Importance of reward and prefrontal circuitry in hunger and satiety: Prader―Willi syndrome vs simple obesity

The majority of research on obesity (OB) has focused primarily on clinical features (eating behavior, adiposity measures) or peripheral appetite-regulatory peptides (leptin, ghrelin). However, recent functional neuroimaging studies have demonstrated that some reward circuitry regions that are associ...

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Bibliographic Details
Published in:International Journal of Obesity 2012-05, Vol.36 (5), p.638-647
Main Authors: HOLSEN, L. M, SAVAGE, C. R, MARTIN, L. E, BRUCE, A. S, LEPPING, R. J, KO, E, BROOKS, W. M, BUTLER, M. G, ZARCONE, J. R, GOLDSTEIN, J. M
Format: Article
Language:English
Subjects:
Adult
Appetite
Biological and medical sciences
Brain
Brain Mapping
Complex syndromes
Decision making
Diet
Eating behavior
Eating disorders
Feeding Behavior - psychology
Female
Food
Functional Neuroimaging - methods
Genetics
Health care
Hormones
Hospitals
Humans
Hunger
Hypothalamus
Magnetic Resonance Imaging - methods
Maintenance
Male
Medical genetics
Medical sciences
Metabolic diseases
Motivation
Obesity
Obesity - physiopathology
Obesity - psychology
Photic Stimulation
Physiological aspects
Postprandial Period
Prader-Willi syndrome
Prader-Willi Syndrome - physiopathology
Prader-Willi Syndrome - psychology
Prefrontal Cortex - physiopathology
Preventive medicine
Reward
Satiation
Stimuli
Surveys and Questionnaires
Womens health
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Summary:The majority of research on obesity (OB) has focused primarily on clinical features (eating behavior, adiposity measures) or peripheral appetite-regulatory peptides (leptin, ghrelin). However, recent functional neuroimaging studies have demonstrated that some reward circuitry regions that are associated with appetite-regulatory hormones are also involved in the development and maintenance of OB. Prader-Willi syndrome (PWS), characterized by hyperphagia and hyperghrelinemia reflecting multi-system dysfunction in inhibitory and satiety mechanisms, serves as an extreme model of genetic OB. Simple (non-PWS) OB represents an OB-control state. This study investigated subcortical food motivation circuitry and prefrontal inhibitory circuitry functioning in response to food stimuli before and after eating in individuals with PWS compared with OB. We hypothesized that groups would differ in limbic regions (that is, hypothalamus, amygdala) and prefrontal regions associated with cognitive control (that is, dorsolateral prefrontal cortex (DLPFC), orbitofrontal cortex (OFC) after eating. A total of 14 individuals with PWS, 14 BMI- and age-matched individuals with OB, and 15 age-matched healthy-weight controls viewed food and non-food images while undergoing functional MRI before (pre-meal) and after (post-meal) eating. Using SPM8, group contrasts were tested for hypothesized regions: hypothalamus, nucleus accumbens (NAc), amygdala, hippocampus, OFC, medial PFC and DLPFC. Compared with OB and HWC, PWS demonstrated higher activity in reward/limbic regions (NAc, amygdala) and lower activity in the hypothalamus and hippocampus in response to food (vs non-food) images pre-meal. Post meal, PWS exhibited higher subcortical activation (hypothalamus, amygdala, hippocampus) compared with OB and HWC. OB showed significantly higher activity versus PWS and HWC in cortical regions (DLPFC, OFC) associated with inhibitory control. In PWS, compared with OB per se, results suggest hyperactivations in subcortical reward circuitry and hypoactivations in cortical inhibitory regions after eating, which provides evidence of neural substrates associated with variable abnormal food motivation phenotypes in PWS and simple OB.
ISSN:0307-0565
1476-5497
DOI:10.1038/ijo.2011.204