The impact of gut hormones on the neural circuit of appetite and satiety: A systematic review

Neuroscience and Biobehavioral Reviews

Volumn 80, Issue , 2017, Pages 457-475

  Zanchi, Davide ^a   Depoorter, Antoinette ^b   Egloff, Laura ^a   Haller, Sven ^c,d,e,f   Mählmann, Laura ^a   Lang, Undine E ^a   Drewe, Jürgen ^g   Beglinger, Christoph ^g   Schmidt, André ^a   Borgwardt, Stefan ^a  

^a UNIVERSITY OF BASEL   (Switzerland)

^b UNIVERSITY CHILDREN S HOSPITAL   (Switzerland)

^c Affidea Centre de Diagnostic Radiologique de Carouge CDRC   (Switzerland)

^d UNIVERSITY OF GENEVA MEDICAL SCHOOL   (Switzerland)

^e UPPSALA UNIVERSITY   (Sweden)

^f UNIVERSITY OF FREIBURG   (Germany)

^g Department of Research ^*  (Switzerland)

Author keywords

Brain; fMRI; Ghrelin; GLP 1; Glucose; Gut; Insulin; Leptin; PYY

Indexed keywords

CHOLECYSTOKININ; FRUCTOSE; GASTROINTESTINAL HORMONE; GHRELIN; GLUCAGON LIKE PEPTIDE 1; GLUCOSE; INSULIN; LEPTIN; PEPTIDE YY; HORMONE;

AMYGDALA; ANTERIOR CINGULATE; APPETITE; BRAIN BLOOD FLOW; BRAIN REGION; CAUDATE NUCLEUS; CORPUS STRIATUM; FUNCTIONAL CONNECTIVITY; FUNCTIONAL MAGNETIC RESONANCE IMAGING; GLUCOSE BLOOD LEVEL; GLUCOSE BRAIN LEVEL; HORMONE BLOOD LEVEL; HUMAN; HYPOTHALAMUS; INFERIOR FRONTAL GYRUS; INSULA; INSULIN BLOOD LEVEL; LIMBIC SYSTEM; LINGUAL GYRUS; MIDDLE FRONTAL GYRUS; NEUROCHEMISTRY; NEUROIMAGING; OBESITY; PREFRONTAL CORTEX; PRIORITY JOURNAL; PUTAMEN; REVIEW; SATIETY; SUPERIOR FRONTAL GYRUS; SUPERIOR TEMPORAL GYRUS; SYSTEMATIC REVIEW; THALAMUS; BRAIN; GASTROINTESTINAL TRACT; METABOLISM; PHYSIOLOGY;

APPETITE; BRAIN; GASTROINTESTINAL TRACT; HORMONES; HUMANS; SATIATION;

EID: 85022208485     PISSN: 01497634     EISSN: 18737528     Source Type: Journal    
DOI: 10.1016/j.neubiorev.2017.06.013     Document Type: Review

References (57)

