Taste sensilla of flies: Function, central neuronal projections, and development

Microscopy Research and Technique

Volumn 39, Issue 6, 1997, Pages 532-546

  Pollack, Gerald S ^a   Balakrishnan, Rohini ^a  

^a MCGILL UNIVERSITY   (Canada)

Author keywords

Precursor cell; Sensilla; Stimulus

Indexed keywords

CYTOLOGY; NEURONS;

PRECURSOR CELLS; SENSILLAE; SINGLE PRECURSORS; STIMULUS; STIMULUS-SENSITIVITY;

CELLS;

ANIMAL BEHAVIOR; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CENTRAL NERVOUS SYSTEM; DROSOPHILA; EMBRYO; FEEDING BEHAVIOR; GUSTATORY NERVOUS SYSTEM; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PRIORITY JOURNAL; SENSE ORGAN; TASTE;

ANIMALIA;

EID: 0031444306     PISSN: 1059910X     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1097-0029(19971215)39:6<532::AID-JEMT6>3.0.CO;2-F     Document Type: Article

References (89)

1. Amakawa, T., Kawata, K., and Ozaki, M. (1992) Nucleotide receptor-site on the labellar sugar receptor cell of the blowfly Phormia regina. J. Insect Physiol., 38:365-371.
2. Arora, K. (1985) Neurogenetic Studies on Taste Mechanisms of Drosophila melanogaster. Ph.D. Thesis, Bombay University.
3. Bate, C.M. (1978) Development of sensory systems in arthropods. In: Handbook of Sensory Physiology, Vol. IX. M. Jacobsen, ed. Springer-Verlag, Berlin, pp. 1-53.
4. Bodmer, R., Carretto, R., and Jan, Y.N. (1989) Neurogenesis of the peripheral nervous system in Drosophila embryos: DNA replication patterns and cell lineages. Neuron, 3:21-32.
5. Buchner, E., Buchner, S., Burg, M.G., Hofbauer, A., Pak, W.L., and Pollack, I. (1993) Histamine is a major mechanosensory neurotransmitter candidate in Drosophila melanogaster. Cell Tissue Res., 273:119-125.
6. Dambly-Chaudière, C., Jamet, E., Burri, M., Bopp, D., Spielmann, P., Ghysen, A., and Noll, M. (1992) The paired box gene par neuro: A determinant of poly-innervated sense orans in Drosophila. Cell, 69:159-172.
7. De Kramer, J.J., and van der Molen, J.N. (1980) The pore mechanism of the contact chemoreceptors of the blowfly, Calliphora vicina. In: Olfaction and Taste IV. H. van der Starre, ed. IRL Press, London, pp. 61-64.
8. De Kramer, J.J., and van der Molen, L.G. (1984) Development of labellar taste hairs in the blowfly, Calliphora vicina (Insecta, Diptera). Zoomorphology, 104:1-10.
9. Dethier, V.G. (1955) The physiology and histology of the contact chemoreceptors of the blowfly. Q. Rev. Biol., 33:348-371.
10. Dethier, V.G. (1957) Communication by insects: Physiology of dancing. Science, 125:331-336.
11. Dethier, V.G. (1976) The Hungry Fly. Harvard University Press, Cambridge 489 pp.
12. Dethier, V.G., and Hanson, F.E. (1965) Taste papillae of the blowfly. J. Cell Comp. Physiol., 65:93-100.
13. Dethier, V.G., and Hanson, F.E. (1968) Electrophysiological responses of the chemoreceptors of the blowfly to sodium salts of fatty acids. Proc. Natl. Acad. Sci. USA, 60:1296-1303.
14. Dethier, V.G., Evans, D.R., and Rhoades, M.V. (1956) Some factors controlling the ingestion of carbohydrates by the blowfly. Biol. Bull., 111:204-222.
15. Edgecomb, R.S. (1986) The Proboscis Extension Response in the Blackblow Fly, Phormia regina Meigen: Neural Correlates and Regulation of Tarsal Taste Threshold. Ph.D. Thesis, Purdue University.
16. Edgecomb, R.S., and Murdock, L.L. (1992). Central projections of axons from taste hairs on the labellum and tarsi of the blowfly, Phormia regina Meigen. J. Comp. Neurol., 315:431-444.
17. Evans, D.R., and de Mellon, F. (1962) Stimulation of a primary taste receptor by salts. J. Gen. Physiol., 4:651-661.
18. Falk, R., Bleiser-Avivi, N., and Atidia, J. (1976) Labellar taste organs of Drosophila melanogaster. J. Morphol., 150:327-342.
19. Felt, B.T., and Vande Berg, J.S. (1976) Ultrastructure of the blowfly chemoreceptor sensillum (Phormia regina). J. Morphol., 150:763-783.
