Association of Disinhibited Eating and Trait of Impulsivity With Insula and Amygdala Responses to Palatable Liquid Consumption

Abstract

Eating behavior is not only influenced by the current energy balance, but also by the behavioral characteristics of eating. One of the recognized eating behavior constructs is ‘disinhibited eating,’ which refers to the tendency to overeat in response to negative emotional states or the presence of highly palatable foods. Food-related disinhibition is involved in binge eating, weight gain, and obesity and is also associated with the trait of impulsivity, which in turn, is linked to weight gain or maladaptive eating. However, the relationships among food-related disinhibition, the trait of impulsivity, and the neural substrates of eating behaviors in adolescence remain unclear. Therefore, we designed a functional magnetic resonance imaging (fMRI) study to examine the associations between brain responses to palatable liquid consumption and disinhibited eating behavior or impulsivity in healthy adolescents. Thirty-four adolescents (mean age ± standard deviation = 17.12 ± 1.91 years, age range = 14–19 years, boys = 15, girls = 19) participated in this study. Disinhibited eating was assessed with the disinhibition subscale of the Three-Factor Eating Questionnaire, while impulsivity was assessed using the Barratt impulsiveness scale. Participants received two fMRI sessions−a palatable liquid consumption fMRI and a resting-state fMRI. The fMRI experiment showed that increased disinhibited eating was positively associated with a greater insular response to palatable liquid consumption, while increased impulsivity was positively correlated with a greater amygdala response. The resting-state fMRI experiment showed that increased disinhibited eating was positively correlated with strengthened intrinsic functional connectivity between the insula and the amygdala, adjusting for sex (estimates of the beta coefficients = 0.146, standard error = 0.068, p = 0.040). Given that the amygdala and insular cortex are structurally and functionally connected and involved in trait impulsivity and ingestive behavior, our findings suggest that increased disinhibited eating would be associated with impulsivity via strengthened intrinsic functional connectivity between the insula and amygdala and linked to maladaptive eating.

Neural circuits mediating food cue-reactivity: Toward a new model shaping the interplay of internal and external factors

“…Self-directedness (linked to emotional stability and goal-directed behavior) ( 29 ), was negatively associated with emotional regulation (amygdala activity) in response to appetizing food vs. non-foods ( 30 ), suggesting that it may represent a protective factor against cue-driven food cravings and intake. Conversely, increased disinhibited eating and trait impulsivity were positively associated with greater insula and amygdala responses to palatable foods ( 31 ).…”

Neural circuits mediating food cue-reactivity: toward a new model shaping the interplay of internal and external factors

“…Conversely, increased disinhibited eating and trait impulsivity, were positively associated with greater insula and amygdala responses to palatable foods (22).…”

Exposure to gestational diabetes mellitus in utero impacts hippocampal functional connectivity in response to food cues in children

“…Higher activation in the striatum and insula in response to food images were observed in children and adolescents with obesity compared to their healthy-weight peers (19)(20)(21). In the resting state, higher striatal and insular network FC was also linked to eating in the absence of hunger, food craving, disinhibited eating, weight gain and obesity in both children and adults (40)(41)(42)(43). Current ndings on FC between the hippocampus and striatum are inconsistent.…”