day of a preexposure phase. Control subjects received the same number of USs during the first half of preexposure and the same number of CSs during the second. Uncorrelated preexposure retarded inhibitory conditioning. Experiment 3 showed, however, that the different patterns of US preexposure experienced by the two groups could in itself influence the course of subsequent inhibitory conditioning. When this factor was equated by restricting the uncorrelated treatment to the first half of the pre-exposure phase (Experiment 2) or by extending the control treatment throughout the phase (Experiment 4) it was found that uncorrelated preexposure retarded excitatory conditioning, but facilitated inhibitory conditioning. This outcome challenges an interpretation in terms of the concept of learned irrelevance, which predicts that uncorrelated preexposure should retard both forms of conditioning.     

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.     

Latent inhibition of a CS during CS-US pairings

In each of three experiments rats were trained by the conditioned-emotional-response technique with a conditioned stimulus (CS) predicting a relatively weak shock, the unconditioned stimulus (US). In the second stage of training the intensity of the shock was increased, and it was found that subjects for whom the same CS was used in both stages acquired further suppression less readily than subjects that experiences a new CS in the second stage. The implication of these results for theories of attention and for theories of habituation is discussed. It is suggested that associations formed by the test CS during the first stage of training reduce the readiness of the stimulus to enter into new associations, either because an association between the stimulus and the context reduces further processing of the stimulus or because the association between the test stimulus and the weak shock attenuates the formation of an association with the stronger shock.     

Context Specificity of Excitation and Inhibition in Ambiguous Stimuli

Two experiments examined the susceptibility of excitation and inhibition to contextual change when the conditioned stimulus (CS) was ambiguous using an appetitive conditioning paradigm. In Experiment 1, excitation to a CS was lost with a context switch when inhibition had been learned to the CS in a prior feature-negative (FN) discrimination. Control groups that had received either more or less excitatory conditioning in the absence of inhibitory pretraining showed no loss. In Experiment 2 inhibition was lost with a context switch in a group that had received excitatory and then inhibitory conditioning with the CS. No loss was observed in a group that had not received excitatory pretraining. The results suggest that contexts are especially likely to control performance to ambiguous CSs when they can modulate the second of two learned associations. Results are discussed in terms of their implications for occasion setting and modern conditioning theory.     

Associability of a previously conditioned stimulus as a function of qualitative changes in the US

Hall and Pearce (1979) reported retarded manifestation of conditioned responding to repeated CS-strong shock pairings as a result of prior CS-weak shock pairings. These authors suggested that a latent inhibition (LI)-like process reduced the associability of the CS during weak shock conditioning despite excitatory associations between CS and weak shock being formed. The present experiments examined the possibility that the negative transfer from CS-weak shock conditioning in Stage 1 to CS-strong shock conditioning in Stage 2 observed by Hall and Pearce was due at least in part to the similarity between weak and strong shock rather than, or in addition to, a general loss of CS associability. Specifically, the transfer of decreased associability to conditioning with a dissimilar US was investigated. Consistent with Hall and Pearce, who gave multiple training trials in Stage 2, Experiment 1 found the development of conditioned responding owing to a single CS-strong shock pairing in Stage 2 to be retarded by prior CS-weak shock pairings and compared this effect to conventional LI. In Experiment 2, partial attenuation of the negative transfer following CS-weak shock was obtained by substituting ice water immersion for strong shock, that is, by making the strong US qualitatively dissimilar from the weak US. In contrast, conventional LI resulting from preconditioning CS-only exposures was equivalent for strong shock in Experiment 1 and ice water immersion in Experiment 2. A possible mechanism for the sensitivity to qualitative US changes of the observed negative transfer is discussed.     

Lasting increases in basolateral amygdala activity after emotional arousal: implications for facilitated consolidation of emotional memories

Manipulations that reduce or enhance the activity of basolateral amygdala (BLA) neurons in the minutes to hours after training have been shown to respectively impair or facilitate retention on the inhibitory avoidance task. Although this suggests that BLA activity is altered after emotional arousal, such changes have not been directly demonstrated. To test this, we devised a feline analog of the inhibitory avoidance task and recorded BLA unit activity before and after a single inescapable footshock. Single-unit recordings revealed that the firing rate of many BLA neurons gradually increased after the footshock, peaking 30-50 min post-shock and then subsiding to baseline levels 2 h later. During this period of increased activity, the discharges of simultaneously recorded BLA cells were more synchronized than before the shock. Although it was known that pairing innocuous (conditioned stimulus, CS) and noxious stimuli modifies the responsiveness of BLA neurons to the CS, our results constitute the first demonstration that emotional arousal produces lasting increases in the spontaneous firing rates of BLA neurons. We propose that these changes in BLA activity may promote Hebbian interactions between coincident but spatially distributed activity patterns in BLA targets, facilitating the consolidation of emotional memories.     

