A Perspective on Candidate Neural Underpinnings of Binge Eating Disorder: Reward and Homeostatic Systems

Author(s): Amelia Romei, Katharina Voigt, Antonio Verdejo-Garcia*

Journal Name: Current Pharmaceutical Design

Volume 26 , Issue 20 , 2020


Become EABM
Become Reviewer
Call for Editor

Abstract:

People with Binge Eating Disorder (BED) exhibit heightened sensitivity to rewarding stimuli and elevated activity in reward-related brain regions, including the orbitofrontal cortex (OFC), ventral striatum (VS) and insula, during food-cue exposure. BED has also been associated with altered patterns of functional connectivity during resting-state. Investigating neural connectivity in the absence of task stimuli provides knowledge about baseline communication patterns that may influence the behavioural and cognitive manifestation of BED. Elevated resting-state functional connectivity (rsFC) between reward-related brain regions may contribute to uncontrolled eating bouts observed in BED, through heightened food-cue sensitivity and food-craving. The impact of homeostatic state on rsFC of the reward system has not yet been investigated in people with BED. Homeostatic dysfunction is a key driver of excessive food consumption in obesity, whereby rsFC between rewardrelated brain regions does not attenuate during satiety. Future studies should investigate BED related differences in rsFC within the reward system during hunger and satiety, in order to determine whether individuals with BED display an abnormal neural response to changes in homeostatic state. This knowledge would further enhance current understandings of the mechanisms contributing to BED, potentially implicating both reward and homeostatic dysfunctions as drivers of BED.

Keywords: Binge eating disorder, resting-state functional magnetic resonance imaging, functional magnetic resonance imaging, reward, hunger, feeding behaviour.

