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.     

Pre-exposure enhances recovery of conditioned responding after extinction

Four experiments used a within-subjects design with rats to study the effects of preexposure on the restoration of fear responses (freezing) to an extinguished conditioned stimulus (CS). In each experiment, rats were preexposed to one CS (A), but not to another (B), and then were exposed to pairings of each of these CSs with an aversive unconditioned stimulus (US). In each experiment, there was less freezing to A than to B across extinction, showing a latent inhibitory effect of preexposure. There was no differential recovery to A and B following either a US reexposure (Experiment 1) or a delay interval (Experiment 2). However, when a delay interval included US reexposure, there was greater recovery to the preexposed CS, A, than to the nonpreexposed CS, B (Experiments 1, 3, and 4). These results suggest that the effects of US reexposure and delay combine to affect recovery from the depressive effects of CS-alone exposure. The results are consistent with the view that US reexposure produces better mediated conditioning of CSs that are strongly associated with the context. The results may additionally reflect an effect of preexposure on the learning produced by extinction.     

Effects of handling and context preexposure on the immediate shock deficit

Theimmediate shock deficit refers to the failure of a shock to become associated with contextual stimuli when the shock is presented simultaneously with the rat’s placement in a context. The basic procedure consists of a presentation of the shock as soon as the animal is placed in an observation chamber. Handling of the animal, which immediately precedes the shock, and the novelty of the chamber in which the immediate shock is delivered are potential variables that might be responsible for this associative deficit. In Experiment 1, handling reduced context conditioning but was not responsible for the immediate shock deficit. Experiment 2 revealed that the novelty of the chamber was not a significant factor. These results discount the possibility that handling and the novelty of the chamber are responsible for the deficit produced by the immediate shock. It is suggested that immediate shock could be employed as a control procedure for the study of context conditioning.     

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.     

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.     

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).     

The postshock activity burst

When a rat receives an electric shock delivered to the floor of an enclosure, it reacts with frenzied activity. On shock termination, the activity persists for a brief period of time and then gradually gives way to a period of freezing. Subsequent grid shocks temporarily disrupt freezing, with the length of disruption determined by shock intensity (Experiment 1). The duration of this activity burst depends predominantly on the test shock intensity but not on the training shock intensity. The reverse is true for the probability of freezing, which is positively related to training shock intensity (Experiment 2). Based on this finding, it is argued that the activity burst is a UR, while freezing is a CR. Further support that freezing is a CR is provided by Experiment 3, which demonstrates that a delay, during which the rat is out of the shock-associated context, between the training and testing periods does not disrupt freezing. A topographical analysis of the behaviors making up the activity burst is provided by Experiment 4. The postshock activity burst was composed predominantly of head movement, turning, and rearing.     

The recency effect in pigeons’ long-term memory

Four experiments are reported in which pigeons first learned one wavelength discrimination (green S+, yellow S?) and then the reversal; finally, after various delays, they were tested for wavelength generalization in extinction. In Experiment 1, the two problems were learned in different contexts; testing in Context 1 produced maximal responding to green in only half of the subjects, even when testing was delayed 30 days. In Experiment 2, testing of the subjects repeatedly in both contexts showed good control by each context after a 30-day delay. In Experiment 3, both problems were learned in the same context, and all gradients showed recency, peaking at yellow, even after 30 days. In Experiment 4, the subjects learned a series of reversals in the same context, terminating in yellow, S+, green, S?, and their gradients peaked at yellow, even after a 30-day delay. In Experiments 3 and 4, the gradients became flatter with increasing delays, and they were flatter in Experiment 4 (after three reversals) than in Experiment 3 (after one reversal). The location of the peak was not affected by delay, but only by testing in a context that had been uniquely associated with Problem 1 (Experiments 1 and 2). It is proposed that the location of gradient peaks indicates what is being remembered, whereas the slope of the obtained gradients indicates how well the target memory has been retrieved.     

