Ghrelin mimics fasting to enhance human hedonic, orbitofrontal cortex, and hippocampal responses to food

Goldstone, Anthony P.; Prechtl, Christina Gabriele; Scholtz, Samantha; Miras, Alexander D.; Chhina, Navpreet; Durighel, Giuliana; Deliran, Seyedeh S; Beckmann, Christian F.; Ghatei, Mohammad A.; Ashby, Damien; Waldman, Adam D.; Gaylinn, Bruce D.; Thorner, Michael O.; Frost, Gary; Bloom, Stephen R.; Bell, Jimmy D.

doi:10.3945/ajcn.113.075291

Cited by 120 publications

(141 citation statements)

References 59 publications

(121 reference statements)

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“…More recently, the CCK plasma values have been showed to correlate negativity with BOLD response in reward (amygdala) and taste (insula) regions in response to ingestion of a high-fat meal (90) . A number of studies have also investigated the cortical response to ghrelin (91)(92)(93) .…”

Section: How Do Hormonal Responses Influence the Cortex?mentioning

confidence: 99%

Imaging methodologies and applications for nutrition research: what can functional MRI offer?

Francis

Eldeghaidy

2014

Proc. Nutr. Soc.

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Food intake is influenced by a complex regulatory system involving the integration of a wide variety of sensory inputs across multiple brain areas. Over the past decade, advances in neuroimaging using functional MRI (f MRI) have provided valuable insight into these pathways in the human brain. This review provides an outline of the methodology of f MRI, introducing the widely used blood oxygenation level-dependent contrast for f MRI and direct measures of cerebral blood flow using arterial spin labelling. A review of f MRI studies of the brain's response to taste, aroma and oral somatosensation, and how fat is sensed and mapped in the brain in relation to the pleasantness of food, and appetite control is given. The influence of phenotype on individual variability in cortical responses is addressed, and an overview of f MRI studies investigating hormonal influences (e.g. peptide YY, cholecystokinin and ghrelin) on appetiterelated brain processes provided. Finally, recent developments in MR technology at ultrahigh field (7 T) are introduced, highlighting the advances this can provide for f MRI studies to investigate the neural underpinnings in nutrition research. In conclusion, neuroimaging methods provide valuable insight into the mechanisms of flavour perception and appetite behaviour. Over the past decade, advances in neuroimaging techniques, particularly functional MRI (f MRI), have provided valuable insight into central food-related pathways in the human brain. This review outlines recent advances in f MRI to understand flavour perception and human appetitive behaviour. A brief overview of the method of f MRI and the blood oxygenation level-dependent (BOLD) contrast generally used in f MRI is provided, together with how more direct measures of cerebral blood flow (CBF) can be assessed. f MRI studies of the brain's response to taste, aroma and flavour perception are outlined. The question of how fat is sensed and mapped in the brain in relation to the pleasantness of food, appetite control and hormonal influences is addressed. The role of neuroimaging studies to assess eating behaviour in obesity will be outlined. Finally, recent developments in MR technology, and the advances they can provide for future f MRI studies to investigate the neural underpinnings in nutrition research will be described. Principles of functional MRIf MRI has revolutionised the research of functional brain mapping and is now the most widely used method for mapping brain activity. f MRI measures brain activity *Corresponding author: Dr S. Francis, email susan.francis@nottingham.ac.uk ‡ The original version of this article was published with incorrect conference details. A notice detailing this has been published and the error rectified in the online and print PDF and HTML copies.

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Section: How Do Hormonal Responses Influence the Cortex?mentioning

confidence: 99%

Imaging methodologies and applications for nutrition research: what can functional MRI offer?

Francis

Eldeghaidy

2014

Proc. Nutr. Soc.

