The cephalic phase insulin response to nutritive and low-calorie sweeteners in solid and beverage form

Physiology and Behavior

Volumn 181, Issue , 2017, Pages 100-109

  Dhillon, Jaapna ^a   Lee, Janice Y ^a   Mattes, Richard D ^a  

^a PURDUE UNIVERSITY   (United States)

Author keywords

Cephalic phase; Food form; Insulin response; Learning; Low calorie sweeteners; Obesity

Indexed keywords

GLUCOSE; INSULIN; NUTRITIVE SWEETENER; SUCRALOSE; SUCROSE; SWEETENING AGENT; TRICHLOROSUCROSE;

ADULT; ARTICLE; BEVERAGE; BLOOD SAMPLING; BODY FAT; BODY MASS; CEPHALIC PHASE INSULIN RESPONSE; CLASSIFICATION; CONTROLLED STUDY; FEMALE; HUMAN; INSULIN BLOOD LEVEL; INSULIN RESPONSE; LOW CALORY DIET; MAJOR CLINICAL STUDY; MALE; OBESITY; PRIORITY JOURNAL; RANDOMIZED CONTROLLED TRIAL; SOLID; STATE DEPENDENT LEARNING; ADOLESCENT; ANALOGS AND DERIVATIVES; ASSOCIATIVE LEARNING; BLOOD; DRUG EFFECT; GLUCOSE BLOOD LEVEL; MIDDLE AGED; PATHOPHYSIOLOGY; PHARMACOLOGY; POWDER; PSYCHOLOGY; YOUNG ADULT;

ADOLESCENT; ADULT; ASSOCIATION LEARNING; BEVERAGES; BLOOD GLUCOSE; FEMALE; HUMANS; INSULIN; MALE; MIDDLE AGED; OBESITY; OVERWEIGHT; POWDERS; SUCROSE; SWEETENING AGENTS; YOUNG ADULT;

EID: 85029475889     PISSN: 00319384     EISSN: 1873507X     Source Type: Journal    
DOI: 10.1016/j.physbeh.2017.09.009     Document Type: Article

References (98)