[1]
Kober H, Boswell RG. Potential psychological & neural mechanisms in binge eating disorder: Implications for treatment. Clin Psychol Rev 2018; 60: 32-44.
[http://dx.doi.org/10.1016/j.cpr.2017.12.004] [PMID: 29329692]
[2]
Balodis IM, Kober H, Worhunsky PD, et al. Monetary reward processing in obese individuals with and without binge eating disorder. Biol Psychiatry 2013; 73(9): 877-86.
[http://dx.doi.org/10.1016/j.biopsych.2013.01.014] [PMID: 23462319]
[3]
Simon JJ, Skunde M, Walther S, Bendszus M, Herzog W, Friederich HC. Neural signature of food reward processing in bulimic-type eating disorders. Soc Cogn Affect Neurosci 2016; 11(9): 1393-401.
[http://dx.doi.org/10.1093/scan/nsw049] [PMID: 27056455]
[4]
Weygandt M, Schaefer A, Schienle A, Haynes JD. Diagnosing different binge-eating disorders based on reward-related brain activation patterns. Hum Brain Mapp 2012; 33(9): 2135-46.
[http://dx.doi.org/10.1002/hbm.21345] [PMID: 22887826]
[5]
Rolls ET, Sienkiewicz ZJ, Yaxley S. Hunger modulates the responses to gustatory stimuli of single neurons in the caudolateral orbitofrontal cortex of the macaque monkey. Eur J Neurosci 1989; 1(1): 53-60.
[http://dx.doi.org/10.1111/j.1460-9568.1989.tb00774.x] [PMID: 12106174]
[6]
Berridge KC, Robinson TE, Aldridge JW. Dissecting components of reward: ‘liking’, ‘wanting’, and learning. Curr Opin Pharmacol 2009; 9(1): 65-73.
[http://dx.doi.org/10.1016/j.coph.2008.12.014] [PMID: 19162544]
[7]
Kringelbach ML, Rolls ET. The functional neuroanatomy of the human orbitofrontal cortex: evidence from neuroimaging and neuropsychology. Prog Neurobiol 2004; 72(5): 341-72.
[http://dx.doi.org/10.1016/j.pneurobio.2004.03.006] [PMID: 15157726]
[8]
Craig AD. How do you feel--now? The anterior insula and human awareness. Nat Rev Neurosci 2009; 10(1): 59-70.
[http://dx.doi.org/10.1038/nrn2555] [PMID: 19096369]
[9]
Raichle ME. A paradigm shift in functional brain imaging. J Neurosci 2009; 29(41): 12729-34.
[http://dx.doi.org/10.1523/JNEUROSCI.4366-09.2009] [PMID: 19828783]
[10]
Fox MD, Snyder AZ, Vincent JL, Corbetta M, Van Essen DC, Raichle ME. The human brain is intrinsically organized into dynamic, anticorrelated functional networks. Proc Natl Acad Sci USA 2005; 102(27): 9673-8.
[http://dx.doi.org/10.1073/pnas.0504136102] [PMID: 15976020]
[11]
Greicius MD, Krasnow B, Reiss AL, Menon V. Functional connectivity in the resting brain: a network analysis of the default mode hypothesis. Proc Natl Acad Sci USA 2003; 100(1): 253-8.
[http://dx.doi.org/10.1073/pnas.0135058100] [PMID: 12506194]
[12]
Avery JA, Powell JN, Breslin FJ, et al. Obesity is associated with altered mid-insula functional connectivity to limbic regions underlying appetitive responses to foods. J Psychopharmacol (Oxford) 2017; 31(11): 1475-84.
[http://dx.doi.org/10.1177/0269881117728429] [PMID: 28944718]
[13]
Hudson JI, Hiripi E, Pope HG Jr, Kessler RC. The prevalence and correlates of eating disorders in the National Comorbidity Survey Replication. Biol Psychiatry 2007; 61(3): 348-58.
[http://dx.doi.org/10.1016/j.biopsych.2006.03.040] [PMID: 16815322]
[14]
American Psychiatric Association. Diagnostic and statistical manual of mental disorders. 5th ed. Washington, DC: American Psychiatric Pub 2013.
[15]
Kessler RC, Berglund PA, Chiu WT, et al. The prevalence and correlates of binge eating disorder in the World Health Organization World Mental Health Surveys. Biol Psychiatry 2013; 73(9): 904-14.
[http://dx.doi.org/10.1016/j.biopsych.2012.11.020] [PMID: 23290497]
[16]
Hudson JI, Lalonde JK, Berry JM, et al. Binge-eating disorder as a distinct familial phenotype in obese individuals. Arch Gen Psychiatry 2006; 63(3): 313-9.
[http://dx.doi.org/10.1001/archpsyc.63.3.313] [PMID: 16520437]
[17]
Wade TD, Treloar SA, Heath AC, Martin NG. An examination of the overlap between genetic and environmental risk factors for intentional weight loss and overeating. Int J Eat Disord 2009; 42(6): 492-7.
