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Clinical Research

Hunger and BMI modulate neural responses to sweet stimuli: fMRI meta-analysis

Subjects

Abstract

Objective

Consuming sweet foods, even when sated, can lead to unwanted weight gain. Contextual factors, such as longer time fasting, subjective hunger, and body mass index (BMI), may increase the likelihood of overeating. Nevertheless, the neural mechanisms underlying these moderating influences on energy intake are poorly understood.

Methods

We conducted both categorical meta-analysis and meta-regression of factors modulating neural responses to sweet stimuli, using data from 30 functional magnetic resonance imaging (fMRI) articles incorporating 39 experiments (Nā€‰=ā€‰995) carried out between 2006 and 2019.

Results

Responses to sweet stimuli were associated with increased activity in regions associated with taste, sensory integration, and reward processing. These taste-evoked responses were modulated by context. Longer fasts were associated with higher posterior cerebellar, thalamic, and striatal activity. Greater self-reported hunger was associated with higher medial orbitofrontal cortex (OFC), dorsal striatum, and amygdala activity and lower posterior cerebellar activity. Higher BMI was associated with higher posterior cerebellar and insular activity.

Conclusions

Variations in fasting time, self-reported hunger, and BMI are contexts associated with differential sweet stimulus responses in regions associated with reward processing and homeostatic regulation. These results are broadly consistent with a hierarchical model of taste processing. Hunger, but not fasting or BMI, was associated with sweet stimulus-related OFC activity. Our findings extend existing models of taste processing to include posterior cerebellar regions that are associated with moderating effects of both state (fast length and self-reported hunger) and trait (BMI) variables.

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Fig. 1
Fig. 2: Activation likelihood estimation meta-analysis of sweet stimuli relative to a basal condition.
Fig. 3: Separate meta-regression results for hours fasted, hunger, and body mass index as predictors of response to sweet stimuli relative to basal conditions.
Fig. 4: Hierarchical model of taste processing of Rolls, 2015, 2016a, 2016b, 2019 [39,40,41,42].

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References

  1. Small DM. Flavor is in the brain. Physiol Behav. 2012;107:540ā€“52.

    CASĀ  PubMedĀ  Google ScholarĀ 

  2. Huerta CI, Sarkar PR, Duong TQ, Laird AR, Fox PT. Neural bases of food perception: coordinate-based meta-analyses of neuroimaging studies in multiple modalities. Obesity. 2014;22:1439ā€“46.

    PubMedĀ  Google ScholarĀ 

  3. Veldhuizen MG, Albrecht J, Zelano C, Boesveldt S, Breslin P, Lundstrom JN. Identification of human gustatory cortex by activation likelihood estimation. Hum Brain Mapp. 2011;32:2256ā€“66.

    PubMedĀ  PubMed CentralĀ  Google ScholarĀ 

  4. Yeung AWK, Tanabe HC, Suen JLK, Goto TK. Taste intensity modulates effective connectivity from the insular cortex to the thalamus in humans. Neuroimage. 2016;135:214ā€“22.

    PubMedĀ  Google ScholarĀ 

  5. Yeung AndyWaiKan, Goto Tazuko K, Keung LW. Basic taste processing recruits bilateral anteroventral and middle dorsal insulae: an activation likelihood estimation metaā€analysis of fMRI studies. Brain Behav. 2017;7:e00655.

    PubMedĀ  PubMed CentralĀ  Google ScholarĀ 

  6. de Castro JM, Elmore DK. Subjective hunger relationships with meal patterns in the spontaneous feeding behavior of humans: evidence for a causal connection. Physiol Behav. 1988;43:159ā€“65.

    PubMedĀ  Google ScholarĀ 

  7. Raynor HA, Epstein LH. The relative-reinforcing value of food under differing levels of food deprivation and restriction. Appetite. 2003;40:15ā€“24.

    PubMedĀ  Google ScholarĀ 

  8. CDC. About adult BMI. 2020. http://www.cdc.gov/healthyweight/assessing/bmi/adult_bmi/index.html.

  9. Kuczmarski RJ, Ogden CL, Guo SS, Grummer-Strawn LM, Flegal KM, Mei Z, et al. 2000 CDC Growth Charts for the United States: methods and development. Vital and health statistics Series 11, Data from the National Health Survey. 2002;246:1ā€“190.

