A subset of broadly responsive Type III taste cells contribute to the detection of bitter, sweet and umami stimuli

Autoři: Debarghya Dutta Banik aff001;  Eric D. Benfey aff001;  Laura E. Martin aff002;  Kristen E. Kay aff002;  Gregory C. Loney aff002;  Amy R. Nelson aff001;  Zachary C. Ahart aff001;  Barrett T. Kemp aff001;  Bailey R. Kemp aff001;  Ann-Marie Torregrossa aff002;  Kathryn F. Medler aff001
Působiště autorů: Department of Biological Sciences, University at Buffalo, Buffalo, New York, United States of America aff001;  Department of Psychology, University at Buffalo, Buffalo, New York, United States of America aff002;  Center for Ingestive Behavior Research, University at Buffalo, Buffalo, New York, United States of America aff003
Vyšlo v časopise: A subset of broadly responsive Type III taste cells contribute to the detection of bitter, sweet and umami stimuli. PLoS Genet 16(8): e32767. doi:10.1371/journal.pgen.1008925
Kategorie: Research Article
doi: 10.1371/journal.pgen.1008925


Taste receptor cells use multiple signaling pathways to detect chemicals in potential food items. These cells are functionally grouped into different types: Type I cells act as support cells and have glial-like properties; Type II cells detect bitter, sweet, and umami taste stimuli; and Type III cells detect sour and salty stimuli. We have identified a new population of taste cells that are broadly tuned to multiple taste stimuli including bitter, sweet, sour, and umami. The goal of this study was to characterize these broadly responsive (BR) taste cells. We used an IP3R3-KO mouse (does not release calcium (Ca2+) from internal stores in Type II cells when stimulated with bitter, sweet, or umami stimuli) to characterize the BR cells without any potentially confounding input from Type II cells. Using live cell Ca2+ imaging in isolated taste cells from the IP3R3-KO mouse, we found that BR cells are a subset of Type III cells that respond to sour stimuli but also use a PLCβ signaling pathway to respond to bitter, sweet, and umami stimuli. Unlike Type II cells, individual BR cells are broadly tuned and respond to multiple stimuli across different taste modalities. Live cell imaging in a PLCβ3-KO mouse confirmed that BR cells use this signaling pathway to respond to bitter, sweet, and umami stimuli. Short term behavioral assays revealed that BR cells make significant contributions to taste driven behaviors and found that loss of either PLCβ3 in BR cells or IP3R3 in Type II cells caused similar behavioral deficits to bitter, sweet, and umami stimuli. Analysis of c-Fos activity in the nucleus of the solitary tract (NTS) also demonstrated that functional Type II and BR cells are required for normal stimulus induced expression.

Klíčová slova:

Animal behavior – Behavior – Citric acid – Mice – Neurons – Taste – Taste buds – Gustatory system


1. Finger TE. Cell types and lineages in taste buds. Chem Senses. 2005;30 Suppl 1:i54–5. doi: 10.1093/chemse/bjh110 15738192.

2. Lawton DM, Furness DN, Lindemann B, Hackney CM. Localization of the glutamate-aspartate transporter, GLAST, in rat taste buds. Eur J Neurosci. 2000;12(9):3163–71. doi: 10.1046/j.1460-9568.2000.00207.x 10998100.

3. Miyoshi MA, Abe K, Emori Y. IP(3) receptor type 3 and PLCbeta2 are co-expressed with taste receptors T1R and T2R in rat taste bud cells. Chem Senses. 2001;26(3):259–65. doi: 10.1093/chemse/26.3.259 11287386.

4. Zhang Y, Hoon MA, Chandrashekar J, Mueller KL, Cook B, Wu D, et al. Coding of sweet, bitter, and umami tastes: different receptor cells sharing similar signaling pathways. Cell. 2003;112(3):293–301. doi: 10.1016/s0092-8674(03)00071-0 12581520.

5. Yan W, Sunavala G, Rosenzweig S, Dasso M, Brand JG, Spielman AI. Bitter taste transduced by PLC-beta(2)-dependent rise in IP(3) and alpha-gustducin-dependent fall in cyclic nucleotides. Am J Physiol Cell Physiol. 2001;280(4):C742–51. doi: 10.1152/ajpcell.2001.280.4.C742 11245589.

6. Dutta Banik D, Martin LE, Freichel M, Torregrossa AM, Medler KF. TRPM4 and TRPM5 are both required for normal signaling in taste receptor cells. Proc Natl Acad Sci U S A. 2018;115(4):E772–E81. doi: 10.1073/pnas.1718802115 29311301.

