DOI QR코드

DOI QR Code

Advances in Optical Tools to Study Taste Sensation

  • Received : 2022.07.21
  • Accepted : 2022.09.15
  • Published : 2022.12.31

Abstract

Taste sensation is the process of converting chemical identities in food into a neural code of the brain. Taste information is initially formed in the taste buds on the tongue, travels through the afferent gustatory nerves to the sensory ganglion neurons, and finally reaches the multiple taste centers of the brain. In the taste field, optical tools to observe cellularlevel functions play a pivotal role in understanding how taste information is processed along a pathway. In this review, we introduce recent advances in the optical tools used to study the taste transduction pathways.

Keywords

Acknowledgement

This work was supported by the Samsung Science and Technology Foundation under Project Number SSTF-BA2002-14 and the Basic Science Research Program through the National Research Foundation of Korea (NRF) funded by the Ministry of Education (2018R1D1A1B07042834, 2019M3E5D2A01058329, 2019M3A9E2061789, 2020M3C1B8016137, 2020R1A5A 1018081).

References

  1. Bando, Y., Sakamoto, M., Kim, S., Ayzenshtat, I., and Yuste, R. (2019). Comparative evaluation of genetically encoded voltage indicators. Cell Rep. 26, 802-813.e4.
  2. Barretto, R.P.J., Gillis-Smith, S., Chandrashekar, J., Yarmolinsky, D.A., Schnitzer, M.J., Ryba, N.J.P., and Zuker, C.S. (2015). The neural representation of taste quality at the periphery. Nature 517, 373-376. https://doi.org/10.1038/nature13873
  3. Caicedo, A. and Roper, S.D. (2001). Taste receptor cells that discriminate between bitter stimuli. Science 291, 1557-1560. https://doi.org/10.1126/science.291.5508.1557
  4. Chandrashekar, J., Kuhn, C., Oka, Y., Yarmolinsky, D.A., Hummler, E., Ryba, N.J.P., and Zuker, C.S. (2010). The cells and peripheral representation of sodium taste in mice. Nature 464, 297-301. https://doi.org/10.1038/nature08783
  5. Chen, K., Kogan, J.F., and Fontanini, A. (2021). Spatially distributed representation of taste quality in the gustatory insular cortex of behaving mice. Curr. Biol. 31, 247-256.e4. https://doi.org/10.1016/j.cub.2020.10.014
  6. Chen, X., Gabitto, M., Peng, Y., Ryba, N.J.P., and Zuker, C.S. (2011). A gustotopic map of taste qualities in the mammalian brain. Science 333, 1262-1266. https://doi.org/10.1126/science.1204076
  7. Choi, M., Kwok, S.J.J., and Yun, S.H. (2015a). In vivo fluorescence microscopy: lessons from observing cell behavior in their native environment. Physiology (Bethesda) 30, 40-49. https://doi.org/10.1152/physiol.00019.2014
  8. Choi, M., Lee, W.M., and Yun, S.H. (2015b). Intravital microscopic interrogation of peripheral taste sensation. Sci. Rep. 5, 8661.
  9. Dando, R., Dvoryanchikov, G., Pereira, E., Chaudhari, N., and Roper, S.D. (2012). Adenosine enhances sweet taste through A2B receptors inthe taste bud. J. Neurosci. 32, 322-330. https://doi.org/10.1523/JNEUROSCI.4070-11.2012
  10. DeFazio, R.A., Dvoryanchikov, G., Maruyama, Y., Kim, J.W., Pereira, E., Roper, S.D., and Chaudhari, N. (2006). Separate populations of receptor cells and presynaptic cells in mouse taste buds. J. Neurosci. 26, 3971-3980. https://doi.org/10.1523/JNEUROSCI.0515-06.2006
  11. Fowler, B.E. and Macpherson, L.J. (2021). In vivo calcium imaging of mouse geniculate ganglion neuron responses to taste stimuli. J. Vis. Exp. (168), 10.3791/62172.
  12. Ghosh, K.K., Burns, L.D., Cocker, E.D., Nimmerjahn, A., Ziv, Y., Gamal, A.E., and Schnitzer, M.J. (2011). Miniaturized integration of a fluorescence microscope. Nat. Methods 8, 871-878. https://doi.org/10.1038/nmeth.1694
