Importance of reward and prefrontal circuitry in hunger and satiety: Prader–Willi syndrome vs simple obesity
Open accessAbstract
Background 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.Objective 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.Design and participants 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.Results 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.Conclusion 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.
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Dysfunction in OFC and ACC results in compulsivity, and this might be part of the mechanism by which low-striatal D2R signalling facilitates hyperphagia.
“Given that dysfunction in OFC and ACC results in compulsivity (see review (85)), this might be part of the mechanism by which low-striatal D2R signalling facilitates hyperphagia (86,87).”
From Obesity and addiction: Neurobiological overlaps (2013) · cites this paper as [87]
Recent studies using BOLD fMRI have shown selective overactivity in the nucleus accumbens and related brain areas in obese compared with lean individuals when shown images of highly palatable food.
“Recent studies that used the conventional blood oxygenation level-dependent fMRI have shown selective overactivity in the nucleus accumbens and related brain areas in obese compared with lean individuals when shown imagines of highly palatable food (6)(7)(8)(9)(10)(11)”
From Effects of dietary glycemic index on brain regions related to reward and craving in men (2013) · cites this paper as [7]
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- 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.
- Affiliations
- Brigham and Women's Hospital (US)
- University of Kansas Medical Center (US)
- University of Missouri–Kansas City (US)
- University of Rochester Medicine (US)
- Corresponding author
- Holsen, L M
- Venue
- International Journal of Obesity
- Published
- 2011-10-25
- Volume
- 36
- Issue
- 5
- Pages
- 638-647
- ISSN
- 0307-0565 (ISSN-L)
- 1476-5497
- PMC
- PMC3270121
- OpenAlex
- W2121866241
- Cited by
- 128
- References
- 66
- Citations by year
- 2026: 8 · 2025: 11 · 2024: 2 · 2023: 8 · 2022: 8 · 2021: 14 · 2020: 9 · 2019: 4 · 2018: 9 · 2017: 5 · 2016: 12 · 2015: 12 · 2014: 9 · 2013: 11 · 2012: 6
- FWCI
- 3.85
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Licence
- www.springer.com/tdm (tdm)
- Locations
- International Journal of Obesity (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Digital Access to Scholarship at Harvard (DASH) (Harvard University) (submittedVersion, cc-by)
- Funders
- U.S. Public Health Service (U22MC03962-02)
- National Institute of Mental Health (K01MH091222)
- Eunice Kennedy Shriver National Institute of Child Health and Human Development (HD041672, K12HD051959, R01HD041672)
- Topics
- Life Sciences › Neuroscience › Endocrine and Autonomic Systems › Regulation of Appetite and Obesity
- Social Sciences › Psychology › Clinical Psychology › Eating Disorders and Behaviors
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetic Syndromes and Imprinting
- Keywords
- Prader-Willi syndrome, simple obesity, hunger and satiety, hyperphagia, nucleus accumbens, amygdala, hypothalamus, orbitofrontal cortex, dorsolateral prefrontal cortex, food motivation, limbic system, genetic obesity model
- MeSH terms
- Adult, Brain Mapping, Feeding Behavior, Female, Humans, Hunger, Magnetic Resonance Imaging, Male, Obesity, Photic Stimulation, Prader-Willi Syndrome, Surveys and Questionnaires, Reward, Satiation, Prefrontal Cortex, Postprandial Period, Functional Neuroimaging
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