Differential effects of hunger and satiety on insular cortex and hypothalamic functional connectivity

Abstract

The insula cortex and hypothalamus are implicated in eating behaviour, and contain receptor sites for peptides and hormones controlling energy balance. The insula encompasses multi-functional subregions, which display differential anatomical and functional connectivities with the rest of the brain. This study aimed to analyse the effect of fasting and satiation on the functional connectivity profiles of left and right anterior, middle, and posterior insula, and left and right hypothalamus. It was hypothesized that the profiles would be altered alongside changes in homeostatic energy balance. Nineteen healthy participants underwent two 7-min resting state functional magnetic resonance imaging scans, one when fasted and one when satiated. Functional connectivity between the left posterior insula and cerebellum/superior frontal gyrus, and between left hypothalamus and inferior frontal gyrus was stronger during fasting. Functional connectivity between the right middle insula and default mode structures (left and right posterior parietal cortex, cingulate cortex), and between right hypothalamus and superior parietal cortex was stronger during satiation. Differences in blood glucose levels between the scans accounted for several of the altered functional connectivities. The insula and hypothalamus appear to form a homeostatic energy balance network related to cognitive control of eating; prompting eating and preventing overeating when energy is depleted, and ending feeding or transferring attention away from food upon satiation. This study provides evidence of a lateralized dissociation of neural responses to energy modulations.

Keywords: appetite; fMRI; homeostatic energy balance.

Figure 1

Seeds superimposed on a typical participant's T1 scan. (A) anterior insula (magenta), middle insula (yellow), and posterior insula (green); (B) left hypothalamus (blue), right hypothalamus (red). L, left; R, right.

Figure 2

Slice locations, insula seeds and connectivity maps. L, left; R, right; AI, anterior insula; MI, mid insula; PI, posterior insula; CER, cerebellum; SFG, superior frontal gyrus; IPC, inferior parietal cortex; PCC, posterior cingulate cortex.

Figure 3

Hypothalamus seeds and connectivity maps. L, left; R, right; A, anterior; P, posterior; IFG, inferior frontal gyrus; SPC, superior parietal cortex.

Figure 4

(A) y axis is Δ connectivity between sessions from left posterior insula (LPI) to SFG; (B) y axis is Δ connectivity between sessions from right middle insula (RMI) to posterior cingulate cortex (PCC); (C) is the connectivity between left hypothalamus/IFG and the cognitive restraint subscale of the TFEQR18; (D) is the connectivity between right hypothalamus/SPC and the cognitive restraint subscale of the TFEQR18.