7. Taruno A, Vingtdeux V, Ohmoto M, Ma Z, Dvoryanchikov G, Li A, et al. CALHM1 ion channel mediates purinergic neurotransmission of sweet, bitter and umami tastes. Nature. 2013;495(7440):223–6. doi: 10.1038/nature11906 23467090; PubMed Central PMCID: PMC3600154.

8. Liu D, Liman ER. Intracellular Ca2+ and the phospholipid PIP2 regulate the taste transduction ion channel TRPM5. Proc Natl Acad Sci U S A. 2003;100(25):15160–5. doi: 10.1073/pnas.2334159100 14657398.

9. Zhang Z, Zhao Z, Margolskee R, Liman E. The transduction channel TRPM5 is gated by intracellular calcium in taste cells. J Neurosci. 2007;27(21):5777–86. Epub 2007/05/25. 27/21/5777 [pii] doi: 10.1523/JNEUROSCI.4973-06.2007 17522321.

10. Perez CA, Huang L, Rong M, Kozak JA, Preuss AK, Zhang H, et al. A transient receptor potential channel expressed in taste receptor cells. Nat Neurosci. 2002;5(11):1169–76. doi: 10.1038/nn952 12368808.

11. Clapp TR, Yang R, Stoick CL, Kinnamon SC, Kinnamon JC. Morphologic characterization of rat taste receptor cells that express components of the phospholipase C signaling pathway. J Comp Neurol. 2004;468(3):311–21. doi: 10.1002/cne.10963 14681927.

12. Yee CL, Yang R, Bottger B, Finger TE, Kinnamon JC. "Type III" cells of rat taste buds: immunohistochemical and ultrastructural studies of neuron-specific enolase, protein gene product 9.5, and serotonin. J Comp Neurol. 2001;440(1):97–108. Epub 2001/12/18. doi: 10.1002/cne.1372 [pii]. 11745610.

13. Simon SA, de Araujo IE, Gutierrez R, Nicolelis MA. The neural mechanisms of gustation: a distributed processing code. Nat Rev Neurosci. 2006;7(11):890–901. doi: 10.1038/nrn2006 17053812.

14. Roper SD. Signal transduction and information processing in mammalian taste buds. Pflugers Arch. 2007;454(5):759–76. doi: 10.1007/s00424-007-0247-x 17468883.

15. Clapp TR, Medler KF, Damak S, Margolskee RF, Kinnamon SC. Mouse taste cells with G protein-coupled taste receptors lack voltage-gated calcium channels and SNAP-25. BMC Biol. 2006;4:7. doi: 10.1186/1741-7007-4-7 16573824.

16. Chang RB, Waters H, Liman ER. A proton current drives action potentials in genetically identified sour taste cells. Proc Natl Acad Sci U S A. 2010;107(51):22320–5. doi: 10.1073/pnas.1013664107 21098668; PubMed Central PMCID: PMC3009759.

17. Ye W, Chang RB, Bushman JD, Tu YH, Mulhall EM, Wilson CE, et al. The K+ channel KIR2.1 functions in tandem with proton influx to mediate sour taste transduction. Proc Natl Acad Sci U S A. 2016;113(2):E229–38. doi: 10.1073/pnas.1514282112 26627720; PubMed Central PMCID: PMC4720319.

18. Lewandowski BC, Sukumaran SK, Margolskee RF, Bachmanov AA. Amiloride-Insensitive Salt Taste Is Mediated by Two Populations of Type III Taste Cells with Distinct Transduction Mechanisms. J Neurosci. 2016;36(6):1942–53. doi: 10.1523/JNEUROSCI.2947-15.2016 26865617; PubMed Central PMCID: PMC4748077.

19. Huang YA, Maruyama Y, Stimac R, Roper SD. Presynaptic (Type III) cells in mouse taste buds sense sour (acid) taste. J Physiol. 2008;586(12):2903–12. doi: 10.1113/jphysiol.2008.151233 18420705; PubMed Central PMCID: PMC2517205.

20. Huang AL, Chen X, Hoon MA, Chandrashekar J, Guo W, Trankner D, et al. The cells and logic for mammalian sour taste detection. Nature. 2006;442(7105):934–8. doi: 10.1038/nature05084 16929298; PubMed Central PMCID: PMC1571047.

21. Kataoka S, Yang R, Ishimaru Y, Matsunami H, Sevigny J, Kinnamon JC, et al. The candidate sour taste receptor, PKD2L1, is expressed by type III taste cells in the mouse. Chem Senses. 2008;33(3):243–54. doi: 10.1093/chemse/bjm083 18156604; PubMed Central PMCID: PMC2642677.

22. Oka Y, Butnaru M, von Buchholtz L, Ryba NJ, Zuker CS. High salt recruits aversive taste pathways. Nature. 2013;494(7438):472–5. Epub 2013/02/15. doi: 10.1038/nature11905 23407495; PubMed Central PMCID: PMC3587117.

