Social interaction modifies learned aversions, sodium appetite, and both palatability and handling-time induced dietary preference in rats (Rattus norvegicus)

In a series of four experiments, I examined the extent to which socially transmitted diet preference could counteract the effects of a learned aversion (Experiment 1), a palatability-based diet preference (Experiment 2), a polyethylene glycol 20,000-induced sodium appetite (Experiment 3), and a handling-time induced dietary preference (Experiment 4). I found that rats poisoned after eating a novel diet ate very substantial amounts of the averted diet following interaction with conspecifics that had eaten the averted diet. Following interaction with conspecifics that had eaten an unpalatable diet, rats offered a choice between palatable and unpalatable diets ate more than twice as much unpalatable diet as did controls lacking social experience. Sodium-deficient rats offered a choice between sodium-enriched and sodium-adequate diets ate less than half as much sodium-enriched diet, following interaction with conspecifics that had eaten sodium-adequate diet as did control rats lacking social experience. Rats offered a choice between isocaloric, roughly equipalatable foods with long and short handling times (e.g., sunflower seeds with and without shells) chose the food having the longer handling time after interacting with conspecifics eating that food. These findings suggest that social influence is a major factor in guiding diet selection by rats.     

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     

Social processes in communication and cognition in callitrichid monkeys: a review

Studies of vocal development in nonhuman primates have found little evidence for plasticity in vocal production, somewhat more for usage of calls, with the greatest plasticity arising in response to calls of others. Generally, similar results were obtained with callitrichid monkeys, the marmosets and tamarins, but with several interesting exceptions. Infant pygmy marmosets show babbling behavior with improvement in adult call structure related to the amount and diversity of babbling. Adult marmosets alter call structure in response to changes in social partners, and wild marmosets have vocal dialects and modify call structure according to how far they are from other group members, suggesting the potential to modify call structure in different social and environmental contexts, though direct learning of novel vocalizations has not been observed. Infant cotton-top tamarins do not produce adult-like calls in appropriate contexts, at least in the first few months of life, but through food sharing from adults infants learn about appropriate foods and the appropriate contexts for food vocalizations. Tamarins modify call structure and usage with changes in social status. Tamarins, unlike other monkeys tested, can learn to avoid noxious foods through observation of other group members, and can learn about novel food locations. Recent studies provide evidence of contextual imitation in marmosets. The plasticity in vocal communication and evidence of social learning in marmosets and tamarins relative to other monkeys may be related to the cooperative breeding system of marmosets and tamarins. With a high degree of behavioral coordination among group members, there is a priority on monitoring signals and behavior of others and adjusting one's own signals and behavior. This creates the context for vocal plasticity and social learning. Accepted after revision: 23 May 2001 Electronic Publication     

Relative potency of foods and drinks as targets in aversion conditioning

The potency of food stimuli as targets in aversion learning was examined using an interference paradigm. In the first study, foods interfered with liquid aversions but liquids did not interfere with food aversions. In the second study, food aversions were found to be resistant to interference by other foods. These findings suggest that foods are relatively potent targets in aversion conditioning in that they are resistant to interference by both foods and drinks. The final study examined the contribution of flavor intensity and nutrient density to the potency of aversion conditioning. The relative potency of foods over drinks may reflect differences in their intensity as well as their different roles in toxin avoidance and nutrient selection.     

Reversal of innate aversions: attempts to induce a preference for chili peppers in rats.

Although humans frequently develop preferences for innately unpalatable bitter or irritant substances, such preferences are extremely rare in animals. An attempt was made to understand the nature of this difference by systematic experiments with laboratory rats, with chili pepper as the unpalatable substance. In parallel with major aspects of the human experience with chili pepper, rats were exposed to it as a flavoring in all their food for periods up to 11 mo from birth, without significant preference enhancement. Gradual introduction of chili into the diet also had no effect, nor did a series of poisoning and safety experiences designed to teach the rats that only chili-flavored foods were safe to eat. A sequence of seven pairings of chili-flavored diet with prompt recovery from thiamine deficiency did significantly attenuate the innate aversion and may have induced a chili preference in at least one case. Extensive experience with chili did not reliably make rats much less sensitive to its oral effects. The only reliable way to eliminate chili aversion in rats is to destroy their chemical irritant sense, which was accomplished in one group of rats. It is concluded that in contrast to humans, it is extremely difficult to reverse innate aversions in rats.     

