Elsevier

Neuroscience & Biobehavioral Reviews

Volume 68, September 2016, Pages 714-726
Neuroscience & Biobehavioral Reviews

Review article
Inhibitory control in obesity and binge eating disorder: A systematic review and meta-analysis of neurocognitive and neuroimaging studies

https://doi.org/10.1016/j.neubiorev.2016.06.041Get rights and content

Highlights

Abstract

The ability to exercise appropriate inhibitory control is critical in the regulation of body weight, but the exact mechanisms are not known. In this systematic review, we identified 37 studies that used specific neuropsychological tasks relevant to inhibitory control performance in obese participants with and without binge eating disorder (BED). We performed a meta-analysis of the studies that used the stop signal task (N = 8). We further examined studies on the delay discounting task, the go/no-go task and the Stroop task in a narrative review. We found that inhibitory control is significantly impaired in obese adults and children compared to individuals with body weight within a healthy range (Standardized Mean Difference (SMD): 0.30; CI = 0.00, 0.59, p = 0.007). The presence of BED in obese individuals did not impact on task performance (SMD: 0.05; CI: −0.22, 0.32, p = 0.419). Neuroimaging studies in obesity suggest that lower prefrontal cortex activity affects inhibitory control and BMI. In summary, impairment in inhibitory control is a critical feature associated with obesity and a potential target for clinical interventions.

Introduction

Obesity is currently considered a global pandemic affecting more than one third of U.S. adults (Ogden et al., 2014, Swinburn et al., 2011) and 13% worldwide, a rate that has doubled since 1980 (World Health Organization, 2015). It is related to increased overall mortality for Alzheimer's disease (Misiak et al., 2012), cancer (Vucenik and Stains, 2012) and heart disease (Lu et al., 2014). Abdominal obesity is also associated with a substantial disease burden with increased risk of type 2 diabetes mellitus and cardiovascular disease (Alberti et al., 2005, Lakka et al., 2002, Lorenzo et al., 2003). Available treatments are often ineffective in modifying the lifestyle and eating behavior that lead to obesity (Fabricatore and Wadden, 2006), therefore the development of innovative treatments that can impact on these domains is now a public health priority.

Binge Eating Disorder (BED) is an eating disorder characterized by recurrent episodes of excessive food consumption accompanied by a sense of loss of control (American Psychiatric Association, 2013). It is the most prevalent type of eating disorder (Hudson et al., 2007) and it affects up to 25% of obese individuals seeking weight-loss treatment (Pull, 2004). Binge episodes have been proposed to be triggered by a breakdown of self-regulation caused by sudden increases in negative affect and tension (Munsch et al., 2012).

