One-trial context fear conditioning with immediate shock: The roles of transport and contextual cues

In three experiments, using a total of 120 albino rats, we assessed whether transportation cues might evoke some of the freezing (i.e., defensive immobility) that we see in a context on a day following a footshock given immediately after placement in that context. The results suggested that immediate shock could directly condition strong fear to both simulated and actual transport cues. Although conditioning to transport cues explains some of the freezing that is seen on the test day, it does not explain all of it. We also found evidence that some of the freezing is due to conditioning to permanent features of the context in which the immediate shock is given. The results support a role for transport cues in theories of context conditioning and argue against shock-processing accounts of the conditioning deficit that results from immediate shock.     

Factors governing one-trial contextual conditioning

When a rat was placed in a chamber and shortly thereafter received a single footshock, it showed conditional freezing upon re-exposure to that chamber but not a different one (Experiment 1). Experiments 2–4 showed that the probability of this freezing decreased linearly with decreases in the delay between placement in the chamber and shock delivery. With very short delays (e.g., less than 27 sec), there was no freezing. Experiments 2 and 3 demonstrated that a 2-mm pre-exposure to the chamber, 24 h prior to shock delivery, reduced the minimum delay necessary to successfully condition freezing. Experiment 4 demonstrated that shorter delays were successful in conditioning freezing if a salient tone was a component of the contextual stimulus. The changes in freezing caused by delay interval and preexposure did not simply reflect the total time in the context, suggesting that there may be two requirements that place temporal restrictions on the conditioning of the freezing response. One is satisfied by sufficient exposure, whether or not that exposure is contiguous with shock. The second requirement is for a small amount of context exposure that is contiguous with shock.     

Pavlovian conditioning to contexts that precede the place where shock occurs as measured by freezing and activity suppression in mice

Three experiments were conducted to demonstrate that the place where an organism has been, before the organism is moved to a place with aversive consequences, can also become aversive through classical conditioning. In Experiment 1, two groups of 8 mice were exposed to three different contexts in succession, with a single shock occurring in the third context. The distal context was a putative 3-min conditioned stimulus (CS) for freezing; the second context was a delay manipulation; and the unconditioned stimulus (US) occurred in the proximal context. The group delayed for 15 sec showed significantly more freezing to the distal CS context than did the group delayed for 3 h. In a second experiment, conditioning to the distal context was demonstrated with a discrimination procedure for 8 more mice by using two different distal contexts as CS+ and CS? for the proximal context with shock. On CS+ days, 3 min of exposure to the distal context was followed within 5 sec by placement in the proximal box where shock occurred, whereas on CS? days, exposure to a second distal context was followed immediately by return to the home cage. Very strong differences in freezing between the CS+ and CS? distal contexts were found in all 8 mice after 14 days of conditioning. In a third experiment, the discriminative procedure was repeated for 9 more mice, with two changes. More objective stabilometertype activity measures were substituted for observed freezing, and, in addition to the CS+ and CS? distal context trials, each mouse was also exposed to a third discriminative distal context, which was followed by 15 min in a delay chamber followed by shock in the proximal context. This discrimination procedure with the activity suppression measure again resulted in significant differences between the contexts. The CS+ context and the context followed by a 15-min delay did not differ, but both of them differed from the CS? context.     

Reinstatement of fear to an extinguished conditioned context

Rats were shocked in the black but not the white compartment of a shuttlebox and then exposed to the black compartment in the absence of the shock unconditioned stimulus (US) to extinguish fear responses (passive avoidance). In five experiments, rats were then shocked in a reinstatement context (distinctively different from the shuttlebox) to determine the conditions that reinstate extinguished fear responding to the black compartment. Rats shocked immediately upon exposure to the reinstatement chamber failed to show either reinstatement of avoidance of the black compartment or fear responses (freezing) when tested in the reinstatement chamber. In contrast, rats shocked 30 sec after exposure to the reinstatement chamber exhibited both reinstatement of avoidance of the black compartment and freezing responses in the reinstatement chamber (Experiment 1). Rats shocked after 30 sec of exposure to the reinstatement chamber but then exposed to that chamber in the absence of shock failed to exhibit reinstatement of the avoidance response and did not freeze when tested in the reinstatement chamber (Experiment 2). Rats exposed to a signaled shock in the reinstatement chamber and then exposed to that chamber in the absence of shock also failed to exhibit reinstatement of the avoidance response (Experiment 5). These rats showed fear responses to the signal but not to the reinstatement chamber. Finally, rats exposed for some time (20 min) to the reinstatement chamber before shock exhibited reinstatement of the avoidance response but failed to freeze when tested in the reinstatement chamber (Experiments 3 and 4). These results are discussed in terms of the contextual conditioning (Bouton, 1994) and the US representation (Rescorla, 1979) accounts of postextinction reinstatement.     

