Brain activity and connectivity changes in response to nutritive natural sugars, non-nutritive natural sugar replacements and artificial sweeteners

References

• Morton GJ, Cummings DE, Baskin DG, Barsh GS, Schwartz MW. Central nervous system control of food intake and body weight. Nature. 2006;443(7109):289–95.
   PubMed Web of Science ®Google Scholar
• Volkow ND, Wise RA, Baler R. The dopamine motive system: implications for drug and food addiction. Nat Rev Neurosci. 2017;18(12):741–52.
   PubMed Web of Science ®Google Scholar
• Volkow ND, Wang GJ, Baler RD. Reward, dopamine and the control of food intake: implications for obesity. Trends Cogn Sci. 2011;15(1):37–46.
   PubMed Web of Science ®Google Scholar
• Carreiro AL, Dhillon J, Gordon S, Higgins KA, Jacobs AG, McArthur BM, et al. The macronutrients, Appetite, and energy intake. Annu Rev Nutr. 2016;36:73–103.
   PubMed Web of Science ®Google Scholar
• Tulloch AJ, Murray S, Vaicekonyte R, Avena NM. Neural responses to macronutrients: hedonic and homeostatic mechanisms. Gastroenterology. 2015;148(6):1205–18.
   PubMed Web of Science ®Google Scholar
• Imamura F, O'Connor L, Ye Z, Mursu J, Hayashino Y, Bhupathiraju SN, et al. Consumption of sugar sweetened beverages, artificially sweetened beverages, and fruit juice and incidence of type 2 diabetes: systematic review, meta-analysis, and estimation of population attributable fraction. Br J Sports Med. 2016;50(8):496–504.
   PubMed Web of Science ®Google Scholar
• Kit BK, Fakhouri TH, Park S, Nielsen SJ, Ogden CL. Trends in sugar-sweetened beverage consumption among youth and adults in the United States: 1999–2010. Am J Clin Nutr. 2013;98(1):180–8.
   PubMed Web of Science ®Google Scholar
• Malik VS, Schulze MB, Hu FB. Intake of sugar-sweetened beverages and weight gain: a systematic review. Am J Clin Nutr. 2006;84(2):274–88.
   PubMed Web of Science ®Google Scholar
• Steinert RE, Frey F, Topfer A, Drewe J, Beglinger C. Effects of carbohydrate sugars and artificial sweeteners on appetite and the secretion of gastrointestinal satiety peptides. Br J Nutr. 2011;105(9):1320–8.
   PubMed Web of Science ®Google Scholar
• Mergenthaler P, Lindauer U, Dienel GA, Meisel A. Sugar for the brain: the role of glucose in physiological and pathological brain function. Trends Neurosci. 2013;36(10):587–97.
   PubMed Web of Science ®Google Scholar
• Grayson BE, Seeley RJ, Sandoval DA. Wired on sugar: the role of the CNS in the regulation of glucose homeostasis. Nat Rev Neurosci. 2013;14(1):24–37.
   PubMed Web of Science ®Google Scholar
• Galgani J, Ravussin E. Energy metabolism, fuel selection and body weight regulation. Int J Obesity. 2008;32(Suppl 7):S109–19.
   Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Smeets PA, Vidarsdottir S, de Graaf C, Stafleu A, van Osch MJ, Viergever MA, et al. Oral glucose intake inhibits hypothalamic neuronal activity more effectively than glucose infusion. Am J Physiol Endocrinol Metab. 2007;293(3):E754–E8.
   PubMed Web of Science ®Google Scholar
• van Opstal AM, vdB-H AA, Hoeksma M, Blonk C, Pijl H, Rombouts SARB, et al. The effect of consumption temperature on the homeostatic and hedonic responses to glucose ingestion in the hypothalamus and the reward system. Am J Clin Nutr. 2018;107(1):20–5.
   PubMed Web of Science ®Google Scholar
• van Opstal AM, Hafkemeijer A, van den Berg-Huysmans AA, Hoeksma M, Blonk C, Pijl H, et al. Brain activity and connectivity changes in response to glucose ingestion. Nutr Neurosci. 2018 May 27:1–8.
