Demonstration of a socially transmitted flavor aversion in rats? Kuan and Colwill (1997) revisited

In each of three experiments that differed only in procedural detail, observer rats interacted with pairs of conspecific demonstrators, one fed a cocoa-flavored diet (Diet Coc) and the other a cinnamon-flavored diet (Diet Cin). Immediately after both members of a pair of demonstrators had been fed, and 5 min before they interacted with an observer or observers, one of the demonstrators was made ill by intraperitoneal injection with lithium chloride. After interacting with a pair of demonstrators for 15 min, each observer was allowed to choose between Diet Cin and Diet Coc for 22 h. In all three experiments, observer rats consumed as much Diet Cin after interacting simultaneously with both an ill demonstrator that had eaten Diet Cin and a healthy demonstrator that had eaten Diet Coc as after interacting simultaneously with both a healthy demonstrator that had eaten Diet Cin and an ill demonstrator that had eaten Diet Coc. These results raise questions about the generality of Kuan and Colwill’s (1997) demonstration of socially transmitted flavor aversions in Norway rats.     

Limitations of a Bidirectional Control Procedure for the Investigation of Imitation in Rats: Odour Cues on the Manipulandum

Magazine-trained observer rats confronted a conspecific demonstrator pushing a joystick to the right or to the left for food reward before the observers were given access to the joystick from the position previously occupied by the demonstrator and rewarded for responses in both directions. For half of the observers (group 0), the joystick was in the same position when acted upon by demonstrators and observers; for the other half (group 180) the manipulandum was rotated 180 within its mounting between observation and test. As in previous experiments using this bidirectional control procedure, rats in group 0 showed demonstratorconsistent responding-that is, they pushed the joystick in the same direction, relative to the actor's body, as had their demonstrators. However, group 180 showed a reverse effect: reliable demonstrator-inconsistent responding. These results suggest that attractive odour or taste cues deposited by demonstrators on the side of the joystick contralateral to the direction of responding are sufficient to produce demonstrator-consistent responding in the bidirectional control procedure.     

Acetylcholine release in the hippocampus and prelimbic cortex during acquisition of a socially transmitted food preference

Interference with cholinergic functions in hippocampus and prefrontal cortex impairs learning and memory for social transmission of food preference, suggesting that acetylcholine (ACh) release in the two brain regions may be important for acquiring the food preference. This experiment examined release of ACh in the hippocampus and prefrontal cortex of rats during training for social transmission of food preference. After demonstrator rats ate a food with novel flavor and odor, a social transmission of food preference group of rats was allowed to interact with the demonstrators for 30 min, while in vivo microdialysis collected samples for later measurement of ACh release with HPLC methods. A social control group observed a demonstrator that had eaten food without novel flavor and odor. An odor control group was allowed to smell but not ingest food with novel odor. Rats in the social transmission but not control groups preferred the novel food on a trial 48 h later. ACh release in prefrontal cortex, with probes that primarily sampled prelimbic cortex, did not increase during acquisition of the social transmission of food preference, suggesting that training-initiated release of ACh in prelimbic cortex is not necessary for acquisition of the food preference. In contrast, ACh release in the hippocampus increased substantially (200%) upon exposure to a rat that had eaten the novel food. Release in the hippocampus increased significantly less (25%) upon exposure to a rat that had eaten normal food and did not increase significantly in the rats exposed to the novel odor; ACh release in the social transmission group was significantly greater than that of the either of the control groups. Thus, ACh release in the hippocampus but not prelimbic cortex distinguished well the social transmission vs. control conditions, suggesting that cholinergic mechanisms in the hippocampus but not prelimbic cortex are important for acquiring a socially transmitted food preference.     

Responses of observer rats (Rattus norvegicus) to complex, diet-related signals emitted by demonstrator rats

We explored the effects of complex, food-identifying signals emitted by demonstrator Long-Evans rats (Rattus norvegicus) on food preferences of their observers. In Experiments 1 and 2, observers identified each of 2 or 3 foods their demonstrators had eaten before interacting with observers. In Experiment 3, individual observers interacted with groups of demonstrators. Some of these demonstrators had eaten one food, some another. Observers then chose between the two foods. The greater the proportion of demonstrators in a group that had eaten a diet, the greater the proportion of that diet the observers ate. In Experiment 4, each observer interacted over several weeks with a series of demonstrators and preferred each of the foods its demonstrators had eaten. In sum, the food preferences of observers were affected by several different types of complex, food-identifying signals like those one might expect rats to encounter outside the laboratory.     