23. Hacker K, Laskowski A, Feng L, Restrepo D, Medler K. Evidence for two populations of bitter responsive taste cells in mice. J Neurophysiol. 2008;99(3):1503–14. doi: 10.1152/jn.00892.2007 18199819.

24. Clapp TR, Stone LM, Margolskee RF, Kinnamon SC. Immunocytochemical evidence for co-expression of Type III IP3 receptor with signaling components of bitter taste transduction. BMC Neurosci. 2001;2:6. doi: 10.1186/1471-2202-2-6 11346454.

25. Hegg CC, Jia C, Chick WS, Restrepo D, Hansen A. Microvillous cells expressing IP3 receptor type 3 in the olfactory epithelium of mice. Eur J Neurosci. 2010;32(10):1632–45. doi: 10.1111/j.1460-9568.2010.07449.x 20958798; PubMed Central PMCID: PMC4331646.

26. Medler KF, Margolskee RF, Kinnamon SC. Electrophysiological characterization of voltage-gated currents in defined taste cell types of mice. J Neurosci. 2003;23(7):2608–17. doi: 10.1523/JNEUROSCI.23-07-02608.2003 12684446.

27. Sukumaran SK, Lewandowski BC, Qin Y, Kotha R, Bachmanov AA, Margolskee RF. Whole transcriptome profiling of taste bud cells. Scientific reports. 2017;7(1):7595. doi: 10.1038/s41598-017-07746-z 28790351; PubMed Central PMCID: PMC5548921.

28. DeFazio RA, Dvoryanchikov G, Maruyama Y, Kim JW, Pereira E, Roper SD, et al. Separate populations of receptor cells and presynaptic cells in mouse taste buds. J Neurosci. 2006;26(15):3971–80. doi: 10.1523/JNEUROSCI.0515-06.2006 16611813.

29. Richter TA, Caicedo A, Roper SD. Sour taste stimuli evoke Ca2+ and pH responses in mouse taste cells. J Physiol. 2003;547(Pt 2):475–83. doi: 10.1113/jphysiol.2002.033811 12562903.

30. Tomchik SM, Berg S, Kim JW, Chaudhari N, Roper SD. Breadth of tuning and taste coding in mammalian taste buds. J Neurosci. 2007;27(40):10840–8. Epub 2007/10/05. 27/40/10840 [pii] doi: 10.1523/JNEUROSCI.1863-07.2007 17913917.

31. Yoshida R, Miyauchi A, Yasuo T, Jyotaki M, Murata Y, Yasumatsu K, et al. Discrimination of taste qualities among mouse fungiform taste bud cells. J Physiol. 2009;587(Pt 18):4425–39. Epub 2009/07/23. jphysiol.2009.175075 [pii] doi: 10.1113/jphysiol.2009.175075 19622604; PubMed Central PMCID: PMC2766648.

32. Wilson CE, Finger TE, Kinnamon SC. Type III Cells in Anterior Taste Fields Are More Immunohistochemically Diverse Than Those of Posterior Taste Fields in Mice. Chem Senses. 2017;42(9):759–67. Epub 2017/10/03. doi: 10.1093/chemse/bjx055 28968659; PubMed Central PMCID: PMC5863558.

33. Shandilya J, Gao Y, Nayak TK, Roberts SG, Medler KF. AP1 transcription factors are required to maintain the peripheral taste system. Cell Death Dis. 2016;7(10):e2433. doi: 10.1038/cddis.2016.343 27787515; PubMed Central PMCID: PMC5133999.

34. Yang R, Crowley HH, Rock ME, Kinnamon JC. Taste cells with synapses in rat circumvallate papillae display SNAP-25-like immunoreactivity. J Comp Neurol. 2000;424(2):205–15. doi: 10.1002/1096-9861(20000821)424:2<205::aid-cne2>3.0.co;2-f 10906698.

35. Larson ED, Vandenbeuch A, Anderson CB, Kinnamon SC. Function, Innervation, and Neurotransmitter Signaling in Mice Lacking Type-II Taste Cells. eNeuro. 2020;7(1). Epub 2020/01/29. doi: 10.1523/ENEURO.0339-19.2020 31988217; PubMed Central PMCID: PMC7004487.

36. King CT, Garcea M, Spector AC. Glossopharyngeal nerve regeneration is essential for the complete recovery of quinine-stimulated oromotor rejection behaviors and central patterns of neuronal activity in the nucleus of the solitary tract in the rat. J Neurosci. 2000;20(22):8426–34. Epub 2000/11/09. doi: 10.1523/JNEUROSCI.20-22-08426.2000 11069950.

