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.     

Extinction of a saccharin—lithium association: Assessment by consumption and taste reactivity

Extinction of a conditioned palatability shift preceded extinction of conditioned taste avoidance whether rats were tested using a within-subjects design or a between-subjects design. In each of two experiments, consumption of 0.1% saccharin was paired with either 20 ml/kg of 0.15 M LiCl or equivolume physiological saline on a single trial. In Experiment 1, on each of 10 extinction trials, rats were given a taste reactivity test immediately prior to a consumption test. In Experiment 2, half of the rats were extinguished by taste reactivity testing and half of the rats were extinguished by a consumption test on each of 10 extinction trials. In both experiments, the aversive reactions of gaping and passive dripping were extinguished in a single trial and the suppression of ingestive reactions was extinguished in 2 trials; however, extinction of taste avoidance required 4–5 trials. These results suggest that rats continue to avoid a lithium-paired flavor even when they do not have an aversion to the taste.     

The relationship between shock magnitude and passive avoidance learning

Three experiments examined the relationship between shock magnitude and the rate of acquisition of a passive avoidance response. Experiment 1 indicated that the use of a relatively large magnitude of shock can disrupt learning to remain on a platform in the center of an open field to avoid shock. The inferior learning of the group trained with high shock was replicated in Experiment 2, which also demonstrated that avoidance learning can occur rapidly with this level of shock if the platform is located in the corner of the apparatus. To explain this, it was proposed that thigmotactic behavior is responsible for the disruption in avoidance behavior when training is conducted in the center with high-magnitude shock. Finally, Experiment 3, essentially a replication of Experiment 1 except that the platform was placed in the corner of the test compartment, demonstrated a direct relationship between shock magnitude and passive avoidance learning. The results are seen as being consistent with accounts which maintain that avoidance learning can be influenced by the occurrence of species-specific defense reactions.     

Avoidance differences between rats and gerbils

Gerbils and rats learned equally well to discriminate the lighted, safe arm from the unsafe arm during Y-maze avoidance trials. Gerbils, however, were inferior to rats in initiating this response in time to avoid shock. Two subsequent experiments on passive avoidance did not support the interpretation of these data based on a greater incidence of shock-induced activity suppression in gerbils. In both experiments, gerbils required more shocks than rats to learn a staying response, indicating a pronounced locomotor response bias in gerbils that is not compatible with the required passive avoidance response. A fourth experiment, using a shuttlebox, found that the relative active avoidance performance by these species depends upon whether intertriai responses are permitted and punished. When they are, gerbils are inferior to rats, since their high level of locomotor responding is not compatible with the behavior required, i.e., staying during the intertrial interval and running during the CS-US interval. On the other hand, gerbils are not inferior when intertrial responses are prohibited, since their locomotor bias is not punished and is compatible with the required avoidance response.     

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).     

Conditioned defensive burying in rats free to escape

Rats shocked once by a stationary, wire-wrapped prod bury it if suitable materials are available. Does this conditioned defensive burying occur when rats have the opportunity to flee from the source of aversive stimulation, or is it limited to situations such as those in which it had previously been studied—those in which the relatively small test chamber confined each rat to the immediate vicinity of the prod? In the present experiments, the capacity of rats to flee from the shock prod was enhanced by increasing the floor dimensions of the test chamber up to 200X80 cm (Experiment 1) or by providing the rats with an opportunity to seek refuge in a separate, safe compartment (Experiment 2). Although both of these modifications to the usual conditioned-defensive-burying paradigm significantly reduced the duration of burying and the height of the accumulated mounds, burying remained well above control levels in all experimental conditions.     

Control over noxious events and choice

Three experiments are reported assessing whether rats prefer controllable over uncontrollable aversive shock. In Experiment 1, subjects chose between escapable and inescapable shock while relative shock duration varied parametrically. In Experiment 2, subjects again chose between escapable and inescapable shock, but duration was held constant and equal. The final experiment gave subjects a choice between avoidable and unavoidable shock under several signaling conditions. Choice behavior proved sensitive to relative shock duration and to predictability of shock but not to controllability of shock.     

Ontogeny of step-through passive avoidance learning in domestic chicks: Effects of prepunishment training and cue distinctiveness

In three experiments, 1- and 4-day-old chicks (N=96) were first trained to move from one compartment into another for heat reward, and then, following 1, 24, or 48 prepunishment trials, the chicks’ step-through responses were punished with aversive wing-shocks during 24 passive avoidance (PA) trials. The major finding of these experiments was that the age dependency of PA learning of the young chick depends upon both the number of prepunishment trials and the cue differences between the safe and shock compartments. The 1-day-old chick showed an improvement in PA learning as both prepunishment trials and cue differences were increased, but the 4-day-old chicks’ PA learning was retarded by increasing the number of prepunishment trials when either identical or distinct cues were in the two compartments. These PA results suggest that the 1-day-old chick, as compared with the 4-day-old chick, is deficient in learning, or detecting changes in, stimulus- and/or response-reinforcement contingencies.     

