Is the context specificity of latent inhibition a sufficient explanation of learned irrelevance?

In three experiments, rats were pre-exposed either to uncorrelated presentations of a light and sucrose pellets (group CS/US) or to equivalent presentations of the light and pellets in separate sessions (control). In Experiment 1, subsequent conditioning to the light proceeded more slowly in group CS/US than in the control group, whether this conditioning was excitatory, with the light signalling the delivery of pellets, or inhibitory, with the light signalling their absence. Bonardi and Hall (1996) have argued that this learned irrelevance effect may be reducible to latent inhibition, which would be stronger in group CS/US because they are both pre-exposed and conditioned to the CS in the presence of traces of previous USs occurring in the same session. This analysis implies that group CS/US should have conditioned more rapidly to the CS than controls on the first trial of each session in Experiment 1, but this did not happen. It also implies that the learned irrelevance effect should be reversed if conditioning trials are given at a rate of one per day . Experiments 2 and 3 found no support for this prediction. We conclude that learned irrelevance effects cannot always be reduced to latent inhibition.     

Latent inhibition of US signal value.

Three experiments with rats examined the effects of preexposure to an unconditioned stimulus (US; a single food pellet) on the subsequent ability of that US to effectively signal the delivery of three food pellets during a US-US conditioning procedure. In Experiment 1, latent inhibition (LI) rats showed attenuated conditioning, compared to control (C) rats, when a single food pellet, delivered 10 minutes into a session, was followed by three additional pellets. In preexposure, one pellet had been delivered 10 minutes into each session (in group LI), or placed into the magazine at the beginning of each session (in group C). Experiment 2 showed that this effect was evident when the conditions of preexposure matched those of conditioning for group C, and Experiment 3 showed that the difference between groups LI and C was not a product of context conditioning, or latent inhibition to the noise of the feeder in group LI. Implications of these results for theories of latent inhibition are considered.     

Learned irrelevance: A contemporary overview

This article reviews the recent literature on the topic of learned irrelevance. It asks whether the retardation of subsequent conditioning produced by uncorrelated preexposure is indeed the result of the animal learning that a conditioned stimulus (CS) and unconditioned stimulus (US) are unrelated, or whether it is better explained either as a result of the context specificity of latent inhibition, or as some other artefact of the uncorrelated schedule employed. The conclusion is that there is as yet no good evidence to support the existence of a “genuine” learned irrelevance effect.     

Latent Inhibition of Contextual Stimuli Reduces the US Preexposure Effect in Rats

Two experiments are reported which utilized latent inhibition of contextual stimuli prior to administering unsignaled presentations of the Us in an attempt to further assess the role of contextual stimuli in the US preexposure effect. Specifically in Experiment 1, rats received either 0-, 5-, 10-, or 15-minute exposure to the context in which the unsignaled Uss were to occur (latent inhibition). Following preexposure to the US, animals were trained in a CER paradigm with a tone CS. Measures of suppression to the tone indicated that the greatest US preexposure effect occurred in the 0 group and that no US preexposure effect was evident in the 15 group. Experiment 2 includec two important control groups which were omitted in Experiment 1 (no US preexposures) and an additional dependent variable (time to initiate licking) to measure fear to contextual stimuli. These results are discussed in terms of the role context conditioning may play in US preexposure.

     

Analysis of the learned irrelevance effect in appetitive Pavlovian conditioning

In Experiments 1 and 2 rats received uncorrelated presentations of a light conditioned stimulus (CS) and a food unconditioned stimulus (US) on each day of a preexposure phase. Control subjects received the same number of USs during the first half of preexposure and the same number of CSs during the second. Uncorrelated preexposure retarded inhibitory conditioning. Experiment 3 showed, however, that the different patterns of US preexposure experienced by the two groups could in itself influence the course of subsequent inhibitory conditioning. When this factor was equated by restricting the uncorrelated treatment to the first half of the pre-exposure phase (Experiment 2) or by extending the control treatment throughout the phase (Experiment 4) it was found that uncorrelated preexposure retarded excitatory conditioning, but facilitated inhibitory conditioning. This outcome challenges an interpretation in terms of the concept of learned irrelevance, which predicts that uncorrelated preexposure should retard both forms of conditioning.     

Contextual Control of Latent Inhibition by the Reinforcer

Three experiments examined the contextual control of latent inhibition (LI) by the unconditioned stimulus (US) using a within-subjects conditioned suppression procedure with rats. The effect of reducing the context change produced by the introduction of the shock US was investigated by presenting this US during preexposure to the conditioned stimulus (CS). Although limited CS preexposure in the absence of the US had no impact on subsequent conditioning, preexposure in the presence of the shock retarded both excitatory and inhibitory conditioning. We conclude that the introduction of the US during the conditioning phase of a normal LI experiment can produce a contextual change that reduces the observed magnitude of LI.     

