Inhibitory associations between neutral stimuli in flavor-aversion conditioning

In Experiments 1 and 2, rats were exposed to two compound flavors, AX and BX, containing one flavor in common (X). Following this exposure phase, an aversion was conditioned to A in the experimental group by pairing its consumption with an injection of lithium, while a control group drank A without being poisoned. The effect of this treatment was to establish B as a conditioned inhibitor. In Experiment 1, experimental animals were slower than controls to condition an aversion to B when its consumption was paired with lithium (a retardation test of conditioned inhibition). In Experiment 2, B alleviated the suppression of intake of another flavor previously paired with lithium (a summation test). Experiments 3 and 4 established that these effects depended upon prolonged prior exposure to AX and BX.     

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.     

Deactivation and reactivation of the inhibitory power of a conditioned inhibitor: Testing the predictions of an attentional-associative model

An attentional-associative model (Schmajuk, Lam, & Gray Journal of Experimental Psychology: Animal Behavior Processes, 22, 321–349, 1996) assumes that nonreinforced presentations of an inhibitory conditioned stimulus (CS) do not decrease its inhibitory associations. However, the model predicts that extended presentations will decrease attention to the inhibitor, thereby decreasing both (1) the expression of its inhibitory power in a summation test and (2) the rate of acquisition in a retardation test. The model also predicts that subsequent presentations of the inhibitory CS with a novel CS will increase both (1) and (2). Using a predictive learning design in humans, Experiment 1 examined the predictions involving the summation tests, whereas Experiments 2 and 3 examined the predictions involving the retardation tests. Experimental results were in agreement with the predictions of the model.     

Summation and overexpectation with qualitatively different outcomes

In five experiments, a Pavlovian appetitive conditioning preparation was used with rats to explore the interaction of associations with different, but equivalently valued, outcomes. Experiment 1 demonstrated summation in magazine responding when two stimuli previously associated with different outcomes were combined. Experiments 2A and 2B found that pairing that stimulus compound with one of the outcomes led to a decrease in performance (overexpectation) for both of the stimulus elements. Experiments 3A and 3B confirmed that result but demonstrated the continued presence of the original stimulus-outcome associations. The results are consonant with a view in which replacing one outcome with another leads to an associative structure containing both stimulus-outcome associations and an outcome-independent depressive process.     

Summation: Assessment of a configural theory

In five experiments, rats were given Pavlovian pairings of auditory and visual stimuli with delivery of food pellets. Experiment 1 found greater responding to an AB compound after training with the individual A and B stimuli, compared with responding both to the A and B elements and to a separately trained CD compound. Experiment 2 found this enhanced responding to depend on the associative strengths of A and B. In Experiment 3, responding was greater to a CD compound than to the other compounds after an AB-, AD+, BC+ training procedure. In Experiment 4, responding to an AB compound was greater than that to the elements after A was reinforced on a 100% schedule and B on a 50% schedule. In Experiment 5, responding to an AC compound was greater than that to either A or C after an AB+, CD+, A-training procedure. A configural theory, such as that proposed by Pearce (1987), anticipates summation in none of these procedures, unless the conditioned context is assumed to have a salience greater than zero. In order to predict summation in Experiments 3, 4, and 5, a context salience greater than that of the elements must be assumed. However, such an assumption also anticipates that extinction of a 100% stimulus should eliminate responding to a 50% stimulus. The results of Experiment 3 contradicted that prediction. These results conform better to the expectations of elemental models of conditioning.     

Conditioned inhibition of analgesia

Stimuli that predict the occurrence of aversive events come to elicit conditioned analgesia. Experiments 1A and 1B examined the possibility that conditioning can inhibit analgesia when stimuli are paired in a backward fashion with a shock US (Pavlovian CS- s). Analgesia conditioned in response to shock context exposure was reversed during the CS- (light) presentation after four sessions. The ability of the CS- to function as a conditioned inhibitor of analgesia was then evaluated in both summation (Experiment 1A) and retardation-of-acquisition testing (Experiments 1A and 1B). The results support the conclusion that a stimulus presented after shock in a backward fashion comes to be a conditioned inhibitor of analgesia. Experiments 2A and 2B examined the assumption that the results obtained with our pain sensitivity measure (tailflicking in response to radiant heat) reflect changes in responsiveness to painful input, rather than a general motor inhibition or general insensitivity to sensory input. In Experiment 2A, tailflick responding to painful and nonpainful input was compared in animals receiving either morphine or saline. In Experiment 2B, tailflick responding to painful and nonpainful input to the tail was compared in both the shock and a neutral context. In both experiments, only the painful input yielded changes in responsivity. The results support the conclusion that the alterations in pain sensitivity produced by the CS- for shock represents a conditioned inhibition specific to pain.     

