Accessible Requires Authentication Published by De Gruyter January 24, 2020

Food reward and gut-brain signalling

Sharmili Edwin Thanarajah and Marc Tittgemeyer
From the journal Neuroforum

Abstract

The increasing availability of ultra-processed, energy dense food is contributing to the spread of the obesity pandemic, which is a serious health threat in today’s world. One possible cause for this association arises from the fact that the brain is wired to derive pleasure from eating. Specifically, food intake activates reward pathways involving dopamine receptor signalling. The reinforcing value of specific food items results from the interplay between taste and nutritional properties. Increasing evidence suggests that nutritional value is sensed in the gut by chemoreceptors in the intestinal tract and the hepatic portal vein, and conveyed to the brain through neuronal and endocrine pathways to guide food selection behaviour. Ultra-processed food is designed to potentiate the reward response through a combination of high fat and high sugar, therebye seeming highly appetizing. There is increasing evidence that overconsumption of processed food distorts normal reward signalling, leading to compulsive eating behaviour and obesity. Hence, it is essential to understand food reward and gut-brain signalling to find an effective strategy to combat the obesity pandemic.

Zusammenfassung

Zur Sicherstellung eines ausgeglichenen Energiehaushalts des Körpers wirkt Essen als primärer Belohnungsreiz. Daher haben Nahrungsmittel einen starken Einfluss auf das Belohnungssystem im Gehirn. Wenn wir essen, wird im Gehirn der Botenstoff Dopamin frei gesetzt. Wie belohnend wir Lebensmittel finden hängt dabei sowohl vom Geschmack als auch vom Nährwert ab. Jüngste Forschungsergebnisse belegen, dass unser Magen-Darm-Trakt im engen Austausch mit dem Gehirn steht und Informationen über den Nährwert an das Gehirn übermittelt. Auf diese Weise kontrollieren Signale aus dem Magen-Darm-Trakt unser Verlangen nach Essen. Industriell verarbeitete Lebensmittel sind so konzipiert, dass sie besonders appetitanregend wirken; außerdem zeichnen sie sich durch einen hohen Kaloriengehalt aus. Fertiggerichte veranlassen Menschen damit offenbar, mehr zu essen als sie benötigen. Die zugrundeliegenden Mechanismen hierfür sind bislang noch nicht hinreichend verstanden. Allerdings ist davon auszugehen, dass hierbei die Vermittlung sensorischer Informationen zwischen Magen-Darm-Trakt und Gehirn eine tragende Rolle spielt. Aktuellen Studienergebnissen zu Folge kommt es bei übermäßigem Verzehr von Fertigprodukten zu anhaltenden Veränderungen im Belohnungssystem. Diese begünstigen ein impulsives Essverhalten und können dadurch zu Übergewicht führen. Das Verständnis dieser Prozesse ist daher grundlegend, um eine wirksame Strategie zur Bekämpfung der Adipositas-Pandemie zu entwickeln.

References

Araujo, I. E. de, Oliveira-Maia, A.J., Sotnikova, T.D., Gainetdinov, R.R., Caron, M.G., Nicolelis, M.A.L., and Simon, S. A. (2008). Food Reward in the Absence of Taste Receptor Signaling. Neuron. 57, 930–941. Search in Google Scholar

Araujo, I. E. de, Ren, X., and Ferreira, J.G. (2011). Metabolic Sensing in Brain Dopamine Systems. Results Probl. Cell Differ. 52, 69–86. Search in Google Scholar

Araujo, I. E. de, Lin, T., Veldhuizen, M.G., and Small, D.M. (2013). Metabolic Regulation of Brain Response to Food Cues. Curr. Biol. 23, 878–883. Search in Google Scholar

Bloemendaal, L. van, IJzerman, R.G., Ten Kulve, J.S., Barkhof, F., Konrad, R.J., Drent, M.L., Veltman, D.J., and Diamant, M. (2014). GLP-1 receptor activation modulates appetite- and reward-related brain areas in humans. Diabetes. 63, 4186–4196. Search in Google Scholar

Cryan, J.F., and Dinan, T.G. (2012). Mind-altering microorganisms: the impact of the gut microbiota on brain and behaviour. Nat. Rev. Neurosci. 13, 701–712. Search in Google Scholar

Cryan, J.F., O’Riordan, K.J., Cowan, C.S.M., Sandhu, K.V., Bastiaanssen, T.F.S., Boehme, … Dinan T.G. (2019). The Microbiota-Gut-Brain Axis. Physiol. Rev. 99, 1877–2013. Search in Google Scholar