Social learning of food types in zebra finches (<Emphasis Type="Italic">Taenopygia guttata</Emphasis>) is directed by demonstrator sex and feeding activity

In this study we examined how social learning of feeding preferences by zebra finches was affected by the identity of different demonstrators. We presented adult zebra finches with two demonstrators, one male and one female, that exhibited different food choices, and we recorded their subsequent preference when given a choice between the two food types. Previously it was found that young zebra finches' patterns of social learning are affected by the sex of the individual demonstrating a feeding behaviour. This result could be explained by the lack of exposure these animals had to the opposite sex, or by their mating status. Therefore, we investigated the social learning preferences of adult mated zebra finches. We found the same pattern of directed social learning of a different type of feeding behaviour (food colour): female zebra finches preferred the colour of food eaten by male demonstrators, whereas male zebra finches showed little evidence of any preference for the colour of food eaten by female demonstrators. Furthermore, we found that female observers' preferences were biased by demonstrators' relative feeding activity: the female demonstrator was only ever preferred if it ate less than its male counterpart. Electronic Publication     

A failure to find socially mediated taste aversion learning in Norway rats (R. norvegicus)

Observer rats interacted with conspecific demonstrators immediately after demonstrators ate a novel diet and were made ill by LiCl injection. Following their interaction with demonstrators, observers were tested for aversion to their ill demonstrator's diet. Previous research has shown that (a) an observer can extract information from a demonstrator sufficient to permit identification of the demonstrator's diet (Galef & Wigmore, 1983) and (b) a rat ill from LiCl toxicosis is an adequate unconditioned stimulus in a taste aversion learning paradigm (Lavin, Freise, & Coombes, 1980). Further, two of the present experiments demonstrated that cues emitted by a rat, reflecting the particular diet it has eaten, are an adequate conditional stimulus in a toxicosis-induced aversion learning situation. Observer avoidance of a diet previously ingested by an ill demonstrator was, however, not demonstrated. The implications of the failure to find socially mediated aversion learning are discussed.     

Imitation in rats: Initial responding and transfer evidence

In two experiments, rats observed a conspecific demonstrator pushing a single manipulandum, a joystick, to the right or to the left for food reward before being given access to the joystick, for the first time, from a different orientation. In Experiment 1, rats that had observed left-pushing made more of their first three responses to the left than did rats that had observed right-pushing. In Experiment 2 the axis of joystick movement was rotated through 90° between observation and testing for half of the animals. These rats, like those that were tested with the joystick in the position it had occupied during demonstrator responding, showed a significant tendency to push the joystick in the same direction relative to their own bodies as had their demonstrators. These results, which cannot be explained in terms of stimulus-reinforcer learning, provide evidence that rats are capable of imitation, i.e. response, or response-reinforcer, learning by observation.     

Dwarf and golden hamsters' differing responses to conspecific signals for food

The author presented dwarf hamsters (Phodopus campbelli) and golden hamsters (Mesocricetus auratus) with conspecific and inanimate signals for food. Both species approached a cardboard stimulus that predicted food. The dwarf hamsters engaged in high levels of social contact directed toward a conspecific conditioned stimulus for food, but the golden hamsters did not. The author also presented dwarf hamsters with a conspecific signal that did not indicate food, and the levels of social behaviors that they directed toward it were significantly lower. These results suggest the presence of a social component in the dwarf hamster feeding system and are consistent with previous findings that the social transmission of food preferences occurs more readily in dwarf hamsters than in golden hamsters.     

An Experiment upon Repeated Reproduction

The author presented dwarf hamsters (Phodopus campbelli) and golden hamsters (Mesocricetus auratus) with conspecific and inanimate signals for food. Both species approached a cardboard stimulus that predicted food. The dwarf hamsters engaged in high levels of social contact directed toward a conspecific conditioned stimulus for food, but the golden hamsters did not. The author also presented dwarf hamsters with a conspecific signal that did not indicate food, and the levels of social behaviors that they directed toward it were significantly lower. These results suggest the presence of a social component in the dwarf hamster feeding system and are consistent with previous findings that the social transmission of food preferences occurs more readily in dwarf hamsters than in golden hamsters.     

Demonstration of a socially transmitted taste aversion in the rat

Observer rats were allowed to interact for 15 min with 2 conspecific demonstrators, 1 that had been fed a cocoa-flavored diet and 1 that had been fed a cinnamon-flavored diet. One of the demonstrators had been made ill immediately following ingestion of its diet. The observer rats were then presented with the cocoa-flavored and cinnamon-flavored diets for 22 h. The observer rats consumed significantly less of the ill demonstrator’s diet than of the healthy demonstrator’s diet. This finding suggests that, under some conditions, rats can acquire a socially transmitted taste aversion.     

