Extinction of the context and latent inhibition

The hypothesis that latent inhibition could be reduced by extinguishing the experimental context, that is, exposing the rats to the context between exposure to the conditional stimulus (CS) and conditioning, was tested. All experiments used the conditioned emotional response procedure. In Experiment 1, extinction was not effective when the animals were exposed to the clicker 40 times off the baseline of responding for food and when the clicker CS was partially reinforced with shocks during the test phase. In Experiments 2 and 3, latent inhibition could be reduced by extinction if the animals were exposed to the CS 24 or 16 times on-baseline, and if continuous reinforcement was used during the test. In Experiments 4, 5, and 6, we attempted to determine which variable was responsible for the discrepant results. In Experiment 4, extinction was effective with 20 or 40 on-baseline exposures to the CS, using continuous reinforcement during the test. In Experiment 5, extinction was not effective with exposure on- or off-baseline, using 24 exposures and partial reinforcement. Finally, in Experiment 6, extinction reduced latent inhibition using continuous, but not partial, reinforcement with 40 exposures off-baseline. From these results, we concluded that Wagner's model of habituation was not sufficient to account for latent inhibition and that a hybrid model, using both associative and cognitive representational processes, was necessary.     

Competitive short-term and long-term memory processes in spatial habituation

Exposure to a spatial location leads to habituation of exploration such that, in a novelty preference test, rodents subsequently prefer exploring a novel location to the familiar location. According to Wagner's (1981) theory of memory, short-term and long-term habituation are caused by separate and sometimes opponent processes. In the present study, this dual-process account of memory was tested. Mice received a series of exposure training trials to a location before receiving a novelty preference test. The novelty preference was greater when tested after a short, rather than a long, interval. In contrast, the novelty preference was weaker when exposure training trials were separated by a short, rather than a long interval. Furthermore, it was found that long-term habituation was determined by the independent effects of the amount of exposure training and the number of exposure training trials when factors such as the intertrial interval and the cumulative intertrial interval were controlled. A final experiment demonstrated that a long-term reduction of exploration could be caused by a negative priming effect due to associations formed during exploration. These results provide evidence against a single-process account of habituation and suggest that spatial habituation is determined by both short-term, recency-based memory and long-term, incrementally strengthened memory.     

Latent inhibition and contextual associations

Attenuated responding to a conditioned stimulus (CS) after preexposure to that CS (latent inhibition) has traditionally been attributed to reductions in CS associability. Alternatively, CS-context associations formed during CS preexposure later interfere with the acquisition or expression of CS-outcome associations. Three lick suppression experiments with rats contrasted these accounts. Presumably, exposure to the context attenuates the CS-context association without altering CS associability. With a fixed amount of CS preexposure, latent inhibition decreased with increasing context exposure during or after (but not before) CS preexposure. When the ratio of context preexposure duration to CS preexposure was fixed, latent inhibition increased with CS preexposure. These results suggest that latent inhibition is a direct function of the strength of CS-context associations formed during preexposure.     

Interaction between preexposure and overshadowing: Further analysis of the extended comparator hypothesis

Three experiments with rats used conditioned suppression of barpress to test predictions of the extended comparator hypothesis, which assumes that the effectiveness of (first-order) comparator stimuli in modulating responding to a target conditioned stimulus (CS) is itself modulated by other (second-order) comparator stimuli. Experiment 1 demonstrated that both pretraining exposure to the target CS alone (i.e., CS-preexposure effect, also known as latent inhibition) and pretraining exposure to a compound of the target CS and nontarget CS (i.e., compound-CS-preexposure effect) counteract overshadowing, and that posttraining deflation (i.e., extinction) of the overshadowing stimulus attenuates responding to the target CS when overshadowing is preceded by a CS-preexposure treatment (i.e., yields a CS-preexposure effect), but not when overshadowing is preceded by a compound-CS-preexposure treatment. Experiment 2 examined the consequences of posttraining associative inflation of the overshadowing stimulus or the preexposure companion stimulus following conjoint compound-CS-preexposure and overshadowing treatment. Experiment 3 examined the consequences of posttraining inflation of the overshadowing stimulus or the context following conjoint CS-alone preexposure and overshadowing treatment. The results support the expression-focused comparator view in contrast to recent acquisition-focused models of retrospective revaluation.     

Reinstatement of latent inhibition following a reminder treatment in a conditioned taste aversion paradigm.

