Human brain responses to gastrointestinal nutrients and gut hormones

Current Opinion in Pharmacology

Volumn 31, Issue , 2016, Pages 8-12

  McLaughlin, John T ^a   McKie, Shane ^b  

^a UNIVERSITY OF MANCHESTER   (United Kingdom)

^b UNIVERSITY OF MANCHESTER   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID; CARBOHYDRATE; CHOLECYSTOKININ; FAT; GASTROINTESTINAL HORMONE; GHRELIN; GLUCAGON LIKE PEPTIDE 1; PEPTIDE YY; PROTEIN;

APPETITE; BOLD SIGNAL; BRAIN FUNCTION; CALORIC INTAKE; CARBOHYDRATE INTAKE; DIET RESTRICTION; EATING DISORDER; FAT INTAKE; FOOD INTAKE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HUMAN; MEDICAL RESEARCH; NONHUMAN; NUTRIENT UPTAKE; OBESITY; PRIORITY JOURNAL; REVIEW; SIGNAL TRANSDUCTION; ANIMAL; BRAIN; BRAIN MAPPING; EATING; FOOD; HOMEOSTASIS; METABOLISM; PATHOPHYSIOLOGY; PHYSIOLOGY;

ANIMALS; BRAIN; BRAIN MAPPING; EATING; FEEDING AND EATING DISORDERS; FOOD; GASTROINTESTINAL HORMONES; HOMEOSTASIS; HUMANS; OBESITY;

EID: 84983514068     PISSN: 14714892     EISSN: 14714973     Source Type: Journal    
DOI: 10.1016/j.coph.2016.08.006     Document Type: Review

References (30)