Interference with avoidance behavior as a function of qualitative properties of inescapable shocks

Temporal form (continuous vs. pulsating) and shock source (alternating current vs. direct current) were factorially combined to produce four shock treatments. The effects of inescapable presentations of these stimuli on subsequent avoidance response acquisition were measured in dogs (Experiment 1) and in rats (Experiment 2) and revealed an interaction of shock variables. Initially, all groups that received ac shock showed impaired performance for the pulsating and continuous shock conditions; groups that received dc continuous shock were also impaired, while those that received dc pulsating shock were not. While this pattern of interference persisted for dogs, it was transient in rats, with only the ac continuous-shock group continuing to be impaired. Mean avoidance performance were positively related to mean activity levels during inescapable shocks for the dc shock groups but not for the ac shock groups.     

Shuttlebox avoidance to intense white noise: Acquisition and the Kamin effect in rats

Experiment I demonstrated shuttlebox avoidance conditioning using intense white noise as a UCS. Ten rats were given 25 trials a day for 6 days. Escape latencies declined and avoidance responses increased over trial blocks. Experiment II provided support for a functional similarity between shock as a UCS and intense noise as a UCS by demonstrating the Kamin effect following incomplete shuttlebox training to noise. Separate groups of rats were given 25 trials followed by an additional 25 trials either 0, 1, 4, or 24 h later. The U-shaped Kamin effect was evident in the avoidance measure. A similar but inverted U-shaped function was obtained for the escape latency measure. Escape latencies were longer on retraining than on original training at 1 h but not at 0, 4, or 24 h after original training.     

Inescapable shock and food-competition dominance in rats

Inescapable electric shock disrupts escape-avoidance learning in another apparatus. This study demonstrates a deficit in a nonlearning task in which no aversive stimulus occurs. In Experiment 1, inescapable shock lowered rats’ dominance in a food-competition situation relative to restrained controls. In Experiment 2, inescapable shock lowered rats dominance in the same food-competition situation relative to a group that received the equivalent amount of escapable shock, demonstrating that the inescapability of the shock caused at least part of the decrement observed in Experiment 1. Experiment 3 does not find that inescapable shock caused a significant difference in food consumed or running time when the rats were tested alone, showing it unlikely that the dominance effects were caused by decreased hunger or reduced running following inescapable shock.     

Conditions that potentiate the effects of electroconvulsive shock administered 24 hours after avoidance training

Three experiments assessed the conditions that potentiate effects of an electroconvulsive shock (ECS) administered 24 h after avoidance training. Stimuli present immediately prior to the ECS were systematically varied. In Experiment 1, which employed a passive avoidance task, the primary determinant of whether the ECS disrupted retention was whether the situational cues present at the time of ECS delivery were those associated with the initial training experience: ECS disrupted performance only when it was administered in the original training apparatus, regardless of whether or not a footshock was presented immediately prior to ECS. In Experiment 2, which employed an active, shuttlebox avoidance task, both the situational cues from the training apparatus and a footshock were necessary to potentiate the disruptive effects of the ECS. Experiment 3 revealed that ECS effects on performance of the active avoidance task can also be potentiated by a combination of apparatus cues and the warning signal used in initial training. These results are interpreted as indicating that informational functions of stimuli present when an ECS is administered are important determinants of the effects of the ECS.     

Additive summation by stimulus compounding irrespective of behavioral contrast during discrimination training: An investigation with positive reinforcement and avoidance schedules

The similarity in the discrimination training leading to behavioral contrast and that preceding tests producing response enhancement to combined discriminative stimuli suggested that the two phenomena might be related. This was investigated by determining if contrast indiscrimination training was necessary for this outcome of stimulus compounding. Responding to tone, light, and to the simultaneous absence of tone and light (T + L) was maintained during baseline training by food reinforcement in Experiment I and by shock avoidance in Experiment II. During subsequent discrimination training, responding was reduced in T + L by programming nonreinforcement in Experiment I and safety or response-punishment in Experiment II. In the first experiment, one rat exhibited positive behavioral contrast, i.e., tone and light rates increased while his T + L rate decreased. In Experiment II, rats punished in T + L showed contrast in tone and light, this being the first demonstration of punishment contrast on an avoidance baseline with rats. The discrimination acquisition data are discussed in the light of current explanations of contrast by Gamzu and Schwartz (1973) and Terrace (1972). During stimulus compounding tests, all subjects in both experiments emitted more responses to tone-plus-light than to tone or light (additive summation). An analysis of the terminal training baselines suggests that the factors producing these test results seem unrelated to whether or not contrast occurred during discrimination training. It was concluded that the stimulus compounding test reveals the operation of the terminal baseline response associations and reinforcement associations conditioned on these multicomponent free-operant schedules of reinforcement.