37. King CT, Travers SP, Rowland NE, Garcea M, Spector AC. Glossopharyngeal nerve transection eliminates quinine-stimulated fos-like immunoreactivity in the nucleus of the solitary tract: implications for a functional topography of gustatory nerve input in rats. J Neurosci. 1999;19(8):3107–21. Epub 1999/04/07. doi: 10.1523/JNEUROSCI.19-08-03107.1999 10191326.

38. Stratford JM, Finger TE. Central representation of postingestive chemosensory cues in mice that lack the ability to taste. J Neurosci. 2011;31(25):9101–10. Epub 2011/06/24. doi: 10.1523/JNEUROSCI.0404-11.2011 21697361; PubMed Central PMCID: PMC3131261.

39. Stratford JM, Thompson JA. MSG-Evoked c-Fos Activity in the Nucleus of the Solitary Tract Is Dependent upon Fluid Delivery and Stimulation Parameters. Chem Senses. 2016;41(3):211–20. Epub 2016/01/15. doi: 10.1093/chemse/bjv082 26762887; PubMed Central PMCID: PMC5006140.

40. Stratford JM, Thompson JA, Finger TE. Immunocytochemical organization and sour taste activation in the rostral nucleus of the solitary tract of mice. J Comp Neurol. 2017;525(2):271–90. Epub 2016/06/14. doi: 10.1002/cne.24059 27292295; PubMed Central PMCID: PMC5138149.

41. Hisatsune C, Yasumatsu K, Takahashi-Iwanaga H, Ogawa N, Kuroda Y, Yoshida R, et al. Abnormal Taste Perception in Mice Lacking the Type 3 Inositol 1,4,5-Trisphosphate Receptor. J Biol Chem. 2007;282(51):37225–31. doi: 10.1074/jbc.M705641200 17925404.

42. Xu J, Lewandowski BC, Miyazawa T, Shoji Y, Yee K, Bryant BP. Spilanthol Enhances Sensitivity to Sodium in Mouse Taste Bud Cells. Chem Senses. 2019;44(2):91–103. Epub 2018/10/27. doi: 10.1093/chemse/bjy069 30364996; PubMed Central PMCID: PMC6350677.

43. Kimura K, Beidler LM. Microelectrode study of taste receptors of rat and hamster. J Cell Comp Physiol. 1961;58:131–9. Epub 1961/10/01. doi: 10.1002/jcp.1030580204 14456037.

44. Sato T, Beidler LM. The response characteristics of rat taste cells to four basic taste stimuli. Comp Biochem Physiol A Comp Physiol. 1982;73(1):1–10. Epub 1982/01/01. doi: 10.1016/0300-9629(82)90083-4 6127183.

45. Sato T, Beidler LM. Broad tuning of rat taste cells for four basic taste stimuli. Chem Senses. 1997;22(3):287–93. Epub 1997/06/01. doi: 10.1093/chemse/22.3.287 9218141.

46. Tonosaki K, Funakoshi M. Intracellular taste cell responses of mouse. Comp Biochem Physiol A Comp Physiol. 1984;78(4):651–6. Epub 1984/01/01. doi: 10.1016/0300-9629(84)90611-x 6149038.

47. Ozeki M. Conductance change associated with receptor potentials of gustatory cells in rat. J Gen Physiol. 1971;58(6):688–99. Epub 1971/12/01. doi: 10.1085/jgp.58.6.688 5120394; PubMed Central PMCID: PMC2226050.

48. Ozeki M, Sato M. Responses of gustatory cells in the tongue of rat to stimuli representing four taste qualities. Comp Biochem Physiol A Comp Physiol. 1972;41(2):391–407. Epub 1972/02/01. doi: 10.1016/0300-9629(72)90070-9 4404316.

49. Caicedo A, Kim KN, Roper SD. Individual mouse taste cells respond to multiple chemical stimuli. J Physiol. 2002;544(Pt 2):501–9. doi: 10.1113/jphysiol.2002.027862 12381822.

50. Gilbertson TA, Boughter JD Jr., Zhang H, Smith DV. Distribution of gustatory sensitivities in rat taste cells: whole-cell responses to apical chemical stimulation. J Neurosci. 2001;21(13):4931–41. doi: 10.1523/JNEUROSCI.21-13-04931.2001 11425921.

51. Barretto RP, Gillis-Smith S, Chandrashekar J, Yarmolinsky DA, Schnitzer MJ, Ryba NJ, et al. The neural representation of taste quality at the periphery. Nature. 2015;517(7534):373–6. doi: 10.1038/nature13873 25383521; PubMed Central PMCID: PMC4297533.

52. Breza JM, Nikonov AA, Contreras RJ. Response latency to lingual taste stimulation distinguishes neuron types within the geniculate ganglion. J Neurophysiol. 2010;103(4):1771–84. doi: 10.1152/jn.00785.2009 20107132; PubMed Central PMCID: PMC2853290.

