Neurotransmitters in Compound Eyes

  • Roger C. Hardie
Conference paper

Abstract

Although chemical transmission had been suggested as early as 1848 by Du Bois-Reymond, it was 1904 before Elliot made the specific suggestion that adrenaline was a chemical mediator released by sympathetic nerve endings, and the concept of a chemical synapse did not become firmly established until the 1930’s. It is thus no wonder that Exner did not consider the role of neurotransmitters in his treatise on the compound eye, and indeed, except, perhaps, with reference to the problem of the mechanisms of light- and dark-adaptation, neurotransmission was not relevant to his study. In recent years, however, neuropharmacology has become such an important part of any neurobiological study that it is relevant to include a survey of neurotransmitters in the optic lobes in the present volume.

Keywords

Dopamine Nicotine Serotonin Noradrenaline Neurol 

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References

  1. Autrum H, Hoffmann E (1957) Die Wirkung von Pikrotoxin und Nikotin auf das Retinogramm von Insekten. Z Naturforsch 12b:752–757.Google Scholar
  2. Barlow HB, Levick WR (1965) The mechanism of directionally sensitive units in rabbit’s retina. J Physiol 178:477–504.PubMedGoogle Scholar
  3. Barlow RB jr, Chamberlain SC, Kaplan E (1977) Efferent inputs and serotonin enhance the sensitivity of the Limulus lateral eye. Biol Bull 153:414 (Abstr).Google Scholar
  4. Bjorklund A, Lindvall O, Svensson LA (1972) Mechanisms of fluorophore formation in the histochemical glyoxylic acid method for monoamines. Histochemie 32:113–131.PubMedCrossRefGoogle Scholar
  5. Buchner E, Rodrigues V (1984) Autoradiographic localisation of [3H]choline uptake in the brain of Drosophila melanogaster. Neurosci Lett 42:25–31.CrossRefGoogle Scholar
  6. Buchner E, Buchner S, Crawford G, Mason WT, Salvaterra PM, Sattelle DB (1986) Choline acetyl-transferase-like immunoreactivity in the brain of Drosophila melanogaster. Cell Tissue Res 246:57–62.CrossRefGoogle Scholar
  7. Budnik V, White K (1988) Catecholamine-containing neurons in Drosophila melanogaster: distribution and development. J Comp Neurol 268:400–413.PubMedCrossRefGoogle Scholar
  8. Bülthoff H, Bülthoff I (1987) Combining neuropharmacology and behavior to study motion detection in flies. Biol Cybernet 55:313–320.CrossRefGoogle Scholar
  9. Biilthoff H, Schmid A (1983) Neuropharmakologische Untersuchungen bewegungsempfindlicher Interneurone in der Lobula-Platte der Fliege. Verh Dtsch Zool Ges 273.Google Scholar
  10. Campos-Ortega JA (1974) Autoradiographic localization of 3H-γ-aminobutyric acid uptake in the lamina ganglionaris of Musca and Drosophila. Z Zeilforsch 147:415–431.CrossRefGoogle Scholar
  11. Chase BA, Kankel DR (1987) A genetic analysis of glutamatergic function in Drosophila. J Neurobiol 18:15–41.PubMedCrossRefGoogle Scholar
  12. Coombe PE (1986) The large monopolar cells L1 and L2 are responsible for ERG transients in Drosophila. J Comp Physiol A 159:655–665.CrossRefGoogle Scholar
  13. Crow T, Bridge MS (1985) Serotonin modulates photoresponses in Hermissenda type B photoreceptors. Neurosci Lett 60:83–88.PubMedCrossRefGoogle Scholar
  14. Datum K-H, Weiler R, Zettler F (1986) Immunocytochemical demonstration of γ-amino butyric acid and glutamic acid decarboxylase in R7 photoreceptors and C2 centrifugal fibres in the blowfly visual system. J Comp Physiol A 159:241–249.CrossRefGoogle Scholar
  15. DeVoe RD, Kaiser W, Ohm J, Stone LS (1982) Horizontal movement detectors of honeybees: directionally selective visual neurons in the lobula and brain. J Comp Physiol A 147:155–170.CrossRefGoogle Scholar