1. Sarles, H., Dani, R., Prezelin, G., Souville, C., Figarella, C., Cephalic phase of pancreatic secretion in man. Gut 9 (1968), 214–221.
2. Mattes, R.D., Oral fat exposure alters postprandial lipid metabolism in humans. Am. J. Clin. Nutr. 63 (1996), 911–917.
3. Teff, K.L., Engelman, K., Oral sensory stimulation improves glucose tolerance in humans: effects on insulin, C-peptide, and glucagon. Am. J. Phys. Regul. Integr. Comp. Phys. 270 (1996), R1371–R1379.
4. Teff, K.L., Townsend, R.R., Early phase insulin infusion and muscarinic blockade in obese and lean subjects. Am. J. Phys. 277 (1999), R198–208.
5. Chen, J.D., Pan, J., Orr, W.C., Role of sham feeding in postprandial changes of gastric myoelectrical activity. Dig. Dis. Sci. 41 (1996), 1706–1712.
6. Nederkoorn, C., Smulders, F.T.Y., Jansen, A., Cephalic phase responses, craving and food intake in normal subjects. Appetite 35 (2000), 45–55, 10.1006/appe.2000.0328.
7. Wisén, O., Björvell, H., Cantor, P., Johansson, C., Theodorsson, E., Plasma concentrations of regulatory peptides in obesity following modified sham feeding (MSF) and a liquid test meal. Regul. Pept. 39 (1992), 43–54.
8. Degen, L., Oesch, S., Matzinger, D., Drewe, J., Knupp, M., Zimmerli, F., Beglinger, C., Effects of a preload on reduction of food intake by GLP-1 in healthy subjects. Digestion 74 (2006), 78–84, 10.1159/000097585.
9. Heath, R.B., Jones, R., Frayn, K.N., Robertson, M.D., Vagal stimulation exaggerates the inhibitory ghrelin response to oral fat in humans. J. Endocrinol. 180 (2004), 273–281.
10. Berthoud, H.R., Bereiter, D.A., Trimble, E.R., Siegel, E.G., Jeanrenaud, B., Cephalic phase, reflex insulin secretion neuroanatomical and physiological characterization. Diabetologia 20 (1981), 393–401, 10.1007/BF00254508.
11. Bernstein, I.L., Woods, S.C., Ontogeny of cephalic insulin release by the rat. Physiol. Behav. 24 (1980), 529–532, 10.1016/0031-9384(80)90247-4.
12. Leblanc, M.-È., Poirier, P., Chapter 14 - Blood Pressure Regulation in Abdominal Obesity. Watson, R.R., (eds.) Nutr. Prev. Treat. Abdom. Obes., Academic Press, San Diego, 2014, 151–161 http://www.sciencedirect.com/science/article/pii/B9780124078697000143 (accessed July 17, 2014).
13. Teff, K.L., Mattes, R.D., Engelman, K., Cephalic phase insulin release in normal weight males: verification and reliability. Am. J. Phys. 261 (1991), E430–436.
14. Teff, K.L., Mattes, R.D., Engelman, K., Mattern, J., Cephalic-phase insulin in obese and normal-weight men: relation to postprandial insulin. Metabolism 42 (1993), 1600–1608.
15. Ahrén, B., Holst, J.J., The cephalic insulin response to meal ingestion in humans is dependent on both cholinergic and noncholinergic mechanisms and is important for postprandial glycemia. Diabetes 50 (2001), 1030–1038.
16. Teff, K.L., Devine, J., Engelman, K., Sweet taste: effect on cephalic phase insulin release in men. Physiol. Behav. 57 (1995), 1089–1095.
17. Goldfine, I.D., Ryan, W.G., Schwartz, T.B., The effect of glucola, diet cola and water ingestion on blood glucose and plasma insulin. Proc. Soc. Exp. Biol. Med. Soc. Exp. Biol. Med. N. Y. N. 131 (1969), 329–330.
18. Bruce, D.G., Storlien, L.H., Furler, S.M., Chisholm, D.J., Cephalic phase metabolic responses in normal weight adults. Metabolism 36 (1987), 721–725.
