The role of spatial and temporal contiguity in defensive burying in rats

The degree of spatial and temporal contiguity between contact with a prod and shock was varied in three experiments to see how these factors contribute to defensive burying. In Experiment 1, rats shocked once through a grid floor while touching a prod buried the prod just as much as did rats shocked through the prod. Experiment 2 showed that rats either shocked through the floor more than 1 min after touching the prod or shocked in the absence of a prod did not bury the prod. Thus, close temporal contiguity between grid shock and prod contact appears necessary for burying. Nevertheless, grid-shocked rats do learn something different from prod-shocked rats, since they bury the prod less and the walls more than do prod-shocked rats when the position of the prod is changed in the test chamber (Experiment 3).     

Defensive burying in the rat: A behavioral field analysis

Time spent in various behaviors by the rat was recorded in a defensive burying paradigm. Experiment 1 revealed that rats spent more time burying the shock prod than a control prod and that doubling the size of the test chamber did not have a significant effect on the time spent in any behavior. In Experiment 2, the location of bedding material in a two-compartment test chamber was found to affect the occurrence of burying (both the shock and control prods) and burrowing behavior. Burying did not occur when bedding was not available in the shock compartment but was located in the escape compartment. Burrowing was more likely to occur when bedding was in both compartments than when it was in only one compartment. Immobility and escape latencies were shorter than burying latencies in all subjects. Burying was viewed as belonging to a second stage of defensive behavior.     

Conditioned defensive burying in rats: Availability of burying materials

Rats shocked once by a stationary, wire-wrapped prod mounted on the wall of the test chamber incorporated sand, wooden blocks, or commercial bedding material on the floor of the chamber into a defensive response. They moved the available material toward and over the shock prod in all three conditions, adapting the response topography to the particular demands of the available material. In the sand and bedding conditions, the rats buried the prod by pushing and spraying piles of the material with snout and forepaws, whereas, in the blocks condition they picked up the blocks with their teeth and placed them individually around the prod. In Experiment 2, the rats buried the shock prod with blocks even when they had to first carry the blocks to the prod from the back of the chamber. Thus, conditioned defensive burying is not a simple, reflexive response to objects paired with a painful stimulus: it is a complex behavioral sequence that can vary as a function of the availability of burying materials.     

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.     

Prolonged exposure to conspecific and predator odors reduces fear reactions to these odors during subsequent prod-shock tests

In Experiment 1, four groups of male rats were given a session as an intruder in either aggressive (i.e., alpha) or nonaggressive colonies of conspecifics and later received either a 2-h exposure to the odors of the alpha colonies or an exposure-control session with the odors of a nonalpha colony. Two additional groups of rats that had been attacked and defeated by alpha residents were later given a 12-h exposure session with alpha-colony odors or nonaipha-control odors. Twenty-four h after the colony-intruder session, all subjects were given a single 6.5-mA shock from a prod with alpha-colony odors present in the bedding of the test chamber. Attacked rats that had been given exposure-control sessions showed significantly less prod burying and greater freezing than nondefeated subjects. This implies that the alpha-colony odors elicited conditioned fear. In contrast, the attacked subjects that had been given a pretest exposure session with alpha-colony odors showed significantly more prod burying and significantly less freezing. This suggests that the alpha-odor exposure resulted in the extinction of fear to these odors. Furthermore, the 12-h exposure to alpha-colony odors was found to be more effective in reducing fear-mediated responses than was the 2-h exposure. In Experiment 2, three groups of rats were exposed to a cat while they were in a protective cage; later they were given a 12-h exposure session with cat odors, a 12-h exposure-control session with no cat odors, or no exposure treatment. Compared with the two control groups, the subjects that were exposed to cat odors showed less freezing during subsequent prod-shock tests in the presence of cat odors, but they did not show prod burying. The reported changes in fear-mediated reactions to the odors of conspecifics and a predator are discussed in terms of both associative and nonassociative processes.     