  16. Du Bois-Reymond E (1848) Untersuchungen über thierische Electricität. Reimer, Berlin.Google Scholar
  17. Dudai Y (1980) Cholinergic receptors of Drosophila. In: Sattelle DB, Hall LM, Hildebrand JG (eds) Receptors for Neurotransmitters, hormones and pheromones in insects. Elsevier, New York North Holland, pp 93–110.Google Scholar
  18. Dymond GR, Evans PD (1979) Biogenic amines in the nervous system of the cockroach Periplaneta americana: association of octopamine with mushroom bodies and dorsal unpaired median (DUM) neurons. Insect Biochem 9:535–545.CrossRefGoogle Scholar
  19. Elias MS, Evans PD (1983) Histamine in the insect nervous sytem: distribution, synthesis and metabolism. J Neurochem 41:562–568.PubMedCrossRefGoogle Scholar
  20. Elias MS, Evans PD (1984) Autoradiographic localization of 3H-histamine accumulation by the visual system of the locust. Cell Tissue Res 238:105–112.CrossRefGoogle Scholar
  21. Elias MS, Lummis SCR, Evans PD (1984) [3H] Mepyramine binding sites in the optic lobes of the locust: autoradiographic and pharmacological studies. Brain Res 294:359–362.PubMedCrossRefGoogle Scholar
  22. Eliot TR (1904) On the action of adrenalin. J Physiol 31:20P.Google Scholar
  23. Elofsson R, Klemm N (1972) Monoamine-containing neurons in the optic ganglia of crustaceans and insects. Z Zeilforsch 133:475–499.CrossRefGoogle Scholar
  24. Elofsson R, Kauri T, Nielsen S-O, Strömberg J-O (1966) Localization of monoaminergic neurons in the central nervous system of A stacus astacus (Crustacea). Z Zeilforsch 74:464–473.CrossRefGoogle Scholar
  25. Eskin A, Maresh RD (1982) Serotonin or electrical nerve stimulation increases the photosensitivity of the Aplysia eye. Comp Biochem Physiol 73C:27–31.Google Scholar
  26. Evans PD (1978) Octopamine distribution in the insect nervous system. J Neurochem 30:1009–1013.CrossRefGoogle Scholar
  27. Evans PD (1985) Octopamine. In: Kerkut GA, Gilbert LI (eds) Comprehensive insect physiology biochemistry and pharmacology vol 9. Pergamon, Oxford New York, pp 499–530.Google Scholar
  28. Falck B, Hillarp NA, Thieme G, Torp A (1962) Fluorescence of catecholamines and related compounds with formaldehyde. J Histochem Cytochem 10:348–354.CrossRefGoogle Scholar
  29. Fingerman M, Hanumante MM, Kulkarni GK, Ikeda R, Vacca LL (1985) Localisation of substance P-like, leucine-enkephalin-like, methionine-enkephalin-like, and FMRF-amide-like immuno-reactivity in the eyestalk of the fiddler crab, Uca pugilator. Cell Tissue Res 241:473–477.PubMedCrossRefGoogle Scholar
  30. Gorczyca MG, Hall JC (1987) Immunohistochemical localization of choline acetyltransferase during. development and in Chats mutants of Drosophila melanogaster. J Neurosci 7:1361–13PubMedGoogle Scholar
  31. Greenspan RJ (1980) Mutations of choline acetyltransferase and associated neural defects in Drosophila melanogaster. J Comp Physiol A 137:83–92.CrossRefGoogle Scholar
  32. Greenspan RJ, Finn JA, Hall JC (1980) Acetylcholinesterase mutants in Drosophila and their effects on. the structure and function of the central nervous system. J Comp Neurol 189:741–774.PubMedCrossRefGoogle Scholar
  33. Hall JC (1982) Genetics of the nervous system in Drosophila. Q Rev Biophys 15:223–4PubMedCrossRefGoogle Scholar
  34. Hamori J, Horridge GA (1966) The lobster optic lamina. II Types of synapses. J Cell Sci 1:257–270.Google Scholar
  35. Hanström B (1924) Untersuchungen über das Gehirn, insbesondere die Sehganglien der Crustaceen. Ark Zool 16:1–119.Google Scholar
  36. Hardie RC (1987) Is histamine a neurotransmitter in insect photoreceptors? J Comp Physiol A 161:201–213.PubMedCrossRefGoogle Scholar