Impairment in executive function is consistently found in several neuropsychiatric syndromes (Etkin et al., 2013), including eating disorders (Van den Eynde et al., 2011). Inhibitory control, one of the fundamental components of executive function, can be operationalized as the overriding of a planned or already initiated action (e.g. responding to a stimulus, or seeking a reward) (Bari and Robbins, 2013). When experiencing strong impulses or urges to eat, a lack of inhibitory control may cause impulsive eating and lead to obesity (Appelhans, 2009). Inhibitory control is experimentally assessed with standardized and validated tests, such as the go/no-go task, stop-signal task (SST), Stroop task and delay discounting task (Chambers et al., 2009). These tasks are thought to measure different facets of inhibitory control. The go-no/go task and the SST are considered typical measures of response inhibition (Chambers et al., 2009). In the go-no/go task, participants are instructed to respond as quickly as possible (e.g. pressing a button) when a frequent go signal appears, but must inhibit the response when an infrequent stop signal occurs. Inhibitory control performance is assessed based on the percentage of responses to stop signals (errors). In the SST, the go signal is interrupted in some trials by a stop signal presented after it. Participants are instructed to cancel the go response when they are shown the stop signal. Typically, the more the presentation of the stop signal is delayed, the more difficult it is for the participant to withhold the response. This situation is usually interpreted with the race model (Logan and Cowan, 1984): whether a participant manages to withhold the response depends on the result of the competition of two independent processes: go and stop. The stop trial won’t be successful (resulting in a failure to inhibit the response) when the go process is completed before the stop process. Traditionally, the most used outcome measure in the SST is the stop signal reaction time (SSRT). The SSRT is calculated subtracting the stop signal delay (the delay between go and stop signal that allows correct inhibition on approximately 50% of the stop trials) from the mean reaction time (mean reaction time to a go trial). Shorter the SSRT better the inhibitory performance. The Stroop task is also used as a measure of response inhibition (Potenza et al., 2003), although it has been suggested that other processes such as conflict resolution and response selection could also be involved (Chambers et al., 2009). In a basic version, the Stroop task is comprised of three conditions. In the reading condition, the participant reads words written in black ink. In the color naming condition, the participant has to name the colors of a series of colored squares. Finally, in the inhibition condition, the participant is presented a series of words written in different colors and is asked to name which color the words are written in. The words are printed in an ink that is incongruent with the word (for example, the word ‘red’ is written in green ink). The participant needs to process task-relevant color information (ink) and inhibit prepotent processing of conflicting task-irrelevant information (word). Performance is measured with completion time (longer response time = worse inhibitory control). In the delay discounting task, poor inhibitory control is defined as the tendency to choose immediate, smaller rewards over larger but postponed ones in a series of trials (steep discounting of value as a function of time). The delay discounting task has been suggested to recruit more affectively charged cognitive processes compared to the previously described response inhibition paradigms (Bari and Robbins, 2013). Inhibitory control as measured in the above laboratory tests is thought to be a relatively stable and general trait which affects several specific domains/contexts (e.g. food intake, smoking or substance abuse) (Bari and Robbins, 2013).

The relationship between inhibitory control, obesity and binge eating has not been fully understood yet. In particular, it is not clear if inhibitory control processes are impaired in obesity in general or more specifically related to binge eating behavior. Since BED has been associated with high co-morbidity with other psychiatric disorders (Hudson et al., 2007, Kessler et al., 2013) and medical disorders (Javaras et al., 2008), it is important to study the specific neurocognitive mechanisms that characterize it, distinguishing them from those that underlie obesity without BED. Schag et al., in a narrative review, reported that obese participants with BED had increased scores in self-report measures of food-related impulsivity compared with normal weight controls and that impulsivity was more pronounced in BED individuals compared to obese participants without BED (Schag et al., 2013). Other studies found lower inhibitory control performance (as measured by SST) to predict the outcome of a weight loss program in obese children and adolescents (Kulendran et al., 2014, Nederkoorn et al., 2007). Nederkoorn and colleagues specifically assessed binge eating: only 2 children of the 26 who participated in the study had binge episodes. The above findings suggest that dysfunctional inhibitory control could be an underlying cognitive deficit in people who gain weight regardless of binge eating patterns. A systematic assessment of the available literature on inhibitory control tasks in obese individuals with and without BED appears to be indicated to gain a better understanding of this issue.

Several lines of clinical evidence suggest that inhibitory control of eating behavior is regulated by the neural circuitry involving the frontal cortex (Knoch and Fehr, 2007, Szczepanski and Knight, 2014). First, frontal lobe dysfunctions have been shown to be associated with altered eating behaviors (Alonso-Alonso and Pascual-Leone, 2007). Hyperphagia as a clinical sign has been reported in neurologic syndromes that are characterized by frontal lobe impairment such as fronto-temporal dementia (Ikeda et al., 2002, Piguet, 2011, Whitwell et al., 2007), Klein-Levin syndrome (Landtblom et al., 2002) and the “Gourmand syndrome” (Regard and Landis, 1997). Second, hyperphagia and overweight were common in patients who underwent frontal leucotomy, a surgical procedure that disconnected the frontal lobes from the rest of the brain in an attempt to treat severe mental illness (Freeman and Watts, 1950). Third, frontal lobe dysfunction has been suggested to be the cause of altered eating behavior in Prader-Willi syndrome, a genetic disorder associated with developmental delay, obesity and hyperphagia (Ogura et al., 2008). A recent neuroimaging study comparing obese participants with Prader-Willi syndrome to obese participants without the syndrome found post-meal hypoactivation of the dorsolateral prefrontal cortex (PFC) during response to food vs non-food images (a measure of inhibitory control)(Holsen et al., 2012). Finally, symptoms related to dysfunction of the frontal cortex have also been reported in obesity with BED: for instance, participants with BED showed higher scores in the Frontal Systems Behavior Scale, a measure of neurobehavioral traits associated with the PFC (Boeka and Lokken, 2011).

