A functional neuroimaging review of obesity, appetitive hormones and ingestive behavior

Physiology and Behavior

Volumn 136, Issue , 2014, Pages 121-127

  Burger, Kyle S ^a   Berner, Laura A ^b  

^a IL   (United States)

^b DREXEL UNIVERSITY COLLEGE OF MEDICINE   (United States)

Author keywords

Appetitive hormones; Food intake; Functional MRI; Ingestive behavior; Obesity; Reward

Indexed keywords

GHRELIN; GLUCAGON LIKE PEPTIDE 1; INSULIN; LEPTIN; PEPTIDE YY;

AMYGDALOID NUCLEUS; ANTERIOR CINGULATE; ANTERIOR INSULA; APPETITE; ARTICLE; BODY WEIGHT; BOLD SIGNAL; CORPUS STRIATUM; ENDOCRINE FUNCTION; FAT INTAKE; FEEDING BEHAVIOR; FOLLOW UP; FOOD; FOOD COMPOSITION; FRONTAL OPERCULUM; FUNCTIONAL NEUROIMAGING; GUSTATORY CORTEX; HUMAN; INSULA; LEAN BODY WEIGHT; OBESITY; PROTEIN EXPRESSION; RISK FACTOR; SECONDARY SOMATOSENSORY CORTEX; SUGAR INTAKE; VENTROMEDIAL PREFRONTAL CORTEX; WEIGHT CHANGE; WEIGHT GAIN; ANIMAL; BRAIN; METABOLISM; NEUROIMAGING; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; VASCULARIZATION;

ANIMALS; APPETITIVE BEHAVIOR; BRAIN; FEEDING BEHAVIOR; HUMANS; NEUROIMAGING; OBESITY;

EID: 84917727498     PISSN: 00319384     EISSN: 1873507X     Source Type: Journal    
DOI: 10.1016/j.physbeh.2014.04.025     Document Type: Article

References (89)

