Context specificity of conditioning and latent inhibition: Evidence for a dissociation of latent inhibition and associative interference

Conditioning may generalize from one context to another when latent inhibition (the effect on subsequent conditioning of prior unreinforced exposure to the stimulus) does not. Experiment 1 studied conditioned approach and licking by rats to a stimulus paired with the delivery of water and confirmed that latent inhibition could be abolished by a change of context, while prior aversive conditioning to the stimulus, produced by pairing it with mild shock, interfered with the acquisition of conditioned approach and licking regardless of this change of context. Thus even when conditioning and latent inhibition were measured in the same way, the former generalized across contexts, and the latter did not. Experiment 2 showed that the effects not only of unreinforced exposure to a stimulus but also of presentation of the stimulus uncorrelated with the delivery of water were confined to the context in which they occurred. Thus the generalization of conditioning from one context to another and the failure of latent inhibition to generalize cannot be attributed to the occurrence of rein-forcers during conditioning and their absence in latent inhibition. This conclusion was confirmed in Experiment 3, where animals received both aversive conditioning trials and unreinforced presentations of other stimuli in the treatment phase of the experiment, but were then conditioned to one of these stimuli paired with water. Once again, the effects of aversive conditioning transferred perfectly from one context to another, while those of unreinforced presentations did not. Latent inhibition, these results suggest, is not easily explained by supposing that animals associate an unreinforced stimulus with zero consequences and have to unlearn this association when the stimulus is then paired with a reinforcer.     

Medial auditory thalamic input to the lateral pontine nuclei is necessary for auditory eyeblink conditioning

Auditory and visual conditioned stimulus (CS) pathways for eyeblink conditioning were investigated with reversible inactivation of the medial (MPN) or lateral (LPN) pontine nuclei. In Experiment 1, Long-Evans rats were given three phases of eyeblink conditioning. Phase 1 consisted of three training sessions with electrical stimulation of the medial auditory thalamic nuclei (MATN) paired with a periorbital shock unconditioned stimulus (US). An additional session was given with a muscimol (0.5 μL, 10 mM) or saline infusion targeting the LPN followed by a recovery session with no infusions. The same training and testing sequence was then repeated with either a tone or light CS in phases 2 and 3 (counterbalanced). Experiment 2 consisted of the same training as Experiment 1 except that muscimol or saline was infused in the MPN during the retention tests. Muscimol infusions targeting the LPN severely impaired retention of eyeblink conditioned responses (CRs) to the MATN stimulation and tone CSs but only partially reduced CR percentage to the light CS. Muscimol infusions that targeted the MPN had a larger effect on CR retention to the light CS relative to MATN stimulation or tone CSs. The results provide evidence that the auditory CS pathway necessary for delay eyeblink conditioning includes the MATN-LPN projection and the visual CS pathway includes the MPN.     

Reinforcement magnitude effects in first- and second-order conditioning of directed action

Three experiments investigated the effects of reinforcement magnitude on conditioned key pecking in pigeons. Experiment 1, which included between-groups and within-subject designs, yielded significant effects of unconditioned stimulus (US) magnitude on the within-conditioned stimulus (CS) distribution of key pecks and on choice behavior, but no effect on the overall rate of key pecking. Experiment 2 employed a larger US-magnitude difference in a within-subject design. This manipulation resulted in differential rates of key pecking as well as a significant choice effect and differential within-CS key-peck distributions. A second-order conditioning procedure was used in Experiment 3, in which diffuse, visual stimuli (S1's) served as Pavlovian reinforcers for two key-light S2's. The S1 previously paired with a large US was more effective in conditioning second-order key-peck behavior to an S2 than was the S1 paired with a small US. The results of these experiments demonstrate that the associative effects of US magnitude can be expressed in the strength of CS-directed motor responding. The distinctive within-CS key-peck distributions in first-order conditioning suggests an interaction between CS- and US-directed responses.     

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.     

The Influence of Retention Interval on the US Preexposure Effect: Changes in Contextual Blocking over Time

