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.     

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.     

Effects of CS preexposure on inhibition of delay

Two experiments examined the effects of preexposure to a stimulus on the subsequent acquisition of conditioned suppression by rats. Variations in the level of suppression within conditioning trials were noted so thatinhibition of delay (taken here to mean less suppression at the beginning of a trial than at the end) could be detected. Inhibition of delay was observed both during the acquisition of suppression and (in Experiment 1) when suppression began to wane with continued postasymptotic training. Preexposure to the to-be-conditioned stimulus retarded acquisition of suppression and slowed the appearance of inhibition of delay both in acquisition and (in Experiment 1) in postasymptotic performance. Experiment 2 demonstrated that inhibition of delay was attenuated during conditioning that followed preexposure in which the stimulus was paired with a weak reinforcer. These results provide no support for the suggestion that preexposure to a stimulus retards later conditioning because it allows the subject to acquire information about stimulus duration that in turn fosters the development of inhibition of delay. Rather, they are compatible with the suggestion that preexposure causes the stimulus to lose associability.     

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.     

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.     

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.     

Circadian-temporal context and latent inhibition of conditioned taste aversion: Effect of restriction in the intake of the conditioned taste stimulus

Latent inhibition of conditioned taste aversion (CTA) is sensitive to changes in the temporal context. A change in the time of day of conditioning with respect to the time of day of the preexposure can disrupt the latent inhibition. This contextual change in the time of day may reveal a temporal specificity of latent inhibition. The optimum procedure to induce this temporal specificity is not well established. For example, it has been shown that a long period of habituation to temporal contexts is one factor that can determine the effect. However, the experimental conditions on the conditioning day that facilitate this phenomenon are unknown. The aim of this study is to elucidate whether a restriction in the intake of the conditioned taste stimulus affects the temporal specificity of latent inhibition. Two main groups of Wistar rats were tested in a latent inhibition of CTA paradigm, in which the temporal specificity of this phenomenon was analyzed by a change in the time of day of conditioning. The intake of the taste stimulus was restricted in the conditioning day in one of the groups, but this restriction was not applied in the other group. The results indicated temporal specificity of latent inhibition only in the group without restriction, but not in the group with limitation in the intake of the taste stimulus during conditioning. These findings can help to elucidate the characteristics of the procedure to induce temporal specificity of latent inhibition.     

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.     

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.     

Contextual effects in latent inhibition with an appetitive conditioning procedure

In three experiments, rats received presentations of a diffuse 30-sec stimulus (a light) and of food, and their tendency to enter the food tray was monitored. Experiment 1 showed that when the light was made to signal the delivery of food, the response of entering the food tray increased in frequency during the stimulus. The acquisition of this conditioned response to the light was retarded in subjects that had received preexposure to the stimulus. In Experiments 2 and 3, subjects received preexposure to the stimulus, some in the same context as that subsequently used for stimulus-food pairings and some in a different context. Those experiencing the change of context acquired the response more readily. It is argued that these results demonstrate a latent inhibition effect that is attenuated by contextual change.     

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.     

Effects of elements or compound preexposure on conditioned taste aversion as a function of retention interval

The effects of element or compound preexposure and retention interval were examined in three experiments with the taste-aversion paradigm. In Experiment 1, preexposure to the elements of a compound flavor produced less latent inhibition to the compound than did preexposure to the compound itself when a 1-day preexposure-conditioning interval was used. However, preexposing the elements or the compound resulted in equivalent latent inhibition effects when a 21-day retention interval was used. In Experiment 2, a similar pattern of results was observed when the conditioning-test interval was manipulated. Experiment 3 explored the effect of element or compound preexposure when preexposure and test were carried out in different contexts. Attenuated latent inhibition following preexposure to the elements was found when preexposure and test were carried out in the same context. In contrast, preexposure to the elements resulted in as much latent inhibition as did preexposure to the compound when the context was switched from preexposure to testing. The implications of these findings for a retrieval-oriented view of latent inhibition are discussed.     

Interval between preexposure and test determines the magnitude of latent inhibition: Implications for an interference account

The effect of a retention interval on latent inhibition was studied in three experiments by using rats and the conditioned taste-aversion procedure. In Experiment 1, we demonstrated an apparent loss of latent inhibition (i.e., a strengthening of the aversion) in preexposed subjects that experienced a retention interval of 12 days between conditioning and the test. In Experiment 2, we found no effect of this retention interval on the habituation of neophobia produced by the phase of exposure to the flavor. In Experiment 3, we showed that interposing a retention interval between preexposure and conditioning produced effects exactly comparable to those seen in Experiment 1. The implications of these results for rival theories of latent inhibition, as an acquisition deficit or as a case of interference at retrieval, are discussed.     