1. 1 Murray, S., Tulloch, A., Gold, M.S., Avena, N.M., Hormonal and neural mechanisms of food reward, eating behaviour and obesity. Nat Rev Endocrinol 10 (2014), 540–552.
2. 2 Schwartz, G.J., The role of gastrointestinal vagal afferents in the control of food intake: current prospects. Nutrition 16 (2000), 866–873.
3. 3 Schaeffer, M., Hodson, D.J., Mollard, P., The blood–brain barrier as a regulator of the gut–brain axis. Front Horm Res 42 (2014), 29–49.
4. 4 Anderson, I.M., McKie, S., Elliott, R., Williams, S.R., Deakin, J.F.W., Assessing human 5-HT function in vivo with pharmacoMRI. Neuropharmacology 55 (2008), 1029–1037.
5. 5 Scholtz, S., Miras, A.D., Chhina, N., Prechtl, C.G., Sleeth, M.L., Daud, N.M., Ismail, N.A., Durighel, G., Ahmed, A.R., Olbers, T., et al. Obese patients after gastric bypass surgery have lower brain-hedonic responses to food than after gastric banding. Gut 63 (2014), 891–902.
6. 6 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. J Clin Invest 121 (2011), 3094–3099.
7. 7 Foerster, B.U., Tomasi, D., Caparelli, E.C., Magnetic field shift due to mechanical vibration in functional magnetic resonance imaging. Magn Reson Med 54 (2005), 1261–1267.
8. 8• 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 The first detailed physMRI mapping of the whole spatiotemporal matrix of human brain responses to glucose infused into the gut, obviating the prior problems with movement and other artefacts.
9. 9 Evans, J.W., Kundu, P., Horovitz, S.G., Bandettini, P.A., Separating slow BOLD from non-BOLD baseline drifts using multi-echo fMRI. Neuroimage 105 (2015), 189–197.
10. 10 Pollak, T.A., De Simoni, S., Barimani, B., Zelaya, F.O., Stone, J.M., Mehta, M.A., Phenomenologically distinct psychotomimetic effects of ketamine are associated with cerebral blood flow changes in functionally relevant cerebral foci: a continuous arterial spin labelling study. Psychopharmacology 232 (2015), 4515–4524.
11. 11 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.
12. 12 Smeets, P.A., de Graaf, C., Stafleu, A., van Osch, M.J., van der Grond, J., Functional MRI of human hypothalamic responses following glucose ingestion. NeuroImage 24 (2005), 363–368.
13. 13 Smeets, P.A., de Graaf, C., Stafleu, A., van Osch, M.J., van der Grond, J., Functional magnetic resonance imaging of human hypothalamic responses to sweet taste and calories. Am J Clin Nutr 82 (2005), 1011–1016.
14. 14 Smeets, P.A., Vidarsdottir, S., de Graaf, C., Stafleu, A., van Osch, M.J., Viergever, M.A., Pijl, H., van der Grond, J., Oral glucose intake inhibits hypothalamic neuronal activity more effectively than glucose infusion. Am J Physiol Endocrinol Metab 293 (2007), E754–E758.
15. 15 Steinert, R.E., Frey, F., Töpfer, A., Drewe, J., Beglinger, C., Effects of carbohydrate sugars and artificial sweeteners on appetite and the secretion of gastrointestinal satiety peptides. Br J Nutr 105 (2011), 1320–1328.
16. 16 Bryant, C.E., Wasse, L.K., Astbury, N., Nandra, G., McLaughlin, J.T., Non-nutritive sweeteners: no class effect on the glycaemic or appetite responses to ingested glucose. Eur J Clin Nutr 68 (2014), 629–631.
17. 17 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 CCK in the lipid induced human brain activation matrix. Gastroenterology 138 (2010), 1514–1524.
18. 18• 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 The first evidence that glucose and fructose produce different patterns of brain response, albeit confounded by the use of different test sugar doses.
19. 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 db151216.
20. 20 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 61 (2012), 1543–1551.
21. 21• Byrne, C.S., Chambers, E.S., Alhabeeb, H., Chhina, N., Morrison, D.J., Preston, T., Tedford, C., Fitzpatrick, J., Irani, C., Busza, A., Garcia-Perez, I., Fountana, S., Holmes, E., Goldstone, A.P., Frost, G.S., Increased colonic propionate reduces anticipatory reward responses in the human striatum to high-energy foods. Am J Clin Nutr, 2016 [Epub ahead of print] The only study to date demonstrating an effect of short chain fatty acids on relevant aspects of brain function.
22. 22 Abdeen, G., le Roux, C.W., Mechanism underlying the weight loss and complications of Roux-en-Y gastric bypass. Obes Surg 26 (2016), 410–421.
23. 23 Batterham, R., Ffytche, D., Rosenthal, J., Zelaya, F.O., Barker, G.J., Withers, D.J., Williams, S.C., PYY modulation of cortical and hypothalamic brain areas predicts feeding behaviour in humans. Nature 450 (2007), 106–109.
24. 24 Pannacciulli, N., Le, D.S., 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.
25. 25•• van Bloemendaal, L., Veltman, D.J., Ten Kulve, J.S., Groot, P.F., Ruhé, H.G., Barkhof, F., Sloan, J.H., Diamant, M., Ijzerman, R.G., Brain reward-system activation in response to anticipation and consumption of palatable food is altered by glucagon-like peptide-1 receptor activation in humans. Diabetes Obes Metab 17 (2015), 878–886 A mechanistic role for GLP-1 in brain responses anticipation of food reward and intake is demonstrated using a GLP-1 receptor antagonist peptide infusion.
26. 26•• Ten Kulve, J.S., Veltman, D.J., van Bloemendaal, L., Groot, P.F., Ruhé, H.G., Barkhof, F., Diamant, M., Ijzerman, R.G., Endogenous GLP1 and GLP1 analogue alter CNS responses to palatable food consumption. J. Endocrinol 229 (2016), 1–12 The same group provided further evidence of GLP-1's role in the regulation of the brain reward systems to palatable foods.
27. 27 Zwanzger, P., Domschke, K., Bradwejn, J., Neuronal network of panic disorder: the role of the neuropeptide cholecystokinin. Depress Anxiety 29 (2012), 762–774.
28. 28 Levin, B.E., Magnan, C., Dunn-Meynell, A., Le Foll, C., Metabolic sensing and the brain: who, what, where, and how?. Endocrinology 152 (2011), 2552–2557.
29. 29•• 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 fMRI studies demonstrate that ghrelin infusion induces the same responses as fasting in appetitive and hedonic brain regions.
30. 30 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 PYY 3-36 and GLP-1 7-36 amide reduce food intake and modulate brain activity in appetite centers in humans. Cell Metab 14 (2011), 700–706.