Superlatent inhibition and spontaneous recovery: differential effects of pre- and postconditioning CS-alone presentations after long delays in different contexts

In two pairs of three-stage conditioned taste aversion experiments, we examined the effects of delay interval (1 or 21 days) between the second and third stages, and of context in which the animals spent the delay (same as or different from the context of the other stages) on latent inhibition (LI) and spontaneous recovery following extinction. In the LI experiments (Experiments 1A and 1B), the first stage comprised nonreinforced presentations to saccharin or to water. In the second stage, rats were conditioned by saccharin paired with LiCl. In the extinction experiments (Experiments 2A and 2B), the order of the stages was reversed. For all experiments, Stage 3, the test stage, consisted of three presentations of saccharin alone. There was a super-LI effect in the saccharin-preexposed group that spent the 21-day delay in the different context (Experiment 1A). When the delay was spent in the same context, there was no difference in the amount of LI between the short- and long-delay groups (Experiment 1B). Conversely, there was a spontaneous recovery effect in the long-delay/same-context group (Experiment 2B), but not in the long-delay/different-context group (Experiment 2A). The pattern of results, incompatible with current explanations of delay-induced changes in memory performance, was interpreted in terms of an interaction between the delay conditions (same or different delay context), which modulate the extinction of previously acquired context-CS-nothing associations (during CS-alone presentations), and primacy effects.     

Delay-induced super-latent inhibition as a function of order of exposure to two flavours prior to compound conditioning

A number of recent conditioned taste aversion (CTA) experiments have demonstrated a super-latent inhibition (LI) effect—namely, a time-induced increase in the effects of stimulus preexposure when the interval between acquisition and test is spent in a context that is different from the other experimental contexts. Two CTA experiments with rats were conducted to examine the role of primacy in producing super-LI. In Experiment 1, one of two flavours was pre-exposed, following which a second flavour was preexposed. After the second preexposure, animals were conditioned by pairing a compound of the two preexposed flavours with LiCl. The test stage was conducted 1 or 21 days after conditioning, with the interval being spent in either the same or different contexts. In the test, animals were confronted with two bottles, each with one of the two preexposed flavours. Super-LI was obtained only for the first preexposed flavour in the 21-day delay group that spent the interval in a different context. Experiment 2 was designed to ensure that the effects in Experiment 1 represented LI, and to control for order of presentation of the flavours and time between preexposure and acquisition. The results replicated those of Experiment 1. The two experiments support the importance of primacy in the general super-LI experiment where CS-alone preexposure precedes CS-US.     

There is a time and a place for everything: Bidirectional modulations of latent inhibition by time-induced context differentiation

Latent inhibition (LI) is defined as poorer evidence of learning with a stimulus that previously was presented without consequence, as compared with a novel or previously attended stimulus. The present article reviews the evidence, mostly from three-stage conditioned taste aversion studies (preexposure, conditioning, and test), that LI can be either attenuated or enhanced depending on the length of the retention interval between conditioning and test and where that interval was spent. Time-induced reduction in LI is observed when the interval context is the same as that of the preexposure, conditioning, and test stages. Super-LI is obtained when a long retention interval is spent in a context that is different from that of the other stages. The differential modulations of LI appear to be the result of the strengthening of primacy effects (i.e., first training disproportionately stronger than subsequent training) by long-interval different contexts, thereby producing super-LI, and the reversal of this effect by long-interval same contexts, thereby producing attenuated LI. The bidirectional effects of time/ context modulations on LI, unaccounted for by current learning theories, are explained, in part, by a time-induced context differentiation process. Implications for theories of LI, learning, and memory are discussed.     

Super-latent inhibition of conditioned taste preference with a long retention interval

A long delay inserted between conditioning and test phases of a 3-stage Latent Inhibition (LI) procedure produces differential effects on LI depending on the delay context. Thus, enhanced LI has been obtained when the delay is spent in a context that is different from the remaining experimental contexts, but not when it is the same. The present paper examined the effect of delayed testing using a conditioned taste preference procedure. In Experiment 1, three groups received preexposure to either water, or almond, or citrus solutions. Subsequently, the animals were conditioned by pairing the almond and the citrus solutions with sucrose. In a two-bottle preference test conducted 1 day after conditioning, the preexposed flavored solutions were consumed less than the non-preexposed flavors (LI). Experiments 2 and 3 used the same basic procedure, but varied the retention interval duration (1 and 21 days) and the delay context, similar (Experiment 2) and different (Experiment 3) from that of the other stages of the experiments. LI was greater after the long than the short-retention interval when the context was different, thereby demonstrating super-LI. The results were explained by a time-induced context differentiation process.     