  10. Expert Panel on the Identification, Treatment of Overweight, Obesity in Adults (US), National Heart, Lung, Blood Institute, National Institute of Diabetes, Digestive, Kidney Diseases (US). Clinical guidelines on the identification, evaluation, and treatment of overweight and obesity in adults: the evidence report. National Institutes of Health, National Heart, Lung, and Blood Institute; 1998.

  11. Eiler WJA, Dzemidzic M, Soeurt CM, Carron CR, Oberlin BG, Considine RV, et al. Family history of alcoholism and the human brain response to oral sucrose. Neuroimage: Clin. 2018;17:1036ā€“46.

    Google ScholarĀ 

  12. Green E, Murphy C. Altered processing of sweet taste in the brain of diet soda drinkers. Physiol Behav. 2012;107:560ā€“7.

    CASĀ  PubMedĀ  PubMed CentralĀ  Google ScholarĀ 

  13. Jacobson A, Green E, Murphy C. Age-related functional changes in gustatory and reward processing regions: an fMRI study. Neuroimage. 2010;53:602ā€“10.

    PubMedĀ  PubMed CentralĀ  Google ScholarĀ 

  14. 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;31:4360ā€“6.

    CASĀ  PubMedĀ  PubMed CentralĀ  Google ScholarĀ 

  15. Burger KS, Stice E. Elevated energy intake is correlated with hyperresponsivity in attentional, gustatory, and reward brain regions while anticipating palatable food receipt. Am J Clin Nutr. 2013;97:1188ā€“94.

    CASĀ  PubMedĀ  PubMed CentralĀ  Google ScholarĀ 

  16. Simmons WK, Rapuano KM, Kallman SJ, Ingeholm JE, Miller B, Gotts SJ, et al. Category-specific integration of homeostatic signals in caudal, but not rostral, human insula. Nat Neurosci. 2013;16:1551ā€“2.

    CASĀ  PubMedĀ  PubMed CentralĀ  Google ScholarĀ 

  17. Stice E, Yokum S. Effects of gymnemic acids lozenge on reward region response to receipt and anticipated receipt of high-sugar food. Physiol Behav. 2018;194:568ā€“76.

    CASĀ  PubMedĀ  Google ScholarĀ 

  18. van Rijn I, de Graaf C, Smeets PA. Tasting calories differentially affects brain activation during hunger and satiety. Behav Brain Res. 2015;279:139ā€“47.

    PubMedĀ  Google ScholarĀ 

  19. Stopyra MA, Friederich H-C, Sailer S, Pauen S, Bendszus M, Herzog W, et al. The effect of intestinal glucose load on neural regulation of food craving. Nutr Neurosci.2019;2:1ā€“10.

    Google ScholarĀ 

  20. Thanarajah SE, Backes H, DiFeliceantonio AG, Albus K, Cremer AL, Hanssen R, et al. Food intake recruits orosensory and post-ingestive dopaminergic circuits to affect eating desire in humans. Cell Metab. 2019;29:695ā€“706.e4.

    CASĀ  PubMedĀ  Google ScholarĀ 

  21. Burger KS, Stice E. Relation of dietary restraint scores to activation of reward-related brain regions in response to food intake, anticipated intake, and food pictures. Neuroimage. 2011;55:233ā€“9.

    PubMedĀ  Google ScholarĀ 

  22. Frank GK, Oberndorfer TA, Simmons AN, Paulus MP, Fudge JL, Yang TT, et al. Sucrose activates human taste pathways differently from artificial sweetener. Neuroimage. 2008;39:1559ā€“69.

    PubMedĀ  Google ScholarĀ 

  23. Sylvetsky AC, Welsh JA, Brown RJ, Vos MB. Low-calorie sweetener consumption is increasing in the United States. Am J Clin Nutr. 2012;96:640ā€“6.

    CASĀ  PubMedĀ  PubMed CentralĀ  Google ScholarĀ 

  24. Burger KS, Stice E. Neural responsivity during soft drink intake, anticipation, and advertisement exposure in habitually consuming youth. Obesity. 2014;22:441ā€“50.