[http://dx.doi.org/10.1002/eat.20668] [PMID: 19235851]
[18]
Fairburn CG, Doll HA, Welch SL, Hay PJ, Davies BA, O’Connor ME. Risk factors for binge eating disorder: a community-based, case-control study. Arch Gen Psychiatry 1998; 55(5): 425-32.
[http://dx.doi.org/10.1001/archpsyc.55.5.425] [PMID: 9596045]
[19]
Striegel-Moore RH, Fairburn CG, Wilfley DE, Pike KM, Dohm FA, Kraemer HC. Toward an understanding of risk factors for binge-eating disorder in black and white women: a community-based case-control study. Psychol Med 2005; 35(6): 907-17.
[http://dx.doi.org/10.1017/S0033291704003435] [PMID: 15997611]
[20]
Stice E, Marti CN, Rohde P. Prevalence, incidence, impairment, and course of the proposed DSM-5 eating disorder diagnoses in an 8-year prospective community study of young women. J Abnorm Psychol 2013; 122(2): 445-57.
[http://dx.doi.org/10.1037/a0030679] [PMID: 23148784]
[21]
Udo T, Grilo CM. Prevalence and correlates of DSM-5-defined eating disorders in a nationally representative sample of U.S. adults. Biol Psychiatry 2018; 84(5): 345-54.
[http://dx.doi.org/10.1016/j.biopsych.2018.03.014] [PMID: 29859631]
[22]
Peterson RE, Latendresse SJ, Bartholome LT, Warren CS, Raymond NC. Binge eating disorder mediates links between symptoms of depression, anxiety, and caloric intake in overweight and obese women. J Obes 2012; 2012407103
[http://dx.doi.org/10.1155/2012/407103] [PMID: 22778917]
[23]
Duarte C, Pinto-Gouveia J, Ferreira C. Expanding binge eating assessment: Validity and screening value of the Binge Eating Scale in women from the general population. Eat Behav 2015; 18: 41-7.
[http://dx.doi.org/10.1016/j.eatbeh.2015.03.007] [PMID: 25880043]
[24]
Linardon J. Rates of abstinence following psychological or behavioral treatments for binge-eating disorder: Meta-analysis. Int J Eat Disord 2018; 51(8): 785-97.
[http://dx.doi.org/10.1002/eat.22897] [PMID: 30058074]
[25]
Vocks S, Tuschen-Caffier B, Pietrowsky R, Rustenbach SJ, Kersting A, Herpertz S. Meta-analysis of the effectiveness of psychological and pharmacological treatments for binge eating disorder. Int J Eat Disord 2010; 43(3): 205-17.
[PMID: 19402028]
[26]
Pope HG Jr, Lalonde JK, Pindyck LJ, et al. Binge eating disorder: a stable syndrome. Am J Psychiatry 2006; 163(12): 2181-3.
[http://dx.doi.org/10.1176/ajp.2006.163.12.2181] [PMID: 17151172]
[27]
Reas DL, Grilo CM. Review and meta-analysis of pharmacotherapy for binge-eating disorder. Obesity (Silver Spring) 2008; 16(9): 2024-38.
[http://dx.doi.org/10.1038/oby.2008.333] [PMID: 19186327]
[28]
Bulik CM, Reichborn-Kjennerud T. Medical morbidity in binge eating disorder. Int J Eat Disord 2003; 34(Suppl.): S39-46.
[http://dx.doi.org/10.1002/eat.10204] [PMID: 12900985]
[29]
Stopyra MA, Simon JJ, Skunde M, et al. Altered functional connectivity in binge eating disorder and bulimia nervosa: A resting-state fMRI study. Brain Behav 2019; 9(2)e01207
[http://dx.doi.org/10.1002/brb3.1207] [PMID: 30644179]
[30]
Davis C. From passive overeating to “food addiction”: a spectrum of compulsion and severity. ISRN Obes 2013; 2013435027
[http://dx.doi.org/10.1155/2013/435027] [PMID: 24555143]
[31]
Fairburn CG, Cooper Z, Doll HA, Norman P, O’Connor M. The natural course of bulimia nervosa and binge eating disorder in young women. Arch Gen Psychiatry 2000; 57(7): 659-65.
[http://dx.doi.org/10.1001/archpsyc.57.7.659] [PMID: 10891036]
[32]
Schag K, Teufel M, Junne F, et al. Impulsivity in binge eating disorder: food cues elicit increased reward responses and disinhibition. PLoS One 2013; 8(10)e76542
[http://dx.doi.org/10.1371/journal.pone.0076542] [PMID: 24146885]
[33]
Dawe S, Loxton NJ. The role of impulsivity in the development of substance use and eating disorders. Neurosci Biobehav Rev 2004; 28(3): 343-51.
[http://dx.doi.org/10.1016/j.neubiorev.2004.03.007] [PMID: 15225976]
[34]