Dickson, S. L., Shirazi, R.H., Hansson, C., Bergquist, F., Nissbrandt, H., and Skibicka, K.P. (2012). The Glucagon-Like Peptide 1 (GLP-1) Analogue, Exendin-4, Decreases the Rewarding Value of Food: A New Role for Mesolimbic GLP-1 Receptors. J. Neurosci. 32, 4812–4820. Search in Google Scholar

DiFeliceantonio, A.G., and Small, D.M. (2019). Dopamine and diet-induced obesity. Nat. Neurosci. 22, 1–2. Search in Google Scholar

DiFeliceantonio, A.G., Coppin, G., Rigoux, L., Edwin Thanarajah, S., Dagher, A., Tittgemeyer, M., and Small, D.M. (2018). Supra-Additive Effects of Combining Fat and Carbohydrate on Food Reward. Cell Metab. 28, 33–44.e3. Search in Google Scholar

Edwin Thanarajah, S., Iglesias, S., Kuzmanovic, B., Rigoux, L., Stephan, K.E., Brüning, J.C., and Tittgemeyer, M. (2019). Modulation of midbrain neurocircuitry by intranasal insulin. NeuroImage. 194, 120–127. Search in Google Scholar

Ferreira, J.G., Tellez, L.A., Ren, X., Yeckel, C.W., and Araujo, I. E. de (2012). Regulation of fat intake in the absence of flavour signalling. J. Physiol. 590, 953–972. Search in Google Scholar

Fletcher, P.C., and Kenny, P.J. (2018). Food addiction: a valid concept? Neuropsychopharmacology. 43, 2506–2513. Search in Google Scholar

Fowler, S.P., Williams, K., Resendez, R.G., Hunt, K.J., Hazuda, H.P., and Stern, M.P. (2008). Fueling the Obesity Epidemic? Artificially Sweetened Beverage Use and Long-term Weight Gain. Obesity. 16, 1894–1900. Search in Google Scholar

Fürnsinn, C. (2015). Die moderne Adipositasepidemie vor dem Hintergrund physiologischer Regulation und biologischer Evolution. J. Klin. Endokrinol. Stoffwechsel. 8, 101–105. Search in Google Scholar

Giessen, E. van de, Fleur, S.E. la, Eggels, L., Bruin, K. de, Brink, W. van den, and Booij, J. (2013). High fat/carbohydrate ratio but not total energy intake induces lower striatal dopamine D2/3 receptor availability in diet-induced obesity. Int. J. Obes. 37, 754–757. Search in Google Scholar

Gosby, A.K., Conigrave, A. D., Raubenheimer, D., and Simpson, S.J. (2014). Protein leverage and energy intake. Obes. Rev. 15, 183–191. Search in Google Scholar

Hajnal, A., Smith, G.P., and Norgren, R. (2004). Oral sucrose stimulation increases accumbens dopamine in the rat. Am. J. Physiol. Regul. Integr. Comp. Physiol. 286, R31–R37. Search in Google Scholar

Hall, K.D., Ayuketah, A., Brychta, R., Cai, H., Cassimatis, T., Chen, K.Y., … Zhou, M. (2019). Ultra-Processed Diets Cause Excess Calorie Intake and Weight Gain: An Inpatient Randomized Controlled Trial of Ad Libitum Food Intake. Cell Metab. 30, 67–77.e3. Search in Google Scholar

Han, W., Tellez, L.A., Perkins, M.H., Perez, I.O., Qu, T., Ferreira, J., … de Araujo, I. E. (2018). A Neural Circuit for Gut-Induced Reward. Cell 175, 665–678.e23. Search in Google Scholar

Hoebel, B.G. (1985). Brain neurotransmitters in food and drug reward. Am. J. Clin. Nutr. 42, 1133–1150. Search in Google Scholar

Johnson, P.M., and Kenny, P.J. (2010). Dopamine D2 receptors in addiction-like reward dysfunction and compulsive eating in obese rats. Nat. Neurosci. 13, 635–641. Search in Google Scholar

Kim, K.-S., Seeley, R.J., and Sandoval, D.A. (2018). Signalling from the periphery to the brain that regulates energy homeostasis. Nat. Rev. Neurosci. 19, 185–196. Search in Google Scholar

Lavin, J., French, S., and Read, N.W. (1997). The effect of sucrose-and aspartame-sweetened drinks on energy intake, hunger and food choice of female, moderately restrained eaters. Int. J. Obes. Relat. Metab. Disord. 21, 37–42. Search in Google Scholar

Liang, J., and Krashes, M.J. (2017). AgRP Accountants Compute Caloric Cost. Cell Rep. 21, 2647–2648. Search in Google Scholar