Pharmacological dissociation of trace and long-delay fear conditioning in young rats

In most studies comparing trace and delay conditioning, CS duration is kept constant across training conditions but the interstimulus interval (ISI), the time from CS onset to US onset, is confounded. In the infrequently used long-delay condition, however, ISI is kept constant across the trace and delay conditions but CS duration varies. A recent study reported that trace and long-delay fear conditioning have the same developmental trajectory, with both emerging later in development than standard-delay conditioning (). Past studies have shown that trace conditioning is mediated by the cholinergic system; given the parallel developmental emergence of trace and long-delay conditioning, the present study examined whether the cholinergic system also mediates long-delay conditioning. Two experiments, both involving Sprague-Dawley-derived rats and using freezing as a measure of learned fear, showed that the cholinergic system is critically involved in trace conditioning but is not involved in long-delay conditioning. Specifically, pre-training injections of the muscarinic receptor antagonist scopolamine impaired acquisition of a CS-US association in 32-day-old rats trained with a trace procedure but had no effect on rats this age trained with a long-delay procedure (Experiment 1). Similarly, pre-training injections of physostigmine, a cholinesterase inhibitor, enhanced acquisition of trace conditioning in 25-day-old rats but had no effect on long-delay conditioning in rats this age (Experiment 2). Taken together, the results indicate that despite the similarities between trace and long-delay conditioning in terms of developmental emergence and level of conditioned responding, they are mediated by different physiological systems.     

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.     

Higher-order conditioning and sensory preconditioning of a taste aversion with an exteroceptive CS1

An exteroceptive stimulus compound (context) was employed as CS₁ in higherorder conditioning (H-OC, Experiments I and II), and sensory preconditioning (SPC, Experiment III) of a saccharin (CS₂) aversion in rats. The results indicated that aversions were established with the H-OC as well as with the SPC procedures. Stimulus generalization and first-order conditioning explanations were ruled out by appropriate controls. A CS₁-extinction period, performed prior to testing, did not affect the H-OC aversion, whereas it reduced the SPC aversion at least partially. These findings imply that interoceptive (taste, nausea) and exteroceptive stimuli (context) are readily associable in rats. Implications of the resemblance between the SPC procedure and long-delay taste-aversion learning are discussed.     

Effects of Early Hippocampal Lesions on Trace, Delay, and Long-Delay Eyeblink Conditioning in Developing Rats

The effects of bilateral hippocampal aspiration lesions on later acquisition of eyeblink conditioning were examined in developing Long-Evans rat pups. Lesions on postnatal day (PND) 10 were followed by evaluation of trace eyeblink conditioning (Experiment 1) and delay eyeblink conditioning (Experiment 2) on PND 25. Pairings of a tone conditioned stimulus (CS) and periocular shock unconditioned stimulus (US, 100 ms) were presented in one of three conditioning paradigms: trace (380 ms CS, 500 ms trace interval, 880 ms interstimulus interval [ISI]), standard delay (380 ms CS, 280 ms ISI), or long delay (980 ms CS, 880 ms ISI). The results of two experiments indicated that hippocampal lesions impaired trace eyeblink conditioning more than either type of delay conditioning. In light of our previous work on the ontogeny of trace, delay, and long-delay eyeblink conditioning (Ivkovich, Paczkowski, & Stanton, 2000) showing that trace and long-delay eyeblink conditioning had similar ontogenetic profiles, the current data suggest that during ontogeny hippocampal maturation may be more important for the short-term memory component than for the long-ISI component of trace eyeblink conditioning. The late development of conditioning over long ISIs may depend on a separate process such as protracted development of cerebellar cortex.     