19. Morricone, L., Bombonato, M., Cattaneo, A.G., Enrini, R., Lugari, R., Zandomenighi, R., Caviezel, F., Food-related sensory stimuli are able to promote pancreatic polypeptide elevation without evident cephalic phase insulin secretion in human obesity. Horm. Metab. Res. Horm. Stoffwechselforschung Horm. Métabolisme. 32 (2000), 240–245, 10.1055/s-2007-978628.
20. Porte, D., Robertson, R., Halter, J., Kulkosky, P., Makous, W., Woods, S., Neuroendocrine recognition of glucose: the glucoreceptor hypothesis and the diabetic syndrome. Senses, Y. Katsubi, Sato, M., Tabogi, S.F., Oomura, Y., (eds.) Food Intake Chem, 1977, Univ Park Press, Baltimore, 336.
21. Just, T., Pau, H.W., Engel, U., Hummel, T., Cephalic phase insulin release in healthy humans after taste stimulation?. Appetite 51 (2008), 622–627, 10.1016/j.appet.2008.04.271.
22. Ford, H.E., Peters, V., Martin, N.M., Sleeth, M.L., Ghatei, M.A., Frost, G.S., Bloom, S.R., Effects of oral ingestion of sucralose on gut hormone response and appetite in healthy normal-weight subjects. Eur. J. Clin. Nutr. 65 (2011), 508–513, 10.1038/ejcn.2010.291.
23. Härtel, B., Graubaum, H., Schneider, B., The influence of sweetener solutions on the secretion of insulin and the blood glucose level. Ernährungsumschau 40 (1993), 152–155.
24. Liang, Y., Maier, V., Steinbach, G., Lalić, L., Pfeiffer, E.F., The effect of artificial sweetener on insulin secretion. II. Stimulation of insulin release from isolated rat islets by Acesulfame K (in vitro experiments). Horm. Metab. Res. Horm. Stoffwechselforschung Horm. Metab. 19 (1987), 285–289, 10.1055/s-2007-1011802.
25. Sjöström, L., Garellick, G., Krotkiewski, M., Luyckx, A., Peripheral insulin in response to the sight and smell of food. Metabolism 29 (1980), 901–909, 10.1016/0026-0495(80)90031-1.
26. Bellisle, F., Louis-Sylvestre, J., Demozay, F., Blazy, D., Le Magnen, J., Reflex insulin response associated to food intake in human subjects. Physiol. Behav. 31 (1983), 515–521, 10.1016/0031-9384(83)90075-6.
27. Berthoud, H.R., Bereiter, D.A., Trimble, E.R., Siegel, E.G., Jeanrenaud, B., Cephalic phase, reflex insulin secretion. Neuroanatomical and physiological characterization. Diabetologia(20 Suppl), 1981, 393–401.
28. Swithers, S.E., Davidson, T.L., A role for sweet taste: calorie predictive relations in energy regulation by rats. Behav. Neurosci. 122 (2008), 161–173, 10.1037/0735-7044.122.1.161.
29. Feijó, F. de M., Ballard, C.R., Foletto, K.C., Batista, B.A.M., Neves, A.M., Ribeiro, M.F.M., Bertoluci, M.C., Saccharin and aspartame, compared with sucrose, induce greater weight gain in adult Wistar rats, at similar total caloric intake levels. Appetite 60 (2013), 203–207, 10.1016/j.appet.2012.10.009.
30. Mattes, R.D., Popkin, B.M., Nonnutritive sweetener consumption in humans: effects on appetite and food intake and their putative mechanisms. Am. J. Clin. Nutr. 89 (2009), 1–14, 10.3945/ajcn.2008.26792.
31. Malik, V.S., Schulze, M.B., Hu, F.B., Intake of sugar-sweetened beverages and weight gain: a systematic review. Am. J. Clin. Nutr. 84 (2006), 274–288.
32. Kant, A.K., Consumption of energy-dense, nutrient-poor foods by adult Americans: nutritional and health implications. The third National Health and Nutrition Examination Survey, 1988–1994. Am. J. Clin. Nutr. 72 (2000), 929–936.
33. Ohara, I., Otsuka, S.I., Yugari, Y., The influence of carrier of gustatory stimulation on the cephalic phase of canine pancreatic secretion. J. Nutr. 109 (1979), 2098–2105.
34. Teff, K.L., Cephalic phase pancreatic polypeptide responses to liquid and solid stimuli in humans. Physiol. Behav. 99 (2009), 317–323.