1. Flegal K.M., Carroll M.D., Kit B.K., Ogden C.L. Prevalence of obesity and trends in the distribution of body mass index among US adults, 1999-2010. J Am Med Assoc 2012, 307:491-497.
2. Luppino F.S., de Wit L.M., Bouvy P.F., Stijnen T., Cuijpers P., Penninx B.W.J.H., et al. Overweight, obesity, and depression a systematic review and meta-analysis of longitudinal studies. Arch Gen Psychiatry 2010, 67:220-229.
3. Lutter M., Nestler E.J. Homeostatic and hedonic signals interact in the regulation of food intake. J Nutr 2009, 139:629-632.
4. Morton G., Cummings D., Baskin D., Barsh G., Schwartz M. Central nervous system control of food intake and body weight. Nature 2006, 443:289-295.
5. Wang G.J., Volkow N.D., Logan J., Pappas N.R., Wong C.T., Zhu W., et al. Brain dopamine and obesity. Lancet 2001, 357:354-357.
6. Davis C., Strachan S., Berkson M. Sensitivity to reward: implications for overeating and overweight. Appetite 2004, 42:131-138.
7. Berridge K.C., Ho C.-Y., Richard J.M., DiFeliceantonio A.G. The tempted brain eats: pleasure and desire circuits in obesity and eating disorders. Brain Res 2010, 1350:43-64.
8. Stice E., Yokum S., Burger K.S., Epstein L.H., Small D.M. Youth at risk for obesity show greater activation of striatal and somatosensory regions to food. J Neurosci 2011, 31:4360-4366.
9. Dimitropoulos A., Tkach J., Ho A., Kennedy J. Greater corticolimbic activation to high-calorie food cues after eating in obese vs. normal-weight adults. Appetite 2012, 58:303-312.
10. Frankort A., Roefs A., Siep N., Roebroeck A., Havermans R., Jansen A. Reward activity in satiated overweight women is decreased during unbiased viewing but increased when imagining taste: an event-related fMRI study. Int J Obes (Lond) 2012, 36:627-637.
11. Bruce A., Holsen L., Chambers R., Martin L., Brooks W., Zarcone J., et al. Obese children show hyperactivation to food pictures in brain networks linked to motivation, reward and cognitive control. Int J Obes (Lond) 2010, 34:1494-1500.
12. Nummenmaa L., Hirvonen J., Hannukainen J.C., Immonen H., Lindroos M.M., Salminen P., et al. Dorsal striatum and its limbic connectivity mediate abnormal anticipatory reward processing in obesity. PLoS One 2012, 7.
13. Rothemund Y., Preuschhof C., Bohner G., Bauknecht H.-C., Klingebiel R., Flor H., et al. Differential activation of the dorsal striatum by high-calorie visual food stimuli in obese individuals. Neuroimage 2007, 37:410-421.
14. Martin L.E., Holsen L.M., Chambers R.J., Bruce A.S., Brooks W.M., Zarcone J.R., et al. Neural mechanisms associated with food motivation in obese and healthy weight adults. Obesity 2009, 18:254-260.
15. Stoeckel L.E., Weller R.E., Cook E.W., Twieg D.B., Knowlton R.C., Cox J.E. Widespread reward-system activation in obese women in response to pictures of high-calorie foods. Neuroimage 2008, 41:636-647.
16. Ng J., Stice E., Yokum S., Bohon C. An fMRI study of obesity, food reward, and perceived caloric density. Does a low-fat label make food less appealing?. Appetite 2011, 57:65-72.
17. Stice E., Spoor S., Bohon C., Veldhuizen M.G., Small D.M. Relation of reward from food intake and anticipated food intake to obesity: a functional magnetic resonance imaging study. J Abnorm Psychol 2008, 117:924-935.
18. Beaver J.D., Lawrence A.D., Van Ditzhuijzen J., Davis M.H., Woods A., Calder A.J. Individual differences in reward drive predict neural responses to images of food. J Neurosci 2006, 26:5160-5166.
19. Babbs R.K., Sun X., Felsted J., Chouinard-Decorte F., Veldhuizen M.G., Small D. Decreased caudate response to milkshake is associated with higher body mass index and greater impulsivity. Physiol Behav 2013, 103-111.
20. Stice E., Spoor S., Bohon C., Small D.M. Relation between obesity and blunted striatal response to food is moderated by TaqIA A1 allele. Science 2008, 322:449-452.
21. Frank G.K., Reynolds J.R., Shott M.E., Jappe L., Yang T.T., Tregellas J.R., et al. Anorexia nervosa and obesity are associated with opposite brain reward response. Neuropsychopharmacology 2012, 37:2031-2046.
