Behind binge eating: A review of food-specific adaptations of neurocognitive and neuroimaging tasks
Introduction
Binge eating, or the consumption of an objectively large amount of food in a discrete time period while experiencing a sense of “loss of control” [1], is associated with significant impairment and represents a major public health concern. Binge eating disorder (BED), defined in part by at least weekly binge eating for a three-month period, is the most prevalent eating disorder, estimated to impact 1.9% to 3.9% of the population [2], [3]. Roughly 30–42% of individuals with BED also meet criteria for obesity [2], [4], [5], [6], and BED shares many overlapping medical complications and health risks with obesity, including cardiovascular disease, diabetes, and metabolic syndrome [3], [7], [8]. Independent of the high degree of comorbidity with obesity, individuals with BED may experience increased levels of morbidity and mortality [9], [10]. BED is also associated with increased likelihood of mood and anxiety disorders [11], [12], [13], [14] and decreased quality of life [15], [16]. Diagnosis of bulimia nervosa (BN), like BED, requires regular binge eating in the last three months but also requires recurrent compensatory behaviors, including but not limited to self-induced vomiting [1]. BN affects 1–3% of women [1], [2] and also is associated with significant disability, medical complications, and high rates of comorbid psychopathology [1], [17], [18]. Anorexia nervosa (AN) has the highest mortality rate of any mental illness, and more than half of individuals who start with pure restricting-type AN develop regular binge eating and/or purging (i.e., the binge-eating/purging subtype of AN, or AN-BP) [19]. High levels of impairment, morbidity, and mortality in populations who engage in binge eating highlight a crucial need for effective treatments.
Depending on the disorder and setting, evidence-based treatments for binge eating produce only modest long-term outcomes for 30–60% of individuals seeking treatment [4], [20], [21], [22], [23]. Given the costly individual and societal impact of binge eating, identification and characterization of neuropsychological abnormalities that could serve as targets for new prevention efforts and interventions are crucial. The National Institute for Mental Health has supported a Research Domain Criteria (RDoC) initiative to examine shared mechanisms across diagnoses [24]. The study of unique mechanisms underlying different categorical eating disorder groups and presentations is useful and important, but identification of potential shared alterations and deficits across eating disorder diagnostic groups that have behavioral symptoms in common may ultimately improve treatment for all presentations. As a result, prior reviews and meta-analyses have integrated findings from individuals with BN, BED, AN-BP, and subthreshold binge eating behavior e.g., [25], [26], [27]. In the current review, we discuss neurocognitive tasks that have been or could be used to shed light on the mechanisms that may contribute to binge eating.
To date, research suggests that an imbalance between reward processes that promote consumption and self-regulatory control processes that limit food consumption may contribute to binge eating [28], [29], [30]. A variety of well-established stimulus-exposure paradigms and neurocognitive tasks have been used to gather neural and behavioral data in reward and self-regulatory domains and across a range of psychiatric disorders. Many of these tasks use generic stimuli such as letters, numbers, or neutral images to assess global deficits in these constructs. Because an imbalance in reward and control systems has been implicated in other psychopathologies (e.g., [31], [32], [33], [34]), use of these general tasks in binge-eating populations is especially useful for identifying transdiagnostic neurocognitive mechanisms. However, improving targeted interventions for binge eating requires an understanding of the unique alterations in interacting reward and control-related processes that specifically underlie dysregulated eating behavior. Tasks that use symptom-specific (i.e., food- or eating-related) stimuli can isolate the distinct or perhaps more pronounced neurocognitive deficits that predispose individuals to or result from eating problems. Several neuroimaging studies in the fields of substance and alcohol use disorders have used both general and substance-specific versions of tasks or stimuli within the same sample of individuals to isolate substance-specific behavioral and neural circuit alterations [35], [36], [37]. Few studies focused on binge eating pathology have followed a similar model, much less combined these two task types with neuroimaging. A thorough understanding of these symptom-specific tasks is necessary to adequately interpret alterations within binge-eating populations.
Moreover, results of existing investigations in binge-eating populations have been somewhat mixed. Some studies have and others have not detected altered behavioral task performance in individuals with binge eating compared with controls, and both hyper- and hypoactivation in reward and self-regulatory control circuits have been documented in binge-eating populations relative to controls (e.g., [38], [39], [40], [41], [42]). Given these inconsistent findings, optimal methods for reliably assessing the contributions of these reward and control-related processes and their neural correlates to binge eating are unclear.