Postshock learning and conditioned defensive burying

Natural sources of aversive stimuli are frequently well-defined material objects that are present both before and after the aversive event. In the present experiment, rats acquired information about such a source after the aversive event and used this information to guide their subsequent defensive reactions to it. The rats were shocked by one of two possible sources, either a black or a striped prod, mounted on opposite end walls of the test chamber. Immediately following the shock, the houselights were momentarily extinguished and the patterns on the two prods were automatically switched for subjects in the experimental condition or left unchanged for subjects in the control condition. The rats were left in the chamber for another 5 min with the patterns in their new positions before being removed for 2 min while the two prods were mounted on the side walls. During the ensuing test of conditioned defensive burying, the rats in the control condition directed the majority of their burying behavior at the prod exhibiting the pattern displayed by the shock source prior to and during the shock administration. In contrast, the rats in the experimental group buried the prod exhibiting the pattern displayed by the shock source during the postshock period more than they did the prod displaying the pattern present on the shock source prior to and during the shock administration.     

Behavioral field analysis in two strains of rats in a conditioned defensive burying paradigm

Two strains of rats (albino Wistar and hooded PVG/c) were exposed to a conditioned defensive burying paradigm that consisted of placing rats in a test chamber with bedding material on the floor, shocking them with a shock prod, and recording the time each rat spent in burying responses toward the prod. Various behaviors other than burying (freezing, grooming/paw licking) were observed by a time-sampling procedure during the control, conditioning, and extinction sessions, each of which was 15 min in duration. Wistar rats generally showed behavioral inhibition, as evidenced by less burying, lower exploratory and ambulatory behavior, and higher freezing behavior. PVG/c rats spent significantly more time engaged in burying and accumulated more bedding material in the conditioning session than did the Wistar rats. No significant differences between the two strains of rats were observed during the extinction session in terms of these measurements. The results indicate that Wistar rats have a greater tendency to freeze when coping with the noxious stimulus in a conditioned defensive burying paradigm, whereas the dominant coping style for PVG/c rats is defensive burying.     

Defensive burying in rats and hamsters

Hooded rats and golden hamsters were shocked by one of two prods in a chamber with a sawdust-covered floor. Rats buried the prod through which they had been shocked, but hamsters displayed no burying behavior. Hamsters may not have buried the prod because they could not perform the required motor pattern. However, hamsters can carry and pile food pellets. Therefore, in a second experiment, rats and hamsters were shocked in a chamber with wooden blocks on the floor. Rats piled blocks around the prod through which they had been shocked, but hamsters did not. The third experiment established that, like rats, hamsters can associate a prod with shock in one trial, since they showed differential avoidance of a prod through which they had been shocked. Since hamsters are nonsocial and rats are social, these results are consistent with suggestions that burying sources of aversive stimulation evolved as an altruistic behavior.     

Influence of conspecific and predatory Stressors and their associated odors on defensive burying and freezing responses

In Experiment 1, male rats were exposed to either aggressive (i.e., alpha) or nonaggressive conspecific colonies and tested 24 h later, with or without alpha odors, for freezing behavior and burying of a wall prod that had been the source of a brief electric shock. The results indicated that prior defeat experience and the presence of alpha odors alone during testing had no significant effects, but the combination of prior defeat and alpha-odor testing significantly decreased burying and increased freezing behavior. In Experiment 2, we examined the effects of noncontact exposure to a cat, as a predatory Stressor, during subsequent prod-shock tests involving the presence or absence of cat odors. Exposure to a cat failed to disrupt later prod burying and did not produce freezing. However, the presence of cat odors during testing significantly reduced the amount of defensive burying,without resulting in an increment in freezing. In Experiment 3, rats were given 1, 5, or 30 inescapable preshocks in the presence of either cat odors or a hedonically neutral citronella odor and were tested 24 h later for prod burying and freezing with or without these odors. Both the cat and the citronella odors resulted in a significant reduction in burying and an increase in freezing for rats given 5 and 30 preshocks and tested in the presence of these respective conditioned odors. For the groups that were given 5 preshocks, preshock and later testing in the presence of cat odors resulted in significantly less prod burying and more freezing than for rats that were preshocked and tested in the presence of citronella. The findings of these three ethoexperimental studies are discussed in terms of the learned-helplessness theory, the stress-coping-fear-defense (SCFD) theory, and the concept of selective CS-US associability.     

