Abstract
To study the interplay of metabolic state (hungry vs. satiated) and glucose administration (including hormonal modulation) on brain function, resting-state functional magnetic resonance imaging (rs-fMRI) and blood samples were obtained in 24 healthy normal-weight men in a repeated measurement design. Participants were measured twice: once after a 36 h fast (except water) and once under satiation (three meals/day for 36 h). During each session, rs-fMRI and hormone concentrations were recorded before and after a 75 g oral dose of glucose. We calculated the amplitude map from blood-oxygen-level-dependent (BOLD) signals by using the fractional amplitude of low-frequency fluctuation (fALFF) approach for each volunteer per condition. Using multiple linear regression analysis (MLRA) the interdependence of brain activity, plasma insulin and blood glucose was investigated. We observed a modulatory impact of fasting state on intrinsic brain activity in the posterior cingulate cortex (PCC). Strikingly, differences in plasma insulin levels between hunger and satiety states after glucose administration at the time of the scan were negatively related to brain activity in the posterior insula and superior frontal gyrus (SFG), while plasma glucose levels were positively associated with activity changes in the fusiform gyrus. Furthermore, we could show that changes in plasma insulin enhanced the connectivity between the posterior insula and SFG. Our results indicate that hormonal signals like insulin alleviate an acute hemostatic energy deficit by modifying the homeostatic and frontal circuitry of the human brain.
Highlights
Food ingestion and energy homeostasis are regulated by central nervous pathways (Schwartz and Porte, 2005; Lam, 2010; Suzuki et al, 2010) and modulated by endocrine signals (Gao and Horvath, 2008)
The interaction was driven by an increased area under curve for glucose following the exogenous glucose challenge in the hunger (M = 7.6 mmol/l, standard deviation (SD) = 1.1) compared to the satiety condition (M = 5.9 mmol/l, SD = 0.6) whereas this was reversed before glucose treatment with higher plasma glucose level in the satiety (M = 4.6 mmol/L, SD = 0.5) compared to the hunger condition (M = 3.9 mmol/L, SD = 0.5)
We investigated the interaction of hunger and satiety with plasma glucose and plasma insulin levels before and after glucose administration and explored this interaction’s impact on changes in resting state functional magnetic resonance imaging (fMRI)
Summary
Food ingestion and energy homeostasis are regulated by central nervous pathways (Schwartz and Porte, 2005; Lam, 2010; Suzuki et al, 2010) and modulated by endocrine signals (Gao and Horvath, 2008). Insulin is one of the hormones that is part of a negative feedback loop that ensures balanced energy homeostasis (Schwartz et al, 2000; Schwartz, 2001; Obici et al, 2002) Of note, both intraventricular injection and intranasal administration of insulin decreases food intake and body weight in rodents (Chavez et al, 1995; Brown et al, 2006) and humans (Benedict et al, 2008). According to Smitha et al (2017), task-based designs focus on a small fraction of the brain’s overall activity only To avoid these disadvantages in the present investigation, we used resting-state fMRI in order to reveal potential links between whole brain activity and insulin and glucose levels in different metabolic states
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