On the generality of conditioned bradycardia in rabbits: Assessment of CS and US modality

To determine whether the magnitude of heart rate (HR) slowing induced by classical conditioning contingencies is comparable under a broad range of stimulus conditions, experiments were conducted in which rabbits were exposed to tones, increases in illumination, or vibratory stimuli as conditioned stimuli (CSs) and in which paraorbital electric shocks, corneal airpuffs, or intraoral pulses of water served as unconditioned stimuli (USs). The results indicated that conditioned bradycardia was elicited by all three CSs. Moreover, when a corneal airpuff served as the US, small but reliable CS-evoked HR decelerations also occurred. Finally, CS-evoked HR slowing also occurred in response to a tone CS employed in an appetitive task, in which water was the US. These findings suggest that HR slowing is a general phenomenon that occurs when rabbits are exposed to signals that systematically predict aversive or appetitive consequences according to a Pavlovian conditioning paradigm.     

One-trial simultaneous and backward excitatory fear conditioning in rats: Lick suppression, freezing, and rearing to CS compounds and their elements

Three experiments with rat subjects sought to enhance one-trial excitatory simultaneous and backward fear conditioning by using a two-element compound conditioned stimulus (CS) instead of only a single element. During conditioning, experimental groups received a 4-sec CS either coextensively with a 1-mA grid-shock unconditioned stimulus (US) or immediately after US termination. In subsequent tests, CSs evoked more lick suppression and freezing in these groups than in various controls. Compound CSs evoked more lick suppression and freezing than did CS elements, but did so equally for experimental and control groups. Therefore, the use of compounds did not enhance conditioning. Unexpectedly, an explicitly unpaired control in which CS followed US termination by 3 min tended to show more CS-evoked suppression and freezing than did a control in which CS preceded US onset by 3 min. This result raises the possibility that associations between the CS and the training context might engender responding to backward-paired CSs.     

Evaluating the TD model of classical conditioning

The temporal-difference (TD) algorithm from reinforcement learning provides a simple method for incrementally learning predictions of upcoming events. Applied to classical conditioning, TD models suppose that animals learn a real-time prediction of the unconditioned stimulus (US) on the basis of all available conditioned stimuli (CSs). In the TD model, similar to other error-correction models, learning is driven by prediction errors-the difference between the change in US prediction and the actual US. With the TD model, however, learning occurs continuously from moment to moment and is not artificially constrained to occur in trials. Accordingly, a key feature of any TD model is the assumption about the representation of a CS on a moment-to-moment basis. Here, we evaluate the performance of the TD model with a heretofore unexplored range of classical conditioning tasks. To do so, we consider three stimulus representations that vary in their degree of temporal generalization and evaluate how the representation influences the performance of the TD model on these conditioning tasks.     

Conditioned suppression of a positively reinforced shuttle response

Rats were trained to run up and down an alleyway for sucrose reinforcement on a variable interval schedule. Differential aversive classical conditioning with auditory CSs was then conducted in a separate apparatus (“off the baseline”) prior to those CSs being presented while the subjects were responding for sucrose in the alleyway. Once the effects of the CSs had extinguished, shock was reintroduced following one CS but not the other (“on the baseline” differential aversive classical conditioning). Both “off the baseline” and “on the baseline” conditioning resulted in conditioned suppression to the CS followed by shock, but little effect of the CS followed by no shock was found. In the “on the baseline” phase, total suppression of baseline responding occurred at moderate US intensities, and this appeared to result from the subject avoiding the location at which he was last shocked. At lower values, both baseline response rate and relative suppression ratio were functions of US intensity. The results are discussed in relation to the effects found in similar experiments using avoidance baselines.     

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.     

The erasure of reinstated fear

Three experiments investigated the reinstatement of fear to a previously conditioned and extinguished CS as a result of separate presentation of the original US. That reinstatement was found to be sharply attenuated by nonreinforcement of a second fear elicitor between presentations of the US and testing of the CS. This “erasure” of reinstatement depended upon the fear-eliciting power of the intervening stimulus and, under some circumstances, was essentially complete. Moreover, erasure reduced not only the response to the CS but also the extinction it underwent as a result of subsequent nonreinforcement. It is argued that neither the conditioning of background stimuli nor stimulus generalization among explicit CSs provides an adequate account of these reinstatement and erasure results. Rather, they are interpreted in terms of the construction and destruction of a nonassociative representation of the US during conditioning, extinction, reinstatement, and erasure. In that context, some inferences can be made about the rules governing these nonassociative changes and the ways in which they interact with modifications in associations.     

