The use of functional MRI to study the endocrinology of appetite

European Journal of Endocrinology

Volumn 173, Issue 2, 2015, Pages R59-R68

  Salem, Victoria ^a   Dhillo, Waljit S ^a  

^a HAMMERSMITH HOSPITAL   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CHOLECYSTOKININ; DOPAMINE RECEPTOR BLOCKING AGENT; GLUCAGON LIKE PEPTIDE 1 [7-36] AMIDE; LEPTIN; PEPTIDE YY [3-36]; GASTROINTESTINAL HORMONE;

ADIPOSE TISSUE; AMYGDALOID NUCLEUS; ANTERIOR CINGULATE; APPETITE; BODY MASS; BOLD SIGNAL; BRAIN BLOOD FLOW; CALORIC INTAKE; CAUDATE NUCLEUS; DIET RESTRICTION; DOPAMINE RELEASE; DOPAMINERGIC TRANSMISSION; DOWN REGULATION; EMOTION; ENERGY BALANCE; ENERGY EXPENDITURE; EXECUTIVE FUNCTION; FOLLOW UP; FOOD INTAKE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; GLOBUS PALLIDUS; HEMODYNAMICS; HIPPOCAMPUS; HUMAN; HYPERPHAGIA; HYPOTHALAMUS; INSULA; LEARNING; MEMORY; MESENCEPHALON; NONHUMAN; NUCLEUS ACCUMBENS; NUTRITIONAL STATUS; OBESITY; ORBITAL CORTEX; OVERNUTRITION; POSITRON EMISSION TOMOGRAPHY; POSTERIOR CINGULATE; POSTOPERATIVE PERIOD; PREFRONTAL CORTEX; PRIMARY MOTOR CORTEX; PRIORITY JOURNAL; PUTAMEN; REPRODUCIBILITY; REVIEW; REWARD; RISK FACTOR; ROUX Y ANASTOMOSIS; SATIETY; SELF MEDICATION; SIGNAL TRANSDUCTION; VENTRAL STRIATUM; VENTROMEDIAL PREFRONTAL CORTEX; WEIGHT GAIN; WEIGHT REDUCTION; WITHDRAWAL SYNDROME; ANIMAL; BRAIN; ENDOCRINOLOGY; ENERGY METABOLISM; FEEDING BEHAVIOR; METABOLISM; NUCLEAR MAGNETIC RESONANCE IMAGING; PHYSIOLOGY; PROCEDURES; UTILIZATION;

ANIMALS; APPETITE; APPETITE REGULATION; BRAIN; ENDOCRINOLOGY; ENERGY METABOLISM; FEEDING BEHAVIOR; GASTROINTESTINAL HORMONES; HUMANS; MAGNETIC RESONANCE IMAGING;

EID: 84938869868     PISSN: 08044643     EISSN: 1479683X     Source Type: Journal    
DOI: 10.1530/EJE-14-0716     Document Type: Review

References (72)