Social transmission and memory of food preferences in pine voles (Microtus pinetorum)

The social transmission of food preferences is affected by factors including the length of time a preference is maintained. The authors investigated the social transmission of food preferences in pine voles (Microtus pinetorum) and whether food items had to be present for memory to persist. A demonstrator vole was fed cocoa-flavored food, a nonpreferred food. After interacting with a demonstrator vole, observer voles preferred cocoa-flavored food as compared with either naive voles that had not interacted with demonstrators or voles that had been exposed to odors. Observers retained this preference for 72 hr after interacting with an observer whether or not flavored foods were present. The ability to learn which food items are palatable and safe may benefit a generalist herbivore that has faced selection to avoid toxic baits.     

A demonstration of observational learning in rats using a bidirectional control

Hungry rats observed a conspecific demonstrator pushing a single manipulandum, a joystick, to the right or to the left for food reward and were then allowed access to the joystick from a different orientation. The effects of right-pushing vs left-pushing observation experience on (1) response acquisition, (2) reversal of a left-right discrimination, and (3) responding in extinction, were examined. Rats that had observed left-pushing made more left responses during acquisition than rats that had observed right-pushing, and rats that had observed demonstrators pushing in the direction that had previously been reinforced took longer to reach criterion reversal and made more responses in extinction than rats that had observed demonstrators pushing in the opposite direction to that previously reinforced. These results provide evidence that rats are capable of learning a response, or a response-reinforcer contingency, through conspecific observation.     

Scent marking by male dwarf hamsters (Phodopus sungorus campbelli) in response to conspecific odors

Male hamsters (Phodopus sungorus campbelli) scent marked at greater frequencies in the presence of conspecific odor, either male or female, than in clean areas. Marking rates were not different between male and female odor conditions. In contrast, the pattern of investigation in response to conspecific odor did differ between the male and the female odor conditions. When male odors were used as stimuli, investigative sniffing increased at the scent marking sites but when female odors were used as stimuli investigative sniffing increased throughout the arena. Thus, male dwarf hamsters direct their scent marks at both male and female conspecifics, discriminate between male and female odor, and investigate in a different manner areas scent marked by males and females.     

Social learning in juvenile lemon sharks, Negaprion brevirostris

Social learning is taxonomically widespread and can provide distinct behavioural advantages, such as in finding food or avoiding predators more efficiently. Although extensively studied in bony fishes, no such empirical evidence exists for cartilaginous fishes. Our aim in this study was to experimentally investigate the social learning capabilities of juvenile lemon sharks, Negaprion brevirostris. We designed a novel food task, where sharks were required to enter a start zone and subsequently make physical contact with a target in order to receive a food reward. Naive sharks were then able to interact with and observe (a) pre-trained sharks, that is, ‘demonstrators’, or (b) sharks with no previous experience, that is, ‘sham demonstrators’. On completion, observer sharks were then isolated and tested individually in a similar task. During the exposure phase observers paired with ‘demonstrator’ sharks performed a greater number of task-related behaviours and made significantly more transitions from the start zone to the target, than observers paired with ‘sham demonstrators’. When tested in isolation, observers previously paired with ‘demonstrator’ sharks completed a greater number of trials and made contact with the target significantly more often than observers previously paired with ‘sham demonstrators’. Such experience also tended to result in faster overall task performance. These results indicate that juvenile lemon sharks, like numerous other animals, are capable of using socially derived information to learn about novel features in their environment. The results likely have important implications for behavioural processes, ecotourism and fisheries.     

Use of public information when foraging: effects of time available to sample foods

It has been proposed that use of socially acquired information by animals should increase as the time available for individual resource sampling decreases. We gave Norway rat “observers” either 2 or 5 h day^–1 to sample four foods. Three of these foods were relatively palatable, but protein-poor; the fourth was relatively unpalatable, but protein-rich. We found that observer rats that for 2 h day^–1 both sampled foods and interacted with demonstrators eating only the protein-rich food ate more of the protein-rich food than did observers that sampled for 2 h day^–1 but had no opportunity to interact with demonstrators. On the other hand, observer rats that could sample foods for 5 h day^–1 ate equal amounts of protein-rich food whether they interacted with a demonstrator fed protein-rich food or not. Subsequent analyses showed that the time available to observers to sample foods, rather than the opportunity to interact with demonstrators determined whether such interaction influenced observers’ food choices. The results are consistent with the hypothesis that animals increase their use of public information in response to temporal constraints on opportunities for resource sampling. Received: 22 December 1998 / Accepted after revision: 27 February 1999     