35. Black, R.M., Tanaka, P., Leiter, L.A., Anderson, G.H., Soft drinks with aspartame: effect on subjective hunger, food selection, and food intake of young adult males. Physiol. Behav. 49 (1991), 803–810.
36. Johnson, W.G., Wildman, H.E., Influence of external and covert food stimuli on insulin secretion in obese and normal persons. Behav. Neurosci. 97 (1983), 1025–1028.
37. Stunkard, A.J., Messick, S., The three-factor eating questionnaire to measure dietary restraint, disinhibition and hunger. J. Psychosom. Res. 29 (1985), 71–83.
38. Garner, D.M., Olmsted, M.P., Bohr, Y., Garfinkel, P.E., The eating attitudes test: psychometric features and clinical correlates. Psychol. Med. 12 (1982), 871–878.
39. Schutz, H.G., Cardello, A.V., Labeled Affective, A., Magnitude (lam) scale for assessing food liking/disliking1. J. Sens. Stud. 16 (2001), 117–159, 10.1111/j.1745-459X.2001.tb00293.x.
40. Bartoshuk, L.M., Duffy, V.B., Green, B.G., Hoffman, H.J., Ko, C.-W., Lucchina, L.A., Marks, L.E., Snyder, D.J., Weiffenbach, J.M., Valid across-group comparisons with labeled scales: the gLMS versus magnitude matching. Physiol. Behav. 82 (2004), 109–114, 10.1016/j.physbeh.2004.02.033.
41. Dietary Reference Intakes for Energy, Carbohydrate, Fiber, Fat, Fatty Acids, Cholesterol, Protein, and Amino Acids (Macronutrients), 2005, National Academies Press, Washington, D.C. http://www.nap.edu/catalog/10490 (accessed March 9, 2016).
42. Flint, A., Raben, A., Blundell, J.E., Astrup, A., Reproducibility, power and validity of visual analogue scales in assessment of appetite sensations in single test meal studies. Int. J. Obes. Relat. Metab. Disord. J. Int. Assoc. Study Obes. 24 (2000), 38–48.
43. Stubbs, R.J., Hughes, D.A., Johnstone, A.M., Rowley, E., Ferris, S., Elia, M., Stratton, R., King, N., Blundell, J.E., Description and evaluation of a Newton-based electronic appetite rating system for temporal tracking of appetite in human subjects. Physiol. Behav. 72 (2001), 615–619.
44. Jamison, R.N., Gracely, R.H., Raymond, S.A., Levine, J.G., Marino, B., Herrmann, T.J., Daly, M., Fram, D., Katz, N.P., Comparative study of electronic vs. paper VAS ratings: a randomized, crossover trial using healthy volunteers. Pain 99 (2002), 341–347.
45. Alvarez, M.A., Portilla, L., Gonzalez, R., Ezcurra, E., Insulin response to a short stress period. Psychoneuroendocrinology 14 (1989), 241–244, 10.1016/0306-4530(89)90022-X.
46. Tepper, B.J., Mattes, R.D., Farkas, B.K., Learned flavor cues influence food intake in humans. J. Sens. Stud. 6 (1991), 89–100.
47. Powley, T.L., Berthoud, H.R., Diet and cephalic phase insulin responses. Am. J. Clin. Nutr. 42 (1985), 991–1002.
48. Malaisse, W.J., Vanonderbergen, A., Louchami, K., Jijakli, H., Malaisse-Lagae, F., Effects of artificial sweeteners on insulin release and cationic fluxes in rat pancreatic islets. Cell. Signal. 10 (1998), 727–733, 10.1016/S0898-6568(98)00017-5.
49. Ionescu, E., Rohner-Jeanrenaud, F., Proietto, J., Rivest, R.W., Jeanrenaud, B., Taste-induced changes in plasma insulin and glucose turnover in lean and genetically obese rats. Diabetes 37 (1988), 773–779.
50. Glendinning, J.I., Stano, S., Holter, M., Azenkot, T., Goldman, O., Margolskee, R.F., Vasselli, J.R., Sclafani, A., Sugar-induced cephalic-phase insulin release is mediated by a T1r2 + T1r3-independent taste transduction pathway in mice. Am. J. Phys. Regul. Integr. Comp. Phys., 2015 ajpregu.00056.2015 http://dx.doi.org/10.1152/ajpregu.00056.2015.