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“…In a study that mirrored these findings, Malik et al (59) demonstrated that the hypo-responsiveness of the reward system to food cues when full can be reinvigorated with the delivery of the appetite hormone ghrelin. Goldstone et al (60) confirmed that the pattern of reward-centre responsivity to food cues when fasted was indistinguishable from that induced by ghrelin, which added weight to the hypothesis that circulating gut hormones are responsible for the physiological modulation of reward reactivity that was first measured in the very earliest fed vs fasted MRI appetite studies. In an interesting twist to this experimental paradigm, Van Oudenhove et al (61) recently showed that gastric fatty acid infusion (which stimulated an endogenous release of the gut hormone CCK) attenuated both the behavioural and neural responses to sad emotion induction (and that this effect was blocked by a CCK receptor antagonist).…”

Section: The Gut-brain Axismentioning

confidence: 94%

IMAGING IN ENDOCRINOLOGY: The use of functional MRI to study the endocrinology of appetite

Salem¹,

Dhillo²

2015

European Journal of Endocrinology

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In the present review article, we summarise current thinking about the neuroendocrinology of appetite and feeding behaviour. We discuss how the homeostatic control of energy balance, wherein the hypothalamus orchestrates food intake and energy expenditure in response to peripheral signals about nutritional status, can be easily overridden by the powerful reward value of food. We focus on how functional magnetic resonance imaging has shed light on our understanding of the way hormones can interact with the brain to modulate appetite.

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“…Brain regions that are involved in reward (11,14), executive function (7,11,15), and recognition (16,17) are more responsive to food stimuli with higher appetitive values than with lower appetitive values. These effects are also modulated by hunger (8,10,13) and satiety (18). However, the interpretation of previous fMRI studies has been limited because 1) the PS of food stimuli has rarely been controlled, and 2) children ,10 y old have rarely been included (7,9,(15)(16)(17)19).…”

Section: Introductionmentioning

confidence: 98%

“…Food intake is controlled by both metabolic and hedonic signals that originate from neuroregulatory systems (5,6). Images of food elicit the activation of brain systems that regulate appetite, reward, and inhibitory control (7)(8)(9)(10)(11)(12)(13). Therefore, food images at different PSs and EDs may differentially engage brain systems.…”

Section: Introductionmentioning

confidence: 99%

Food portion size and energy density evoke different patterns of brain activation in children

Fearnbach

Wilson

Fisher

et al. 2017

The American Journal of Clinical Nutrition

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Background: Large portions of food promote intake, but the mechanisms that drive this effect are unclear. Previous neuroimaging studies have identified the brain-reward and decision-making systems that are involved in the response to the energy density (ED) (kilocalories per gram) of foods, but few studies have examined the brain response to the food portion size (PS). Objective: We used functional MRI (fMRI) to determine the brain response to food images that differed in PSs (large and small) and ED (high and low). Design: Block-design fMRI was used to assess the blood oxygen leveldependent (BOLD) response to images in 36 children (7-10 y old; girls: 50%), which was tested after a 2-h fast. Pre-fMRI fullness and liking were rated on visual analog scales. A whole-brain cluster-corrected analysis was used to compare BOLD activation for main effects of the PS, ED, and their interaction. Secondary analyses were used to associate BOLD contrast values with appetitive traits and laboratory intake from meals for which the portions of all foods were increased. Results: Compared with small-PS cues, large-PS cues were associated with decreased activation in the inferior frontal gyrus (P , 0.01). Compared with low-ED cues, high-ED cues were associated with increased activation in multiple regions (e.g., in the caudate, cingulate, and precentral gyrus) and decreased activation in the insula and superior temporal gyrus (P , 0.01 for all). A PS 3 ED interaction was shown in the superior temporal gyrus (P , 0.01). BOLD contrast values for high-ED cues compared with low-ED cues in the insula, declive, and precentral gyrus were negatively related to appetitive traits (P , 0.05). There were no associations between the brain response to the PS and either appetitive traits or intake. Conclusions: Cues regarding food PS may be processed in the lateral prefrontal cortex, which is a region that is implicated in cognitive control, whereas ED activates multiple areas involved in sensory and reward processing. Possible implications include the development of interventions that target decision-making and reward systems differently to moderate overeating.Am J Clin Nutr 2017;105:295-305.

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Ghrelin mimics fasting to enhance human hedonic, orbitofrontal cortex, and hippocampal responses to food

Cited by 120 publications

References 59 publications

Imaging methodologies and applications for nutrition research: what can functional MRI offer?

Imaging methodologies and applications for nutrition research: what can functional MRI offer?

IMAGING IN ENDOCRINOLOGY: The use of functional MRI to study the endocrinology of appetite

Food portion size and energy density evoke different patterns of brain activation in children

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