1. Dombrowski SU, Knittle K, Avenell A, Araújo-Soares V & Sniehotta FF. Long term maintenance of weight loss with non-surgical interventions in obese adults: systematic review and meta-analyses of randomised controlled trials. British Medical Journal 2014 348 g2646. (doi:10.1136/bmj.g2646)
2. Salem V & Bloom SR. Approaches to the pharmacological treatment of obesity. Expert Review of Clinical Pharmacology 2010 3 73-88. (doi:10.1586/ecp.09.54)
3. Chaudhri OB, Salem V, Murphy KG & Bloom SR. Gastrointestinal satiety signals. Annual Review of Physiology 2008 70 239-255. (doi:10.1146/annurev.physiol.70.113006.100506)
4. Berthoud HR. The neurobiology of food intake in an obesogenic environment. Proceedings of the Nutrition Society 2012 71 478-487. (doi:10.1017/S0029665112000602)
5. Farooqi IS & O'Rahilly S. 20 years of leptin: human disorders of leptin action. Journal of Endocrinology 2014 223 T63-T70. (doi:10.1530/JOE-14-0480)
6. Berthoud HR. Homeostatic and non-homeostatic pathways involved in the control of food intake and energy balance. Obesity 2006 14 197S-200S. (doi:10.1038/oby.2006.308)
7. Kanoski SE. Cognitive and neuronal systems underlying obesity. Physiology &Behavior2012 106 337-344. (doi:10.1016/j.physbeh.2012.01.007)
8. O'Doherty JP, Deichmann R, Critchley HD & Dolan RJ. Neural responses during anticipation of a primary taste reward. Neuron 2002 33 815-826. (doi:10.1016/S0896-6273(02)00603-7)
9. Stice E, Spoor S, Bohon C, Veldhuizen M & Small D. Relation of reward from food intake and anticipated food intake to obesity: a functional magnetic resonance imaging study. Journal of Abnormal Psychology 2008 117 924-935. (doi:10.1037/a0013600)
10. van den Bos R & de Ridder D. Evolved to satisfy our immediate needs: self-control and the rewarding properties of food. Appetite 2006 47 24-29. (doi:10.1016/j.appet.2006.02.008)
11. Salamone J & Correa M. Dopamine and food addiction: lexicon badly needed. Biological Psychiatry 2013 73 e15-e24. (doi:10.1016/j.biopsych. 2012.09.027)
12. Castro DC & Berridge KC. Advances in the neurobiological bases for food 'liking' and 'wanting'. Physiology & Behavior 2014 136 22-30. (doi:10.1016/j.physbeh.2014.05.022)
13. Robinson TE & Berridge KC. Incentive-sensitization and addiction. Addiction 2001 96 103-114. (doi:10.1046/j.1360-0443.2001.9611038.x)
14. Bryant EJ, King NA & Blundell JE. Disinhibition: its effect on appetite and weight regulation. Obesity Reviews 2008 9 409-419. (doi:10.1111/j.1467-789X.2007.00426.x)
15. Berthoud HR & Morrison C. The brain, appetite and obesity. Annual Review of Psychology 2008 59 55-92. (doi:10.1146/annurev.psych.59. 103006.093551)
16. Shin AC, Zheng H & Berthoud HR. An expanded view of energy homeostasis: neural integration of metabolic, cognitive, and emotional drives to eat. Physiology & Behavior 2009 97 572-580. (doi:10.1016/j. physbeh.2009.02.010)
17. Schur EA, Kleinhans NM, Goldberg J, Buchwald D, Schwartz MW &Maravilla K. Activation in brain energy regulation and reward centers by food cues varies with choice of visual stimulus. International Journal of Obesity 2009 33 653-661. (doi:10.1038/ijo.2009.56)
18. Kanoski SE & Davidson TL. Western diet consumption and cognitive impairment: links to hippocampal dysfunction and obesity. Physiology & Behavior 2011 103 59-68. (doi:10.1016/j.physbeh.2010.12.003)
19. Fulton S. Neurosystems linking corticolimbic and hypothalamic pathways in energy balance: view from the Chair. International Journal of Obesity 2009 33 S3-S7. (doi:10.1038/ijo.2009.64)
20. Ogawa S, Tank DW, Menon R, Ellerman JM, Kim SG, Merkle H &Ugurbil K. Intrinsic signal changes accompanying sensory stimulation: functional brain mapping with magnetic resonance imaging. PNAS 1992 89 5951-5955. (doi:10.1073/pnas.89.13.5951)
21. Detre JA & Wang J. Technical aspects and utility of fMRI using BOLD and ASL. Clinical Neurophysiology 2002 113 621-634. (doi:10.1016/ S1388-2457(02)00038-X)
22. Beaver JD, Lawrence AD, van Ditzhuijzen J, Davis MH, Woods A &Calder AJ. Individual differences in reward drive predict neural responses to images of food. Journal of Neuroscience 2006 26 5160-5166. (doi:10.1523/JNEUROSCI.0350-06.2006)
