Deepened extinction from compound stimulus presentation

Three experiments with rats and 2 with pigeons explored the effect of presenting 2 extinguished excitatory stimuli in compound. Four learning situations were used: Pavlovian magazine approach, Pavlovian fear conditioning, and instrumental discriminative instrumental learning in rats, as well as Pavlovian sign tracking in pigeons. All 5 experiments confirmed D. Reberg's (1972) observation that even after extinction of the individual stimuli, presenting them in compound evoked substantial responding. Moreover, nonreinforcement of that compound deepened extinction of an element more substantially than did additional presentation of that element alone. Such compound exposure reduced spontaneous recovery, reduced reinstatement, and slowed subsequent reconditioning. The primary determinant seemed to be the enhanced associative strength rather than the enhanced conditioned responding that occurred during the nonreinforced compound.     

Spontaneous recovery after extinction of the conditioned proboscis extension response in the honeybee

In honeybees, the proboscis extension response (PER) can be conditioned by associating an odor stimulus (CS) to a sucrose reward (US). Conditioned responses to the CS, which are acquired by most bees after a single CS-US pairing, disappear after repeated unrewarded presentations of the CS, a process called extinction. Extinction is usually thought to be based either on (1) the disruption of the stored CS-US association, or (2) the formation of an inhibitory "CS-no US" association that is better retrieved than the initial CS-US association. The observation of spontaneous recovery, i.e., the reappearance of responses to the CS after time passes following extinction, is traditionally interpreted as a proof for the formation of a transient inhibitory association. To provide a better understanding of extinction in honeybees, we examined whether time intervals during training and extinction or the number of conditioning and extinction trials have an effect on the occurrence of spontaneous recovery. We found that spontaneous recovery mostly occurs when conditioning and testing took place in a massed fashion (1-min intertrial intervals). Moreover, spontaneous recovery depended on the time elapsed since extinction, 1 h being an optimum. Increasing the number of conditioning trials improved the spontaneous recovery level, whereas increasing the number of extinction trials reduced it. Lastly, we show that after single-trial conditioning, spontaneous recovery appears only once after extinction. These elements suggest that in honeybees extinction of the PER actually reflects the impairment of the CS-US association, but that depending on training parameters different memory substrates are affected.     

Some types of conditioned inhibitors carry collateral excitatory associations

Two experiments using summation tests in conditioned suppression with rats examined whether conditioned inhibitors generated by five different conditioning procedures have an associative structure which includes collateral excitatory associations. The existence of collateral conditioned excitation was inferred from an increase in the amount of manifest conditioned inhibition after a conditioned inhibitory stimulus (CS-) extinction treatment. The five CS-s evaluated were differential, explicitly unpaired, conditional, backward, and trace. With abbreviated conditioning (Experiment 1), the differential and explicitly unpaired CS-s exhibited conditioned inhibitory properties; the conditional, backward, and trace CS-s did not. Repeated extinction presentations of the CS- in the absence of the unconditioned stimulus unmasked conditioned inhibition to the conditional, backward, and trace CS-s revealing moderate degrees of conditioned inhibition for all five CS-s. After more extensive conditioning (Experiment 2), the explicitly unpaired and conditional CS-s were strongly inhibitory and the differential and trace CS-s were moderately inhibitory. The backward CS- was not inhibitory. Repeated presentations of the CS- in extinction unmasked conditioned inhibition to trace and backward CS-s. All five CS-s were now nearly equally inhibitory. That the measured inhibitory power of backward, trace, and conditional (after few trials) CS-s can be modulated by a CS- extinction treatment suggests that they have similar associative structures and carry, in addition to inhibitory associations, collateral excitatory associations that mask the expression of conditioned inhibition.     

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.     

