The main finding of the study was that rats classified as binge-eating prone (BEP), for their increased food intake in the presence of palatable food, not only consumed more of this food but were also willing to tolerate higher levels of footshock to retrieve and consume it compared to binge-eating resistant rats (BERs). This was observed in the rats despite their sated condition and despite the presence of chow, free of shock, in an adjacent arm of the maze. The data collected during their acclimation to the maze suggests that this difference in motivation between the groups was not caused by differences in anxiety, motor ability, or learning capacity, since BEPs did not differ from BERs in the required number of exposures to the maze or time in the maze to retrieve the palatable food for the first time.
A subsequent experiment imposed the rats with a brief cyclic history of food restriction and refeeding meant to simulate human-like dieting. Given that this study was confounded by the rats' last experience in the maze, which was with a highly aversive level of footshock (one too aversive to tolerate for palatable food), and given the low Ns from sub-diving BEP/BER groups so that half of each would experience cyclic caloric restriction-refeeding (N=5/group), we must regard the results as pilot data for further exploration. Nonetheless, despite these shortcomings, the results suggest that in otherwise non-binge-eating prone rats (BERs), a history of human-like dieting may alter their motivation for palatable food. We previously reported that a history of cyclic caloric restriction-refeeding is a necessary trigger of binge-eating in stressed rats (8
), a phenomenon now observed in other laboratories using rats and mice (33
). In the present study, prior experience in the shock maze could be regarded as stressful. Among the BER group, only those with a history of cyclic caloric restriction-refeeding showed a trend to retrieve and consume significantly more palatable food than BERs without this history. Therefore, despite normal body weights and satiety following restriction-refeeding protocol, stress combined with this history may have once again served to augment food intake, even in rats not disposed to binge-eat (in BERs).
BEPs did not respond in kind to the experience of cyclic caloric restriction-refeeding. One reason for this may be that, compared to BERs, their last experience in the maze was with a much higher level of shock than that experienced by BERs. However, another explanation is that BEPs are dispositionally unaffected by periods of caloric restriction. We previously reported that under a state of acute food deprivation, one producing hunger (as evidenced by overeating of BERs after the same acute food deprivation), BEPs did not consume any more palatable food than they did when not deprived of food (17
). That is, BEPs consume as much palatable food when sated as when hungry. This suggests that, when confronted with palatable food, BEPs are eating for reasons outside of metabolic need. Hence, their motivation for palatable food as tested here may be unaffected by a prior history of cyclic caloric restriction-refeeding. In this way, BEPs may be more representative of individuals with binge eating disorder (BED) and obesity resulting from compulsive overeating, since in these conditions, a history of dieting is not always present (1
). Bulimia nervosa may be more accurately modeled by BERs with a history of cyclic caloric restriction-refeeding. These are rats that typically eat less palatable food than BEPs (a mode of self-restriction) but that can be changed to consume more after a bout of caloric restriction or ‘dieting’ (1
). To optimally use this model to study these clinical subgroups, it will first be necessary to repeat this experiment with a larger number of animals that are subjected to a history of cyclic caloric restriction-refeeding protocol prior
to being tested for palatable food motivation in the shock maze.
In the final test, when all rats had access to the consequence-associated M&Ms in the safety of their home cages for the first time, BERs ate as much of this palatable food as BEPs. This could not be due to a change in their BEP/BER status, since the Oreo test confirmed that BERs still ate less than BEPs. One could argue that BERs simply preferred or liked M&Ms more than BEPs did and, therefore, ate more of them when shock was no longer a threat. We cannot definitively rule out this possibility, but it is not a likely explanation given that BEPs were willing to tolerate higher shock intensities for this type of palatable food. An alternate possibility for increased consumption of M&Ms by BERs to match that of BEPs is that the M&Ms were now accessible free of shock and previous association between this food and aversive footshock could have increased the salience and appetitive quality of this food when freely accessible. shows that even BEPs ate more palatable food kcals than usual when they ate M&Ms vs. Oreos. This increased intake likely reached a ceiling effect in BEPs. As for BERs, increased kcal intake in the presence of shock-free M&Ms (vs. Oreos) may have also been due to an increased salience and appetitive nature of this food from its previous forbidden-like quality. Dieters voluntarily restrain from highly palatable foods, and it is well-established that restraint from these foods increases their saliency and appetitive nature (35
). Recently our lab reported that even non-food cues associated with palatable food are enough to elicit overeating in rats (36
). A caveat to these conclusions, however, is that a test of M&M intake in the home cage was only performed once. We do not know if, with repetition, BERs would revert back to their typical BER status, consuming less M&M kcals than BEPs. It is possible that a subset of the BERs might have continued this BEP-like pattern with previously forbidden palatable food. This would suggest interesting genetic diversity within the BER phenotype. There is, however, evidence to suspect that BERs would have eventually returned to eating less M&Ms than BEPs, despite their now free access. This is based on the stubborn nature of the BEP/BER phenotype that we have observed in past studies. The BEP/BER phenotypes persist over time, across various experiences with hunger, with footshock, and with exposures to different kinds of palatable foods (see ref.17
for these tests). Furthermore, K. Klump and colleagues recently found that even ovariectomy did not abolish BEP/BER status in post-pubertal rats. Interestingly, female rats do not significantly converge into BEP/BER groups until puberty, raising a potentially critical role of reproductive hormones on the onset of binge-eating (personal communication, Oct. 2009).
Despite the limitations in the secondary tests conducted in this study, the main finding of increased motivation for palatable food in BEP compared to BER rats is important for several reasons. First, it extends the BEP phenotype to include an aspect that is understudied in binge-eating animal models yet is very salient in clinical binge-eating. Secondly, the action of non-food deprived, normal-weight rats to tolerate high levels of electric shock for a favored food should not be regarded as anything but strikingly abnormal and a powerful testament of motivation. This is emphasized by the fact that, in the past, we obtained similar behavior in rats but only when injected centrally with peptide YY, a powerful orexigenic (37
). Other studies using footshock to test for motivation in rats involved, not food, but drugs of abuse (38
). Hence, this study is unique in that untreated (drug-naïve) rats were found to willingly tolerate aversive levels of footshock, not for rewarding drugs but rewarding food. Thirdly, the results highlight the powerful role of palatable foods to trigger binge-eating. Given our observations in rodents, the power of palatable foods to motivate feeding even in the face of punishment may be more biologically rooted than contingent on complex cognitive processes (e.g., calorie-counting or cognitive disinihibition). This has important implications for treatment strategies and the prevention of relapse in humans with binge-eating disorders who must repeatedly encounter these substances in today's hedonic food environment.
Gene x environment interaction studies of human eating disorders are rare and very much needed (40
). The BEP/BER animal model of binge-eating represents a gene x environment interaction, with the environmental factor being the presence of palatable food. Palatable food has an effect on BEP rats that it does not have in BER rats. Our palatable food-centric environment is not likely to change. By identifying the genes that predispose some humans to react differently to palatable foods should guide novel treatments for bulimia, BED, and obesity caused by eating in the absence of hunger. These are treatments aimed at curbing an abnormal motivation for palatable foods and may also be effective on abnormal motivation for other appetitive stimuli (e.g., sex, alcohol, illicit substances, gambling). The BEP/BER model can be used as a vehicle to these gene discoveries.