Humans with obesity have disordered brain responses to food images during physiological hyperglycemia

American Journal of Physiology - Endocrinology and Metabolism

Volumn 314, Issue 5, 2018, Pages E522-E529

  Belfort DeAguiar, Renata ^a   Seo, Dongju ^a   Lacadie, Cheryl ^a   Naik, Sarita ^a   Schmidt, Christian ^a   Lam, Wai ^a   Hwang, Janice ^a   Constable, Todd ^a   Sinha, Rajita ^a   Sherwin, Robert S ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Brain activity; FMRI; Food cues; Hyperglycemia; Obesity

Indexed keywords

GLUCOSE;

ADULT; ASSOCIATION; BRAIN; BRAIN DISEASE; CHEMICALLY INDUCED; COGNITION; COMPLICATION; CONTROLLED STUDY; DIAGNOSTIC IMAGING; FEMALE; FOOD; HUMAN; HYPERGLYCEMIA; INTRAVENOUS DRUG ADMINISTRATION; MALE; NUCLEAR MAGNETIC RESONANCE IMAGING; OBESITY; PATHOPHYSIOLOGY; PHOTOSTIMULATION; PHYSIOLOGY; PSYCHOLOGY; RANDOMIZED CONTROLLED TRIAL; YOUNG ADULT;

ADMINISTRATION, INTRAVENOUS; ADULT; BRAIN; BRAIN DISEASES; COGNITION; CUES; FEMALE; FOOD; GLUCOSE; HUMANS; HYPERGLYCEMIA; MAGNETIC RESONANCE IMAGING; MALE; OBESITY; PHOTIC STIMULATION; YOUNG ADULT;

EID: 85053536347     PISSN: 01931849     EISSN: 15221555     Source Type: Journal    
DOI: 10.1152/AJPENDO.00335.2017     Document Type: Article

References (41)