Manwaring JL, Green L, Myerson J, Strube MJ, Wilfley DE. Discounting of Various types of rewards by women with and without binge eating Disorder: Evidence for general rather than specific Differences. Psychol Rec 2011; 61(4): 561-82.
[http://dx.doi.org/10.1007/BF03395777] [PMID: 24039301]
[35]
Meule A, Küppers C, Harms L, et al. Food cue-induced craving in individuals with bulimia nervosa and binge-eating disorder. PLoS One 2018; 13(9)e0204151
[http://dx.doi.org/10.1371/journal.pone.0204151] [PMID: 30212574]
[36]
Ng L, Davis C. Cravings and food consumption in Binge Eating Disorder. Eat Behav 2013; 14(4): 472-5.
[http://dx.doi.org/10.1016/j.eatbeh.2013.08.011] [PMID: 24183139]
[37]
Boswell RG, Kober H. Food cue reactivity and craving predict eating and weight gain: a meta-analytic review. Obes Rev 2016; 17(2): 159-77.
[http://dx.doi.org/10.1111/obr.12354] [PMID: 26644270]
[38]
Sobik L, Hutchison K, Craighead L. Cue-elicited craving for food: a fresh approach to the study of binge eating. Appetite 2005; 44(3): 253-61.
[http://dx.doi.org/10.1016/j.appet.2004.12.001] [PMID: 15876472]
[39]
Kringelbach ML. Food for thought: hedonic experience beyond homeostasis in the human brain. Neuroscience 2004; 126(4): 807-19.
[http://dx.doi.org/10.1016/j.neuroscience.2004.04.035] [PMID: 15207316]
[40]
Higgs S. Cognitive processing of food rewards. Appetite 2016; 104: 10-7.
[http://dx.doi.org/10.1016/j.appet.2015.10.003] [PMID: 26458961]
[41]
Saper CB, Chou TC, Elmquist JK. The need to feed: homeostatic and hedonic control of eating. Neuron 2002; 36(2): 199-211.
[http://dx.doi.org/10.1016/S0896-6273(02)00969-8] [PMID: 12383777]
[42]
O’Doherty J, Rolls ET, Francis S, et al. Sensory-specific satiety-related olfactory activation of the human orbitofrontal cortex. Neuroreport 2000; 11(4): 893-7.
[http://dx.doi.org/10.1097/00001756-200003200-00046] [PMID: 10757540]
[43]
Critchley HD, Rolls ET. Hunger and satiety modify the responses of olfactory and visual neurons in the primate orbitofrontal cortex. J Neurophysiol 1996; 75(4): 1673-86.
[http://dx.doi.org/10.1152/jn.1996.75.4.1673] [PMID: 8727405]
[44]
De Araujo IE, Rolls ET. Representation in the human brain of food texture and oral fat. J Neurosci 2004; 24(12): 3086-93.
[http://dx.doi.org/10.1523/JNEUROSCI.0130-04.2004] [PMID: 15044548]
[45]
Frank S, Linder K, Kullmann S, et al. Fat intake modulates cerebral blood flow in homeostatic and gustatory brain areas in humans. Am J Clin Nutr 2012; 95(6): 1342-9.
[http://dx.doi.org/10.3945/ajcn.111.031492] [PMID: 22572644]
[46]
Heni M, Kullmann S, Ketterer C, et al. Differential effect of glucose ingestion on the neural processing of food stimuli in lean and overweight adults. Hum Brain Mapp 2014; 35(3): 918-28.
[http://dx.doi.org/10.1002/hbm.22223] [PMID: 23307469]
[47]
Smeets PA, de Graaf C, Stafleu A, van Osch MJ, van der Grond J. Functional MRI of human hypothalamic responses following glucose ingestion. Neuroimage 2005; 24(2): 363-8.
[http://dx.doi.org/10.1016/j.neuroimage.2004.07.073] [PMID: 15627579]
[48]
Matsuda M, Liu Y, Mahankali S, et al. Altered hypothalamic function in response to glucose ingestion in obese humans. Diabetes 1999; 48(9): 1801-6.
[http://dx.doi.org/10.2337/diabetes.48.9.1801] [PMID: 10480611]
[49]
Ely AV, Wierenga CE, Bischoff-Grethe A, et al. Response in taste circuitry is not modulated by hunger and satiety in women remitted from bulimia nervosa. J Abnorm Psychol 2017; 126(5): 519-30.
[http://dx.doi.org/10.1037/abn0000218] [PMID: 28691842]
[50]
Rudebeck PH, Murray EA. The orbitofrontal oracle: cortical mechanisms for the prediction and evaluation of specific behavioral outcomes. Neuron 2014; 84(6): 1143-56.
[http://dx.doi.org/10.1016/j.neuron.2014.10.049] [PMID: 25521376]
[51]
de Araujo IET, Rolls ET, Kringelbach ML, McGlone F, Phillips N. Taste-olfactory convergence, and the representation of the pleasantness of flavour, in the human brain. Eur J Neurosci 2003; 18(7): 2059-68.
[http://dx.doi.org/10.1046/j.1460-9568.2003.02915.x] [PMID: 14622239]
[52]