CS modality,context conditioning,and conditioned freezing

Two studies used a one-trial-a-day aversive conditioning procedure with rats as subjects to investigate the effects of a noise versus a light CS on conditioned freezing. Experiment 1 demonstrated that less conditioned freezing was elicited by the light, although the two CSs led to similar levels of freezing to the contextual cues of the conditioning chamber. Experiment 2 replicated these outcomes and showed that the manipulation of CS intensity produced results similar to those of modality, with the more intense CSs eliciting less freezing. The second experiment also determined that freezing to contextual cues resulted from context conditioning. According to the Rescorla-Wagner model, CSs that condition poorly should generate little competition with context conditioning. Since neither the modality nor intensity factor reliably influenced context conditioning, as measured by context-evoked freezing, the studies provide no support for the view that the effects on CS-evoked freezing represent differences in the strength of conditioning to the various stimuli. This finding raises the possibility that all of the CSs conditioned well but varied in their abilities to elicit freezing because they differed in terms of the form of defensive behavior under their control.     

Temporal integration in second-order conditioning and sensory preconditioning

Lick suppression experiments with rats revealed that the magnitude of both second-order conditioning (Experiment 1) and sensory preconditioning (Experiment 2) was superior when that conditioning was based on backward (US→CS) relative to forward (CS→US) first-order pairings of a CS and US. The superiority of backward relative to forward first-order conditioning on suppression to the higher order cues can be understood by assuming that the magnitude of higher order conditioning was determined by a memory representation of the higher order cues that provided information about the expected temporal location of the US. The results suggest that temporal information such as order between paired CSs and USs was encoded, preserved, and integrated with memory for the higher order stimuli. The relevance of these findings to memory integration in Pavlovian learning, the temporal coding hypothesis (Barnet, Arnold, & Miller, 1991; Matzel, Held, & Miller, 1988), backward excitatory conditioning, and the associative structure that underlies second-order Pavlovian fear conditioning are discussed.     

Brain mechanisms for changes in processing of conditioned stimuli in Pavlovian conditioning: Implications for behavior theory

This article is a review of the results of a series of experiments designed to identify brain systems involved in appetitive conditioning of rats. It discusses some of their implications for behavioral theories of learning, especially those that concern changes in processing of conditioned stimuli (CSs). Evidence is presented which suggests that separable brain circuits are involved in (1) the production of CS-dependent conditioned orienting responses, (2) the enhancement of CS associability produced when expectancies about upcoming events are violated, (3) the reduction of CS associability produced when stimuli are consistent predictors of other events or are presented without consequence, and (4) the abilities of CSs to serve as reinforcers for second-order conditioning and to be sensitive to postconditioning changes in the value of the unconditioned stimulus (US). Finally, none of these circuits seems critical for normal acquisition of the most common indicator of Pavlovian conditioning, US-dependent conditioned responses (CRs). Although the independence of brain pathways does not demand independence of behavioral function, clustering of behavioral phenomena on anatomical grounds may provide useful guides for constructing behavior theories.     

Overshadowing and associability change: Examining the contribution of differential stimulus exposure

In two appetitive conditioning experiments with rats, we investigated the mechanisms responsible for demonstrations of the superior associability of overshadowed conditioned stimuli (CSs) relative to control CSs. In Experiment 1, we investigated whether previous demonstrations were a consequence of differences in the relationship between the CSs and the unconditioned stimulus (US) or of differences in the conditions of exposure to the CSs. Rats received trials with X, Y, and an AB compound, but no delivery of the US (X–, Y–, AB–). A subsequent AY–, AX+, BY + test discrimination revealed that the AY/BY component of the discrimination was solved more readily than the AY/AX component—suggesting the contribution of an exposure effect. In Experiment 2, we better equated the conditions of exposure between A and Y by using AB+, XY+, X– training in Stage 1. In Stage 2, instrumental responses were rewarded during an AY compound. A final test revealed that Y took better control of instrumental responding than did A. The results of these experiments are discussed in terms of classical and contemporary theories of learning and attention.     

Secondary extinction in Pavlovian fear conditioning

Pavlov (1927/1960) reported that following the conditioning of several stimuli, extinction of one conditioned stimulus (CS) attenuated responding to others that had not undergone direct extinction. However, this secondary extinction effect has not been widely replicated in the contemporary literature. In three conditioned suppression experiments with rats, we further explored the phenomenon. In Experiment 1, we asked whether secondary extinction is more likely to occur with target CSs that have themselves undergone some prior extinction. A robust secondary extinction effect was obtained with a nonextinguished target CS. Experiment 2 showed that extinction of one CS was sufficient to reduce renewal of a second CS when it was tested in a neutral (nonextinction) context. In Experiment 3, secondary extinction was observed in groups that initially received intermixed conditioning trials with the target and nontarget CSs, but not in groups that received conditioning of the two CSs in separate sessions. The results are consistent with the hypothesis that CSs must be associated with a common temporal context during conditioning for secondary extinction to occur.     