Learned irrelevance and retrospective correlation learning

In 1973 Mackintosh reported an interference effect that he called learned irrelevance in which exposure to uncorrelated (CS/US) presentation of the unconditional stimulus (US) and the conditioned stimulus (CS) interfered with future Pavlovian conditioning. It has been argued that there is no specific interference effect in learned irrelevance; rather the interference is the sum of independent CS and US exposure effects (CS + US). We review previous research on this question and report two new experiments. We conclude that learned irrelevance is a consequence of a contingency learning and a specific learned irrelevance mechanism. Moreover even the “independent exposure controls”, used in previous experiments to support the CS and US exposure account, provide support for the correlation learning process.     

Lithium-mediated disruptions of latent inhibition: Overshadowing by the unconditioned stimulus in flavor conditioning

In a series of experiments, the ability of a single lithium preexposure to disrupt CS effectiveness was assessed using a latent inhibition procedure. Lithium preexposure administered proximal (90 min) to a saccharin familiarization trial reduced latent inhibition whereas a similar administration more distal (360 min) to flavor familiarization failed to do so. Additional experiments demonstrated that this socalled “US overshadowing” effect was not attributable to sensitization (Experiment 2), excitatory backward conditioning (Experiment 3), or state dependency (Experiment 4). The implications of US overshadowing for proximal US-preexposure effects are discussed.     

Recent Learned Helplessness/Irrelevance Research in Japan: Conceptual Framework and Some Experiments on Learned Irrelevance

In Section 1, a conceptual framework within which to study learned helplessness (LH), learned irrelevance (LI) and the related phenomena is introduced. In Section 2, three rat experiments on LI conducted in our laboratory using a conditioned suppression of licking preparation are introduced. In Experiment 1, the phenomena of LI and general LI were confirmed. In Experiment 2, random presentations of CST/US were found to interfere with subsequent initial excitatory conditioning to CSL under random CSL/US presentations. In Experiment 3, pre-paired presentations of CSN or CST with US before random CST/US presentations was found to have an attenuating effect on the development of general LI.     

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.     

Latent inhibition experiments with goldfish (Carassius auratus)

Evidence of latent inhibition was sought in a series of experiments with goldfish. In Experiment 1, goldfish were given nonreinforced preexposure to a color that subsequently predicted shock in an activity conditioning situation; their performance did not differ from that of control animals preexposed to a markedly different color. In Experiment 2, a group of goldfish given nonreinforced preexposure to a tone and an unstimulated control group were trained in an appetitive situation, with the tone serving either as a conditioned excitor or as a conditioned inhibitor. Preexposure had no significant effect in the conditioned excitation training, but it reduced the level of responding both to the positive stimulus and to the negative compound in the conditioned inhibition training. In Experiments 3 and 4, classical aversive conditioning was studied in the shuttle box. In Experiment 3, excitatory conditioning to a color was found to be impaired (relative to the performance of nonpreexposed control animals) as much by nonreinforced preexposure to the training color as by nonreinforced preexposure to a markedly different color; substantial variation in amount of preexposure was without significant effect. In the conditioned inhibition training of Experiment 4, animals with nonreinforced preexposure responded less than did unstimulated control animals both to the positive stimulus and to the negative compound. The results for goldfish can be understood on the assumption that the effect of preexposure in these animals is simply to reduce general responsiveness or level of arousal.     

Recent learned helplessness/irrelevance research in Japan: Conceptual framework and some experiments on learned irrelevance

In Section 1, a conceptual framework within which to study learned helplessness (LH), learned irrelevance (LI) and the related phenomena is introduced. In Section 2, three rat experiments on LI conducted in our laboratory using a conditioned suppression of licking preparation are introduced. In Experiment 1, the phenomena of LI and general LI were confirmed. In Experiment 2, random presentations of CSt/US were found to interfere with subsequent initial excitatory conditioning to CSl under random CSl/US presentations. In Experiment 3, pre-paired presentations of CSn or CSt with US before random CSt/US presentations was found to have an attenuating effect on the development of general LI.     

Contextual control over conditioned responding in a latent inhibition paradigm

We used 1-, 2-, and 3-context designs to study the control exerted by contexts over freezing in rats exposed to a conditioned stimulus (CS) in advance of its pairing with a shock unconditioned stimulus. The latent inhibition observed when preexposure, conditioning, and testing occurred in the same context was attenuated if preexposure occurred in a different context to conditioning and testing. Latent inhibition (i.e., attenuated performance) was restored in a CS-specific manner if preexposure and testing occurred in the same context and conditioning in a different one. Latent inhibition was also reduced by a long retention interval but remained specific for a particular context-CS relation. Finally, CS preexposure resulted in contextual control over the expression of excitatory conditioned performance. The results are discussed in terms of memory, associative, and associative-performance models of CS-preexposure effects.     

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.     