Reminder treatments have been shown to facilitate the retrieval of a variety of conditioned responses. Whether or not similar results would occur with an experimental paradigm which involves primarily memory for a stimulus, i.e., where no particular response is specified, is unclear. Accordingly, using Sprague-Dawley rats, we employed a latent inhibition paradigm with a long (10 days) retention interval between sucrose (CS) preexposure and sucrose-illness pairing (training). The results demonstrated a loss of latent inhibition following the 10-day retention interval suggesting "forgetting" of the CS preexposure. However, placing a single reminder exposure to the CS within the preexposure-to-training interval reinstated the preexposure effect. Controls indicated that in the absence of the initial preexposure the reminder per se did not produce latent inhibition. Thus, a reminder can reinstate a stimulus attribute (flavor representation) and explicit conditioned responses.     

Latent inhibition and stimulus generalization of the classically conditioned nictitating membrane response in rabbits (Oryctolagus cuniculus) following dorsal hippocampal ablation.

Rabbits received 0 to 450 exposures of a tone conditioned stimulus (CS) prior to classical defensive conditioning of the nicitating membrane response based on an infraorbital eye shock unconditioned stimulus. Tone preexposure resulted in retarded conditioning in normal rabbits. This latent inhibition effect was not present in animals with bilateral dorsal hippocampectomy produced by aspiration. Control animals with bilateral neocortical and callosal aspiration lesions demonstrated a latent inhibition effect similar to that shown by normal nonoperated animals. The failure of CS preexposure to retard conditioning in hippocampal rabbits was not due to differences in threshold of the conditioned response to the CS or to differences in response mechanisms as determined by tests of habituation and dishabituation of the unconditioned response. A subsequent experiment employed combined-cue summation tests to confirm the fact that preexposure did not endow the tone with conditioned as well as latent inhibitiory properties. Finally, tests of stimulus generalization along the auditory frequency dimension indicated flatter relative gradients for hippocampals than for nonoperated controls, with cortical controls in between. These findings were discussed in terms of Douglas' model of hippocampal function.     

Enhanced Latent Inhibition Following Compound Pre-exposure

The influence of non-reinforced exposure to compound stimuli on subsequent appetitive classical conditioning was examined in five experiments with rats as the subjects. Non-reinforced exposure to a visual stimulus retarded subsequent acquisition of conditioned responding relative to a non-pre-exposed condition (latent inhibition). If the target stimulus was pre-exposed in compound with a second (non-target) stimulus, then latent inhibition was abolished. Exposure to the non-target stimulus prior to compound exposure had varying effects on subsequent conditioning to the target: 40 exposures to the non-target stimulus resulted in latent inhibition to the target stimulus that was comparable in magnitude to that observed when the target stimulus was exposed in isolation; 120 exposures to the non-target stimulus enhanced latent inhibition to the target stimulus.     

Contextual Pavlovian conditioning in the crab Chasmagnathus

In contextual conditioning, a complex pattern of information is processed to associate the characteristics of a particular place with incentive or aversive reinforcements. This type of learning has been widely studied in mammals, but studies of other taxa are scarce. The context-signal memory (CSM) paradigm of the crab Chasmagnathus has been extensively used as a model of learning and memory. Although initially interpreted as habituation, some characteristics of contextual conditioning have been described. However, no anticipatory response has been detected for animals exposed to the training context. Thus, CSM could be interpreted either as an associative habituation or as contextual conditioning that occurs without a context-evoked anticipatory response. Here, we describe a training protocol developed for contextual Pavlovian conditioning (CPC). For each training trial, the context (conditioned stimulus, CS) was discretely presented and finished together with the unconditioned stimulus (US). In agreement with the CSM paradigm, a robust freezing response was acquired during the 15 training trials, and clear retention was found when tested with the US presentation after short (2 and 4 h) and long (1–4 days) delays. This CPC memory showed forward but not simultaneous presentation conditioning and was context specific and protein synthesis dependent. Additionally, a weak CPC memory was enhanced during consolidation. One day after training, CPC was extinguished by repeated CS presentation, while one presentation induced a memory labilisation–reconsolidation process. Finally, we found an anticipatory conditioned response (CR) during the CS presentation for both short-term (4 h) and long-term memory (24 h). These findings support the conditioning nature of the new paradigm.     