Trial spacing effects in pavlovian conditioning: A role for local context

Two conditioned lick-suppression experiments with rats were conducted in order to replicate and extend findings by Ewing, Larew, and Wagner (1985). Ewing et al. observed that excitatory responding to a CS paired with a footshock US was attenuated when the ITIs thatpreceded each CS-US trial were short (60 sec) relative to when they were long (600 sec). This effect was isolated in the influence of the preceding ITI because the preceding ITI was consistently short for one CS and consistently long for a different CS, while the following ITIs were equally often short and long for both CSs. Ewing et al. interpreted this finding in the framework of Wagner’s (1981) SOP model. Experiment 1 replicated this trial-spacing effect and demonstrated a similar effect under conditions in which thefollowing ITI was consistently short for one CS and consistently long for a different CS, while the durations of preceding ITIs were equally often short and long for both CSs. Experiment 2 revealed that the detrimental effect of a short preceding or a short following ITI could be alleviated by extinguishing the conditioning context after CS-US training. The latter observation indicates that the trial-spacing effect is not mediated by a failure of a CS trained with a short ITI to enter into excitatory associations with the US, a conclusion that is not wholly consistent with the SOP model. Finally, we suggest that short pretrial and short posttrial ITIs may enhance the excitatory value of local context cues that modulate responding to a CS.     

Outcome-specific conditioned inhibition in Pavlovian backward conditioning

In the present experiments, the outcome specificity of learning was explored in an appetitive Pavlovian backward conditioning procedure with rats. The rats initially were administered Pavlovian backward training with two qualitatively different unconditioned stimulus conditioned-stimulus (US-CS) pairs of stimuli (e.g., pellet --> noise or sucrose --> light), and then the effects of this training were assessed in Pavlovian-to-instrumental transfer (Experiment 1) and retardation-of-learning (Experiment 2) tests. In the transfer test, it was shown that during the last 10-sec interval, the CSs selectively reduced the rate of the instrumental responses with which they shared a US, relative to the instrumental responses with which they did not share a US. The opposite result was obtained when the USs (in the absence of the CSs) were presented noncontingently. In the retardation test, conditioned magazine approach, responding to the CSs was acquired more slowly when the stimulus-outcome combinations in the backward and the forward conditioning phases were the same, as compared with when they were reversed. These results are collectively in accord with the view that Pavlovian backward conditioning can result in the formation of outcome-specific inhibitory associations. Alternative views of backward conditioning are also examined.     

Temporal encoding in trace conditioning

Conditioned lick suppression in rats was used to explore the role of timing in trace conditioning. In Experiment 1, two groups of rats were exposed to pairings of a CS (CS1) with a US, under conditions in which the interstimulus interval (ISI) that separated CS1 offset and US onset was either 0 or 5 sec. Two additional groups were also exposed to the same CS1→US pairings with either a 0 or a 5-sec ISI, and then received “backward” second-order conditioning in which CS1 was immediately followed by a novel CS2 (i.e., CS1→CS2). A trace conditioning deficit was observed in that the CS1 conditioned with the 5-sec gap supported less excitatory responding than the CS1 conditioned with the 0-sec gap. However, CS2 elicited more conditioned responding in the group trained with the 5-sec CS1-US gap than in the group trained with the 0-sec CS1-US gap. Thus, the CS1-US interval had inverse effects on first- and second-order conditioned responding. Experiment 2 was conducted as a sensory preconditioning analogue to Experiment 1. In Experiment 2, rats received the CS1?CS2 pairings prior to the CS1→US pairings (in which CS1 was again conditioned with either a 0 or a 5-sec ISI). Experiment 2 showed a dissociation between first- and second-order conditioned responding similar to that observed in Experiment 1. These outcomes are not compatible with the view that differences in responding to CSs conditioned with different ISIs are mediated exclusively by differences in associative value. The results are discussed in the framework of the temporal coding hypothesis, according to which temporal relationships between events are encoded in elementary associations.     

