Skip to main content
SpringerLink
Log in
Book cover

Sensory and Metabolic Control of Energy Balance pp 69–86Cite as

Metabolic Sensing in Brain Dopamine Systems

  • Chapter
  • First Online:

Part of the book series: Results and Problems in Cell Differentiation ((RESULTS,volume 52))

Abstract

The gustatory system allows the brain to monitor the presence of chemicals in the oral cavity and initiate appropriate responses of acceptance or rejection. Among such chemicals are the nutrients that must be rapidly recognized and ingested for immediate oxidation or storage. In the periphery, the gustatory system consists of a highly efficient sensing mechanism, where distinct cell types express receptors that bind specifically to chemicals associated with one particular taste quality. These specialized receptors connect to the brain via dedicated pathways, the stimulation of which triggers stereotypic behavioral responses as well as neurotransmitter release in brain reward dopamine systems. However, evidence also exists in favor of the concept that the critical regulators of long-term nutrient choice are physiological processes taking place after ingestion and independently of gustation. We will appraise the hypothesis that organisms can develop preferences for nutrients independently of oral taste stimulation. Of particular interest are recent findings indicating that disrupting nutrient utilization interferes with activity in brain dopamine pathways. These findings establish the metabolic fate of nutrients as previously unanticipated reward signals that regulate the reinforcing value of foods. In particular, it suggests a role for brain dopamine reward systems as metabolic sensors, allowing for signals generated by the metabolic utilization of nutrients to regulate neurotransmitter release and food reinforcement.

This is a preview of subscription content, log in via an institution.

Chapter
USD   29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD   129.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD   169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD   169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Learn about institutional subscriptions

References

  • Ackoff K (2009) Learned flavor preferences. The variable potency of post-oral nutrient reinforcers. Appetite 51:743–746

    Article  Google Scholar 

  • Ackroff K, Sclafani A, Axen KV (1997) Diabetic rats prefer glucose-paired flavors over fructose-paired flavors. Appetite 28:73–83

    Article  PubMed  CAS  Google Scholar 

  • Adler E, Hoon MA, Mueller KL, Chrandrashekar J, Ryba NJP, Zucker CS (2000) A novel family of mammalian taste receptors. Cell 100:693–702

    Article  PubMed  CAS  Google Scholar 

  • Andrews ZB, Erion D, Beiler R, Liu ZW, Abizaid A, Zigman J, Elsworth JD, Savitt JM, DiMarchi R, Tschoep M, Roth RH, Gao XB, Horvath TL (2009) Ghrelin promotes and protects nigrostriatal dopamine function via a UCP2-dependent mitochondrial mechanism. J Neurosci 29:14057–14065

    Google Scholar 

  • Bailey CS, Hsiao S, King JE (1986) Hedonic reactivity to sucrose in rats: modification by pimozide. Physiol Behav 38:447–452

    Article  PubMed  CAS  Google Scholar 

  • Baldo BA, Alsene KM, Negron A, Kelley AE (2005) Hyperphagia induced by GABAA receptor-mediated inhibition of the nucleus accumbens shell: dependence on intact neural output from the central amygdaloid region. Behav Neurosci 119:1195–1206

    Article  PubMed  CAS  Google Scholar 

  • Bermudez-Rattoni F (2004) Molecular mechanisms of taste-recognition memory. Nat Rev Neurosci 5:209–217

    Article  PubMed  CAS  Google Scholar 

  • Bezençon C, le Coutre J, Damak S (2007) Taste-signaling proteins are coexpressed in solitary intestinal epithelial cells. Chem Senses 32:41–49

    Article  PubMed  Google Scholar 

  • Bufe B, Breslin PAS, Kuhn C, Reed DR, Tharp CD, Slack JP, Kim UK, Drayna D, Meyerhof W (2005) The molecular basis of individual differences in phenylthiocarbamide and propylthiouracil bitterness perception. Curr Biol 15:322–327

    Article  PubMed  CAS  Google Scholar 

  • Chandrashekar J, Kuhn C, Oka Y, Yarmolinsky DA, Hummler E, Ryba NJ, Zuker CS (2010) The cells and peripheral representation of sodium taste in mice. Nature 464:297–301

    Article  PubMed  CAS  Google Scholar 

  • Chrandrashekar J, Mueller KL, Hoon MA, Adler E, Feng L, Guo W, Zucker CS, Ryba NJP (2000) T2Rs function as bitter taste receptors. Cell 100:703–711