23. White MA, Whisenhunt BL, Williamson DA, Greenway FL &Netemeyer RG. Development and validation of the food-craving inventory. Obesity Research 2002 10 107-114. (doi:10.1038/oby.2002.17)
24. van der Laan LN, De Ridder DT, Viergever MA & Smeets PA. The first taste is always with the eyes: a meta-analysis on the neural correlates of processing visual food cues. NeuroImage 2011 55 296-303. (doi:10. 1016/j.neuroimage.2010.11.055)
25. Blechert J, Meule A, Busch NA & Ohla K. Food-pics: an image database for experimental research on eaing and appetite. Frontiers in Psychology 2014 5 617. (doi:10.3389/fpsyg.2014.00617)
26. Jastreboff A, Sinha R, Lacadie C, Small DM, Sherwisn RS & Potenza MN. Neural correlates of stress- and food cue-induced food craving in obesity: association with insulin levels. Diabetes Care 2013 36 395-492. (doi:10.2337/dc12-1112)
27. LaBar KS, Gitelman DR, Parrish TB, Kim YH, Nobre AC & Mesulam MM. Hunger selectively modulates corticolimbic activation to food stimuli in humans. Behavioral Neuroscience 2001 115 493-500. (doi:10.1037/ 0735-7044.115.2.493)
28. Killgore WD, Young AD, Femia LA, Bogorodzki P, Rogowska J &Yurgelun-Todd DA. Cortical and limbic activation during viewing of high- versus low-calorie foods. NeuroImage 2003 19 1381-1394. (doi:10.1016/S1053-8119(03)00191-5)
29. Fuhrer D, Zysset S & Stumvoll M. Brain activity in hunger and satiety: an exploratory visually stimulated FMRI study. Obesity 2008 16 945-950. (doi:10.1038/oby.2008.33)
30. Siep N, Roefs A, Roebroeck A, Havermans R, Bonte ML & Jansen A. 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. Behavioral Brain Research 2009 198 149-158. (doi:10.1016/j.bbr.2008.10.035)
31. Goldstone AP, Prechtl de Hernandex CG, Beaver JD, Muhammed K, Croese C, Bell G, Durighel G, Hughes E, Waldman AD, Frost G et al. Fasting biases brain reward systems towards high-calorie foods. European Journal of Neuroscience 2009 30 1625-1635. (doi:10.1111/j.1460-9568.2009.06949.x)
32. Stice E, Burger K & Yokum S. Caloric deprivation increases responsivity of attention and reward brain regions to intake, anticipated intake, and images of palatable foods. Addiction Biology 2013 18 855-862. (doi:10.1111/j.1369-1600.2012.00489.x)
33. Pelchat ML, Johnson A, Chan R, Valdez J & Ragland JD. Images of desire: food-craving activation during fMRI. NeuroImage 2004 23 1486-1493. (doi:10.1016/j.neuroimage.2004.08.023)
34. DelParigi A, Chen K, Salbe AD, Reiman EM & Tataranni PA. Sensory experience of food and obesity: a positron emission tomography study of the brain regions affected by tasting a liquid meal after a prolonged fast. NeuroImage 2005 24 436-443. (doi:10.1016/j.neuroimage.2004.08.035)
35. DelParigi A, Chen K, Salbe AD, Hill JO, Wing RR, Reiman EM &Tataranni PA. Persistence of abnormal neural responses to a meal in postobese individuals. International Journal of Obesity and Related Metabolic Disorders 2004 28 370-377. (doi:10.1038/sj.ijo.0802558)
36. Rothemund Y, Preuschhof C, Bohner G, Bauknecht CH, Klingebiel R, Flor H & Klapp BF. Differential activation of the dorsal striatum by highcalorie visual food stimuli in obese individuals. NeuroImage 2007 37 410-421. (doi:10.1016/j.neuroimage.2007.05.008)
37. Stoeckel LE, Weller RE, Cook EW, Twieg DB, Knowlton RC & Cox JE. Widespread reward-system activation in obese women in response to pictures of high-calorie foods. NeuroImage 2008 41 636-647. (doi:10.1016/j.neuroimage.2008.02.031)
38. Scharmuller W, Ubel S, Ebner F & Schienle A. Appetite regulation during food cue exposure: a comparison of normal-weight and obese women. Neuroscience Letters 2012 518 106-110. (doi:10.1016/j.neulet. 2012.04.063)
39. Burger KS & Stice E. Greater striatopallidal adaptive coding during cuereward learning and food reward habituation predict future weight gain. NeuroImage 2014 99 122-128. (doi:10.1016/j.neuroimage.2014.05.066)