Posttraining flavor exposure in hungry rats after simultaneous conditioning with a nutrient converts the CS into a conditioned inhibitor

The present study investigated the decrement in nutrient-based conditioned flavor preference found in hungry rats exposed to a flavor following simultaneous flavor–sucrose conditioning while thirsty. Although a significant decrease in preference was found in the experimental group in each experiment, there was no evidence of either spontaneous recovery (Experiment 1) or reinstatement (Experiment 2). In addition, posttraining flavor exposure weakened the original flavor–sucrose association (Experiment 3). These results suggested that the flavor–US association might have been impaired after posttraining flavor exposure. Two further experiments assessed whether the flavor acquired the properties of a net inhibitor, using the retardation and summation tests for conditioned inhibition. Experiment 4 revealed that the flavor suffered retardation when retraining was conducted after the exposure phase. In Experiment 5, the target flavor decreased the preference shown for a different flavor previously paired simultaneously with sucrose when both were presented forming an unreinforced compound in the summation tests. None of these effects was found in a control group, which had received serial flavor → nutrient presentations during training. Together, these results suggest that a flavor simultaneously paired with sucrose acquires the properties of a net inhibitor when it is subsequently presented outside the compound to hungry animals.     

Associative learning phenomena in the snail (Helix aspersa): conditioned inhibition

Two experiments using garden snails (Helix aspersa) showed conditioned inhibition using both retardation and summation tests. Conditioned inhibition is a procedure by which a stimulus becomes a predictor of the absence of a relevant event—the unconditioned stimulus (US). Typically, conditioned inhibition consists of pairings between an initially neutral conditioned stimulus, CS₂, and an effective excitatory conditioned stimulus, CS₁, in the absence of the US. Retardation and summation tests are required in order to confirm that CS₂ has acquired inhibitory properties. Conditioned inhibition has previously been found in invertebrates; however, these demonstrations did not use the retardation and summation tests required for an unambiguous demonstration of inhibition, allowing for alternative explanations. The implications of our results for the fields of comparative cognition and invertebrate physiological models of learning are discussed.     

Impact of brief or extended extinction of a taste aversion on inhibitory associations: Evidence from summation,retardation, and preference tests

In five conditioned taste aversion experiments with rats, summation, retardation, and preference tests were used to assess the effects of extinguishing a conditioned saccharin aversion for three or nine trials. In Experiment 1, a summation test showed that saccharin aversion extinguished over nine trials reduced the aversion to a merely conditioned flavor (vinegar), whereas three saccharin extinction trials did not subsequently influence the vinegar aversion. Experiment 2 clarified that result, with unpaired controls equated on flavor exposure prior to testing; the results with those controls suggested that the flavor extinguished for nine trials produced generalization decrement during testing. In Experiment 3, the saccharin aversion reconditioned slowly after nine extinction trials, but not after three. Those results suggested the development of latent inhibition after more than three extinction trials. Preference tests comparing saccharin consumption with a concurrently available fluid (water in Experiment 4, saline in Experiment 5) showed that the preference for saccharin was greater after nine extinction trials than after three. However, saccharin preference after nine extinction trials was not greater, as compared with that for either latent inhibition controls (Experiments 4 and 5) or a control given equated exposures to saccharin and trained to drink saline at a high rate prior to testing (Experiment 5). Concerns about whether conditioned inhibition has been demonstrated in any flavor aversion procedure are discussed. Our findings help explain both successes and failures in demonstrating postextinction conditioned response recovery effects reported in the conditioned taste aversion literature, and they can be explained using a memory interference account.     

Acquisition and extinction of facilitation in the C57BL/6J mouse

Acquisition, extinction, and transfer of facilitation were explored in a series of experiments with C57BL/6J mice. With a procedure in which an auditory target was followed by food only in the presence of a visual facilitator, Experiments 1—4 showed that the facilitator promoted magazine entries to the auditory target. This enhancement effect was eliminated by training the facilitator as a conditioned inhibitor (Experiments 1 and 3B). Enhancement was also reduced by nonreinforced presentations of the facilitator in a discrimination procedure (Experiment 1) and by simple nonreinforcement of the facilitator (Experiments 2, 3A, and 4). In contrast to the results obtained with a facilitator, simple nonreinforcement of an inhibitor, a visual cue that had signaled when an auditory target would not be reinforced, did not reduce its ability to modulate responding to that target (Experiment 4). However, both the facilitator and the inhibitor were found to transfer their modulatory effects to other targets (Experiment 4). Finally, mice demonstrated no evidence of differential responding on a biconditional discrimination procedure in which one auditory target (A1) was reinforced in the presence of one visual stimulus (L1) but not in the presence of another (L2), and a different auditory target (A2) was reinforced in L2 but not in L1 (Experiment 5). The implications of these results for analysis of the function of a facilitator are discussed.     