    Article  Google Scholar 

  • Danilova V, Danilov Y, Roberts T, Hellekant G (2002) Sense of taste of the common marmoset: recordings from the chorda tympani and glossopharyngeal nerves. J Neurophys 88:579–594

    Google Scholar 

  • de Araujo IE, Oliveira-Maia AJ, Sotnikova TD, Gainetdinov RR, Caron MG, Nicolelis MA, Simon SA (2008) Food reward in the absence of taste receptor signaling. Neuron 57:930–941

    Article  PubMed  Google Scholar 

  • Di Chiara G, Bassareo V (2007) Reward system and addiction: what dopamine does and doesn’t do. Curr Opin Pharmacol 7:69–76

    Article  PubMed  Google Scholar 

  • Figlewicz DP (2003) Insulin, food intake, and reward. Semin Clin Neuropsychiatry 8:82–93

    Article  PubMed  Google Scholar 

  • Figlewicz DP, Evans SB, Murphy J, Hoen M, Baskin DG (2003) Expression of receptors for insulin and leptin in the ventral tegmental area/substantia nigra (VTA/SN) of the rat. Brain Res 964:107–115

    Article  PubMed  CAS  Google Scholar 

  • Figlewicz DP, Bennett JL, Naleid AM, Davis C, Grimm JW (2006) Intraventricular insulin and leptin decrease sucrose self-administration in rats. Physiol Behav 89:611–616

    Article  PubMed  CAS  Google Scholar 

  • Finger TE, Simon SA (2002) The cell biology of lingual epithelia. In: Finger TF, Silver WL, Restrepo D (eds) The Neurobiology of Taste and Smell, Wiley-Liss, New York, pp. 287–314

    Google Scholar 

  • Fulton S, Pissios P, Manchon RP, Stiles L, Frank L, Pothos EN, Maratos-Flier E, Flier JS (2006) Leptin regulation of the mesoaccumbens dopamine pathway. Neuron 51:811–822

    Article  PubMed  CAS  Google Scholar 

  • Ganchrow JR, Steiner JE, Daher M (1983) Neonatal facial expressions in response to different qualities and intensities of gustatory stimuli. Infant Behav Dev 6:473–484

    Article  Google Scholar 

  • Geary N, Smith GP (1985) Pimozide decreases the positive reinforcing effect of sham fed sucrose in the rat. Pharmacol Biochem Behav 22:787–790

    Article  PubMed  CAS  Google Scholar 

  • Hajnal A, Smith GP, Norgren R (2004) Oral sucrose stimulation increases accumbens dopamine in the rat. Am J Physiol Regul Integr Comp Physiol 286:R31–R37

    Article  PubMed  CAS  Google Scholar 

  • Hall WG, Bryan TE (1981) The ontogeny of feeding in rats: IV. Taste development as measured by intake and behavioral responses to oral infusions of sucrose and quinine. J Comp Physiol Psychol 95:240–251

    Article  PubMed  CAS  Google Scholar 

  • Hamilton RB, Norgren R (1984) Central projections of gustatory nerves in the rat. J Comp Neurol 222:560–577

    Article  PubMed  CAS  Google Scholar 

  • Hanamori T, Miller IJ Jr, Smith DV (1988) Gustatory responsiveness of fibers in the hamster glossopharyngeal nerve. J Neurophysiol 60:478–498

    PubMed  CAS  Google Scholar 

  • Hernandez L, Hoebel BG (1988) Food reward and cocaine increase extracellular dopamine in the nucleus accumbens as measured by microdialysis. Life Sci 42:1705–1712

    Article  PubMed  CAS  Google Scholar 

  • Hofer D, Puschel B, Drenckhahn D (1996) Taste receptor-like cells in the rat gut identified by expression of alpha-gustducin. Proc Natl Acad Sci USA 93:6631–6634

    Article  PubMed  CAS  Google Scholar 

  • Hommel JD, Trinko R, Sears RM, Georgescu D, Liu ZW, Gao XB, Thurmon JJ, Marinelli M, DiLeone RJ (2006) Leptin receptor signaling in midbrain dopamine neurons regulates feeding. Neuron 51:801–810

    Article  PubMed  CAS  Google Scholar 

  • Houpt KA, Houpt TR, Pond WG (1977) Food intake controls in the suckling pig: glucoprivation and gastrointestinal factors. Am J Physiol 232:E510–514

    PubMed  CAS  Google Scholar 

  • Huang L, Shanker YG, Dubauskaite J, Zheng JZ, Yan W, Rosenzweig S, Spielman AI, Max M, Margolskee RF (1999) Ggamma13 colocalizes with gustducin in taste receptor cells and mediates IP3 responses to bitter denatonium. Nat Neurosci 2:1055–1062