20. Ghysen, A., and Dambly-Chaudière, C. (1993) The specification of sensoryneuron identity in Drosophila. Bioessays, 15:293-298.
21. Ghysen, A., Dambly-Chaudière, C., Jan, L.Y., and Jan, Y.-N. (1993) Cell interactions and gene interactions in peripheral neurogenesis. Genes Dev., 7:723-733.
22. Gillary, H.L. (1966) Stimulation of the salt receptor of the blowfly. J. Gen. Physiol., 50:359-368.
23. Goldrich, N.R. (1973) Behavioral responses of Phormia regina (Meigen) to labellar stimulation with amino acids. J. Gen. Physiol., 61:74-88.
24. Grabowski, C.T., and Dethier, V.G. (1954) The structure of tarsal chemoreceptors of the blowfly, Phormia regina Meigen. J. Morphol., 94:1-20.
25. Hansen, K., and Hansen-Delkeskamp, E. (1983) The development of taste and tactile hairs in the pharate fly Protophormia terraenovae (Diptera, Calliphoridae) and in the embryonal cricket Acheta domestica (Orthopteroidea, Ensifera). Zoomorphology, 102:241-259.
26. Hartenstein, V. (1988) Development of Drosophila larval sensory organs: Spatiotemporal pattern of sensory neurones, peripheral axonal pathways and sensilla differentiation. Development, 102:869-886.
27. Hartenstein, V., and Posakony, J.W. (1989) Development of adult sensilla on the wing and notum of Drosophila melanogaster. Development, 107:389-405.
28. Hodgson, E.S., Lettvin, J.Y., and Roeder, K.D. (1955) Physiology of a primary chemoreceptor unit. Science, 122:417-418.
29. Huang, F., Dambly-Chaudière, C., and Ghysen, A. (1991) The emergence of sense organs in the wing disc of Drosophila. Development, 111:1087-1095.
30. Jiménez, F., and Modolell, J. (1993) Neural fate specification in Drosophila. Curr. Opin. Genet. Dev., 3:626-632.
31. Kijima, H., Nagata, K., Nishiyama, A., and Morita, H. (1988) Receptor current fluctuation analysis in the labellar sugar receptor of the fleshfly. J. Gen. Physiol., 91:29-47.
32. Kinnamon, S.C. (1988) Taste transduction: A diversity of mechanisms. Trends Neurosci., 11:491-496.
33. Lakes, R., and Pollack, G.S. (1990a) Development of sensory cells of the labella and the legs of the blowfly, Phormia regina. In: Sensory Systems and Communication of Arthropods. F.G. Gribakin, K. Wiese, and A.V. Popov, eds. Birkhauser Verlag, Basel, pp. 275-279.
34. Lakes, R., and Pollack, G.S. (1990b) The development of the sensory organs of the legs in the blowfly, Phormia regina. Cell Tissue Res., 259:93-104.
35. McCutchan, M.C. (1969a) Responses of tarsal chemoreceptive hairs of the blowfly, Phormia regina. J. Insect Physiol., 15:2059-2068.
36. McCutchan, M.C. (1969b) Behavioral and electrophysiological responses of the blowfly, Phormia regina Meigen, to acids. Z. Vergl. Physiol., 65:131-152.
37. McIver, S.B. (1985) Mechanoreception. In: Comprehensive Insect Physiology, Biochemistry and Pharmacology, Vol. 6. L.I. Gilbert and G.A. Kerkut, eds. Pergamon Press, New York, pp. 71-132.
38. Menco, B.P.M., and van der Wölk, P.M. (1982) Freeze-fracture characteristics of insect gustatory and olfactory sensilla. Cell Tissue Res., 223:1-27.
39. Merritt, D.J., and Rice, M.J. (1984) Innervation of the cereal sensilla on the ovipositor of the Australian sheep blowfly (Lucilia cuprina). Physiol. Entomol., 9:39-47.
40. Morita, H. (1992) Transduction process and impulse initiation in insect contact chemoreceptor. Zool. Sci., 9:1-16.
41. Morita, H., and Yamashita, S. (1959) Generator potential of insect chemoreceptor. Science, 130:922.
42. Morita, H., Doira, S., Takeda, K., and Kuwabara, M. (1957) Electrical responses of contact chemoreceptor on tarsus of the butterfly, Vanessa indica. Mem. Fac. Sci. Kyushu Univ., 2:119-139.
43. Murphey, R.K. (1981) The structure and development of a somatotopic map in crickets: The cereal afferent projection. Dev. Biol., 88:236-246.
44. Murphey, R.K., Possidente, D., Pollack, G., and Merritt, D.J. (1989) Modality-specific axonal projections in the CNS of the flies Phormia and Drosophila. J. Comp. Neurol., 290:185-200.