    CASĀ  PubMedĀ  Google ScholarĀ 

  25. Nakamura Y, Imafuku M, Nakatani H, Nishida A, Koike S. Difference in neural reactivity to taste stimuli and visual food stimuli in neural circuits of ingestive behavior. Brain Imaging Behav. 2019;8:1ā€“11.

    CASĀ  Google ScholarĀ 

  26. Boutelle K, Wierenga CE, Bischoff-Grethe A, Melrose AJ, Grenesko-Stevens E, Paulus MP, et al. Increased brain response to appetitive tastes in the insula and amygdala in obese compared with healthy weight children when sated. Int J Obes. 2015;39:620.

    CASĀ  Google ScholarĀ 

  27. Lancaster JL, Tordesillasā€GutiĆ©rrez D, Martinez M, Salinas F, Evans A, Zilles K, et al. Bias between MNI and Talairach coordinates analyzed using the ICBMā€152 brain template. Human Brain Mapp. 2007;28:1194ā€“205.

    Google ScholarĀ 

  28. Eickhoff SB, Laird AR, Grefkes C, Wang LE, Zilles K, Fox PT. Coordinateā€based activation likelihood estimation metaā€analysis of neuroimaging data: a randomā€effects approach based on empirical estimates of spatial uncertainty. Human Brain Mapp. 2009;30:2907ā€“26.

    Google ScholarĀ 

  29. Eickhoff SB, Laird AR, Fox PM, Lancaster JL, Fox PT. Implementation errors in the GingerALE Software: description and recommendations. Human Brain Mapp. 2017;38:7ā€“11.

    Google ScholarĀ 

  30. Turkeltaub PE, Eden GF, Jones KM, Zeffiro TA. Meta-analysis of the functional neuroanatomy of single-word reading: method and validation. Neuroimage. 2002;16:765ā€“80.

    PubMedĀ  Google ScholarĀ 

  31. Muller VI, Cieslik EC, Laird AR, Fox PT, Radua J, Mataix-Cols D, et al. Ten simple rules for neuroimaging meta-analysis. Neurosci Biobehav Rev. 2018;84:151ā€“61.

    PubMedĀ  Google ScholarĀ 

  32. Radua J, Mataix-Cols D. Meta-analytic methods for neuroimaging data explained. Biol Mood Anxiety Disord. 2012;2:6.

    PubMedĀ  PubMed CentralĀ  Google ScholarĀ 

  33. Radua J, Mataix-Cols D, Phillips ML, El-Hage W, Kronhaus D, Cardoner N, et al. A new meta-analytic method for neuroimaging studies that combines reported peak coordinates and statistical parametric maps. Eur Psychiatry. 2012;27:605ā€“11.

    CASĀ  PubMedĀ  Google ScholarĀ 

  34. Radua J, Rubia K, Canales-RodrĆ­guez EJ, Pomarol-Clotet E, Fusar-Poli P, Mataix-Cols D. Anisotropic kernels for coordinate-based meta-analyses of neuroimaging studies. Front Psychiatry. 2014;5:13.

    PubMedĀ  PubMed CentralĀ  Google ScholarĀ 

  35. Haase L, Cerf-Ducastel B, Murphy C. Cortical activation in response to pure taste stimuli during the physiological states of hunger and satiety. Neuroimage. 2009;44:1008ā€“21.

    PubMedĀ  Google ScholarĀ 

  36. Curley LB, Newman E, Thompson WK, Brown TT, Hagler DJ, Akshoomoff N, et al. Cortical morphology of the pars opercularis and its relationship to motor-inhibitory performance in a longitudinal, developing cohort. Brain Struct Funct. 2018;223:211ā€“20.

    PubMedĀ  Google ScholarĀ 

  37. Aron AR, Fletcher PC, Bullmore ET, Sahakian BJ, Robbins TW. Stop-signal inhibition disrupted by damage to right inferior frontal gyrus in humans. Nat Neurosci. 2003;6:115ā€“6.

