Motivation for Palatable Food Despite Consequences in an Animal Model of Binge-Eating

Binge-eating is characterized by the compulsion to seek out and consume large quantities of food in a discrete time period (1). While the macronutrient composition of binges is often similar to normal meals (2), it is highly palatable food that is greatly craved and preferred during binges. These are foods that are typically high in sucrose and fat and, because they are calorie-dense, are commonly “forbidden” between binges (3-7). The motivation to repeatedly seek out and consume palatable food can be construed as abnormal given the many consequences that result from ingesting these foods. For example, palatable foods are known to trigger binges (7, 8), and they contribute to weight gain and ensuing preoccupation with weight gain (7-8). Binges lead to worsening body image, low self-esteem, mood disturbances, increased perceived life stress, and adverse medical consequences (9-13). Repeatedly returning to intake of palatable foods with full knowledge that a binge, along with worsening of binge-eating symptoms and consequences, is likely to follow cannot be regarded as adaptive. Animal models are valuable in that they aid in identifying the physiological underpinnings of complex human behaviors, of which binge-eating is certainly an example. The validity of an animal model of binge-eating is in part contingent on the number of clinical features it reproduces. One feature not previously investigated in these models is the compulsive nature of eating palatable food despite aversive consequences. Consuming significantly more palatable food can imply an increased motivation for that food. However, tolerating punishment for it is stronger evidence of abnormal motivation for palatable foods. Therefore, the main goal of this study was to ascertain whether binge-eating prone (BEP) rats are also characterized by heightened motivation for palatable food, as defined by the voluntary tolerance of punishment for a particular palatable food. Here, the voluntary punishment was incrementing levels of electrical foot shock delivered immediately after the retrieval of a highly palatable food. The voluntary nature of this behavior was ensured by allowing the rat freedom to enter and escape the palatable food-baited alley at any time, by providing plain rat chow in an alley free of shock, and by not restricting the rat of any food intake prior to being placed into the food choice alley. A second aim of the study was to determine the extent to which exposure to a brief history of cyclic caloric restriction followed by ad lib refeeding changes the motivation of BEP and BER rats to tolerate footshock for palatable food. Cyclic caloric restriction was designed to simulate restrictive dieting which is common among many with binge-eating disorders, including bulimia nervosa and binge eating disorder (10, 14-16). Our BEP/BER model is based on indentifying inherent and stable differences in consumption of palatable food in rats in a discrete, 1-4hr, period of time (17). Rats of the same age and sex generally consume very similar amounts of standard rat chow, their maintenance diet. However, they can vary vastly in how much palatable food they consume when given a choice between these foods and chow. BEP rats are those that consistently consume > 40% more palatable food than those rats consistently eating the least amount of palatable food (BER rats). BEPs are not simply “big eaters,” because they do not overeat on their standard and less palatable maintenance diet of rat chow. Hence, BEPs require palatable food to trigger an abnormal response to their food intake, likely reflecting a gene x environment interaction on their feeding behavior, an interaction that is likely also present in human binge-eating. Since the BEPs do not compensate for their greater intake of palatable food by eating less chow, their total food intake is also greater than that of BERs. Besides eating larger amounts of food in a discrete and same period of time as BER rats, the BEP rats also display other behaviors that are characteristic of human binge-eating. These are described elsewhere (17), but briefly, they include: 1) eating beyond satiety, since they consume as much food after a period of food deprivation as when sated; 2) forsaking healthier chow for palatable food when stressed (BERs do the opposite, forsaking palatable food over more nutritious chow when stressed); 3) rebounding more quickly from stress-induced hypophagia (any stress-induced hypophagia is no longer apparent in BEPs within one hour), and 4) BEP status does not always predict obesity (10, 18-22). When placed on a steady high-fat diet, just as many BEPs as BERs develop obesity and as many of each group resist obesity (17). Similarly, among humans that binge-eat, not all develop obesity because some will compensate in various ways, typically in maladaptive ways, to resist obesity (1). BEPs and BERs that resist obesity do so by voluntarily eating less of the high-fat diet (17). The present study used the BEP/BER model to further validate its use in binge-eating research by determining if BEPs were also characterized by an abnormal motivation for palatable food. We tested the hypothesis that rats assigned BEP status would retrieve and consume more palatable food despite experiencing incrementing levels of footshock for doing so. We secondly hypothesized that BEP and BER rats subjected to a history of cyclic caloric restriction-refeeding, a simulation of human dieting, would seek out and consume more palatable food despite the aversive consequence of footshock. Hence, it was predicted that experience with caloric restriction would turn BERs into more BEP-like rats and, in BEPs, the experience would increase their motivation for palatable food to an even greater extent. Lastly, we measured the food intake of BEPs and BERs when they had access to the previously shock-paired palatable food for the first time in the safe confines of their home cage vs. the shock-delivering maze. We predicted that BERs would consume as much of this palatable food as BEPs due to increased incentive value produced by its former unattainable nature, a simulation of “forbidden” food.