Obesity is marked by distinct functional connectivity in brain networks involved in food reward and salience

Behavioural Brain Research

Volumn 287, Issue , 2015, Pages 127-134

  Wijngaarden, M A ^a   Veer, I M ^b,c   Rombouts, S A R B ^a,b   van Buchem, M A ^a,b   Willems van Dijk, K ^a   Pijl, H ^a   van der Grond, J ^a  

^a LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

^b LEIDEN UNIVERSITY   (Netherlands)

^c CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

Author keywords

Amygdala; Default mode network; Fasting; Functional MRI; Hypothalamus; Obesity

Indexed keywords

ADULT; AMYGDALOID NUCLEUS; ANTERIOR CINGULATE; ARTICLE; BRAIN FUNCTION; CLINICAL ARTICLE; CONNECTOME; CONTROLLED STUDY; DEFAULT MODE NETWORK; FEMALE; FUNCTIONAL CONNECTIVITY; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HUMAN; HYPOTHALAMUS; INSULA; MALE; OBESITY; POSTERIOR CINGULATE; PREFRONTAL CORTEX; PRIORITY JOURNAL; RESTING STATE NETWORK; REWARD; BRAIN; BRAIN MAPPING; DIET RESTRICTION; FOOD; NERVE TRACT; NUCLEAR MAGNETIC RESONANCE IMAGING; PATHOPHYSIOLOGY; PHYSIOLOGY; REST;

ADULT; BRAIN; BRAIN MAPPING; FASTING; FEMALE; FOOD; HUMANS; MAGNETIC RESONANCE IMAGING; MALE; NEURAL PATHWAYS; OBESITY; REST; REWARD;

EID: 84926217996     PISSN: 01664328     EISSN: 18727549     Source Type: Journal    
DOI: 10.1016/j.bbr.2015.03.016     Document Type: Article

References (58)