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.     

Superlatent inhibition and spontaneous recovery: Differential effects of pre- and postconditioning CS-alone presentations after long delays in different contexts

In two pairs of three-stage conditioned taste aversion experiments, we examined the effects of delay interval (1 or 21 days) between the second and third stages, and of context in which the animals spent the delay (same as or different from the context of the other stages) on latent inhibition (LI) and spontaneous recovery following extinction. In the LI experiments (Experiments 1A and 1B), the first stage comprised nonreinforced presentations to saccharin or to water. In the second stage, rats were conditioned by saccharin paired with LiCl. In the extinction experiments (Experiments 2A and 2B), the order of the stages was reversed. For all experiments, Stage 3, the test stage, consisted of three presentations of saccharin alone. There was a super-LI effect in the saccharin-preexposed group that spent the 21- day delay in the different context (Experiment 1A). When the delay was spent in the same context, there was no difference in the amount of LI between the short- and long-delay groups (Experiment 1B). Conversely, there was a spontaneous recovery effect in the long-delay/same-context group (Experiment 2B), but not in the long-delay/different-context group (Experiment 2A). The pattern of results, incompatible with current explanations of delay-induced changes in memory performance, was interpreted in terms of an interaction between the delay conditions (same or different delay context), which modulate the extinction of previously acquired context-CS-nothing associations (during CS-alone presentations), and primacy effects.     

Extinction context as a conditioned inhibitor

Two lick suppression experiments using rats were conducted to determine whether extinction of a punctate excitor in a particular context would result in that context becoming a conditioned inhibitor, as defined by passing both summation and retardation tests. The role of extinction trial spacing was investigated as a possible determinant of whether the extinction context would become inhibitory. Experiment 1 demonstrated that, although inhibition was evident using either massed or spaced extinction trials, spaced trials reduced measurable inhibition as assessed by the summation test, but trial spacing had no influence on retardation test performance. Experiment 2 confirmed Experiment 1’s conclusions while controlling for the influence of latent inhibition on the retardation test. In Experiment 2, the context proved inhibitory only following massed extinction trials. These data suggest that, at least with select parameters, an extinction context can become inhibitory.     

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.     

Short-term memory for visual and auditory stimuli in pigeons

Separate groups of pigeons were trained to perform symbolic delayed matching to sample with auditory and visual sample stimuli. For animals in the auditory group, ambient tones that varied in frequency served as sample stimuli; for animals in the visual group, ambient red and green lights served as sample stimuli. In both cases, the sample stimuli were mapped onto the yellow and blue comparison stimuli presented on left and right pecking keys. In Experiments 1 and 2, it was found that visual and auditory delayed matching were affected in the same ways by several temporal variables: delay, length of exposure to the sample stimulus, and intertrial interval. In Experiments 3, 4A, and 4B, a houselight presented during the delay interval strongly interfered with retention in both visual and auditory groups, but white noise presented during the delay had little effect in either group. These results seem to be more in line with a prospective memory model, in which visual and auditory sample stimuli are coded into the same instructional memories, than with a model based on concepts of retrospective memory and modality specificity.     

An associative analysis of instrumental biconditional discrimination learning

Three different techniques were employed to analyze the associative structures mediating performance on an instrumental biconditional discrimination. In all three experiments, rats were trained concurrently on two tasks in which different stimuli signaled which one of two responses would be followed by reward. In each task, one response was rewarded in one stimulus and the other response was rewarded in the other stimulus. Correct responses earned pellets in one task and sucrose in the other task. The transfer procedure was used in Experiment 1A to identify whether or not an association developed between a biconditional discriminative stimulus and its instrumental outcome. Evidence was obtained that a biconditional cue elevated preferentially a new response trained with the same outcome. Experiments 1B and 3 examined the potential contribution of this stimulus-outcome association to biconditional performance by training the biconditional cues as signals (S-s) for the nonreinforcement of a different response. There was no evidence that this operation interfered with the ability of a biconditional cue to control performance of its correct response. In Experiments 1B and 2, the value of the instrumental outcome was reduced in an attempt to assess the contribution of stimulus-response associations to performance on the biconditional discrimination. The results of Experiments 1B and 2 reveal that correct responses were depressed following devaluation of the outcome used to train them, suggesting that learning about the response-outcome relation occurs. The implications of these results for binary and hierarchical models of instrumental learning are discussed.     