Relation between food preference and food-elicited vocalizations in golden lion tamarins (Leontopithecus rosalia).

We report the results of 2 studies on food-elicited vocalizations in golden lion tamarins (Leontopithecus rosalia). First, we investigated the preferences of 10 golden lion tamarins for 6 foods. Tamarins prefer mealworms and raisins significantly more than apple, egg, carrot, or marmoset diet. Food preference rank was significantly and positively correlated with the rank of latency to choose a particular food. Second, we investigated the relation between food preference and 15 vocal parameters measured from the calls emitted by 5 tamarins to a subset of the foods. Only 1 parameter was significantly correlated with food preference across animals. Within-subjects multivariate analysis of variance showed that the vocalizations to foods are significantly different. Our results support an hypothesis that food-elicited vocalizations vary in ways that correspond to the caller's preference but not in a manner that labels food type.     

Lack of interference in long-term memory for socially learned food preferences in rats (Rattus norvegicus)

Outside the laboratory, rats (Rattus norvegicus) are likely both to interact with several conspecifics that have eaten various foods and to eat a variety of foods themselves before they encounter any particular food for which they have a socially enhanced preference. Here the authors examine the stability of rats' socially learned food preferences following 6 days of potentially disruptive ingestive experiences. The authors found that 6 days of (a) eating unfamiliar foods, (b) interacting with demonstrators that had eaten unfamiliar foods, or (c) both eating unfamiliar foods and interacting with demonstrators that had eaten those foods had no measurable effect on rats' socially learned food preferences. The stability of socially enhanced food preferences over time and despite potentially disruptive experiences is consistent with the view that social learning about foods is an important determinant of the food choices of free-living Norway rats.     

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.     

Using stop signals to inhibit chronic dieters' responses toward palatable foods

Palatable foods in the environment can unintentionally trigger reactions to obtain them, which may interfere with dieting attempts. We tested a strategy to facilitate dieting behavior that makes use of behavioral stop signals that should instantly inhibit chronic dieters’ responses toward palatable foods. Participants performed a go/no-go task in which go cues and no-go cues (i.e., the behavioral stop signals) were presented with pictures of palatable foods and control objects. In Study 1, we tested the immediate behavioral effect of presenting stop signals near palatable foods in a reaction time paradigm. In Study 2 we assessed consumption of palatable food that had either consistently been associated with no-go cues, or not. Results show that no-go cues instantly inhibited responses toward palatable foods especially among chronic dieters. Moreover, across a one day period chronic dieters consumed less of a food that had consistently been associated with no-go cues. Stop signals thus appear a promising tool for chronic dieters to control behavior to palatable foods, and we discuss the merits and potential applications of this tool for facilitating dieting behavior.     

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.     

Food Avoidance Learning in Squirrel Monkeys and Common Marmosets

Using a conditioned food avoidance learning paradigm, six squirrel monkeys (Saimiri sciureus) and six common marmosets (Callithrix jacchus) were tested for their ability to (1) reliably form associations between visual or olfactory cues of a potential food and its palatability and (2) remember such associations over prolonged periods of time. We found (1) that at the group level both species showed one-trial learning with the visual cues color and shape, whereas only the marmosets were able to do so with the olfactory cue, (2) that all individuals from both species learned to reliably avoid the unpalatable food items within 10 trials, (3) a tendency in both species for quicker acquisition of the association with the visual cues compared with the olfactory cue, (4) a tendency for quicker acquisition and higher reliability of the aversion by the marmosets compared with the squirrel monkeys, and (5) that all individuals from both species were able to reliably remember the significance of the visual cues, color and shape, even after 4 months, whereas only the marmosets showed retention of the significance of the olfactory cues for up to 4 weeks. Furthermore, the results suggest that in both species tested, illness is not a necessary prerequisite for food avoidance learning but that the presumably innate rejection responses toward highly concentrated but nontoxic bitter and sour tastants are sufficient to induce robust learning and retention.     