1. Flegal K.M., Graubard B.I., Williamson D.F., Gail M.H. Cause-specific excess deaths associated with underweight, overweight, and obesity. JAMA 2007, 298(17):2028-2037.
2. World Health Organization Obesity and overweight 2011, World Health Organization, [Fact Sheet No 311].
3. Schwartz M.W., Woods S.C., Porte D., Seeley R.J., Baskin D.G. Central nervous system control of food intake. Nature 2000, 404(6778):661-671.
4. Berthoud H.R. Neural control of appetite: cross-talk between homeostatic and non-homeostatic systems. Appetite 2004, 43(3):315-317.
5. Baskin D.G., Figlewicz L.D., Seeley R.J., Woods S.C., Porte D., Schwartz M.W. Insulin and leptin: dual adiposity signals to the brain for the regulation of food intake and body weight. Brain Res 1999, 848(1-2):114-123.
6. Cornier M.A., Von Kaenel S.S., Bessesen D.H., Tregellas J.R. Effects of overfeeding on the neuronal response to visual food cues. Am J Clin Nutr 2007, 86(4):965-971.
7. Tregellas J.R., Wylie K.P., Rojas D.C., Tanabe J., Martin J., Kronberg E., et al. Altered default network activity in obesity. Obesity (Silver Spring) 2011, 19:2316-2321.
8. Carnell S., Gibson C., Benson L., Ochner C.N., Geliebter A. Neuroimaging and obesity: current knowledge and future directions. Obes Rev 2011, 14(1):19-28.
9. Alkan A., Sahin I., Keskin L., Cikim A.S., Karakas H.M., Sigirci A., et al. Diffusion-weighted imaging features of brain in obesity. Magn Reson Imaging 2008, 26(4):446-450.
10. Del P.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.
11. DelParigi A., Chen K., Salbe A.D., Reiman E.M., Tataranni P.A. 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(2):436-443.
12. Gautier J.F., Chen K., Salbe A.D., Bandy D., Pratley R.E., Heiman M., et al. Differential brain responses to satiation in obese and lean men. Diabetes 2000, 49(5):838-846.
13. Gautier J.F., Del P.A., Chen K., Salbe A.D., Bandy D., Pratley R.E., et al. Effect of satiation on brain activity in obese and lean women. Obes Res 2001, 9(11):676-684.
14. Karhunen L.J., Lappalainen R.I., Vanninen E.J., Kuikka J.T., Uusitupa M.I. Regional cerebral blood flow during food exposure in obese and normal-weight women. Brain 1997, 120(Pt 9):1675-1684.
15. 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(4):924-935.
16. Shin A.C., Zheng H., Berthoud H.R. An expanded view of energy homeostasis: neural integration of metabolic, cognitive, and emotional drives to eat. Physiol Behav 2009, 97(5):572-580.
17. Fox M.D., Raichle M.E. Spontaneous fluctuations in brain activity observed with functional magnetic resonance imaging. Nat Rev Neurosci 2007, 8(9):700-711.
18. Biswal B.B., Mennes M., Zuo X.N., Gohel S., Kelly C., Smith S.M., et al. Toward discovery science of human brain function. Proc Natl Acad Sci U S A 2010, 107(10):4734-4739.
19. Smith S.M., Fox P.T., Miller K.L., Glahn D.C., Fox P.M., Mackay C.E., et al. Correspondence of the brain's functional architecture during activation and rest. Proc Natl Acad Sci U S A 2009, 106(31):13040-13045.
20. Kullmann S., Heni M., Veit R., Ketterer C., Schick F., Haring 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(5):1052-1061.
21. Lips M.A., Wijngaarden M.A., van der Grond J., van Buchem M.A., de Groot G.H., Rombouts S.A., et al. Resting-state functional connectivity of brain regions involved in cognitive control, motivation, and reward is enhanced in obese females. Am J Clin Nutr 2014, 100(2):524-531.
22. Sande-Lee S., Pereira F.R., Cintra D.E., Fernandes P.T., Cardoso A.R., Garlipp C.R., et al. Partial reversibility of hypothalamic dysfunction and changes in brain activity after body mass reduction in obese subjects. Diabetes 2011, 60(6):1699-1704.
23. Thaler J.P., Yi C.X., Schur E.A., Guyenet S.J., Hwang B.H., Dietrich M.O., et al. Obesity is associated with hypothalamic injury in rodents and humans. J Clin Invest 2012, 122(1):153-162.
24. Pessoa L., Adolphs R. Emotion processing and the amygdala: from a 'low road' to 'many roads' of evaluating biological significance. Nat Rev Neurosci 2010, 11(11):773-783.
25. Baxter M.G., Murray E.A. The amygdala and reward. Nat Rev Neurosci 2002, 3(7):563-573.
26. Ahn S., Phillips A.G. Modulation by central and basolateral amygdalar nuclei of dopaminergic correlates of feeding to satiety in the rat nucleus accumbens and medial prefrontal cortex. J Neurosci 2002, 22(24):10958-10965.
27. Loscher W., Brandt C., Ebert U. Excessive weight gain in rats over extended kindling of the basolateral amygdala. Neuroreport 2003, 14(14):1829-1832.
28. Wijngaarden M.A., van der Zon G.C., van Dijk K.W., Pijl H., Guigas B. Effects of prolonged fasting on AMPK signaling, gene expression, and mitochondrial respiratory chain content in skeletal muscle from lean and obese individuals. Am J Physiol Endocrinol Metab 2013, 304(9):E1012-E1021.
29. Smith S.M., Jenkinson M., Woolrich M.W., Beckmann C.F., Behrens T.E., Johansen-Berg H., et al. Advances in functional and structural MR image analysis and implementation as FSL. Neuroimage 2004, 23(Suppl. 1):S208-S219.
30. Woolrich M.W., Jbabdi S., Patenaude B., Chappell M., Makni S., Behrens T., et al. Bayesian analysis of neuroimaging data in FSL. Neuroimage 2009, 45(Suppl. 1):S173-S186.