Conditioned inhibition of analgesia

Stimuli that predict the occurrence of aversive events come to elicit conditioned analgesia. Experiments 1A and 1B examined the possibility that conditioning can inhibit analgesia when stimuli are paired in a backward fashion with a shock US (Pavlovian CS- s). Analgesia conditioned in response to shock context exposure was reversed during the CS- (light) presentation after four sessions. The ability of the CS- to function as a conditioned inhibitor of analgesia was then evaluated in both summation (Experiment 1A) and retardation-of-acquisition testing (Experiments 1A and 1B). The results support the conclusion that a stimulus presented after shock in a backward fashion comes to be a conditioned inhibitor of analgesia. Experiments 2A and 2B examined the assumption that the results obtained with our pain sensitivity measure (tailflicking in response to radiant heat) reflect changes in responsiveness to painful input, rather than a general motor inhibition or general insensitivity to sensory input. In Experiment 2A, tailflick responding to painful and nonpainful input was compared in animals receiving either morphine or saline. In Experiment 2B, tailflick responding to painful and nonpainful input to the tail was compared in both the shock and a neutral context. In both experiments, only the painful input yielded changes in responsivity. The results support the conclusion that the alterations in pain sensitivity produced by the CS- for shock represents a conditioned inhibition specific to pain.     

Overshadowing of situational cues with variable but not fixed intertrial intervals

In two experiments, we examined the conditions under which signaling an unconditioned stimulus (US) with a nominal conditioned stimulus (CS) interferes with the conditioning of situational cues in defensive freezing in the rat. Subjects received footshock USs that were (1) either signaled or unsignaled and (2) either varied or fixed in their temporal location within the conditioning session. Experiment 1, with only one trial per session, yielded no evidence that signaling affected pretrial freezing using either a fixed or variable interval between placement in the context and shock onset. In a test in which no CSs or footshocks were presented, groups that previously had received footshock at a fixed temporal location showed greatest freezing at around that same time. For groups that had received footshocks at various times, freezing declined across the test session. Experiment 2 showed overshadowing of pretrial freezing after more extensive conditioning with many trials per session, but only if the intershock intervals were variable rather than fixed.     

Super-latent inhibition with delayed conditioned taste aversion testing

In three conditioned taste aversion experiments with rats, latent inhibition (LI) was examined as a function of the time interval (1 or 21 days) between the conditioning and the test phases. In Experiments 1 and 2, the effects of US intensity on LI were examined. LI increased in the 21-day condition, as compared with the 1-day condition, with medium and high US intensity, but not with weak US intensity. Groups not preexposed to the CS flavor had similar aversions when testing was conducted 1 day after conditioning, as compared with 21 days. In Experiment 3A, delay-induced super-LI was obtained when the delay was spent in the home cage and the experimental stages took place in a different context (as in Experiments 1 and 2). In Experiment 3B, when all the stages, including the delay period, were conducted in the home cage, there was no super-LI effect. The modulation of delay-induced super-LI as a function of US intensity and context extinction is discussed in relation to association deficit and retrieval interference theories of LI.     

One-trial context fear conditioning as a function of the interstimulus interval

In two experiments, we examined the effects of a wide range of interstimulus intervals (2.5, 15, 45, 120, 135, and 405 sec) on one-trial context fear conditioning with rats. Here, the interstimulus interval (ISI) denotes the time between placement in a conditioning chamber and the onset of a single footshock. On the conditioning day, we observed that the rats’ behavior at the time of shock onset varied systematically across ISI values. On the subsequent test day, we used context-evoked freezing as a measure of context conditioning and found the well-known inverted U-shaped ISI function. We also found that conditioned freezing for the shortest ISI values was concentrated early in the test session, whereas freezing at longer ISIs was distributed more evenly throughout the test session. The freezing results found here are more consistent with the literature on conditioning with punctate cues than are previously described results from one-trial context fear-conditioning procedures.     

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.     

Serial overshadowing of taste aversion learning by stimuli preceding the target taste

Three experiments tested whether events taking place before a rat has access to a target taste, sucrose, can proactively interfere with the acquisition of a sucrose aversion when sucrose is followed by a lithium chloride injection. Using a serial overshadowing procedure with various delays before lithium injection, proactive interference by a taste (Experiments 1 and 3) and by a novel context (Experiment 2) was found following two conditioning sessions, but not after a single conditioning session. Conversely, overshadowing by a taste given after the target was detectable after a single conditioning trial (Experiment 3) and, thus, indicated that retroactive interference involves a process different from that producing proactive interference. A simulation confirmed that the results are consistent with a modified Rescorla and Wagner (1972) interpretation of Revusky??s (1971) concurrent interference theory of delay learning.     