Additional exposures to a compound of two preexposed stimuli deepen latent inhibition

The present experiments studied the role of error correction mechanisms in the latent inhibition of conditioned fear responses by conditioned stimulus (CS) preexposure. They demonstrated that a preexposed CS subjected to additional exposures in compound with either another preexposed stimulus or a novel stimulus was more latently inhibited than a preexposed CS which received additional exposures in isolation. They also showed that a preexposed CS subjected to additional exposures in compound with another preexposed stimulus was more latently inhibited than a preexposed CS given additional exposures in compound with a novel stimulus. These results were discussed in terms of the Hall-Rodriguez (2010) model of latent inhibition.     

Music training enhances the rapid plasticity of P3a/P3b event-related brain potentials for unattended and attended target sounds

Neurocognitive studies have shown that extensive musical training enhances P3a and P3b event-related potentials for infrequent target sounds, which reflects stronger attention switching and stimulus evaluation in musicians than in nonmusicians. However, it is unknown whether the short-term plasticity of P3a and P3b responses is also enhanced in musicians. We compared the short-term plasticity of P3a and P3b responses to infrequent target sounds in musicians and nonmusicians during auditory perceptual learning tasks. Target sounds, deviating in location, pitch, and duration with three difficulty levels, were interspersed among frequently presented standard sounds in an oddball paradigm. We found that during passive exposure to sounds, musicians had habituation of the P3a, while nonmusicians showed enhancement of the P3a between blocks. Between active tasks, P3b amplitudes for duration deviants were reduced (habituated) in musicians only, and showed a more posterior scalp topography for habituation when compared to P3bs of nonmusicians. In both groups, the P3a and P3b latencies were shortened for deviating sounds. Also, musicians were better than nonmusicians at discriminating target deviants. Regardless of musical training, better discrimination was associated with higher working memory capacity. We concluded that music training enhances short-term P3a/P3b plasticity, indicating training-induced changes in attentional skills.     

Latent inhibition, context specificity, and context familiarity

In two appetitive licking experiments, thirsty rats were pre-exposed to two stimuli prior to conditioning sessions in which one or both of these stimuli were paired with water. Consistent with other results, latent inhibition was disrupted when conditioning took place in a context different from that in which stimulus pre-exposure had occurred. But in animals given prior exposure to the context of stimulus pre-exposure before the start of stimulus pre-exposure, substantial and equivalent latent inhibition was evident whether or not there was a change of context between stimulus pre-exposure and conditioning. These results are discussed in terms of current theories of latent inhibition.     

Taking a bright view of negative priming in the light of dim stimuli: further evidence for memory confusion during episodic retrieval.

A same-different letter-matching task was used to examine the effects of stimulus intensity on negative priming, which is poorer performance when target letters have been presented as distractor letters on the immediately preceding trial. In Experiment 1, stimulus intensity was manipulated between-participants, whereas in Experiment 2, it varied randomly from trial-to-trial within-participants. In Experiment 1, negative priming was equivalent for both stimulus intensities. In Experiment 2, negative priming effects were larger for repeated intensity stimuli than for nonrepeated intensity stimuli, when stimulus intensity was dim. Furthermore, for repeated intensity stimuli, negative priming effects were enhanced when the overt response required to the stimulus was repeated from prime to probe trial. These results are consistent with the hypothesis that negative priming may be due to memory confusion, rather than to inhibition of the distractor stimuli.     

Mechanisms underlying retarded emergence of conditioned responding following inhibitory training: evidence for the comparator hypothesis

The comparator hypothesis posits that conditioned responding is determined by a comparison at the time of testing between the associative strengths of the conditioned stimulus (CS) and stimuli proximal to the CS at the time of conditioning. The hypothesis treats all associations as being excitatory and treats conditioned inhibition as the behavioral consequence of a CS that is less excitatory than its comparator stimuli. Conditioned lick suppression by rats was used to differentiate four possible sources of retarded responding to an inhibitory CS. These include habituation to the unconditioned stimulus (US), latent inhibition to the CS, blocking of the CS-US association by the conditioning context, and enhanced excitatory associations to the comparator stimuli. Prior research has demonstrated the first three phenomena. Therefore, we employed parameters expected to highlight the fourth one--the comparator process. In Experiment 1, our negative contingency training was shown to produce a conditioned inhibitor that passed inhibitory summation and retardation tests. In Experiment 2 we found transfer of retardation from an inhibitory CS to a novel stimulus when the location where retardation-test training occurred was excitatory, which is indicative of contextual blocking and/or comparator effects. In Experiment 3, extinction of the conditioning context was found to attenuate retardation regardless of whether extinction occurred before or after the CS-US pairings of the retardation test. This indicates that much of the present retardation was due to the comparator process rather than to contextual blocking. Experiment 4 demonstrated that habituation to the US did not contribute to retardation in the present case. Collectively, these studies suggest that retardation following inhibitory training can be explained without recourse to any of the traditional mechanisms of conditioned inhibition.     