   Web of Science ®Google Scholar
• van Opstal AM, Kaal I, van den Berg-Huysmans AA, Hoeksma M, Blonk C, Pijl H, et al. Dietary sugars and non-caloric sweeteners elicit different homeostatic and hedonic responses in the brain. Nutrition. 2019 April;60:80–86.
   PubMed Web of Science ®Google Scholar
• Barinaga M. Neuroscience: what makes brain neurons run? Science. 1997;276(5310):196–8.
   PubMed Web of Science ®Google Scholar
• Grill HJ, Berridge KC, Ganster DJ. Oral glucose is the prime elicitor of preabsorptive insulin secretion. Am J Physiol. 1984;246(1 Pt 2):R88–R95.
   PubMedGoogle Scholar
• Lam CK, Chari M, Lam TK. CNS regulation of glucose homeostasis. Physiology (Bethesda). 2009;24:159–70.
   PubMed Web of Science ®Google Scholar
• Ulrich M, Endres F, Kolle M, Adolph O, Widenhorn-Muller K, Gron G. Glucose modulates food-related salience coding of midbrain neurons in humans. Hum Brain Mapp. 2017;16(1):55.
   Google Scholar
• Lohner S, Toews I, Meerpohl JJ. Health outcomes of non-nutritive sweeteners: analysis of the research landscape. Nutr J. 2017;16:55.
   PubMed Web of Science ®Google Scholar
• Tappy L, Le KA. Metabolic effects of fructose and the worldwide increase in obesity. Physiol Rev. 2010;90(1):23–46.
   PubMed Web of Science ®Google Scholar
• Page KA, Chan O, Arora J, Belfort-Deaguiar R, Dzuira J, Roehmholdt B, et al. Effects of fructose vs glucose on regional cerebral blood flow in brain regions involved with appetite and reward pathways. JAMA. 2013;309(1):63–70.
   PubMed Web of Science ®Google Scholar
• Purnell JQ, Fair DA. Fructose ingestion and cerebral, metabolic, and satiety responses. JAMA. 2013;309(1):85–6.
   PubMed Web of Science ®Google Scholar
• Rogers PJ, Hogenkamp PS, de Graaf C, Higgs S, Lluch A, Ness AR, et al. 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 (Lond). 2016;40(3):381–94.
   PubMed Web of Science ®Google Scholar
• Swithers SE. Artificial sweeteners produce the counterintuitive effect of inducing metabolic derangements. Trends Endocrinol Metab. 2013;24(9):431–41.
   PubMed Web of Science ®Google Scholar
• Fantino M, Fantino A, Matray M, Mistretta F. Beverages containing low energy sweeteners do not differ from water in their effects on appetite, energy intake and food choices in healthy, non-obese French adults. Appetite. 2018;125:557–65.
   PubMed Web of Science ®Google Scholar
• Oshima H, Kimura I, Izumori K. Psicose contents in various food products and its origin. Food Sci Technol Res. 2006;12(2):137–43.
   Web of Science ®Google Scholar
• Sclafani A, Zukerman S, Ackroff K. Postoral glucose sensing, not caloric content, determines sugar reward in C57BL/6J mice. Chem Senses. 2015;40(4):245–58.
   PubMed Web of Science ®Google Scholar
• Noronha JC, Braunstein CR, Glenn AJ, Khan TA, Viguiliouk E, Noseworthy R, et al. The effect of small doses of fructose and allulose on postprandial glucose metabolism in type 2 diabetes: A double-blind, randomized, controlled, acute feeding, equivalence trial. Diabetes Obes Metab. 2018;20(10):2361–70.
   PubMed Web of Science ®Google Scholar
• Chung MY, Oh DK, Lee KW. Hypoglycemic health benefits of D-psicose. J Agric Food Chem. 2012;60(4):863–9.
   PubMed Web of Science ®Google Scholar
• Morton GJ, Meek TH, Schwartz MW. Neurobiology of food intake in health and disease. Nat Rev Neurosci. 2014;15(6):367–78.