Inhibition of exploratory behavior in the rat by handling

The effect of tail-handling on exploratory behavior of the rat, measured as step-through latency in a well-lighted, two-box apparatus, was investigated. Male adult Wistar rats, aged 60 days, were employed in all three experiments. Experiment 1, in which the subjects were handled at different times after entering the goal chamber (0, 10, 30, 60, 300, and 600 sec), showed that immediate handling, relative to detention in the goal chamber (delay of handling) had an inhibitory effect on exploration. Experiment 2 showed that groups handled immediately after entering the goal chamber but then detained there for different durations all showed the same progressive inhibition of exploration. Experiment 3 showed that the inhibition of exploration (very long step-through latencies) due to tail-handling immediately after entering the goal chamber could be significantly decreased by further trials in which handling was delayed for a sufficient duration (30 sec or more). Handling is discussed as a stimulus that is aversive enough to elicit conditioned passive-avoidance responses (inhibition of exploratory behavior), although it is subject to rapid extinction.     

Immediate shock,passive avoidance,and potentiated startle: Implications for the unconditioned response to shock

Three experiments were performed to study the immediate-shock freezing deficit, a deficit in freezing in rats that results when electric shock is delivered immediately upon exposure to a novel context. This deficit was accompanied by failures to detect evidence of passive avoidance (Experiment 1) or potentiation of the auditory startle response (Experiment 2). The deficit in freezing was attenuated by preexposure to the shocked context (Experiment 3). The results support the view that fear-related behaviors are activated by signals for shock rather than by shock itself. They also suggest that the immediate-shock freezing deficit is due to a failure to process the to-be-conditioned contextual cues (Fanselow, 1986a, 1990).     

Counterconditioning of shock by a water reinforcer in rabbits

Three experiments studied the counterconditioning of certain properties of eyeshock in rabbits by establishing the shock as an appetitive CS for a jaw-movement response reinforced by intraoral water injections in a Pavlovian conditioning procedure. Although Experiment 1 demonstrated that such appetitive conditioning did not attenuate the unconditioned eyeblink elicited by the shock, it reduced the capacity of the shock to suppress leverpress responses reinforced by direct water injections in a signaled punishment procedure in Experiment 2. By contrast, when instrumentally reinforced licking was punished by eyeshock in Experiment 3, no such reduction in the suppressive capacities of the shock was found. The results were considered in terms of whether counterconditioning alters the response-eliciting or motivational and reinforcing properties of the shock.     

Context specificity of conditioning in flavor-aversion learning: Extinction and blocking tests

In three experiments using rats as subjects, we investigated the degree to which a conditioned flavor aversion transfers from one context to another. Experiment 1, using a one-trial conditioning procedure, found no effect of a change of context on a conditioned aversion. Experiment 2 employed a multitrial procedure and demonstrated that a conditioned aversion was extinguished more rapidly after a change of context. Experiment 3 showed that context change decreased the effectiveness with which a conditioned flavor could block acquisition of an aversion by a second flavor. It is argued that these data cannot be explained in associative terms, and that they constitute evidence of conditionality in a simple aversive conditioning procedure.     

CS modality,context conditioning,and conditioned freezing

Two studies used a one-trial-a-day aversive conditioning procedure with rats as subjects to investigate the effects of a noise versus a light CS on conditioned freezing. Experiment 1 demonstrated that less conditioned freezing was elicited by the light, although the two CSs led to similar levels of freezing to the contextual cues of the conditioning chamber. Experiment 2 replicated these outcomes and showed that the manipulation of CS intensity produced results similar to those of modality, with the more intense CSs eliciting less freezing. The second experiment also determined that freezing to contextual cues resulted from context conditioning. According to the Rescorla-Wagner model, CSs that condition poorly should generate little competition with context conditioning. Since neither the modality nor intensity factor reliably influenced context conditioning, as measured by context-evoked freezing, the studies provide no support for the view that the effects on CS-evoked freezing represent differences in the strength of conditioning to the various stimuli. This finding raises the possibility that all of the CSs conditioned well but varied in their abilities to elicit freezing because they differed in terms of the form of defensive behavior under their control.     