Small DM, Zatorre RJ, Dagher A, Evans AC, Jones-Gotman M. Changes in brain activity related to eating chocolate: from pleasure to aversion. Brain 2001; 124(Pt 9): 1720-33.
[http://dx.doi.org/10.1093/brain/124.9.1720] [PMID: 11522575]
[53]
Schienle A, Schäfer A, Hermann A, Vaitl D. Binge-eating disorder: reward sensitivity and brain activation to images of food. Biol Psychiatry 2009; 65(8): 654-61.
[http://dx.doi.org/10.1016/j.biopsych.2008.09.028] [PMID: 18996508]
[54]
Wallis JD. Orbitofrontal cortex and its contribution to decision-making. Annu Rev Neurosci 2007; 30(1): 31-56.
[http://dx.doi.org/10.1146/annurev.neuro.30.051606.094334] [PMID: 17417936]
[55]
Kringelbach ML, O’Doherty J, Rolls ET, Andrews C. Activation of the human orbitofrontal cortex to a liquid food stimulus is correlated with its subjective pleasantness. Cereb Cortex 2003; 13(10): 1064-71.
[http://dx.doi.org/10.1093/cercor/13.10.1064] [PMID: 12967923]
[56]
Hutson PH, Balodis IM, Potenza MN. Binge-eating disorder: Clinical and therapeutic advances. Pharmacol Ther 2018; 182: 15-27.
[http://dx.doi.org/10.1016/j.pharmthera.2017.08.002] [PMID: 28830840]
[57]
Ostlund SB, Balleine BW. Orbitofrontal cortex mediates outcome encoding in Pavlovian but not instrumental conditioning. J Neurosci 2007; 27(18): 4819-25.
[http://dx.doi.org/10.1523/JNEUROSCI.5443-06.2007] [PMID: 17475789]
[58]
Rolls ET. The functions of the orbitofrontal cortex. Brain Cogn 2004; 55(1): 11-29.
[http://dx.doi.org/10.1016/S0278-2626(03)00277-X] [PMID: 15134840]
[59]
Rahman S, Sahakian BJ, Hodges JR, Rogers RD, Robbins TW. Specific cognitive deficits in mild frontal variant frontotemporal dementia. Brain 1999; 122(Pt 8): 1469-93.
[http://dx.doi.org/10.1093/brain/122.8.1469] [PMID: 10430832]
[60]
Small DM, Gregory MD, Mak YE, Gitelman D, Mesulam MM, Parrish T. Dissociation of neural representation of intensity and affective valuation in human gustation. Neuron 2003; 39(4): 701-11.
[http://dx.doi.org/10.1016/S0896-6273(03)00467-7] [PMID: 12925283]
[61]
Frank GK. Recent advances in neuroimaging to model eating disorder neurobiology. Curr Psychiatry Rep 2015; 17(4): 559.
[http://dx.doi.org/10.1007/s11920-015-0559-z] [PMID: 25749747]
[62]
Stoeckel LE, Weller RE, Cook EW III, Twieg DB, Knowlton RC, Cox JE. Widespread reward-system activation in obese women in response to pictures of high-calorie foods. Neuroimage 2008; 41(2): 636-47.
[http://dx.doi.org/10.1016/j.neuroimage.2008.02.031] [PMID: 18413289]
[63]
Critchley HD, Wiens S, Rotshtein P, Ohman A, Dolan RJ. Neural systems supporting interoceptive awareness. Nat Neurosci 2004; 7(2): 189-95.
[http://dx.doi.org/10.1038/nn1176] [PMID: 14730305]
[64]
Kranczioch C, Debener S, Schwarzbach J, Goebel R, Engel AK. Neural correlates of conscious perception in the attentional blink. Neuroimage 2005; 24(3): 704-14.
[http://dx.doi.org/10.1016/j.neuroimage.2004.09.024] [PMID: 15652305]
[65]
Stephan E, Pardo JV, Faris PL, et al. Functional neuroimaging of gastric distention. J Gastrointest Surg 2003; 7(6): 740-9.
[http://dx.doi.org/10.1016/S1091-255X(03)00071-4] [PMID: 13129550]
[66]
Craig AD. How do you feel? Interoception: the sense of the physiological condition of the body. Nat Rev Neurosci 2002; 3(8): 655-66.
[http://dx.doi.org/10.1038/nrn894] [PMID: 12154366]
[67]
Balodis IM, Molina ND, Kober H, et al. Divergent neural substrates of inhibitory control in binge eating disorder relative to other manifestations of obesity. Obesity (Silver Spring) 2013; 21(2): 367-77.
[http://dx.doi.org/10.1002/oby.20068] [PMID: 23404820]
[68]
Simon JJ, Skunde M, Hamze Sinno M, et al. Impaired cross-talk between mesolimbic food reward processing and metabolic signaling predicts body mass index. Front Behav Neurosci 2014; 8: 359.
[PMID: 25368558]
[69]
Stice E, Yokum S, Burger KS, Epstein LH, Small DM. Youth at risk for obesity show greater activation of striatal and somatosensory regions to food. J Neurosci 2011; 31(12): 4360-6.