Attenuation of latent inhibition after compound conditioning

Using a conditioned suppression procedure with rats, three experiments examined the effects of compound conditioning on the degree of latent inhibition. Experiment 1 suggested that latent inhibition of the preexposed target was not enhanced but rather attenuated when a second stimulus was presented in compound conditioning. Experiment 2 showed that a similar result was obtained when, in subjects given only compound conditioning, the salience of the target was reduced to the level where it was overshadowed by the second stimulus. Experiment 3 proved that addition of the second stimulus only during preexposure, or during both preexposure and conditioning, did not attenuate the latent inhibition to the target. These results are difficult to explain by any model of Pavlovian conditioning which assumes that both latent inhibition and overshadowing effects are a consequence of acquisition deà cit; other possible accounts are discussed.     

Priming and trial spacing in extinction: Effects on extinction performance,spontaneous recovery,and reinstatement in appetitive conditioning

Previous research in this laboratory suggests that priming of the conditional stimulus (CS) in short-term memory may play a role in the trial-spacing effects in appetitive conditioning. For example, a nonreinforced presentation of a CS 60 s before a reinforced trial with the same CS produced slower acquisition than a CS presentation that occurred 240 s before the reinforced trial. The results were consistent with the self-generated priming mechanism proposed by Wagner (e.g., Wagner 1978, 1981). The present experiments extended the earlier work by examining the effects of trial spacing in extinction rather than acquisition. After conditioning with a mixture of intertrial intervals (ITIs), rats received extinction with ITIs of 60 or 240 s, longer or shorter values, or different ways of “chunking” extinction trials in time. Although trial spacing produced effects on extinction performance that were consistent with our previous research on acquisition, there were few long-term differences in spontaneous recovery or in reinstatement. Short ITIs in extinction appear to affect extinction performance more than they affect extinction learning. Mechanisms of trial spacing in conditioning and extinction are discussed.     

Mismatch between what is expected and what actually occurs triggers memory reconsolidation or extinction

In previous experiments on contextual memory, we proposed that the unreinforced re-exposure to the learning context (conditioned stimulus, CS) acts as a switch guiding the memory course toward reconsolidation or extinction, depending on reminder duration. This proposal implies that the system computes the total exposure time to the context, from CS onset to CS offset, and therefore, that the reminder presentation must be terminated for the switching mechanism to become operative. Here we investigated to what extent this requirement is necessary, and we explored the relation between diverse phases in the reconsolidation and extinction processes. We used the contextual memory model of the crab Chasmagnathus which involves an association between the learning context (CS) and a visual danger stimulus (unconditioned stimulus, US). Administration of cycloheximide was used to test the lability state of memory at different time points. The results show that two factors, no-reinforcement during the reminder (i.e., CS re-exposure) and CS offset are the necessary conditions for both processes to occur. Regardless of the reminder duration, memory retrieved by unreinforced CS re-exposure emerges intact and consolidated when tested before CS offset, suggesting that neither reconsolidation nor extinction is concomitant with CS re-exposure. Either process could only be triggered once the definitive mismatch between CS and US is confirmed by CS termination without the expected reinforcement.     

The influence of a distractor during compound preexposure on latent inhibition

Nonreinforced exposure to a nontarget stimulus that was followed by nonreinforced exposure to a target/nontarget simultaneous compound stimulus resulted in enhanced latent inhibition of the target. Conditioning was slower after this treatment than after nonreinforced exposure to the target stimulus alone (Experiment 1). However, a salient auditory stimulus presented immediately after the compound in the second phase reduced levels of latent inhibition, relative to the enhanced latent inhibition produced when no such extracompound stimulus was presented (Experiments 2 and 3). This effect was not noted if the salient auditory cue was presented 10 sec after the termination of the compound stimulus (Experiment 4). In Experiment 5, there was no disruption of simple latent inhibition produced by a salient stimulus. These results are consistent with enhanced latent inhibition's being produced by the formation of within-compound associations, which are disrupted by the salient extracompound stimuli.     

