Reward-related brain activity and behavior are associated with peripheral ghrelin levels in obesity

Volodymyr B. Bogdanov, Olena V. Bogdanova, Sandra Dexpert, Ines Delgado, Helen Beyer, Agnès Aubert, Bixente Dilharreguy, Cédric Beau, Damien Forestier, Patrick Ledaguenel, Eric Magne, Bruno Aouizerate, Sophie Layé, Guillaume Ferreira, Jennifer Felger, Giuseppe Pagnoni, Lucile Capuron
Psychoneuroendocrinology. 2020-02-01; 112: 104520
DOI: 10.1016/j.psyneuen.2019.104520

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Bogdanov VB(1), Bogdanova OV(2), Dexpert S(3), Delgado I(3), Beyer H(3), Aubert A(3), Dilharreguy B(4), Beau C(5), Forestier D(5), Ledaguenel P(5), Magne E(5), Aouizerate B(3), Layé S(3), Ferreira G(3), Felger J(6), Pagnoni G(7), Capuron L(8).

Author information:
(1)Univ. Bordeaux, INRA, Bordeaux INP, NutriNeuro, UMR 1286, F-33000, Bordeaux, France; Univ. Lyon, Ecole Nationale des Travaux Publics de l’Etat, Laboratoire Génie Civil et Bâtiment, F-69518, Vaulx-en-Velin, France. Electronic address:.
(2)INSERM U1028 – CNRS UMR5292, 16 avenue Doyen Lépine, F-69676, Bron, France.
(3)Univ. Bordeaux, INRA, Bordeaux INP, NutriNeuro, UMR 1286, F-33000, Bordeaux, France.
(4)Univ. Bordeaux, INCIA, CNRS, UMR 5287, F-33076, Bordeaux, France.
(5)Digestive and Parietal Surgery, Clinique Tivoli, F-33000, Bordeaux, and Clinique Jean Villar, F-33520, Bruges, France.
(6)Dpt of Psychiatry and Behavioral Sciences, Emory University School of Medicine, Atlanta, GA 30322, USA.
(7)Dept of Neural, Biomedical, and Metabolic Sciences, University of Modena and Reggio Emilia, I-41125, Modena, Italy; Center for Neuroscience and Neurotechnology, University of Modena and Reggio Emilia, I-41125, Modena, Italy.
(8)Univ. Bordeaux, INRA, Bordeaux INP, NutriNeuro, UMR 1286, F-33000, Bordeaux, France. Electronic address: .

BACKGROUND/OBJECTIVES:

While excessive food consumption represents a key factor in the development of obesity, the underlying mechanisms are still unclear. Ghrelin, a gut-brain hormone involved in the regulation of appetite, is impaired in obesity. In addition to its role in eating behavior, this hormone was shown to affect brain regions controlling reward, including the striatum and prefrontal cortex, and there is strong evidence of impaired reward processing in obesity. The present study investigated the possibility that disrupted reward-related brain activity in obesity relates to ghrelin deficiency.

SUBJECTS/METHODS:

Fifteen severely obese subjects (BMI > 35 kg/m2) and fifteen healthy non-obese control subjects (BMI < 30 kg/m2) were recruited. A guessing-task paradigm, previously shown to activate the ventral striatum, was used to assess reward-related brain neural activity by functional magnetic resonance imaging (fMRI). Fasting blood samples were collected for the measurement of circulating ghrelin.

RESULTS:

Significant activations in the ventral striatum, ventromedial prefrontal cortex and extrastriate visual cortex were elicited by the fMRI task in both obese and control subjects. In addition, greater reward-related activations were present in the dorsolateral prefrontal cortex, and precuneus/posterior cingulate of obese subjects compared to controls. Obese subjects exhibited longer choice times after repeated reward and lower circulating ghrelin levels than lean controls. Reduced ghrelin levels significantly predicted slower post-reward choices and reward-related hyperactivity in dorsolateral prefrontal cortices in obese subjects.

CONCLUSION:

This study provides evidence of association between circulating ghrelin and reward-related brain activity in obesity and encourages further exploration of the role of ghrelin system in altered eating behavior in obesity.

 

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