Differential effect of glucose ingestion on the neural processing of food stimuli in lean and overweight adults

Human Brain Mapping

Volumn 35, Issue 3, 2014, Pages 918-928

  Heni, Martin ^a   Kullmann, Stephanie ^a   Ketterer, Caroline ^a   Guthoff, Martina ^a   Bayer, Margarete ^a   Staiger, Harald ^a   Machicao, Fausto ^a   Häring, Hans Ulrich ^a   Preissl, Hubert ^a   Veit, Ralf ^a   Fritsche, Andreas ^a  

^a UNIVERSITY OF TÜBINGEN   (Germany)

Author keywords

FMRI; Food; Insulin; Obesity

Indexed keywords

GLUCOSE; GLUCOSE BLOOD LEVEL; INSULIN; WATER;

BLOOD; BODY WEIGHT; BRAIN; BRAIN MAPPING; CLASSIFICATION; COMPARATIVE STUDY; DEVICES; FEEDING BEHAVIOR; FEMALE; FOOD; GLUCOSE BLOOD LEVEL; HUMAN; MALE; METABOLISM; OBESITY; PATHOPHYSIOLOGY; PHYSIOLOGY; PROCEDURES; TIME; YOUNG ADULT;

BLOOD GLUCOSE; BODY WEIGHT; BRAIN; BRAIN MAPPING; FEEDING BEHAVIOR; FEMALE; FOOD; GLUCOSE; HUMANS; INSULIN; MALE; OVERWEIGHT; TIME FACTORS; WATER; YOUNG ADULT;

EID: 84893766301     PISSN: 10659471     EISSN: 10970193     Source Type: Journal    
DOI: 10.1002/hbm.22223     Document Type: Article

References (48)