    CASĀ  PubMedĀ  Google ScholarĀ 

  38. Aron AR, Robbins TW, Poldrack RA. Inhibition and the right inferior frontal cortex. Trends Cogn Sci. 2004;8:170ā€“7.

    PubMedĀ  Google ScholarĀ 

  39. Rolls ET. Taste, olfactory, and food reward value processing in the brain. Prog Neurobiol. 2015;127:64ā€“90.

    PubMedĀ  Google ScholarĀ 

  40. Rolls ET. Functions of the anterior insula in taste, autonomic, and related functions. Brain Cogn. 2016;110:4ā€“19.

    PubMedĀ  Google ScholarĀ 

  41. Rolls ET. Reward systems in the brain and nutrition. Annu Rev Nutr. 2016;36:435ā€“70.

    CASĀ  PubMedĀ  Google ScholarĀ 

  42. Rolls ET. The orbitofrontal cortex. Oxford University: Oxford University Press; 2019.

  43. van Meer F, van der Laan LN, Adan RA, Viergever MA, Smeets PA. What you see is what you eat: an ALE meta-analysis of the neural correlates of food viewing in children and adolescents. NeuroImage. 2015;104:35ā€“43.

    PubMedĀ  Google ScholarĀ 

  44. Voon V, Reiter A, Sebold M, Groman S. Model-based control in dimensional psychiatry. Biol Psychiatry. 2017;82:391ā€“400.

    PubMedĀ  Google ScholarĀ 

  45. Yousuf M, Heldmann M, Gottlich M, Munte TF, Donamayor N. Neural processing of food and monetary rewards is modulated by metabolic state. Brain Imaging Behav. 2018;12:1379ā€“92.

    PubMedĀ  Google ScholarĀ 

  46. Devoto F, Zapparoli L, Bonandrini R, Berlingeri M, Ferrulli A, Luzi L, et al. Hungry brains: A meta-analytical review of brain activation imaging studies on food perception and appetite in obese individuals. Neurosci Biobehav Rev. 2018;94:271ā€“85.

    CASĀ  PubMedĀ  Google ScholarĀ 

  47. Van der Laan LN, De Ridder DT, Viergever MA, Smeets PA. Appearance matters: neural correlates of food choice and packaging aesthetics. PloS ONE. 2012;7:e41738.

    PubMedĀ  PubMed CentralĀ  Google ScholarĀ 

  48. Monello LF, Seltzer CC, Mayer J. Hunger and satiety sensations in men, women, boys and girls: a preliminary report. Ann N Y Acad Sci. 1965;131:593ā€“602.

    CASĀ  PubMedĀ  Google ScholarĀ 

  49. Monello LF, Mayer J. Hunger and satiety sensations in men, women, boys, and girls. Am J Clin Nutr. 1967;20:253ā€“61.

    CASĀ  PubMedĀ  Google ScholarĀ 

  50. Paolini BM, Laurienti PJ, Norris J, Rejeski WJ. Meal replacement: calming the hot-state brain network of appetite. Front Psychol. 2014;5:249.

    PubMedĀ  PubMed CentralĀ  Google ScholarĀ 

  51. Paolini BM, Laurienti PJ, Simpson SL, Burdette JH, Lyday RG, Rejeski WJ. Global integration of the hot-state brain network of appetite predicts short term weight loss in older adult.Front Aging Neurosci. 2015;7:70.

    PubMedĀ  PubMed CentralĀ  Google ScholarĀ 

  52. Wardak C. The role of the supplementary motor area in inhibitory control in monkeys and humans. J Neurosci. 2011;31:5181ā€“3.

    CASĀ  PubMed CentralĀ  Google ScholarĀ 

  53. Chiu Y-C, Jiang J, Egner T. The caudate nucleus mediates learning of stimulusā€“control state associations. J Neurosci. 2017;37:1028ā€“38.

    CASĀ  PubMedĀ  Google ScholarĀ 

  54. Everitt BJ, Robbins TW. Drug addiction: updating actions to habits to compulsions ten years on. Annu Rev Psychol. 2016;67:23ā€“50.

    PubMedĀ  Google ScholarĀ 

  55. Kennedy J, Dimitropoulos A. Influence of feeding state on neurofunctional differences between individuals who are obese and normal weight: a meta-analysis of neuroimaging studies. Appetite. 2014;75:103ā€“9.

    PubMedĀ  Google ScholarĀ 

  56. GarcĆ­aā€GarcĆ­a I, Horstmann A, Jurado MA, Garolera M, Chaudhry SJ, Margulies DS, et al. Reward processing in obesity, substance addiction and nonā€substance addiction. Obes Rev. 2014;15:853ā€“69.

