Elsevier

NeuroImage

Volume 83, December 2013, Pages 669-678
NeuroImage

The role of neural impulse control mechanisms for dietary success in obesity

https://doi.org/10.1016/j.neuroimage.2013.07.028Get rights and content

Highlights

  • Behavioral impulse control is linked to future dietary success.

  • Brain activity related to impulse control correlates with dietary success.

  • Functional connectivity of reward and control areas is linked to dietary success.

  • Simultaneously, this connectivity correlates with behavioral impulse control.

  • fMRI signals can be highly informative for real-world outcome measures.

Abstract

Deficits in impulse control are discussed as key mechanisms for major worldwide health problems such as drug addiction and obesity. For example, obese subjects have difficulty controlling their impulses to overeat when faced with food items. Here, we investigated the role of neural impulse control mechanisms for dietary success in middle-aged obese subjects. Specifically, we used a food-specific delayed gratification paradigm and functional magnetic resonance imaging to measure eating-related impulse-control in middle-aged obese subjects just before they underwent a twelve-week low calorie diet. As expected, we found that subjects with higher behavioral impulse control subsequently lost more weight. Furthermore, brain activity before the diet in VMPFC and DLPFC correlates with subsequent weight loss. Additionally, a connectivity analysis revealed that stronger functional connectivity between these regions is associated with better dietary success and impulse control. Thus, the degree to which subjects can control their eating impulses might depend on the interplay between control regions (DLPFC) and regions signaling the reward of food (VMPFC). This could potentially constitute a general mechanism that also extends to other disorders such as drug addiction or alcohol abuse.

Introduction

Obesity is a major and increasing worldwide health problem due to its high prevalence and severe medical consequences (Bray, 2004). A variety of factors in the development and maintenance of obesity are currently discussed, including psychological (e.g., Ng and Jeffery, 2003, Rodin et al., 1989, Rothemund et al., 2007, Torres and Nowson, 2007, Weygandt et al., 2012), behavioral (e.g., Bellisle et al., 2004, Hays and Roberts, 2008), genetic (e.g., Dina et al., 2007, Frayling et al., 2007), and endocrinological (e.g., Ahima, 2008, Farooqi et al., 2007, Klok et al., 2007, Page et al., 2011, Rosenbaum et al., 2008). Within the latter framework, also (insufficient) cerebral insulin suppression during stressful events is discussed, a topic especially referred to in the literature on the ‘selfish-brain theory’ (cf. Peters, 2011). Among psychological factors, impaired impulse control is believed to play an important role for obesity (e.g., Batterink et al., 2010, Kishinevsky et al., 2012, Masheb and Grilo, 2002, McGuire et al., 2001, Nijs et al., 2010, Weller et al., 2008) as well as for other major health problems, such as drug addiction (e.g., Barrós-Loscertales et al., 2011, Goldstein et al., 2007, Volkow et al., 2004) and alcohol abuse (e.g., Li et al., 2009). The association of obesity and impulse control has been tested in behavioral studies that found that impulse control measured with delay discounting (DD) paradigms or questionnaires is negatively associated with body weight (Masheb and Grilo, 2002, McGuire et al., 2001, Weller et al., 2008). Neuroimaging studies have investigated the neural foundations of decision-making and impulse control in eating-related tasks (Hare et al., 2009, Hare et al., 2011). They suggest that food decisions in self-reported dieters rely not only on value signals in ventromedial prefrontal cortex (VMPFC), but also on the degree to which control signals in dorsolateral prefrontal cortex (DLPFC) exert an influence over these value signals. Studies searching for neural correlates of longitudinal weight changes and impulse control exclusively investigated non-dieting subjects and either they failed to identify such signals (Batterink et al., 2010), or they were able to identify neural predictors of weight changes but were not able to link them to control behavior (Kishinevsky et al., 2012). Correspondingly, the complex relation between neurobehavioral parameters of impulse control and dietary success in obese subjects is still unclear.

Here, we investigated the link between behavioral impulsivity and their neural correlates acquired before the onset of a twelve-week low calorie diet in obese subjects and the corresponding weight loss obtained after the diet. We separately assessed the prognostic information contained in behavioral parameters of control, its neural correlates and the network connectivity of areas involved in decision-making. We found that a) higher impulse control is associated with better dietary success, b) future dietary success correlates with local brain activity in reward-related areas and areas involved in impulse control, and finally c) dietary success correlates with functional connectivity between reward- and control-related brain structures reflecting the degree of control applied to food-decisions.

Section snippets

Participants

Participants were first invited via newspaper announcements and notifications in hospitals to participate in a larger dietary study. The inclusion criteria for this study were an age in the range of 18 to 70 years and a BMI of at least 30 when no cardiovascular risk factor such as arterial hypertension was present or a BMI of at least 27 when such a factor was present. Subjects with endocrine diseases, malabsorption, food allergies, hypertonia, recent changes in smoking behavior, and

Analysis 1: Association of behavioral impulsivity and dietary weight loss

In this analysis, we investigated the degree to which future dietary weight loss is associated across subjects with pre-diet behavioral impulsivity assessed in a food-specific delayed gratification task by calculating the Pearson correlation coefficient for the two variables. The results show that higher impulsivity was associated with poorer dietary success (r =  0.42; p = 0.048), i.e. subjects with better impulse control lost more weight. See Fig. 2 for details.

Analysis 2: Association of brain activity and dietary weight loss

Here, we assessed the degree to

Discussion

In this study, we demonstrate that behavioral impulse control and neural substrates of decision-making measured preceding a diet contain information for the weight loss obtained by middle-aged obese subjects during the twelve-week low calorie diet. Moreover, we show that functional connectivity between brain regions involved in impulse control and reward signaling measured before the onset of the diet correlates with dietary success and simultaneously the degree of control applied to

Conclusion

To summarize, we have shown that behavioral impulse control measures and neural substrates of decision-making measured preceding a diet contain information for the degree of dietary weight loss of obese subjects. Moreover, the study shows that connectivity between brain regions involved in impulse control and reward signaling reflects dietary success in obese subjects and simultaneously the degree of control applied to food-decisions. Specifically, stronger connectivity of these regions is

Role of the funding source

This work was funded by a clinical research group (KFO218/1) of the German Research Foundation and the Bernstein Computational Neuroscience Program of the German Federal Ministry of Education and Research (Grant Number 01GQ0411). The funding sources had no involvement in the study design, the collection, analysis, and interpretation of data, the writing of the report, and the decision to submit the paper for publication.

Disclosure statement

The authors report no biomedical financial interests or potential conflicts of interest in the context of this work.

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