Defensive burying by mice: Intraspecific genetic variation and retention

Genotypically based within-species differences in defensive burying were examined in 180 mice representing 15 inbred strains. Each mouse was tested twice in a cylindrical test chamber containing two similar prods. In the first test, one of the prods was electrified, whereas in the second test (24 h later), neither prod was. Although most strains selectively buried the shock prod in the first test (as determined by bedding-height-at-prod and position-of-highest-bedding-pile criteria), some strains did not discriminate between the shock and dummy prods and still others displayed little prod-directed bedding displacement at all (thereby resembling a heterogeneous nonshocked control group). In general, burying tended to be somewhat reduced in the second test, but strain differences in retention were observed. Factors contributory to the observed differences among strains and the need for multiple measures of burying are discussed. Collectively, these findings indicate that intraspecific genetic variation, acting at multiple burying-relevant behavioral levels, can be an important determinant of the expression of the defensive-burying response in mice.     

Genotype and environment interactively determine the magnitude,directionality, and abolition of defensive burying in mice

Genotypic and environmental contributions to the defensive burying response were examined by testing four sublines of two inbred strains of mice in test chambers of three different lengths. Burying was found to be dependent on both the particular subline tested and the length of the test chamber employed. For two sublines, specific increases in the length of the test chamber resulted in the complete abolition of defensive burying. A third subline never displayed defensive burying, and the fourth buried in all three chamber-length conditions. Sex differences in burying were never observed. Rather than being viewed as a species-specific defensive reaction, it was proposed that defensive burying should more appropriately be viewed as a genotypically dependent response, the expression of which is contingent on the specific environmental context in which an aversive stimulus is encountered. Apparent conflicts in the defensive-burying literature were reconciled in accordance with this interpretation.     

Defensive behavior of the rat in a shock-prod situation: Effects of the subject’s location preference

Experiment 1 investigated the proposition that rats cover the source of aversive stimulation with the bedding material available to them and sought to determine whether familiarization with this material would affect burying. The results indicated that rats are no more likely to cover an aversive object than they are not to cover it, although they collect a considerable amount of bedding material in the area surrounding the aversive object. Experiment 2 demonstrated that the rat’s defensive “burying” toward an aversive object is affected by the subject’s predisposition to displace material toward the front side of the apparatus. Some theoretical complexities involved in considering the act of “burying” toward an aversive object as a defensive behavior are discussed.     

Defensive burying in the Mongolian gerbil (Meriones unguiculatus) as a function of size and shape of the test chamber

Attempts to establish the generality of the defensive-burying response have proved quite successful with several strains of albino and hooded rats and with mice. However, three previous attempts to demonstrate this behavior in gerbils have been completely unsuccessful. Three additional defensive-burying experiments employing gerbils as subjects are reported. Defensive burying did not occur when testing took place in a rectangular chamber (Experiments 1 and 3), but did occur when a circular chamber was employed (Experiments 2 and 3). Hence, the geometric shape of the test chamber appears to be a crucial factor in determining the elicitation of this behavior in gerbils. Furthermore, the overall topography of the gerbil defensive-burying response was found to be different from that of previously examined species.     

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.     