    PubMedĀ  Google ScholarĀ 

  57. Brooks SJ, Cedernaes J, Schiƶth 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.

    CASĀ  PubMedĀ  PubMed CentralĀ  Google ScholarĀ 

  58. Rolls ET, Scott TR, Sienkiewicz ZJ, Yaxley S. The responsiveness of neurones in the frontal opercular gustatory cortex of the macaque monkey is independent of hunger. J Physiol. 1988;397:1ā€“12.

    CASĀ  PubMedĀ  PubMed CentralĀ  Google ScholarĀ 

  59. Cerf-Ducastel B, Murphy C. fMRI activation in response to odorants orally delivered in aqueous solutions. Chemical Senses. 2001;26:625ā€“37.

    CASĀ  PubMedĀ  Google ScholarĀ 

  60. Rudenga K, Green B, Nachtigal D, Small DM. Evidence for an integrated oral sensory module in the human anterior ventral insula. Chem Senses. 2010;35:693ā€“703.

    CASĀ  PubMedĀ  PubMed CentralĀ  Google ScholarĀ 

  61. Veldhuizen MG, Nachtigal D, Teulings L, Gitelman DR, Small DM. The insular taste cortex contributes to odor quality coding.Front Hum Neurosci.2010;4:1ā€“11.

    Google ScholarĀ 

  62. Yaxley S, Rolls ET, Sienkiewicz ZJ. The responsiveness of neurons in the insular gustatory cortex of the macaque monkey is independent of hunger. Physiol Behav. 1988;42:223ā€“9.

    CASĀ  PubMedĀ  Google ScholarĀ 

  63. Haber SN, Knutson B. The reward circuit: linking primate anatomy and human imaging. Neuropsychopharmacology. 2010;35:4ā€“26.

    PubMedĀ  Google ScholarĀ 

  64. Critchley HD, Rolls ET. Hunger and satiety modify the responses of olfactory and visual neurons in the primate orbitofrontal cortex. J Neurophysiol. 1996;75:1673ā€“86.

    CASĀ  PubMedĀ  Google ScholarĀ 

  65. Kringelbach ML, Oā€™Doherty J, Rolls ET, Andrews C. Activation of the human orbitofrontal cortex to a liquid food stimulus is correlated with its subjective pleasantness. Cerebral Cortex. 2003;13:1064ā€“71.

    CASĀ  PubMedĀ  Google ScholarĀ 

  66. 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;1:53ā€“60.

    PubMedĀ  Google ScholarĀ 

  67. Rolls ET, Treves A. The neuronal encoding of information in the brain. Prog Neurobiol. 2011;95:448ā€“90.

    PubMedĀ  Google ScholarĀ 

  68. Grabenhorst F, Rolls ET, Parris BA, dā€™Souza AA. How the brain represents the reward value of fat in the mouth. Cerebral Cortex. 2010;20:1082ā€“91.

    PubMedĀ  Google ScholarĀ 

  69. Rolls ET, Critchley HD, Browning AS, Hernadi I, Lenard L. Responses to the sensory properties of fat of neurons in the primate orbitofrontal cortex. J Neurosci. 1999;19:1532ā€“40.

    CASĀ  PubMedĀ  PubMed CentralĀ  Google ScholarĀ 

  70. Rolls ET, Critchley HD, Verhagen JV, Kadohisa M. The representation of information about taste and odor in the orbitofrontal cortex.Chemosens Percept. 2010;3:16ā€“33.

    Google ScholarĀ 

  71. Berridge KC, Kringelbach ML. Pleasure systems in the brain. Neuron. 2015;86:646ā€“64.

    CASĀ  PubMedĀ  PubMed CentralĀ  Google ScholarĀ 

  72. Castro DC, Berridge KC. Opioid hedonic hotspot in nucleus accumbens shell: mu, delta, and kappa maps for enhancement of sweetness ā€œlikingā€ and ā€œwantingā€. J Neurosci. 2014;34:4239ā€“50.

    CASĀ  PubMedĀ  PubMed CentralĀ  Google ScholarĀ 

  73. Everitt BJ, Robbins TW. From the ventral to the dorsal striatum: devolving views of their roles in drug addiction. Neurosci Biobehav Rev. 2013;37:1946ā€“54.

