One-trial context fear conditioning as a function of the interstimulus interval

In two experiments, we examined the effects of a wide range of interstimulus intervals (2.5, 15, 45, 120, 135, and 405 sec) on one-trial context fear conditioning with rats. Here, the interstimulus interval (ISI) denotes the time between placement in a conditioning chamber and the onset of a single footshock. On the conditioning day, we observed that the rats’ behavior at the time of shock onset varied systematically across ISI values. On the subsequent test day, we used context-evoked freezing as a measure of context conditioning and found the well-known inverted U-shaped ISI function. We also found that conditioned freezing for the shortest ISI values was concentrated early in the test session, whereas freezing at longer ISIs was distributed more evenly throughout the test session. The freezing results found here are more consistent with the literature on conditioning with punctate cues than are previously described results from one-trial context fear-conditioning procedures.     

Associative properties of a conditioned inhibitor as a function of age in kittens

The efficacy of conditioned inhibition in a novel conditioned stimulus/conditioned inhibitor (CS/CI) compound was tested in 6-, 10-, and 14-week-old kittens. The conditioned response was suppression of respiration elicited by a 5.1-sec CS paired with a brief, mild footshock. During original inhibitory training, a CI was presented 2 sec after the onset of the CS, and the stimuli coterminated 3 sec later without the shock. As previously reported, the CI trained in this paradigm is more potent in older kittens but passes a summation test in all age groups (Dess & Soltysik, 1989). In the transfer test, the order of the CS and CI was reversed, so that the CI preceded the CS with no stimulus overlap. Transfer of inhibition to this new compound was virtually absent in the 6-week-old kittens and nearly perfect in the 14-week-old kittens. The CI alone (before CS onset) elicited a strong fear response in the youngest kittens, moderate fear in the 10-week-old group, and very little fear in the oldest group. The transferability of inhibitory training to a different temporal configuration of the CS and CI is absent at 6 weeks of age and fully developed 8 weeks later.     

Pavlovian conditioning in multiple contexts: Competition between contexts for comparator status

Water-deprived rats were used to investigate the effects of training a CS in more than one context on conditioned lick suppression. In each experiment, partial reinforcement of the CS was intermingled with unsignaled presentations of the US. In Experiment 1, subjects were either trained in one context alone, trained consecutively in two contexts (such that all training in one context occurred prior to any training in the second context), or trained alternately in two contexts. Following training, the first context, the second context, or neither context was extinguished. Testing of the CS occurred in a third (neutral) context. To the extent that either training context became established as a comparator stimulus for the CS, the comparator hypothesis (Miller & Matzel, 1988) predicts an increase in excitatory responding to the CS following extinction of that context. Subjects trained in a single context exhibited appreciable fear of the CS only when the CS’s training context had been extinguished. Additionally, subjects trained consecutively in the two contexts showed increased fear of the CS following extinction of the second, but not the first training context (i.e., a recency effect). Subjects trained alternately in the two contexts showed no increased fear of the CS as a result of either context alone being extinguished. In Experiment 2, subjects trained alternately in two contexts showed increased fear of the CS only when both training contexts were extinguished, suggesting that both training contexts had become comparator stimuli. These data indicate that multiple training contexts can either compete or act synergistic-ally in modulating responding to a Pavlovian trained CS as a function of the order of training in the different contexts.     

Food as a contextual cue in counterconditioning experiments: Is there a counterconditioning process?

In three experiments, counterconditioning was found to reduce fear less effectively than extinction. In Experiments 1 and 2, the resistance to extinction of avoidance was greater if food was given during extinction of fear to the CS than if no food was given, even when exposure to the CS and numbers of food and no food confinement trials were equated. It is suggested that these results could be attributed to contextual control of fear extinction by the food cue and/or to frustration produced by removing food for the counterconditioning group. Experiment 3 also found counterconditioning to be less effective than extinction and provided evidence that this difference occurs because of contextual control of fear extinction by the food cue. Measuring conditioned suppression of licking, in a test with no food present, less fear was shown if no food had been present during fear extinction, and greater fear was shown if no food had been present during fear conditioning. These results indicate that food is an important part of the context controlling fear and fear extinction. It is suggested that there may be no unique counterconditioning process. Rather, when counterconditioning procedures are employed, rules governing interference paradigms in general may apply. Thus, in a test for fear following counterconditioning, fear will be shown to the extent the test situation is similar to that in which fear conditioning occurred rather than that in which fear reduction occurred.     