1. Appelhans BM (2009): Neurobehavioral inhibition of reward-driven feeding: implications for dieting and obesity. Obesity 17:640-647.
2. Bagdade JD, Bierman EL, Porte D Jr (1967): The significance of basal insulin levels in the evaluation of the insulin response to glucose in diabetic and nondiabetic subjects. J Clin Invest 46:1549-1557.
3. Braet C, Crombez G (2003): Cognitive interference due to food cues in childhood obesity. J Clin Child Adolesc Psychol 32:32-39.
4. Camilleri M (2009): Peripheral mechanisms in the control of appetite and related experimental therapies in obesity. Regul Pept 156:24-27.
5. de Graaf C, Blom WA, Smeets PA, Stafleu A, Hendriks HF (2004): Biomarkers of satiation and satiety. Am J Clin Nutr 79:946-961.
6. Del Parigi A, Gautier JF, Chen K, Salbe AD, Ravussin E, Reiman E, Tataranni PA (2002): Neuroimaging and obesity: Mapping the brain responses to hunger and satiation in humans using positron emission tomography. Ann NY Acad Sci 967:389-397.
7. Frank S, Laharnar N, Kullmann S, Veit R, Canova C, Hegner YL, Fritsche A, Preissl H (2010): Processing of food pictures: Influence of hunger, gender and calorie content. Brain Res 1350:159-166.
8. Fuhrer D, Zysset S, Stumvoll M (2008): Brain activity in hunger and satiety: an exploratory visually stimulated FMRI study. Obesity 16:945-950.
9. Fung TT, Schulze M, Manson JE, Willett WC, Hu FB (2004): Dietary patterns, meat intake, and the risk of type 2 diabetes in women. Arch Intern Med 164:2235-2240.
10. Grichisch Y, Cavusoglu M, Preissl H, Uludag K, Hallschmid M, Birbaumer N, Haring HU, Fritsche A, Veit R (2011): Differential effects of intranasal insulin and caffeine on cerebral blood flow. Hum Brain Mapp 33:280-287.
11. Guthoff M, Grichisch Y, Canova C, Tschritter O, Veit R, Hallschmid M, Haring HU, Preissl H, Hennige AM, Fritsche A (2010): Insulin modulates food-related activity in the central nervous system. J Clin Endocrinol Metab 95:748-755.
12. Guthoff M, Stingl KT, Tschritter O, Rogic M, Heni M, Stingl K, Hallschmid M, Haring HU, Fritsche A, Preissl H, Hennige AM (2011): The insulin-mediated modulation of visually evoked magnetic fields is reduced in obese subjects. PLoS One 6:e19482.
13. Halford JC, Gillespie J, Brown V, Pontin EE, Dovey TM.2004.Effect of television advertisements for foods on food consumption in children. Appetite 42:221-225.
14. Hallschmid M, Schultes B (2009): Central nervous insulin resistance:A promising target in the treatment of metabolic and cognitive disorders? Diabetologia 52:2264-2269.
15. Heni M, Kullmann S, Ketterer C, Guthoff M, Linder K, Wagner R, Stingl KT, Veit R, Staiger H, Haring HU, Preissl H, Fritsche A (2012): Nasal insulin changes peripheral insulin sensitivity simultaneously with altered activity in homeostatic and reward-related human brain regions. Diabetologia 55:1773-1782.
16. Johnson F, Pratt M, Wardle J (2011): Dietary restraint and self-regulation in eating behavior. Int J Obes 36:665-674.
17. Ketterer C, Tschritter O, Preissl H, Heni M, Haring HU, Fritsche A (2011): Insulin sensitivity of the human brain. Diabetes Res Clin Pract 93(Suppl 1):S47-S51.
18. Killgore WD, Yurgelun-Todd DA (2007): Positive affect modulates activity in the visual cortex to images of high calorie foods. Int J Neurosci 117:643-653.
19. Kroemer NB, Krebs L, Kobiella A, Grimm O, Vollstadt-Klein S, Wolfensteller U, Kling R, Bidlingmaier M, Zimmermann US, Smolka MN (2012): (Still) longing for food: Insulin reactivity modulates response to food pictures. Hum Brain Mapp. DOI: 10.1002/hbm.22071.
20. Kullmann S, Frank S, Heni M, Ketterer C, Veit R, Haring HU, Fritsche A, Preissl H (2012a): Intranasal insulin modulates intrinsic reward and prefrontal circuitry of the human brain in lean women. Neuroendocrinology. DOI: 10.1159/000341406.
21. Kullmann S, Heni M, Veit R, Ketterer C, Schick F, Haring HU, Fritsche A, Preissl H (2012b): The obese brain: Association of body mass index and insulin sensitivity with resting state network functional connectivity. Hum Brain Mapp 33:1052-1061.
22. Le DS, Pannacciulli N, Chen K, Del Parigi A, Salbe AD, Reiman EM, Krakoff J (2006): Less activation of the left dorsolateral prefrontal cortex in response to a meal: A feature of obesity. Am J Clin Nutr 84:725-731.
23. Liu Y, Gao JH, Liu HL, Fox PT (2000): The temporal response of the brain after eating revealed by functional MRI. Nature 405:1058-1062.
24. Löwe B, Spitzer RL, Zipfel S, Herzog W (2002): PHQ-D. Gesundheitsfragebogen für Patienten. Karlsruhe, DEU:Pfitzer.