    PubMedĀ  Google ScholarĀ 

  74. Ho C-Y, Berridge KC. An orexin hotspot in ventral pallidum amplifies hedonic ā€˜likingā€™ for sweetness. Neuropsychopharmacology. 2013;38:1655ā€“64.

    CASĀ  PubMedĀ  PubMed CentralĀ  Google ScholarĀ 

  75. Pecina S, Berridge KC. Hedonic hot spot in nucleus accumbens shell: where do Ī¼-opioids cause increased hedonic impact of sweetness? J Neurosci. 2005;25:11777ā€“86.

    CASĀ  PubMedĀ  PubMed CentralĀ  Google ScholarĀ 

  76. Smith DG, Robbins TW. The neurobiological underpinnings of obesity and binge eating: a rationale for adopting the food addiction model. Biol Psychiatry. 2013;73:804ā€“10.

    PubMedĀ  Google ScholarĀ 

  77. Volkow ND, Wang GJ, Baler RD. Reward, dopamine and the control of food intake: implications for obesity. Trends Cogn Sci. 2011;15:37ā€“46.

    CASĀ  PubMedĀ  Google ScholarĀ 

  78. Wang G-J, Volkow ND, Fowler JS. The role of dopamine in motivation for food in humans: implications for obesity. Expert Opin Ther Targets. 2002;6:601ā€“9.

    CASĀ  PubMedĀ  Google ScholarĀ 

  79. Wang GJ, Volkow ND, Thanos PK, Fowler JS. Positron emission tomographic evidence of similarity between obesity and drug addiction. Psychiatr Ann. 2003;33:104ā€“11.

    Google ScholarĀ 

  80. King BM. The modern obesity epidemic, ancestral hunter-gatherers, and the sensory/reward control of food intake. Am Psychol. 2013;68:88ā€“96.

    PubMedĀ  Google ScholarĀ 

  81. Volkow ND, Baler RD. NOW vs. LATER brain circuits: implications for obesity and addiction. Trends Neurosci. 2015;38:345ā€“52.

    CASĀ  PubMedĀ  Google ScholarĀ 

  82. Stice E, Yokum S. Neural vulnerability factors that increase risk for future weight gain. Psychol Bull. 2016;142:447ā€“71.

    PubMedĀ  PubMed CentralĀ  Google ScholarĀ 

  83. Haines D, Dietrichs E, An HRP. study of hypothalamoā€cerebellar and cerebelloā€hypothalamic connections in squirrel monkey (Saimiri sciureus). J Comp Neurol. 1984;229:559ā€“75.

    CASĀ  PubMedĀ  Google ScholarĀ 

  84. Haines DE, Dietrichs E, Mihailoff GA, McDonald EF. The cerebellar-hypothalamic axis: basic circuits and clinical observations. International Rev Neurobiol. 1997;41:83ā€“107.

    CASĀ  Google ScholarĀ 

  85. Dietrichs E, Haines D, RĆøste G, RĆøste L. Hypothalamocerebellar and cerebellohypothalamic projectionsā€”circuits for regulating nonsomatic cerebellar activity? Histol Histopathol. 1994;9:603ā€“14.

    CASĀ  PubMedĀ  Google ScholarĀ 

  86. Min C, Zhang T-m, Luo S-l, Cheng Z, Wu X-m, Zhou N-n, et al. Functional magnetic resonance imaging and immunohistochemical study of hypothalamic function following oral glucose ingestion in rats. Chin Med J. 2007;120:1232ā€“5.

    Google ScholarĀ 

  87. 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;19:1381ā€“94.

    PubMedĀ  Google ScholarĀ 

  88. Park B-y, Seo J, Park H. Functional brain networks associated with eating behaviors in obesity. Sci Rep. 2016;6:23891.

    CASĀ  PubMedĀ  PubMed CentralĀ  Google ScholarĀ 

  89. Wright H, Li X, Fallon NB, Crookall R, Giesbrecht T, Thomas A, et al. Differential effects of hunger and satiety on insular cortex and hypothalamic functional connectivity. Eur J Neurosci. 2016;43:1181ā€“9.

    PubMedĀ  PubMed CentralĀ  Google ScholarĀ 

  90. Demirtas-Tatlidede A, Freitas C, Pascual-Leone A, Schmahmann JD. Modulatory effects of theta burst stimulation on cerebellar nonsomatic functions. Cerebellum. 2011;10:495ā€“503.