   PubMed Web of Science ®Google Scholar
• Forster BB, MacKay AL, Whittall KP, Kiehl KA, Smith AM, Hare RD, et al. Functional magnetic resonance imaging: the basics of blood-oxygen-level dependent (BOLD) imaging. Can Assoc Radiol J. 1998;49(5):320–9.
   PubMed Web of Science ®Google Scholar
• Smeets PA, de Graaf C, Stafleu A, van Osch MJ, van der Grond J. Functional magnetic resonance imaging of human hypothalamic responses to sweet taste and calories. Am J Clin Nutr. 2005;82(5):1011–6.
   PubMed Web of Science ®Google Scholar
• Vidarsdottir S, Smeets PA, Eichelsheim DL, van Osch MJ, Viergever MA, Romijn JA, et al. Glucose ingestion fails to inhibit hypothalamic neuronal activity in patients with type 2 diabetes. Diabetes. 2007;56(10):2547–50.
   PubMed Web of Science ®Google Scholar
• Rombouts SA, Scheltens P, Kuijer JP, Barkhof F. Whole brain analysis of T2* weighted baseline FMRI signal in dementia. Hum Brain Mapp. 2007;28(12):1313–7.
   PubMed Web of Science ®Google Scholar
• Beckmann CF, DeLuca M, Devlin JT, Smith SM. Investigations into resting-state connectivity using independent component analysis. Philos Trans R Soc Lond B Biol Sci. 2005;360(1457):1001–13.
   PubMed Web of Science ®Google Scholar
• Tregellas JR, Wylie KP, Rojas DC, Tanabe J, Martin J, Kronberg E, et al. Altered default network activity in obesity. Obesity (Silver Spring, Md). 2011;19(12):2316–21.
   PubMed Web of Science ®Google Scholar
• Kullmann S, Heni M, Veit R, Ketterer C, Schick F, Haring HU, et al. The obese brain: association of body mass index and insulin sensitivity with resting state network functional connectivity. Hum Brain Mapp. 2012;33(5):1052–61.
   PubMed Web of Science ®Google Scholar
• Garcia-Garcia I, Jurado MA, Garolera M, Segura B, Sala-Llonch R, Marques-Iturria I, et al. Alterations of the salience network in obesity: a resting-state fMRI study. Hum Brain Mapp. 2013;34(11):2786–97.
   PubMed Web of Science ®Google Scholar
• Seeley WW, Menon V, Schatzberg AF, Keller J, Glover GH, Kenna H, et al. Dissociable intrinsic connectivity networks for salience processing and executive control. J Neurosci. 2007;27(9):2349–56.
   PubMed Web of Science ®Google Scholar
• Bolo NR, Musen G, Simonson DC, Nickerson LD, Flores VL, Siracusa T, et al. Functional connectivity of insula, basal ganglia, and prefrontal executive control networks during Hypoglycemia in type 1 diabetes. J Neurosci. 2015;35(31):11012–23.
   PubMed Web of Science ®Google Scholar
• Lohmann G, Margulies DS, Horstmann A, Pleger B, Lepsien J, Goldhahn D, et al. Eigenvector centrality mapping for analyzing connectivity patterns in fMRI data of the human brain. PLoS One. 2010;5(4):e10232.
   PubMed Web of Science ®Google Scholar
• Wink AM, de Munck JC, van der Werf YD, van den Heuvel OA, Barkhof F. Fast eigenvector centrality mapping of voxel-wise connectivity in functional magnetic resonance imaging: implementation, validation, and interpretation. Brain Connect. 2012;2(5):265–74.
   PubMedGoogle Scholar
• Jenkinson M, Beckmann CF, Behrens TE, Woolrich MW, Smith SM. FSL. Neuroimage. 2012;62(2):782–90.
   PubMed Web of Science ®Google Scholar
• Smith SM, Nichols TE. Threshold-free cluster enhancement: addressing problems of smoothing, threshold dependence and localisation in cluster inference. Neuroimage. 2009;44(1):83–98.
   PubMed Web of Science ®Google Scholar
• Pruim RH, Mennes M, van Rooij D, Llera A, Buitelaar JK, Beckmann CF. ICA-AROMA: a robust ICA-based strategy for removing motion artifacts from fMRI data. Neuroimage. 2015;112:267–77.