Cholinergic modulation of the hippocampus during encoding and retrieval of tone/shock-induced fear conditioning

We investigated the role of acetylcholine (ACh) during encoding and retrieval of tone/shock-induced fear conditioning with the aim of testing Hasselmo's cholinergic modulation model of encoding and retrieval using a task sensitive to hippocampal disruption. Lesions of the hippocampus impair acquisition and retention of contextual conditioning with no effect on tone conditioning. Cholinergic antagonists also impair acquisition of contextual conditioning. Saline, scopolamine, or physostigmine was administered directly into the CA3 subregion of the hippocampus 10 min before rats were trained on a tone/shock-induced fear conditioning paradigm. Freezing behavior was used as the measure of learning. The scopolamine group froze significantly less during acquisition to the context relative to controls. The scopolamine group also froze less to the context test administered 24 h posttraining. A finer analysis of the data revealed that scopolamine disrupted encoding but not retrieval. The physostigmine group initially froze less during acquisition to the context, although this was not significantly different from controls. During the context test, the physostigmine group froze less initially but quickly matched the freezing levels of controls. A finer analysis of the data indicated that physostigmine disrupted retrieval but not encoding. These results suggest that increased ACh levels are necessary for encoding new spatial contexts, whereas decreased ACh levels are necessary for retrieving previously learned spatial contexts.     

The role of context in the inhibitory conditioning of honeybees

Conditioned inhibition or CI training (A+/AB-) was compared with S- training (A+/B-) in three experiments on proboscis-extension conditioning in harnessed honeybees. The purpose was to test the Rescorla-Wagner assumption, widely credited in the vertebrate literature, that a nonreinforced stimulus acquires inhibitory properties in proportion to the excitatory value of the context in which it is presented. In prior work with free-flying honeybees pretrained with sucrose to come of their own accord to the experimental situation, no differences were found in the consequences of CI and S- training, perhaps because A added little to the excitatory value of the context (already very high) in which B occurred. In the new experiments, with harnessed subjects brought involuntarily into the training situation, negative results again were obtained. The possibility is considered that inhibitory conditioning in honeybees is independent of the excitatory value of the context.     

Relative novelty of conditioning context influences directionality of glycemic conditioning

Previous experiments in which insulin was administered in a Pavlovian conditioning procedure obtained both hyperglycemic and hypoglycemic conditioned responses (CRs). In the present experiment the relationship of the conditioning context and the housing environment was varied. Two environments, wastebasket (WB) and metal cage (MC), were varied factorially as housing and conditioning contexts. Subgroups were injected with either insulin or saline for 6 days and then, on a test day for conditioning, all animals were administered saline. The results suggested that a hyperglycemic CR could be expected when the conditioning context is different from the housing context, but a hypoglycemic CR could be expected when the conditioning context and housing context are similar. The magnitude and reliability of conditioning were greater when it was conducted in the WB context than when conditioning was conducted in the MC context. These results are discussed in terms of stress arising from relative novelty of the conditioning environment and in terms of the salience of the conditioned stimulus (CS) used in glycemic conditioning studies.     

Conditioned suppression tests of the context-blocking hypothesis: testing in the absence of the preconditioned context

Two experiments are reported that use rats in a conditioned suppression situation. The experiments, designed to remove confounds that have complicated interpretations of prior research, tested the context-blocking hypothesis, the proposition that static apparatus cues or conditioning contexts can block conditioning to discrete conditioned stimuli (CSs). Experiment 1, like previous work, tested for conditioning to the target CS in the same context that had been preconditioned and in which target conditioning had occurred; the experiment demonstrated a context-blocking like effect. Experiment 2 tested for conditioning not only in the preconditioned context but also in a nonpreconditioned context. Evidence for context blocking appeared similar in the two test situations. This suggests that conditioned contexts block the acquisition of associative strength by discrete CSs at the time of target conditioning (e.g., Rescorla & Wagner, 1972) and not through performance factors at the time of testing (e.g., Gibbon & Balsam, 1981).     

Within-compound associations between the context and the conditioned stimulus

Three experiments were conducted to test for the presence of associations between contextual cues and the nominal conditioned stimulus (CS) in fear conditioning. Rats were given tone-footshock pairings and were tested for their fear of the nominal CS, the tone, in a different context. Experiments 1 and 2 demonstrated that rats given nonreinforced exposure to the training context following conditioning were less fearful of the CS. Experiment 3 indicated that additional footshock presentations in the training context following conditioning produced greater fear of the CS. In both procedures postconditioning treatments designed to directly alter only the associative strength of the training context yielded parallel changes in the conditioned response to the CS. These data suggest that within-compound associations are formed between the context and the CS during classical conditioning.     