Slow extinction of conditioned responding following exposure to two bouts of massed shock

Extinction of rats’ conditioned defensive freezing responses in a context associated with two bouts of massed shock (3 sec) separated by a long unreinforced interbout interval was slower than that in a context associated with distributed shock (60 sec). Resistance to extinction following two bouts of massed shock depended on the rats’ remaining undisturbed in the conditioning context during the long unreinforced interbout interval. Slow extinction of freezing was attributed to either the summation of temporal conditioning at the early and late session times or the formation of an association between the early and late bouts of shock. Importantly, the effects of the two bouts of massed shock could not be explained by what is known about the reinforcing effectiveness of massed shock.     

Overshadowing of situational cues with variable but not fixed intertrial intervals

In two experiments, we examined the conditions under which signaling an unconditioned stimulus (US) with a nominal conditioned stimulus (CS) interferes with the conditioning of situational cues in defensive freezing in the rat. Subjects received footshock USs that were (1) either signaled or unsignaled and (2) either varied or fixed in their temporal location within the conditioning session. Experiment 1, with only one trial per session, yielded no evidence that signaling affected pretrial freezing using either a fixed or variable interval between placement in the context and shock onset. In a test in which no CSs or footshocks were presented, groups that previously had received footshock at a fixed temporal location showed greatest freezing at around that same time. For groups that had received footshocks at various times, freezing declined across the test session. Experiment 2 showed overshadowing of pretrial freezing after more extensive conditioning with many trials per session, but only if the intershock intervals were variable rather than fixed.     

One-trial excitatory backward conditioning as assessed by conditioned suppression of licking in rats: Concurrent observations of lick suppression and defensive behaviors

Twenty-eight male albino rats were given a single 4-sec 1-mA electric-grid-shock unconditioned stimulus (US). In the same session they received two 12-sec conditioned stimuli (CSs). One CS (explicitly unpaired) terminated 180 sec before the US began; the other (backward paired) began immediately after the US terminated. The CSs used were a 1000-Hz 85-dB tone and an 84-dB click; their roles were counterbalanced. Over the next 2 days, each CS was presented for 2 min while the rats drank from a water bottle. The backward-paired CS was found to suppress licking more than the explicitly unpaired CS. This suppression was accompanied by an increase in defensive behavior (freezing and freeze/nod) and by a decrease in other activity. The suppression did not seem to be due to a maintained or enhanced CS-orienting response reflex, nor could it be attributed to an adventitiously reinforced interfering operant. The results support the presumption made in previous reports that the lick suppression evoked by a backward CS reflected one-trial backward excitatory fear conditioning.     

Inhibition of delay of the two-way avoidance response and warning-signal salience

Effects of extended training (nine sessions, 50 trials each) on two-way avoidance response latencies were studied. For each rat, auditory and visual warning signals (CS) were presented on separate trials, either according to a Gellermann series or in 25-trial blocks. Intermittent presentation of the two kinds of trials yielded shorter latencies and higher levels of avoidance performance in response to the noise CS than in response to the darkness CS. Presentation of trials in blocks revealed stronger response-eliciting properties of stimuli presented during the second half of the session than of those presented during the first half. A significant decrease of avoidance performance in the early portions of the delay period, an index of inhibition of delay, was obtained on auditory trials presented in the second half of the sessions. Results indicate that strong fear of the warning signal is required for inhibition of delay of avoidance responses.     

Integration of cardiac responses to serial stimuli after Pavlovian conditioning in rats

The expression of cardiac responses to sequences of two sounds was studied in restrained rats following discriminative trace or delay conditioning. Stimuli paired with a tail shock 10 sec later (CS1) elicited conditioned bradycardia. Unpaired or neutral stimuli (CS0) elicited mostly tachycardia. Rats did not learn to suppress responding to nonreinforced sequences with an interval of 6 sec between sounds. Responses to the second stimulus were significantly augmented following a CS1 stimulus, but not following a CS0 stimulus. Real-time summation of simple responses provided a more complete and quantitative prediction of dual responses than did resetting or facilitation. These results extend the time range over which summation may be observed from less than 2 sec to at least 16 sec. They appear to be inconsistent with models involving competition between unitary representations of stimuli in short-term memory and suggest the existence of multiple stimulus traces with independent time courses.     

