Extinction of enhanced latent inhibition

Hungry rats were used in a classical conditioning procedure in which visual stimuli were paired with food. Conditions in which nonreinforced exposure to a nontarget stimulus was followed by exposure to a simultaneous compound nontarget/target stimulus (a blocking procedure) resulted in enhanced latent inhibition to the target relative to exposure to the nontarget, followed by exposure to the target stimulus alone. A third phase of nonreinforced exposure training, in which the target was exposed alone following the compound, reduced levels of latent inhibition relative to results obtained with the blocking procedure. Experiments also suggested that this was not the result of restoration of associability by the omission of an expected presentation of the nontarget stimulus in the final preexposure phase. These results suggest that enhanced latent inhibition is due to summation of a direct-target-no-event association and a second-order association of these elements via target-nontarget and nontarget-no-event association. Exposure to the target after compound exposure extinguished the target-nontarget association and reduced the sources of no-event learning for the target.     

Stimulus preexposure speeds or slows subsequent acquisition of associative learning depending on learning test procedures and response measure

Prior exposure to a conditioned stimulus (CS) typically results in latent inhibition—slower acquisition of associative learning about that stimulus in subsequent training. Here, we found that CS preexposure had different effects on the appetitive conditioning of rats with a sucrose unconditioned stimulus (US) depending on training test procedures, the similarity of preexposure and training procedures, and the choice of response measure. Preexposure to a visual or an auditory stimulus produced facilitation of acquisition of food-cup-directed responding when both of those cues were (separately) paired with sucrose delivery in the training test (Experiments 1 and 3). By contrast, the same preexposure procedure resulted in latent inhibition of food-cup learning if the second stimulus in the test phase was of the same modality as the preexposed stimulus (Experiment 2). In Experiment 3, latent inhibition was enhanced if both phases included a single CS or both phases included both auditory and visual CSs, compared to treatments in which only one CS was presented in one phase but two CSs were presented in the other phase. In Experiment 4, preexposure of an auditory cue slowed subsequent learning about it if the context was salient but enhanced learning if the context was of weaker salience. Finally, a measure of general activity revealed latent inhibition after preexposure in all conditions in all 4 experiments. We discuss the results within several classes of latent inhibition theories, none of which provides a comprehensive account.     

The effects of compound stimulus preexposure of two elements differing in salience on the acquisition of conditioned suppression

Conditioned attention theory (CAT) of latent inhibition (LI) states that parallel learning processes occur during reinforced and nonreinforced stimulus presentation. The present experiments investigated the effects of nonreinforced preexposure of either a compound CS or elements of that compound which differed in salience. Three predictions were advanced: (1) Both the compound and its elements will show an increase in LI as a function of the number of preexposures; (2) the two elements will show different levels of LI, with more LI accruing to the more salient element; (3) overshadowing will occur during compound preexposure. Two experiments, using rats as subjects and a conditioned suppression test, are reported. In Experiment 1, groups received 0, 20, 40, or 80 nonreinforced preexposures to a compound whose elements differed in salience. The results of the subsequent test confirmed predictions 1 and 2. Experiment 2, in which groups were preexposed to either the elements or the compound, provided evidence for an overshadowing effect, confirming prediction 3 from CAT.     

Stimulus generalization decrement in latent inhibition to a compound following exposure to the elements or the compound

In two experiments using the taste-aversion paradigm, we attempted to replicate a result reported by Holland and Forbes (1980), in which exposure to the elements of a compound produced more interference with future conditioning (latent inhibition) to the compound than did exposure to the compound itself. In our first experiment, a compound of HC1 and sucrose was used and the amount of fluid consumed during exposure and the first conditioning trial was controlled. Rather than finding enhanced interference produced by exposure to the elements, we found reduced interference relative to exposure to the compound. In Experiment 2, a compound of NaCl and sucrose was used and a method similar to that used by Holland and Forbes was employed. We replicated the result of our Experiment 1. We interpret these results as posing problems for some associative accounts of latent inhibition but as being easily explained as an instance of stimulus generalization decrement.     

The effect of nonreinforced stimulus exposure on the strength of a conditioned taste aversion as a function of retention interval: Do latent inhibition and extinction involve a shared process?