51. Dušková, M., Macourek, M., Šrámková, M., Hill, M., Stárka, L., The role of taste in cephalic phase of insulin secretion. Prague Med. Rep. 114 (2013), 222–230.
52. Assadi-Porter, F.M., Maillet, E.L., Radek, J.T., Quijada, J., Markley, J.L., Max, M., Key amino acid residues involved in multi-point binding interactions between brazzein, a sweet protein, and the T1R2-T1R3 human sweet receptor. J. Mol. Biol. 398 (2010), 584–599, 10.1016/j.jmb.2010.03.017.
53. Jiang, P., Ji, Q., Liu, Z., Snyder, L.A., Benard, L.M.J., Margolskee, R.F., Max, M., The cysteine-rich region of T1R3 determines responses to intensely sweet proteins. J. Biol. Chem. 279 (2004), 45068–45075, 10.1074/jbc.M406779200.
54. Masuda, K., Koizumi, A., Nakajima, K., Tanaka, T., Abe, K., Misaka, T., Ishiguro, M., Characterization of the modes of binding between human sweet taste receptor and low-molecular-weight sweet compounds. PLoS One, 7, 2012, e35380, 10.1371/journal.pone.0035380.
55. Ohta, K., Masuda, T., Tani, F., Kitabatake, N., The cysteine-rich domain of human T1R3 is necessary for the interaction between human T1R2–T1R3 sweet receptors and a sweet-tasting protein, thaumatin. Biochem. Biophys. Res. Commun. 406 (2011), 435–438, 10.1016/j.bbrc.2011.02.063.
56. Koizumi, A., Nakajima, K., Asakura, T., Morita, Y., Ito, K., Shmizu-Ibuka, A., Misaka, T., Abe, K., Taste-modifying sweet protein, neoculin, is received at human T1R3 amino terminal domain. Biochem. Biophys. Res. Commun. 358 (2007), 585–589, 10.1016/j.bbrc.2007.04.171.
57. Maillet, E.L., Cui, M., Jiang, P., Mezei, M., Hecht, E., Quijada, J., Margolskee, R.F., Osman, R., Max, M., Characterization of the binding site of aspartame in the human sweet taste receptor. Chem. Senses 40 (2015), 577–586, 10.1093/chemse/bjv045.
58. Nakagawa, Y., Nagasawa, M., Mogami, H., Lohse, M., Ninomiya, Y., Kojima, I., Multimodal function of the sweet taste receptor expressed in pancreatic β-cells: generation of diverse patterns of intracellular signals by sweet agonists. Endocr. J. 60 (2013), 1191–1206, 10.1507/endocrj.EJ13-0282.
59. Laffitte, A., Neiers, F., Briand, L., Functional roles of the sweet taste receptor in oral and extraoral tissues. Curr. Opin. Clin. Nutr. Metab. Care. 17 (2014), 379–385, 10.1097/MCO.0000000000000058.
60. Kojima, I., Nakagawa, Y., Ohtsu, Y., Medina, A., Nagasawa, M., Sweet taste-sensing receptors expressed in pancreatic β-cells: sweet molecules act as biased agonists. Endocrinol. Metab. 29 (2014), 12–19, 10.3803/EnM.2014.29.1.12.
61. Simon, C., Schlienger, J.L., Sapin, R., Imler, M., Cephalic phase insulin secretion in relation to food presentation in normal and overweight subjects. Physiol. Behav. 36 (1986), 465–469, 10.1016/0031-9384(86)90316-1.
62. Sahakian, B.J., Lean, M.E.J., Robbins, T.W., James, W.P.T., Salivation and insulin secretion in response to food in non-obese men and women. Appetite 2 (1981), 209–216, 10.1016/S0195-6663(81)80043-8.
63. Yamazaki, M., Sakaguchi, T., Effects of D-glucose anomers on sweetness taste and insulin release in man. Brain Res. Bull. 17 (1986), 271–274, 10.1016/0361-9230(86)90126-7.
64. Zhao, G.Q., Zhang, Y., Hoon, M.A., Chandrashekar, J., Erlenbach, I., Ryba, N.J.P., Zuker, C.S., The receptors for mammalian sweet and umami taste. Cell 115 (2003), 255–266, 10.1016/S0092-8674(03)00844-4.
