Neural correlates of taste and pleasantness evaluation in the metabolic syndrome

Abstract

Metabolic syndrome (MetS) is a constellation of cardiometabolic abnormalities that commonly occur together and increase risk for cardiovascular disease and type II diabetes. Having MetS, especially during middle-age, increases the risk for dementia in later life. Abdominal obesity is a central feature of MetS; therefore, increased efforts to prevent obesity and identify predictors of weight gain are of extreme importance. Altered processing of food reward in the brain of obese individuals has been suggested to be a possible mechanism related to overeating. We scanned fifteen healthy middle-aged controls (aged 44-54) and sixteen middle-aged adults with MetS after a fast (hungry) and after a preload (sated), while they rated the pleasantness of sucrose (sweet) and caffeine (bitter) solutions. Data were analyzed using voxelwise linear mixed-effects modeling, and a region of interest analysis to examine associations between hypothalamic activation to sweet taste and BMI during hunger and satiety. The results indicate that middle-aged individuals with MetS respond with significantly less brain activation than controls without MetS during pleasantness evaluation of sweet and bitter tastes in regions involved in sensory and higher-level taste processing. Participants with higher BMI had greater hypothalamic response during pleasantness evaluation of sucrose in the sated condition. Importantly, this study is the first to document differential brain circuitry in middle-aged adults with MetS, a population at risk for poor physical and cognitive outcomes. Future research aimed at better understanding relationships among MetS, obesity, and brain function is warranted to better conceptualize and develop interventions for overeating in these disorders.

Keywords: Aging; Hunger; Metabolic syndrome; Obesity; Reward; Satiety; Taste; fMRI.

Figure 1

Main effects of metabolic syndrome and taste: (a) Statistical map of the main effect (F values) of metabolic syndrome during hunger (controls > MetS) in left cerebellum⁽¹⁾, right inferior temporal gyrus/BA 20, fusiform gyrus⁽²⁾, right lentiform nucleus, insula, putamen⁽³⁾, and left superior temporal gyrus/BA 42, insula⁽⁴⁾. (b) Statistical map of the main effect (F values) of taste, during hunger, in the left anterior cingulate (sucrose > caffeine)⁽⁵⁾, right paracentral lobule and left cingulate gyrus (caffeine > sucrose)⁽⁶⁾, left lingual gyrus (caffeine > sucrose)⁽⁷⁾, and right anterior cingulate and Brodmann Area 10 (sucrose > caffeine)⁽⁸⁾. (c) Statistical map of the main effect of metabolic syndrome during satiety. Healthy controls demonstrated greater activation than the group with MetS in the right prefrontal cortex/Brodmann Area 10⁽¹⁾ and Cerebellum⁽²⁾.

Figure 2

Positive Pearson correlation between BMI and hypothalamus (ROI) activation during pleasantness evaluation of sucrose, while in the sated condition

Figure 3

Modified general labeled magnitude scale (gLMS) for pleasantness