22. Green E., Jacobson A., Haase L., Murphy C. Reduced nucleus accumbens and caudate nucleus activation to a pleasant taste is associated with obesity in older adults. Brain Res 2011, 1386:109-117.
23. Berkman E.T., Falk E.B. Beyond brain mapping using neural measures to predict real-world outcomes. Curr Dir Psychol Sci 2013, 22:45-50.
24. Yokum S., Ng J., Stice E. Attentional bias to food images associated with elevated weight and future weight gain: an fMRI study. Obesity 2011, 19:1775-1783.
25. Demos K.E., Heatherton T.F., Kelley W.M. Individual differences in nucleus accumbens activity to food and sexual images predict weight gain and sexual behavior. J Neurosci 2012, 32:5549-5552.
26. Stice E., Yokum S., Burger K.S. Elevated reward region responsivity predicts future substance use onset but not overweight/obesity onset. Biol Psychiatry 2013, 73:869-876.
27. Murdaugh D.L., Cox J.E., Cook E.W., Weller R.E. fMRI reactivity to high-calorie food pictures predicts short- and long-term outcome in a weight-loss program. Neuroimage 2012, 59:2709-2721.
28. Geha P.Y., Aschenbrenner K., Felsted J., O'Malley S.S., Small D.M. Altered hypothalamic response to food in smokers. Am J Clin Nutr 2013, 97:15-22.
29. Cornier M.-A., Melanson E.L., Salzberg A.K., Bechtell J.L., Tregellas J.R. The effects of exercise on the neuronal response to food cues. Physiol Behav 2012, 105:1028-1034.
30. Stice E., Yokum S., Blum K., Bohon C. Weight gain is associated with reduced striatal response to palatable food. J Neurosci 2010, 30:13105-13109.
31. Abizaid A., Liu Z.-W., Andrews Z.B., Shanabrough M., Borok E., Elsworth J.D., et al. Ghrelin modulates the activity and synaptic input organization of midbrain dopamine neurons while promoting appetite. J Clin Invest 2006, 116:3229-3239.
32. Campfield L.A., Smith F.J., Guisez Y., Devos R., Burn P. Recombinant mouse OB protein: evidence for a peripheral signal linking adiposity and central neural networks. Science 1995, 269:546-549.
33. Schwartz M.W., Woods S.C., Porte D., Seeley R.J., Baskin D.G. Central nervous system control of food intake. Nature 2000, 404:661-671.
34. Williams K.W., Scott M.M., Elmquist J.K. From observation to experimentation: leptin action in the mediobasal hypothalamus. Am J Clin Nutr 2009, 89:985S-990S.
35. Considine R.V., Sinha M.K., Heiman M.L., Kriauciunas A., Stephens T.W., Nyce M.R., et al. Serum immunoreactive leptin concentrations in normal-weight and obese humans. N Engl J Med 1996, 334:292-295.
36. Havel P.J., KasimKarakas S., Mueller W., Johnson P.R., Gingerich R.L., Stern J.S. Relationship of plasma leptin to plasma insulin and adiposity in normal weight and overweight women: effects of dietary fat content and sustained weight loss. J Clin Endocrinol Metab 1996, 81:4406-4413.
37. Schwartz M.W., Peskind E., Raskind M., Boyko E.J., Porte D. Cerebrospinal fluid leptin levels: relationship to plasma levels and to adiposity in humans. Nat Med 1996, 2:589-593.
38. Enriori P.J., Evans A.E., Sinnayah P., Cowley M.A. Leptin resistance and obesity. Obesity 2006, 14:254-258.
39. Klok M., Jakobsdottir S., Drent M. The role of leptin and ghrelin in the regulation of food intake and body weight in humans: a review. Obes Rev 2007, 8:21-34.
40. Baicy K., London E.D., Monterosso J., Wong M.-L., Delibasi T., Sharma A., et al. Leptin replacement alters brain response to food cues in genetically leptin-deficient adults. Proc Natl Acad Sci 2007, 104:18276-18279.
41. Farooqi I.S., Bullmore E., Keogh J., Gillard J., O'Rahilly S., Fletcher P.C. Leptin regulates striatal regions and human eating Behavior. Science 2007, 317:1355.
42. Batterham R.L., Cohen M.A., Ellis S.M., Le Roux C.W., Withers D.J., Frost G.S., et al. Inhibition of food intake in obese subjects by peptide YY3-36. N Engl J Med 2003, 349:941-948.
43. Näslund E., Barkeling B., King N., Gutniak M., Blundell J., Holst J., et al. Energy intake and appetite are suppressed by glucagon-like peptide-1 (GLP-1) in obese men. Int J Obes (Lond) 1999, 23:304-311.