Two experiments examined the effects of nonreinforced flavor exposure on the strength of a conditioned taste aversion. Rats were conditioned by pairing maple flavor with LiC1. Prior to or subsequent to this pairing, some animals received nonreinforced exposure to either maple or saccharin. In separate subjects, preference for maple was tested 1 or 21 days after the last training episode. In the first experiment, the nonreinforced stimulus exposure occurred before conditioning (latent inhibition, or LI, procedure); in the second experiment, the nonreinforced exposure occurred after conditioning (extinction, or EXT, training). In both experiments, nonreinforced exposure to maple or saccharin reduced the magnitude of a conditioned maple aversion when testing occurred soon after conditioning. When testing was delayed, however, the attenuation due to nonreinforced saccharin exposure dissipated, both with the LI procedure and with EXT. In contrast, the nonreinforced exposure to maple was found to attenuate conditioned reactions at both short and long retention intervals. The release from generalized LI and spontaneous recovery following generalized EXT training are discussed in terms of retrieval processing. The possibility that the same mechanism may underlie LI and EXT is considered.     

Savings test for associations between neutral stimuli

Three experiments showed a savings procedure to be an effective and sensitive alternative to sensory preconditioning procedures as a measure of associations among neutral stimuli. Experiment 1 showed that within-compound associations developed more rapidly in reinforced appetitive serial compound conditioning when nonreinforced preexposure to the serial compound was given than when separate element or no preexposure was given. Experiment 2 showed the savings effect to be highly stimulus specific. Experiment 3 examined the facilitation of serial compound conditioning after either simultaneous or serial nonreinforced preexposure to the elements of the compound. The results of that experiment were consistent with those of analogous sensory preconditioning experiments. When preexposure involved only the two elements of the subsequently reinforced compound, serial preexposure produced more savings than simultaneous preexposure. But when preexposure involved a three-stimulus procedure like that used by Rescorla (1980b), simultaneous preexposure resulted in more savings. Advantages of the savings procedure over sensory preconditioning as a measure of association among neutral stimuli 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.     

Release from latent inhibition with delayed testing

A conditioned emotional response procedure was used to study the interactive effects of stimulus preexposure and retention interval in rats. In Experiment 1, the subjects were conditioned by presenting a light CS paired with mild footshock as the US. Half of the subjects were given nonreinforced preexposure to the CS, and the others were not. Separate preexposed and nonpreexposed groups were then tested 1,7, or 21 days after conditioning. Suppression of ongoing activity was used to assess the degree of conditioned fear. Latent inhibition was found at the 1-day retention interval; the preexposed subjects displayed less conditioned fear than did the nonpreexposed subjects. In contrast, equally strong conditioned fear was expressed by the preexposed and the nonpreexposed groups tested after the 7- and the 21-day retention intervals. These results indicate a release from latent inhibition similar to that obtained with conditioned taste aversions (Kraemer & Roberts, 1984). The results of Experiment 2 suggest that retention-interval-induced increases in sensitization, pseudoconditioning, or neophobia cannot account for the release from latent inhibition effect obtained in Experiment 1. The implications of these findings for a retrievaloriented view of latent inhibition are discussed.     

Some determinants of second-order conditioning

In a Pavlovian conditioning situation, an initially neutral stimulus may be made excitatory by nonreinforced presentations in compound with an established conditioned excitor [i.e., second-order conditioning (SOC)]. The established excitor may be either a punctate cue or the training context. In four conditioned suppression experiments using rats, we investigated whether SOC phenomena parallel other cue interaction effects. In Experiment 1, we found that the response potential of a target stimulus was directly related to the intertrial interval when SOC was mediated by a punctate cue, and inversely related to the intertrial interval when SOC was mediated by the training context. Experiment 2 demonstrated that punctate- and context-mediated SOC are oppositely affected by posttraining context extinction, and Experiments 3 and 4 demonstrated that context- and punctate-mediated SOC are differentially affected by conditioned stimulus (Experiment 3) and unconditioned stimulus (Experiment 4) preexposure treatments. These findings parallel phenomena in conditioned inhibition and cue competition situations.     

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.     