    Article  PubMed  CAS  Google Scholar 

  • Huang AL, Chen X, Hoon MA, Chandrashekar J, Guo W, Trankner D, Ryba NJ, Zuker CS (2006) The cells and logic for mammalian sour taste detection. Nature 442:934–938

    Article  PubMed  CAS  Google Scholar 

  • Ishimaru Y, Inada H, Kubota M, Zhuang H, Tominaga M, Matsunami H (2006) Transient receptor potential family members PKD1L3 and PKD2L1 form a candidate sour taste receptor. Proc Natl Acad Sci U S A 103:12569–12574

    Article  PubMed  CAS  Google Scholar 

  • Kare MR (1971) Comparative study of taste. In: Beidler LM (ed) Handbook of sensory physiology. Springer, Berlin, pp 278–292

    Google Scholar 

  • Kellenberger S, Schild L (2002) Epithelial sodium channel/degenerin family of ion channels: a variety of functions for a shared structure. Physiol Rev 82:735–767

    PubMed  CAS  Google Scholar 

  • Kelley AE, Schiltz CA, Landry CF (2005) Neural systems recruited by drug- and food-related cues: studies of gene activation in corticolimbic regions. Physiol Behav 86:11–14

    Article  PubMed  CAS  Google Scholar 

  • Kretz O, Barbry P, Bock R, Lindemann B (1999) Differential expression of RNA and protein of the three pore-forming subunits of the amiloride-sensitive epithelial sodium channel in taste buds of the rat. J Histochem Cytochem 47:51–64

    Article  PubMed  CAS  Google Scholar 

  • Li CS, Cho YK, Smith DV (2005) Modulation of parabrachial taste neurons by electrical and chemical stimulation of the lateral hypothalamus and amygdala. J Neurophys 93:1183–1196

    Article  Google Scholar 

  • Liu D, Liman ER (2003) Intracellular Ca2+ and the phospholipid PIP2 regulate the taste transduction ion channel TRPM5. Proc Natl Acad Sci U S A 100:15160–15165

    Article  PubMed  CAS  Google Scholar 

  • LopezJimenez ND, Cavenagh MM, Sainz E, Cruz-Ithier MA, Battey JF, Sullivan SL (2006) Two members of the TRPP family of ion channels, Pkd1l3 and Pkd2l1, are co-expressed in a subset of taste receptor cells. J Neurochem 98:68–77

    Article  PubMed  CAS  Google Scholar 

  • Margolskee RF, Dyer J, Kokrashvili Z, Salmon KS, Ilegems E, Daly K, Maillet EL, Ninomiya Y, Mosinger B, Shirazi-Beechey SP (2007) T1R3 and gustducin in gut sense sugars to regulate expression of Na+-glucose cotransporter 1. Proc Natl Acad Sci U S A 104(38):15075–15080

    Article  PubMed  CAS  Google Scholar 

  • Maruyama Y, Pereira E, Margolskee RF, Chaudhari N, Roper SD (2006) Umami responses in mouse taste cells indicate more than one receptor. J Neurosci 26:2227–2234

    Article  PubMed  CAS  Google Scholar 

  • Max M, Shankar G, Huang L, Rong M, Liu Z, Campagne F, Weinstein H, Damak S, Margolskee RF (2001) Tas1r3, encoding a new candidate taste receptor, is allelic to the sweet responsiveness locus. Sac Nat Gen 28:58–63

    CAS  Google Scholar 

  • McLaughlin SK, McKinnon PJ, Margolskee RF (1992) Gustducin is a taste-cell specific G protein closely related to transducins. Nature 357:563–569

    Article  PubMed  CAS  Google Scholar 

  • Montmayeur JP, Liberlis SD, Matsunami H, Buck L (2001) A candidate taste receptor gene near a sweet taste locus. Nat Neurosci 4:492–498

    PubMed  CAS  Google Scholar 

  • Mueller KL, Hoon MA, Erlenbach I, Chandrashekar J, Zuker CS, Ryba NJP (2005) The receptors and coding logic for bitter taste. Nature 434:225–229

    Article  PubMed  CAS  Google Scholar 

  • Nelson G, Hoon MA, Chandrashekar J, Ryba NJP, Zuker CS (2001) Mammalian sweet taste receptors. Cell 106:381–390

    Article  PubMed  CAS  Google Scholar 

  • Nelson G, Chandrashekar J, Hoon MA, Feng L, Zhao G, Ryba NJP, Zucker CS (2002) An amino-acid taste receptor. Nature 726:1–4