CS preexposure: Latent inhibition and Pavlovian conditioning of heart rate and eyeblink responses as a function of sex and CS intensity in rabbits

Male and female rabbits received Pavlovian conditioning in which a 1, 216-Hz tone served as the CS and a 3-mA paraorbital electric shock train served as the US. Eyeblink (EB) and heart rate (HR) CRs were assessed. Half of the animals received prior exposure to the CS, while half were restrained in the chamber for a similar length of time but did not receive prior CS exposure. Different groups of each sex received three different CS intensities including 60, 75, and 90 dB (SPL) during both preexposure and conditioning. The results revealed that latent inhibition of the EB CR occurred only at the intermediate CS intensity, as indicated by a significant impairment of EB conditioning in this group. However, the magnitude of the decelerative HR CR was attenuated by prior CS exposure at all three CS intensities. Females showed faster EB conditioning than males, but latent inhibition occurred in both sexes. These results suggest that somatomotor and autonomic systems are affected differently by prior CS exposure.     

An empirical analysis of the super-latent inhibition effect

In three conditioned taste aversion experiments, we examined the roles of several variables in producing super-latent inhibition (LI). This effect, greater LI after a long interval than after a short interval between the conditioning and the test stages (De la Casa & Lubow, 2000), was shown to increase with the number of stimulus preexposures (0, 2, or 4; Experiment 1) and with the length of the delay interval (1, 7, 14, or 21 days; Experiment 2). Furthermore, super-LI was obtained when the delay interval was introduced between the conditioning and the test stages (Experiments 1 and 2), but not when it was introduced between the preexposure and the conditioning stages (Experiment 3). The results are discussed in relation to interference explanations of LI.     

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.     

Effects of compound or element preexposure on compound flavor aversion conditioning

Two experiments with rat subjects examined conditioning of an aversion to a compound flavor stimulus after preexposing the compound, its constituent elements, or no explicit flavor stimulus. Experiment 1 used a short-term procedure in which preexposure and conditioning treatments occurred on the same day; Experiment 2 used a long-term procedure in which more extensive preexposure was administered several days before conditioning. In both experiments, preexposure of the elements slowed conditioning to the compound more than did preexposure of the compound itself. These effects were apparently not mediated by changes in pseudoconditioned or neophobic responses. The results were related to Lubow’s conditioned attention theory of stimulus preexposure effects.     

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.     

Flattening generalization gradients, context, and perceptual learning

The present research investigated the effects of physical context change and perceptual learning on generalization. In a video game, participants learned to suppress their mouse-clicking behavior in the presence of one stimulus (AX). Generalization was observed between the AX stimulus and another stimulus (BX) that was designed to be similar. When testing was conducted in a context different from that in which AX was used in training, responding to AX was attenuated, and responding to BX was enhanced. That is, the generalization gradient flattened. The latter effect was only evident in groups for which generalization had been reduced through a preexposure manipulation believed to produce perceptual learning. Experiment 2 demonstrated that the increase in generalization observed in the first experiment was due to the context change between the preexposure and test rather than to a change between the conditioning and test contexts. Implications for flattening generalization gradients and mechanisms of perceptual learning are discussed.     

Overshadowing of explicitly unpaired conditioned inhibition is disrupted by preexposure to the overshadowed inhibitor

In two conditioned lick-suppression experiments with rats, the interaction of preexposure to a target stimulus and subsequent overshadowing of conditioned inhibition treatment was examined. Blaisdell, Bristol, Gunther, and Miller (1998) have demonstrated that stimulus preexposure and overshadowing counteract each other in their effects on Pavlovian excitation, producing strong excitatory responding to the target stimulus. In the present experiments, a conditioned inhibition analogue of this effect was examined. Overshadowing of conditioned inhibition (i.e., attenuation of inhibitory control of behavior by the target stimulus) was demonstrated when a more salient stimulus was compounded with the target inhibitor during conditioned inhibition training. However, the overshadowing deficit was attenuated by preexposing the target stimulus prior to overshadowing treatment. To account for this phenomenon, we contrast the comparator hypothesis (Miller & Matzel, 1988) with contemporary models that focus on associative acquisition.