45. Murray, M.A., Schubiger, M., and Palka, J. (1984) Neuron differentiation and axon growth in the developing wing of Drosophila melanogaster. Dev. Biol., 104:259-273.
46. Nayak, S.V., and Singh, R.N. (1983) Sensilla on the tarsal segments and mouthparts of adult Drosophila melanogaster Meigen (Diptera: Drosophilidae). Int. J. Insect Morphol. Embryol., 12:273-291.
47. Nayak, S.V., and Singh, R.N. (1985) Primary sensory projections from the labella to the brain of Drosophila melanogaster Meigen ( Diptera: Drosophilidae). Int. J. Insect Morphol. Embryol., 14:115-129.
48. Nottebohm, E., Dambly-Chaudière, C., and Ghysen, A. (1992) Connectivity of chemosensory neurons is controlled by the gene poxn in Drosophila. Nature, 359:829-831.
49. Nottebohm, E., Usui, A., Therianos, S., Kimura, K., Dambly-Chaudière, C., and Ghysen, A. (1994). The gene poxn controls different steps of the formation of chemosensory organs in Drosophila. Neuron, 12:25-34.
50. Omand, E., and Dethier, V.G. (1969) An electrophysiological analysis of the action of carbohydrates on the sugar receptor of the blowfly. Proc. Natl. Acad. Sci. USA, 62:136-143.
51. Ozaki, M., Amakawa, T., Ozaki, K., and Tokunaga, F. (1993) Two types of sugar-binding protein in the labellum of the fly: Putative taste receptor molecules for sweetness. J. Gen. Physiol., 102:201-216.
52. Peters, W. (1965) Die Sinnesorgane an den Labellen von Calliphora erythrocephala Mg. (Diptera). Z. Morphol. Okol. Tiere, 5:259-320.
53. Pflüger, H.J., Braunig, P., and Hustert, R. (1988) The organization of mechanosensory neuropiles in locust thoracic ganglia. Proc. R. Soc. Lond. [Biol.], 321:1-26.
54. Pollack, G.S. (1977) Labellar lobe spreading in the blowfly: Regulation by taste and satiety. J. Comp. Physiol., 121:115-134.
55. Pollack, G.S., and Lakes-Harlan, R. (1995) Birth times of neurons in labellar taste sensilla of the blowfly Phormia regina. J. Neurobiol., 26:17-32.
56. Possidente, D.R., and Murphey, R.K. (1989) Genetic control of sexually dimorphic axon morphology in Drosophila sensory neurons. Dev. Biol., 132:448-457.
57. Ray, K., Hartenstein, V., and Rodrigues, V. (1993) Development of the taste bristles on the labellum of Drosophila melanogaster. Dev. Biol., 155:26-37.
58. Rees, C.J.C. (1970) The primary process of reception in the type 3 ("water") receptor cell of the fly, Phormia terraenovae. Proc. R. Soc. Lond. [Biol.], 174:469-490.
59. Rhyu, M.S., Jan, L.Y., and Jan, Y.N. (1994) Asymmetric distribution of Numb protein during division of the sensory organ precursor cell confers distinct fates to daughter cells. Cell, 76:477-191.
60. Rodrigues, V., and Siddiqi, O. (1978) Genetic analysis of chemosensory pathway. Proc. Indian Acad. Sci. Sect. B., 87:147-160.
61. Rodrigues, V., and Siddiqi, O. (1981) A gustatory mutant of Drosophila defective in pyranose receptors. Mol. Gen. Genet., 181:406-408.
62. Schnuch, M., and Hansen, K. (1990) Sugar sensitivity of a labellar salt receptor of the blowfly Protophormia terraenovae. J. Insect Physiol., 36:409-417.
63. Shanbhag, S.R., and Singh, R.N. (1992) Functional implications of the projections of neurons from individual labellar sensillum of Drosophila melanogaster as revealed by neuronal-marker horseradish peroxidase. Cell Tissue Res., 267:273-282.
64. Shimada, I., and Isono, K. (1978) The specific receptor site for aliphatic carboxylate anion in the labellar sugar receptor of the fleshfly. J. Insect Physiol., 24:807-811.
65. Shimada, I., Shiraishi, A., Kijima, H., and Morita, H. (1974) Separation of two receptor sites in a single labellar sugar receptor of the flesh-fly by treatment with p-chloromecuribenzoate. J. Insect Physiol., 20:605-621.
66. Shimada, I., Horiki, H., Ohrui, H., and Meguro, H. (1985) Taste response to 2,5-anhydro-D-hexitols; rigid stereospecificity of the furanose site in the sugar receptor of the flesh fly. J. Comp. Physiol. [A], 157:477-482.