A number of studies manipulating the length of the interval between conditioning and testing indicate spontaneous recovery from overshadowing, suggesting that certain instances of overshadowing represent a deficit in memory retrieval rather than a failure of animals to form an association between the overshadowed stimulus and the US. The present series of experiments examined the influence of lengthening the retention interval on blocking, another stimulus selection phenomenon that is typically interpreted as an acquisition deficit. The results indicated that when subjects were tested shortly (3 days) after training conditioning to a taste blocked subsequent conditioning to an odor conditioned in compound with that taste (Experiment 1), whereas prior conditioning to an odor did not block subsequent conditioning to a taste conditioned in compound with that odor (Experiment 2). This pattern of results was essentially unchanged when testing occurred at a longer (21-day) retention interval. However, there was evidence of a US preexposure effect in Experiment 2 when subjects in the US ONLY control condition were tested at the 3-day retention interval, but not when testing occurred 21 days after conditioning. Experiments 3 and 4 examined whether this loss of the US preexposure effect over time might actually represent a change in the degree of contextual blocking as the retention interval is lengthened. Exposure to the conditioning context either during the interval between Phase 1 and Phase 2 of conditioning (Experiment 3) or prior to Phase 1 of conditioning (Experiment 4) alleviated this US preexposure effect suggesting that the loss of the US preexposure effect as the retention interval is lengthened observed in Experiment 2 is due to changes in the degree of blocking by contextual stimuli over time. The results are discussed in terms of differential susceptibility of forgetting of two functional roles played by a contextual stimuli in the current situation-context as a CS and context as a retrieval cue for other CS-US associations.     

The Importance of Context in the US Preexposure Effect in CTA: Novel versus Latently Inhibited Contextual Stimuli

Three experiments were conducted to examine the role of novel contextual stimuli in producing the unconditioned stimulus (US) preexposure effect. Experiment 1 demonstrated that novel contextual stimuli produce a significantly stronger US preexposure effect than familiar or “latently inhibited” contextual stimuli. Moreover, subjects preexposed in the presence of latently inhibited contextual cues failed to show a significant US preexposure effect. Experiments 2 and 3 attempted to provide evidence that the addition of a single novel stimulus to the latently inhibited context would result in a significantly stronger US preexposure effect than when no such novel cue was present. Experiment 3 was able to demonstrate this effect. Results are consistent with the Rescorla–Wagner (1972) model of conditioning.     

The effects of context extinction on US signal value

Two experiments with rats examined the effects of context extinction on responding to the signal value of an unconditioned stimulus (US). In Experiment 1, US signal value was first trained when a single food pellet signaled the delivery of three additional pellets. After training, rats received either context extinction (CE) or home cage (HC) exposure before testing US signal value by single food pellet presentations. Results showed responding was significantly reduced in Group CE compared to Group HC. Experiment 2 replicated Experiment 1 and showed that exposure to a different context did not reduce responding to the signal value of a US. The results complement research by Kehoe et al. [Kehoe, E. J., Weidemann, G., & Dartnall, S. (2004). Apparatus exposure produces profound declines in conditioned nictitating-membrane responses to discrete conditioned stimuli by the rabbit (Oryctolagus cuniculus). Journal of Experimental Psychology: Animal Behavior Processes, 30, 259–270.] and have key implications for prominent theories of conditioning.     

Rearing in response to a visual conditioned stimulus: An index of associative strength or of associability?

Two procedures for observing rearing behavior during a localized visual CS paired with an appetitive US were compared within subjects during classical conditioning and extinction procedures. When rearing was observed using the method and response definition described by P. C. Holland (1977, Journal of Experimental Psychology: Animal Behavior Processes, 3, 77–104), responding was acquired and maintained during conditioning trials in rats receiving paired presentations of the CS and US, but not in rats receiving the stimuli according to a “truly random” procedure. When rearing of the same rats was observed using the method and response definition described by H. Kaye and J. M. Pearce (1984, Journal of Experimental Psychology: Animal Behavior Processes, 10, 90–109), responding declined across conditioning trials in both groups. Furthermore, in extinction, rearing during the CS declined according to Holland's scoring method but was temporarily restored according to Kaye and Pearce's scoring. Observations of a second behavior, magazine responding, revealed essentially the same pattern of responding for both methods of scoring. These results support the position that the response criteria used by Holland and by Kaye and Pearce assess different components of behavior that occur in response to a visual CS, reflecting associative strength (i.e., a CR) and associability of the CS (i.e., an OR), respectively.     

Associations in Pavlovian conditioned inhibition

Two experiments with rat subjects used a variety of transfer tests to examine the associations learned when Pavlovian inhibition is established by an A+, AX− paradigm. Experiment 1 found in a conditioned suppression situation that inhibition conditioned to X with one exciter (A) readily transferred to another exciter (B) which had been paired with the same shock US. Transfer occurred even when the response to A had been extinguished prior to testing with B. However, X did not inhibit a general activity response produced by a B which had been subsequently paired with a food US. Experiment 2 employed a Pavlovian conditioning situation in which A and B, when separately paired with the same food US, evoked dissimilar responses. Nevertheless, an inhibitor trained in an A+, AX− paradigm successfully inhibited the different response evoked by B. However, such an X did not inhibit the behaviors acquired by A or B when they were subsequently paired with a shock US. The transfer of Pavlovian inhibition across conditioned stimuli and responses but not across unconditioned stimuli is consistent with the notion that a conditioned inhibitor acts to prevent activation of a US representation which would normally be activated by conditioned exciters.     