1. Abizaid, A., Liu, Z.-W., Andrews, Z.B., Shanabrough, M., Borok, E., Elsworth, J.D., Roth, R.H., Sleeman, M.W., Picciotto, M.R., Tschöp, M.H., Gao, X.-B., Horvath, T.L., Ghrelin modulates the activity and synaptic input organization of midbrain dopamine neurons while promoting appetite. J. Clin. Invest. 116 (2006), 3229–3239, 10.1172/JCI29867.
2. Batterham, R.L., ffytche, D.H., Rosenthal, J.M., Zelaya, F.O., Barker, G.J., Withers, D.J., Williams, S.C.R., PYY modulation of cortical and hypothalamic brain areas predicts feeding behaviour in humans. Nature 450 (2007), 106–109, 10.1038/nature06212.
3. Becker, B., Wagner, D., Koester, P., Tittgemeyer, M., Mercer-Chalmers-Bender, K., Hurlemann, R., Zhang, J., Gouzoulis-Mayfrank, E., Kendrick, K.M., Daumann, J., Smaller amygdala and medial prefrontal cortex predict escalating stimulant use. Brain 138 (2015), 2074–2086, 10.1093/brain/awv113.
4. Borgwardt, S., Hammann, F., Scheffler, K., Kreuter, M., Drewe, J., Beglinger, C., Neural effects of green tea extract on dorsolateral prefrontal cortex. Eur. J. Clin. Nutr. 66 (2012), 1187–1192, 10.1038/ejcn.2012.105.
5. Cummings, D.E., Purnell, J.Q., Frayo, R.S., Schmidova, K., Wisse, B.E., Weigle, D.S., A preprandial rise in plasma ghrelin levels suggests a role in meal initiation in humans. Diabetes 50 (2001), 1714–1719.
6. De Silva, A., Salem, V., Long, C.J., Makwana, A., Newbould, R.D., Rabiner, E.A., Ghatei, M.A., Bloom, S.R., Matthews, P.M., Beaver, J.D., Dhillo, W.S., The gut hormones PYY3-36 and GLP-17-36 amide reduce food intake and modulate brain activity in appetite centers in humans. Cell Metab. 14 (2011), 700–706, 10.1016/j.cmet.2011.09.010.
7. De Silva, A., Salem, V., Matthews, P.M., Dhillo, W.S., De Silva, A., Salem, V., Matthews, P.M., Dhillo, W.S., The use of functional MRI to study appetite control in the CNS, the use of functional MRI to study appetite control in the CNS. J. Diabetes Res. J. Diabetes Res., 2012(2012), 2012, e764017, 10.1155/2012/764017.
8. Diano, S., Farr, S.A., Benoit, S.C., McNay, E.C., da Silva, I., Horvath, B., Gaskin, F.S., Nonaka, N., Jaeger, L.B., Banks, W.A., Morley, J.E., Pinto, S., Sherwin, R.S., Xu, L., Yamada, K.A., Sleeman, M.W., Tschöp, M.H., Horvath, T.L., Ghrelin controls hippocampal spine synapse density and memory performance. Nat. Neurosci. 9 (2006), 381–388, 10.1038/nn1656.
9. Douglas, S.M., Lasley, T.R., Leidy, H.J., Consuming beef vs. soy protein has little effect on appetite, satiety, and food intake in healthy adults. J. Nutr., 2015, 10.3945/jn.114.206987 jn206987.
10. Eldeghaidy, S., Marciani, L., Hort, J., Hollowood, T., Singh, G., Bush, D., Foster, T., Taylor, A.J., Busch, J., Spiller, R.C., Gowland, P.A., Francis, S.T., Prior consumption of a fat meal in healthy adults modulates the brain's response to fat. J. Nutr., 2016, 10.3945/jn.116.234104 jn234104.
11. Figlewicz, D.P., Adiposity signals and food reward: expanding the CNS roles of insulin and leptin. Am. J. Physiol. Regul. Integr. Comp. Physiol. 284 (2003), R882–892, 10.1152/ajpregu.00602.2002.
12. Gautier, J.F., Chen, K., Salbe, A.D., Bandy, D., Pratley, R.E., Heiman, M., Ravussin, E., Reiman, E.M., Tataranni, P.A., Differential brain responses to satiation in obese and lean men. Diabetes 49 (2000), 838–846.
13. Goldstone, A.P., Prechtl, C.G., Scholtz, S., Miras, A.D., Chhina, N., Durighel, G., Deliran, S.S., Beckmann, C., Ghatei, M.A., Ashby, D.R., Waldman, A.D., Gaylinn, B.D., Thorner, M.O., Frost, G.S., Bloom, S.R., Bell, J.D., Ghrelin mimics fasting to enhance human hedonic, orbitofrontal cortex, and hippocampal responses to food. Am. J. Clin. Nutr. 99 (2014), 1319–1330, 10.3945/ajcn.113.075291.
14. Grosshans, M., Vollmert, C., Vollstädt-Klein, S., Tost, H., Leber, S., Bach, P., Bühler, M., von der Goltz, C., Mutschler, J., Loeber, S., Hermann, D., Wiedemann, K., Meyer-Lindenberg, A., Kiefer, F., Association of leptin with food cue-induced activation in human reward pathways. Arch. Gen. Psychiatry 69 (2012), 529–537, 10.1001/archgenpsychiatry.2011.1586.
