A Review of the Relationship Between Eating Behavior, Obesity and Functional Brain Network Organization

Shannon D. Donofry; Chelsea M. Stillman; Kirk I. Erickson

Disclosures

Soc Cogn Affect Neurosci. 2020;15(10):1157-1181. 

In This Article

Abstract and Introduction

Abstract

Obesity is a major public health issue affecting nearly 40% of American adults and is associated with increased mortality and elevated risk for a number of physical and psychological illnesses. Obesity is associated with impairments in executive functions such as decision making and inhibitory control, as well as in reward valuation, which is thought to contribute to difficulty sustaining healthy lifestyle behaviors, including adhering to a healthy diet. Growing evidence indicates that these impairments are accompanied by disruptions in functional brain networks, particularly those that support self-regulation, reward valuation, self-directed thinking and homeostatic control. Weight-related differences in task-evoked and resting-state connectivity have most frequently been noted in the executive control network (ECN), salience network (SN) and default mode network (DMN), with obesity generally being associated with weakened connectivity in the ECN and enhanced connectivity in the SN and DMN. Similar disruptions have been observed in the much smaller literature examining the relationship between diet and disordered eating behaviors on functional network organization. The purpose of this narrative review was to summarize what is currently known about how obesity and eating behavior relate to functional brain networks, describe common patterns and provide recommendations for future research based on the identified gaps in knowledge.

Introduction

Within the last several decades, the prevalence of obesity has risen dramatically, with over one-third of American adults meeting clinical criteria for the condition [body mass index (BMI) ≥ 30; Ogden et al., 2014]. Numerous studies have demonstrated an adverse effect of having overweight or obesity on health and psychosocial functioning (Kopelman, 2000; Wadden and Stunkard, 2002; Finkelstein et al., 2005; Cawley and Meyerhoefer, 2012), making the rise in rates of obesity a significant threat to public health. Obesity is associated with higher mortality and increased rates of cardiovascular disease, diabetes, hypertension, metabolic syndrome, depression (Stunkard et al., 2003), anxiety (Gariepy et al., 2010) as well as neurological illnesses such as Alzheimer's disease (Kivipelto et al., 2005). Further, individuals with overweight and obesity are more likely to experience discrimination in employment, education and health care settings (Cawley and Meyerhoefer, 2012). Obesity is one of the most costly conditions to treat, with obesity-related illness comprising up to 21% of yearly healthcare expenditures in the USA (Cawley and Meyerhoefer, 2012). These findings highlight the fundamental importance of identifying mechanisms underlying obesity to facilitate the development of more effective prevention and treatment interventions.

Obesity is associated with deficits in executive functioning, suggesting that functional differences in the brain regions that support these functions may contribute to the etiology of obesity. Executive function is defined as the ability to select appropriate actions based on ongoing evaluation of environmental demands, current goals, current emotional state, past experiences and social norms and encompasses elements of decision making and behavioral self-regulation (e.g. control of reward-driven impulses; Baumeister and Heatherton, 1996; Heatherton and Wagner, 2011). There is evidence that components of executive functioning, such as self-regulation, as well as the exertion of control over reward-driven impulses may be impaired in obesity (Schag et al., 2013). For instance, individuals with obesity exhibit difficulty inhibiting automatic responses on inhibitory control tasks, tending to engage in habitual or overlearned behaviors (Batterink et al., 2010; Davis et al., 2010; Gunstad et al., 2007). Individuals with obesity also show a preference for smaller, immediate rewards over larger, delayed rewards relative to normal weight individuals (Weller et al., 2008). Importantly, steeper discounting of delayed future rewards has been associated with increased purchasing (Nederkoorn et al., 2009) and consumption (Nederkoorn et al., 2009; Appelhans et al., 2011) of highly palatable, calorie-dense foods, as well as binge eating disorder (BED) (Davis et al., 2010). These findings indicate that deficits in self-regulation and reward processing may predispose some individuals to obesity by influencing decisions regarding diet and exercise.

Poor self-regulation has also been shown to predict the probability of treatment failure during a weight loss intervention, with more impulsive individuals losing less weight than those with a greater capacity for self-regulation (Nederkoorn et al., 2007). Indeed, greater capacity for self-regulation has been associated with more frequent consumption of healthy low-calorie foods and regular engagement in physical activity, both in healthy weight adults and adults with obesity (Wills et al., 2007; Gerrits et al., 2010; Crescioni et al., 2011). Conversely, impaired self-regulation is associated with consumption of high-calorie foods and sedentary lifestyle, even during concerted weight loss attempts (Crescioni et al., 2011). Moreover, one study demonstrated that specifically targeting deficits in self-regulation in a weight loss intervention promoted long-term maintenance of weight loss (Wing et al., 2006). These data highlight the central role of self-regulation and reward processing in the etiology of obesity. These intervention studies also provide evidence that deficits in self-regulation and reward processing are modifiable via intervention and that mitigation of these deficits improves weight loss and weight maintenance outcomes.

In this review, we will first synthesize the literature on brain networks and obesity among adults. We will focus specifically on how functional network organization relates to obesity, as well as aberrant eating behaviors such as binge eating. We will then review what is known from longitudinal and clinical trial data regarding the effects of weight loss and specialized diets (e.g. the Mediterranean diet) on functional connectivity patterns. We seek to address the following questions: (i) How are functional brain networks that support self-regulation and reward processing associated with obesity and maladaptive eating behaviors? (ii) Can weight loss (via any means) modify obesity- and eating-related functional connectivity patterns? (iii) Are there specific nutrient or dietary patterns that are more effective than others for influencing brain connectivity patterns? This review focuses on evidence from adults with overweight and obesity, though it is important to note that there is a growing literature exploring these questions in children and adolescents (e.g. Chodkowski et al., 2016; Liang et al., 2014; Moreno-Lopez et al., 2016) including prospective investigations of how regional brain activation relates to future weight gain (e.g. Yokum et al., 2011). This research, which is critical to understanding the development of obesity and its impact on maturation, is beyond the scope of this review.

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