  37. Hardie RC (1988a) The use of local ionophoresis to identify neurotransmitter candidates in the housefly, Musca domestica. J Physiol 396:7P.Google Scholar
  38. Hardie RC (1988b) Effects of antagonists on putative histamine receptors in the first visual neuropile of the housefly (Musca domestica). J Exp Biol 138:221–241.Google Scholar
  39. Hausen K (1981) Monocular and binocular computation of motion in the lobula plate ot the fly. Verh Dtsch Zool Ges 1981:49–70.Google Scholar
  40. Heisenberg M (1971) Separation of receptor and lamina potentials in the electroretinogram of normal and mutant Drosophila. J Exp Biol 55:85–100.PubMedGoogle Scholar
  41. Homberg U, Kingan TG, Hildebrand JG (1987) Immunocytochemistry of GABA in the brain and suboesophagéal ganglion of Manduca sexta. Cell Tissue Res 248:1–24.PubMedCrossRefGoogle Scholar
  42. Hotta Y, Benzer S (1970) Genetic dissection of the Drosophila nervous system by means of mosaics. Proc Natl Acad Sci USA 73:4154–4158.CrossRefGoogle Scholar
  43. Hue B, Pelhate M, Chanelet J (1979) Pre-and postsynaptic effects of taurine and GABA in the cockroach central nervous system. J Can Sci Neurol 6:243–250.Google Scholar
  44. Kingan JG, Hildebrand JG (1985) GABA in the CNS of metamorphosing and mature Manduca sexta. Insect Biochem 15:667–675.CrossRefGoogle Scholar
  45. Klemm N (1976) Histochemistry of putative transmitter substances in the insect brain. Prog Neurobiol 7:99–169.PubMedCrossRefGoogle Scholar
  46. Klemm N, Nässel DR, Osborne NN (1985) Dopamine-β-hydroxylase like immunoreactive neurons in two insect species, Calliphora erythrocephala and Periplaneta americana. Histochemistry 83:159–164.PubMedCrossRefGoogle Scholar
  47. Konopka RJ (1972) Abnormal concentrations of dopamine in a Drosophila mutant. Nature (London) 239:281–282.CrossRefGoogle Scholar
  48. Kulkarni GD, Fingerman M (1986) Distal retinal pigment of the fiddler crab, Uca pugilat or: evidence for stimulation of release of light-adapting and dark-adapting hormones by neurotransmitters. Comp Biochem Physiol 84C:2–9-224.Google Scholar
  49. Langer H, Lues I, Rivera ME (1976) Arginine phosphate in compound eyes. J Comp Physiol A 107:179–184.Google Scholar
  50. Laughlin SB, Hardie RC (1978) Common strategies for light adaptation in the peripheral visual systems of fly and dragonfly. J Comp Physiol A 128:319–340.CrossRefGoogle Scholar
  51. Lee AN, Metcalf RL, Booth GM (1973) House cricket acetylcholine esterase: histochemical localization and in situ inhibition by O,O-dimethyl s-aryl phosphorothiates. Ann Entomol Soc Am 66:333–343.Google Scholar
  52. Mancillas JR, McGinty JF, Selverston A, Karten H, Bloom FE (1981) Immunocytochemical localization of enkephalin and substance P in retina and eyestalk neurons of lobster. Nature (London) 293:576–578.CrossRefGoogle Scholar
  53. Maxwell GD, Hildebrand JG (1981) Anatomical and neurochemical consequences of deafferentiation in the development of the visual system of the moth Manduca sexta. J Comp Neurol 195:667–680.PubMedCrossRefGoogle Scholar
  54. Maxwell GD, Tait JF, Hildebrand JG (1978) Regional synthesis of neurotransmitter candidates in the CNS of the moth Manduca sexta. Comp Biochem Physiol 61C:109–119.Google Scholar
  55. McCaman RE, Weinrich D (1985) Histaminergic synaptic transmission in the cerebral ganglion of Aplysia. J Neurophysiol 53:1016–1037.PubMedGoogle Scholar
  56. Mercer AR, Mobbs PG, Davenport AP, Evans PD (1983) Biogenic amines in the brain of the honeybee, Apis mellifera. Cell Tissue Res 234:655–677.PubMedCrossRefGoogle Scholar