Effects of multiple contexts and context similarity on the renewal of extinguished conditioned behaviour in an ABA design with humans

The ABA renewal procedure involves pairing a conditional stimulus (CS) and an unconditional stimulus (US) in one context (A), presenting extinction trials of the CS alone in a second context (B), and nonreinforced test trials of the CS in the acquisition context (A). The renewal of extinguished conditioned behaviour is observed during test. The current study tested the effects of multiple extinction contexts and context similarity in attenuating renewal. Participants (N = 99) took part in a fear conditioning ABA renewal procedure. Using a measure of self-reported expectancy of the US, ABA renewal was observed when a single extinction context that was dissimilar to the test context was used. Renewal was attenuated, though still present, when extinction occurred in multiple dissimilar extinction contexts or in a single extinction context that was similar to the test context. Renewal was completely abolished when multiple extinction contexts that were similar to the test context were combined. Multiple extinction contexts and context similarity act additively in their effect on attenuating renewal. The results are discussed in relation to the design of exposure therapy programs that seek to reduce relapse that can occur via renewal.     

Temporally graded,context-specific retrograde amnesia and its alleviation by context preexposure: effects of postconditioning exposures to morphine in the rat

Five experiments studied retrograde impairments in Pavlovian fear conditioning following prolonged exposure to the opioid receptor agonist morphine. Injections of morphine commencing 1-7 days but not 14 days after conditioning produced amnesia for that conditioning episode. This amnesia was (a) selective such that morphine impaired freezing to the conditioning context but not to the auditory conditioned stimulus, (b) independent of the interval between the last injection of morphine and test, and (c) accompanied by a failure of contextual discrimination. Context preexposure protected context conditioning and discrimination from the amnestic effects of morphine. These results show that retrograde deficits in contextual fear conditioning are mediated by failures to consolidate a contextual representation.     

The effects of a flavour - toxicosis pairing upon long-delay, flavour aversion learning

Mackintosh (1973) has suggested that rats readily associate flavours with illnesses in cue-to-consequence studies because they have already learned that changes in internal states are unrelated to changes in external stimuli. An implication of this suggestion is that learned predispositions may also subserve the ability of rats to form long-delay, flavour-illness associations. Six experiments tested this idea by examining the strengths of aversions in a delayed flavour-toxicosis paradigm after exposure to a paired or unpaired relation between another flavour and toxicosis. Exposure to a paired relation enhanced the strengths of subsequently established flavour aversions (Experiment I). The enhanced aversions were associative in origin (Experiment II), observed with delays of 3 h and 1·5 h in, respectively, a forward (Experiment III) and backward (Experiment IV) delayed conditioning paradigm and with a 10-day interval between the flavour-toxin pairing and the delayed paradigm (Experiment V). The enhanced aversions, however, were removed by the extinction of the original flavour aversion prior to the delayed flavour-toxin pairing (Experiment VI). The results supported the idea that the ability of the rat to form long-delay, flavour-illness associations reflects an associative history involving flavours and internal changes and were discussed in terms of Mackintosh's (1975) theory of the mechanism underlying stimulus selection. The effects of a flavour-toxicosis pairing upon long-delay, flavour aversion learning.     

Contextual conditioning in infants, but not older animals, is facilitated by CS conditioning