Pavlovian conditioning to contexts that precede the place where shock occurs as measured by freezing and activity suppression in mice

Three experiments were conducted to demonstrate that the place where an organism has been, before the organism is moved to a place with aversive consequences, can also become aversive through classical conditioning. In Experiment 1, two groups of 8 mice were exposed to three different contexts in succession, with a single shock occurring in the third context. The distal context was a putative 3-min conditioned stimulus (CS) for freezing; the second context was a delay manipulation; and the unconditioned stimulus (US) occurred in the proximal context. The group delayed for 15 sec showed significantly more freezing to the distal CS context than did the group delayed for 3 h. In a second experiment, conditioning to the distal context was demonstrated with a discrimination procedure for 8 more mice by using two different distal contexts as CS+ and CS? for the proximal context with shock. On CS+ days, 3 min of exposure to the distal context was followed within 5 sec by placement in the proximal box where shock occurred, whereas on CS? days, exposure to a second distal context was followed immediately by return to the home cage. Very strong differences in freezing between the CS+ and CS? distal contexts were found in all 8 mice after 14 days of conditioning. In a third experiment, the discriminative procedure was repeated for 9 more mice, with two changes. More objective stabilometertype activity measures were substituted for observed freezing, and, in addition to the CS+ and CS? distal context trials, each mouse was also exposed to a third discriminative distal context, which was followed by 15 min in a delay chamber followed by shock in the proximal context. This discrimination procedure with the activity suppression measure again resulted in significant differences between the contexts. The CS+ context and the context followed by a 15-min delay did not differ, but both of them differed from the CS? context.     

Analysis of a trial-spacing effect with relatively long intertrial intervals

In three experiments with rat subjects, we examined the effects of trial spacing in appetitive conditioning. Previous research in this preparation suggests that self-generated priming of the conditional stimulus (CS) and/or unconditional stimulus (US) in short-term memory is a cause of the trial-spacing effect that occurs with intertrial intervals (ITIs) of less than 240 sec. Experiment 1 nonetheless showed that a trial-spacing effect still occurs when ITIs are increased beyond 240 sec, and that the effect of ITI over 60–1,920 sec on conditioned responding is best described as a linear function. In Experiment 2, some subjects were removed from the context during the ITIs, preventing extinction of the context. Removal abolished the advantage of the long ITI, suggesting the importance of exposure to the context during the long ITI. Experiment 3 still produced a trial-spacing effect in a within-subjects design that controlled for the level of context conditioning and reinforcement rate in the absence of the CS. Overall, the results are most consistent with the idea that adding time to the ITI above 240 sec facilitates conditioning by extinguishing context-CS associations—and possibly context-US associations—that otherwise interfere with CS-US learning through retrieval-generated priming (see, e.g., Wagner, 1981).     

Local context and the comparator hypothesis

“Comparator” accounts of associative conditioning (e.g., Gibbon & Balsam, 1981; Miller & Matzel, 1988) suggest that performance to a Pavlovian CS is determined, by a comparison of the US expectancy of the CS with the US expectancy of general background cues. Recent research indicates that variation in the excitatory value of cues in the local temporal context of a CS may have a profound impact on conditioned responding to the CS (e.g., Kaplan & Hearst, 1982), implicating US expectancy based on local, rather than overall, background cues as the critical comparator term for a CS. In two experiments, an excitatory training context attenuated responding to a target CS. In Experiment 1, the context was made excitatory by interspersing unsignaled USs with target CS-US trials. In this case, posttraining extinction of the conditioning context restored responding to the target CS. In Experiment 2, the target CS’s local context was made excitatory by the placement of excitatory “cover” stimuli in the immediate temporal proximity of each target CS-US trial. In this experiment, posttraining extinction of the proximal cover stimuli, not extinction of the conditioning context alone, restored responding to the target CS. An observation from both experiments was that signaling the otherwise unsignaled USs did not appear to influence the associative value of the conditioning context. The results are discussed in relation to a local context version of the comparator hypothesis and serve to emphasize the importance of local context cues in the modulation of acquired behavior. Taken together with other recent reports (e.g., Cooper, Aronson, Balsam, & Gibbon, 1990; Schachtman & Reilly, 1987), the present observations encourage contemporary comparator theories to reevaluate which aspects of the conditioning situation comprise the CS’s comparator term.     

