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.     

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.     

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 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.     

Conditioning of simultaneous and serial feature-positive discriminations

Three experiments with rat subjects examined the development of simultaneous and serial feature-positive discriminations in appetitive conditioning. In Experiment 1, reinforced presentations of a simultaneous light-tone compound were intermixed with nonreinforced presentations of either the light or the tone. The compound stimulus acquired conditioned behaviors of a form characteristic of the predictive feature alone; the element common to reinforced and nonreinforced trials did not evoke conditioned behavior. In Experiment 2, reinforced presentations of a serial light-trace-tone compound were intermixed with nonreinforced tone-alone presentations. The light feature stimulus acquired conditioned behaviors characteristic of visual CSs. The tone stimulus, common to reinforced and nonreinforced trials, evoked conditioned behaviors characteristic of auditory CSs, but only when preceded by the light. In Experiment 3, variations in the interval between the light and tone on reinforced trials had little effect on responding to the light CS but substantially altered the pattern of responding to the tone CS. These results suggested that simultaneous and serial feature-positive discriminations may be solved differently. Performance in simultaneous feature-positive discriminations may be determined solely by associations between the feature stimulus and the reinforcer, but performance in serial discriminations may also involve the acquisition of a conditional cue function to the feature.     

Evaluating conditioning of related and unrelated stimuli using a compound test

Three experiments used a compound test procedure to evaluate whether superior conditioning results from the pairing of stimuli that are related to each other. In each case, a stimulus compound was tested after its component conditioned stimuli (CSs) had been conditioned by the same unconditioned stimuli (USs) arranged such that either related or unrelated CSs and USs were paired. Experiment 1 explored auditory and gustatory stimuli conditioned by LiCl or shock, using rats. Experiments 2 and 3 used second-order conditioning in pigeons to pair stimuli that were similar by virtue either of qualitative features or of shared physical location. In each case, the compound test provided clear evidence that pairing related stimuli produces superior associative learning.     

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.     

Directed approach responses and positive conditioned suppression in the rat

Three experiments evaluated an alternative to accounts of positive conditioned suppression that stress central (i.e., motivational or emotional) states. This “competing-response” interpretation was tested by analyzing directed movements that develop in rats during a visual or an auditory stimulus (CS) that signals an appetitive reinforcer (US) in a situation where the subject is also emitting an instrumental response for food. In each experiment, positive conditioned suppression (i.e., a reduction in the rate of such instrumental responding during CS presentations) was accompanied by responses directed toward the CS source and/or the US-delivery site. In Experiment 1, a diffuse (auditory) CS signaled a US delivered at some specific place in the chamber and rats approached the US-delivery site during CS. In Experiments 2 and 3, the spatial proximity of a localized visual CS and US-delivery site determined whether CS-directed or US-directed behavior predominated during the CS. The results suggest that the topographies of conditioned responses on any positive conditioned suppression procedure depend upon the spatial arrangements of features that elicit and support these behaviors. They further suggest that the identification of these features and their spatial arrangements is necessary for the analysis of appetitive classical-instrumental interactions.     

Renewal of Pavlovian conditioned inhibition

Prior research has demonstrated renewal, which is the ability of contextual cues to modulate excitatory responding to a Pavlovian conditioned stimulus (CS). In the present research, conditioned lick suppression in rats was used to examine similar contextual modulation of Pavlovian conditioned inhibition. After Pavlovian conditioned inhibition training with a CS in one context, subjects were exposed to pairings of the CS with an unconditioned stimulus (US) either in the same or in a second context. Results indicated that, when the CS was paired with the US in the second context, the CS retained its inhibitory control over behavior, provided that testing occurred in the context used for inhibition training. However, when the CS-US pairings occurred in the inhibition training context, the CS subsequently proved to be excitatory regardless of where testing occurred. These observations indicate that conditioned inhibition is subject to renewal.     