The role of context in the inhibitory conditioning of honeybees

Conditioned inhibition or CI training (A+/AB-) was compared with S- training (A+/B-) in three experiments on proboscis-extension conditioning in harnessed honeybees. The purpose was to test the Rescorla-Wagner assumption, widely credited in the vertebrate literature, that a nonreinforced stimulus acquires inhibitory properties in proportion to the excitatory value of the context in which it is presented. In prior work with free-flying honeybees pretrained with sucrose to come of their own accord to the experimental situation, no differences were found in the consequences of CI and S- training, perhaps because A added little to the excitatory value of the context (already very high) in which B occurred. In the new experiments, with harnessed subjects brought involuntarily into the training situation, negative results again were obtained. The possibility is considered that inhibitory conditioning in honeybees is independent of the excitatory value of the context.     

The biological function of Pavlovian conditioning: Learned inhibition of aggressive behavior in territorial fish

Following Pavlovian discrimination training, stimuli predicting the appearance of a territory intruder (an excitatory conditional stimulus, CS+) or the absence of that event (an inhibitory conditional stimulus, CS−) were presented to pairs of territorial male fish immediately before their first aggressive interaction. Pairmates that both received excitatory stimuli prior to the confrontation were significantly more aggressive than a control group which received the same training but which received neither a CS+ nor a CS− in the test. Pairmates in which both received a CS− were significantly less aggressive than the control group. In these three groups, no differences in aggression were observed between the individual members of a single pair. Two additional groups were composed of pairs whose members received different stimuli prior to the test. Although no differences were found between pairmates in the group in which one member received a pretest CS− while the other member received no stimulus presentation, large differences in aggressive behavior were obtained when one fish received a CS+ and its pairmate received a CS−. We discuss the behavioral ecology of terriorial behavior in fish and attempt to show the potential importance of these results in this naturalistic context. In addition, we discuss the implications of an ecological approach for causal analyses of inhibitory learning.     

Constraints on Pavlovian aversive conditioning: Implications for avoidance learning in the rat

Four experiments investigated the relative degree of control exerted by several conditional stimuli when each stimulus: (a) preceded shock, (b) followed shock, and preceded a shock-free interval, (c) was independent of shock, or (d) was novel. When the onset of an auditory stimulus had preceded shock (Experiments 1, 2A, and 3), it always exerted conditioned excitatory control. When the same stimulus preceded a shock-free interval, it never exerted conditioned inhibitory control. When the onset of light (Experiments 2B, 4), silence (2C), or darkness (1, 2D) preceded a shock-free interval, it always exerted conditioned inhibitory control. However, when one of the latter stimuli preceded shock, it failed to exert excitatory control. Several models of this phenomenon were tested. The implications of these results for the species-specific defence reaction and two-factor theory accounts of avoidance learning were outlined.     

Acquisition and retention of control of instrumental behavior by a cue-signaling airblast: How specific are conditioned anticipations?

The conditioned state evoked by a CS that had been paired with an aversive airblast was assessed by superimposing the CS on baselines of instrumental responding. The first experiment used a shock avoidance baseline; CS-airblast pairings were administered on the baseline, with the shock avoidance schedule in effect. The CS that signaled airblast came, over trails, to accelerate shock avoidance responding. As further CS-airblast trials were administered, however, the acceleratory effect of the CS decreased, producing an inverted-U-shaped acquisition curve. A second experiment used off-baseline CS-airblast conditioning, and the CS was tested on both shock avoidance and water reinforcement baselines. After 20 CS-airblast pairings the CS accelerated shock avoidance and suppressed water-reinforced responding. After 10o pairings, however, the acceleratory effect on shock avoidance was much attenuated, although the suppressions of the water-reinforced behavior did not differ between 20- and 100-trial groups. Two further experiments examined retention, over a 45-day interval, of the attenuation of the CS's effects on shock avoidance. Over the retention interval, this attenuation disappeared. It was, however, reinstated by giving the animals “reminder” presentations of the airblast. These results are interpreted as representing systematic changes in the specificity of the conditioned state evoked by a Pavlovian CS.     

The overshadowing of background stimuli: Some effects of varying amounts of training and ucs intensity

Two experiments investigated the capacity of a nominal CS to overshadow background stimuli. Rats received CS-shock pairings in one compartment of a double compartment apparatus. After training the shock compartment was represented, but in the absence of both the CS and shock. Overshadowing was then assessed by measuring rats' latency to enter this compartment. If rats readily entered the shock compartment this indicated that the background cues in that compartment had acquired little or no associative strength during training, and overshadowing was therefore inferred. If however rats avoided the shock compartment, then this indicated that the background stimuli must have become aversive during training, and overshadowing could not then be inferred. In both experiments it was found that the capacity of a CS to overshadow background stimuli was directly related to the amount of training given. The experiments also showed that this capacity is inversely related to shock intensity. The results are discussed in terms of Rescorla and Wagner's (1972) model of conditioning.