Different mechanisms of fear extinction dependent on length of time since fear acquisition

Fear extinction is defined as a decline in conditioned fear responses (CRs) following nonreinforced exposure to a feared conditioned stimulus (CS). Behavioral evidence indicates that extinction is a form of inhibitory learning: Extinguished fear responses reappear with the passage of time (spontaneous recovery), a shift of context (renewal), and unsignaled presentations of the unconditioned stimulus (reinstatement). However, there also is evidence to suggest that extinction is an "unlearning" process corresponding to depotentiation of potentiated synapses within the amygdala. Because depotentiation is induced more readily at short intervals following LTP induction and is not inducible at all at a sufficient delay, it may be that extinction initiated shortly following fear acquisition preferentially engages depotentiation/"unlearning," whereas extinction initiated at longer delays recruits a different mechanism. We investigated this possibility through a series of behavioral experiments examining the recoverability of conditioned fear following extinction. Consistent with an inhibitory learning mechanism of extinction, rats extinguished 24-72 h following acquisition exhibited moderate to strong reinstatement, renewal, and spontaneous recovery. In contrast, and consistent with an erasure mechanism, rats extinguished 10 min to 1 h after acquisition exhibited little or no reinstatement, renewal, or spontaneous recovery. These data support a model in which different neural mechanisms are recruited depending on the temporal delay of fear extinction.     

Extinguishing conditioned inhibition in flavour-aversion learning: Effects of repeated testing and extinction of the excitatory element

Three conditioned inhibition experiments using an A+/AX- design are reported in which lithium-mediated excitatory conditioning occurred to distinctive environmental stimuli and inhibitory conditioning to a vinegar flavour. Increased vinegar preferences were observed (i.e., conditioned inhibition) in each experiment, and these preferences extinguished with repeated testing as well as following extinction of the excitatory element. Vinegar preferences could be reinstated through reconditioning of the extinguished excitatory stimulus. These experiments speak to the status of inhibitory responding as a “slave” process to conditioned excitation.     

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.     

Recovery of the US representation over time during extinction

Four experiments used a conditioned suppression procedure in rats to explore changes in the US representation over time during the course of extinction. They employed two previously reported effects: reinstatement of responding to an extinguished CS by separate US presentation, and the erasure of that effect by interposed nonreinforcement of a second excitatory CS. These effects have been interpreted as enhancing and depressing the US representation, respectively. Experiment 1 found the erasing effect to decrease but still to remain substantial after over a 4-day period, suggesting a partial recovery with time of a deliberately depressed US representation. Experiment 2 implicated this change as a contributor to the phenomenon of spontaneous recovery by showing that recovery to be sensitive to erasure effects. Experiments 3 and 4 found evidence for an interaction between the state of the US representation and the amount of associative change which results from nonreinforcement of an excitatory CS. When the US representation was strong, either because of reinstatement or the passage of time, nonreinforcement of a CS was especially effective in producing associative change. When the US representation had been depressed by erasure, those nonreinforcements produced relatively less associative loss. Moreover, these effects upon associations were reasonably stable in the sense that they left asymptotic differences in the strength of associations after extinction. Together with previous findings, these results point to an important role for the US representation in the performance and learning which occurs during extinction.     

Recent and Remote Extinction Cues Reduce Spontaneous Recovery

Five appetitive conditioning experiments with rats examined the ability of extinction cues (ECs) to reduce spontaneous recovery after extinction procedures that varied the temporal relation between the ECs and the conditioned stimulus (CS) and included presentations of additional events (e.g. other stimuli correlated with extinction, CSs, and the US). In extinction, two different ECs were presented either closely in time before (i.e. recent to), or more distant (i.e. remote) from a nonreinforced CS. Both recent and remote ECs reduced spontaneous recovery to the CS when present during testing (Experiments 1-4). Each EC reduced recovery despite the addition during extinction of a second EC and CS (Experiments 1, 3, and 4), and the US (Experiment 3). Experiments 4 and 5 investigated the recent and remote ECs' tendency to control a serial occasion setting discrimination involving the target CS under explicit training conditions. Neither EC gained such discriminative control. Possible explanations of the results are discussed, including configural learning, occasion setting, and contextual cue control.     

Reinstatement of fear to an extinguished conditioned stimulus.

Four experiments are reported which demonstrate the ability of an unconditioned stimulus (UCS) presentation following extinction to partially reinstate the conditioned response. These experiments are interpreted in terms of the strengthening of an extinction-reduced UCS representation. The first two experiments address alternative interpretations in terms of sensitization, reinstating the stimulus conditions of acquisition, conditioning of background cues, and stimulus generalization. Experiment 3 suggests that reinstatement is possible with a UCS qualitatively different from that used in conditioning. Experiment 4 explores an alternative extinction procedure which especially preserves the conditioned stimulus-unconditioned stimulus association while encouraging modification of the UCS representation. The results are discussed both in terms of related empirical phenomena, such as spontaneous recovery and sensory preconditioning, and in relation to the general role of the UCS representation in conditioning.     

Stimulus generalization of excitation and inhibition

Five sign-tracking experiments with pigeons investigated the breadth of stimulus generalization of excitatory and inhibitory conditioning. Using a compound stimulus test procedure, these experiments found evidence for a narrower generalization of associative strength in excitation than in inhibition. They also found a narrower associative gradient with a more strongly conditioned excitatory stimulus, although this did not seem to account for the difference between exciters and inhibitors. These results confirm earlier findings comparing generalization after acquisition and extinction and raise various theoretical issues about generalization.     

Stimulus generalization of excitation and inhibition

Five sign-tracking experiments with pigeons investigated the breadth of stimulus generalization of excitatory and inhibitory conditioning. Using a compound stimulus test procedure, these experiments found evidence for a narrower generalization of associative strength in excitation than in inhibition. They also found a narrower associative gradient with a more strongly conditioned excitatory stimulus, although this did not seem to account for the difference between exciters and inhibitors. These results confirm earlier findings comparing generalization after acquisition and extinction and raise various theoretical issues about generalization.     

Comparing excitatory backward and forward conditioning

Three Pavlovian lick suppression studies with rats were conducted to compare the role of the conditioning context in excitatory backward and forward conditioning. The experiments explored the possibility that excitatory backward conditioning, but not forward conditioning, is mediated by the context. That is, in excitatory backward conditioning, the conditioning context may function as an excitatory mediator, which supports second-order conditioning of the target cue. This possibility contrasts with traditional accounts, which suggests that common processes underlie excitatory backward and forward conditioning. Experiment 1 found that conditioned responding following backward conditioning was attenuated as a result of posttraining extinction of the training context, but the same manipulation elevated responding after forward conditioning. Experiments 2 and 3 found that posttraining and pretraining associative inflation of the context (presenting unsignalled USs) increased conditioned responding to the target of a backward conditioning procedure but either had no effect or reduced responding to the target of a forward conditioning procedure. Thus, excitatory backward and forward conditioning appear to differ in their dependence on the status of the conditioning context.     

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.     

Instrumental to Pavlovian transfer: Learning about response-reinforcer contingencies affects subsequent learning about stimulus-reinforcer contingencies

Two experiments examined the interaction between response-reinforcer (R-S) and stimulus-reinforcer (S-S) learning. In both experiments, three groups of rats were exposed to escapable, yoked inescapable, or no shocks. All groups were then exposed to either two or four sessions of truly random control (TRC) conditioning (Experiment 1) or to an excitatory conditioning procedure (Experiment 2) in which the shock US occurred with either moderate or low probability. Excitatory strength of the CS was assessed during extinction by a conditioned emotional response (CER) test. Inescapably shocked rats conditioned less than did their escapably shocked and nonshocked partners under all TRC conditions of Experiment 1, but only conditioned less than their partners in Experiment 2 when exposed to the moderate CS-US contingency for four sessions. These results provide a clear demonstration of transfer between instrumental training and Pavlovian excitatory conditioning and thus, support the influence of learning about R-S contingencies upon subsequent learning about S-S contingencies. Both a contextual blocking interpretation and an expansion of the learned helplessness theory were discussed as possible explanations of this transfer.     

Extinction, spontaneous recovery and renewal of flavor preferences based on taste-taste learning

This paper presents evidence of extinction, spontaneous recovery and renewal in a conditioned preferences paradigm based on taste-taste associations. More specifically, in three experiments rats exposed to a simultaneous compound of citric acid-saccharin solution showed a preference for the citric solution when the preference was measured with a two-bottle test (citric vs. water). Experiment 1 revealed that conditioned preferences were extinguished by repeated presentations of the citric acid solution without the saccharin. In Experiment 2, an additional test trial was introduced 21 days after the extinction treatment. Delayed testing resulted in the recovery of the extinguished preference for the citric, reflecting a spontaneous recovery effect. Experiment 3 revealed a preference renewal effect that was obtained when the extinction was conducted in a context different from that of the remaining experimental stages. The implications of these results are analyzed with attention paid to the mechanisms underlying learning of flavor preferences.     

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.     

Effects of contextual conditioning and unconditional stimulus presentation on performance in appetitive conditioning

Four experiments with rat subjects examined the effects of contextual conditioning on conditioned appetitive performance. Experiment 1 compared the effects of contextual conditioning on performance to conditioned stimuli (CSs) with different conditioning histories. Contextual conditioning enhanced performance to the CS if the CS had first been conditioned and then extinguished, but had no effect on performance when the CS had been merely paired or unpaired with food. Experiments 2 and 3 then asked whether the effect on the extinguished CS was due to contextual conditioning acting as a cue for conditioning. In Experiment 2, extinction procedures in which extra unconditioned stimuli (USs) were presented during the intertrial intervals were found to reduce the CS's sensitivity to enhancement by contextual conditioning, but had no effect on spontaneous recovery. In Experiment 3, USs added to conditioning or extinction acquired the ability to cue the corresponding performance. Under some conditions, USs added to conditioning could suppress performance (Experiment 4). The results suggest that contextual conditioning has complex effects that can be better understood by recognizing that contextual conditioning, as well as the USs that create it,Mayacquire discriminative control over conditioned responding.     

Backward conditioning: mediation by the context

The information acquired in backward conditioning (i.e., outcome-->cue) was assessed in 3 Pavlovian lick-suppression experiments with water-deprived rats as subjects. Experiment 1 confirmed previous research that few outcome-->cue pairings made the cue into a conditioned excitor and additionally showed that massive posttraining extinction of the training context attenuated a backward-trained cue's excitatory value. Experiment 2 found that many outcome-->cue pairings made the cue into a conditioned inhibitor and that the same context manipulation attenuated this inhibitory value. Experiment 3 confirmed the observations of Experiments 1 and 2 and demonstrated that these effects of context extinction were specific to backward-trained cues conditioned in the extinguished context. These results are interpreted in terms of cue-->context and context-->outcome associations.     

No sex difference in contextual control over the expression of latent inhibition and extinction in Pavlovian fear conditioning in rats

Three experiments with Wistar rats searched for a sex difference in contextual control over the expression of latent inhibition and extinction. Experiment 1 used a latent inhibition procedure; Experiments 2 and 3 employed an extinction preparation. All experiments used a shock as the unconditioned stimulus, a tone as the conditioned stimulus, and suppression of food magazine visits as the measure of conditioned responding to the tone. Each experiment revealed a reliable context effect on conditioned responding to the tone; after conditioning in a separate context, conditioned responding in the former latent inhibition or extinction context was attenuated relative to conditioned responding in a control context. There was no sex difference in the magnitude of this effect. These results are discussed in the framework of sex differences in the hippocampus and of the putative role of this structure in various instances of contextual learning.