Gaining new insights into food reward with functional neuroimaging.

The notion that eating is intimately related to feelings of pleasure is not new. Indeed, in an environment characterised by many varied and palatable foods, hedonistic drives are likely to play a greater role in modulating food intake than homeostatic ones. Until recently however, a neurobiological account of the rewarding properties of food was lacking. The ability to reveal functional brain activity has been made possible with the advent of functional neuroimaging techniques such as electroencephalography (EEG), magnetoencephalography (MEG), positron emission tomography (PET) and most recently, functional magnetic resonance imaging (fMRI). Neuroimaging studies in fed and fasted, lean and obese, normal and pathological states have revealed variations in food-related reward processing. Eating is a multi-sensory experience and understanding the precise mechanisms by which food modulates reward circuits will be important in understanding the aetiology of obesity and eating disorders. Here we review the development of functional neuroimaging as a research tool and recent neuroimaging studies relating to food reward. In particular, we evaluate the ability of leptin and the gut hormones peptide YY3-36 and ghrelin to modulate activity in reward-related brain regions. Finally, we discuss the potential to use such information to guide development of pharmaceuticals, functional foods and life-style modifications.

[1]  K. Wynne,et al.  Attenuated peptide YY release in obese subjects is associated with reduced satiety. , 2006, Endocrinology.

[2]  R. Q. Edwards,et al.  Image Separation Radioisotope Scanning , 1963 .

[3]  Joy Hirsch,et al.  Leptin reverses weight loss-induced changes in regional neural activity responses to visual food stimuli. , 2008, The Journal of clinical investigation.

[4]  J. Speakman,et al.  The contribution of animal models to the study of obesity , 2008, Laboratory animals.

[5]  J. Neel Diabetes mellitus: a "thrifty" genotype rendered detrimental by "progress"? , 1962, American journal of human genetics.

[6]  Ernst Fernando Lopes Da Silva Niedermeyer,et al.  Electroencephalography, basic principles, clinical applications, and related fields , 1982 .

[7]  K. Berridge,et al.  Parsing reward , 2003, Trends in Neurosciences.

[8]  James R C Parkinson,et al.  Imaging Appetite-Regulating Pathways in the Central Nervous System Using Manganese-Enhanced Magnetic Resonance Imaging , 2008, Neuroendocrinology.

[9]  R. Schultz,et al.  Food-related Neural Circuitry in Prader-Willi Syndrome: Response to High- Versus Low-calorie Foods , 2008, Journal of autism and developmental disorders.

[10]  A. Roebroeck,et al.  Behavioural Brain Research , 2015 .

[11]  Sidney A. Simon,et al.  Food Reward in the Absence of Taste Receptor Signaling , 2008, Neuron.

[12]  Edythe D. London,et al.  Leptin replacement alters brain response to food cues in genetically leptin-deficient adults , 2007, Proceedings of the National Academy of Sciences.

[13]  J. Jansen,et al.  Coffee stimulation of cholecystokinin release and gallbladder contraction in humans. , 1990, The American journal of clinical nutrition.

[14]  Deborah A Yurgelun-Todd,et al.  Body mass predicts orbitofrontal activity during visual presentations of high-calorie foods , 2005, Neuroreport.

[15]  X Golay,et al.  Non-invasive Measurement of Perfusion: a Critical Review of Arterial Spin Labelling Techniques , 2022 .

[16]  R. Batterham,et al.  Gut hormones: implications for the treatment of obesity. , 2009, Pharmacology & therapeutics.

[17]  Vijay K. Venkatraman,et al.  Altered reward processing in women recovered from anorexia nervosa. , 2007, The American journal of psychiatry.

[18]  D. Le Bihan,et al.  Direct and fast detection of neuronal activation in the human brain with diffusion MRI. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[19]  C. Carter,et al.  Altered brain activity in women recovered from bulimic-type eating disorders after a glucose challenge: a pilot study. , 2006, The International journal of eating disorders.

[20]  Piotr Bogorodzki,et al.  Cortical and limbic activation during viewing of high- versus low-calorie foods , 2003, NeuroImage.

[21]  G Andrew James,et al.  Enhanced activation of reward mediating prefrontal regions in response to food stimuli in Prader–Willi syndrome , 2006, Journal of Neurology, Neurosurgery & Psychiatry.