53. Frank ME, Lundy RF Jr., Contreras RJ. Cracking taste codes by tapping into sensory neuron impulse traffic. Prog Neurobiol. 2008;86(3):245–63. doi: 10.1016/j.pneurobio.2008.09.003 18824076; PubMed Central PMCID: PMC2680288.

54. Hellekant G, Danilova V, Ninomiya Y. Primate sense of taste: behavioral and single chorda tympani and glossopharyngeal nerve fiber recordings in the rhesus monkey, Macaca mulatta. J Neurophysiol. 1997;77(2):978–93. doi: 10.1152/jn.1997.77.2.978 9065862.

55. Wu A, Dvoryanchikov G, Pereira E, Chaudhari N, Roper SD. Breadth of tuning in taste afferent neurons varies with stimulus strength. Nat Commun. 2015;6:8171. doi: 10.1038/ncomms9171 26373451; PubMed Central PMCID: PMC4573454.

56. Zhang J, Jin H, Zhang W, Ding C, O'Keeffe S, Ye M, et al. Sour Sensing from the Tongue to the Brain. Cell. 2019;179(2):392–402 e15. Epub 2019/09/24. doi: 10.1016/j.cell.2019.08.031 31543264.

57. Lemon CH, Smith DV. Neural representation of bitter taste in the nucleus of the solitary tract. J Neurophysiol. 2005;94(6):3719–29. doi: 10.1152/jn.00700.2005 16107527.

58. Geran LC, Travers SP. Single neurons in the nucleus of the solitary tract respond selectively to bitter taste stimuli. J Neurophysiol. 2006;96(5):2513–27. doi: 10.1152/jn.00607.2006 16899635.

59. Carleton A, Accolla R, Simon SA. Coding in the mammalian gustatory system. Trends Neurosci. 2010;33(7):326–34. doi: 10.1016/j.tins.2010.04.002 20493563; PubMed Central PMCID: PMC2902637.

60. Samuelsen CL, Gardner MP, Fontanini A. Thalamic contribution to cortical processing of taste and expectation. J Neurosci. 2013;33(5):1815–27. doi: 10.1523/JNEUROSCI.4026-12.2013 23365221; PubMed Central PMCID: PMC3711560.

61. Fontanini A, Katz DB. State-dependent modulation of time-varying gustatory responses. J Neurophysiol. 2006;96(6):3183–93. doi: 10.1152/jn.00804.2006 16928791.

62. Katz DB, Simon SA, Nicolelis MA. Dynamic and multimodal responses of gustatory cortical neurons in awake rats. J Neurosci. 2001;21(12):4478–89. doi: 10.1523/JNEUROSCI.21-12-04478.2001 11404435.

63. Accolla R, Bathellier B, Petersen CC, Carleton A. Differential spatial representation of taste modalities in the rat gustatory cortex. J Neurosci. 2007;27(6):1396–404. doi: 10.1523/JNEUROSCI.5188-06.2007 17287514.

64. Zocchi D, Wennemuth G, Oka Y. The cellular mechanism for water detection in the mammalian taste system. Nat Neurosci. 2017;20(7):927–33. doi: 10.1038/nn.4575 28553944.

65. Tu YH, Cooper AJ, Teng B, Chang RB, Artiga DJ, Turner HN, et al. An evolutionarily conserved gene family encodes proton-selective ion channels. Science. 2018;359(6379):1047–50. Epub 2018/01/27. doi: 10.1126/science.aao3264 29371428; PubMed Central PMCID: PMC5845439.

66. Teng B, Wilson CE, Tu YH, Joshi NR, Kinnamon SC, Liman ER. Cellular and Neural Responses to Sour Stimuli Require the Proton Channel Otop1. Curr Biol. 2019;29(21):3647–56 e5. Epub 2019/09/24. doi: 10.1016/j.cub.2019.08.077 31543453.

67. Adler E, Hoon MA, Mueller KL, Chandrashekar J, Ryba NJ, Zuker CS. A novel family of mammalian taste receptors. Cell. 2000;100(6):693–702. doi: 10.1016/s0092-8674(00)80705-9 10761934.

68. Chandrashekar J, Hoon MA, Ryba NJ, Zuker CS. The receptors and cells for mammalian taste. Nature. 2006;444(7117):288–94. doi: 10.1038/nature05401 17108952.

69. Chandrashekar J, Mueller KL, Hoon MA, Adler E, Feng L, Guo W, et al. T2Rs function as bitter taste receptors. Cell. 2000;100(6):703–11. doi: 10.1016/s0092-8674(00)80706-0 10761935.

70. Nelson G, Chandrashekar J, Hoon MA, Feng L, Zhao G, Ryba NJ, et al. An amino-acid taste receptor. Nature. 2002;416(6877):199–202. doi: 10.1038/nature726 11894099.