Place conditioning with d-amphetamine: The effect of the CS-UCS interval and evidence of a place avoidance

In Experiment 1, a dose-response study of place conditioning with amphetamine was conducted. Male Sprague-Dawley rats receiving 0.0, 0.05, 0.1, 0.5, 2.0, 5.0, 7.5, or 10.0 mg/kg of d-amphetamine underwent 104-day cycles of place conditioning. On alternate days, each rat was injected with its designated dose of amphetamine while confined to its originally nonpreferred end of a three-compartment, straight alley box. On intervening days, each rat was injected with saline while confined to its originally preferred compartment. Following each 4-day cycle, a choice test was administered in which each rat was allowed 20 min of access to the entire alley box. Doses of amphetamine (≥0.5 mg/kg) induced a significant avoidance of the compartment in which amphetamine had been administered. In Experiment 2, animals received 0.0, 0.5, 2.0, or 5.0 mg/kg of amphetamine and underwent place conditioning procedures identical to those for the animals in Experiment 1. Unlike in Experiment 1, the animals were given a single choice test following 104-day place conditioning cycles. All groups that received amphetamine exbibited-a-eonditioned place avoidance. In Experiment 3, the effect of various CS-UCS intervals on place conditioning with 2.0 mg/kg of amphetamine was examined. Animals that received amphetamine immediately following their removal from the chamber exhibited a conditioned place avoidance.     

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.     

Frustration and the production of schedule-induced polydipsia

In two experiments, the hypothesis that frustration mediates the production of schedule-induced polydipsia was tested. In Experiment I, a group in which reward was reduced from 6 to 2 pellets of food in an operant chamber was found to increase water intake compared to a group maintained at 2 pellets reward. In Experiment II, rats trained to approach food on a partial reinforcement schedule in a runway subsequently showed lower levels of water intake in the operant test for polydipsia than rats given continuous reinforcement during runway training. The results are interpreted as supporting a frustration hypothesis of schedule-induced polydipsia and are discussed within the context of persistence theory.     

Transfer of facilitation in the rat

In two experiments, rats solved two concurrent discrimination problems in which one stimulus (i.e., a facilitator) signaled the reinforcement of another stimulus (i.e., a target). Then a transfer test assessed the capacity of facilitators trained in one problem to promote responding to targets trained in the other. Experiment 1 found that a facilitator promoted as much responding to such a transfer target as to the target with which it was originally trained. Transfer was not obtained with a pseudofacilitator that was uninformative, in training, about the reinforcement of its target. Experiment 2 manipulated the stimulus modality of the targets and facilitators. Its results indicated that transfer performance was not due to generalization between training and transfer targets or facilitators. These results parallel those from comparable autoshaping paradigms with pigeons, and they agree with the view that facilitators promote responding by lowering the threshold for activation of the US representation.     

Two-choice,observational learning and reversal in the rat: S-S versus S-R effects

In Experiment 1, male rats were trained to press both bars in a two-choice apparatus and were then given observational training of a go/no-go discrimination in which the observed operation of two inaccessible, dissimilar bars by a hidden experimenter constituted S+ and S?. After discrimination was established, individual rats were permitted access to the two bars. Six of the seven rats consistently pressed the S+ bar on 10 test trials, but failed to reverse bar preference after observational training was reversed. In Experiment 2, nine naive males received the same observational training as in Experiment 1, but without any pretraining to press either bar. All rats pressed the S+ bar on initial test and did so consistently throughout the 10 trials. Six of these rats received reversal training of the go/no-go discrimination after the 10 test trials. As in Experiment 1, all rats failed to press the new S+ bar. However, five of six rats in another group, which received reversal trainingprior to any test trials, did reverse and press the new S+ bar. In Experiment 3, controls for possible confounding effects of overtraining trials were conducted. These manipulations had no effect; the rats tested before reversal still failed to press the S+ bar, and the rats reversed before testing all reversed or pressed the most recent S+ bar. That is, S-R learning predominated over S-S learning if active, though unreinforced, responding to a particular bar intervened. In contrast, however, a cognitive (S-S) interpretation of directed response learning was supported by the results of Experiment 4, in which the rats that learned the go/no-go discrimination without responding (only by auditory and light cues) failed to press the S+ bar consistently.     

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.