  57. Meyer EP, Matute C, Streit P, Nässel DR (1986) Insect optic lobe neurons identifiable with monoclonal antibodies to GABA. Histochemistry 84:207–216.PubMedCrossRefGoogle Scholar
  58. Nässel DR (1987) Serotonin and serotonin-immunoreactive neurons in the nervous system of insects. Prog Neurobiol 30:1–85.CrossRefGoogle Scholar
  59. Nässel DR, Klemm N (1983) Serotonin-like immunoreactivity in the optic lobes of three insect species. Cell Tissue Res 232:129–140.PubMedCrossRefGoogle Scholar
  60. Nässel DR, Laxmyr L (1983) Quantitative determination of biogenic amines and DOPA in the CNS of adult and larval blowflies Calliphora erythrocephala. Comp Biochem Physiol 75C:259–265.Google Scholar
  61. Nässel DR, O’Shea M (1987) Proctolin-like immunoreactive neurons in the blowfly central nervous system. J Comp Neurol 265:437–454.PubMedCrossRefGoogle Scholar
  62. Nässel DR, Hagberg M, Seyan HS (1983) A new, possibly serotonergic neuron in the lamina of the blowfly optic lobe: an immunocytochemical and Golgi-EM study. Brain Res 280:361–367.PubMedCrossRefGoogle Scholar
  63. Nässel DR, Meyer EP, Klemm N (1985) Mapping and ultrastructure of serotonin-immunoreactive neurons in the optic lobes of three insect species. J Comp Neurol 232:190–204.PubMedCrossRefGoogle Scholar
  64. Nässel DR, Ohlsson L, Sivasubramanian P (1987) Postembryonic differentiation of serotonih-im-munoreactive neurons in fleshfly optic lobes developing in situ or cultured in vivo without eye discs. J Comp Neurol 255:327–340.PubMedCrossRefGoogle Scholar
  65. Nässel DR, Holmqvist MH, Hardie RC, Hakånson R, Sundler F (1988) Histamine-like immunoreactivity in photoreceptors of the compound eyes and ocelli of flies. Cell Tissue Res 253:639–646.PubMedCrossRefGoogle Scholar
  66. Oja SS, Kontro P (1983) Taurine. In: Lathja A (ed) Handbook of Neurochemistry, vol 3, pp 501-533.Google Scholar
  67. Pitman RM (1971) Transmitter substances in insects: a review. Comp Gen Pharmacol 2:347–371.PubMedCrossRefGoogle Scholar
  68. Prell GD, Green JP (1986) Histamine as a neuroregulator. Annu Rev Neurosci 9:209–254.PubMedCrossRefGoogle Scholar
  69. Quackenbush LS, Fingerman M (1984) Regulation of neurohormone release in the fiddler crab, Uca pugilator. effects of gamma-aminobutyric acid, octopamine met-enkephalin and beta-endorphin. Comp Biochem Physiol 79C:77–84.Google Scholar
  70. Rao KR (1985) Pigmentary effectors. In: Bliss DE (ed) The biology of Crustacea, vol 9. Academic Press, Orlando New York London, pp 395–462.Google Scholar
  71. Salvaterra PM, Crawford GD, Klotz JL, Ikeda K (1983) Production and use of monoclonal antibodies to biochemically defined insect neuronal antigens. In: Breer H, Miller TA (eds) Neuroehemical techniques in insect research. Springer, Berlin Heidelberg New York, pp 223–242.Google Scholar
  72. Sattelle DB (1985) Acetylcholine receptors. In: Kerkut GA, Gilbert LI (eds) Comprehensive Insect Physiology Biochemistry and Pharmacology. Pergamon, Oxford New York, pp 395–434.Google Scholar
  73. Schäfer S (1987) Immunocytologische Untersuchungen am Bienengehirn. Phd Thesis Free Univ Berlin.Google Scholar
  74. Schäfer S, Bicker G (1986a) Common projection areas of 5-HT and GABA-like immunoreactive fibres in the visual system of the honeybee. Brain Res 380:368–370.PubMedCrossRefGoogle Scholar
  75. Schäfer S, Bicker G (1986b) Distribution of GABA-like immunoreactivity in the brain of the honeybee. J Comp Neurol 246:287–300.PubMedCrossRefGoogle Scholar
  76. Schäfer S, Bicker G, Ottersen OP, Storm-Mathiesen J (1988) Taurine-like immunoreactivity in the brain of the honeybee. J Comp Neurol 268:60–70.PubMedCrossRefGoogle Scholar