Lippert, R.N., Cremer, A.L., Edwin Thanarajah, S., Korn, C., Jahans-Price, T., Burgeno, L.M., … Backes, H. (2019). Time-dependent assessment of stimulus-evoked regional dopamine release. Nat. Commun. 10, 336. Search in Google Scholar

Lutsey, P.L., Steffen, L.M., and Stevens, J. (2008). Dietary intake and development of the metabolic syndrome: The atherosclerosis risk in communities study. Circulation. 117, 754–761. Search in Google Scholar

McCutcheon, J.E., Beeler, J.A., and Roitman, M.F. (2012). Sucrose-predictive cues evoke greater phasic dopamine release than saccharin-predictive cues. Synapse. 66, 346–351. Search in Google Scholar

Palmiter, R.D. (2007). Is dopamine a physiologically relevant mediator of feeding behavior? Trends Neurosci. 30, 375–381. Search in Google Scholar

Pepino, M.Y. (2015). Metabolic effects of non-nutritive sweeteners. Physiol. Behav. 152, 450–455. Search in Google Scholar

Prentice, A.M., Goldberg, G.R., Jebb, S. A., Black, A.E., Murgatroyd, P.R., and Diaz, E.O. (1991). Physiological responses to slimming. Proc. Nutr. Soc. 50, 441–458. Search in Google Scholar

Qu, T., Han, W., Niu, J., Tong, J., and Araujo, I. E. de (2019). On the roles of the Duodenum and the Vagus nerve in learned nutrient preferences. Appetite. 139, 145–151. Search in Google Scholar

Ritter, S., and Taylor, J.S. (1990). Vagal sensory neurons are required for lipoprivic but not glucoprivic feeding in rats. Am. J. Physiol. Regul. Integr. Comp. Physiol. 258, R1395–R1401. Search in Google Scholar

Rogers, P.J., and Blundell, J.E. (1989). Separating the actions of sweetness and calories: effects of saccharin and carbohydrates on hunger and food intake in human subjects. Physiol. Behav. 45, 1093–9. Search in Google Scholar

Schneider, L.H. (1989). Orosensory Self‐Stimulation by Sucrose Involves Brain Dopaminergic Mechanisms. Ann. N. Y. Acad. Sci. 575, 307–320. Search in Google Scholar

Schultz, W. (2016). Dopamine reward prediction-error signalling: a two-component response. Nat. Rev. Neurosci. 17, 183–195. Search in Google Scholar

Schwartz, M.W., Woods, S.C., Porte, D., Seeley, R.J., and Baskin, D.G. (2000). Central nervous system control of food intake. Nature. 404, 661–671. Search in Google Scholar

Sclafani, A., and Ackroff, K. (2012). Role of gut nutrient sensing in stimulating appetite and conditioning food preferences. Am. J. Physiol. Regul. Integr. Comp. Physiol. 302, R1119–R1133. Search in Google Scholar

Simpson, S.J., and Raubenheimer, D. (2005). Obesity: the protein leverage hypothesis. Obes. Rev. 6, 133–42. Search in Google Scholar

Skibicka, K.P., Hansson, C., Egecioglu, E., and Dickson, S. L. (2012). Role of ghrelin in food reward: impact of ghrelin on sucrose self-administration and mesolimbic dopamine and acetylcholine receptor gene expression. Addict. Biol. 17, 95–107. Search in Google Scholar

Small, D.M., Jones-Gotman, M., and Dagher, A. (2003). Feeding-induced dopamine release in dorsal striatum correlates with meal pleasantness ratings in healthy human volunteers. NeuroImage. 19, 1709–1715. Search in Google Scholar

Smith, G.P. (2004). Accumbens dopamine mediates the rewarding effect of orosensory stimulation by sucrose. Appetite. 43, 11–13. Search in Google Scholar

Steiner, J.E., Glaser, D., Hawilo, M. E., and Berridge, K.C. (2001). Comparative expression of hedonic impact: affective reactions to taste by human infants and other primates. Neurosci. Biobehav. Rev. 25, 53–74. Search in Google Scholar

Stellman, S. D., and Garfinkel, L. (1988). Patterns of artificial sweetener use and weight change in an American Cancer Society prospective study. Appetite. 11, 85–91. Search in Google Scholar

Stice, E., Spoor, S., Bohon, C., and Small, D.M. (2008). Relation between obesity and blunted striatal response to food is moderated by TaqIA A1 allele. Science. 322, 449–452. Search in Google Scholar

Stouffer, M.A., Woods, C.A., Patel, J.C., Lee, C.R., Witkovsky, P., Bao, L., … Rice, M. E. (2015). Insulin enhances striatal dopamine release by activating cholinergic interneurons and thereby signals reward. Nat. Commun. 6, 8543. Search in Google Scholar