Changes in inhibition during differential eyeblink conditioning with increased training

Three experiments examined inhibitory learning in rats, using Pavlovian and differential inhibitory eyeblink conditioning procedures. Experiment 1 was designed to compare summation and retardation effects following Pavlovian conditioned inhibition (A1/XA) or differential inhibition (A1/X) training using auditory and visual conditioned stimuli (CSs). After ten 100-trial sessions of training, both Pavlovian conditioned inhibition and differential inhibition produced a retardation effect. However, a summation effect was obtained only for rats given Pavlovian conditioned inhibition training. Experiment 2 showed that increasing differential inhibition training to twenty 100-trial sessions produced summation and retardation effects. In Experiment 3, rats were trained with either ten or twenty 100-trial sessions of intramodal inhibitory training with two tone CSs (2 kHz vs. 8 kHz). Summation and retardation effects were obtained after only 20 sessions of differential conditioning. The findings indicate that extensive training is needed to establish conditioned inhibition with intermodal or intramodal differential conditioning.     

Stimulus-reinforcer interactions in Pavlovian conditioning of pigeons: Implications for selective associations

In a Pavlovian procedure, groups of pigeons were presented with a compound auditory-visual stimulus that terminated with either response-independent electric shock or food. In a subsequent test, the tone CS was dominant in aversive conditioning, reliably eliciting conditioned head raising and prancing. The red light CS was dominant in appetitive conditioning, reliably eliciting pecking. This result was replicated in a second experiment, in which trials were widely spaced. Pour additional groups of pigeons received pairings of the separate element CSs with the USs. Red light, but not tone, was an effective CS in appetitive conditioning, whereas tone, but not red light, was effective in aversive conditioning. There was no discriminative responding in zero-contingency control groups. Several theoretical accounts of these data are discussed.     

Pavlovian appetitive discriminative conditioning inAplysia californica

Three experiments demonstrated Pavlovian appetitive discrimination learning in the marine mollusc,Aplysia californica. In each experiment, subjects were exposed to two conditioned stimuli; one stimulus (CS+) was paired with food presentations and the other stimulus (CS?) was never followed by food. In Experiments 1 and 3 different chemosensory stimuli were used, and in Experiment 2 different tactile stimuli were used. For both types of conditioned stimuli, bite responses occurred significantly more often to the CS+ than to the CS?. Experiment 2 also showed thatAplysia could learn a reversal of this discrimination. Experiment 3 showed that nonreinforced presentations of CS+ resulted in a decline in the frequency of conditioned biting. The implications of these results for neurobiological analyses of learning are discussed.     

Posttrial effects of presenting vs. omitting expected shock USs in the conditioned suppression procedure: Concurrent measurement of barpress suppression and freezing

Barpress suppression in a 1-min interval following CS trials was investigated using 16 rats in a conditioned suppression procedure with a two-stage design. For one group, each CS co-terminated with a brief shock US in Stage 1; then, in Stage 2, only half the CSs ended with a shock, which in turn was followed 1 min later by a second shock. For a second group, the two stages were reversed. When CSs were followed by single shocks in Stage 1, posttrial suppression weakened across trials; but when, in Stage 2, double shocks followed half the CSs, posttrial suppression grew stronger. When half the trials were followed by double shocks in Stage 1, posttrial suppression was maintained at initial levels but weakened in Stage 2 when single shocks followed each trial. In both stages, posttrial suppression was stronger on nonreinforced than on reinforced trials. Two factors were hypothesized to control posttrial suppression. First, posttrial suppression weakens with training under the single-shock procedure because post-shock temporal stimuli come to inhibit fear unless themselves paired with shock. Second, posttrial suppression is stronger on nonreinforced trials than on reinforced trials because freezing behaviors initiated during the CS are not disrupted by a US and so persist into the posttrial interval.     

Solving Pavlov's puzzle: Attentional, associative, and flexible configural mechanisms in classical conditioning

This article introduces a new "real-time" model of classical conditioning that combines attentional, associative, and "flexible" configural mechanisms. In the model, attention to both conditioned (CS) and configural (CN) stimuli are modulated by the novelty detected in the environment. Novelty increases with the unpredicted presence or absence of any CS, unconditioned stimulus (US), or context. Attention regulates the magnitude of the associations CSs and CNs form with other CSs and the US. We incorporate a flexible configural mechanism in which attention to the CN stimuli increases only after the model has unsuccessfully attempted learn input-output combinations with CS-US associations. That is, CSs become associated with the US and other CSs on fewer trials than they do CNs. Because the CSs activate the CNs through unmodifiable connections, a CS can become directly and indirectly (through the CN) associated with the US or other CSs. In order to simulate timing processes, we simply assume that a CS is formed by a temporal spectrum of short-duration CSs that are activated by the nominal CS trace. The model accurately describes 94?% of the basic properties of classical conditioning, using fixed model parameters and simulation values in all simulations.     