1. American Diabetes Association.
2. Classification and diagnosis of diabetes. Diabetes Care 40, Suppl 1: S11-S24, 2017. doi:10.2337/dc17-S005.
3. Anthony K, Reed LJ, Dunn JT, Bingham E, Hopkins D, Marsden PK, Amiel SA. Attenuation of insulin-evoked responses in brain networks controlling appetite and reward in insulin resistance: the cerebral basis for impaired control of food intake in metabolic syndrome? Diabetes 55: 2986-2992, 2006. doi:10.2337/db06-0376.
4. Belfort-DeAguiar R, Seo D, Naik S, Hwang J, Lacadie C, Schmidt C, Constable RT, Sinha R, Sherwin R. Food image-induced brain activation is not diminished by insulin infusion. Int J Obes 40: 1679-1686, 2016. doi:10.1038/ijo.2016.152.
5. Biswal B, Yetkin FZ, Haughton VM, Hyde JS. Functional connectivity in the motor cortex of resting human brain using echo-planar MRI. Mag Reson Med 34: 537-541, 1995. doi:10.1002/mrm.1910340409.
6. Campfield LA, Smith FJ, Rosenbaum M, Hirsch J. Human eating: evidence for a physiological basis using a modified paradigm. Neurosci Biobehav Rev 20: 133-137, 1996. doi:10.1016/0149-7634(95)00043-E.
7. Carnell S, Gibson C, Benson L, Ochner CN, Geliebter A. Neuroimaging and obesity: current knowledge and future directions. Obes Rev 13: 43-56, 2012. doi:10.1111/j.1467-789X.2011.00927.x.
8. Centers for Disease Control and Prevention. Adult Obesity Causes & Consequences (Online). https://www.cdc.gov/obesity/adult/causes.html.
9. Cohen DA. Obesity and the built environment: changes in environmental cues cause energy imbalances. Int J Obes 32, Suppl 7: S137-S142, 2008. doi:10.1038/ijo.2008.250.
10. Connolly L, Coveleskie K, Kilpatrick LA, Labus JS, Ebrat B, Stains J, Jiang Z, Tillisch K, Raybould HE, Mayer EA. Differences in brain responses between lean and obese women to a sweetened drink. Neurogastroenterol Motil 25: 579-e460, 2013. doi:10.1111/nmo.12125.
11. Dale AM. Optimal experimental design for event-related fMRI. Hum Brain Mapp 8: 109-114, 1999. doi:10.1002/(SICI)1097-0193(1999)8:2/ 3_109::AID-HBM7_3.0.CO;2-W.
12. DeFronzo RA, Tobin JD, Andres R. Glucose clamp technique: a method for quantifying insulin secretion and resistance. Am J Physiol Endocrinol Metab 237: E214-E223, 1979. doi:10.1152/ajpendo.1979.237.3.E214.
13. De Silva A, Salem V, Matthews PM, Dhillo WS. The use of functional MRI to study appetite control in the CNS. Exp Diabetes Res 2012: 764017, 2012. doi:10.1155/2012/764017.
14. 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 58: 303-312, 2012. doi:10.1016/j.appet.2011.10.014.
15. Dunn-Meynell AA, Sanders NM, Compton D, Becker TC, Eiki J, Zhang BB, Levin BE. Relationship among brain and blood glucose levels and spontaneous and glucoprivic feeding. J Neurosci 29: 7015-7022, 2009. doi:10.1523/JNEUROSCI.0334-09.2009.
16. Eklund A, Nichols TE, Knutsson H. Cluster failure: why fMRI inferences for spatial extent have inflated false-positive rates. Proc Natl Acad Sci USA 113: 7900-7905, 2016. [Erratum in Proc Natl Acad Sci USA 113: E4929, 2016. doi:10.1073/pnas.1612033113.] doi:10.1073/pnas.1602413113.
17. Freckmann G, Hagenlocher S, Baumstark A, Jendrike N, Gillen RC, Rössner K, Haug C. Continuous glucose profiles in healthy subjects under everyday life conditions and after different meals. J Diabetes Sci Technol 1: 695-703, 2007. doi:10.1177/193229680700100513.
18. Gao Q, Horvath TL. Neurobiology of feeding and energy expenditure. Annu Rev Neurosci 30: 367-398, 2007. doi:10.1146/annurev.neuro.30. 051606.094324.
19. Haruno M, Kawato M. Different neural correlates of reward expectation and reward expectation error in the putamen and caudate nucleus during stimulus-action-reward association learning. J Neurophysiol 95: 948-959, 2006. doi:10.1152/jn.00382.2005.
20. Heni M, Kullmann S, Ketterer C, Guthoff M, Bayer M, Staiger H, Machicao F, Häring HU, Preissl H, Veit R, Fritsche A. Differential effect of glucose ingestion on the neural processing of food stimuli in lean and overweight adults. Hum Brain Mapp 35: 918-928, 2014. doi:10.1002/ hbm.22223.
21. Hwang JJ, Jiang L, Hamza M, Sanchez Rangel E, Dai F, Belfort- DeAguiar R, Parikh L, Koo BB, Rothman DL, Mason G, Sherwin RS. Blunted rise in brain glucose levels during hyperglycemia in adults with obesity and T2DM. JCI Insight 2: 95913, 2017. doi:10.1172/jci.insight.95913.