[http://dx.doi.org/10.1523/JNEUROSCI.6604-10.2011] [PMID: 21430137]
[70]
Haber SN, Knutson B. The reward circuit: linking primate anatomy and human imaging. Neuropsychopharmacology 2010; 35(1): 4-26.
[http://dx.doi.org/10.1038/npp.2009.129] [PMID: 19812543]
[71]
Tellez LA, Han W, Zhang X, et al. Separate circuitries encode the hedonic and nutritional values of sugar. Nat Neurosci 2016; 19(3): 465-70.
[http://dx.doi.org/10.1038/nn.4224] [PMID: 26807950]
[72]
Rothemund Y, Preuschhof C, Bohner G, et al. Differential activation of the dorsal striatum by high-calorie visual food stimuli in obese individuals. Neuroimage 2007; 37(2): 410-21.
[http://dx.doi.org/10.1016/j.neuroimage.2007.05.008] [PMID: 17566768]
[73]
Frank GK, Shott ME, Riederer J, Pryor TL. Altered structural and effective connectivity in anorexia and bulimia nervosa in circuits that regulate energy and reward homeostasis. Transl Psychiatry 2016; 6(11): e932
[http://dx.doi.org/10.1038/tp.2016.199] [PMID: 27801897]
[74]
Raichle ME, Mintun MA. Brain work and brain imaging. Annu Rev Neurosci 2006; 29: 449-76.
[http://dx.doi.org/10.1146/annurev.neuro.29.051605.112819] [PMID: 16776593]
[75]
Fox MD, Snyder AZ, Vincent JL, Raichle ME. Intrinsic fluctuations within cortical systems account for intertrial variability in human behavior. Neuron 2007; 56(1): 171-84.
[http://dx.doi.org/10.1016/j.neuron.2007.08.023] [PMID: 17920023]
[76]
Vaidya CJ, Gordon EM. Phenotypic variability in resting-state functional connectivity: current status. Brain Connect 2013; 3(2): 99-120.
[http://dx.doi.org/10.1089/brain.2012.0110] [PMID: 23294010]
[77]
Seeley WW, Menon V, Schatzberg AF, et al. Dissociable intrinsic connectivity networks for salience processing and executive control. J Neurosci 2007; 27(9): 2349-56.
[http://dx.doi.org/10.1523/JNEUROSCI.5587-06.2007] [PMID: 17329432]
[78]
Contreras-Rodríguez O, Martín-Pérez C, Vilar-López R, Verdejo-Garcia A. Ventral and dorsal striatum networks in obesity: link to food craving and weight gain. Biol Psychiatry 2017; 81(9): 789-96.
[http://dx.doi.org/10.1016/j.biopsych.2015.11.020] [PMID: 26809248]
[79]
Kullmann S, Heni M, Linder K, et al. Resting-state functional connectivity of the human hypothalamus. Hum Brain Mapp 2014; 35(12): 6088-96.
[http://dx.doi.org/10.1002/hbm.22607] [PMID: 25131690]
[80]
Heimer L, Zahm DS, Churchill L, Kalivas PW, Wohltmann C. Specificity in the projection patterns of accumbal core and shell in the rat. Neuroscience 1991; 41(1): 89-125.
[http://dx.doi.org/10.1016/0306-4522(91)90202-Y] [PMID: 2057066]
[81]
Usuda I, Tanaka K, Chiba T. Efferent projections of the nucleus accumbens in the rat with special reference to subdivision of the nucleus: biotinylated dextran amine study. Brain Res 1998; 797(1): 73-93.
[http://dx.doi.org/10.1016/S0006-8993(98)00359-X] [PMID: 9630528]
[82]
Zahm DS, Heimer L. Two transpallidal pathways originating in the rat nucleus accumbens. J Comp Neurol 1990; 302(3): 437-46.
[http://dx.doi.org/10.1002/cne.903020302] [PMID: 1702109]
[83]
Al-Zubaidi A, Heldmann M, Mertins A, Jauch-Chara K, Münte TF. Influences of hunger, satiety and oral glucose on functional brain connectivity: a multimethod resting-state fMRI study. Neuroscience 2018; 382: 80-92.
[http://dx.doi.org/10.1016/j.neuroscience.2018.04.029] [PMID: 29723574]
[84]
Wright H, Li X, Fallon NB, et al. Differential effects of hunger and satiety on insular cortex and hypothalamic functional connectivity. Eur J Neurosci 2016; 43(9): 1181-9.
[http://dx.doi.org/10.1111/ejn.13182] [PMID: 26790868]
[85]
Lips MA, Wijngaarden MA, van der Grond J, 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): 524-31.
[http://dx.doi.org/10.3945/ajcn.113.080671] [PMID: 24965310]


Rights & PermissionsPrintExport Cite as

Article Details

VOLUME: 26
ISSUE: 20
Year: 2020
Published on: 20 June, 2020
Page: [2327 - 2333]
Pages: 7
DOI: 10.2174/1381612826666200309152321
Price: $65

Article Metrics

PDF: 19
HTML: 3