    Google Scholar 

  • Norgren R (1976) Taste pathways to hypothalamus and amygdala. J Comp Neurol 166:17–30

    Article  PubMed  CAS  Google Scholar 

  • Norgren R, Hajnal A (2005) Taste pathways that mediate accumbens dopamine release by sapid sucrose. Physiol Behav 84:363–369

    Article  PubMed  Google Scholar 

  • Norgren R, Leonard CM (1971) Taste pathways in rat brainstem. Science 173:1136–1139

    Article  PubMed  CAS  Google Scholar 

  • Norgren R, Leonard CM (1973) Ascending central gustatory pathways. J Comp Neurol 150:217–238

    Article  PubMed  CAS  Google Scholar 

  • Norgren R, Pfaffmann C (1975) The pontine taste area in the rat. Brain Res 91:99–117

    Article  PubMed  CAS  Google Scholar 

  • Norgren R, Wolf G (1975) Projections of thalamic gustatory and lingual areas in the rat. Brain Res 92:123–129

    Article  PubMed  CAS  Google Scholar 

  • Norgren R, Hajnal A, Mungarndee SS (2006) Gustatory reward and the nucleus accumbens. Physiol Behav 89:531–535

    Article  PubMed  CAS  Google Scholar 

  • Pardini AW, Nguyen HT, Figlewicz DP, Baskin DG, Williams DL, Kim F, Schwartz MW (2006) Distribution of insulin receptor substrate-2 in brain areas involved in energy homeostasis. Brain Res 1112:169–178

    Article  PubMed  CAS  Google Scholar 

  • Pellerin L, Bouzier-sore AK, Aubert S, Serres S, Merle M, Costalat R, Magistretti PJ (2007) Activity-dependent regulation of energy metabolism by astrocytes: an update. Glia 55:1251–1262

    Article  PubMed  Google Scholar 

  • Perez CA, Huang L, Rong M, Kozak JA, Preuss AK, Zhang H, Max M, Margolskee RF (2002) A transient receptor potential channel expressed in taste receptor cells. Nat Neurosci 5:1169–1176

    Article  PubMed  CAS  Google Scholar 

  • Perez CA, Margolskee RF, Kinnamon SC, Ogura T (2003) Making sense with TRP channels: store-operated calcium entry and the ion channel Trpm5 in taste receptor cells. Cell Calcium 33:541–549

    Article  PubMed  CAS  Google Scholar 

  • Ren X, Ferreira JG, Zhou L, Shammah-Lagnado SJ, Yeckel CW, De Araujo IE (2010) Nutrient selection in the absence of taste receptor signaling. J Neurosci 30:8012–8023

    Google Scholar 

  • Rong M, He W, Yasumatsu K, Kokrashvili Z, Perez CA, Mosinger B, Ninomiya Y, Margolskee RF, Damak S (2005) Signal transduction of umami taste: insights from knockout mice. Chem Sens 30:i33–i34

    Article  CAS  Google Scholar 

  • Sclafani A, Lucas F (1996) Abdominal vagotomy does not block carbohydrate-conditioned flavor preferences in rats. Physiol Behav 60:447–453

    Article  PubMed  CAS  Google Scholar 

  • Sclafani A, Vigorito M (1987) Effects of SOA and saccharin adulteration on polycose preference in rats. Neurosci Biobehav Rev 11:163–168

    Article  PubMed  CAS  Google Scholar 

  • Sclafani A, Xenakis S (1984) Sucrose and polysaccharide induced obesity in the rat. Physiol Behav 32:169–174

    Article  PubMed  CAS  Google Scholar 

  • Sclafani A, Zukerman S, Glendinning JI, Margolskee RF (2007) Fat and carbohydrate preferences in mice: the contribution of {alpha}-Gustducin and Trpm5 taste signaling proteins. Am J Physiol Regul Integr Comp Physiol 293:R1504–R1513

    Article  PubMed  CAS  Google Scholar 

  • Scott TR, Verhagen JV (2000) Taste as a factor in the management of nutrition. Nutrition 16:874–885

    Article  PubMed  CAS  Google Scholar 

  • Small DM, Jones-Gotman M, Dagher A (2003) Feeding-induced dopamine release in dorsal striatum correlates with meal pleasantness ratings in healthy human volunteers. Neuroimage 19:1709–1715

    Article  PubMed  Google Scholar 

  • Snowdon CT, Epstein A (1970) Oral and intragastric feeding in vagotomized rats. J Comp Physiol Psychol 71:59–67

