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.     

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.     

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.     

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.     

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.     

Role of exteroceptive background context in taste-aversion conditioning and extinction

In two experiments, saccharin (CS) and lithium chloride (US) were paired in a context consisting of specific visual, auditory, tactual, and olfactory cues. The saccharin aversion was then extinguished in a context free from conditioning-context cues. Later, saccharin preference tests were given in the presence and absence of these cues. The results indicated that the background cues of the conditioning trial controlled the amount of saccharin drunk on extinction trials, and, furthermore, that extinction of the taste aversion was context specific; i.e., groups given extinction trials in a different (from conditioning) context retained their saccharin aversion in the conditioning context only. The results indicate an important role played by the exteroceptive context in taste-aversion conditioning.     

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).     

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.     

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.     

The learned function of food-deprivation cues: A role for conditioned modulation

Rats trained in one context to use stimuli arising from food deprivation as discriminative signals for shock were tested in other contexts to assess the basis of conditioned responding (i.e., freezing or behavioral immobility). In Experiment 1, discriminative control by 24-h food-deprivation cues failed to promote transfer responding in a test context that had no association with shock. This indicated that food deprivation cues had little direct excitatory power. However, transfer of behavioral control by 24-h food-deprivation cues was obtained in a context paired with shock only when the rats were 19 h water deprived. This finding agrees with the idea that food-deprivation cues become conditioned modulators of the capacity of external stimuli to activate their association with an unconditioned stimulus. In Experiment 2, rats trained to use 24-h food-deprivation cues as signals for shock exhibited significantly greater transfer performance when the transfer context had undergone partial extinction relative to when the transfer context had undergone only simple excitatory training. This finding with deprivation cues and transfer contexts (1) paralleled earlier results obtained with discrete (auditory and visual) conditioned modulators and transfer targets, and (2) posed difficulties for associative summation and generalization interpretations of transfer performance.     

Latent inhibition of the conditioning context: Further evidence of contextual potentiation of retrieval in the absence of appreciable context-US associations

Previous research in our laboratory has found superior performance when classically conditioned responses are observed in the training context as opposed to outside it, even when direct context-US associations have been minimized by either the choice of conditioning parameters or extinction to the context. The present experiment used latent inhibition of the conditioning context as an alternative method of examining contextual cue effects in the absence of appreciable direct context-US associations. Water-deprived rats received tone-footshock pairings in one of two distinctly different apparatuses, but all were tested in a common apparatus. Animals conditioned in the test enclosure displayed more lick suppression than those conditioned outside the test enclosure. Other animals tested without the tone present also exhibited more suppression if conditioning had occurred in the test context rather than outside it, indicating that direct associations between the conditioning context and shock had been formed. However, when formation of direct associations to the conditioning context was attenuated in additional animals through extensive preexposure to the context prior to conditioning, more suppression to the tone was still seen when conditioning had occurred in the test context rather than outside it. These results add support to the position that the training context augments recall even when direct associations between the context and the US are attenuated. The phenomenon is discussed in terms of facilitated retrieval of nominal CS-US associations, configural retrieval cues, and conditional discriminations.     

Contextual associations in trace conditioning

Rats were given tone-footshock pairings with a 0-, 10-, or 30-sec trace interval between tone offset and shock onset. Half the rats within each trace interval were tested for their conditioned fear of the tone through a lick suppression procedure; the remaining rats were evaluated for their fear of the background or contextual cues through their avoidance of the compartment in which conditioning had occurred. Less conditioning was observed to the tone with increasing trace intervals. However, conditioned fear of the context increased with increases in the trace duration. The ability of the more predictive stimulus, the tone, to overshadow the contextual cues was determined by the tone’s temporal contiguity with the footshock. The need to incorporate temporal parameters within current theories of conditioning is discussed.     

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.     