  77. Scheidler A, Kaulen P, Bruning G, Erber J (1986) Autoradiographic localisation of octopamine and serotonin-binding sites in the brain of the honeybee. Verh Dtsch Zool Ges 79:293.Google Scholar
  78. Schmidt-Nielsen BK, Gepner JI, Teng NNH, Hall LM (1977) Characterisation of an α-bungarotoxin binding component from Drosophila melanogaster. J Neurochem 29:1013–1031.PubMedCrossRefGoogle Scholar
  79. Schoofs L, Jegou S, Vaudry H, Verhaert P, De Loof A (1987) Localization of melanotropin-like peptides in the central nervous system of two insect species, the migratory locust, Locusta migratoria, and the fleshfly, Sarcophaga bullata. Cell Tissue Res.248:25–31.CrossRefGoogle Scholar
  80. Schürmann FW, Klemm N (1984) Serotonin-immunoreactive neurons in the brain of the honey bee. J Comp Neurol 225:570–580.PubMedCrossRefGoogle Scholar
  81. Schwartz J-C, Arrang J-M, Garbarg M, Korner M (1986) Properties and roles of the three subclasses of histamine receptors in brain. J Exp Biol 124:203–224.PubMedGoogle Scholar
  82. Shaw SR (1984) Early visual processing in insects. J Exp Biol 112:225–251.PubMedGoogle Scholar
  83. Simmons PJ, Hardie RC (1988) Evidence that histamine is a neurotransmitter of photoreceptors in the locust ocellus. J Exp Biol 138:205–219.Google Scholar
  84. Steinbusch HWM, Verhofstad AAJ, Joosten HWJ (1978) Localization of serotonin in the central nervous system by immunocytochemistry: description of a specific and sensitive technique and some applications. Neuroscience 3:811–819.PubMedCrossRefGoogle Scholar
  85. Strausfeld NJ, Blest AD (1970) Golgi studies on insects. Pt 1. The optic lobes of lepidoptera. Philos Trans R Soc London Ser B 258:81–134.CrossRefGoogle Scholar
  86. Strausfeld NJ, Nässel DR (1981) Neuroarchitecture of brain regions that subserve the compound eyes of Crustacea and Insects. In: Autrum H (ed) In: Handbook of sensory physiology, vol VII/6B. Springer, Berlin Heidelberg New York, pp 1–134.Google Scholar
  87. Torre V, Poggio T (1978) A synaptic mechanism possibly underlying directional selectivity to motion. Proc R Soc London Ser B 202:409–416.CrossRefGoogle Scholar
  88. Usherwood PNR (1978) Amino acids as neurotransmitters. Adv Comp Physiol Biochem 7:227–309.PubMedGoogle Scholar
  89. Vieillemaringe J, Duris P, Geffard M, Moal Ml, Delaage M, Bensch C, Girardie J (1984) Immu-nohistochemical localisation of dopamine in the brain of the insect Locusta migratoria migratorioides in comparison with the catecholamine distribution determined by the histofluorescence technique. Cell Tissue Res 237:391–394.PubMedCrossRefGoogle Scholar
  90. Wafford KA, Sattelle DB (1986) Effects of amino-acid neurotransmitter candidates on an identified insect motoneurone. Neurosci Lett 63:135–140.PubMedCrossRefGoogle Scholar
  91. White K, Hurteau T, Punsal P (1986) Neuropeptide-FMRFamide-like immunoreactivity in Drosophila: Development and distribution. J Comp Neurol 247:430–438.PubMedCrossRefGoogle Scholar
  92. Whitton PS, Strang RHC, Nicholson RA (1987) The distribution of taurine in the tissues of some species of insects. Insect Biochem 17:573–577.CrossRefGoogle Scholar
  93. Wright TRF (1987) Genetics of Biogenic Amine Metabolism, sclerotization and melanization in Drosophila melanogaster. Adv Genet 25:00–00.Google Scholar
  94. Zimmerman RP (1978) Field potential analysis and the physiology of second-order neurons in the visual system of the fly. J Comp Physiol A 126:297–317.CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 1989

Authors and Affiliations

  • Roger C. Hardie
    • 1
  1. 1.CambridgeEngland

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