US habituation,like CS extinction,produces a decrement in conditioned fear responding that is NMDA dependent and subject to renewal and reinstatement

Just as fear can be learned, it can also be inhibited. The most common way of reducing learned fear is through extinction, where the conditioned stimulus (CS) previously paired with an aversive unconditioned stimulus (US) is repeatedly presented on its own. Another, much less commonly studied, way to inhibit learned fear is by habituating, or devaluing, the US. In this procedure, fear responding to a CS is reduced by repeatedly presenting the US in the absence of the CS following the conditioning phase. The purpose of the present study was to directly compare the effects of US habituation and CS extinction on a learned fear response (freezing). Experiment 1 demonstrated that US habituation given either after (Experiment 1A) or before (Experiment 1B) fear conditioning reduced freezing to the CS at test. We then showed that the reduction in freezing resulting from either US habituation or CS extinction was context-specific (i.e., a change in context led to a renewal of the learned fear response; Experiment 2) and, furthermore, was attenuated when a pre-test shock was given (i.e., reinstatement of fear was observed in both cases; Experiment 3). Finally, Experiment 4 demonstrated that an injection of the NMDA antagonist MK-801 prior to US habituation impaired long-term retention of the learning that takes place during this procedure. Together, these results suggest that the decrement in conditioned fear responses produced by US habituation and CS extinction could rely on overlapping processes.     

Long-term repetition priming with symmetrical polygons and words

In two different tasks, subjects were asked to make lexical decisions (word or nonword) and symmetry judgments (symmetrical or nonsymmetrical) about two-dimensional polygons. In both tasks, every stimulus was repeated at one of four lags (0, 1, 4, or 8 items interposed between the first and second stimulus presentations). This paradigm, known as repetition priming, revealed comparable short-term priming (Lag 0) and long-term priming (Lags 1, 4, and 8) both for symmetrical polygons and for words. A shorter term component (Lags 0 and 1) of priming was observed for nonwords, and only very short-term priming (Lag 0) was observed for nonsymmetrical polygons. These results indicate that response facilitation accruing from repeated exposure can be observed for stimuli that have no preexisting memory representations and suggest that perceptual factors contribute to repetition-priming effects.     

Trace decay and the priming of short-term memory in long-delay taste aversion learning: Disruptive effects of novel exteroceptive stimulation

A variation of Kalat and Rozin's two-presentation paradigm was used to test the hypothesis that the first, as opposed to the second, presentation of a flavor conditioned stimulus (CS) constitutes the functional CS in two-presentation experiments involving moderate interflavor intervals (IFIs), and results in flavor aversions that are a function of the primary, as opposed to the secondary, conditioned stimulus-unconditioned stimulus (CS-US) interval. Contrary to the hypothesis, it was shown in Experiment 1 that holding the primary CS-US interval constant at 4 hr for each of three groups, while decreasing the secondary CS-US interval (i.e., the interval between the second flavor presentation and the illness) from 3.75 hr to 2.5 hr to .5 hr, resulted in the flavor aversion increasing as the secondary CS-US interval decreased. However, the aversion acquired by the group with a 0.5 hr secondary CS-US interval was also found to be significantly weaker than that acquired by a single-presentation 0.5 hr control group. In Experiment 2 it was demonstrated that animals exposed to novel exteroceptive stimulation (NES) immediately prior to a second flavor presentation that preceded the US by 0.5 hr acquired an aversion as strong as that acquired by a 0.5-hr control group. In Experiment 3 it was demonstrated that, in the absence of a second flavor presentation, animals exposed to novel exteroceptive stimulation 0.5 hr prior to the US acquired a weaker flavor aversion than did animals not exposed to novel exteroceptive stimulation during the 4-hr flavor CS-illness US interval. The contrasting effects of novel exteroceptive stimulation observed in Experiments 2 and 3 were replicated in Experiment 4. The results suggest, consistent with the trace-decay hypothesis and Wagner's (1976) general model of stimulus processing, that exposure to novel exteroceptive stimulation disrupts continued processing of the short-term memory (STM) trace of the initial presentation of a flavor CS, and hence minimizes stimulus preexposure effects attributable to the priming of STM.