Functional neuroimaging studies are important to understand the neuroanatomical and functional mechanisms of inhibitory control deficits in obesity and binge eating, and to devise cognitive and brain targets for novel neuromodulatory techniques (Alonso-Alonso, 2013).

The aims of this systematic review and meta-analysis are twofold: a) to evaluate the presence of alterations in inhibitory control performance in obese participants with and without BED; and b) to assess neural correlates of inhibitory control performance in obese participants compared to normal weight controls. Accordingly, the proposed systematic review will address the following questions:

  • 1.

    Do obese participants have impairments in inhibitory control indexed by performance in specific neurocognitive tests compared to normal weight controls?

  • 2.

    Do obese participants with binge eating disorder have more severe impairments in inhibitory control compared to obese participants without the disorder?

  • 3.

    Is neural activation in the prefrontal cortex measured by neuroimaging techniques altered in obese participants compared to normal weight controls during a standard inhibitory control task?

We hypothesize that inhibitory control is impaired in obese participants compared to normal weight controls and in obese participants with BED compared to obese controls; we also expect to find reduced PFC activation during inhibitory control tasks in obese participants compared to controls.

Section snippets

Search strategy

The review process was conducted according to the principles of the PRISMA-Statement (Liberati et al., 2009, Moher et al., 2009, Shamseer et al., 2015). Searches were conducted up to April 2015; all relevant articles published before the end of April 2015 were considered for inclusion. We did not establish any restrictions on publication date. The PRISMA flow chart for study inclusion is reported in Fig. 1. Entire PubMed, EMBASE and PsychInfo were searched for published experimental studies

Study selection

Searches resulted in 1793 eligible studies of which 37 met inclusion criteria. Fig. 1 provides a flow chart with reasons for exclusion and Table 1, Table 2, Table 3 summarize the details of the studies included. Inhibitory control has shown significant differences in performance between children and young adults (Williams et al., 1999) likely as a consequence of different developmental stages. Therefore, the studies reporting on adults (Table 1) and children and adolescents (Table 2) will be

Discussion

Our main findings are that there is a decrease in inhibitory control performance in adult obese participants without BED compared to controls and in obese children and adolescents compared to controls. There was no significant difference in inhibitory performance in obese participants with and without BED. Functional neuroimaging of neural activation during inhibitory control tasks in obese participants with BED compared to obese participants without BED reveal a consistent pattern of reduced

Conclusions and future directions

In conclusion, we found sufficient evidence to support the presence of inhibitory control deficits in obese participants compared to controls. No significant differences in inhibitory control were found in obese participants with BED compared to obese participants without BED. Impairments in inhibitory control assessed with standardized neurocognitive tests appear thus to be associated with obesity independently from binge eating. Neuroimaging studies suggest that reduced function in an

Conflict of interest

Prof. Soares has participated in research funded by Forest, Merck, BMS, GSK, Johnson&Johnson and has been a speaker for Pfizer and Abbott. All other authors declare that they have no conflict of interests.

Acknowledgements

We thank Dr. Bongers, Dr. Nederkoorn and Dr. Voon who kindly provided information on their studies and additional data. We also wish to thank Emily Couvillon at the Texas Medical Center Library for her assistance in database search.

The present study was supported in part by the Pat Rutherford, Jr. Endowed Chair in Psychiatry (Jair C. Soares). Danilo Arnone’s research is supported by the Academy of Medical Sciences (AMS-SGCL8).

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