A Comparison of Latent Inhibition and Learned Irrelevance Pre-Exposure Effects in Rabbit and Human Eyeblink Conditioning

The learning of an association between a CS and a US can be retarded by unreinforced presentations of the CS alone (termed latent inhibition or LI) or by un-correlated presentations of the CS and US (termed learned irrelevance or LIRR). In rabbit eyeblink conditioning, there have been some recent failures to replicate LI. LIRR has been hypothesized as producing a stronger retardation effect than LI based on both empirical studies and computational models. In the work presented here, we examined the relative strength of LI and LIRR in eyeblink conditioning in rabbits and humans. In both species, a number of preexposure trials sufficient to produce LIRR failed to produce LI (Experiments 1 & 3). Doubling the number of CS pre-exposures did produce LI in rabbits (Experiment 2), but not in humans (Experiment 4). LI was demonstrated in humans only after manipulations including an increased inter-trial interval or ITI (Experiment 5). Overall, it appears that LIRR is a more easily producible pre-exposure retardation effect than LI for eyeblink conditioning in both rabbits and humans. Several theoretical mechanisms for LI including the conditioned attention theory, stimulus compression, novelty, and the switching theory are discussed as possible explanations for the differences between LIRR and LI. Overall, future work involving testing the neural substrates of pre-exposure effects may benefit from the use of LIRR rather than LI.     

Integrating incremental learning and episodic memory models of the hippocampal region

By integrating previous computational models of corticohippocampal function, the authors develop and test a unified theory of the neural substrates of familiarity, recollection, and classical conditioning. This approach integrates models from 2 traditions of hippocampal modeling, those of episodic memory and incremental learning, by drawing on an earlier mathematical model of conditioning, SOP (A. Wagner, 1981). The model describes how a familiarity signal may arise from parahippocampal cortices, giving a novel explanation for the finding that the neural response to a stimulus in these regions decreases with increasing stimulus familiarity. Recollection is ascribed to the hippocampus proper. It is shown how the properties of episodic representations in the neocortex, parahippocampal gyrus, and hippocampus proper may explain phenomena in classical conditioning. The model reproduces the effects of hippocampal, septal, and broad hippocampal region lesions on contextual modulation of classical conditioning, blocking, learned irrelevance, and latent inhibition.     

Associative regulation of Pavlovian fear conditioning: unconditional stimulus intensity, incentive shifts, and latent inhibition.

Conditional stimuli (CS) associated with painful unconditional stimuli (US) produce a naloxone-reversible analgesia. The analgesia serves as a negative-feedback regulation of fear conditioning that can account for the impact of US intensity and CS predictiveness on Pavlovian fear conditioning. In Experiment 1 training under naloxone produced learning curves that approached the same high asymptote despite US intensity. Shifting drug treatment during acquisition had effects that paralleled US intensity shifts. In Experiment 3 naloxone reversed Hall-Pearce (1979) negative transfer using a contextual CS, indicating that conditional analgesia acquired during the CS-weak-footshock phase retards acquisition in the CS-strong-footshock phase. Experiment 5 used a tone CS in both a latent-inhibition and a negative-transfer procedure. Only negative transfer was blocked by naloxone. Therefore, negative transfer but not latent inhibition is mediated by a reduction of US processing.     

Selective entorhinal and nonselective cortical-hippocampal region lesions,but not selective hippocampal lesions,disrupt learned irrelevance in rabbit eyeblink conditioning

Prior experiments, as well as computational models, have implicated the hippocampal region in mediating the influence of nonreinforced stimulus preexposure on subsequent learning. Learned irrelevance (LIRR) is a preexposure task in which uncorrelated preexposures to the conditioned stimulus (CS) and the unconditioned stimulus (US) produce a retardation of subsequent CS-US conditioning. In the work presented here, we report the results of tests of LIRR in eyeblink conditioning in rabbits with sham lesions, nonselective cortical-hippocampal region lesions, selective hippocampal lesions, and selective entorhinal lesions. Sham-lesioned rabbits that had been preexposed to the CS and the US exhibited slower acquisition of conditioned response, as compared with context-preexposed controls. Nonselective cotical-hippocampal region lesions disrupted LIRR, whereas selective hippocampal lesions had no detrimental effect on LIRR. Selective entorhinal lesions disrupted LIRR. These findings fit other recent empirical findings and theoretical predictions that some classical conditioning tasks previously thought to depend on the hippocampus depend, rather, on the entorhinal cortex.     

Latent inhibition in human adults without masking

Latent inhibition refers to attenuated responding to Cue X observed when the X-outcome pairings are preceded by X-alone presentations. It has proven difficult to obtain in human adults unless the preexposure (X-alone) presentations are embedded within a masking (i.e., distracting) task. The authors hypothesized that the difficulty in obtaining latent inhibition with unmasked tasks is related to the usual training procedures, in which the preexposure and conditioning experiences are separated by a set of instructions. Experiment 1 reports latent inhibition without masking in a task in which preexposure and conditioning occur without interruption. Experiments 2 and 3 demonstrate that this attenuation in responding to target Cue X does not pass a summation test for conditioned inhibition and is context specific, thereby confirming that it is latent inhibition. Experiments 3 and 4 confirm that introducing instructions between preexposure and conditioning disrupts latent inhibition.