71. Nelson G, Hoon MA, Chandrashekar J, Zhang Y, Ryba NJ, Zuker CS. Mammalian sweet taste receptors. Cell. 2001;106(3):381–90. doi: 10.1016/s0092-8674(01)00451-2 11509186.

72. Stone LM, Barrows J, Finger TE, Kinnamon SC. Expression of T1Rs and gustducin in palatal taste buds of mice. Chem Senses. 2007;32(3):255–62. doi: 10.1093/chemse/bjl053 17229761.

73. Yoshida R, Ninomiya Y. Taste information derived from T1R-expressing taste cells in mice. Biochem J. 2016;473(5):525–36. doi: 10.1042/BJ20151015 26912569.

74. Hoon MA, Adler E, Lindemeier J, Battey JF, Ryba NJ, Zuker CS. Putative mammalian taste receptors: a class of taste-specific GPCRs with distinct topographic selectivity. Cell. 1999;96(4):541–51. doi: 10.1016/s0092-8674(00)80658-3 10052456.

75. Kim MR, Kusakabe Y, Miura H, Shindo Y, Ninomiya Y, Hino A. Regional expression patterns of taste receptors and gustducin in the mouse tongue. Biochem Biophys Res Commun. 2003;312(2):500–6. doi: 10.1016/j.bbrc.2003.10.137 14637165.

76. Kusakabe Y, Kim MR, Miura H, Shindo Y, Ninomiya Y, Hino A. Regional expression patterns of T1r family in the mouse tongue. Chem Senses. 2005;30 Suppl 1:i23–4. Epub 2005/03/02. doi: 10.1093/chemse/bjh094 15738129.

77. Treesukosol Y, Blonde GD, Spector AC. T1R2 and T1R3 subunits are individually unnecessary for normal affective licking responses to Polycose: implications for saccharide taste receptors in mice. Am J Physiol Regul Integr Comp Physiol. 2009;296(4):R855–65. doi: 10.1152/ajpregu.90869.2008 19158407; PubMed Central PMCID: PMC2698609.

78. Treesukosol Y, Smith KR, Spector AC. Behavioral evidence for a glucose polymer taste receptor that is independent of the T1R2+3 heterodimer in a mouse model. J Neurosci. 2011;31(38):13527–34. doi: 10.1523/JNEUROSCI.2179-11.2011 21940444; PubMed Central PMCID: PMC3251913.

79. Treesukosol Y, Spector AC. Orosensory detection of sucrose, maltose, and glucose is severely impaired in mice lacking T1R2 or T1R3, but Polycose sensitivity remains relatively normal. Am J Physiol Regul Integr Comp Physiol. 2012;303(2):R218–35. doi: 10.1152/ajpregu.00089.2012 22621968; PubMed Central PMCID: PMC3404635.

80. Zukerman S, Glendinning JI, Margolskee RF, Sclafani A. T1R3 taste receptor is critical for sucrose but not Polycose taste. Am J Physiol Regul Integr Comp Physiol. 2009;296(4):R866–76. doi: 10.1152/ajpregu.90870.2008 19091911; PubMed Central PMCID: PMC2698610.

81. Kusuhara Y, Yoshida R, Ohkuri T, Yasumatsu K, Voigt A, Hubner S, et al. Taste responses in mice lacking taste receptor subunit T1R1. J Physiol. 2013;591(7):1967–85. doi: 10.1113/jphysiol.2012.236604 23339178; PubMed Central PMCID: PMC3624863.

82. Ohkuri T, Yasumatsu K, Horio N, Jyotaki M, Margolskee RF, Ninomiya Y. Multiple sweet receptors and transduction pathways revealed in knockout mice by temperature dependence and gurmarin sensitivity. Am J Physiol Regul Integr Comp Physiol. 2009;296(4):R960–71. doi: 10.1152/ajpregu.91018.2008 19211717.

83. Chaudhari N, Landin AM, Roper SD. A metabotropic glutamate receptor variant functions as a taste receptor. Nat Neurosci. 2000;3(2):113–9. doi: 10.1038/72053 10649565.

84. Chaudhari N, Maruyama Y, Roper S, Trubey K. Multiple pathways for signaling glutamate taste in rodents. Chem Senses. 2005;30 Suppl 1:i29-i30. doi: 10.1093/chemse/bjh097 15738162.

85. Chaudhari N, Pereira E, Roper SD. Taste receptors for umami: the case for multiple receptors. Am J Clin Nutr. 2009;90(3):738S–42S. Epub 2009/07/03. ajcn.2009.27462H [pii] doi: 10.3945/ajcn.2009.27462H 19571230.