Prior meta-analyses and reviews provide helpful syntheses of the results of neuroimaging and neurocognitive studies that assess general and symptom-specific impulsivity, reward responsivity, inhibitory control deficits, and reward-related decision-making alterations in binge-eating populations [25], [43], [44], [45], [46]. Several reviews also provide comprehensive summaries of the ventral and dorsal fronto-striatal reward and control-related circuit abnormalities hypothesized to be integral to binge eating and other behaviors [30], [44], [47], [48], [49]. However, to date, no paper has focused primarily on tasks that assess food-specific alterations in these processes among individuals with binge eating.
The purpose of the current review is to summarize and discuss the advantages and disadvantages of food-specific adaptations of well-established tasks designed to assess reward-related processes and self-regulatory control, with or without concurrent neuroimaging. The current review focuses on reward responsivity, reward-related decision-making, and inhibitory control assessments because of robust research findings implicating these constructs in binge eating [25], [27], [42], [43], [45], [50] and the proliferation of food-adapted measures for these constructs. Of note, food-specific versions of tasks that assess and train other cognitive constructs, such as attentional bias to food cues [51], [52], [53], [54] and food-specific memory bias [55], have been applied to binge-eating populations, and new studies are constantly emerging in this nascent field. However, the overwhelming majority of the literature has focused on the roles of self-regulation and reward-based processes in binge eating. Thus, we highlight these areas in detail to provide an in-depth analysis of food-specific tasks designed to investigate these constructs.
A summary of the food-specific tasks that have been used to study binge-eating populations are presented in Table 1 for reference, but we include example findings only for illustrative purposes. Additional food-specific task adaptations have only been studied in healthy or overweight populations, but because their application to binge eating may significantly improve our understanding of this transdiagnostic behavior, we describe these tasks as well. We discuss the advantages and limitations of food-specific approaches and outline directions for future research. By focusing on design considerations, this review is meant to serve as a methodological reference for researchers and a guide for future investigations within this population.
Section snippets
Reward responsivity, valuation, and learning
Reward abnormalities have been implicated consistently in binge eating. Literature dedicated to the understanding of reward has parsed this construct into three distinct components: liking, wanting, and learning [56]. In this model, liking refers to the hedonic valuation of a rewarding stimulus; wanting refers to the incentive salience of a stimulus; learning refers to associations formed between a predictive cue and the likelihood of a subsequent reward. Theoretical models posit that
Self-regulatory control
The broad construct of self-regulatory control encompasses attention, decision-making, response selection, action execution, conflict monitoring, response inhibition, and the ability to regulate emotional responses [93]. Difficulties with motor inhibitory control may be particularly relevant to understanding binge eating, since a sense of “loss of control” over eating is a defining, key element of binge eating episodes [94]. This sense of loss of control has, in fact, been suggested to be a
Food-specific task challenges and considerations
Results of studies using food-specific adaptations of classic paradigms have helped to identify differences between individuals with and without binge eating [25], [30], [44], [45], [46], [47], [48], [49]. However, these paradigms have several limitations. Slight differences in task designs translate to the assessment of slightly different constructs using the same task type, and the extent to which increased food-specific reward responsivity and impaired control over eating-related responses
Future directions
Review of existing food-specific task adaptations and consideration of the methodological challenges unique to these tasks and the study of binge-eating populations suggest several directions for future study. First, future research should replicate previous designs. The exact same food-specific task is rarely used twice, and traditional and food-specific tasks are rarely matched on all parameters, thereby making it difficult to isolate consistent correlates and/or predictors of binge eating.
Conclusion
Methodological inconsistencies and the limited ecological validity of existing paradigms make it difficult to draw definitive conclusions about the reward- and control-related alterations that may contribute to binge eating. However, replication, continued development of food-specific adaptations of traditional neurocognitive tasks, and creative combinations of these tasks with neuroimaging and the study of eating behavior have potential to reveal the precise mechanisms of this behavior.
Acknowledgements
Preparation of this manuscript was supported in part by the National Institutes of Health (F31 MH097406 and F32 MH108311 to LAB). Dr. Michael Lowe is a consultant to the Renfrew Center for Eating Disorders.
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