Second-order conditioning: Different outcomes in fear and eyelid conditioning

Second-order conditioning has been frequently observed with the fear response but not with the eyelid response. The present experiments manipulated the temporal relationship between the second-order and first-order stimulus on second-order conditioning trials. Our results indicated that a trace second-order procedure is not effective with either response system. Second-order fear conditioning was most prominent when the second-order CS terminated at the onset of the first-order CS. This arrangement, however, did not produce second-order eyelid CRs. In eyelid conditioning, the second-order CS appears to inhibit responding to the first-order CS which immediately follows it.     

Effects of context exposure during conditioning on conditioned taste aversions

Rats were used in a conditioned taste aversion procedure in order to examine the effects of context exposure duration during the conditioning sessions on conditioned responding. One flavor was paired with lithium chloride during a long session in one context, whereas another flavor was conditioned during a short session in another context. Testing occurred in the home cage. The results showed that conditioning during short sessions produced strong conditioned taste aversions. Conditioning during long sessions produced strong conditioned taste aversions when the conditioned-stimulus-unconditionedstimulus (CS-US) pairing occurred at the end of the lengthy session. Other results showed that context-US associations were formed during the short duration sessions and that these associations supported conditioned responding to the CS trained in that context. The results are discussed with respect to the different influences that contextual cues can exert on conditioned responding.     

Latent inhibition as a performance deficit resulting from CS—context associations

Treatments that attenuate latent inhibition (LI) were examined using conditioned suppression in rats. In Experiment 1, retarded conditioned responding was produced by nonreinforced exposure to the CS prior to the CS-US pairings used to assess retardation (i.e., conventional LI). In Experiment la, retarded conditioned responding was induced by preexposure to pairings of the CS and a weak US prior to retardation-test pairings of the CS with a strong US (i.e., Hall-Pearce [1979] LI). Both types of LI were attenuated by extensive exposure to the training context (i.e., context extinction) following the CS-US pairings of the retardation test. Experiment 2 examined the specificity of the attenuated LI effect observed in Experiment 1. After preexposure to two different CSs in two different contexts, each CS was paired with a US in its respective preexposure context. One of the two contexts was then extinguished. This attenuated LI to a greater degree for the CS that had been trained in the extinguished context. Experiment 3 differentiated the roles in LI of CS-context associations and context-US associations. Following preexposure to the CS in the training context, LI was reduced by further exposure to the CS outside the training context. This observation was interpreted as implicating the CS-context association as a factor in LI. Thus, the results of these experiments suggest that LI is a performance deficit mediated by unusually strong CS-context associations. Implications for Wagner’s (1981) SOP model and Miller and Matzel’s (1988) comparator hypothesis are discussed.     

Preweanling and adult rats treat conditioned light-tone combinations differently

Ontogenetic differences in processing light-tone compounds were discovered in preweanling (17-day-old) and adult (60–80-day-old) rats. Suppression of general activity was used as an index of the magnitude of conditioned fear following a single training session in which a CS+ was paired with mild footshock. In Experiment 1, rats were trained on discriminations in which the CS? consisted of a light and the CS+ was either a tone alone (simple discrimination) or a light-tone compound (simultaneous feature-positive discrimination). Adults and preweanlings given each type of discrimination were then tested for fear of the CS? and a target stimulus (tone alone or light-tone compound). Adults in all groups displayed greater fear of the target than of the CS?. Preweanlings, however, discriminated the CS? from the target only when the target was the same as the original CS+. Experiment 2 revealed that age-related differences in conventional stimulus generalization is not a likely explanation for the pattern of results found in Experiment 1. Experiment 3 revealed age-related differences in expressed fear of a serial feature-positive discrimination; adults, but not preweanlings, showed greater fear of the compound than of the CS?. Alternative interpretations of the results from these experiments are discussed, and the general conclusion is that adults appear more inclined to process elements of a compound stimulus selectively, whereas preweanlings seem more likely to process the compound unselectively, with roughly equivalent processing of each element.     