Sun, X., Luquet, S., and Small, D.M. (2017). DRD2: Bridging the Genome and Ingestive Behavior. Trends Cognit. Sci. 21, 372–384. Search in Google Scholar

Swinburn, B., Sacks, G., and Ravussin, E. (2009). Increased food energy supply is more than sufficient to explain the US epidemic of obesity. Am. J. Clin. Nutr. 90, 1453–1456. Search in Google Scholar

Swithers, S.E., Sample, C.H., and Davidson, T.L. (2013). Adverse effects of high-intensity sweeteners on energy intake and weight control in male and obesity-prone female rats. Behav. Neurosci. 127, 262–274. Search in Google Scholar

Szczypka, M.S., Kwok, K., Brot, M.D., Marck, B.T., Matsumoto, A.M., Donahue, B.A., and Palmiter, R.D. (2001). Dopamine production in the caudate putamen restores feeding in dopamine-deficient mice. Neuron. 30, 819–828. Search in Google Scholar

Taber, M.T., and Fibiger, H.C. (1997). Activation of the mesocortical dopamine system by feeding: lack of a selective response to stress. Neuroscience. 77, 295–298. Search in Google Scholar

Tang, D.W., Fellows, L.K., and Dagher, A. (2014). Behavioral and neural valuation of foods is driven by implicit knowledge of caloric content. Psychol. Sci. 25, 2168–2176. Search in Google Scholar

Tellez, L.A., Medina, S., Han, W., Ferreira, J.G., Licona-Limon, P., Ren, X., … Araujo, I. E. de (2013). A Gut Lipid Messenger Links Excess Dietary Fat to Dopamine Deficiency. Science. 341, 800–802. Search in Google Scholar

Thanarajah, S.E., Backes, H., DiFeliceantonio, A.G., Albus, K., Cremer, A.L., Hanssen, R., … Tittgemeyer, M. (2019). Food Intake Recruits Orosensory and Post-ingestive Dopaminergic Circuits to Affect Eating Desire in Humans. Cell Metab. 29, 695–706.e4. Search in Google Scholar

Tiedemann, L.J., Schmid, S.M., Hettel, J., Giesen, K., Francke, P., Büchel, C., and Brassen, S. (2017). Central insulin modulates food valuation via mesolimbic pathways. Nat. Commun. 8, 16052. Search in Google Scholar

Tordoff, M.G., and Alleva, M.A. (1990). Oral stimulation with aspartame increases hunger. Physiol. Behav. 47, 555–559. Search in Google Scholar

Veldhuizen, M.G., Babbs, R.K., Patel, B., Fobbs, W., Kroemer, N.B., Garcia, E., Yeomans, M.R., and Small, D.M. (2017). Integration of Sweet Taste and Metabolism Determines Carbohydrate Reward. Curr. Biol. 27, 2476–2485.e6. Search in Google Scholar

Volkow, N.D., and Wise, R.A. (2005). How can drug addiction help us understand obesity? Nat. Neurosci. 8, 555–560. Search in Google Scholar

Wang, G.J., Volkow, N.D., Logan, J., Pappas, N.R., Wong, C.T., Zhu, W., Netusil, N., and Fowler, J.S. (2001). Brain dopamine and obesity. Lancet. 357, 354–357. Search in Google Scholar

Warren, C.M., Tona, K.D., Ouwerkerk, L., Paridon, J. van, Poletiek, F., Steenbergen, H. van, Bosch, J.A., and Nieuwenhuis, S. (2019). The neuromodulatory and hormonal effects of transcutaneous vagus nerve stimulation as evidenced by salivary alpha amylase, salivary cortisol, pupil diameter, and the P3 event-related potential. Brain Stimul. 12, 635–642. Search in Google Scholar

World Health Organization. (2000). Obesity: preventing and managing the global epidemic. Report of a WHO Consultation (WHO Technical Report Series 894). Search in Google Scholar

Yeomans, M.R., Leitch, M., Gould, N.J., and Mobini, S. (2008). Differential hedonic, sensory and behavioral changes associated with flavor–nutrient and flavor–flavor learning. Physiol. Behav. 93, 798–806. Search in Google Scholar

Zhang, L., Han, W., Lin, C., Li, F., and Araujo, I. E. de (2018). Sugar Metabolism Regulates Flavor Preferences and Portal Glucose Sensing. Front. Integr. Neurosci. 12, 57. Search in Google Scholar

Zhou, Q.Y., and Palmiter, R.D. (1995). Dopamine-deficient mice are severely hypoactive, adipsic, and aphagic. Cell. 83, 1197–1209. Search in Google Scholar

Published Online: 2020-01-24
Published in Print: 2020-02-25

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