Factors affecting rats’ location during conditioned suppression training

If freezing underlies barpress conditioned suppression, then it seems odd that auditory cues paired with shock evoke more freezing than do visual cues, yet evoke similar suppression. Bevins and Ayres (1992) found that auditory and visual cues also evoked similar withdrawal from the bar and dipper areas and suggested that such withdrawal could explain the similar suppression. Seeking to understand that withdrawal, we found evidence in the present study that it was due either to adventitious punishment or to place-aversion learning. The cue for shock seemed to set the occasion for such learning. For example, we found that, as training progressed, rats’ tendency to leave the bar area during the cue first increased, then decreased, then increased again, reflecting, presumably, shock occurrence first inside, then outside, then inside the bar area again. Despite these changes in the rats’ location, barpress suppression remained stable, implying that leaving the bar area, though sufficient for barpress suppression, is unnecessary.     

Nonassociative habituation,US preexposure,and backward inhibitory conditioning with signaled and unsignaled USs

In a conditioned suppression experiment, rats received a single, massed session of conditioning in which one backward conditioned inhibitory stimulus (CS-) followed shocks that were signaled by a visual cue, and a second backward CS-followed shocks that were unsignaled. Conditioning was preceded by a preexposure phase in which some groups of rats were preexposed to unsignaled shock, while others were not preexposed and remained in the experimental apparatus in the absence of shock. The groups were further distinguished by whether US preexposure and conditioning occurred in the same or different contexts, and by whether conditioning began immediately or after a 24-h rest period in the home cage. Although the conditioning itself was effective in establishing the visual cue as a conditioned excitor in the nonpreexposed groups, it was not effective in establishing the two backward cues as reliable inhibitors with either signaled or unsignaled USs. After 210 US preexposures, however, the same conditioning sessions did yield conditioned inhibition to both CS-s. A 24-h rest period in the home cage reduced the magnitude of, but did not completely abolish, the facilitative effect of US preexposure on inhibitory conditioning. Other tests demonstrated that US preexposure had retarded excitatory conditioning to the visual cue. This interference with excitatory conditioning was unchanged in magnitude after the 24-h rest period. The facilitative effect of US preexposure on backward inhibitory conditioning, and the interference effect on excitatory conditioning, were both eliminated by a change in context between US preexposure and conditioning. These observations encourage predominantly associative accounts of the effects, but allow for a small nonassociative habituation component.     

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.     

Rats’ location during conditioned suppression training

Freezing is often cited as the interfering behavior responsible for barpress conditioned suppression. However, auditory cues that precede shock can evoke more freezing than can visual cues despite producing similar suppression. In two experiments, we sought to resolve this paradox by measuring rats’ location in the box in addition to recording freezing during conditioned-suppression training to tones and lights. Tone evoked more freezing than light but similar suppression. During both cues, rats left the bar and dipper areas and moved to the lower middle and rear of the box. When the bar was then removed and the dipper entry sealed, the preference for the middle and rear of the box disappeared. Apparently, frightened rats do not simply prefer the middle and rear of our box. The fact that rats leave the bar and dipper areas equally during both auditory and visual cues explains how the two cues can foster similar suppression despite evoking different levels of freezing. But the fact that rats leave the bar and dipper areas at all remains to be explained.     

Conditioned fear assessed by freezing and by the suppression of three different baselines

Rats received either forward or backward pairings of an auditory CS and shock. They were then tested for conditioned suppression to the CS while barpressing for food, licking a sucrose solution, or being spontaneously active. Behavior was simultaneously observed using a time-sampling method. In each case, forward-conditioned animals exhibited more freezing than controls, and freezing was reliably correlated with suppression of the baseline. These results suggest that the different loss-of-baseline measures of aversive conditioning reflect the amount of defensive behavior evoked by the CS. They also suggest the utility of freezing as an index of conditioning. Freezing assayed by the time-sampling method was comparable to the more conventional indices of conditioning in sensitivity to the effects of conditioning.     

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.     

The effect of predictive cues on freezing in rats

Rats were given five shocks over a 5-min period and then observed for 20 min. Much more freezing was observed in animals that remained in the shock situation than in animals moved to another situation. Freezing, therefore, seems to be controlled primarily by external shock-related cues. Freezing appears to be also partly controlled by the inherent stimulus properties of the situation.