31. Veer I.M., Oei N.Y., Spinhoven P., van Buchem M.A., Elzinga B.M., Rombouts S.A. Beyond acute social stress: increased functional connectivity between amygdala and cortical midline structures. Neuroimage 2011, 57(4):1534-1541.
32. Fox M.D., Snyder A.Z., Vincent J.L., Corbetta M., Van E., Raichle M.E. The human brain is intrinsically organized into dynamic, anticorrelated functional networks. Proc Natl Acad Sci U S A 2005, 102(27):9673-9678.
33. Worsley K.J., Jezzard P., Matthews P.M., Smith S. Statistical analysis of activation images. Functional magnetic resonance imaging. An introduction to methods 2001, Oxford University Press.
34. Murphy K., Birn R.M., Handwerker D.A., Jones T.B., Bandettini P.A. The impact of global signal regression on resting state correlations: are anti-correlated networks introduced?. Neuroimage 2009, 44(3):893-905.
35. Saad Z.S., Gotts S.J., Murphy K., Chen G., Jo H.J., Martin A., et al. Trouble at rest: how correlation patterns and group differences become distorted after global signal regression. Brain Connect 2012, 2(1):25-32.
36. Rombouts S.A., Barkhof F., Goekoop R., Stam C.J., Scheltens P. Altered resting state networks in mild cognitive impairment and mild Alzheimer's disease: an fMRI study. Hum Brain Mapp 2005, 26(4):231-239.
37. Swanson N., Eichele T., Pearlson G., Kiehl K., Yu Q., Calhoun V.D. Lateral differences in the default mode network in healthy controls and patients with schizophrenia. Hum Brain Mapp 2011, 32(4):654-664.
38. Kullmann S., Heni M., Veit R., Ketterer C., Schick F., Haring H.U., et al. The obese brain: association of body mass index and insulin sensitivity with resting state network functional connectivity. Hum Brain Mapp 2011, 10.
39. Greicius M.D., Krasnow B., Reiss A.L., Menon V. Functional connectivity in the resting brain: a network analysis of the default mode hypothesis. Proc Natl Acad Sci U S A 2003, 100(1):253-258.
40. Raichle M.E., MacLeod A.M., Snyder A.Z., Powers W.J., Gusnard D.A., Shulman G.L. A default mode of brain function. Proc Natl Acad Sci U S A 2001, 98(2):676-682.
41. Kaufmann C., Wehrle R., Wetter T.C., Holsboer F., Auer D.P., Pollmacher T., et al. Brain activation and hypothalamic functional connectivity during human non-rapid eye movement sleep: an EEG/fMRI study. Brain 2006, 129(Pt 3):655-667.
42. Roy A.K., Shehzad Z., Margulies D.S., Kelly A.M., Uddin L.Q., Gotimer K., et al. Functional connectivity of the human amygdala using resting state fMRI. Neuroimage 2009, 45(2):614-626.
43. Peters J., Buchel C. Neural representations of subjective reward value. Behav Brain Res 2010, 213(2):135-141.
44. Lee Y., Chong M.F., Liu J.C., Libedinsky C., Gooley J.J., Chen S., et al. Dietary disinhibition modulates neural valuation of food in the fed and fasted states. Am J Clin Nutr 2013, 97(5):919-925.
45. Sescousse G., Caldu X., Segura B., Dreher J.C. Processing of primary and secondary rewards: a quantitative meta-analysis and review of human functional neuroimaging studies. Neurosci Biobehav Rev 2013, 37(4):681-696.
46. Frank S., Laharnar N., Kullmann S., Veit R., Canova C., Hegner Y.L., et al. Processing of food pictures: influence of hunger, gender and calorie content. Brain Res 2010, 1350:159-166.
47. 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(2):636-647.
48. Eiler W.J., Dzemidzic M., Case K.R., Armstrong C.L., Mattes R.D., Cyders M.A., et al. Ventral frontal satiation-mediated responses to food aromas in obese and normal-weight women. Am J Clin Nutr 2014, 99(6):1309-1318.
49. Berthoud H.R. The vagus nerve, food intake and obesity. Regul Pept 2008, 149(1-3):15-25.
50. Volkow N.D., Wang G.J., Fowler J.S., Tomasi D., Baler R. Food and drug reward: overlapping circuits in human obesity and addiction. Curr Top Behav Neurosci 2011, 11:1-24.
51. Critchley H.D., Wiens S., Rotshtein P., Ohman A., Dolan R.J. Neural systems supporting interoceptive awareness. Nat Neurosci 2004, 7(2):189-195.
52. Menon V., Uddin L.Q. Saliency, switching, attention and control: a network model of insula function. Brain Struct Funct 2010, 214(5-6):655-667.
53. Kullmann S., Pape A.A., Heni M., Ketterer C., Schick F., Haring H.U., et al. Functional network connectivity underlying food processing: disturbed salience and visual processing in overweight and obese adults. Cereb Cortex 2013, 23(5):1247-1256.
54. Garcia-Garcia I., Jurado M.A., Garolera M., Segura B., Sala-Llonch R., Marques-Iturria I., et al. Alterations of the salience network in obesity: a resting-state fMRI study. Hum Brain Mapp 2013, 34(11):2786-2797.
55. Brooks S.J., Cedernaes J., Schioth H.B. 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(4):e60393.
56. Laufs H., Walker M.C., Lund T.E. 'Brain activation and hypothalamic functional connectivity during human non-rapid eye movement sleep: an EEG/fMRI study' - its limitations and an alternative approach. Brain 2007, 130(Pt 7):e75.
57. Fox M.D., Zhang D., Snyder A.Z., Raichle M.E. The global signal and observed anticorrelated resting state brain networks. J Neurophysiol 2009, 101(6):3270-3283.
58. Wijngaarden M.A., Pijl H., van Dijk K.W., Klaassen E.S., Burggraaf J. Obesity is associated with an altered autonomic nervous system response to nutrient restriction. Clin Endocrinol (Oxf) 2013, 79(5):648-651.