Context conditioning in infant Sprague-Dawley rats (postnatal days [PD] 15, 17, and 19), juveniles (PD 25), adolescents (PD 35), and adults (PD 71-89) was compared when CS conditioning did or did not occur in the context. Degree of CS conditioning within that context was equated across age, and separate groups at each age were given unpaired presentations of the CS and US within that context. Infants conditioned more effectively to context when CS-US pairings occurred in that context than when they did not, juveniles conditioned to context about equally with and without CS-US pairings in the context, and adolescents and adults conditioned less effectively to context when CS and US were paired than when unpaired. Adolescents had significant context conditioning despite CS-US pairings in the context but adults did not, and overall, context conditioning was strongest for adolescents. Supplementary experiments indicated that with more extensive conditioning experience, the infants' pattern of context conditioning became more similar to that of older animals, and with less conditioning experience the pattern of context conditioning by adults became more similar to that of younger animals, but infants never attained the adult pattern of context conditioning nor did adults attain the infant pattern. The potentiation of context conditioning by CS conditioning observed in infants is consistent with previous evidence derived from compound conditioning. Alternative explanations place common emphasis on infant-specific amodal processing. One views potentiation as a result of the greater perceived intensity of the stimulus compound (CS and context, in this case) during conditioning and the lesser generalization decrement in infants than adults when tested with a single element after conditioning with a compound. The other explanation emphasizes consequences of the redundancy inherent in intersensory compounds, within the theory of Bahrick and Lickliter.     

The resistance of renewal to instructions that devalue the role of contextual cues in a conditioned suppression task with humans

The renewal of extinguished conditioned behaviour appears to reflect context-dependent learning. The present research used a conditioned suppression task with humans to examine whether instructions concerning the context could influence renewal. Pairings of a conditional stimulus (CS) and unconditional stimulus (US) were made in one context, followed by extinction trials of CS alone in a second context, and test trials of CS alone upon return to the original learning context. Four experiments tested whether the renewal of conditioned suppression observed during test would be attenuated if participants were instructed that the context changes were irrelevant to the predictive relationship between the CS and US. Using a differential conditioning design, no attenuation was found when the instructions were given prior to conditioning (Experiment 1) or immediately prior to the test trials (Experiment 2). The latter result was replicated with a single-cue conditioning design and further controls for exposure to the extinction contexts (Experiment 3). The collection of on-line ratings about the relationship between the contextual changes and the predictive nature of the CS indicated that participants did attend to and believe the instructions (Experiment 4). The results point to the resistance of renewal to explicit instructions that attempt to devalue the role of the contextual cues.     

Reinstatement of fear to an extinguished conditioned stimulus: two roles for context

The authors studied the role of context in reinstatement. Freezing was reinstated when the conditioned stimulus (CS) was extinguished in 1 context and rats moved to another context for reexposure to the shock unconditioned stimulus (US) and test. It was also reinstated (rather than renewed) when rats were shocked in the extinction context and moved to another context for test. This reinstatement was CS specific and reduced by nonreinforced exposures to the extinction context. Rats shocked in the context in which a stimulus had been preexposed froze when tested in another context. These findings suggest 2 roles for context in reinstatement: conditioning of the test context (M. E. Bouton, 1993) and mediated conditioning by the extinction context (P. C. Holland, 1990).     

The comparator hypothesis of conditioned response generation: manifest conditioned excitation and inhibition as a function of relative excitatory strengths of CS and conditioning context at the time of testing

In the present research water-deprived rats were used in a conditioned lick suppression paradigm to test and further develop Rescorla's (1968) contingency theory, which posits that excitatory associations are formed when a conditioned stimulus (CS) signals an increase in unconditioned stimulus (US) likelihood and that inhibitory associations develop when the CS signals a decrease in US likelihood. In Experiment 1 we found that responding to a CS varied inversely with the associative status of the context in which the CS was trained and that this response was unaltered when testing occurred in a distinctively dissimilar context with a different conditioning history, provided associative summation with the test context was minimized. These results suggest that manifest excitatory and inhibitory conditioned responding is modulated by the associative value of the training context rather than that of the test context. In Experiment 2 it was demonstrated that postconditioning decreases in the associative value of the CS training context reduced the effective inhibitory value of the CS even when testing occurred outside of the training context. Moreover, this contextual deflation effect was specific to the CS training context as opposed to any other excitatory context. Collectively, these studies support the comparator hypothesis, which states that conditioned responding is determined by a comparison of the associative strengths of the CS and its training context that occurs at the time of testing rather than at the time of conditioning. This implies that all associations are excitatory and that responding indicative of conditioned inhibition reflects a CS-US association that is below (or near) the associative strength of its comparator stimulus. It is suggested that response rules which go beyond a monotonic relation between associative value and response strength can partially relieve learning theories of their explanatory burdens, thereby allowing for simpler models of acquisition.