86. Maruyama Y, Pereira E, Margolskee RF, Chaudhari N, Roper SD. Umami responses in mouse taste cells indicate more than one receptor. J Neurosci. 2006;26(8):2227–34. doi: 10.1523/JNEUROSCI.4329-05.2006 16495449.

87. Delay ER, Hernandez NP, Bromley K, Margolskee RF. Sucrose and monosodium glutamate taste thresholds and discrimination ability of T1R3 knockout mice. Chem Senses. 2006;31(4):351–7. doi: 10.1093/chemse/bjj039 16495435.

88. Eddy MC, Eschle BK, Delay ER. Comparison of the Tastes of L-Alanine and Monosodium Glutamate in C57BL/6J Wild Type and T1r3 Knockout Mice. Chem Senses. 2017;42(7):563–73. doi: 10.1093/chemse/bjx037 28605507.

89. Pal Choudhuri S, Delay RJ, Delay ER. L-Amino Acids Elicit Diverse Response Patterns in Taste Sensory Cells: A Role for Multiple Receptors. PLoS One. 2015;10(6):e0130088. doi: 10.1371/journal.pone.0130088 26110622; PubMed Central PMCID: PMC4482487.

90. Pal Choudhuri S, Delay RJ, Delay ER. Metabotropic glutamate receptors are involved in the detection of IMP and L-amino acids by mouse taste sensory cells. Neuroscience. 2016;316:94–108. doi: 10.1016/j.neuroscience.2015.12.008 26701297.

91. Shigemura N, Shirosaki S, Ohkuri T, Sanematsu K, Islam AA, Ogiwara Y, et al. Variation in umami perception and in candidate genes for the umami receptor in mice and humans. Am J Clin Nutr. 2009;90(3):764S–9S. Epub 2009/07/25. ajcn.2009.27462M [pii] doi: 10.3945/ajcn.2009.27462M 19625681.

92. Sukumaran SK, Yee KK, Iwata S, Kotha R, Quezada-Calvillo R, Nichols BL, et al. Taste cell-expressed alpha-glucosidase enzymes contribute to gustatory responses to disaccharides. Proc Natl Acad Sci U S A. 2016;113(21):6035–40. Epub 2016/05/11. doi: 10.1073/pnas.1520843113 27162343; PubMed Central PMCID: PMC4889361.

93. Dvoryanchikov G, Hernandez D, Roebber JK, Hill DL, Roper SD, Chaudhari N. Transcriptomes and neurotransmitter profiles of classes of gustatory and somatosensory neurons in the geniculate ganglion. Nat Commun. 2017;8(1):760. Epub 2017/10/04. doi: 10.1038/s41467-017-01095-1 28970527; PubMed Central PMCID: PMC5624912.

94. Carr CE, Konishi M. A circuit for detection of interaural time differences in the brain stem of the barn owl. J Neurosci. 1990;10(10):3227–46. Epub 1990/10/01. doi: 10.1523/JNEUROSCI.10-10-03227.1990 2213141.

95. Joris PX, Smith PH, Yin TC. Coincidence detection in the auditory system: 50 years after Jeffress. Neuron. 1998;21(6):1235–8. Epub 1999/01/12. doi: 10.1016/s0896-6273(00)80643-1 9883717.

96. Oertel D, Bal R, Gardner SM, Smith PH, Joris PX. Detection of synchrony in the activity of auditory nerve fibers by octopus cells of the mammalian cochlear nucleus. Proc Natl Acad Sci U S A. 2000;97(22):11773–9. Epub 2000/10/26. doi: 10.1073/pnas.97.22.11773 11050208; PubMed Central PMCID: PMC34348.

97. Ala-Laurila P, Rieke F. Coincidence detection of single-photon responses in the inner retina at the sensitivity limit of vision. Curr Biol. 2014;24(24):2888–98. Epub 2014/12/03. doi: 10.1016/j.cub.2014.10.028 25454583; PubMed Central PMCID: PMC4269560.

98. Sakmann B. From single cells and single columns to cortical networks: dendritic excitability, coincidence detection and synaptic transmission in brain slices and brains. Exp Physiol. 2017;102(5):489–521. Epub 2017/02/01. doi: 10.1113/EP085776 28139019; PubMed Central PMCID: PMC5435930.

99. Brill MF, Meyer A, Rossler W. It takes two-coincidence coding within the dual olfactory pathway of the honeybee. Front Physiol. 2015;6:208. Epub 2015/08/19. doi: 10.3389/fphys.2015.00208 26283968; PubMed Central PMCID: PMC4516877.

100. Gupta N, Singh SS, Stopfer M. Oscillatory integration windows in neurons. Nat Commun. 2016;7:13808. Epub 2016/12/16. doi: 10.1038/ncomms13808 27976720; PubMed Central PMCID: PMC5171764.