65. Stockhorst, U., Steingrüber, H.-J., Scherbaum, W.A., Classically conditioned responses following repeated insulin and glucose administration in humans. Behav. Brain Res. 110 (2000), 143–159, 10.1016/S0166-4328(99)00192-8.
66. Abdallah, L., Chabert, M., Louis-Sylvestre, J., Cephalic phase responses to sweet taste. Am. J. Clin. Nutr. 65 (1997), 737–743.
67. Taylor, I.L., Feldman, M., Effect of cephalic-vagal stimulation on insulin, gastric inhibitory polypeptide, and pancreatic polypeptide release in humans. J. Clin. Endocrinol. Metab. 55 (1982), 1114–1117, 10.1210/jcem-55-6-1114.
68. Broberg, D.J., Bernstein, I.L., Cephalic insulin release in anorexic women. Physiol. Behav. 45 (1989), 871–874.
69. Lucas, F., Bellisle, F., Di Maio, A., Spontaneous insulin fluctuations and the preabsorptive insulin response to food ingestion in humans. Physiol. Behav. 40 (1987), 631–636, 10.1016/0031-9384(87)90109-0.
70. Calles-Escandon, J., Robbins, D.C., Loss of early phase of insulin release in humans impairs glucose tolerance and blunts thermic effect of glucose. Diabetes 36 (1987), 1167–1172.
71. Steffens, A.B., Influence of the oral cavity on insulin release in the rat. Am. J. Phys. 230 (1976), 1411–1415.
72. Parra-Covarrubias, A., Rivera-Rodriguez, I., Almaraz-Ugalde, A., Cephalic phase of insulin secretion in obese adolescents. Diabetes 20 (1971), 800–802.
73. Cerasi, E., Luft, R., The plasma insulin response to glucose infusion in healthy subjects and in diabetes mellitus. Acta Endocrinol. 55 (1967), 278–304, 10.1530/acta.0.0550278.
74. Del Prato, S., Tiengo, A., The importance of first-phase insulin secretion: implications for the therapy of type 2 diabetes mellitus. Diabetes Metab. Res. Rev. 17 (2001), 164–174.
75. Davies, M.J., Rayman, G., Grenfell, A., Gray, I.P., Day, J.L., Hales, C.N., Loss of the first phase insulin response to intravenous glucose in subjects with persistent impaired glucose tolerance. Diabet. Med. J. Br. Diabet. Assoc. 11 (1994), 432–436.
76. Pepino, M.Y., Tiemann, C.D., Patterson, B.W., Wice, B.M., Klein, S., Sucralose affects glycemic and hormonal responses to an oral glucose load. Diabetes Care 36 (2013), 2530–2535, 10.2337/dc12-2221.
77. Wu, T., Bound, M.J., Standfield, S.D., Bellon, M., Young, R.L., Jones, K.L., Horowitz, M., Rayner, C.K., Artificial sweeteners have no effect on gastric emptying, glucagon-like peptide-1, or glycemia after oral glucose in healthy humans. Diabetes Care 36 (2013), e202–e203, 10.2337/dc13-0958.
78. Sylvetsky, A.C., Brown, R.J., Blau, J.E., Walter, M., Rother, K.I., Hormonal responses to non-nutritive sweeteners in water and diet soda. Nutr. Metab., 13, 2016, 71, 10.1186/s12986-016-0129-3.
79. Temizkan, S., Deyneli, O., Yasar, M., Arpa, M., Gunes, M., Yazici, D., Sirikci, O., Haklar, G., Imeryuz, N., Yavuz, D.G., Sucralose enhances GLP-1 release and lowers blood glucose in the presence of carbohydrate in healthy subjects but not in patients with type 2 diabetes. Eur. J. Clin. Nutr. 69 (2015), 162–166.
80. Anton, S.D., Martin, C.K., Han, H., Coulon, S., Cefalu, W.T., Geiselman, P., Williamson, D.A., Effects of stevia, aspartame, and sucrose on food intake, satiety, and postprandial glucose and insulin levels. Appetite 55 (2010), 37–43, 10.1016/j.appet.2010.03.009.
81. Woods, S.C., The eating paradox: how we tolerate food. Psychol. Rev. 98 (1991), 488–505.