40. Killgore WD, Weber M, Schwab ZJ, Kipman M, DelDonno SR, Webb CA & Rauch SL. Cortico-limbic responsiveness to high-calorie food images predicts weight status among women. International Journal of Obesity 2013 37 1435-1442. (doi:10.1038/ijo.2013.26)
41. Cornier MA, Shott ME, Thomas EA, Bechtell JL, Bessesen DH, Tregellas JR & Frank GK. The effects of energy balance, obesity-proneness and sex on the neuronal response to sweet taste. Behavioural Brain research 2014 278 446-452. (doi:10.1016/j.bbr.2014.10.024)
42. Brooks SJ, Cedernaes J & Schiöth HB. Increased prefrontal and parahippocampal activation with reduced dorsolateral prefrontal and insular cortex activation to food images in obesity: a meta-analysis of fMRI studies. PLoS ONE 2013 8 e60393. (doi:10.1371/journal.pone. 0060393)
43. Le DS, Pannacciulli N, Chen K, Salbe AD, Del Parigi A, Hill JO, Wing RR, Reiman EM & Krakoff J. Less activation in the left dorsolateral prefrontal cortex in the reanalysis of the response to a meal in obese than in lean women and its association with successful weight loss. American Journal of Clinical Nutrition 2007 86 573-579.
44. Stice E, Spoor S, Bohon C & Small DM. Relation between obesity and blunted striatal response to food is moderated by TaqIA A1 allele. Science 2008 322 449-452. (doi:10.1126/science.1161550)
45. Volkow ND, Wang GJ, Maynard L, Jayne M, Fowler JS, Zhu W, Logan J, Gatley SJ, Ding YS, Wong C et al. Brain dopamine is associated with eating behavior in humans. International Journal of Eating Disorders 2003 33 136-142. (doi:10.1002/eat.10118)
46. Small DM, Jones-Gotman M & Dagher A. Feeding-induced dopamine release in dorsal striatum correlates with meal pleasantness ratings in healthy human volunteers. NeuroImage 2003 19 1709-1715. (doi:10.1016/S1053-8119(03)00253-2)
47. Blum K, Braverman ER, Holder JM, Lubar JF, Monastra VJ, Miller D, Lubar JO, Chen TJ & Comings DE. Reward deficiency syndrome: a biogenetic model for the diagnosis and treatment of impulsive, addictive, and compulsive behaviors. Journal of Psychoactive Drugs 2000 32 (Suppl i-iv) 1-112.
48. Wang GJ, Volkow ND, Logan J, Pappas NR, Wong C, Zhu W, Netsuil N & Fowler NS. Brain dopamine and obesity. Lancet 2001 357 354-357. (doi:10.1016/S0140-6736(00)03643-6)
49. Volkow ND, Wang GJ, Telang F, Fowler JS, Thanos PK, Logan J, Alexoff D, Ding YS, Wong C, Ma Y et al. Low dopamine striatal D2 receptors are associated with prefrontal metabolism in obese subjects: possible contributing factors. NeuroImage 2008 42 1537-1543. (doi:10.1016/j.neuroimage.2008.06.002)
50. Stice E, Yokum S, Blum K & Bohon C. Weight gain is associated with reduced striatal response to palatable food. Journal of Neuroscience 2010 30 13105-13109. (doi:10.1523/JNEUROSCI.2105-10.2010)
51. Davis C, Strachan S & Berkson M. Sensitivity to reward: implications for overeating and obesity. Appetite 2004 42 131-138. (doi:10.1016/ j.appet.2003.07.004)
52. Stice E, Yokum S, Zald D & Dagher A. Dopamine-based reward circuitry responsivity, genetics, and overeating. Current Topics in Behavioral Neurosciences 2011 6 81-93. (doi:10.1007/7854-2010-89)
53. Ziauddeen H & Fletcher PC. Is food addiction a valid and useful concept? Obesity Reviews 2013 14 19-28. (doi:10.1111/j.1467-789X. 2012.01046.x)
54. Farooqi IS, Jebb SA, Langmack G, Lawrence E, Cheetham CH, Prentice AM, Hughes IA, McCamish MA & O'Rahilly S. Effects of recombinant leptin therapy in a child with congenital leptin deficiency. New England Journal of Medicine 1999 341 879-884. (doi:10.1056/NEJM199909163411204)
55. Farooqi IS, Bullmore E, Keogh J, Gillard J, O'Rahilly S & Fletcher PC. Leptin regulates striatal regions and human eating behavior. Science 2007 317 1355. (doi:10.1126/science.1144599)
56. Grosshans M, Vollmert C, Vollstadt-Klein S, Tost H, Leber S, Bach P, Buhler M, Von Der Goltz C, Mutschler J, Loeber S et al. Association of leptin with food cue-induced activation in human reward pathways. Archives of General Psychiatry 2012 69 529-537. (doi:10.1001/archgenpsychiatry.2011.1586)