    Article  PubMed  CAS  Google Scholar 

  • Sotak BN, Hnasko TS, Robinson S, Kremer EJ, Palmiter RD (2005) Dysregulation of dopamine signaling in the dorsal striatum inhibits feeding. Brain Res 1061:88–96

    Article  PubMed  CAS  Google Scholar 

  • Spector AC, Travers SP (2005) The representation of taste quality in the mammalian nervous system. Behav Cogn Neurosci Rev 4:143–191

    Article  PubMed  Google Scholar 

  • Swithers SE, Davidson TL (2008) A role for sweet taste: calorie predictive relations in energy regulation by rats. Behav Neurosci 122:161–173

    Article  PubMed  Google Scholar 

  • Touzani K, Bodnar R, Sclafani A (2008) Activation of dopamine D1-like receptors in nucleus accumbens is critical for the acquisition, but not the expression, of nutrient-conditioned flavor preferences in rats. Eur J Neurosci 27:1525–1533

    Article  PubMed  Google Scholar 

  • Travagli RA, Hermann GE, Browning KN, Rogers RC (2006) Brainstem circuits regulating gastric function. Annu Rev Physiol 68:279–305

    Article  PubMed  CAS  Google Scholar 

  • Tsang YC (1938) Hunger motivation in gastrectomized rats. J Comp Physiol Psychol 26:1–17

    Article  Google Scholar 

  • Tschop M, Smiley DL, Heiman ML (2000) Ghrelin induces adiposity in rodents. Nature 407:908–913

    Article  PubMed  CAS  Google Scholar 

  • Wise RA (2006) Role of brain dopamine in food reward and reinforcement. Philos Trans R Soc Lond B Biol Sci 361:1149–1158

    Article  PubMed  CAS  Google Scholar 

  • Xenakis S, Sclafani A (1981) The effects of pimozide on the consumption of a palatable saccharin–glucose solution in the rat. Pharmacol Biochem Behav 15:435–442

    Article  PubMed  CAS  Google Scholar 

  • Zhang Y, Hoon MA, Chandrashekar J, Mueller KL, Cook BWD, Zucker CS, Ryba NJ (2003) Coding of sweet, bitter, and umami tastes: different receptor cells sharing similar signaling pathways. Cell 112:293–301

    Article  PubMed  CAS  Google Scholar 

  • Zhao GQ, Zhang Y, Hoon MA, Chandrashekar J, Erienbach I, Ryba NJP, Zuker CS (2003) The receptors for mammalian sweet and umami taste. Cell 115:255–266

    Article  PubMed  CAS  Google Scholar 

  • Zukerman S, Touzani K, Margolskee R, Sclafani A (2009) Role of olfaction in the conditioned sucrose preference of sweet-ageusic T1R3 knockout mice. Chem Sens 35:685–694

    Article  Google Scholar 

Download references

Acknowledgments

We thank Prof Dietmar Richter for editorial assistance and Theddy Gonçalves for Fig.1.

Author information

Authors and Affiliations

  1. The John B Pierce Laboratory and Department of Psychiatry, Yale University School of Medicine, 290 Congress Avenue, New Haven, CT, 06519, USA

    Ivan E. de Araujo, Xueying Ren & Jozélia G. Ferreira

Authors
  1. Ivan E. de Araujo
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Xueying Ren
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jozélia G. Ferreira
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Ivan E. de Araujo .

Editor information

Editors and Affiliations

  1. Potsdam-Rehbrücke (DIFE), Abt. Molekulare Genetik, Deutsches Institut für Ernährungsforschu, Arthur-Scheunert-Allee 114-116, Nuthetal, 14558, Brandenburg, Germany

    Wolfgang Meyerhof

  2. Martinistr. 52, Hamburg, 20246, Germany

    Ulrike Beisiegel

  3. German Institute of Human Nutrition Pots, Arthur-Scheunert-Allee 114-116, Nuthetal, 14558, Germany

    Hans-Georg Joost

Rights and permissions

Reprints and permissions

Copyright information

© 2011 Springer Berlin Heidelberg

About this chapter

Cite this chapter

de Araujo, I.E., Ren, X., Ferreira, J.G. (2011). Metabolic Sensing in Brain Dopamine Systems. In: Meyerhof, W., Beisiegel, U., Joost, HG. (eds) Sensory and Metabolic Control of Energy Balance. Results and Problems in Cell Differentiation, vol 52. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-14426-4_7

Download citation

Publish with us

Policies and ethics

Search

Navigation