Elevated energy intake is correlated with hyperresponsivity in attentional, gustatory, and reward brain regions while anticipating palatable food receipt

Abstract

Background: Obese compared with lean individuals show greater attention-, gustatory-, and reward-region responsivity to food cues but reduced reward-region responsivity during food intake. However, to our knowledge, research has not tested whether an objectively measured caloric intake is positively associated with neural responsivity independent of excess adipose tissue.

Objective: We tested the hypothesis that objectively measured energy intake, which accounts for basal needs and the percentage of body fat, correlates positively with the neural response to anticipated palatable food intake but negatively with a response to food intake in healthy-weight adolescents.

Design: Participants (n = 155; mean ± SD age: 15.9 ± 1.1 y) completed functional magnetic resonance imaging scans while anticipating and receiving palatable food compared with a tasteless solution, a doubly labeled water assessment of energy intake, and assessments of resting metabolic rate and body composition.

Results: Energy intake correlated positively with activation in the lateral visual and anterior cingulate cortices (visual processing and attention), frontal operculum (primary gustatory cortex) when anticipating palatable food, and greater striatal activation when anticipating palatable food in a more-sensitive region of interest analysis. Energy intake was not significantly related to neural responsivity during palatable food intake.

Conclusions: Results indicate that objectively measured energy intake that accounts for basal needs and adipose tissue correlates positively with activity in attentional, gustatory, and reward regions when anticipating palatable food. Although hyperresponsivity of these regions may increase risk of overeating, it is unclear whether this is an initial vulnerability factor or a result of previous overeating. This trial was registered at clinicaltrials.gov as NCT01807572.

FIGURE 1.

Blood oxygen level–dependent response during anticipated palatable food intake (> anticipated tasteless intake) as a function of energy intake (kcal/d) with the resting metabolic rate and percentage of body fat controlled for in the lateral visual cortex (P = 7.6 × 10^–6) (A) and the frontal operculum (P = 3.3 × 10^–5) (B) and parameter estimates from those peaks. The color bar indicates the T value of the activation (n = 155; P < 0.05 corrected for multiple comparisons). Additional details are shown in Table 2.