[22]  Jimmy D Bell,et al.  Critical role for peptide YY in protein-mediated satiation and body-weight regulation. , 2006, Cell metabolism.

[23]  E. Bullmore,et al.  Leptin Regulates Striatal Regions and Human Eating Behavior , 2007, Science.

[24]  Jeroen van der Grond,et al.  Effect of satiety on brain activation during chocolate tasting in men and women. , 2006, The American journal of clinical nutrition.

[25]  W. Langhans,et al.  Overview of the physiological control of eating. , 2010, Forum of nutrition.

[26]  Hans-Christian Bauknecht,et al.  Differential activation of the dorsal striatum by high-calorie visual food stimuli in obese individuals , 2007, NeuroImage.

[27]  K. Berridge,et al.  Erratum to: “Parsing reward” [Trends Neurosci. 26 (2003) 507–513] , 2003, Trends in Neurosciences.

[28]  M. Tschöp,et al.  Ghrelin induces adiposity in rodents , 2000, Nature.

[29]  N. Hwalla,et al.  Variation of Postprandial PYY3–36Response following Ingestion of Differing Macronutrient Meals in Obese Females , 2008, Annals of Nutrition and Metabolism.

[30]  S. Ogawa,et al.  Oxygenation‐sensitive contrast in magnetic resonance image of rodent brain at high magnetic fields , 1990, Magnetic resonance in medicine.

[31]  A. Klibanski,et al.  Elevated peptide YY levels in adolescent girls with anorexia nervosa. , 2006, The Journal of clinical endocrinology and metabolism.

[32]  M. Stumvoll,et al.  Brain Activity in Hunger and Satiety: An Exploratory Visually Stimulated fMRI Study , 2008, Obesity.

[33]  J. W. Aldridge,et al.  Dissecting components of reward: 'liking', 'wanting', and learning. , 2009, Current opinion in pharmacology.

[34]  A. Alavi,et al.  The [18F]Fluorodeoxyglucose Method for the Measurement of Local Cerebral Glucose Utilization in Mane , 1979, Circulation research.

[35]  A. Villringer,et al.  Simultaneous EEG–fMRI , 2006, Neuroscience & Biobehavioral Reviews.

[36]  H. Berger Über das Elektrenkephalogramm des Menschen , 1933, Archiv für Psychiatrie und Nervenkrankheiten.

[37]  James A King,et al.  Influence of resistance and aerobic exercise on hunger, circulating levels of acylated ghrelin, and peptide YY in healthy males. , 2009, American journal of physiology. Regulatory, integrative and comparative physiology.

[38]  H. Berger Über das Elektrenkephalogramm des Menschen , 1929, Archiv für Psychiatrie und Nervenkrankheiten.

[39]  E. Mittra,et al.  Positron emission tomography/computed tomography: the current technology and applications. , 2009, Radiologic clinics of North America.

[40]  J. Gore Principles and practice of functional MRI of the human brain. , 2003, The Journal of clinical investigation.

[41]  R. Turner,et al.  Dynamic magnetic resonance imaging of human brain activity during primary sensory stimulation. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[42]  Donald B. Twieg,et al.  Widespread reward-system activation in obese women in response to pictures of high-calorie foods , 2008, NeuroImage.

[43]  D. Cohen Magnetoencephalography: Evidence of Magnetic Fields Produced by Alpha-Rhythm Currents , 1968, Science.

[44]  Alain Dagher,et al.  Ghrelin modulates brain activity in areas that control appetitive behavior. , 2008, Cell metabolism.

[45]  J. Salles,et al.  Hyperghrelinemia precedes obesity in Prader-Willi syndrome. , 2008, The Journal of clinical endocrinology and metabolism.

[46]  D. Ffytche,et al.  PYY modulation of cortical and hypothalamic brain areas predicts feeding behaviour in humans , 2007, Nature.

[47]  A. Dagher,et al.  Genetic variation in dopaminergic reward in humans. , 2010, Forum of nutrition.

[48]  Fernando Lopes da Silva,et al.  Comprar Niedermeyer's Electroencephalography, 6/e (Basic Principles, Clinical Applications, and Related Fields ) | Fernando Lopes Da Silva | 9780781789424 | Lippincott Williams & Wilkins , 2010 .