15. Heni, M., Kullmann, S., Ketterer, C., Guthoff, M., Bayer, M., Staiger, H., Machicao, F., Häring, H.-U., 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 (2014), 918–928, 10.1002/hbm.22223.
16. Heni, M., Kullmann, S., Gallwitz, B., Häring, H.-U., Preissl, H., Fritsche, A., Dissociation of GLP-1 and insulin association with food processing in the brain: GLP-1 sensitivity despite insulin resistance in obese humans. Mol. Metab. 4 (2015), 971–976, 10.1016/j.molmet.2015.09.007.
17. Hinkle, W., Cordell, M., Leibel, R., Rosenbaum, M., Hirsch, J., Effects of reduced weight maintenance and leptin repletion on functional connectivity of the hypothalamus in obese humans. PLoS One, 8, 2013, 10.1371/journal.pone.0059114.
18. Huda, M.S.B., Wilding, J.P.H., Pinkney, J.H., Gut peptides and the regulation of appetite. Obes. Rev. Off. J. Int. Assoc. Study Obes. 7 (2006), 163–182, 10.1111/j.1467-789X.2006.00245.x.
19. Jastreboff, A.M., Sinha, R., Arora, J., Giannini, C., Kubat, J., Malik, S., Van Name, M.A., Santoro, N., Savoye, M., Duran, E.J., Pierpont, B., Cline, G., Constable, R.T., Sherwin, R.S., Caprio, S., Altered brain response to drinking glucose and fructose in obese adolescents. Diabetes, 2016, 10.2337/db15-1216.
20. Jenkins, D.J., Wolever, T.M., Collier, G.R., Ocana, A., Rao, A.V., Buckley, G., Lam, Y., Mayer, A., Thompson, L.U., Metabolic effects of a low-glycemic-index diet. Am. J. Clin. Nutr. 46 (1987), 968–975.
21. Jones, R.B., McKie, S., Astbury, N., Little, T.J., Tivey, S., Lassman, D.J., McLaughlin, J., Luckman, S., Williams, S.R., Dockray, G.J., Thompson, D.G., Functional neuroimaging demonstrates that ghrelin inhibits the central nervous system response to ingested lipid. Gut, 2012, 10.1136/gutjnl-2011-301323 gutjnl-2011-301323.
22. Karra, E., O'Daly, O.G., Choudhury, A.I., Yousseif, A., Millership, S., Neary, M.T., Scott, W.R., Chandarana, K., Manning, S., Hess, M.E., Iwakura, H., Akamizu, T., Millet, Q., Gelegen, C., Drew, M.E., Rahman, S., Emmanuel, J.J., Williams, S.C.R., Rüther, U.U., Brüning, J.C., Withers, D.J., Zelaya, F.O., Batterham, R.L., A link between FTO, ghrelin, and impaired brain food-cue responsivity. J. Clin. Invest. 123 (2013), 3539–3551, 10.1172/JCI44403.
23. Kojima, M., Hosoda, H., Date, Y., Nakazato, M., Matsuo, H., Kangawa, K., Ghrelin is a growth-hormone-releasing acylated peptide from stomach. Nature 402 (1999), 656–660, 10.1038/45230.
24. Kroemer, N.B., Krebs, L., Kobiella, A., Grimm, O., Pilhatsch, M., Bidlingmaier, M., Zimmermann, U.S., Smolka, M.N., Fasting levels of ghrelin covary with the brain response to food pictures. Addict. Biol. 18 (2013), 855–862, 10.1111/j.1369-1600.2012.00489.x.
25. Kroemer, N.B., Krebs, L., Kobiella, A., Grimm, O., Vollstädt-Klein, S., Wolfensteller, U., Kling, R., Bidlingmaier, M., Zimmermann, U.S., Smolka, M.N., (Still) longing for food: insulin reactivity modulates response to food pictures. Hum. Brain Mapp. 34 (2013), 2367–2380, 10.1002/hbm.22071.
26. Kroemer, N.B., Wuttig, F., Bidlingmaier, M., Zimmermann, U.S., Smolka, M.N., Nicotine enhances modulation of food-cue reactivity by leptin and ghrelin in the ventromedial prefrontal cortex. Addict. Biol. 20 (2015), 832–844, 10.1111/adb.12167.
27. Lassman, D.J., McKie, S., Gregory, L.J., Lal, S., D'Amato, M., Steele, I., Varro, A., Dockray, G.J., Williams, S.C.R., Thompson, D.G., Defining the role of cholecystokinin in the lipid-induced human brain activation matrix. Gastroenterology 138 (2010), 1514–1524, 10.1053/j.gastro.2009.12.060.
28. Leidy, H.J., Ortinau, L.C., Douglas, S.M., Hoertel, H.A., Beneficial effects of a higher-protein breakfast on the appetitive, hormonal, and neural signals controlling energy intake regulation in overweight/obese, breakfast-skipping, late-adolescent girls. Am. J. Clin. Nutr. 97 (2013), 677–688, 10.3945/ajcn.112.053116.