Latent habituation of the orienting response in the preweanling rat

The effect of inhibiting the orienting response on information processing was examined in four experiments. A nonsignal auditory stimulus was presented four times to preweanhng rats either 30 sec or 15 min after they had been placed in an unfamiliar environment (Experiments 1A and 2), shocked (Experiment 1B)5 or experienced a shift in environmental context (Experiment 1C). Both an autonomic (heart rate) and a behavioral componentx of the orienting response to the novel stimulus were recorded. In the 15-min condition, the auditory stimulus elicited a consistent orienting response on the first trial that habituated rapidly with successive trials. In contrast, the auditory stimulus did not elicit a detectable orienting response in the 30-sec condition on any of the four trials. However, when the auditory stimulus was re-presented after a brief retention interval, a comparable level of habituation was seen in both groups. These results demonstrate that animals in the 30-sec condition detected, attended to, and encoded the auditory stimulus even though they did not orient, either autonomically or behaviorally, to that stimulus when it was first presented. This process of response-independent habituation is best described as latent habituation. Like latent learning, latent habituation took place in the absence of any observable change in behavior. The implications of this effect for current theories of habituation and of the orienting response are discussed.     

Reward devaluation disrupts latent inhibition in fear conditioning

Three experiments explored the link between reward shifts and latent inhibition (LI). Using consummatory procedures, rewards were either downshifted from 32% to 4% sucrose (Experiments 1–2), or upshifted from 4% to 32% sucrose (Experiment 3). In both cases, appropriate unshifted controls were also included. LI was implemented in terms of fear conditioning involving a single tone-shock pairing after extensive tone-only preexposure. Nonpreexposed controls were also included. Experiment 1 demonstrated a typical LI effect (i.e., disruption of fear conditioning after preexposure to the tone) in animals previously exposed only to 4% sucrose. However, the LI effect was eliminated by preexposure to a 32%-to-4% sucrose devaluation. Experiment 2 replicated this effect when the LI protocol was administered immediately after the reward devaluation event. However, LI was restored when preexposure was administered after a 60-min retention interval. Finally, Experiment 3 showed that a reward upshift did not affect LI. These results point to a significant role of negative emotion related to reward devaluation in the enhancement of stimulus processing despite extensive nonreinforced preexposure experience.     

Effect of extended training on generalization of latent inhibition: an instance of perceptual learning

Four experiments examined generalization of latent inhibition (LI) as a function of the length of preexposure in a conditioned taste aversion procedure with rats. Experiment 1 showed that one or four nonreinforced presentations of a flavor compound (BX) retarded subsequent conditioning to another compound (AX). However, after eight presentations of BX, conditioning to AX occurred at the same rate as with no preexposure. These results indicate that generalization of LI decreased as the length of preexposure to BX increased. Experiment 2 replicated this effect of reducing generalization, as well as demonstrating that LI actually increased as the length of preexposure to AX increased. Experiment 3 extended the generality of the effect to a procedure in which both BX and AX were preexposed. Experiment 4 demonstrated a similar reducing-generalization effect when generalization of LI from BX to X was assessed. All of these data are consistent with the notion that prolonged preexposure to BX enhances its discriminability. Different learning mechanisms that might be responsible for this perceptual learning effect are discussed.     

Target-absent controls in blocking experiments with rats

In three between-groups blocking experiments with rats, two concurrent and one forward, several common control procedures were employed: Reinforced trials with the putative blocking stimulus were either omitted entirely (Kamin control), replaced by unsignaled reinforcements (Wagner control), or replaced by reinforced trials with a different stimulus (C1 control). In each experiment, parallel treatments with the target stimulus absent during training served to examine the possibility that differential responding in tests with the target stimulus might be traced solely to differential exposure to the nontarget stimuli. In Experiment 1, responding by a concurrent blocking group during the test was no different than responding by a Kamin control group, and responding by a Wagner control group was greater than that of either of the other groups—a pattern of results, mirrored in the performance of the target-absent groups, that could be attributed to the elevation of contextual excitation by unsignaled reinforcement. In Experiment 2, responding in the test by a concurrent blocking group was no different than that by a C1 control group. In Experiment 3, a finding of less responding by a forward blocking group than by a C1 control group when the target stimulus was present during training, but not when it was absent, provided plausible evidence of blocking.     