22. Jais A, Solas M, Backes H, Chaurasia B, Kleinridders A, Theurich S, Mauer J, Steculorum SM, Hampel B, Goldau J, Alber J, Förster CY, Eming SA, Schwaninger M, Ferrara N, Karsenty G, Brüning JC. Myeloid-cell-derived VEGF maintains brain glucose uptake and limits cognitive impairment in obesity. Cell 165: 882-895, 2016. [Erratum in Cell 166: 1338-1340, 2016. doi:10.1016/j.cell.2016.08.010.] doi:10.1016/ j.cell.2016.03.033.
23. Janowitz HD, Ivy AC. Role of blood sugar levels in spontaneous and insulin-induced hunger in man. J Appl Physiol 1: 643-645, 1949. doi:10. 1152/jappl.1949.1.9.643.
24. Kyle UG, Zhang FF, Morabia A, Pichard C. Longitudinal study of body composition changes associated with weight change and physical activity. Nutrition 22: 1103-1111, 2006. doi:10.1016/j.nut.2006.08.003.
25. Lennerz BS, Alsop DC, Holsen LM, Stern E, Rojas R, Ebbeling CB, Goldstein JM, Ludwig DS. Effects of dietary glycemic index on brain regions related to reward and craving in men. Am J Clin Nutr 98: 641-647, 2013. doi:10.3945/ajcn.113.064113.
26. Louis-Sylvestre J, Le Magnen J. Fall in blood glucose level precedes meal onset in free-feeding rats. Neurosci Biobehav Rev 4, Suppl 1: 13-15, 1980. doi:10.1016/0149-7634(80)90041-X.
27. Ludwig DS, Majzoub JA, Al-Zahrani A, Dallal GE, Blanco I, Roberts SB. High glycemic index foods, overeating, and obesity. Pediatrics 103: E26, 1999. doi:10.1542/peds.103.3.e26.
28. Martin LE, Holsen LM, Chambers RJ, Bruce AS, Brooks WM, Zarcone JR, Butler MG, Savage CR. Neural mechanisms associated with food motivation in obese and healthy weight adults. Obesity (Silver Spring) 18: 254-260, 2010. doi:10.1038/oby.2009.220.
29. Matsuda M, Liu Y, Mahankali S, Pu Y, Mahankali A, Wang J, DeFronzo RA, Fox PT, Gao JH. Altered hypothalamic function in response to glucose ingestion in obese humans. Diabetes 48: 1801-1806, 1999. doi:10.2337/diabetes.48.9.1801.
30. Mayer J. Glucostatic mechanism of regulation of food intake. N Engl J Med 249: 13-16, 1953. doi:10.1056/NEJM195307022490104.
31. Morton GJ, Meek TH, Schwartz MW. Neurobiology of food intake in health and disease. Nat Rev Neurosci 15: 367-378, 2014. doi:10.1038/ nrn3745.
32. Musen G, Simonson DC, Bolo NR, Driscoll A, Weinger K, Raji A, Théberge J, Renshaw PF, Jacobson AM. Regional brain activation during hypoglycemia in type 1 diabetes. J Clin Endocrinol Metab 93: 1450-1457, 2008. doi:10.1210/jc.2007-2007.
33. Page KA, Chan O, Arora J, Belfort-Deaguiar R, Dzuira J, Roehmholdt B, Cline GW, Naik S, Sinha R, Constable RT, Sherwin RS. Effects of fructose vs glucose on regional cerebral blood flow in brain regions involved with appetite and reward pathways. JAMA 309: 63-70, 2013. doi:10.1001/jama.2012.116975.
34. Page KA, Seo D, Belfort-DeAguiar R, Lacadie C, Dzuira J, Naik S, Amarnath S, Constable RT, Sherwin RS, Sinha R. Circulating glucose levels modulate neural control of desire for high-calorie foods in humans. J Clin Invest 121: 4161-4169, 2011. doi:10.1172/JCI57873.
35. Pursey KM, Stanwell P, Callister RJ, Brain K, Collins CE, Burrows TL. Neural responses to visual food cues according to weight status: a systematic review of functional magnetic resonance imaging studies. Front Nutr 1: 7, 2014. doi:10.3389/fnut.2014.00007.
36. Rodin J, Wack J, Ferrannini E, DeFronzo RA. Effect of insulin and glucose on feeding behavior. Metabolism 34: 826-831, 1985. doi:10. 1016/0026-0495(85)90106-4.
37. Scharmüller W, Übel S, Ebner F, Schienle A. Appetite regulation during food cue exposure: a comparison of normal-weight and obese women. Neurosci Lett 518: 106-110, 2012. doi:10.1016/j.neulet.2012.04.063.
38. Schultes B, Panknin AK, Hallschmid M, Jauch-Chara K, Wilms B, de Courbière F, Lehnert H, Schmid SM. Glycemic increase induced by intravenous glucose infusion fails to affect hunger, appetite, or satiety following breakfast in healthy men. Appetite 105: 562-566, 2016. doi:10. 1016/j.appet.2016.06.032.
39. Schwartz MW, Porte D Jr. Diabetes, obesity, and the brain. Science 307: 375-379, 2005. doi:10.1126/science.1104344.
40. Schwartz MW, Woods SC, Porte D Jr, Seeley RJ, Baskin DG. Central nervous system control of food intake. Nature 404: 661-671, 2000. doi:10.1038/35007534.
41. Smeets PA, Vidarsdottir S, de Graaf C, Stafleu A, van Osch MJ, Viergever MA, Pijl H, van der Grond J. Oral glucose intake inhibits hypothalamic neuronal activity more effectively than glucose infusion. Am J Physiol Endocrinol Metab 293: E754-E758, 2007. doi:10.1152/ajpendo. 00231.2007.