Association of Body Mass and Brain Activation during Gastric Distention: Implications for Obesity

Abstract

BackgroundGastric distention (GD), as it occurs during meal ingestion, signals a full stomach and it is one of the key mechanisms controlling food intake. Previous studies on GD showed lower activation of the amygdala for subjects with higher body mass index (BMI). Since obese subjects have dopaminergic deficits that correlate negatively with BMI and the amygdala is innervated by dopamine neurons, we hypothesized that BMI would correlate negatively with activation not just in the amygdala but also in other dopaminergic brain regions (midbrain and hypothalamus).Methodology/Principal FindingsWe used functional magnetic resonance imaging (fMRI) to evaluate brain activation during GD in 24 healthy subjects with BMI range of 20–39 kg/m2. Using multiple regression and cross-correlation analyses based on a family-wise error corrected threshold P = 0.05, we show that during slow GD to maximum volumes of 500 ml and 700 ml subjects with increased BMI had increased activation in cerebellum and left posterior insula, and decreased activation of dopaminergic (amygdala, midbrain, hypothalamus, thalamus) and serotonergic (pons) brain regions and anterior insula, regions that were functionally interconnected with one another.ConclusionsThe negative correlation between BMI and BOLD responses to gastric distention in dopaminergic (midbrain, hypothalamus, amygdala, thalamus) and serotonergic (pons) brain regions is consistent with disruption of dopaminergic and serotonergic signaling in obesity. In contrast the positive correlation between BMI and BOLD responses in posterior insula and cerebellum suggests an opposing mechanism that promotes food intake in obese subjects that may underlie their ability to consume at once large food volumes despite increasing gastric distention.

Food and Drug Reward: Overlapping Circuits in Human Obesity and Addiction

“…Indeed, gastric distention results in activation of the posterior insula, which is likely to reflect its role in the awareness of body states (in this case of fullness) (Wang et al 2008). Moreover, in lean but not in obese subjects gastric distention resulted in activation of the amygdala and deactivation of the anterior insula (Tomasi et al 2009). The lack of amygdalar response in obese subjects could reflect a blunted interoceptive awareness of bodily states linked with satiety (full stomach).…”

Mood Disorders and Obesity: Understanding Inflammation as a Pathophysiological Nexus

“…Evidence of amygdalar deficiency in modulating the activation in the orbitofrontal cortex and nucleus accumbens has been identified in obese subjects (Shin et al 2009;Stoeckel et al 2009). Increased BMI is also associated with decreased activation of amygdala during gastric distention (Tomasi et al 2009). The deficient projections from the amygdala in obese individuals might relate to suboptimal modulation of the affective aspects that are linked to the reward value and motivational salience associated with foods (Stoeckel et al 2009).…”

Body weight and the reward system: the volume of the right amygdala may be associated with body mass index in young overweight men

“…There are many functional neuroimaging studies which have analyzed the neural mechanism of human food intake, body weight regulation, and the pathomechanism of obesity (Grabenhorst et al 2010;Holsen and Zarcone 2005;Holsen et al 2006;Passamonti et al 2009;Stoeckel et al 2009;Tomasi et al 2009;Wang et al 2009). There are also seven studies investigating the morphological changes associated with BMI (see Table 1).…”