57. Batterham RL, Ffytche DH, Rosenthal JM, Zelaya FO, Barker GJ, Withers DJ & Williams SC. PYY modulation of cortical and hypothalamic brain areas predicts feeding behaviour in humans. Nature 2007 450 106-109. (doi:10.1038/nature06212)
58. De Silva A, Salem V, Long CJ, Makwana A, Newbould RD, Rabiner EA, Ghatei MA, Bloom SR, Matthews PM, Beaver JD et al. The gut hormones PYY 3-36 and GLP-1 7-36 amide reduce food intake and modulate brain activity in appetite centers in humans. Cell Metabolism 2011 14 700-706. (doi:10.1016/j.cmet.2011.09.010)
59. Malik S, McGlone F, Bedrossian D & Dagher A. Ghrelin modulates brain activity in areas that control appetitive behavior. Cell Metabolism 2008 7 400-409. (doi:10.1016/j.cmet.2008.03.007)
60. Goldstone AP, Prechtl CG, Scholtz S, Miras AD, Chhina N, Durighel G, Deliran SS, Beckmann C, Ghatei MA, Ashby DR et al. Ghrelin mimics fasting to enhance human hedonic, orbitofrontal cortex, and hippocampal responses to food. American Journal of Clinical Nutrition 2014 99 1319-1330. (doi:10.3945/ajcn.113.075291)
61. Van Oudenhove L, McKie S, Lassman D, Uddin B, Paine P, Coen S, Gregory L, Tack J & Aziz Q. Fatty acid-induced gut-brain signaling attenuates neural and behavioral effects of sad emotion in humans. Journal of Clinical Investigation 2011 121 3094-3099. (doi:10.1172/ JCI46380)
62. Kroemer NB, Krebs L, Kobiella A, Grimm O, Pilhatsch M, Bidlingmaier M, Zimmermann US & Smolka MN. Fasting levels of ghrelin covary with the brain response to food pictures. Addiction Biology 2013 18 855-862. (doi:10.1111/j.1369-1600.2012.00489.x)
63. Li J, An R, Zhang Y, Li X & Wang S. Correlations of macronutrient-induced functional magnetic resonance imaging signal changes in human brain and gut hormone responses. American Journal of Clinical Nutrition 2012 96 275-282. (doi:10.3945/ajcn.112.037440)
64. van Bloemendaal L, IJzerman RG, Ten Kulve JS, Barkhof F, Konrad RJ, Drent ML, Veltman DJ & Diamant M. GLP-1 receptor activation modulates appetite- and reward-related brain areas in humans. Diabetes 2014 63 4186-4196. (doi:10.2337/db14-0849)
65. Akkary E. Bariatric surgery evolution from the malabsorptive to the hormonal era. Obesity Surgery 2012 22 827-831. (doi:10.1007/s11695- 012-0623-2)
66. Bueter M, Miras AD, Chichger H, Fenske W, Ghatei MA, Bloom SR, Unwin RJ, Lutz TA, Spector AC & le Roux CW. Alterations of sucrose preference after Roux-en-Y gastric bypass. Physiology & Behavior 2011 104 709-721. (doi:10.1016/j.physbeh.2011.07.025)
67. van de Sande-Lee S, Pereira FR, Cintra DE, Fernandes PT, Cardoso AR, Garlipp CR, Chaim EA, Pareja JC, Geloneze B, Li LM et al. Partial reversibility of hypothalamic dysfunction and changes in brain activity after body mass reduction in obese subjects. Diabetes 2011 60 1699-1704. (doi:10.2337/db10-1614)
68. Ochner CN, Kwok Y, Conceicao E, Pantazatos SP, Puma LM, Carnell S, Teixera J, Hirsch J & Geliebter A. Selective reduction in neural responses to high calorie foods following gastric bypass surgery. Annals of Surgery 2011 253 502-507. (doi:10.1097/SLA.0b013e318203a289)
69. Ochner CN, Stice E, Hutchins E, Afifi L, Geliebter A, Hirsch J & Teixera J. Relation between changes in neural responsivity and reductions in desire to eat high-calorie foods following gastric bypass surgery. Neuroscience 2012 209 128-135. (doi:10.1016/j.neuroscience.2012.02.030)
70. Bruce AS, Bruce JM, Ness AR, Lepping RJ, Malley S, Hancock L, Powell J, Patrician TM, Breslin FJ, Martin LE et al. A comparison of functional brain changes associated with surgical versus behavioral weight loss. Obesity 2014 22 337-343. (doi:10.1002/oby.20630)
71. Dunn JP, Cowan RL, Volkow ND, Feurer ID, Li R, Williams DB, Kessler RM & Abumrad NN. Decreased dopamine type 2 receptor availability after bariatric surgery: preliminary findings. Brain Research 2010 2 123-130. (doi:10.1016/j.brainres.2010.03.064)
72. Scholtz S, Miras AD, Chhina N, Prechtl CG, Sleeth ML, Daud NM, Ismail NA, Durighel G, Ahmed AR, Olbers T et al. Obese patients after gastric bypass surgery have lower brain-hedonic responses to food than after gastric banding. Gut 2014 63 891-902. (doi:10.1136/gutjnl-2013-305008)