Automated assessment of conditioning parameters for context and cued fear in mice

A behavioral technique often used to evaluate the cognitive performance of rats and mice is the fear conditioning paradigm. During conditioned fear experiments, freezing responses shown by rodents after exposure to environmental stimuli previously paired to an aversive experience provide a behavioral index of the animal's associative abilities. The present study examined the ability of a computer-controlled automated Freeze Monitor system for recording immobility behavior in mice. The sensitivity of the automated procedure to detect group differences caused by the application of various training protocols was also evaluated. Statistical analyses revealed significant positive correlations between immobility scores obtained with the automated apparatus and hand-scored data collected by a continuous or a time-sampling method. Behavioral patterns recorded by the computerized system were very similar to those obtained by the hand-scoring methods adopted. In particular, during context testing, exposure to environmental stimuli previously paired with a mild foot shock (unconditioned stimulus [US]) evoked increased immobility behavior in mice conditioned with the US compared with levels of immobility displayed by mice previously confined to the same contextual stimuli without receiving the US. Moreover, although during conditioned stimulus (CS) testing, mice previously exposed to the US displayed high levels of immobility when confined to environmental cues much different from those paired with the US (contextual fear generalization), both hand-scored and automated results revealed the effect of CS–US pairing (increased immobility) only in mice trained to associate the two stimuli (paired group) but not in mice exposed to both CS and US separated by a 40-sec time interval (unpaired group) or in mice receiving only the US (US group) during conditioning sessions. Overall, the results show associative conditioning measured in an automated apparatus and highlight the utility of obtaining both latency as well as beam interruption parameters.     

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.     

Transfer of inhibition after serial feature negative discrimination training

Three experiments examined the transfer of inhibition in Pavlovian serial feature negative (A+, X→ A−) discriminations in a conditioned suppression situation with rat subjects. Consistent with our previous report (P. C. Holland & J. Lamarre, Learning and Motivation, 15, 219–243), the feature (X) showed little or no ability to inhibit suppression to another conditioned excitor (B) that had been consistently reinforced. Nor was substantial transfer observed to excitors that had been partially reinforced, or conditioned, extinguished, and then reconditioned. However, X readily inhibited suppression to an excitor that had been trained within another serial feature negative discrimination (B+, Y → B−). These latter data are difficult to reconcile with our previous proposal that inhibitors established with serial procedures act on particular conditioned stimulus-unconditioned stimulus associations. We suggest that serial feature negative discriminations endow both the feature (X) and the excitor (A) with special properties.     

Latent inhibition and conditioning after preexposure to the training context

Experiment 1, using the conditioned suppression technique with rats, showed that the retardation of learning produced by prior exposure to a stimulus (latent inhibition) was more marked in subjects given an initial phase of preexposure to the training context. This effect was confirmed and extended in Experiment 2 in which an appetitive conditioning procedure was used. Experiments 3 and 4, again using conditioned suppression, found no effect of preexposure to the context on the acquisition of suppression when training was given with a novel stimulus, either immediately after preexposure or after a delay; but context preexposure was again found to be effective when exposure to the to-be-conditioned stimulus was given in the delay interval between context preexposure and conditioning. The implications of these findings for accounts of the role of contextual factors in latent inhibition are discussed.     

Pavlovian second-order conditioned analgesia

Three experiments with rat subjects assessed conditioned analgesia in a Pavlovian second-order conditioning procedure by using inhibition of responding to thermal stimulation as an index of pain sensitivity. In Experiment 1, rats receiving second-order conditioning showed longer response latencies during a test of pain sensitivity in the presence of the second-order conditioned stimulus (CS) than rats receiving appropriate control procedures. Experiment 2 found that extinction of the first-order CS had no effect on established second-order conditioned analgesia. Experiment 3 evaluated the effects of post second-order conditioning pairings of morphine and the shock unconditioned stimulus (US). Rats receiving paired morphine-shock presentations showed significantly shorter response latencies during a hot-plate test of pain sensitivity in the presence of the second-order CS than did groups of rats receiving various control procedures; second-order analgesia was attenuated. These data extend the associative account of conditioned analgesia to second-order conditioning situations and are discussed in terms of the mediation of both first- and second-order analgesia by an association between the CS and a representation or expectancy of the US, which may directly activate endogenous pain inhibition systems.     