The role of US novelty in retention interval effects in single-element taste-aversion learning

Retention interval effects are seen in taste-aversion learning when single-element aversions are significantly weaker 24 h after conditioning compared with tests at later intervals. This report contains three experiments which suggest that the source of the increased drinking at the 1-day interval is nonassociative interference produced by the novel conditioning episode. In Experiment 1, a parametric analysis demonstrated that aversion strength increased monotonically over a 30-h period following conditioning, and that by 48 h after conditioning it was stabilized. In Experiment 2, a single US preexposure was used to reduce the novelty of the US prior to conditioning. As a result, animals preexposed to the US had stronger taste aversions than did non-preexposed controls at a 1-day retention interval; however, no differences were seen at a 5-day interval. Experiment 3 investigated whether the counterintuitive outcome of Experiment 2 was due to the summation of environment-illness and taste-illness associations at the 1-day test. The results ruled out the summation argument; the US preexposure did not need to be presented in the conditioning context to strengthen the aversion at the 1-day interval. Collectively, these results suggest that the presentation of a surprising US can interfere with the retrieval of the taste-illness association for a short period after conditioning, and that this contributes to the retention interval effect.     

Escape acquisition following inescapable shock in the rat

Male rats which had received approximately 21 min of pulsed, inescapable tail shock during a 6-h session in a wheel-turn chamber were markedly deficient in acquisition of an FR 2 crossing escape response in a shuttlebox when first tested 22 or 70 h later (Experiments 1 and 2). Rats which had received identical amounts and patterns of escapable/avoidable shock, however, were not deficient (Experiment 1). Preventing wheel-turn responses during the inescapable shocks prevented the occurrence of the subsequent escape deficit, whereas reducing the feedback provided for the first crossing response of the FR 2 requirement enhanced the deficit (Experiment 3). These data can be best explained by the learned helplessness hypothesis and indicate that the types of responses available and made during the inescapable shocks are more important than previously indicated.     

Contribution of conditioned opioid analgesia to the shock-induced associative US-preexposure deficit

The modulatory effect of conditioned opioid analgesia on learning in the US-preexposure paradigm was examined in three experiments using water-deprived rats. In Experiment 1, it was found that tailflick latencies increased immediately after the rats were exposed to a context in which footshock had previously been administered. Prolonged nonreinforced exposure to the context attenuated this analgesia. Experiment 2 tested the possibility that the effectiveness of CS-US pairings in an excitatory context might be reduced by a conditioned analgesic response that lessens the perceived intensity of the US. Administration of the opiate antagonist naloxone prior to CS-US pairings in the excitatory context reduced the US-preexposure deficit—that is, the retarded response to the CS—but did not eliminate it, suggesting that part of the observed deficit resulted from conditioned activation of the endogenous opioid system. In Experiment 3, it was found that exposure to the excitatory context immediately prior to a CS-US pairing in an associatively neutral context resulted in a conditioned response deficit, indicating that the analgesia elicited by the excitatory context was sufficient to reduce US effectiveness. In combination with other recent reports, these results suggest that the associative deficit resulting from preexposure to a shock US may, in certain instances, represent the sum of several different associative processes.     

A Pavlovian analysis of food-attraction conditioning in the snailHelix aspersa

Following brief pairing of an odor with a feeding experience (food-attraction conditioning), snails will lower their tentacles when subsequently presented with that odor alone. Three experiments investigated the possible behavioral mechanism mediating food-attraction conditioning in the snailHelix aspersa. It is suggested that food-attraction conditioning is an example of Pavlovian conditioning. In this case, the odor (conditioned stimulus) is paired with oral stimulation (unconditioned stimulus), which elicits lowering of the tentacles (unconditioned response). Following conditioning, the odor comes to elicit lowering of the tentacles (conditioned response). Experiment 1 ruled out nonassociative effects, such as habituation and sensitization, using an unpaired control group. Experiment 2 provided further evidence against a role for habituation of neophobia, through the demonstration of extinction following conditioning. In Experiment 3, an omission procedure was used to rule out the possible role of instrumental contingencies.     

