High definition transcranial pink noise stimulation of anterior cingulate cortex on food craving: An explorative study

Abstract

Dysfunctional neural activity in the cortical reward system network has been implicated in food addiction. This is the first study exploring the potential therapeutic effects of high definition transcranial pink noise stimulation (HD-tPNS) targeted at the anterior cingulate cortex (ACC) on craving and brain activity in women with obesity who showed features of food addiction (Yale Food Addiction Scale score of ≥3). Sixteen eligible females participated in a randomized, double-blind, parallel group study. Participants received six 20-minute sessions of either 1 mA (n = 8) or sham (n = 8) stimulation with HD-tPNS over two weeks. Anode was placed above the ACC (Fz) with 4 cathodes (F7, T3, F8, and T4). Food craving was assessed using the Food Cravings Questionnaire State (FCQ-S) and brain activity was measured using electroencephalogram (EEG). Assessments were at baseline, and two days, four weeks, and six weeks after stimulation. A 22% decrease (mean decrease of −1.11, 95% CI -2.09, −0.14) was observed on the 5-point ‘intense desire to eat’ subscale two days after stimulation in the HD-tPNS group compared to sham. Furthermore, whole brain analysis showed a significant decrease in beta 1 activity in the ACC in the stimulation group compared to sham (threshold 0.38, p = 0.04). These preliminary findings suggest HD-tPNS of the ACC transiently inhibits the desire to eat and, thus, warrants further examination as a potential tool in combating food craving.

Introduction

Obesity continues to be a significant public health concern. In 2014, the World Health Organization (WHO) estimated that 1.9 billion adults were overweight and 600 million were obese globally (World Health Organization, 2016). Efforts to curb the obesity epidemic have not had significant wide-spread success (Mann et al., 2007). Approaches that target the underlying drive to overeat and enable an individual to exist in an obesogenic environment without overconsumption could be beneficial.

Craving can be defined as the intense persistent desire for a certain stimulus. Studies have shown a strong link between craving and high fat/high sugar foods (Kelley et al., 2002, Kringelbach et al., 2003). The rewarding properties of certain foods can result in neural activation patterns and specific behaviors seen in other addictions (Pelchat, 2009), as defined by the Diagnostic and Statistical Manual of Mental Disorder- IV (DSM-IV). The Yale Food Addiction Scale (YFAS) is a validated tool used to identify those that display signs of food addiction similar to the DSM-IV characteristics of substance addiction (Gearhardt, Corbin, & Brownell, 2009).

Neuroimaging studies using electroencephalogram (EEG) (De Ridder et al., 2016b, De Ridder et al., 2016c) have shown that food craving among individuals with obesity may be associated with abnormal brain activity in multiple interacting brain networks, more specifically the anterior cingulate cortex (ACC) (principal cortical area in the salience network), dorsal medial prefrontal cortex (dmPFC), pregenual anterior cingulate cortex (pgACC), dorsal anterior cingulate cortex (dACC) and precuneus, as well as the parahippocampal area. The ACC is involved in craving, both for alcohol, nicotine, cocaine, and food. The areas for food craving and craving for other substances are adjacent in the ACC. Therefore, the ACC could be a good target for neuromodulation in order to decrease food craving in individuals with features of food addiction.

Studies assessing the effects of non-invasive neurostimulation using repetitive transcranial magnetic stimulation (rTMS) and transcranial direct stimulation (tDCS) on the dorsolateral prefrontal cortex (DLPFC) to decrease food cravings have shown positive encouraging results (McClelland, Bozhilova, Campbell, & Schmidt, 2013). These findings indicate that overeating could/may be decreased via a top-down approach by modulating the excitability of the DLPFC (perhaps through increasing inhibitory control), and consequently suppressing the reward network involved in food craving (Bravo et al., 2016, Gluck et al., 2015, Ljubisavljevic et al., 2016, Potenza and Grilo, 2014). Another approach to combating food craving among individuals with obesity would be to target the desire to eat using a ‘bottom-up’ strategy, focusing on reducing the salience attached to food and, thus, the urge to eat (De Ridder et al., 2016b). The ACC, a higher-order executive control area of the salience network has been reported to play a role in the pleasurable aspects of food (hedonistic eating) and, thus, influences overeating (Sescousse, Redouté, & Dreher, 2010). Although not in food addicted individuals, it has been shown in a case report that rTMS targeting the ACC induced a three-week reduction in alcohol craving (De Ridder, Vanneste, Kovacs, Sunaert, & Dom, 2011b). Moreover, a following case study reported that an alcohol dependent patient remained free of alcohol intake for more than 18 months after having an electrode implanted over the ACC (De Ridder et al., 2016a). The mechanistic similarities in alcohol and food craving mean that the ACC is a plausible target to curb food craving.

Previous non-invasive neuromodulation studies for food craving have utilized rTMS and tDCS (McClelland et al., 2013). Another technique, transcranial pink noise stimulation (tPNS) has yet to be examined. The use of smaller ‘high definition (HD)’ electrodes stimulation has an increased spatial specificity compared to traditional larger saline soaked sponge electrodes and is suitable for focal targeting of cortical regions (Datta et al., 2009, Edwards et al., 2013). With regards to pink noise (1/f), it has been postulated that this frequency spectrum resembles the naturally occurring signals in the self-organization of the brain (Van Orden et al., 2003), thus, when applied, may be more effective than standard electrical stimulation parameters. One possible explanation could be that the brain habituates to repetitive electrical parameters that are dissimilar to its own naturally occurring rhythm.

The aim of this study was to explore the effect of HD-tPNS of the ACC on food craving in individuals with obesity with features of food addiction. It was hypothesized that participants undergoing HD-tPNS targeted at the ACC will report decreased food craving compared to participants undergoing placebo tPNS. We further hypothesized that HD-tPNS will, compared to placebo, induce decreased activity in the ACC.