  13. Giovannucci, A., Friedrich, J., Gunn, P., Kalfon, J., Brown, B.L., Koay, S.A., Taxidis, J., Najafi, F., Gauthier, J.L., Zhou, P., et al. (2019). CaImAn an open source tool for scalable calcium imaging data analysis. Elife 8, e38173.
  14. Gunaydin, L.A., Grosenick, L., Finkelstein, J.C., Kauvar, I.V., Fenno, L.E., Adhikari, A., Lammel, S., Mirzabekov, J.J., Airan, R.D., Zalocusky, K.A., et al. (2014). Natural neural projection dynamics underlying social behavior. Cell 157, 1535-1551. https://doi.org/10.1016/j.cell.2014.05.017
  15. Han, J. and Choi, M. (2018). Comprehensive functional screening of taste sensation in vivo. BioRxiv, https://doi.org/10.1101/371682
  16. Han, J., Choi, P., and Choi, M. (2021a). µTongue: a microfluidics-based functional imaging platform for the tongue in vivo. J. Vis. Exp. (170), 10.3791/62361.
  17. Han, J., Kim, S., Choi, P., Lee, S., Jo, Y., Kim, E., and Choi, M. (2021b). Robust functional imaging of taste sensation with a Bessel beam. Biomed. Opt. Express 12, 5855-5864. https://doi.org/10.1364/BOE.430643
  18. Huang, Y.A., Dando, R., and Roper, S.D. (2009). Autocrine and paracrine roles for ATP and serotonin in mouse taste buds. J. Neurosci. 29, 13909-13918. https://doi.org/10.1523/JNEUROSCI.2351-09.2009
  19. Huang, Y.A., Pereira, E., and Roper, S.D. (2011). Acid stimulation (sour taste) elicits GABA and serotonin release from mouse taste cells. PLoS One 6, e25471.
  20. Jin, H., Fishman, Z.H., Ye, M., Wang, L., and Zuker, C.S. (2021). Top-down control of sweet and bitter taste in the mammalian brain. Cell 184, 257-271.e16. https://doi.org/10.1016/j.cell.2020.12.014
  21. Lambert, T.J. (2019). FPbase: a community-editable fluorescent protein database. Nat. Methods 16, 277-278. https://doi.org/10.1038/s41592-019-0352-8
  22. Lecoq, J., Oliver, M., Siegle, J.H., Orlova, N., Ledochowitsch, P., and Koch, C. (2021). Removing independent noise in systems neuroscience data using DeepInterpolation. Nat. Methods 18, 1401-1408. https://doi.org/10.1038/s41592-021-01285-2
  23. Lee, S., Augustine, V., Zhao, Y., Ebisu, H., Ho, B., Kong, D., and Oka, Y. (2019). Chemosensory modulation of neural circuits for sodium appetite. Nature 568, 93-97. https://doi.org/10.1038/s41586-019-1053-2
  24. Li, X., Zhang, G., Wu, J., Zhang, Y., Zhao, Z., Lin, X., Qiao, H., Xie, H., Wang, H., Fang, L., et al. (2021). Reinforcing neuron extraction and spike inference in calcium imaging using deep self-supervised denoising. Nat. Methods 18, 1395-1400. https://doi.org/10.1038/s41592-021-01225-0
  25. Lundy, R.F., Jr. and Contreras, R.J. (1999). Gustatory neuron types in rat geniculate ganglion. J. Neurophysiol. 82, 2970-2988. https://doi.org/10.1152/jn.1999.82.6.2970
  26. Nomura, K., Nakanishi, M., Ishidate, F., Iwata, K., and Taruno, A. (2020). All-electrical Ca2+-independent signal transduction mediates attractive sodium taste in taste buds. Neuron 106, 816-829.e6. https://doi.org/10.1016/j.neuron.2020.03.006
  27. Ogata, T. and Ohtubo, Y. (2020). Quantitative analysis of taste bud cell numbers in the circumvallate and foliate taste buds of mice. Chem. Senses 45, 261-273. https://doi.org/10.1093/chemse/bjaa017
  28. Oka, Y., Butnaru, M., Von Buchholtz, L., Ryba, N.J.P., and Zuker, C.S. (2013). High salt recruits aversive taste pathways. Nature 494, 472-475. https://doi.org/10.1038/nature11905
  29. Ozdener, M.H. and Rawson, N.E. (2013). Primary culture of mammalian taste epithelium. Methods Mol. Biol. 945, 95-107. https://doi.org/10.1007/978-1-62703-125-7_7
  30. Peng, Y., Gillis-Smith, S., Jin, H., Trankner, D., Ryba, N.J.P., and Zuker, C.S. (2015). Sweet and bitter taste in the brain of awake behaving animals. Nature 527, 512-515. https://doi.org/10.1038/nature15763
  31. Pnevmatikakis, E.A., Soudry, D., Gao, Y., Machado, T.A., Merel, J., Pfau, D., Reardon, T., Mu, Y., Lacefield, C., Yang, W., et al. (2016). Simultaneous denoising, deconvolution, and demixing of calcium imaging data. Neuron 89, 285-299. https://doi.org/10.1016/j.neuron.2015.11.037