Local context and the comparator hypothesis

“Comparator” accounts of associative conditioning (e.g., Gibbon & Balsam, 1981; Miller & Matzel, 1988) suggest that performance to a Pavlovian CS is determined, by a comparison of the US expectancy of the CS with the US expectancy of general background cues. Recent research indicates that variation in the excitatory value of cues in the local temporal context of a CS may have a profound impact on conditioned responding to the CS (e.g., Kaplan & Hearst, 1982), implicating US expectancy based on local, rather than overall, background cues as the critical comparator term for a CS. In two experiments, an excitatory training context attenuated responding to a target CS. In Experiment 1, the context was made excitatory by interspersing unsignaled USs with target CS-US trials. In this case, posttraining extinction of the conditioning context restored responding to the target CS. In Experiment 2, the target CS’s local context was made excitatory by the placement of excitatory “cover” stimuli in the immediate temporal proximity of each target CS-US trial. In this experiment, posttraining extinction of the proximal cover stimuli, not extinction of the conditioning context alone, restored responding to the target CS. An observation from both experiments was that signaling the otherwise unsignaled USs did not appear to influence the associative value of the conditioning context. The results are discussed in relation to a local context version of the comparator hypothesis and serve to emphasize the importance of local context cues in the modulation of acquired behavior. Taken together with other recent reports (e.g., Cooper, Aronson, Balsam, & Gibbon, 1990; Schachtman & Reilly, 1987), the present observations encourage contemporary comparator theories to reevaluate which aspects of the conditioning situation comprise the CS’s comparator term.     

Stimulus control of immunization against chronic learned helplessness

Two experiments investigated the effectiveness of multiple (five) sessions of signaled eseapable-shock pretraining in preventing (immunizing against) the shack-escape impairment produced by an equal number of sessions of signaled inescapable shock. In Experiment 1, rats were exposed to 50 pairings per session of a white-noise stimulus with escapable shock during the immunization phase. Subsequently, they were exposed to 50 pairings per session of a different (houselight) stimulus with inescapable shock. Shock-escape performance in a shuttlebox test with constant illumination revealed no evidence of immunization relative to the performance of rats given five prior sessions of light-signaled inescapable shock only. Experiment 2 was identical in all respects to Experiment 1, except that both the escapable- and the inescapable-shock phases for animals in the immunization treatment group involved the same stimulus (houseüght) as a shock signal. Under these circumstances, the prior escapable-shock training significantly reduced the shuttle-box escape deficit engendered by chronic exposure to signaled inescapable shock; performance in the shuttle-box was not reliably different from that of rats exposed to signaled escapable shock alone. These findings suggest that, under chronic conditions, the development of stimulus control using Pavlovian conditioning procedures may serve to modulate the normally prophylactic influence on later shock-escape acquisition of serial exposure to escapable and inescapable shocks.     

The dual role of the context in postpeak performance decrements resulting from extended training

The context??s role in Pavlovian conditioning depends on the trial spacing during training, with massed trials revealing a function akin to that of discrete stimuli, and spaced trials revealing a modulatory function (Urcelay & Miller, Journal of Experimental Psychology. Animal Behavior Processes, 36, 268?C280, 2010). Here we examined the contextual determinants of a common but largely ignored effect: attenuated conditioned responding with extended reinforced training (i.e., a postpeak performance deficit [PPD]). Contextual sources of PPDs were investigated in four fear-conditioning experiments with rats. In Experiment 1, as the number of reinforced trials increased, conditioned responding decreased, even when testing occurred outside the training context. Experiment 2 revealed opposing influences of context on the PPD based on trial spacing, which interacted with whether testing occurred in the training context. This finding reconciles Experiment 1??s results with previous data (Bouton, Frohardt, Sunsay, Waddell, & Morris, Journal of Experimental Psychology. Animal Behavior Processes, 34, 223?C236, 2008). Experiment 3 suggested that extended training with these parameters did not lead to habituation to conditioned or unconditioned stimuli. In Experiment 4, few or many massed training trials were followed orthogonally by context extinction or no context extinction. After many pairings, context extinction reduced the PPD (i.e., enhanced responding), suggesting a competitive role of the context. These results, together with prior data suggesting that context modulates expressions of the PPD, are consistent with the view that contexts can play two distinctly different roles.     