Conditioned taste aversion is enhanced when the unconditioned stimulus is presented in a different context

Using a conditioned taste aversion procedure with rats as the subjects, two experiments examined the effect of presenting a conditioned stimulus (CS saccharin solution) in one context followed by an unconditioned stimulus (US LiCl) in a different context. Experiment 1 showed that animals which received the above-mentioned procedure (Group D) showed a more marked conditioned aversion to the CS than animals which were given both the CS and the US in the same context (Group S). Experiment 2 found that in both Group D and Group S, aversion to the CS increased when the subjects were exposed to the conditioned context after the conditioning. These findings supported the argument that the strength of the CS-US association acquired during conditioning is compared with that of the context-US to determine the magnitude of aversion revealed to the CS.     

The role of injection cues in the associative control of the US pre-exposure effect in flavour aversion learning

Two experiments, using rats as subjects, examined the role of contextual cues in producing the unconditioned stimulus (US) pre-exposure effect in conditioned taste aversion. Experiment 1 showed a significant US pre-exposure effect, when the pre-exposure was conducted in a familiar context, and that a change of context between the pre-exposure and conditioning phases did not attenuate this effect. Experiment 2 demonstrated that extinction of injection-related cues after the pre-exposure stage attenuated the US pre-exposure effect, when the pre-exposure was conducted in either a familiar or a novel context. Taken together, these results support the associative explanation of the US pre-exposure effect in terms of blocking, incorporating a role for injection-related cues in the context blocking analysis of the US pre-exposure effect.     

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.     

Contextual control of inhibition with reinforcement: adaptation and timing mechanisms

Four experiments with rats studied the effects of switching the context after Pavlovian conditioning. In three conditioned suppression experiments, a large number of conditioning trials created "inhibition with reinforcement" (IWR), in which fear of the conditional stimulus (CS) reached a maximum and then declined despite continued CS-unconditional stimulus pairings. When IWR occurred, a context switch augmented fear of the CS; IWR and augmentation were highly correlated. Neither IWR nor augmentation resulted from inhibition of delay (IOD): In conditioned suppression, IWR and augmentation occurred without IOD (Experiment 3), and in appetitive conditioning (Experiment 4), IOD occurred without IWR or augmentation. IWR may occur in conditioned suppression because the animal adapts to fear of the CS in a context-specific manner. The authors discuss several implications.     

Associability of a previously conditioned stimulus as a function of qualitative changes in the US

Hall and Pearce (1979) reported retarded manifestation of conditioned responding to repeated CS-strong shock pairings as a result of prior CS-weak shock pairings. These authors suggested that a latent inhibition (LI)-like process reduced the associability of the CS during weak shock conditioning despite excitatory associations between CS and weak shock being formed. The present experiments examined the possibility that the negative transfer from CS-weak shock conditioning in Stage 1 to CS-strong shock conditioning in Stage 2 observed by Hall and Pearce was due at least in part to the similarity between weak and strong shock rather than, or in addition to, a general loss of CS associability. Specifically, the transfer of decreased associability to conditioning with a dissimilar US was investigated. Consistent with Hall and Pearce, who gave multiple training trials in Stage 2, Experiment 1 found the development of conditioned responding owing to a single CS-strong shock pairing in Stage 2 to be retarded by prior CS-weak shock pairings and compared this effect to conventional LI. In Experiment 2, partial attenuation of the negative transfer following CS-weak shock was obtained by substituting ice water immersion for strong shock, that is, by making the strong US qualitatively dissimilar from the weak US. In contrast, conventional LI resulting from preconditioning CS-only exposures was equivalent for strong shock in Experiment 1 and ice water immersion in Experiment 2. A possible mechanism for the sensitivity to qualitative US changes of the observed negative transfer is discussed.     

No sex difference in contextual control over the expression of latent inhibition and extinction in Pavlovian fear conditioning in rats

Three experiments with Wistar rats searched for a sex difference in contextual control over the expression of latent inhibition and extinction. Experiment 1 used a latent inhibition procedure; Experiments 2 and 3 employed an extinction preparation. All experiments used a shock as the unconditioned stimulus, a tone as the conditioned stimulus, and suppression of food magazine visits as the measure of conditioned responding to the tone. Each experiment revealed a reliable context effect on conditioned responding to the tone; after conditioning in a separate context, conditioned responding in the former latent inhibition or extinction context was attenuated relative to conditioned responding in a control context. There was no sex difference in the magnitude of this effect. These results are discussed in the framework of sex differences in the hippocampus and of the putative role of this structure in various instances of contextual learning.