101. Wang L, Gillis-Smith S, Peng Y, Zhang J, Chen X, Salzman CD, et al. The coding of valence and identity in the mammalian taste system. Nature. 2018;558(7708):127–31. Epub 2018/06/01. doi: 10.1038/s41586-018-0165-4 29849148; PubMed Central PMCID: PMC6201270.

102. Pfaff DW. Theoretical consideration of cross-fiber pattern coding in the neural signalling of pheromones and other chemical stimuli. Psychoneuroendocrinology. 1975;1:79–93.

103. Han SK, Mancino V, Simon MI. Phospholipase Cbeta 3 mediates the scratching response activated by the histamine H1 receptor on C-fiber nociceptive neurons. Neuron. 2006;52(4):691–703. doi: 10.1016/j.neuron.2006.09.036 17114052.

104. Xie W, Samoriski GM, McLaughlin JP, Romoser VA, Smrcka A, Hinkle PM, et al. Genetic alteration of phospholipase C beta3 expression modulates behavioral and cellular responses to mu opioids. Proc Natl Acad Sci U S A. 1999;96(18):10385–90. doi: 10.1073/pnas.96.18.10385 10468617; PubMed Central PMCID: PMC17897.

105. Hacker K, Medler KF. Mitochondrial calcium buffering contributes to the maintenance of Basal calcium levels in mouse taste cells. J Neurophysiol. 2008;100(4):2177–91. doi: 10.1152/jn.90534.2008 18684902; PubMed Central PMCID: PMC2576209.

106. Laskowski AI, Medler KF. Sodium-calcium exchangers contribute to the regulation of cytosolic calcium levels in mouse taste cells. J Physiol. 2009;587(Pt 16):4077–89. doi: 10.1113/jphysiol.2009.173567 19581381; PubMed Central PMCID: PMC2756439.

107. Maliphol AB, Garth DJ, Medler KF. Diet-induced obesity reduces the responsiveness of the peripheral taste receptor cells. PLoS One. 2013;8(11):e79403. doi: 10.1371/journal.pone.0079403 24236129; PubMed Central PMCID: PMC3827352.

108. Rebello MR, Maliphol AB, Medler KF. Ryanodine Receptors Selectively Interact with L Type Calcium Channels in Mouse Taste Cells. PLoS One. 2013;8(6):e68174. doi: 10.1371/journal.pone.0068174 23826376; PubMed Central PMCID: PMC3694925.

109. Rebello MR, Medler KF. Ryanodine receptors selectively contribute to the formation of taste-evoked calcium signals in mouse taste cells. Eur J Neurosci. 2010;32(11):1825–35. Epub 2010/10/20. doi: 10.1111/j.1460-9568.2010.07463.x 20955474; PubMed Central PMCID: PMC2994989.

110. Szebenyi SA, Laskowski AI, Medler KF. Sodium/calcium exchangers selectively regulate calcium signaling in mouse taste receptor cells. J Neurophysiol. 2010;104(1):529–38. Epub 2010/05/14. jn.00118.2010 [pii] doi: 10.1152/jn.00118.2010 20463203; PubMed Central PMCID: PMC2904227.

111. Bartel DL, Sullivan SL, Lavoie EG, Sevigny J, Finger TE. Nucleoside triphosphate diphosphohydrolase-2 is the ecto-ATPase of type I cells in taste buds. J Comp Neurol. 2006;497(1):1–12. doi: 10.1002/cne.20954 16680780; PubMed Central PMCID: PMC2212711.

112. Martin LE, Nikonova LV, Kay K, Paedae AB, Contreras RJ, Torregrossa AM. Salivary proteins alter taste-guided behaviors and taste nerve signaling in rat. Physiol Behav. 2017;184:150–61. doi: 10.1016/j.physbeh.2017.11.021 29162505.

113. Torregrossa AM, Nikonova L, Bales MB, Villalobos Leal M, Smith JC, Contreras RJ, et al. Induction of salivary proteins modifies measures of both orosensory and postingestive feedback during exposure to a tannic acid diet. PLoS One. 2014;9(8):e105232. doi: 10.1371/journal.pone.0105232 25162297; PubMed Central PMCID: PMC4146545.

114. Harrer MI, Travers SP. Topographic organization of Fos-like immunoreactivity in the rostral nucleus of the solitary tract evoked by gustatory stimulation with sucrose and quinine. Brain Res. 1996;711(1–2):125–37. Epub 1996/03/04. doi: 10.1016/0006-8993(95)01410-1 8680855.

115. Preacher KJ. Calculation for the chi-square test: An interactive calculation tool for chi-square tests of goodness of fit and independence [Computer software]. 2001. Available from http://quantpsy.org.

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