Social transmission of food preferences in Japanese monkeys (Macaca fuscata) after mere exposure or aversion training

In Experiment 1, 3 mother-child pairs of Japanese monkeys (Macaca fuscata) were given simultaneous choice tests between raisins and popcorn. The mothers and offspring showed different choice patterns. Cofeeding opportunities were then alternated with individual choice tests. In Experiment 2,2 other pairs were added. Each animal was again offered simultaneous choice tests between marshmallows and almonds. Food aversion conditioning was used to create different choice patterns for mothers and offspring. After cofeeding and choice tests, the differences in choice patterns disappeared in both experiments. The changes after contact with the other's eating pattern during cofeeding was as follows: foods consumed by either came to be eaten by both; foods consumed by both continued to be eaten by both; and foods consumed by neither continued to be ignored. The results provide evidence for social transmission of food preferences in this species.     

Social desirability and self-reported driving behaviours: Should we be worried?

There is widespread use of self-report measures of driving behaviour in the traffic psychology literature, despite the frequent criticism that such measures are subject to social desirability bias. However, no research has yet investigated the more recently developed measures of driving anxiety and avoidance behaviour for socially desirable responding. Furthermore, relatively little research has investigated the issue of socially desirable responding on self-reported driver behaviour in general, and that which does exist has several shortcomings. The present study used a repeated measures design to assess the effect of social desirability on a measure of driving avoidance, the Driving and Riding Avoidance Scale (DRAS), and the Driver Behaviour Questionnaire (DBQ). A sample of 228 undergraduate students completed the DRAS, DBQ and a measure of socially desirable responding in class, which constituted a public place, and then again 2 months later in the privacy of their homes. None of the DBQ items were significantly different across the two locations. However, two of the DRAS general avoidance items were higher in the public setting, perhaps demonstrating the effect of socially desirable responding on driving avoidance due to environmental or practical concern. Nevertheless, overall it appears as though the DRAS and DBQ are not particularly vulnerable to socially desirable responding, although further well-designed research on the effects of such bias on these and other self-report measures of driving behaviour should be undertaken.     

Social Information Guides Infants' Selection of Foods

Two experiments investigated the influence of socially conveyed emotions and speech on infants' choices among food. After watching films in which two unfamiliar actresses each spoke while eating a different kind of food, 12-month-old infants were allowed to choose between the two foods. In Experiment 1, infants selected a food endorsed by a speaker of their native language who displayed positive affect over a food endorsed by a foreign-language speaker who displayed negative affect. In Experiment 2, both actresses displayed positive affect, but they spoke in different languages, and infants again selected the food associated with the speaker of their native language. The findings contrast with previous research in which infants and toddlers have shown little selectivity when presented with foods that differ in their intrinsic properties such as color, texture, and familiarity. Although infants may lack capacities for evaluating foods on their own, they do look to other people for guidance in food selection.     

Types of food aversions: animal, vegetable, and texture

Despite a growing body of research investigating the origins and effects of food aversions, few research instruments have been developed to measure aversions to specific types or categories of food. Undergraduates (N = 209) responded to a series of food aversion questionnaires. The results suggest that people tend to be averse to 2 types of foods (vegetables and meats or fats) and to the texture and taste of certain foods (e.g., oysters). Aversions were slightly more prevalent among women than among men and were correlated with lower educational levels. The authors provide a means of advancing future research on this problem by reliably identifying 3 categories of food aversions. Future researchers should evaluate additional food categories and expand the focus on food aversions beyond the current concern with learned avoidance of specific food items.     

