Journal of Comparative Physiology A

, Volume 161, Issue 2, pp 201–213 | Cite as

Is histamine a neurotransmitter in insect photoreceptors?

  • R. C. Hardie


Intracellular recordings were made from the large monopolar cells (LMC's) in the first visual neuropil (lamina) of the flyMusca, whilst applying pharmacological agents from a three-barrelled ionophoretic pipette (Fig. 1). Most of the known neurotransmitter candidates (except the neuropeptides) were tested. The LMC's were most sensitive to histamine, saturating with ionophoretic pulses of less than 2 nC. The responses to histamine were fast hyperpolarizations with maximum amplitudes similar to that of the light-induced response (Fig. 3). Like the light response, the histamine response was associated with a conductance increase (Fig. 5). The histamine responses were not blocked by a synaptic blockade induced by ionophoretic application of cobalt ions (Fig. 6). Several histamine antagonists, and also atropine, were effective at blocking or reducing both the response to histamine and the response to light (Fig. 7). Other transmitter candidates having marked effects on the LMC's were: a) the acidic amino-acids, L-aspartate and L-glutamate, which evoked slower hyperpolarizations that could be blocked by cobalt (Fig. 11); b) GABA, which induced a depolarization associated with an inhibition of the light response (Fig. 9); and c) acetylcholine which also caused a depolarization (Fig. 10). Substances with no obvious effect on the LMC's included serotonin (5-HT),β-alanine, dopamine, octopamine, glycine, taurine and noradrenalin. Together with the evidence of Elias and Evans (1983), which shows the presence, synthesis and inactivation of histamine in the retina and optic lobes of the locust, the data suggest that histamine is a neurotransmitter in insect photoreceptors.


Histamine Taurine Light Response Octopamine Optic Lobe 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.





γ-amino butyric acid




5-hydroxy-tryptamine (or serotonin)


class of fly photoreceptors


large monopolar cell

L1, L2 andL3

classes thereof


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Autrum H, Hoffmann E (1957) Die Wirkung von Pikrotoxin und Nikotin auf das Retinogramm von Insekten. Z Naturforsch 12b:752–757Google Scholar
  2. Buchner E, Buchner S, Crawford O, Mason WT, Salvaterra PM, Sattelle DB (1986) Choline acetyltransferase-like immunoreactivity in the brain ofDrosophila melanogaster. Cell Tissue Res 246:57–62Google Scholar
  3. Campos-Ortega JA (1974) Autoradiographic localization of3H-γ-aminobutyric acid uptake in the lamina ganglionaris ofMusca andDrosophila. Z Zellforsch 147:415–431Google Scholar
  4. Clairborne BJ, Selverston AI (1984) Histamine as a neurotransmitter in the stomatogastric nervous system of the spiny lobster. J Neurosci 4:708–721Google Scholar
  5. Datum K-H, Weiler R, Zettler F (1986) Immunocytochemical demonstration ofγ-amino butyric acid and ‘glutamic acid’ decarboxylase in R7 photoreceptors and C2 centrifugal fibres in the blowfly visual system. J Comp Physiol A 159:241–249Google Scholar
  6. Dudai Y (1980) Cholinergic receptors ofDrosophila. In: Sattelle DB, Hall LM, Hildebrand JG (eds) Receptors for neurotransmitters, hormones and pheromones in insects. Elsevier North Holland, New York, pp 93–110Google Scholar
  7. Elias MS, Evans PD (1983) Histamine in the insect nervous system: distribution, synthesis and metabolism. J Neurochem 41:562–568Google Scholar
  8. Elias MS, Evans PD (1984) Autoradiographic localization of3H-histamine accumulation by the visual system of the locust. Cell Tissue Res 238:105–112Google Scholar
  9. Elias MS, Lummis SCR, Evans PD (1984) [3H] mepyramine binding sites in the optic lobes of the locust: autoradiographic and pharmacological studies. Brain Res 294:359–362Google Scholar
  10. Greenspan RJ (1980) Mutations of choline acetyltransferase and associated neural defects inDrosophila melanogaster. J Comp Physiol 137:83–92Google Scholar
  11. Hall JC (1982) Genetics of the nervous system inDrosophila. Q Rev Biophys 15:223–479Google Scholar
  12. Hall JG, Hicks TP, McLennan H, Richardson TL, Wheal HV (1979) The excitation of mammalian central neurones by amino acids. J Physiol 286:29–39Google Scholar
  13. Heisenberg M (1971) