Differential acquisition,extinction, and reinstatement of conditioned suppression in mice

In animals, the reappearance of conditioned fear responses after extinction has been primarily investigated using single-cue conditioning paradigms. However, a differential paradigm can overcome several of the disadvantages associated with a single-cue procedure. In the present study, the reinstatement phenomenon was assessed in mice using a differential conditioned suppression paradigm. In a first phase, one conditioned stimulus (CS + ) was consistently paired with an unconditioned stimulus (US; footshock) while another CS (CS–) was not, resulting in selective suppression of previously trained instrumental behaviour during the CS + . After the extinction phase, half of the animals (reinstatement group) were presented with unsignalled USs, while the other half were not (control group). A differential return of conditioned responding was observed in the reinstatement group, but not in the control group. The implications of these findings for future conditioning research are discussed.     

Differential acquisition, extinction, and reinstatement of conditioned suppression in mice

In animals, the reappearance of conditioned fear responses after extinction has been primarily investigated using single-cue conditioning paradigms. However, a differential paradigm can overcome several of the disadvantages associated with a single-cue procedure. In the present study, the reinstatement phenomenon was assessed in mice using a differential conditioned suppression paradigm. In a first phase, one conditioned stimulus (CS + ) was consistently paired with an unconditioned stimulus (US; footshock) while another CS (CS-) was not, resulting in selective suppression of previously trained instrumental behaviour during the CS + . After the extinction phase, half of the animals (reinstatement group) were presented with unsignalled USs, while the other half were not (control group). A differential return of conditioned responding was observed in the reinstatement group, but not in the control group. The implications of these findings for future conditioning research are discussed.     

Conditioned suppression of an avoidance response by a stimulus paired with food

Three food-deprived Long-Evans rats were exposed to a non-discriminated shock avoidance procedure. Superimposed upon this operant avoidance baseline were periodic presentations of a conditioned stimulus that was paired with food, the unconditioned stimulus. These pairings resulted in increases in the rate of shock over that recorded when the conditioned stimulus was not present. A traditional suppression ratio failed to reveal any differential effect of the conditioned stimulus on the overall rate of avoidance responding, although all subjects showed a consistent pattern of pausing and postshock response bursts during presentations of the conditioned stimulus. When food was withheld during a final extinction phase, the conditioned stimulus ceased to occasion increases in shock rates and disruptive postshock response bursts were eliminated. An analysis of conditioned suppression procedures is proposed that stresses not only operant-Pavlovian or appetitive-aversive incompatibility, but also the manner in which the baseline schedule of reinforcement affects operant behavior changes that are elicited by the superimposed Pavlovian procedure.     

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.     

Conditioned suppression under positive, negative, and no contingency between conditioned and unconditioned stimuli

Using a conditioned suppression procedure, the effects of three contingent relationships between conditioned (CS) and unconditioned (US) stimuli were investigated. A traditional positive (if CS—then US) contingency suppressed response rate during the CS relative to responding during stimulus-free minutes of the session. A negative (if CS—then no US) contingency resulted in suppressed responding during CS-off minutes, and rate increases during the CS. A no-contingency control procedure, during which CS and US were randomly related, almost totally suppressed responding throughout the session and showed no differential effects of the CS on response rate. An analysis of changes in response rate during the minute after US-offset revealed acceleration under the no-contingency condition and, to a somewhat lesser degree, under the negative contingency. Both conditioned suppression and non-suppression are analyzed in terms of the temporal relationship between CS and US.     

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.     

Summation of conditioned suppression

Four rats were trained to suppress responses in the presence of two separately presented stimuli that signalled shock in a conditioned-suppression paradigm. The two stimuli that signalled shock were then presented simultaneously to evaluate the effect of stimulus compounding on conditioned suppression. Two rats were tested by presenting the compound conditioned stimulus while conditioned suppression was being maintained to the individual conditioned stimuli. The other two rats were tested by giving them random presentations of the compound conditioned stimulus and the single conditioned stimuli during extinction of conditioned suppression. All four rats showed greater suppression to the compound stimulus than to either stimulus presented alone.     

Lesions of Periaqueductal Gray Dissociate-Conditioned Freezing From Conditioned Suppression Behavior in Rats

It is commonly assumed that suppression of an ongoing behavior is an indirect measure of freezing behavior. We tested whether conditioned suppression and freezing are the same or distinct conditioned responses. Rats were trained to press a bar for food and then given fear-conditioning sessions in which a tone was paired with a foot shock (two pairings a day for 2 days). They then received either sham or electrolytic lesions of the periaqueductal gray (PAG). Post-training PAG lesions blocked freezing to the conditioned stimulus (CS), but had no effect on the suppression of operant behavior to the same CS. Thus, conditioned suppression and freezing, which both cause a cessation in activity, appear to be mediated by separate processes.     

Frequency of reinforcement as a parameter of conditioned suppression

Two pigeons were trained on a multiple VI-1; VI-4 min schedule for food reinforcement until a stable differential rate of response was established. Each component of the multiple schedule was in effect for 10 min and was separated from the other by 1 min time out. An Estes-Skinner conditioned suppression procedure was superimposed on each component of the schedule. The relative magnitude of the suppression behavior was measured during its acquisition and extinction, and at CS durations of 100, 200, and 300 sec. The initial magnitude of the suppression behavior was less severe on the VI-1 baseline than on the VI-4, and it extinguished more rapidly on the VI-1. As the relative duration of the CS was increased, the suppression behavior became less severe on both baselines, but the initial differential magnitude in the suppression remained intact.     

Effects of similarity of location and temporal intensity pattern of conditioned and unconditioned stimuli on the acquisition of conditioned suppresion in rats.

This article two studies that examined the effect of similarity of location and temporal intensity patterns of the conditioned stimulus (CS) and the unconditioned stimulus (UCS) on the acquision of conditioned suppression. Experiment 1 showed that greater suppression occurs during a stimulus generalization test when the tested stimulus has a location and temporal intensity pattern that is similar to the previously presented UCS. Experiment 2 showed that conditioned suppression is acquired more rapidly if the CS and UCS have similar locations and temporal intensity patterns. These similarity factors were interpreted as forms of event covariation, which aided in associative formation. Several applications of these data are discussed.     

Conditioned suppression to odorous stimuli in pigeons,

The conditioned suppression technique was employed to establish criterion discrimination of an amyl acetate concentration of 3% of vapor saturation, and to generate differential response rates in the presence of equal concentrations of amyl acetate and butyl acetate. The magnitude of suppression was also recorded as a function of amyl acetate concentration, with the concentrations presented in descending, ascending, and irregular series. The three stimulus presentation procedures generated approximately equivalent suppression versus concentration functions. Amyl acetate suppression thresholds were 0.16%, 0.50%, and 0.73% of vapor saturation for three subjects. Amyl acetate, butyl acetate, and butyric acid thresholds for two additional subjects were approximately 0.10% of vapor saturation. No suppression was recorded during control trials.     

The resistance of renewal to instructions that devalue the role of contextual cues in a conditioned suppression task with humans

The renewal of extinguished conditioned behaviour appears to reflect context-dependent learning. The present research used a conditioned suppression task with humans to examine whether instructions concerning the context could influence renewal. Pairings of a conditional stimulus (CS) and unconditional stimulus (US) were made in one context, followed by extinction trials of CS alone in a second context, and test trials of CS alone upon return to the original learning context. Four experiments tested whether the renewal of conditioned suppression observed during test would be attenuated if participants were instructed that the context changes were irrelevant to the predictive relationship between the CS and US. Using a differential conditioning design, no attenuation was found when the instructions were given prior to conditioning (Experiment 1) or immediately prior to the test trials (Experiment 2). The latter result was replicated with a single-cue conditioning design and further controls for exposure to the extinction contexts (Experiment 3). The collection of on-line ratings about the relationship between the contextual changes and the predictive nature of the CS indicated that participants did attend to and believe the instructions (Experiment 4). The results point to the resistance of renewal to explicit instructions that attempt to devalue the role of the contextual cues.     

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.     

Motivational properties of conditioned suppression

Two experiments were performed to investigate the interaction of baseline appetitive drive and incentive on the conditioned suppression of instrumental behavior exhibited in the presence of a preaversive stimulus. In one experiment, suppression of lever pressing of rats working on an intermittent food reinforcement schedule was considerably enhanced following partial satiation with food. In a second experiment, using a similar baseline, suppression was shown to be diminished by an increase in concentration of the baseline incentive. These results are consistent with the hypothesis that the instrumental suppression of the conditioned emotional response (CER) is a consequence of an algebraic interaction of hunger with fear.     

Transfer of conditioned inhibition across different aversive reinforcers in the rat

Three experiments using a conditioned suppression procedure in rats assessed transfer of conditioned inhibition across different aversive reinforcers. Experiment 1, using shock and car horn blast as reinforcers, showed that a noise negatively correlated with 0.7-mA shock between sessions attenuated suppression of lever pressing elicited by the signals for 0.7-mA shock and 110-db horn blast. Similarly, when the noise signaled the omission of horn blast, it attenuated suppression elicited by the signals for horn blast and shock. Experiment 2, using the same procedure, replicated transfer of conditioned inhibition from shock to horn found in Experiment 1, and indicated that such effects should be attributed to associative factors. Experiment 3, using the conditioned inhibition paradigm and different chambers during training and testing, replicated transfer from horn to shock and indicated that transfer cannot be attributed to multiple-background-reinforcer associations established during inhibitory training. The results of these experiments have implications for theories of conditioned inhibition.     

The effect of on‐ or off‐line extinction of a first‐order conditioned stimulus on a second‐order conditioned response in rats

In a water‐licking experiment with rats, the effects of the extinction of a first‐order conditioned stimulus (CS1) on the suppression of licking established for a second‐order conditioned stimulus (CS2) were explored. Extinction of the first‐order conditioned response (CR1) attenuated the conditioned suppression induced by CS2 when the rats had been allowed to lick water during the CR1 extinction phase. However, if water had been unavailable during the CR1 extinction phase, suppression by CS2 was not affected. The latter result is consistent with other studies of rats' conditioned suppression and suggests that the underlying mechanism of second‐order conditioning in this experiment is a connection between CS2 and the response elicited by CS1 rather than a CS2‐CS1 connection. The former result was interpreted as the CR1 extinction phase encouraging the rats to lick water despite the fear elicited by CS1, and thus, in testing, they licked despite the fear elicited by CS2.     

Transfer of inhibition after serial feature negative discrimination training

Three experiments examined the transfer of inhibition in Pavlovian serial feature negative (A+, X→ A−) discriminations in a conditioned suppression situation with rat subjects. Consistent with our previous report (P. C. Holland & J. Lamarre, Learning and Motivation, 15, 219–243), the feature (X) showed little or no ability to inhibit suppression to another conditioned excitor (B) that had been consistently reinforced. Nor was substantial transfer observed to excitors that had been partially reinforced, or conditioned, extinguished, and then reconditioned. However, X readily inhibited suppression to an excitor that had been trained within another serial feature negative discrimination (B+, Y → B−). These latter data are difficult to reconcile with our previous proposal that inhibitors established with serial procedures act on particular conditioned stimulus-unconditioned stimulus associations. We suggest that serial feature negative discriminations endow both the feature (X) and the excitor (A) with special properties.     

Conditioned suppression, punishment, and aversion

Three experiments were conducted to assess the aversive properties of a visual stimulus in the presence of which one group of birds received response-contingent shock (discriminated punishment) while a yoked group of birds received non-contingent shocks (conditioned suppression). In Experiment 1, presentation of the visual stimulus contingent on key pecking reduced the response rate (conditioned punishment effect) for birds under the conditioned suppression procedure but did not reduce the response rate of birds under the discriminative punishment procedure. Non-contingent shocks also produced greater suppression of responding maintained by positive reinforcement in the presence of a visual stimulus than did response-contingent shocks. In Experiment 2, a greater shock intensity (2 mA) was used. All the differences between the two groups found in Experiment 1 were also found in Experiment 2. Experiment 3 demonstrated that response-contingent shock did not result in a conditioned punishment effect even when positive reinforcers were unavailable during the discriminative punishment schedule. The exteroceptive stimulus that was paired with shock in the conditioned suppression procedure acquired the ability to punish behavior. The exteroceptive stimulus in the discriminative punishment schedule did not acquire this ability.     

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.     

Associative structure of differential inhibition: implications for models of conditioned inhibition

Following A+/X- training (with A, X, and + being a light, tone, and footshock, respectively), rats received extinction of A and the training context, extinction of the training context alone, or no extinction. The inhibitory potential of X was then assessed with conditioned lick suppression in a neutral context using both summation and retardation tests. Extinction of the training context alone and extinction of A and the training context reduced the inhibitory potential of X appreciably and equally. Hence, what is traditionally called differential inhibition appears to depend not on the excitatory value of A but on the excitatory value of the training context. In conjunction with what is known about other inhibitory training procedures, these results suggest that a conditioned inhibitor is a stimulus that has been paired with little or no reinforcement in the presence of an accompanying stimulus that predicts greater reinforcement.