Cross-modal transfer as a function of similarities between training tasks in classical conditioning of the rabbit

The present experiments examined transfer of training from visual to auditory sensory modalities in classical conditioning of the rabbit’s nictitating membrane response. Experiment 1 examined transfer from initial training with a single visual CS to subsequent auditory discrimination training, and Experiment 2 examined transfer from visual discrimination training to auditory discrimination training. The major findings were that (1) initial conditioning of a visual CS facilitated the overall rate of CR acquisition to the auditory CSs separate from the requirements for discrimination learning (Experiments 1 and 2), and (2) initial visual discrimination training facilitated auditory discrimination learning (Experiment 2). Thus, the animals appeared to encode separately both contiguous CS-US relations and CS+ versus CS? relations during initial visual training. The results are discussed with respect to theories of extradimensional transfer.     

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.     

Context effects on conditioning,extinction, and reinstatement in an appetitive conditioning preparation

Three experiments with rat subjects examined the effects of contextual stimuli on performance in appetitive conditioning. A 10-sec tone conditioned stimulus (CS) was paired with a food-pellet unconditioned stimulus (US); conditioning was indexed by the observation of headjerking, a response of the rat to auditory stimuli associated with food. In Experiment 1, a context switch following initial conditioning did not affect conditioned responding to the tone; however, when the response was extinguished in the different context, a return to the original conditioning context “renewed” extinguished responding. These results were replicated in Experiments 2 and 3 after equating exposure to the two contexts (Experiment 2) and massing the conditioning and extinction trials (Experiment 3). The results of Experiment 1 also demonstrated that separate exposure to the US following extinction reinstates extinguished responding to the tone; this effect was further shown to depend at least partly on presenting the US in the context in which testing is to occur (Experiments 2 and 3). Overall, the results are consistent with previous data from aversive conditioning procedures. In either appetitive or aversive conditioning, the context may be especially important in affecting performance after extinction.     

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.     

Signaling and affective functions in Pavlovian conditioning

The present study employed a Pavlovian-instrumental-transfer paradigm to investigate the role of conditioned fear in appetitive discrimination learning. Each of three Pavlovian training procedures was used to establish a conditioned fear excitor (CS+), a “neutral” CS (CSo), and a conditioned fear inhibitor (CS?). Then, the CSs were administered to rats in the three groups contingent upon the rewarded response in a difficult visual discrimination. In addition, half of each group received shock punishment for each incorrect response. Relative to CSo, CS+ facilitated performance in contrast to the usual interfering effect of conditioned suppressors; conversely, CS? retarded performance even when its reinforcing action (fear inhibition) was potentiated by punishment for the incorrect response. These results, together with other findings showing a reversed outcome when the CSs are administered for the incorrect response, indicate that Pavlovian conditioning comprises both general signaling and affective functions, the former reflecting a basic “expectancy” or nominal type of cognitive processing in the rat.     

The CS− effect in simple conditioning and stimulus selection during development

Changes in affect toward a particular stimulus can take place very rapidly through Pavlovian conditioning, if presentation of the conditioned stimulus (CS+) paired with the unconditioned stimulus (US) is accompanied by presentation of a “CS?,” another value of the same dimension as the CS+ but not paired with a US. This effect has considerable generality. It has been observed in terms of both olfactory and visual CSs, in terms of appetitive as well as aversive conditioning, and for adult as well as infant rats. The CS? effect has seemed especially important for infants, which may be related to the general tendency for infants to exhibit less stimulus selection than older animals. Finally, the CS? effect has enabled the development of a simple test of short-term retention that can quite effectively assess memory for either incidental or target events. These tests so far have indicated a clear ontogenetic decrease in rate of forgetting over short intervals, corresponding to the well-known development-related decrease in forgetting over long intervals (infantile amnesia). The tests also have shown that short-term forgetting of intentional and target events is surprisingly similar, with some indication of more rapid forgetting for the incidental events. Alternative interpretations of the CS? effect and some preliminary tests of these interpretations are discussed.