    PubMedĀ  PubMed CentralĀ  Google ScholarĀ 

  91. Scalera G. Effects of corticocerebellar lesions on taste preferences, body weight gain, food and fluid intake in the rat. Journal Physiol. 1991;85:214ā€“22.

    CASĀ  Google ScholarĀ 

  92. Zhu J-N, Wang J-J. The cerebellum in feeding control: possible function and mechanism. Cell Mol Neurobiol. 2008;28:469ā€“78.

    PubMedĀ  Google ScholarĀ 

  93. Li B, Guo C-L, Tang J, Zhu J-N, Wang J-J. Cerebellar fastigial nuclear inputs and peripheral feeding signals converge on neurons in the dorsomedial hypothalamic nucleus. Neurosignals. 2009;17:132ā€“43.

    CASĀ  PubMedĀ  Google ScholarĀ 

  94. Li B, Zhuang Q-X, Gao H-R, Wang J-J, Zhu J-N. Medial cerebellar nucleus projects to feeding-related neurons in the ventromedial hypothalamic nucleus in rats. Brain Struct Funct. 2017;222:957ā€“71.

    CASĀ  PubMedĀ  Google ScholarĀ 

  95. Berman SM, Paz-Filho G, Wong ML, Kohno M, Licinio J, London ED. Effects of leptin deficiency and replacement on cerebellar response to food-related cues. Cerebellum. 2013;12:59ā€“67.

    CASĀ  PubMedĀ  PubMed CentralĀ  Google ScholarĀ 

  96. Rosenbaum M, Sy M, Pavlovich K, Leibel RL, Hirsch J. Leptin reverses weight loss-induced changes in regional neural activity responses to visual food stimuli. J Clin Investig. 2008;118:2583ā€“91.

    CASĀ  PubMedĀ  Google ScholarĀ 

  97. Scuteri A, Sanna S, Chen W-M, Uda M, Albai G, Strait J, et al. Genome-wide association scan shows genetic variants in the FTO gene are associated with obesity-related traits. PLoS Genet. 2007;3:e115.

    PubMedĀ  PubMed CentralĀ  Google ScholarĀ 

  98. Frayling TM, Timpson NJ, Weedon MN, Zeggini E, Freathy RM, Lindgren CM, et al. A common variant in the FTO gene is associated with body mass index and predisposes to childhood and adult obesity. Science. 2007;316:889ā€“94.

    CASĀ  PubMedĀ  PubMed CentralĀ  Google ScholarĀ 

  99. Smemo S, Tena JJ, Kim K-H, Gamazon ER, Sakabe NJ, GĆ³mez-MarĆ­n C, et al. Obesity-associated variants within FTO form long-range functional connections with IRX3. Nature. 2014;507:371ā€“5.

    CASĀ  PubMedĀ  PubMed CentralĀ  Google ScholarĀ 

  100. de Araujo TM, Razolli DS, Correa-da-Silva F, de Lima-Junior JC, Gaspar RS, Sidarta-Oliveira D, et al. The partial inhibition of hypothalamic IRX3 exacerbates obesity. EBioMedicine. 2019;39:448ā€“60.

    PubMedĀ  Google ScholarĀ 

  101. Moher D, Liberati A, Tetzlaff J, Altman DG, The PG. Preferred reporting items for systematic reviews and meta-analyses: The PRISMA Statement. PLoS Medi. 2009;6:e1000097.

  102. Chen EY, Olino TM, Conklin CJ, Mohamed FB, Hoge WS, Foster GD, et al. Genetic and neural predictors of behavioral weight loss treatment: A preliminary study. Obesity. 2017;25:66ā€“75.

    PubMedĀ  Google ScholarĀ 

  103. Doornweerd S, De Geus EJ, Barkhof F, Van Bloemendaal L, Boomsma DI, Van Dongen J, et al. Brain reward responses to food stimuli among female monozygotic twins discordant for BMI. Brain Imaging Behav. 2018;12:718ā€“27.

    PubMedĀ  Google ScholarĀ 

  104. Galvan A, McGlennen KM. Enhanced striatal sensitivity to aversive reinforcement in adolescents versus adults. J Cogn Neurosci. 2013;25:284ā€“96.

