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Cell and Tissue Research

, Volume 221, Issue 2, pp 351–39 | Cite as

Fine structural localisation of acetylcholinesterase activity in the compound eye of the honeybee (Apis mellifica L.)

  • Karl Kral
  • Lothar Schneider
Article

Summary

Acetylcholinesterase (AChE) activity was demonstrated histochemically at the electron microscopic level in the compound eye of the worker bee (Apis mellifica L.) by use of the method of Lewis and Shute (1969).

All photoreceptor axons (short and long visual fibres) display AChE activity. The reaction product is located in the axoplasm and at the plasma membrane. Substantial amounts of the reaction product can be detected in the intercellular spaces between the visual fibres. Along the visual fibres, the enzyme activity is unevenly distributed. High AChE activity is present in the distal parts of the axons, in contrast to lower enzyme levels in the lamina. However, AChE is also present in the proximal terminals of the visual fibres as well as in the intercellular spaces between visual fibre terminals and the postsynaptic neurones (monopolar cells). Intracellular enzyme activity is almost absent in the monopolars.

The authors assume the high AChE activity in the visual fibres to be indicative of acetylcholine as the transmitter at the first synapse of the compound eye. This hypothesis is discussed in view of the results of autoradiographic, electrophysiological and pharmacological investigations of the compound eye and of the ocellus. Our data are at variance with results of studies on the eyes of Diptera.

Key words

Visual system, bee Photoreceptor cells Acetylcholinesterase Electron-microscopic histochemistry 