     

Conditioning history and inhibitory instrumental stimulus control: Independent-groups and within-subjects measures

The effects of excitatory conditioning history on establishing inhibitory stimulus control have been investigated in classical conditioning, but not in the free-operant paradigm. The present experiments address this question within the context of discriminated free-operant avoidance in which rats’ barpressing postponed shock. When a stimulus with only a history of signaling safety was combined, on a summation test, with a stimulus that maintained avoidance, avoidance rate was reduced, on average, by 60%. In comparison, after a stimulus acquired an excitatory free-operant avoidance history, nonreinforcement alone was not adequate to make it a predictable and effective inhibitor of avoidance on a summation test. These results, consistent with the classical conditioning literature, were produced by both between-group (Experiment 1) and within-subject (Experiment 2) comparisons. These findings are discussed in terms of (1) Konorski’s distinction between “primary” and “secondary” inhibitory stimuli, (2) the Rescorla-Wagner model, (3) the potential contribution of the “reinstatement of fear” to the outcome of summation tests, and (4) their implications for assaying the effectiveness of behavior-modification treatments of phobias.     

Preexposure to situational cues and shock intensity in two-way avoidance learning

Four groups of rats (n = 16) received 65 two-way avoidance learning trials. The groups differed with respect to the amount of exposure (0 or 4 h) to the situational cues of the apparatus prior to avoidance learning and the intensity of shock (.3 or 1.6 mA) during learning. Superior avoidance performance with weak as compared to strong shock was obtained in the nonpreexposed groups. This inverse relationship between avoidance performance and shock intensity, typical of two-way avoidance learning, was eliminated in the preexposed groups. Presumably, a latent inhibition effect occurred in the strong-shock group, which resulted in a retardation of the conditioning of fear to the situational cues and a consequent improvement in performance. The results are consistent with the effective reinforcement theory, which emphasizes in aversive learning the detrimental effect of large amounts of fear remaining following a response.     

Discriminated and nondiscriminated avoidance conditioning of the rearing response in rats

Experiment 1 employed a shock box in which light beams ran at 10, 15, 20, or 25 cm above the floor level of the box. Four groups of nine rats each were trained to avoid shock by cutting the light beams or letting them pass by, which the animal accomplished by upward or downward change of its posture. Training employed a discriminated avoidance paradigm, 60 trials per day for 5 days, with a 5-sec CS-US interval. Acquisition of the rearing avoidance response was observed only in the 15-cm condition. Using the same apparatus as in Experiment 1 and with a beam height of 15 cm, the rearing avoidance response was successfully conditioned in five rats using a nondiscriminated avoidance conditioning paradigm. There was good evidence of temporal discrimination in these animals.     

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.     

Generality of US preexposure effects: Transfer from food to shock or shock to food with and without the same response requirements

A series of four experiments, employing mice, investigated the generality of the learned helplessness phenomenon. The first two experiments used preexposure to aversive stimuli (shock), while the other two used preexposure to appetitive stimuli (food). In all of the studies, subjects were preexposed to contingent, noncontingent, or no stimuli (except for Experiment 2) in a Skinner box. During the test, animals preexposed to shock were tested with food, and those preexposed to food were tested with shock. The test was conducted in a similar situation, a Skinner box (Experiments 1, 3), or a different situation—a runway (Experiments 2, 4). Performance decrements were evident when subjects that were preexposed to a noncontingent stimulus were compared with subjects preexposed to contingent stimuli. The differences between the contingent and the noncontingent groups were significant, as were the differences between the contingent and the nonpreexposed groups (except for Experiment 1). The effects cut across the different types of stimuli, situations, and response requirements of the preexposure and test phases.     

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.     

Aversive, appetitive and flavour avoidance responses in the presence of contextual cues

Appetitive, aversive and avoidance responses to a flavoured solution in distinct contexts were examined. Rats placed in either a white or black box were given access to saccharin. Consumption was followed by an injection of a toxin in one but not the other box. Rats showed more aversive responses in anticipation of and during the presentation of saccharin in the box paired with the toxin than in the box paired with vehicle. The reverse was true for appetitive responses. The acquisition of conditioned avoidance paralleled the acquisition of aversive and appetitive responses. These findings demonstrate that the toxin does not have to overlap exposure to contextual cues to produce conditioned aversive responses, that the aversive and appetitive responses to a flavour can be modulated by visually distinct environments that predict the toxin, and that conditioned avoidance and conditioned aversions develop simultaneously during acquisition. Thus, environmental cues can modulate anticipatory nausea and may prove helpful in the control of nausea in clinical settings.