Trial number and compound stimuli temporal relationship as joint determinants of second-order conditioning and conditioned inhibition

Two conditioned lick suppression experiments with rats used feature-negative training (A-footshock trials intermixed with nonreinforced XA presentations) to analyze the role of the number of XA compound presentations and the temporal relationship of the elements within the compound (simultaneous or serial) as determinants of the resulting behavioral control. Second-order conditioning (i.e., excitatory behavioral control by X) was observed to decline as the number of XA compound trials was increased. This decline was more rapid if X and A were presented simultaneously, as opposed to serially (i.e., X before A; Experiment 1). Conditioned inhibition to X, as assessed by a summation test (Experiment 1) and a retardation test (Experiment 2), increased with the number of XA trials and did so more quickly for simultaneous than for serial pairings of X and A. The results help to clarify previously discrepant findings regarding factors that promote excitation versus inhibition with this protocol.     

Effects of postconditioning inflation on odor + taste compound conditioning

The within-compound association approach has been proposed as an account of synergistic conditioning in flavor aversion learning. One prediction from the within-compound association approach is that following taste + odor compound conditioning, postconditioning inflation of one element of the compound should increase responding to the second element. In four experiments with rats, the AX+/A+ design was used to determine whether postconditioning inflation of A would increase responding to X. In Experiments 1 and 3, responding to X was significantly stronger after AX+/A+ conditioning, as compared with AX+ conditioning. In Experiments 2 and 4, the specificity of the inflation effect was demonstrated, because AX+/A+ conditioning produced a stronger aversion to X than did AX+/B+ conditioning. Furthermore, it appears that the taste + odor association is symmetrical because inflation of the taste aversion increased responding to the odor (Experiments 1 and 2) and inflation of the odor aversion increased responding to the taste (Experiments 3 and 4).     

Conditioning of tentacle lowering in the snail (Helix aspersa): Acquisition, latent inhibition, overshadowing, second-order conditioning, and sensory preconditioning

In a series of related experiments, we studied associative phenomena in snails (Helix aspersa), using the conditioning procedure of tentacle lowering. Experiments 1A and 1B demonstrated a basic conditioning effect in which the pairing of an odor (apple) as the conditioned stimulus (CS) with the opportunity to feed on carrot as the unconditioned stimulus (US) made snails exhibit increased levels of tentacle lowering in the presence of the CS. Experiments 2 and 3 showed that the magnitude of the conditioning was reduced when snails were exposed to the CS prior to the conditioning trial (a latent inhibition effect). Experiment 4 examined the effects produced by pairing a compound CS (apple—pear) with food presentations and demonstrated the existence of an overshadowing effect between the two odors. Experiment 5 revealed that pairing one CS with another previously conditioned stimulus increased tentacle lowering to the new CS (a second-order conditioning effect). Finally, Experiment 6 showed that pairing two odors prior to conditioning of one of them promoted an increase in tentacle lowering in response to the other (a sensory preconditioning effect). The results are discussed in terms of an associative analysis of conditioning and its implications for the study of cognition in invertebrates.     

Conditioned inhibitory effects of discriminated Pavlovian training with food in rats depend on interactions of search modes, related repertoires, and response measures

Like other accounts of conditioned inhibition, behavior systems predicts (and Experiment 1 shows) that during summation and retardation tests, presentation of a negative conditioned stimulus (a CS−) created by discriminative Pavlovian food conditioning will interfere with a focal search response, such as nosing in the feeder. Unlike most other views, behavior systems predicts (and Experiment 2 shows) that the same CS− can potentiate a general search response, like attending to a moving artificial prey stimulus. Contacting the prey stimulus in extinction increased over baseline when a CS- but not a CS Novel preceded it. Experiment 3 showed this effect was not due to unconditioned qualities of the CS−. It appears that the effects of a discriminative CS-depend on the interaction of the training contingency with search modes related to the unconditioned stimulus (US), their perceptual-motor repertoires and environmental support, and the choice of response measure.