Fear of the CS and of the context in two-way avoidance learning: Between- and within-subjects manipulations

The roles of CS fear and of context fear in signaled two-way avoidance learning were examined in two experiments in which shock intensity was manipulated either between or within subjects. For each subject, two discrete CSs, a light and a white noise, were used. For between-subjects comparisons, both CSs were paired with the same shock intensity, weak or strong. Under this condition, in which fear of the CSs and the context was greater with strong than with weak shock, avoidance performance varied inversely with shock intensity. For within-subjects comparisons, the light was paired with strong shock and the white noise with weak shock, or vice versa. In this case, context fear was constant during presentation of each CS, and avoidance performance varied directly with shock intensity. Additionally, intertrial responding was directly related to the amount of context fear. These results support effective reinforcement theory, an extension of two-factor theory, which acknowledges the contribution to avoidance learning both of CS fear and of context fear. The interchangeable effectiveness of visual and auditory stimuli as CSs is discussed with regard to stimulus specificity in avoidance learning.     

Spacing extinction trials alleviates renewal and spontaneous recovery

Studies of extinction in classical conditioning situations can reveal techniques that maximize the effectiveness of exposure-based behavior therapies. In three experiments, we investigated the effect of varying the intertrial interval during an extinction treatment in a fear-conditioning preparation with rats as subjects. In Experiment 1, we found less fear at test (i.e., more effective extinction) when extinction trials were widely spaced, relative to intermediate or massed extinction trials. In Experiment 2, we used an ABA renewal procedure and observed that spaced trials attenuated renewal of conditioned fear relative to massed trials. In Experiment 3, we used a similar design, but instead of changing the physical context at the time of testing, we interposed a retention interval after the extinction treatment to produce a change in the temporal context. The results showed less spontaneous recovery of fear after spaced than after massed extinction trials. These results suggest that extinction is more enduring when the extinction trials are spaced rather than massed. Although the benefits of spacing trials are small when there is no contextual change from extinction to testing, a change in either physical or temporal context following massed extinction trials leads to a recovery from extinction, which is reduced when the trials are spaced.     

Cross-modality transfer effects in conditioning-enhanced neophobia in chicks (Gallus domesticus): Evidence for the separability of novelty from specific stimulus characteristics

In this study, we investigated the separability of novelty from specific stimulus characteristics (e.g., color or taste quality) in the transfer of aversion effects. Ninety-six chicks (Gallus domesticus) received a novel visual (red water) or taste (3.0% vinegar) CS paired with an injection of lithium chloride or saline. The chicks were then tested for aversion to the CS or for conditioning-enhanced neophobia in response to a different novel visual cue (green water) or taste cue (1.0% saline). Aversions to the CSs were reliable and similar to each other. Reliable evidence of conditioning-enhanced neophobia occurred with respect to each test stimulus, irrespective of the type of CS, but conditioning with the vinegar CS produced reliably greater enhancement of neophobia than did conditioning with red water. For each CS, postconditioning neophobia was more persistent in testing with saline than with green water. The results for postconditioning neophobia suggested that novelty is a general stimulus property that is separable from specific stimulus characteristics.     

The role of temporal variables in inhibition produced through extinction

In two experiments with rats as subjects, the temporal characteristics of inhibition produced through extinction were investigated. Each experiment established two independent signals for unconditioned stimulus presentation, one trace and one delay. Following initial training, either the trace or the delay conditioned stimulus (CS) was massively extinguished. In Experiment 1, a summation test established that an extinguished delay CS (but not a neutral CS) passed a summation test with a delay, but not with a trace, transfer excitor, and an extinguished trace CS (but not a neutral CS) passed a summation test with a trace, but not with a delay, transfer excitor. In Experiment 2, a retardation test showed retarded behavioral control by an extinguished delay CS when the CS was retrained as a delay CS, but not as a trace CS, and by an extinguished trace CS when the CS was retrained as a trace CS, but not as a delay CS. The results are discussed in terms of contemporary theories of extinction.