Blocking and enhancement of fear conditioning by appetitive CSs

Prior research on Pavlovian-to-instrumental transfer has shown that when a CS previously associated with shock (AvCS+) is presented contingent upon a choice response to a discriminative stimulus for food reinforcement, it facilitates discrimination learning. Conversely, a response-contingent CS previously associated with the absence of shock (AvCS?) retards discrimination learning. To evaluate whether these findings reflect across-reinforcement blocking and enhancement effects, two experiments investigated the effects of appetitively conditioned stimuli on fear conditioning to a novel stimulus that was serially compounded with the appetitive CS during conditioned-emotional-response (CER) training. Although there were no differential effects of the appetitive CSs in CER acquisition, Experiment 1, using a relatively weak shock US, showed that a CS previously associated with food (ApCS+) retarded CER extinction to the novel stimulus, in evidence of enhanced fear conditioning to that stimulus. In addition, Experiment 2, using a stronger shock US, showed that a CS previously associated with the absence of food (ApCS?) facilitated CER extinction to the novel stimulus, in evidence of weaker fear conditioning to that stimulus. These results parallel traditional blocking effects and indicate not only that an ApCS+ and an ApCS? are functionally similar to AvCSs of opposite sign, but that their functional similarity is mediated by common central emotional states.     

A contingency analysis of taste aversion conditioning

The acquisition of conditioned taste aversion was assessed relative to five control procedures. That is, forward conditioning using multiple-trial, brief-duration taste CSs and weak USs over a 30-min CS-US delay was compared to backward, CS alone, US alone, sham CS and sham US, and random control procedures. The outcome supported an associative conditioning interpretation of the learned aversion. While there were no differences between the various control procedures, all were different from the forward conditioning group. The argument was made that some of the distinctive associative and nonassociative phenomena attributed to taste aversion conditioning (but not seen in the present study) may in part be due to the duration and intensity of both the CS and US events.     

Sudden,rapid acquisition of conditioned suppression (CER)

Trial-by-trial acquisition of the CER was measured in a number of groups with different CSs. Analysis of the acquisition curves for individual animals revealed that, for the majority of animals, CS-US associations developed in a stepwise rather than a gradual fashion. In some cases, with the most effective CS, conditioning occurred with one CS-US pairing.     

US inflation with trace and simultaneous fear conditioning

Two experiments with rat subjects in a conditioned punishment paradigm are reported. These experiments attempted to determine if the events entering into association with the CS following conditioning with informative (forward) and noninformative (simultaneous) CSs were comparable. In Experiment 1, exposure to intense shock alone following trace (ISI = 10 sec) conditioning with moderate shock enhanced the suppressive effects of a 2-sec CS. A similar manipulation following explicitly unpaired CS-US presentations (ISI = 2 min) had no effect. These data were taken as evidence that the CS and US were associated during trace conditioning. Experiment 2 showed that exposure to intense shock following simultaneous conditioning also enhanced suppression to the CS. These results suggested that simultaneous and forward conditioning procedures yield similar forms of associative learning.     

CS-duration and partial-reinforcement effects counteract overshadowing in select situations

Two experiments used rats in a conditioned lick suppression preparation to investigate how the conditioned stimulus (CS)-duration and partial-reinforcement effects (i.e., weakened responding due to conditioning with a CS of longer duration and presenting nonreinforced CSs intermingled with CS—unconditioned stimulus [US] pairings, respectively) interact with overshadowing. Experiment 1 found that when overshadowing treatment was combined with either extended CS duration or partial reinforcement, the response deficit was weaker than when either of these three treatments was administered alone. In Experiment 2, the generality of the findings in Experiment 1 was investigated by replicating it with various US—US intervals. This time counteraction was observed only when both the absolute duration of total CS exposure and the US—US interval were short. The results support neither the view that the ratio between the total CS exposure and total time in the context determines the CS-duration and the partial-reinforcement effects nor the view that these two effects arise from a loss of effectiveness of the excitatory CS—US association during CS-alone exposures in partial reinforcement or early periods of CS exposure with long CSs.     

Pre-exposure enhances recovery of conditioned responding after extinction

Four experiments used a within-subjects design with rats to study the effects of preexposure on the restoration of fear responses (freezing) to an extinguished conditioned stimulus (CS). In each experiment, rats were preexposed to one CS (A), but not to another (B), and then were exposed to pairings of each of these CSs with an aversive unconditioned stimulus (US). In each experiment, there was less freezing to A than to B across extinction, showing a latent inhibitory effect of preexposure. There was no differential recovery to A and B following either a US reexposure (Experiment 1) or a delay interval (Experiment 2). However, when a delay interval included US reexposure, there was greater recovery to the preexposed CS, A, than to the nonpreexposed CS, B (Experiments 1, 3, and 4). These results suggest that the effects of US reexposure and delay combine to affect recovery from the depressive effects of CS-alone exposure. The results are consistent with the view that US reexposure produces better mediated conditioning of CSs that are strongly associated with the context. The results may additionally reflect an effect of preexposure on the learning produced by extinction.