25. Martin LE, Holsen LM, Chambers RJ, Bruce AS, Brooks WM, Zarcone JR, Butler MG, Savage CR (2009): Neural mechanisms associated with food motivation in obese and healthy weight adults. Obesity. (Silver Spring) 18:254-260.
26. Matsuda M, DeFronzo RA (1999): Insulin sensitivity indices obtained from oral glucose tolerance testing: Comparison with the euglycemic insulin clamp. Diabetes Care 22:1462-1470.
27. Matsuda M, Liu Y, Mahankali S, Pu Y, Mahankali A, Wang J, DeFronzo RA, Fox PT, Gao JH (1999): Altered hypothalamic function in response to glucose ingestion in obese humans. Diabetes 48:1801-1806.
28. McNair DM, Lorr M, Droppelmann LF (1981): Manual for the Profile of Mood States. San Diego:Educational and Industrial Testing Service.
29. Morton GJ, Cummings DE, Baskin DG, Barsh GS, Schwartz MW (2006): Central nervous system control of food intake and body weight. Nature 443:289-295.
30. Nijs IM, Muris P, Euser AS, Franken IH (2010): Differences in attention to food and food intake between overweight/obese and normal-weight females under conditions of hunger and satiety. Appetite 54:243-254.
31. Oomura Y, Ooyama H, Sugimori M, Nakamura T, Yamada Y (1974): Glucose inhibition of the glucose-sensitive neurone in the rat lateral hypothalamus. Nature 247:284-286.
32. Page KA, Arora J, Qiu M, Relwani R, Constable RT, Sherwin RS (2009): Small decrements in systemic glucose provoke increases in hypothalamic blood flow prior to the release of counterregulatory hormones. Diabetes 58:448-452.
33. Page KA, Seo D, Belfort-DeAguiar R, Lacadie C, Dzuira J, Naik S, Amarnath S, Constable RT, Sherwin RS, Sinha R (2011): Circulating glucose levels modulate neural control of desire for high-calorie foods in humans. J Clin Invest 121:4161-4169.
34. Porubska K, Veit R, Preissl H, Fritsche A, Birbaumer N (2006): Subjective feeling of appetite modulates brain activity: An fMRI study. Neuroimage 32:1273-1280.
35. Pudel D, Westenhöfer J (1989): Fragebogen zum Eßverhalten (FEV). Handanweisung. Göttingen:Hogrefe.
36. Rothemund Y, Preuschhof C, Bohner G, Bauknecht HC, Klingebiel R, Flor H, Klapp BF (2007): Differential activation of the dorsal striatum by high-calorie visual food stimuli in obese individuals. Neuroimage 37:410-421.
37. Rotte M, Baerecke C, Pottag G, Klose S, Kanneberg E, Heinze HJ, Lehnert H (2005): Insulin affects the neuronal response in the medial temporal lobe in humans. Neuroendocrinology 81:49-55.
38. Schloegl H, Percik R, Horstmann A, Villringer A, Stumvoll M (2011): Peptide hormones regulating appetite-focus on neuroimaging studies in humans. Diabetes Metab Res Rev 27:104-112.
39. Schur EA, Kleinhans NM, Goldberg J, Buchwald D, Schwartz MW, Maravilla K (2009): Activation in brain energy regulation and reward centers by food cues varies with choice of visual stimulus. Int J Obes 33:653-661.
40. Siep N, Roefs A, Roebroeck A, Havermans R, Bonte ML, Jansen A (2009): Hunger is the best spice: An fMRI study of the effects of attention, hunger and calorie content on food reward processing in the amygdala and orbitofrontal cortex. Behav Brain Res 198:149-158.
41. Smeets PA, de Graaf C, Stafleu A, van Osch MJ, van der Grond J (2005a): Functional magnetic resonance imaging of human hypothalamic responses to sweet taste and calories. Am J Clin Nutr 82:1011-1016.
42. Smeets PA, de Graaf C, Stafleu A, van Osch MJ, van der Grond J (2005b): Functional MRI of human hypothalamic responses following glucose ingestion. Neuroimage 24:363-368.
43. Stice E, Spoor S, Bohon C, Small DM (2008): Relation between obesity and blunted striatal response to food is moderated by TaqIA A1 allele. Science 322:449-452.
44. Stingl KT, Kullmann S, Guthoff M, Heni M, Fritsche A, Preissl H (2010): Insulin modulation of magnetoencephalographic resting state dynamics in lean and obese subjects. Front Syst Neurosci 4:157.
45. Stoeckel LE, Weller RE, Cook EWIII, Twieg DB, Knowlton RC, Cox JE (2008): Widespread reward-system activation in obese women in response to pictures of high-calorie foods. Neuroimage 41:636-647.
46. Tataranni PA, Gautier JF, Chen K, Uecker A, Bandy D, Salbe AD, Pratley RE, Lawson M, Reiman EM, Ravussin E (1999): Neuroanatomical correlates of hunger and satiation in humans using positron emission tomography. Proc Natl Acad Sci USA 96:4569-4574.
47. Tschritter O, Preissl H, Hennige AM, Stumvoll M, Porubska K, Frost R, Marx H, Klosel B, Lutzenberger W, Birbaumer N, Haring HU, Fritsche A (2006): The cerebrocortical response to hyperinsulinemia is reduced in overweight humans: A magnetoencephalographic study. Proc Natl Acad Sci USA 103:12103-12108.
48. Wang GJ, Volkow ND, Logan J, Pappas NR, Wong CT, Zhu W, Netusil N, Fowler JS (2001): Brain dopamine and obesity. Lancet 357:354-357.