References

  1. Autrum H, Zettler F, Järvilehto M (1970) Postsynaptic potentials from a single monopolar neuron of the ganglion opticum I of the blowfly Calliphora. Z vergl Physiol 70:414–424Google Scholar
  2. Barker DL, Herbert E, Hildebrand JG, Kravitz EA (1972) Acetylcholine and lobster sensory neurones. J Physiol 226:205–229Google Scholar
  3. Breer H (1981) Comparative studies on cholinergic activities in the central nervous system of Locusta migratoria. J Comp Physiol 141:271–275Google Scholar
  4. Campos-Ortega JA (1974) Autoradiographic localization of 3H-γ-aminobutyric acid uptake in the lamina ganglionaris of Musca and Drosophila. Z Zellforsch 147:415–431Google Scholar
  5. Chappell RL, Dowling JE (1972) Neural organization of the median ocellus of the dragonfly. I. Intracellular electrical activity. J Gen Physiol 60:121–147Google Scholar
  6. Dudai Y (1980) Cholinergic receptors of Drosophila. In: Satelle DB et al. (eds) Receptors for neurotransmitters, hormones and pheromones in insects. Elsevier/North-Holland Biomedical Press, Amsterdam, pp 93–110Google Scholar
  7. Dudai Y, Amsterdam A (1977) Nicotinic receptors in the brain of Drosophila melanogaster demonstrated by autoradiography with (125J)α-bungarotoxin. Brain Res 130:551–555Google Scholar
  8. Emson PC, Bush BMH, Joseph MH (1976) Transmitter metabolizing enzymes and free amino acid levels in sensory and motor nerves and ganglia of the shore crab Carcinus maenas. J Neurochem 26:779–783Google Scholar
  9. Florey E (1967) Neurotransmitters and modulators in the animal kingdom. Fed Proc 26:1164–1178Google Scholar
  10. Florey E (1973) Acetylcholine as sensory transmitter in Crustacea. J Comp Physiol 83:1–16Google Scholar
  11. Florey E, Michelson MJ (1973) Occurrence, pharmacology and significance of cholinergic mechanisms in the animal kingdom In: Michelson MJ (ed) I.E.P.T., Section 85, Comparative Pharmacology, Chapter 21 pp 11–41Google Scholar
  12. Frontali N, Piazza R, Scopelliti R (1971) Localization of acetylcholinesterase in the brain of Periplaneta americana. J Insect Physiol 17: 1833–1842Google Scholar
  13. 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 189:741–774Google Scholar
  14. Guy RG, Goodman LJ, Mobbs PG (1979) Visual interneurons in the bee brain: synaptic organisation and transmission by graded potentials (A). J Comp Physiol 134:253–264Google Scholar
  15. Hildebrand JG, Townsel JG, Kravitz EA (1974) Distribution of ACh, choline, choline acetyltransferase and acetylcholinesterase in regions and single identified axons of the lobster nervous system. J Neurochem 23:951–963Google Scholar
  16. Järvilehto M, Zettler F (1973) Electrophysiological — hislological studies on some functional properties of visual cells and second order neurones of an insect retina. Z Zellforsch 136:291–306Google Scholar
  17. Kerkut GA, Cottrell (1963) Acetylcholine and 5-hydroxytryptamine in the snail brain. Comp Biochem Physiol 8: 53–63Google Scholar
  18. Klingman A, Chappell RL (1978) Feedback synaptic interaction in the dragonfly ocellar retina. J Gen Physiol 71:157–175Google Scholar
  19. Kral K (1980) Acetylcholinesterase in the ocellus of Apis mellifica, J Insect Physiol 26:807–809Google Scholar
  20. Laughlin SB (1976) Adaptations of the dragonfly retina for contrast detection and the elucidation of neural principles in the peripheral visual system. In: Zettler F, Weiler A (eds) Neural principles in vision. Springer, Berlin Heidelberg New York, p 175Google Scholar
  21. Leake LD, Walker RJ (1980) Invertebrate neuropharmacology. Blackie, Glasgow and LondonGoogle Scholar
  22. Lehman J, Fibiger HC (1979) Acetylcholinesterase and the cholinergic neuron. Life Sciences 25:1939–1947Google Scholar
  23. Lewis PR, Shute CCD (1969) An electron microscopic study of cholinesterase distribution in the rat adrenal medulla. J Microsc 89:181–193Google Scholar
  24. Patterson JA, Goodman LJ (1974a) Intracellular responses of receptor cells and second-order cells in the ocelli of the desert locust, Schistocerca gregaria. J Comp Physiol 95:237–250Google Scholar
  25. Pichon Y (1974) The pharmacology of the insect nervous system. In: Rockstein M (ed) The physiology of Insecta. Academic Press, New York, 2nd Edn Vol IVGoogle Scholar
  26. Prescott DJ, Hildebrand JG, Sanes JR, Jewett S (1977) Biochemical and developmental studies of ACh metabolism in the CNS of the moth Manduca sexta. Comp Biochem Physiol 56 C: 77–84Google Scholar
  27. Ribi WA (1979) The first optic ganglion of the bee III. Regional comparison of the morphology of photoreceptor-cell axons. Cell Tissue Res 200:345–357Google Scholar
  28. Rudloff E (1978) Acetylcholine receptors in the central nervous system of Drosophila melanogaster. Exp Cell Res 111:185–190Google Scholar
  29. Sanes JR, Hildebrand JG (1976) Acetylcholine and its metabolic enzymes in developing antennae of the moth Manduca sexta. Dev Biol 52:105–120Google Scholar
  30. Smith DS, Treherne JE (1965) Electron microscope localization of acetylcholinesterase activity in the central nervous system of an insect (Periplaneta americana). J Cell Biol 26:445–465Google Scholar
  31. Storm-Methisen J (1977) Localization of transmitter candidates in the brain: the hippocampal formation as a model. Progr Neurobiol 8:119–181Google Scholar
  32. Treherne JE (1974) The environment and function of insect nerve cells. In: Treherne JE (ed) Insect neurobiology. North-Holland Publishing Company, Amsterdam-Oxford, p 233Google Scholar
  33. Vogt M (1946) Response of the imaginal disc to experimental defects, Drosophila. Biol Zentralbl 65:223–238Google Scholar
  34. Wilson M (1978b) Generation of graded potential signals in the second order cells of locust ocellus. J Comp Physiol 124:317–331Google Scholar
  35. Winteringham FPW (1966) Metabolism and significance of acetylcholine in the brain of the adult housefly, Musca domestica L. J Insect Physiol 12:909–924Google Scholar
  36. Zettler F, Weiler R (1976) Neuronal processing in the first optic neuropile of the compound eye of the fly. In: Zettler F, Weiler R (eds) Neural principles in vision. Springer, Berlin Heidelberg New York, p 227Google Scholar
  37. Zimmerman RP (1978) Field potential analysis and the physiology of second-order neurons in the visual system of the fly. J Comp Physiol 126:297–316Google Scholar

Copyright information

© Springer-Verlag 1981

Authors and Affiliations

  • Karl Kral
    • 1
    • 2
  • Lothar Schneider
    • 1
    • 2
  1. 1.Department of ZoologyUniversity of GrazGrazAustria
  2. 2.Department of ZoologyUniversity of WürzburgWürzburgFederal Republic of Germany

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