  32. Richter, T.A., Caicedo, A., and Roper, S.D. (2003). Sour taste stimuli evoke Ca2++ and pH responses in mouse taste cells. J. Physiol. 547, 475-483. https://doi.org/10.1113/jphysiol.2002.033811
  33. Roper, S.D. and Chaudhari, N. (2017). Taste buds: cells, signals and synapses. Nat. Rev. Neurosci. 18, 485-497. https://doi.org/10.1038/nrn.2017.68
  34. Ruiz, C.J., Stone, L.M., Mcpheeters, M., Ogura, T., Bottger, B., Lasher, R.S., Finger, T.E., and Kinnamon, S.C. (2001). Maintenance of rat taste buds in primary culture. Chem. Senses 26, 861-873. https://doi.org/10.1093/chemse/26.7.861
  35. Schiff, H.C., Bouhuis, A.L., Yu, K., Penzo, M.A., Li, H., He, M., and Li, B. (2018). An insula-central amygdala circuit for guiding tastant-reinforced choice behavior. J. Neurosci. 38, 1418-1429. https://doi.org/10.1523/JNEUROSCI.1773-17.2017
  36. Shrestha, B. and Lee, Y. (2021). Mechanisms of carboxylic acid attraction in Drosophila melanogaster. Mol. Cells 44, 900-910. https://doi.org/10.14348/molcells.2021.0205
  37. Stelzer, E.H.K., Strobl, F., Chang, B.J., Preusser, F., Preibisch, S., McDole, K., and Fiolka, R. (2021). Light sheet fluorescence microscopy. Nat. Rev. Methods Primers 1, 73.
  38. Venkatesan, N., Boggs, K., and Liu, H.X. (2016). Taste bud labeling in whole tongue epithelial sheet in adult mice. Tissue Eng. Part C Methods 22, 332-337. https://doi.org/10.1089/ten.tec.2015.0377
  39. Wang, H., Jing, M., and Li, Y. (2018). Lighting up the brain: genetically encoded fluorescent sensors for imaging neurotransmitters and neuromodulators. Curr. Opin. Neurobiol. 50, 171-178. https://doi.org/10.1016/j.conb.2018.03.010
  40. Wu, A. and Dvoryanchikov, G. (2015). Live animal calcium imaging of the geniculate ganglion. Research Square, https://doi.org/10.1038/protex.2015.106
  41. Wu, A., Dvoryanchikov, G., Pereira, E., Chaudhari, N., and Roper, S.D. (2015). Breadth of tuning in taste afferent neurons varies with stimulus strength. Nat. Commun. 6, 8171.
  42. Yarmolinsky, D.A., Zuker, C.S., and Ryba, N.J.P. (2009). Common sense about taste: from mammals to insects. Cell 139, 234-244. https://doi.org/10.1016/j.cell.2009.10.001
  43. Yokota, Y. and Bradley, R.M. (2016). Receptive field size, chemical and thermal responses, and fiber conduction velocity of rat chorda tympani geniculate ganglion neurons. J. Neurophysiol. 115, 3062-3072. https://doi.org/10.1152/jn.00045.2016
  44. Yokota, Y. and Bradley, R.M. (2017). Geniculate ganglion neurons are multimodal and variable in receptive field characteristics. Neuroscience 367, 147-158. https://doi.org/10.1016/j.neuroscience.2017.10.032
  45. Yoshida, R., Miyauchi, A., Yasuo, T., Jyotaki, M., Murata, Y., Yasumatsu, K., Shigemura, N., Yanagawa, Y., Obata, K., Ueno, H., et al. (2009). Discrimination of taste qualities among mouse fungiform taste bud cells. J. Physiol. 587, 4425-4439. https://doi.org/10.1113/jphysiol.2009.175075
  46. Zhang, Y., Hoon, M.A., Chandrashekar, J., Mueller, K.L., Cook, B., Wu, D., Zuker, C.S., and Ryba, N.J. (2003). Coding of sweet, bitter, and umami tastes: different receptor cells sharing similar signaling pathways. Cell 112, 293-301. https://doi.org/10.1016/S0092-8674(03)00071-0
  47. Zhang, J., Jin, H., Zhang, W., Ding, C., O'Keeffe, S., Ye, M., and Zuker, C.S. (2019). Sour sensing from the tongue to the brain. Cell 179, 392-402.e15. https://doi.org/10.1016/j.cell.2019.08.031
  48. Zhao, G.Q., Zhang, Y., Hoon, M.A., Chandrashekar, J., Erlenbach, I., Ryba, N.J.P., and Zuker, C.S. (2003). The receptors for mammalian sweet and umami taste. Cell 115, 255-266. https://doi.org/10.1016/S0092-8674(03)00844-4