   PubMed Web of Science ®Google Scholar
• Pruim RH, Mennes M, Buitelaar JK, Beckmann CF. Evaluation of ICA-AROMA and alternative strategies for motion artifact removal in resting state fMRI. Neuroimage. 2015;112:278–87.
   PubMed Web of Science ®Google Scholar
• Trivedi BP. Neuroscience: dissecting appetite. Nature. 2014;508(7496):S64–S5.
   PubMed Web of Science ®Google Scholar
• 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(9):1181–9.
   PubMed Web of Science ®Google Scholar
• Uddin LQ. Salience processing and insular cortical function and dysfunction. Nat Rev Neurosci. 2015;16(1):55–61.
   PubMed Web of Science ®Google Scholar
• Menon V, Uddin LQ. Saliency, switching, attention and control: a network model of insula function. Brain Struct Funct. 2010;214(5):655–67.
   PubMed Web of Science ®Google Scholar
• de Araujo IE, Lin T, Veldhuizen MG, Small DM. Metabolic regulation of brain response to food cues. Current Biology: CB. 2013;23(10):878–83.
   PubMed Web of Science ®Google Scholar
• Purnell JQ, Klopfenstein BA, Stevens AA, Havel PJ, Adams SH, Dunn TN, et al. Brain functional magnetic resonance imaging response to glucose and fructose infusions in humans. Diabetes Obes Metab. 2011;13(3):229–34.
   PubMed Web of Science ®Google Scholar
• Theytaz F, de Giorgi S, Hodson L, Stefanoni N, Rey V, Schneiter P, et al. Metabolic fate of fructose ingested with and without glucose in a mixed meal. Nutrients. 2014;6(7):2632–49.
   PubMed Web of Science ®Google Scholar
• Veldhuizen MG, Babbs RK, Patel B, Fobbs W, Kroemer NB, Garcia E, et al. Integration of sweet taste and metabolism Determines carbohydrate reward. Curr Biol. 2017;27(16):2476–85. e6.
   PubMed Web of Science ®Google Scholar
• Davidson TL, Martin AA, Clark K, Swithers SE. Intake of high-intensity sweeteners alters the ability of sweet taste to signal caloric consequences: implications for the learned control of energy and body weight regulation. Q J Exp Psychol (Hove. 2011;64(7):1430–41.
   PubMed Web of Science ®Google Scholar
• Davidson TL, Swithers SE. A Pavlovian approach to the problem of obesity. Int J Obes Relat Metab Disord. 2004;28(7):933–5.
   PubMed Web of Science ®Google Scholar
• Swithers SE, Davidson TL. A role for sweet taste: calorie predictive relations in energy regulation by rats. Behav Neurosci. 2008;122(1):161–73.
   PubMed Web of Science ®Google Scholar
• Fowler SP. Low-calorie sweetener use and energy balance: results from experimental studies in animals, and large-scale prospective studies in humans. Physiol Behav. 2016;164(Pt B):517–23.
   PubMedGoogle Scholar
• Magnan C, Levin BE, Luquet S. Brain lipid sensing and the neural control of energy balance. Mol Cell Endocrinol. 2015;418(Pt 1):3–8.
   PubMedGoogle Scholar
• DiFeliceantonio AG, Coppin G, Rigoux L, Edwin Thanarajah S, Dagher A, Tittgemeyer M, et al. Supra-additive effects of combining fat and carbohydrate on food reward. Cell Metab. 2018;28(1):33–44. e3.
   PubMed Web of Science ®Google Scholar
• Führer D, Zysset S, Stumvoll M. Brain activity in hunger and satiety: an exploratory visually stimulated fMRI study. Obesity. 2008;16(5):945–50.
   PubMed Web of Science ®Google Scholar
• Varlamov O, Bethea CL, Roberts CT Jr. Sex-specific differences in lipid and glucose metabolism. Front Endocrinol (Lausanne). 2014;5:241.
   PubMed Web of Science ®Google Scholar