Observational learning in monkeys

Observer monkeys were housed next to demonstrator monkeys that were conditioned to respond on a multiple reinforcement schedule whose components were fixed-ratio 32, variable-interval 3-min, and extinction 5-min followed by an additional 30 sec of extinction during which every response started a new 30-sec interval. After observational periods from 113 to 210 hr long, during which observers could not perform the response and were given no extrinsic reinforcers, their first-response latencies to fixed ratio and variable interval were as short as the demonstrators; and their rates of responding were well above pre-observational baseline levels. About 8 hr later, a temporal pattern of responding appropriate to the multiple schedule emerged, including non-emission of responses during extinction. Controls lacking the chance to observe did not develop typically patterned responding after 60 hr in one case and, in two other cases, after 80 hr during which, on two occasions, every one of 50 responses was reinforced. In a second experiment, the stimulus lights associated with fixed ratio and variable interval were presented simultaneously. Subjects chose one of the schedules by responding to one of the levers beneath the lights. All subjects initially chose fixed ratio. Seeing the demonstrators switch to variable interval, due to increases in the fixed-ratio requirement, had no effect upon observers, which continued to choose fixed ratio.     

Social mediation of puberty: an adaptive female strategy?

Females of two hamster species with contrasting degrees of gregariousness were tested for social influences on the timing of sexual maturation. When female dwarf hamsters (Phodopus sungorus campbelli), a gregarious species, were housed with an adult male at weaning, they began estrous cycles significantly earlier than when they were housed alone or with their family. Females housed with one or two female siblings at weaning matured significantly later than did all other females. Once mature, females housed with familiar males conceived later than did females housed with unfamiliar males. Rearing conditions also affected body weight; those housed with female siblings grew more slowly and attained a lower weight at 8 weeks of age than did females in all other groups. In contrast, when weanling female golden hamsters (Mesocricetus auratus), a solitary species, were housed with either an adult male, two female siblings, or alone, they did not differ in their rate of sexual maturation or growth. It is suggested that the degree to which social factors can accelerate or delay puberty is an adaptive characteristic and may be correlated with the degree of gregariousness of a species.     

Social identification of toxic diets by Norway rats (Rattus norvegicus)

In the present experiment, a naive rat (an observer) interacted with two conspecifics (demonstrators) that had recently eaten a diet unfamiliar to the observer, ate two unfamiliar foods in succession, one of which was the food its demonstrators had eaten, suffered toxicosis, and finally, was offered a simultaneous choice between the two diets it had eaten prior to toxicosis induction. During the choice test, observers exhibited an aversion to that diet their respective demonstrators had not eaten. This result indicates that exposure of a rat to conspecifics that have eaten a diet can act, as does actual ingestion of a diet, to reduce that diet's subsequent associability with toxicosis. I discuss this finding as suggesting that interaction with conspecifics may provide an alternative to individual trial and error learning in identification of toxic foods by rats that ingest a number of novel foods in succession before becoming ill.     

How does dominance rank status affect individual and social learning performance in the dog (<Emphasis Type="Italic">Canis familiaris</Emphasis>)?

Dogs can learn effectively to detour around a V-shaped fence after observing a demonstration from either an unfamiliar human or dog demonstrator. We found earlier that there is substantial individual variation between the dogs’ performance, even when using the same experimental conditions. Here, we investigate if the subjects’ relative dominance rank with other dogs had an effect on their social learning performance. On the basis of the owners’ answers to a questionnaire, subjects from multi-dog homes were sorted into groups of dominant and subordinate dogs. In Experiment 1, dominant and subordinate dogs were tested without demonstration and we did not find any difference between the groups—they had similarly low detour performances on their own. In Experiment 2 and 3, dogs from single dog and multi-dog households were tested in the detour task with demonstration by an unfamiliar dog, or human, respectively. The results showed that social learning performance of the single dogs fell between the dominant and subordinate multi-dogs with both dog and human demonstration. Subordinate dogs displayed significantly better performance after having observed a dog demonstrator in comparison to dominant dogs. In contrast, the performance of dominant and subordinate dogs was almost similar, when they observed a human demonstrator. These results suggest that perceived dominance rank in its own group has a strong effect on social learning in dogs, but this effect seems to depend also on the demonstrator species. This finding reveals an intricate organization of the social structure in multi-dog households, which can contribute to individual differences existing among dogs.     

Sensory modalities in depth perception by golden hamsters

Golden hamsters are able to detect differences in the height of a platform from which they jump, as measured by their increasing latencies prior to jumping from increased elevations. This ability is very effective when optical information is available, but it is also present when hamsters jump in total darkness. A second experiment shows that, when hamsters are placed on a real physical cliff, they preferentially use tactile information over visual information to guide their choice of the side from which to descend. In a nonvisual setting, tactile stimulation is used in conjunction with other types of cues. Evidence is provided to suggest that these cues are of an acoustical nature.