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.     

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.     

What observer rats don’t learn about foods from demonstrator rats

Naive “observer” rats that interact with conspecific “demonstrators” fed a distinctive food increase intake of the food their demonstrators have eaten. Here we found that observer rats that had interacted simultaneously with 2 demonstrator rats, 1 fed a distinctively flavored, protein-poor food, the other a distinctively flavored, protein-rich food, did not prefer the former. Similarly, observer rats ate equal amounts of two distinctively flavored foods after interacting simultaneously with 2 demonstrator rats, 1 that had consumed all food available to it, the other fed from a surplus of the second food. Last, observer rats that had interacted with both a “trustworthy” demonstrator (1 an observer had learned ate only nutritious foods) and an “untrustworthy” demonstrator (1 an observer had learned ate noxious substances) did not prefer unfamiliar foods eaten by trustworthy demonstrators to those eaten by untrustworthy demonstrators. These findings suggest limits on social information observers use in selecting foods.     

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.     

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.     

Further evidence that Norway rats do not socially transmit learned aversions to toxic baits

Three experiments were undertaken to examine the effects of interactions with demonstrator rats made ill by injection of lithium chloride (LiCl) on the later food choices of their observers. We found that (1) observer rats that had been taught an aversion to an unfamiliar diet exhibited a substantial reduction of that aversion after interacting with poisoned demonstrators that had eaten the diet to which the observers had learned an aversion, (2) exposure of an observer rat to poisoned demonstrator rats that had eaten a diet interfered with later acquisition by the observer of an aversion to the diet that the poisoned demonstrators had eaten, and (3) after interacting with poisoned demonstrators that had eaten one of two diets, observers that ate both diets and were then made ill formed an aversion to whichever diet their respective, poisoned demonstrators had not eaten. The present experiments, like previous studies both in our laboratory and elsewhere, failed to provide any evidence that naive observer rats will learn to avoid a food as a result of interacting with demonstrator rats that had eaten the food and exhibit symptoms of toxicosis. To the contrary, observer rats in the present experiments exhibited an enhanced preference for foods eaten by sick demonstrators.     

Demonstrator influence on observer diet preference: Analyses of critical social interactions and olfactory signals

Previous studies have shown that interaction of an observer rat with a previously fed conspecific demonstrator enhances the observer’s subsequent preference for the diet its demonstrator ate. The present series of experiments were undertaken to explore both the conditions sufficient to permit demonstrator influence on observer diet preference and the behavioral processes underlying such influence. We found (1) that an observer rat can be influenced in its subsequent diet selection by interaction for as little as 2 min with a demonstrator, (2) that during such brief interactions mouth-to-mouth contact between demonstrator and observer is necessary for demonstrator influence on observer diet preference, (3) that both cues emerging from the digestive tract of a rat fed by intragastric intubation and particles of food clinging to the fur of a demonstrator are sufficient to permit observers to identify their respective demonstrators’ diets, (4) that exposure to a diet is effective in enhancing an observer’s subsequent preference for that diet only if the diet is experienced in the presence of another rat, and (5) that diets experienced on the anterior of a live rat are more effective in altering observers’ subsequent diet preferences than the same diets experienced either on the anterior of a dead rat or the posterior of a live one.     

Social influences on the identification of toxic foods by Norway rats

In the present experiments, a naive “observer” rat first interacted with a “demonstrator” rat previously fed a diet unfamiliar to the observer. The observer then sampled two unfamiliar diets, one of which was the diet its demonstrator had eaten. The observer was then injected with LiCl and, following recovery from toxicosis, was offered a choice between the two diets it sampled prior to toxicosis induction. It was found that: (1) each observer rat formed an aversion to whichever diet its demonstrator had not eaten, (2) effects of demonstrators on aversion learning by observers were present even if there was a 7- or 8-day delay between interaction of a demonstrator and observer and diet sampling by the observer, and (3) observers interacting with 3 demonstrators, each fed a different diet, subsequently exhibited a reduced tendency to form an aversion to each of the diets eaten by their demonstrators. Taken together, the results indicate that information acquired from conspecifics as to the diets they have eaten can play an important role in determining the foods to which otherwise naive rats will learn aversions.     

Social learning and social transmission of foraging information in Norway rats (Rattus norvegicus)

Adult male Norway rats were tested in a first experiment to see whether foraging efficiency could be improved by social learning. Observers were placed in one of four conditions in which they were paired with demonstrators that either had or had not been previously trained to dig for buried carrot pieces, and in which the demonstrators either did or did not have carrot buried in the experimental enclosure. Observers in the group with trained demonstrators that did have carrot pieces buried in the experimental area during the observation period subsequently unearthed more buried carrot, did so more rapidly, and were generally more active than were the observers in the other three groups. In a second experiment, chains of transmission were established by allowing each observer to act as a demonstrator for the next naive observer. Enhanced levels of digging behavior were maintained across eight transmission episodes in three transmission groups relative to a no-transmission control group, the performance levels becoming stable after five transmission episodes at a level significantly above that of the control group. The study demonstrates that social learning and transmission mechanisms exist which might result in the diffusion of certain patterns of behavior through populations of Norway rats.     

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.     

Transfer of information concerning distant foods in rats: A robust phenomenon

Following interaction with a “demonstrator” rat, an “observer” rat prefers that diet eaten by its demonstrator prior to their interaction (Galef & Wigmore, 1983). The present series of studies demonstrates that such demonstrator influence on observer diet preference can be found in: (1) first-generation laboratory bred wild rats as well as domesticated rats, (2) food-deprived as well as nondeprived observers, (3) unfamiliar as well as familiar demonstrator-observer pairs, (4) both 21-day-old and adult observers, and (5) rats selecting fluids as well as solids for ingestion. These data indicate that the social transmission of information concerning distant diets is a general and robust phenomenon, observable under a wide variety of experimental conditions.     