Latent inhibition in honeybees

Aversive conditioning was studied in individual honeybees flying back and forth between the hive and the sill of an open laboratory window, where they took sucrose solution from a target so constructed that shock could be delivered while the proboscis was in contact with the solution. During feeding, a conditioned stimulus—substrate vibration or airstream—was paired with brief shock avoidable by interruption of feeding. In Experiment 1, unreinforced preexposure of the conditioned stimulus was found to retard acquisition (latent inhibition). In Experiment 2, which was designed to inquire into the stimulus specificity of the effect, differential conditioning was found to be impaired by unreinforced preexposure of the positive stimulus and facilitated by unreinforced preexposure of the negative stimulus. In Experiment 3, a summation experiment designed to test various alternative explanations of the effect, a preexposed stimulus was found to suppress response to an excitatory conditioned stimulus when the two stimuli were presented together.     

Conditioned avoidance responses survive contingency degradation in the garden slug,Lehmannia valentiana

Joint presentations of a conditioned stimulus (CS) and an unconditioned stimulus (US) strengthen the contingency between them, whereas presentations of one stimulus without the other degrade this contingency. For example, the CS can be presented without the US either before conditioning (CS–no US and then CS–US; latent inhibition) or after conditioning (CS–US and then CS–no US; extinction). In vertebrate subjects and several invertebrate species, a time lapse usually results in a return of the conditioned response, or spontaneous recovery. However, in land mollusks, spontaneous recovery from extinction has only recently been reported, and response recovery after latent inhibition has not been reported. In two experiments, using conditioned aversion to a food odor as a measure of learning and memory retention, we observed contingency degradation via latent inhibition (Experiment 1) and extinction (Experiment 2) in the common garden slug, Lehmannia valentiana. In both situations, the contingency degradation procedure successfully attenuated conditioned responding, and delaying testing by several days resulted in recovery of the conditioned response. This suggests that the CS–US association survived the degradation manipulation and was retained over an interval of several days.     

Positive and negative patterning after CS preexposure in flavor aversion conditioning

Three experiments examined rats’ ability to discriminate a compound conditioned stimulus (CS) from the individual elements of that compound in a flavor aversion conditioning paradigm. In Experiment 1, presentations of a compound of sucrose and saline solutions were followed by lithium chloride injections, but presentations of those elements individually were nonrein-forced (positive patterning). Conversely, in Experiments 2 and 3, presentations of the individual elements were followed by lithium chloride injection, but compound presentations were non-reinforced (negative patterning). The discriminations were acquired in all three experiments. In addition, all three experiments investigated the effects of preexposure of the discriminative stimuli on subsequent acquisition of the patterned discriminations. In positive patterning, preexposure had no measurable effect on the acquisition of responding (suppression) to the reinforced compound stimulus, but slowed the loss of suppression to the nonreinforced elements. In negative patterning, preexposure slowed the acquisition of suppression to the reinforced elements but had little effect on the loss of suppression to the nonreinforced compound.     

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.     

Intrinsic reinforcing properties of putatively neutral stimuli in an instrumental two-lever discrimination task

Four experiments examined the influence of a stimulus presented after one response in a two-lever choice task. In Experiment 1, food-deprived rats trained on a concurrent variable-interval extinction schedule responded more often on the extinction lever when such responding periodically produced a visual stimulus than when it did not. In Experiments 2 and 3, a similar signal-induced enhancement effect was found even when food was delivered randomly with respect to responding on both levers or when no food was presented. In Experiment 4, a response-contingent visual stimulus elevated responding to the lever on which it was presented, but an auditory cue suppressed responding. These findings indicate that visual stimuli may possess intrinsically reinforcing properties for rats.     

Massive preexposure and preexposure in multiple contexts attenuate the context specificity of latent inhibition

Latent inhibition, which refers to attenuated responding to a conditioned stimulus (CS) after CS-unconditioned stimulus (CS-US) pairings as a result of CS-alone presentations prior to the pairings, is often attenuated if preexposure and conditioning occur in different contexts (i.e., it is context specific). Here we report two conditioned lick suppression experiments, using rat subjects, that examined whether manipulations known to attenuate the context specificity of extinction could also eliminate the context specificity of latent inhibition. Context specificity of latent inhibition was eliminated when the CS was preexposed in multiple contexts (Experiment 1) and when the CS was massively pre-exposed in the training context alone (Experiment 2). These results and their practical implications are discussed in the framework of contemporary theories of latent inhibition.