29. Lennerz, B.S., Alsop, D.C., Holsen, L.M., Stern, E., Rojas, R., Ebbeling, C.B., Goldstein, J.M., Ludwig, D.S., Effects of dietary glycemic index on brain regions related to reward and craving in men1234. Am. J. Clin. Nutr. 98 (2013), 641–647, 10.3945/ajcn.113.064113.
30. 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. Am. J. Clin. Nutr. 96 (2012), 275–282, 10.3945/ajcn.112.037440.
31. Little, T.J., McKie, S., Jones, R.B., D'Amato, M., Smith, C., Kiss, O., Thompson, D.G., McLaughlin, J.T., Mapping glucose-mediated gut-to-brain signalling pathways in humans. Neuroimage 96 (2014), 1–11, 10.1016/j.neuroimage.2014.03.059.
32. Liu, Y., Gao, J.H., Liu, H.L., Fox, P.T., The temporal response of the brain after eating revealed by functional MRI. Nature 405 (2000), 1058–1062, 10.1038/35016590.
33. Malik, S., McGlone, F., Bedrossian, D., Dagher, A., Ghrelin modulates brain activity in areas that control appetitive behavior. Cell Metab. 7 (2008), 400–409, 10.1016/j.cmet.2008.03.007.
34. Moher, D., Shamseer, L., Clarke, M., Ghersi, D., Liberati, A., Petticrew, M., Shekelle, P., Stewart, L.A., PRISMA-P Group, Preferred reporting items for systematic review and meta-analysis protocols (PRISMA-P) 2015 statement. Syst. Rev., 4, 2015, 1, 10.1186/2046-4053-4-1.
35. Nakazato, M., Murakami, N., Date, Y., Kojima, M., Matsuo, H., Kangawa, K., Matsukura, S., A role for ghrelin in the central regulation of feeding. Nature 409 (2001), 194–198, 10.1038/35051587.
36. Page, K.A., Arora, J., Qiu, M., Relwani, R., Constable, R.T., Sherwin, R.S., Small decrements in systemic glucose provoke increases in hypothalamic blood flow prior to the release of counterregulatory hormones. Diabetes 58 (2009), 448–452, 10.2337/db08-1224.
37. Page, K.A., Seo, D., Belfort-DeAguiar, R., Lacadie, C., Dzuira, J., Naik, S., Amarnath, S., Constable, R.T., Sherwin, R.S., Sinha, R., Circulating glucose levels modulate neural control of desire for high-calorie foods in humans. J. Clin. Invest. 121 (2011), 4161–4169, 10.1172/JCI57873.
38. Page, K.A., Chan, O., Arora, J., Belfort-Deaguiar, R., Dzuira, J., Roehmholdt, B., Cline, G.W., Naik, S., Sinha, R., Constable, R.T., Sherwin, R.S., Effects of fructose vs glucose on regional cerebral blood flow in brain regions involved with appetite and reward pathways. JAMA 309 (2013), 63–70, 10.1001/jama.2012.116975.
39. Pannacciulli, N., Le, D.S.N.T., Salbe, A.D., Chen, K., Reiman, E.M., Tataranni, P.A., Krakoff, J., Postprandial glucagon-like peptide-1 (GLP-1) response is positively associated with changes in neuronal activity of brain areas implicated in satiety and food intake regulation in humans. Neuroimage 35 (2007), 511–517, 10.1016/j.neuroimage.2006.12.035.
40. Purnell, J.Q., Klopfenstein, B.A., Stevens, A.A., Havel, P.J., Adams, S.H., Dunn, T.N., Krisky, C., Rooney, W.D., Brain functional magnetic resonance imaging response to glucose and fructose infusions in humans. Diabetes Obes. Metab. 13 (2011), 229–234, 10.1111/j.1463-1326.2010.01340.x.
41. Rosenbaum, M., Sy, M., Pavlovich, K., Leibel, R.L., Hirsch, J., Leptin reverses weight loss–induced changes in regional neural activity responses to visual food stimuli. J. Clin. Invest. 118 (2008), 2583–2591, 10.1172/JCI35055.
42. Savage, S.W., Zald, D.H., Cowan, R.L., Volkow, N.D., Marks-Shulman, P.A., Kessler, R.M., Abumrad, N.N., Dunn, J.P., Regulation of novelty seeking by midbrain dopamine D2/D3 signaling and ghrelin is altered in obesity. Obes. Silver Spring Md. 22 (2014), 1452–1457, 10.1002/oby.20690.
43. Schilling, T.M., Ferreira de Sá, D.S., Westerhausen, R., Strelzyk, F., Larra, M.F., Hallschmid, M., Savaskan, E., Oitzl, M.S., Busch, H.-P., Naumann, E., Schächinger, H., Intranasal insulin increases regional cerebral blood flow in the insular cortex in men independently of cortisol manipulation. Hum. Brain Mapp. 35 (2014), 1944–1956, 10.1002/hbm.22304.
