Neurobehavioral Inhibition of Reward‐driven Feeding: Implications for Dieting and Obesity

Abstract

The development of effective weight loss interventions requires a thorough understanding of the motivational factors that drive and inhibit the overconsumption of food. Obesity was once believed to result purely from disruptions of homeostatic mechanisms controlling food intake. However, it is increasingly recognized that much of the excess caloric intake in obesity is driven by pleasure or the rewarding properties of readily available palatable food (1,2). It is important to note that the motivation underlying this reward-driven or "hedonic" feeding appears to have a different neurophysiological basis than homeostatic controls over energy balance, though the hedonic and homeostatic systems do interact (3). Recently, a surge of research has linked the appetitive motivation to consume palatable food to activation of the mesolimbic dopaminergic system, a neural pathway also implicated in drug addiction and addictive behaviors such as gambling (4). As a result of these findings, a view of obesity as a "disorder of appetitive motivation" has gained prominence among a growing number of obesity researchers. However, a model of hedonic feeding based purely on appetitive motivation has limitations, including an inability to explain instances of feeding behavior parsimoniously in both dieters and nondieters. The aim of this review is to summarize the strengths and weaknesses of the appetitive model, present the extant literature linking control of hedonic feeding to inhibitory processes localized in the prefrontal cortex (PFC), and delineate a theoretical model in which hedonic feeding is viewed as the product of an interaction between appetitive motivation and inhibitory control. The human feeding system leaves room for dessert. Humans will continue to consume palatable food even after energy requirements have been met and homeostatic satiety signals have been engaged. This consumption is clearly not driven by an acute need for calories, and hedonic factors (taste, pleasure, reward) play a large role in this type of feeding. Simply stated, the hedonic feeding model holds that palatable food consumption in the absence of an energy deficit (or the physiological signals associated with energy deficit) is driven by an appetitive motivational state referred to as "hedonic hunger" (2), and not by homeostatic controls over feeding. (For discussion of the role of reward in homeostatic feeding, which may be subjectively associated with escape from hunger rather than the pleasant tastes and textures of palatable food, see ref. (5).) Hedonic feeding has an evolutionary basis. Modern humans preferentially overconsume sweet and high-fat palatable foods (6). Hominids subsisted as hunter-gatherers for the majority of evolutionary history and access to these types of foods (e.g., fruits, animal meat) was presumably limited. Hunting or prolonged foraging would often have been required to obtain sweet and high-fat foods, and it is likely that the capacity to find these foods pleasurable and highly rewarding motivated ancestral humans to engage in these food-seeking behaviors. After expending many calories to obtain them, consuming palatable foods in excess of one's current need for calories would have allowed some energy to be stored as fat, which could buffer against starvation in instances of short-term food shortage or famine. Thus, the ability of palatable food to promote overconsumption by overriding satiety signals was preserved in our species (3,7). In modern times, when palatable food is abundant and accessible, our evolutionarily derived capacity for hedonic feeding has contributed to an epidemic of overconsumption and obesity. Hedonic feeding is driven by both sensory and motivational processes that also play a role in drug addiction. The sensory pleasure resulting from tasting and ingesting palatable foods (and drugs) has been referred to as "liking." Liking is distinct from the motivational process of "wanting," which refers to the incentive value of a stimulus (8). Although humans generally want the foods they like, and like the foods that they want, liking and wanting have separate neurophysiological underpinnings and are dissociable under several circumstances. For example, drug-addicted individuals report a greater desire to consume a drug over time despite a gradual decrease in the degree to which they find consumption pleasurable, and selective lesioning of the neural system underlying wanting (described below) results in animals who show affective facial expressions of pleasure upon tasting palatable foods but are unmotivated to obtain them (8). Thus, although the sensory process of liking and the motivational process of wanting typically converge with respect to individual foods, instances of dissociation indicate separate neural underpinnings. Some have suggested that wanting plays a stronger role in obesity than liking given that obese individuals do not consistently appear to derive greater pleasure from tasti