The US-preexposure effect in honeybees

Signaled avoidance was studied in individual honeybees that visited the laboratory regularly to take sucrose solution from a target set on the sill of an open window. During feeding, substrate vibration or airstream was used to signal a brief shock that could be avoided by breaking off contact with the food for a few seconds. Aversive conditioning of the context was measured in terms of return time (the time between successive visits). In Experiment 1, experience with unsignaled shock was found to lengthen return time—which experience with signaled shock did not—and to impair performance in subsequent avoidance training with signaled shock (the US-preexposure effect). In Experiment 2, experience with unsignaled shock given after signaled avoidance training lengthened return time but had no effect on response to the signal in a subsequent extinction test. These results closely resemble the results obtained in analogous experiments with vertebrates.     

Retrieval practice after multiple context changes,but not long retention intervals,reduces the impact of a final context change on instrumental behavior

Recent evidence from this laboratory suggests that a context switch after operant learning consistently results in a decrement in responding. One way to reduce this decrement is to train the response in multiple contexts. One interpretation of this result, rooted in stimulus sampling theory, is that conditioning of a greater number of common stimulus elements arising from more contexts causes better generalization to new contexts. An alternative explanation is that each change of context causes more effortful retrieval, and practice involving effortful retrieval results in learning that is better able to transfer to new situations. The current experiments were designed to differentiate between these two explanations for the first time in an animal learning and memory task. Experiment 1 demonstrated that the detrimental impact of a context change on an instrumental nose-poking response can be reduced by training the response in multiple contexts. Experiment 2 then found that a training procedure which inserted extended retention intervals between successive training sessions did not reduce the detrimental impact of a final context change. This occurred even though the inserted retention intervals had a detrimental impact on responding (and, thus, presumably retrieval) similar to the effect that context switches had in Experiment 1. Together, the results suggest that effortful retrieval practice may not be sufficient to reduce the negative impact of a context change on instrumental behavior. A common elements explanation which supposes that physical and temporal contextual cues do not overlap may account for the findings more readily.     

Context effects on conditioning,extinction, and reinstatement in an appetitive conditioning preparation

Three experiments with rat subjects examined the effects of contextual stimuli on performance in appetitive conditioning. A 10-sec tone conditioned stimulus (CS) was paired with a food-pellet unconditioned stimulus (US); conditioning was indexed by the observation of headjerking, a response of the rat to auditory stimuli associated with food. In Experiment 1, a context switch following initial conditioning did not affect conditioned responding to the tone; however, when the response was extinguished in the different context, a return to the original conditioning context “renewed” extinguished responding. These results were replicated in Experiments 2 and 3 after equating exposure to the two contexts (Experiment 2) and massing the conditioning and extinction trials (Experiment 3). The results of Experiment 1 also demonstrated that separate exposure to the US following extinction reinstates extinguished responding to the tone; this effect was further shown to depend at least partly on presenting the US in the context in which testing is to occur (Experiments 2 and 3). Overall, the results are consistent with previous data from aversive conditioning procedures. In either appetitive or aversive conditioning, the context may be especially important in affecting performance after extinction.     

Maintenance of responding when reinforcement becomes delayed

In four experiments with rats, we examined the persistence of behavior when reinforcement was switched from immediate to delayed. In Experiment 1, lever pressing elicited by instrumental training with immediate reinforcement continued when a 20-sec delay of reinforcement was introduced (easy-to-hard condition), whereas when the delay condition was introduced from the start (hard-to-hard condition), responding remained low throughout. A similar result was obtained in Experiment 2, in which lever pressing was elicited by a classical conditioning (autoshaping) procedure. In Experiment 3, rats initially trained with delayed reinforcement continued to respond at a low rate when switched to immediate reinforcement (hard-to-easy condition). By measuring magazine entry (goal tracking) as well as lever pressing (sign tracking) in Experiment 4, we confirmed that such transfer effects at least partly involve the persistence of whatever type of behavior was initially dominant.