44. Schmidt, A., Hammann, F., Wölnerhanssen, B., Meyer-Gerspach, A.C., Drewe, J., Beglinger, C., Borgwardt, S., Green tea extract enhances parieto-frontal connectivity during working memory processing. Psychopharmacology (Berl.) 231 (2014), 3879–3888, 10.1007/s00213-014-3526-1.
45. Spetter, M.S., de Graaf, C., Mars, M., Viergever, M.A., Smeets, P.A.M., The sum of its Parts—Effects of gastric distention, nutrient content and sensory stimulation on brain activation. PLoS One, 9, 2014, 10.1371/journal.pone.0090872.
46. Steinert, R.E., Feinle-Bisset, C., Asarian, L., Horowitz, M., Beglinger, C., Geary, N., Ghrelin, CCK, GLP-1, and PYY(3–36): secretory controls and physiological roles in eating and glycemia in health, obesity, and after RYGB. Physiol. Rev. 97 (2017), 411–463, 10.1152/physrev.00031.2014.
47. Sun, X., Veldhuizen, M.G., Wray, A.E., de Araujo, I.E., Sherwin, R.S., Sinha, R., Small, D.M., The neural signature of satiation is associated with ghrelin response and triglyceride metabolism. Physiol. Behav. 0 (2014), 63–73, 10.1016/j.physbeh.2014.04.017.
48. Sun, X., Kroemer, N.B., Veldhuizen, M.G., Babbs, A.E., Araujo, I.E., Gitelman, de, Sherwin, D.R., Sinha, R.S., Small, R., Basolateral amygdala response to food cues in the absence of hunger is associated with weight gain susceptibility. J. Neurosci 35 (2015), 7964–7976, 10.1523/jneurosci.3884-14.2015.
49. Tataranni, P.A., Gautier, J.-F., Chen, K., Uecker, A., Bandy, D., Salbe, A.D., Pratley, R.E., Lawson, M., Reiman, E.M., Ravussin, E., Neuroanatomical correlates of hunger and satiation in humans using positron emission tomography. Proc. Natl. Acad. Sci. U. S. A. 96 (1999), 4569–4574.
50. van Bloemendaal, L., Izerman, J., Kulve, R.G., ten, J.S., Barkhof, F., Konrad, R.J., Drent, M.L., Veltman, D.J., Diamant, M., GLP-1 receptor activation modulates appetite- and reward-related brain areas in humans. Diabetes 63 (2014), 4186–4196, 10.2337/db14-0849.
51. Wölnerhanssen, B.K., Meyer-Gerspach, A.C., Schmidt, A., Zimak, N., Peterli, R., Beglinger, C., Borgwardt, S., Dissociable behavioral, physiological and neural effects of acute glucose and fructose ingestion: a pilot study. PLoS One, 10, 2015, e0130280, 10.1371/journal.pone.0130280.
52. Wallner-Liebmann, S., Koschutnig, K., Reishofer, G., Sorantin, E., Blaschitz, B., Kruschitz, R., Unterrainer, H.F., Gasser, R., Freytag, F., Bauer-Denk, C., Schienle, A., Schäfer, A., Mangge, H., Insulin and hippocampus activation in response to images of high-calorie food in normal weight and obese adolescents. Obes. Silver Spring Md. 18 (2010), 1552–1557, 10.1038/oby.2010.26.
53. Woelnerhanssen, B., Peterli, R., Steinert, R.E., Peters, T., Borbély, Y., Beglinger, C., Effects of postbariatric surgery weight loss on adipokines and metabolic parameters: comparison of laparoscopic Roux-en-Y gastric bypass and laparoscopic sleeve gastrectomy-a prospective randomized trial. Surg. Obes. Relat. Dis. Off. J. Am. Soc. Bariatr. Surg. 7 (2011), 561–568, 10.1016/j.soard.2011.01.044.
54. Woods, S.C., Seeley, R.J., Porte, D., Schwartz, M.W., Signals that regulate food intake and energy homeostasis. Science 280 (1998), 1378–1383, 10.1126/science.280.5368.1378.
55. Wren, A.M., Bloom, S.R., Gut hormones and appetite control. Gastroenterology 132 (2007), 2116–2130, 10.1053/j.gastro.2007.03.048.
56. Wright, H., Li, X., Fallon, N.B., Crookall, R., Giesbrecht, T., Thomas, A., Halford, J.C.G., Harrold, J., Stancak, A., Differential effects of hunger and satiety on insular cortex and hypothalamic functional connectivity. Eur. J. Neurosci. 43 (2016), 1181–1189, 10.1111/ejn.13182.
57. Zhang, B., Tian, D., Yu, C., Li, M., Zang, Y., Liu, Y., Walter, M., Altered baseline brain activity differentiates regional mechanisms subserving biological and psychological alterations in obese men. Sci. Rep., 5, 2015, 10.1038/srep11563.