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Resting state hypothalamic response to glucose predicts glucose-induced attenuation in the ventral striatal response to food cues.

ABSTRACT: Feeding behavior is regulated by a complex interaction of central nervous system responses to metabolic signals that reflect nutrient availability and to food cues that trigger appetitive responses. Prior work has shown that the hypothalamus is a key brain area that senses and responds to changes in metabolic signals, and exposure to food cues induces the activation of brain areas involved in reward processing. However, it is not known how the hypothalamic responses to changes in metabolic state are related to reward responses to food cues. This study aimed to understand whether changes in hypothalamic activity in response to glucose-induced metabolic signals are linked to food-cue reactivity within brain areas involved in reward processing. We combined two neuroimaging modalities (Arterial Spin Labeling and Blood Oxygen Level Dependent) to measure glucose-induced changes in hypothalamic cerebral blood flow (CBF) and food-cue task induced changes in brain activity within reward-related regions. Twenty-five participants underwent a MRI session following glucose ingestion and a subset of twenty individuals underwent an additional water session on a separate day as a control condition (drink order randomized). Hunger was assessed before and after drink consumption. We observed that individuals who had a greater reduction in hypothalamic CBF exhibited a greater reduction in left ventral striatum food cue reactivity (Spearman's rho = 0.46, P = 0.048) following glucose vs. water ingestion. These results are the first to use multimodal imaging to demonstrate a link between hypothalamic metabolic signaling and ventral striatal food cue reactivity.

SUBMITTER: Luo S

PROVIDER: S-EPMC5557629 | biostudies-literature | 2017 Sep

REPOSITORIES: biostudies-literature

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Resting state hypothalamic response to glucose predicts glucose-induced attenuation in the ventral striatal response to food cues.

Luo Shan S Melrose A James AJ Dorton Hilary H Alves Jasmin J Monterosso John R JR Page Kathleen A KA

Appetite 20170525

Feeding behavior is regulated by a complex interaction of central nervous system responses to metabolic signals that reflect nutrient availability and to food cues that trigger appetitive responses. Prior work has shown that the hypothalamus is a key brain area that senses and responds to changes in metabolic signals, and exposure to food cues induces the activation of brain areas involved in reward processing. However, it is not known how the hypothalamic responses to changes in metabolic state ...[more]

PMID: 28551112

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Project description:ImportanceEating disorders are severe psychiatric disorders; however, disease models that cross subtypes and integrate behavior and neurobiologic factors are lacking.ObjectiveTo assess brain response during unexpected receipt or omission of a salient sweet stimulus across a large sample of individuals with eating disorders and healthy controls and test for evidence of whether this brain response is associated with the ventral striatal-hypothalamic circuitry, which has been associated with food intake control, and whether salient stimulus response and eating disorder related behaviors are associated.Design, setting, and participantsIn this cross-sectional functional brain imaging study, young adults across the eating disorder spectrum were matched with healthy controls at a university brain imaging facility and eating disorder treatment program. During a sucrose taste classic conditioning paradigm, violations of learned associations between conditioned visual and unconditioned taste stimuli evoked the dopamine-related prediction error. Dynamic effective connectivity during expected sweet taste receipt was studied to investigate hierarchical brain activation between food intake relevant brain regions. The study was conducted from June 2014 to November 2019. Data were analyzed from December 2019 to February 2020.Main outcomes and measuresPrediction error brain reward response across insula and striatum; dynamic effective connectivity between hypothalamus and ventral striatum; and demographic and behavior variables and their correlations with prediction error brain response and connectivity edge coefficients.ResultsOf 317 female participants (197 with eating disorders and 120 healthy controls), the mean (SD) age was 23.8 (5.6) years and mean (SD) body mass index was 20.8 (5.4). Prediction error response was elevated in participants with anorexia nervosa (Wilks λ, 0.843; P = .001) and in participants with eating disorders inversely correlated with body mass index (left nucleus accumbens: r = -0.291; 95% CI, -0.413 to -0.167; P < .001; right dorsal anterior insula: r = -0.228; 95% CI, -0.366 to -0.089; P = .001), eating disorder inventory-3 binge eating tendency (left nucleus accumbens: r = -0.207; 95% CI, -0.333 to -0.073; P = .004; right dorsal anterior insula: r = -0.220; 95% CI, -0.354 to -0.073; P = .002), and trait anxiety (left nucleus accumbens: r = -0.148; 95% CI, -0.288 to -0.003; P = .04; right dorsal anterior insula: r = -0.221; 95% CI, -0.357 to -0.076; P = .002). Ventral striatal to hypothalamus directed connectivity was positively correlated with ventral striatal prediction error in eating disorders (r = 0.189; 95% CI, 0.045-0.324; P = .01) and negatively correlated with feeling out of control after eating (right side: r = -0.328; 95% CI, -0.480 to -0.164; P < .001; left side: r = -0.297; 95% CI, -0.439 to -0.142; P = .001).Conclusions and relevanceThe results of this cross-sectional imaging study support that body mass index modulates prediction error and food intake control circuitry in the brain. Once altered, this circuitry may reinforce eating disorder behaviors when paired with behavioral traits associated with overeating or undereating.

Dataset Information

Resting state hypothalamic response to glucose predicts glucose-induced attenuation in the ventral striatal response to food cues.

Publications

Resting state hypothalamic response to glucose predicts glucose-induced attenuation in the ventral striatal response to food cues.

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