82. Woods, S.C., Schwartz, M.W., Baskin, D.G., Seeley, R.J., Food intake and the regulation of body weight. Annu. Rev. Psychol. 51 (2000), 255–277, 10.1146/annurev.psych.51.1.255.
83. 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, 10.1038/ejcn.2014.19.
84. Mezitis, N.H., Maggio, C.A., Koch, P., Quddoos, A., Allison, D.B., Pi-Sunyer, F.X., Glycemic effect of a single high oral dose of the novel sweetener sucralose in patients with diabetes. Diabetes Care 19 (1996), 1004–1005.
85. Kyriazis, G.A., Soundarapandian, M.M., Tyrberg, B., Sweet taste receptor signaling in beta cells mediates fructose-induced potentiation of glucose-stimulated insulin secretion. Proc. Natl. Acad. Sci. 109 (2012), E524–E532, 10.1073/pnas.1115183109.
86. Vahl, T.P., Drazen, D.L., Seeley, R.J., D'Alessio, D.A., Woods, S.C., Meal-anticipatory glucagon-like peptide-1 secretion in rats. Endocrinology 151 (2010), 569–575, 10.1210/en.2009-1002.
87. Drazen, D.L., Vahl, T.P., D'Alessio, D.A., Seeley, R.J., Woods, S.C., Effects of a fixed meal pattern on ghrelin secretion: evidence for a learned response independent of nutrient status. Endocrinology 147 (2006), 23–30, 10.1210/en.2005-0973.
88. Frecka, J.M., Mattes, R.D., Possible entrainment of ghrelin to habitual meal patterns in humans. Am. J. Physiol. Gastrointest. Liver Physiol. 294 (2008), G699–707, 10.1152/ajpgi.00448.2007.
89. Woods, S.C., Vasselli, J.R., Kaestner, E., Szakmary, G.A., Milburn, P., Vitiello, M.V., Conditioned insulin secretion and meal feeding in rats. J. Comp. Physiol. Psychol. 91 (1977), 128–133.
90. Woods, S.C., Ramsay, D.S., Pavlovian influences over food and drug intake. Behav. Brain Res. 110 (2000), 175–182.
91. Strubbe, J.H., Steffens, A.B., Rapid insulin release after ingestion of a meal in the unanesthetized rat. Am. J. Phys. 229 (1975), 1019–1022.
92. Takai, S., Yasumatsu, K., Inoue, M., Iwata, S., Yoshida, R., Shigemura, N., Yanagawa, Y., Drucker, D.J., Margolskee, R.F., Ninomiya, Y., Glucagon-like peptide-1 is specifically involved in sweet taste transmission. FASEB J. Off. Publ. Fed. Am. Soc. Exp. Biol. 29 (2015), 2268–2280, 10.1096/fj.14-265355.
93. Wise, P.M., Nattress, L., Flammer, L.J., Beauchamp, G.K., Reduced dietary intake of simple sugars alters perceived sweet taste intensity but not perceived pleasantness. Am. J. Clin. Nutr. 103 (2016), 50–60, 10.3945/ajcn.115.112300.
94. Griffioen-Roose, S., Smeets, P.A.M., Weijzen, P.L.G., van Rijn, I., van den Bosch, I., de Graaf, C., Effect of replacing sugar with non-caloric sweeteners in beverages on the reward value after repeated exposure. PLoS One, 8, 2013, e81924, 10.1371/journal.pone.0081924.
95. Storlien, L.H., Bruce, D.G., Mind over metabolism: the cephalic phase in relation to non-insulin-dependent diabetes and obesity. Biol. Psychol. 28 (1989), 3–23, 10.1016/0301-0511(89)90108-7.
96. Tordoff, M.G., How do non-nutritive sweeteners increase food intake?. Appetite 11:Suppl. 1 (1988), 5–11.
97. Renwick, A.G., Molinary, S.V., Sweet-taste receptors, low-energy sweeteners, glucose absorption and insulin release. Br. J. Nutr. 104 (2010), 1415–1420, 10.1017/S0007114510002540.
98. Rogers, P.J., Hogenkamp, P.S., de Graaf, C., Higgs, S., Lluch, A., Ness, A.R., Penfold, C., Perry, R., Putz, P., Yeomans, M.R., Mela, D.J., Does low-energy sweetener consumption affect energy intake and body weight? A systematic review, including meta-analyses, of the evidence from human and animal studies. Int. J. Obes. 40 (2016), 381–394, 10.1038/ijo.2015.177.