Slow extinction of conditioned responding following exposure to two bouts of massed shock

Extinction of rats’ conditioned defensive freezing responses in a context associated with two bouts of massed shock (3 sec) separated by a long unreinforced interbout interval was slower than that in a context associated with distributed shock (60 sec). Resistance to extinction following two bouts of massed shock depended on the rats’ remaining undisturbed in the conditioning context during the long unreinforced interbout interval. Slow extinction of freezing was attributed to either the summation of temporal conditioning at the early and late session times or the formation of an association between the early and late bouts of shock. Importantly, the effects of the two bouts of massed shock could not be explained by what is known about the reinforcing effectiveness of massed shock.     

Some determinants of second-order conditioning

In a Pavlovian conditioning situation, an initially neutral stimulus may be made excitatory by nonreinforced presentations in compound with an established conditioned excitor [i.e., second-order conditioning (SOC)]. The established excitor may be either a punctate cue or the training context. In four conditioned suppression experiments using rats, we investigated whether SOC phenomena parallel other cue interaction effects. In Experiment 1, we found that the response potential of a target stimulus was directly related to the intertrial interval when SOC was mediated by a punctate cue, and inversely related to the intertrial interval when SOC was mediated by the training context. Experiment 2 demonstrated that punctate- and context-mediated SOC are oppositely affected by posttraining context extinction, and Experiments 3 and 4 demonstrated that context- and punctate-mediated SOC are differentially affected by conditioned stimulus (Experiment 3) and unconditioned stimulus (Experiment 4) preexposure treatments. These findings parallel phenomena in conditioned inhibition and cue competition situations.     

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.     

Influence of conspecific stress odors and shock controllability on conditioned defensive burying

In Experiment 1, rats received a session of 80 inescapable tail shocks or no shocks while restrained in a tube. During tests of conditioned defensive burying 24 h later, the bedding of the chamber contained odors from either stressed or nonstressed conspecific donor rats. Following a single prod shock, subjects that had had prior shocks or that were tested with the stress odors spent significantly less time burying the prod, made smaller piles of bedding, and displayed more freezing behavior. The combination of prior shock and stress odors during later testing enhanced these effects. In Experiment 2, a yoked group of rats that was given inescapable shocks, in contrast to a group that had wheel-turn escape training and one that was restrained but not shocked, later showed significantly less burying and more freezing when tested for defensive burying with stress odors present. In both experiments the duration of burying and the heights of piles were positively correlated, and both of these measures were negatively correlated with freezing. The demonstrated capacity of unconditioned stress odors to mediate different degrees of fear, depending upon the controllability of prior shock, is related to other studies of learned helplessness, and the predominance of freezing over burying is discussed in terms of various types of defensive strategies, stimulus-control processes, and the author’s stress-coping-fear-defense (SCFD) theory.     

Effects of contextual cues previously paired with footshock or illness on behavior and pain sensitivity in the rat

Rats were used in four experiments to study the effects on behavior and pain sensitivity of exposure to a context previously paired with footshock or injection of the emetic drug lithium chloride (LiCl). Exposure to a context previously paired with footshock or injection of LiCl provoked the species-typical defense response of freezing (Experiments 1A and 1B). Exposure to a context previously paired with footshock additionally produced hypoalgesia when rats were tested using the tailflick test (Experiment 1A). By contrast, exposure to a context previously paired with injection of LiCl produced hyperalgesia when rats were tested using the tailflick test (Experiment 1B). However, exposure to a context previously paired with injection of LiCl did provoke hypoalgesia when rats were tested for pain sensitivity using either the hotplate or formalin tests (Experiment 2), which was mediated by the release of endogenous opioid peptides (Experiment 3). These results are discussed with reference to the processes governing associative regulation of defensive behavior and pain control.