Brain PET Imaging in Obesity and Food Addiction: Current Evidence and Hypothesis

The ongoing epidemics of obesity is one main health concern of the present time. Overeating in some obese individuals shares similarities with the loss of control and compulsive behavior observed in drug-addicted subjects, suggesting that obesity may involve food addiction. Here, we review the contributions provided by the use of positron emission tomography to the current understanding of the cerebral control of obesity and food intake in humans. The available studies have shown that multiple areas in the brain are involved with the reward properties of food, such as prefrontal, orbitofrontal, somatosensory cortices, insula, thalamus, hypothalamus, amygdala, and others. This review summarizes the current evidence, supporting the concepts that i) regions involved in the somatosensory response to food sight, taste, and smell are activated by palatable foods and may be hyperresponsive in obese individuals, ii) areas controlling executive drive seem to overreact to the anticipation of pleasure during cue exposure, and iii) those involved in cognitive control and inhibitory behavior may be resistant to the perception of reward after food exposure in obese subjects. All of these features may stimulate, for different reasons, ingestion of highly palatable and energy-rich foods. Though these same regions are similarly involved in drug abusers and game-addicted individuals, any direct resemblance may be an oversimplification, especially as the heterogeneities between studies and the prevalent exclusion of sensitive groups still limit a coherent interpretation of the findings. Further work is required to comprehensively tackle the multifaceted phenotype of obesity and identify the role of food dependency in its pathophysiology.

[1]  E. Reiman,et al.  Less activation of the left dorsolateral prefrontal cortex in response to a meal: a feature of obesity. , 2006, The American journal of clinical nutrition.

[2]  Rita Z. Goldstein,et al.  Inverse Association Between BMI and Prefrontal Metabolic Activity in Healthy Adults , 2009, Obesity.

[3]  V L Villemagne,et al.  Activation of memory circuits during cue-elicited cocaine craving. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[4]  Activation of brain regions in rats during food-intake operant behavior , 1984, Physiology & Behavior.

[5]  F. Gonon,et al.  Prefrontal cortex regulates burst firing and transmitter release in rat mesolimbic dopamine neurons studied in vivo , 1993, Neuroscience Letters.

[6]  P. Dupont,et al.  Regional brain activation during proximal stomach distention in humans: A positron emission tomography study. , 2005, Gastroenterology.

[7]  Emer Hughes,et al.  Fasting biases brain reward systems towards high‐calorie foods , 2009, The European journal of neuroscience.

[8]  J S Fowler,et al.  Regional brain metabolic activation during craving elicited by recall of previous drug experiences. , 1999, Life sciences.

[9]  N. Kiriike,et al.  D2 receptors in the ventrolateral striatum are involved in feeding behavior in rats , 1995, Pharmacology Biochemistry and Behavior.

[10]  A. Heinz,et al.  Psychopathological correlates of reduced dopamine receptor sensitivity in depression, schizophrenia, and opiate and alcohol dependence. , 2001, Pharmacopsychiatry.

[11]  J. Metcalfe,et al.  Neural Systems and Cue-Induced Cocaine Craving , 2002, Neuropsychopharmacology.

[12]  M E Phelps,et al.  Positron emission tomography provides molecular imaging of biological processes. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[13]  N. Volkow,et al.  Decreased dopamine D2 receptor availability is associated with reduced frontal metabolism in cocaine abusers , 1993, Synapse.

[14]  Yu-Shin Ding,et al.  Brain dopamine is associated with eating behaviors in humans. , 2003, The International journal of eating disorders.

[15]  Nora D. Volkow,et al.  Profound Decreases in Dopamine Release in Striatum in Detoxified Alcoholics: Possible Orbitofrontal Involvement , 2007, The Journal of Neuroscience.

[16]  Nora D. Volkow,et al.  Enhanced resting activity of the oral somatosensory cortex in obese subjects , 2002, Neuroreport.

[17]  Jean Logan,et al.  Brain dopamine and obesity , 2001, The Lancet.

[18]  J. Votaw,et al.  Acute brain metabolic effects of cocaine in rhesus monkeys with a history of cocaine use , 2010, Brain Imaging and Behavior.

[19]  E M Reiman,et al.  Effect of satiation on brain activity in obese and lean women. , 2001, Obesity research.

[20]  Yu-Shin Ding,et al.  Low dopamine striatal D2 receptors are associated with prefrontal metabolism in obese subjects: Possible contributing factors , 2008, NeuroImage.

[21]  S Minoshima,et al.  Gastric distention correlates with activation of multiple cortical and subcortical regions. , 2001, Gastroenterology.

[22]  Sang Soo Cho,et al.  Altered Regional Cerebral Glucose Metabolism in Internet Game Overusers: A 18F-fluorodeoxyglucose Positron Emission Tomography Study , 2010, CNS Spectrums.

[23]  Tao Wang,et al.  Cerebellar interpositus nucleus modulates neuronal activity of lateral hypothalamic area , 1995, Neuroreport.

[24]  J S Fowler,et al.  Low level of brain dopamine D2 receptors in methamphetamine abusers: association with metabolism in the orbitofrontal cortex. , 2001, The American journal of psychiatry.

[25]  Frank Telang,et al.  High levels of dopamine D2 receptors in unaffected members of alcoholic families: possible protective factors. , 2006, Archives of general psychiatry.

[26]  M. Lutter,et al.  Homeostatic and hedonic signals interact in the regulation of food intake. , 2009, The Journal of nutrition.

[27]  O B Paulson,et al.  No effect of insulin on glucose blood-brain barrier transport and cerebral metabolism in humans. , 1999, Diabetes.

[28]  E. Ravussin,et al.  Neuroanatomical correlates of hunger and satiation in humans using positron emission tomography. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[29]  H. Pijl,et al.  Blocking Dopamine D2 Receptors by Haloperidol Curtails the Beneficial Impact of Calorie Restriction on the Metabolic Phenotype of High‐Fat Diet Induced Obese Mice , 2011, Journal of neuroendocrinology.

[30]  Kewei Chen,et al.  Sex differences in the human brain's response to hunger and satiation. , 2002, The American journal of clinical nutrition.

[31]  Jyrki T. Kuikka,et al.  Regional cerebral blood flow during exposure to food in obese binge eating women , 2000, Psychiatry Research: Neuroimaging.

[32]  N. Volkow,et al.  “Nonhedonic” food motivation in humans involves dopamine in the dorsal striatum and methylphenidate amplifies this effect , 2002, Synapse.

[33]  J. Holst,et al.  Glucagon-Like Peptide-1 Inhibits Blood-Brain Glucose Transfer in Humans , 2008, Diabetes.

[34]  S. Nesterov,et al.  Effects of Insulin on Brain Glucose Metabolism in Impaired Glucose Tolerance , 2011, Diabetes.

[35]  E T Rolls,et al.  Taste and olfactory processing in the brain and its relation to the control of eating. , 1997, Critical reviews in neurobiology.

[36]  Wei Zhu,et al.  Exposure to appetitive food stimuli markedly activates the human brain , 2004, NeuroImage.

[37]  E M Reiman,et al.  Differential brain responses to satiation in obese and lean men. , 2000, Diabetes.

[38]  E. Reiman,et al.  Successful dieters have increased neural activity in cortical areas involved in the control of behavior , 2007, International Journal of Obesity.

[39]  José V. Pardo,et al.  Functional neuroimaging of gastric distention , 2003, Journal of Gastrointestinal Surgery.