Demonstrator influence on observer diet preference: Effects of simple exposure and the presence of a demonstrator

Previous studies in our laboratory have demonstrated that a naive rat (an observer), after interacting briefly with a previously fed conspecific (a demonstrator), will exhibit an enhanced preference for the diet its demonstrator had been fed. The present studies were undertaken to determine whether demonstrator-induced alterations in observer diet preference were the result of simple exposure of observers to diet-identifying cues emitted by demonstrators during the period of demonstrator-observer interaction. Our results indicated that observer experience of diet-related cues in the stimulus context provided by the presence of a demonstrator was sufficient to enhance observer preference for a diet, whereas simple exposure to that diet was not. We concluded that demonstrator influence on observer diet preferences was not the consequence of simple exposure of observers to demonstrator-emitted cues reflecting demonstrators’ diet.     

Social transmission of information about multiflavored foods

We fed demonstrator rats diets made by adding three, four, or five different flavorants to powdered Purina Rat Chow. We then allowed each of these demonstrator rats to interact with a naive observer rat for 30 min. We found that (1) observers exhibited enhanced preferences for many of the individual flavorants in the multiflavored diets that their respective demonstrators had eaten and (2) the probability of an observer exhibiting enhanced preference for an individual flavorant in its demonstrator’s diet decreased as the number of flavorants in that diet increased. In Experiment 2, the individual members of pairs of subjects were each fed one of two different four-flavored diets. The subjects in each pair interacted for 30 min, then each chose between two single-flavored diets. One of these single-flavored diets contained a flavorant in the four-flavored food that a subject had itself eaten; the other single-flavored diet contained a flavorant in the four-flavored diet that a subject’s partner had eaten. The subjects showed enhanced preferences for six of eight flavorants in the four-flavored diets that their respective partners had eaten.     

Delays after eating: Effects on transmission of diet preferences and aversions

Previous studies have demonstrated that a naive rat (an observer), after interacting with a previously fed conspecific (a demonstrator), will exhibit an enhanced preference for the diet its demonstrator ate. Furthermore, observers poisoned after interacting with demonstrators exhibit an aversion to their respective demonstrators’ diets. In the present paper, we examined the effects, on transmission of information from demonstrator to observer, of introducing delays between the end of demonstrator feeding and initiation of demonstrator-observer interaction. We found that (1) for at least 4 h after ingestion, demonstrator rats emitted diet-related cues sufficient to alter observers’ subsequent diet preferences, and (2) diet-related cues emitted by demonstrators for 1 to 2 h after a meal were adequate conditional stimuli for aversion learning by their observers.     

Familiarity and relatedness: Effects on social learning about foods by Norway rats and Mongolian gerbils

In recent experiments in which the social influences on feeding in Mongolian gerbils were investigated, observer gerbils acquired food preferences from conspecific demonstrators only if the demonstrators and observers were either related or familiar. Even then, the effects of demonstrator gerbils on observers’ food choices lasted less than 24 h. In similar experiments with Norway rats, the familiarity/relatedness of demonstrators and observers had little effect on social learning, and the demonstrators’ influence on observers’ food choices lasted many days. We examined the causes of these differences and found that, after observer gerbils interacted with either unfamiliar or familiar conspecific demonstrators that had been fed using procedures typically used to feed demonstrator rats, they showed long-lasting social learning about foods, whereas observer rats interacting with conspecific demonstrators that had been fed as demonstrator gerbils normally are fed showed effects of familiarity/relatedness to demonstrators on their social learning about foods. Procedural differences, rather than species differences, seem to be responsible for reported inconsistencies in social learning about foods by rats and gerbils.     

Socially transmitted food preferences can be used to study long-term memory in rats

Immediately after a recently fed rodentdemonstrator interacts with a conspecificobserver, the observer shows a substantially enhanced preference for whatever food its demonstrator ate. Here we show that (1) influence of a single, 30-min interaction with a demonstrator on an observer’s food preference lasts for at least 1 month, and (2) observers interacting on 2 successive days with a demonstrator fed a different diet on each day show significantly enhanced preferences for both diets a month later. Such enduring effects of single, brief interactions between a demonstrator rat and its observer provide an efficient means for studying physiological and behavioral substrates of long-term memory in rodents. Together with the results of previous studies of social influences on food choices of rats, the present results also suggest that rats may use information acquired from conspecifics to identify both toxic and safe foods for many weeks after they have acquired this information.     

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.     

Imitative learning in Japanese quail (<Emphasis Type="Italic">Coturnix japonica</Emphasis>) using the bidirectional control procedure

In the bidirectional control procedure, observers are exposed to a conspecific demonstrator responding to a manipulandum in one of two directions (e.g., left vs. right). This procedure controls for socially mediated effects (the mere presence of a conspecific) and stimulus enhancement (attention drawn to a manipulandum by its movement), and it has the added advantage of being symmetrical (the two different responses are similar in topography). Imitative learning is demonstrated when the observers make the response in the direction that they observed it being made. Recently, however, it has been suggested that when such evidence is found with a predominantly olfactory animal, such as the rat, it may result artifactually from odor cues left on one side of the manipulandum by the demonstrator. In the present experiment, we found that Japanese quail, for which odor cues are not likely to play a role, also showed significant correspondence between the direction in which the demonstrator and the observer push a screen to gain access to reward. Furthermore, control quail that observed the screen move, when the movement of the screen was not produced by the demonstrator, did not show similar correspondence between the direction of screen movement observed and that performed by the observer. Thus, with the appropriate control, the bidirectional procedure appears to be useful for studying imitation in avian species.     

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.