67. Shiraishi, A., and Kuwabara, M. (1970) The effects of amino acids on the labellar hair chemosensory cells of the fly. J. Gen. Physiol., 56:768-782.
68. Shiraishi, A., and Tanabe, Y. (1974) The proboscis extension response and tarsai and labellar chemosensory hairs in the blowfly. J. Comp. Physiol., 92:161-179.
69. Siddiqi, O., Joshi, S., Arora, K., and Rodrigues, V. (1989) Genetic investigation of salt reception in Drosophila melanogaster. Genome, 31:646-651.
70. Stocker, R.F., and Schorderet, M. (1981) Cobalt filling of sensory projections from internal and external mouthparts in Drosophila. Cell Tissue Res., 216:513-523.
71. Stürckow, B. (1967) Occurrence of a viscous substance at the tip of a labellar taste hair of the blowfly. In: Olfaction and Taste II. T. Hayashi, ed. Pergamon Press, Oxford, pp. 707-720.
72. Stürckow, B. (1971) Electrical impedance of the labellar taste hair of the blowfly, Calliphora erhythroceophala Mg. Z. Vergl. Physiol., 72:131-143.
73. Stürckow, B., Holbert, P.E., Adams, J.R., and Anstead, R.J. (1973) Fine structure of the tip of the labellar taste hair of the blow flies, Phormia regina (Mg.) and Calliphora vicina R.-D. (Diptera, Calliphoridae). Z. Morphol. Tiere, 75:87-109.
74. Tanimura, T., and Shimada, I. (1981) Multiple receptor proteins for sweet taste in Drosophila discriminated by papain treatment. J. Comp. Physiol. [A], 141:265-269.
75. Tanimura, T., Isono, K., Takamura, T., and Shimada, I. (1982) Genetic dimorphism in the taste sensitivity to trehalose in Drosophila melanogaster. J. Comp. Physiol. [A], 147:433-437.
76. Technau, G.M., and Campos-Ortega, J.A. (1986) Lineage analysis of transplanted individual cells in embryos of Drosophila melanogaster. II. Commitment and proliferative capabilities of neural and epidermal cell progenitors. Roux Arch. Dev. Biol., 95:445-454.
77. Thurm, U., and Küppers, J. (1980) Epithelial physiology of insect sensilla. In: Insect Biology in the Future. M. Locke and D.S. Smith, eds. Academic Press, New York, pp. 735-763.
78. Tominaga, Y., Kabuta, H., and Kuwabara, M. (1969) The fine structure of the interpseudotracheal papilla of a fleshfly. Ann. Zool. Jpn., 42:91-104.
79. Van der Starre, H. (1972) Tarsal taste discrimination in the blowfly, Calliphora vicina Robineau-Desvoidy. Neth. J. Zool., 22:227-282.
80. Van der Wolk, F.M. (1980) A comparative ultrastructural study of contact chemoreceptors of the blow fly Calliphora vicina. Ultramicroscopy, 5:129.
81. Wieczorek, H. (1980) Sugar reception by an insect water receptor. J Comp. Phsiol. [A], 138:167-172.
82. Wieczorek, H., and Köppl, R. (1978) Effect of sugars on the labellar water receptor of the fly. J. Comp. Physiol. [A], 126:131-136.
83. Wieczorek, H., and Köppl, R. (1982) Reaction spectra of sugar receptors in different taste hairs of the fly. J. Comp. Physiol. [A], 149:207-213.
84. Wieczorek, H., Shimada, I., and Hopperdietzel, C. (1988) Treatment with pronase uncouples water and sugar reception in the labellar water receptor of the blowfly. J. Comp. Physiol. [A], 163:413-419.
85. Wilczek, M. (1967) The distribution and neuroanatomy of the labellar sense organs of the blowfly Phormia regina Meigen. J. Morphol., 122:175-201.
86. Wolbarsht, M.L., and Dethier, V.G. (1958) Electrical activity in the chemoreceptors of the blowfly. I. Responses to chemical and mechanical stimulation. J. Gen. Physiol., 42:393-412.
87. Wu, C.-F., and Ganetzky, B. (1980) Genetic alteration of nerve membrane excitability in temperature-sensitive paralytic mutants of Drosophila melanogaster. Nature, 286:814-816.
88. Yetman, S., and Pollack, G.S. (1986) Central projections of labellar taste hairs in the blowfly, Phormia regina Meigen. Cell Tissue Res., 245:555-561.
89. Yetman, S., and Pollack, G.S. (1987) Proboscis extension in the blowfly: Directional responses to stimulation of identified chemosensitive hairs. J. Comp. Physiol. [A], 160:367-374.