44. Verdich C., Flint A., Gutzwiller J.P., Naslund E., Beglinger C., Hellstrom P.M., et al. A meta-analysis of the effect of glucagon-like peptide-1 (7-36) amide on ad libitum energy intake in humans. J Clin Endocrinol Metab 2001, 86:4382-4389.
45. Ranganath L.R., Beety J.M., Morgan L.M., Wright J.W., Howland R., Marks V. Attenuated GLP-1 secretion in obesity: cause or consequence?. Gut 1996, 38:916-919.
46. Naslund E., Gutniak M., Skogar S., Rossner S., Hellstrom P.M. Glucagon-like peptide 1 increases the period of postprandial satiety and slows gastric emptying in obese men. Am J Clin Nutr 1998, 68:525-530.
47. 7-36 amide reduce food intake and modulate brain activity in appetite centers in humans. Cell Metab 2011, 14:700-706.
48. Pannacciulli N., Le D.S.N., Salbe A.D., Chen K., Reiman E.M., Tataranni P.A., et al. Postprandial glucagon-like peptide-1 (GLP-1) response is positively associated with changes in neuronal activity of brain areas implicated in satiety and food intake regulation in humans. Neuroimage 2007, 35:511-517.
49. Kojima M., Hosoda H., Date Y., Nakazato M., Matsuo H., Kangawa K. Ghrelin is a growth-hormone-releasing acylated peptide from stomach. Nature 1999, 402:656-660.
50. Nakazato M., Murakami N., Date Y., Kojima M., Matsuo H., Kangawa K., et al. A role for ghrelin in the central regulation of feeding. Nature 2001, 409:194-198.
51. Tschöp M., Weyer C., Tataranni P.A., Devanarayan V., Ravussin E., Heiman M.L. Circulating ghrelin levels are decreased in human obesity. Diabetes 2001, 50:707-709.
52. English P., Ghatei M., Malik I., Bloom S., Wilding J. Food fails to suppress ghrelin levels in obese humans. J Clin Endocrinol Metab 2002, 87:2984.
53. Druce M., Wren A., Park A., Milton J., Patterson M., Frost G., et al. Ghrelin increases food intake in obese as well as lean subjects. Int J Obes (Lond) 2005, 29:1130-1136.
54. Wren A., Seal L., Cohen M., Brynes A., Frost G., Murphy K., et al. Ghrelin enhances appetite and increases food intake in humans. J Clin Endocrinol Metab 2001, 86:5992.
55. Malik S., McGlone F., Bedrossian D., Dagher A. Ghrelin modulates brain activity in areas that control appetitive behavior. Cell Metab 2008, 7:400-409.
56. Karra E., O'Daly O.G., Choudhury A.I., Yousseif A., Millership S., Neary M.T., et al. A link between FTO, ghrelin, and impaired brain food-cue responsivity. J Clin Invest 2013, 123:3539.
57. Björntorp P. Obesity, atherosclerosis and diabetes mellitus 1987, 443-448. Springer, Kongreß.
58. Guthoff M., Grichisch Y., Canova C., Tschritter O., Veit R., Hallschmid M., et al. Insulin modulates food-related activity in the central nervous system. J Clin Endocrinol Metab 2010, 95:748-755.
59. Tataranni P.A., Gautier J.-F., Chen K., Uecker A., Bandy D., Salbe A.D., et al. Neuroanatomical correlates of hunger and satiation in humans using positron emission tomography. Proc Natl Acad Sci 1999, 96:4569-4574.
60. Kullmann S., Heni M., Veit R., Ketterer C., Schick F., Häring H.U., et al. The obese brain: association of body mass index and insulin sensitivity with resting state network functional connectivity. Hum Brain Mapp 2012, 33:1052-1061.
61. Kenny P.J. Common cellular and molecular mechanisms in obesity and drug addiction. Nat Rev Neurosci 2011, 12:638-651.
62. Volkow N.D., Wang G.-J., Fowler J.S., Telang F. Overlapping neuronal circuits in addiction and obesity: evidence of systems pathology. Philos Trans R Soc Lond B Biol Sci 2008, 363:3191-3200.
63. Tang D.W., Fellows L.K., Small D.M., Dagher A. Food and drug cues activate similar brain regions: a meta-analysis of functional MRI studies. Physiol Behav 2012, 106:317-324.
64. Nolan-Poupart S., Veldhuizen M.G., Geha P., Small D.M. Midbrain response to milkshake correlates with ad libitum milkshake intake in the absence of hunger. Appetite 2013, 60:168-174.
65. Lawrence N.S., Hinton E.C., Parkinson J.A., Lawrence A.D. Nucleus accumbens response to food cues predicts subsequent snack consumption in women and increased body mass index in those with reduced self-control. Neuroimage 2012, 415-422.