    PubMedĀ  Google ScholarĀ 

  105. Sun X, Veldhuizen MG, Wray AE, de Araujo IE, Sherwin RS, Sinha R, et al. The neural signature of satiation is associated with ghrelin response and triglyceride metabolism. Physiol Behav. 2014;136:63ā€“73.

    CASĀ  PubMedĀ  Google ScholarĀ 

  106. Uher R, Treasure J, Heining M, Brammer MJ, Campbell IC. Cerebral processing of food-related stimuli: effects of fasting and gender. Behav Brain Res. 2006;169:111ā€“9.

    CASĀ  PubMedĀ  Google ScholarĀ 

  107. van den Bosch I, Dalenberg JR, Renken R, van Langeveld AW, Smeets PA, Griffioen-Roose S, et al. To like or not to like: Neural substrates of subjective flavor preferences. Behav Brain Res. 2014;269C:128ā€“37.

    Google ScholarĀ 

  108. Felsted JA, Ren X, Chouinard-Decorte F, Small DM. Genetically determined differences in brain response to a primary food reward. J Neurosci. 2010;30:2428ā€“32.

    CASĀ  PubMedĀ  PubMed CentralĀ  Google ScholarĀ 

  109. Frank GK, Reynolds JR, Shott ME, Jappe L, Yang TT, Tregellas JR, et al. Anorexia nervosa and obesity are associated with opposite brain reward response. Neuropsychopharmacology. 2012;37:2031ā€“46.

    CASĀ  PubMedĀ  PubMed CentralĀ  Google ScholarĀ 

  110. Geha PY, Aschenbrenner K, Felsted J, Oā€™Malley SS, Small DM. Altered hypothalamic response to food in smokers. Am J Clin Nutr. 2013;97:15ā€“22.

    CASĀ  PubMedĀ  Google ScholarĀ 

  111. Kishi M, Sadachi H, Nakamura J, Tonoike M. Functional magnetic resonance imaging investigation of brain regions associated with astringency. Neurosci Res. 2017;122:9ā€“16.

    PubMedĀ  Google ScholarĀ 

  112. McCabe C, Woffindale C, Harmer CJ, Cowen PJ. Neural processing of reward and punishment in young people at increased familial risk of depression. Biol Psychiatry. 2012;72:588ā€“94.

    PubMedĀ  Google ScholarĀ 

  113. Murray E, Brouwer S, McCutcheon R, Harmer CJ, Cowen PJ, McCabe C. Opposing neural effects of naltrexone on food reward and aversion: implications for the treatment of obesity. Psychopharmacology. 2014;231:4323ā€“35.

    CASĀ  PubMedĀ  Google ScholarĀ 

  114. Nakamura Y, Goto TK, Tokumori K, Yoshiura T, Kobayashi K, Honda H, et al. The temporal change in the cortical activations due to salty and sweet tastes in humans: fMRI and time-intensity sensory evaluation. Neuroreport. 2012;23:400ā€“4.

    PubMedĀ  Google ScholarĀ 

  115. Oberndorfer TA, Frank GK, Simmons AN, Wagner A, McCurdy D, Fudge JL, et al. Altered insula response to sweet taste processing after recovery fromanorexia and bulimia nervosa. Am J Psychiatry. 2013;170:1143ā€“51.

    PubMedĀ  PubMed CentralĀ  Google ScholarĀ 

  116. Spetter MS, Smeets PA, de Graaf C, Viergever MA. Representation of sweet and salty taste intensity in the brain. Chem Senses. 2010;35:831ā€“40.

    CASĀ  PubMedĀ  Google ScholarĀ 

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Acknowledgements

We would like to thank these individuals for generously sharing unpublished details of their studies. Sonia Yokum Ph.D., Eric Stice Ph.D., Kyle Burger Ph.D., Kyle Simmons Ph.D., Inge van Rinj Ph.D., Marion A Stopyra Ph.D., Heiko Backes Ph.D., and David Karaken Ph.D. We would also like to thank Sunny Koey and Retta Zeffiro for their support and interest in this work.

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Chen, E.Y., Zeffiro, T.A. Hunger and BMI modulate neural responses to sweet stimuli: fMRI meta-analysis. Int J Obes 44, 1636ā€“1652 (2020). https://doi.org/10.1038/s41366-020-0608-5

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