Palatability of food as a factor influencing obese and normal-weight children''s eating habits

The type and amount of food leftover from school lunches by normal-weight and obese elementary school children was examined for its similarity to the pattern reported by Krassner et al. (1979) in a study of normal-weight and obese college students. In this study 102 observations of children between the ages of 9–11, were taken over eight lunch periods in their school cafeteria. Overall, the normal-weight children left only slightly more food uneaten than did the obese children. However, when food palatability was examined, it was found that normal-weight children left over twice as much palatable food as did obese children. Children did not differ on the amount of unpalatable food left uneaten.

These results suggest that Krassner et al.'s observation that obese adults leave less food on their plates may be extended to children and, further, that like obese adults, obese children may be more influenced by the palatability of food than their normal-weight peers.     

Types of Food Aversions: Animal,Vegetable, and Texture

Despite a growing body of research investigating the origins and effects of food aversions, few research instruments have been developed to measure aversions to specific types or categories of food. Undergraduates (N = 209) responded to a series of food aversion questionnaires. The results suggest that people tend to be averse to 2 types of foods (vegetables and meats or fats) and to the texture and taste of certain foods (e.g., oysters). Aversions were slightly more prevalent among women than among men and were correlated with lower educational levels. The authors provide a means of advancing future research on this problem by reliably identifying 3 categories of food aversions. Future researchers should evaluate additional food categories and expand the focus on food aversions beyond the current concern with learned avoidance of specific food items.     

限制性饮食者对食物线索的注意偏向：基于目标矛盾理论模型

采用点探测变式探讨了120名成功和失败女性限制性饮食者对两类食物线索的注意偏向机制。结果发现, 当只启动享乐目标时, 成功的限制者存在对美味食物线索的注意回避, 失败的限制者存在对美味食物线索的注意脱离困难; 当相继启动享乐目标和节食目标时, 成功和失败两类限制者均存在对美味食物线索的注意回避, 但失败者仍然存在注意脱离困难。从目标矛盾模型理论对实验结果进行了讨论。     

Regulatory interactions of stress and reward on rat forebrain opioidergic and GABAergic circuitry

Palatable food intake reduces stress responses, suggesting that individuals may consume such ?comfort? food as self-medication for stress relief. The mechanism by which palatable foods provide stress relief is not known, but likely lies at the intersection of forebrain reward and stress regulatory circuits. Forebrain opioidergic and gamma-aminobutyric acid ergic signaling is critical for both reward and stress regulation, suggesting that these systems are prime candidates for mediating stress relief by palatable foods. Thus, the present study (1) determines how palatable ?comfort? food alters stress-induced changes in the mRNA expression of inhibitory neurotransmitters in reward and stress neurocircuitry and (2) identifies candidate brain regions that may underlie comfort food-mediated stress reduction. We used a model of palatable ?snacking? in combination with a model of chronic variable stress followed by in situ hybridization to determine forebrain levels of pro-opioid and glutamic acid decarboxylase (GAD) mRNA. The data identify regions within the extended amygdala, striatum, and hypothalamus as potential regions for mediating hypothalamic-pituitary-adrenal axis buffering following palatable snacking. Specifically, palatable snacking alone decreased pro-enkephalin-A (ENK) mRNA expression in the anterior bed nucleus of the stria terminalis (BST) and the nucleus accumbens, and decreased GAD65 mRNA in the posterior BST. Chronic stress alone increased ENK mRNA in the hypothalamus, nucleus accumbens, amygdala, and hippocampus; increased dynorphin mRNA in the nucleus accumbens; increased GAD65 mRNA in the anterior hypothalamus and BST; and decreased GAD65 mRNA in the dorsal hypothalamus. Importantly, palatable food intake prevented stress-induced gene expression changes in subregions of the hypothalamus, BST, and nucleus accumbens. Overall, these data suggest that complex interactions exist between brain reward and stress pathways and that palatable snacking can mitigate many of the neurochemical alterations induced by chronic stress.