66. Burger K.S., Stice E. Elevated energy intake is correlated with hyperresponsivity in attentional, gustatory, and reward brain regions while anticipating palatable food receipt. Am J Clin Nutr 2013, 97:1188-1194.
67. Burger K.S., Stice E. Neural responsivity during soft drink intake, anticipation, and advertisement exposure in habitually consuming youth. Obesity 2014, 22:441-450.
68. Green E., Murphy C. Altered processing of sweet taste in the brain of diet soda drinkers. Physiol Behav 2012, 107:560-567.
69. Rudenga K., Small D. Amygdala response to sucrose consumption is inversely related to artificial sweetener use. Appetite 2012, 58:504-507.
70. Burger K.S., Stice E. Frequent ice cream consumption is associated with reduced striatal response to receipt of an ice cream-based milkshake. Am J Clin Nutr 2012, 95:810-817.
71. Grabenhorst F., Rolls E.T., Parris B.A., d'Souza A.A. How the brain represents the reward value of fat in the mouth. Cereb Cortex 2010, 20:1082-1091.
72. De Araujo I.E., Rolls E.T. Representation in the human brain of food texture and oral fat. J Neurosci 2004, 24:3086-3093.
73. Stice E., Burger K.S., Yokum S. Relative ability of fat and sugar tastes to activate reward, gustatory, and somatosensory regions. Am J Clin Nutr 2013, 98:1377-1384.
74. Popkin B.M., Nielsen S.J. The sweetening of the world's diet. Obes Res 2003, 11:1325-1332.
75. Leibowitz S.F., Dourmashkin J.T., Chang G.-Q., Hill J.O., Gayles E.C., Fried S.K., et al. Acute high-fat diet paradigms link galanin to triglycerides and their transport and metabolism in muscle. Brain Res 2004, 1008:168-178.
76. Wang J., Akabayashi A., Yu H.J., Dourmashkin J., Alexander J.T., Silva I., et al. Hypothalamic galanin: control by signals of fat metabolism. Brain Res 1998, 804:7-20.
77. Parrado C., Diaz-Cabiale Z., Garcia-Coronel M., Agnati L., Covenas R., Fuxe K., et al. Region specific galanin receptor/neuropeptide Y Y1 receptor interactions in the tel- and diencephalon of the rat. Relevance for food consumption. Neuropharmacology 2007, 52:684-692.
78. Schultz W., Apicella P., Ljungberg T. Responses of monkey dopamine neurons to reward and conditioned-stimuli during successive steps of learning a delayed-response task. J Neurosci 1993, 13:900-913.
79. Berridge K.C., Robinson T.E. What is the role of dopamine in reward: hedonic impact, reward learning, or incentive salience?. Brain Res Rev 1998, 28:309-369.
80. Koob G.F., Le Moal M. Drug addiction, dysregulation of reward, and allostasis. Neuropsychopharmacology 2001, 24:97-129.
81. Epstein L.H., Dearing K.K., Temple J.L., Cavanaugh M.D. Food reinforcement and impulsivity in overweight children and their parents. Eat Behav 2008, 9:319-327.
82. Nederkoorn C., Jansen E., Mulkens S., Jansen A. Impulsivity predicts treatment outcome in obese children. Behav Res Ther 2007, 45:1071-1075.
83. Stoeckel L.E., Murdaugh D.L., Cox J.E., Cook E.W., Weller R.E. Greater impulsivity is associated with decreased brain activation in obese women during a delay discounting task. Brain Imaging Behav 2013, 1-13.
84. Kishinevsky F.I., Cox J.E., Murdaugh D.L., Stoeckel L.E., Cook E.W., Weller R.E. fMRI reactivity on a delay discounting task predicts weight gain in obese women. Appetite 2012, 58:582-592.
85. Batterink L., Yokum S., Stice E. Body mass correlates inversely with inhibitory control in response to food among adolescent girls: an fMRI study. Neuroimage 2010, 52:1696-1703.
86. Cornier M.-A., Salzberg A.K., Endly D.C., Bessesen D.H., Tregellas J.R. Sex-based differences in the behavioral and neuronal responses to food. Physiol Behav 2010, 99:538-543.
87. Del Parigi A., Gautier J.-F., Chen K., Salbe A.D., Ravussin E., Reiman E., et al. Neuroimaging and obesity: mapping the brain responses to hunger and satiation in humans using positron emission tomography. Ann N Y Acad Sci 2002, 967:389-397.
88. Berthoud H.R., Zheng H., Shin A.C. Food reward in the obese and after weight loss induced by calorie restriction and bariatric surgery. Ann N Y Acad Sci 2012, 1264:36-48.
89. Kenny P.J. Reward mechanisms in obesity: new insights and future directions. Neuron 2011, 69:664-679.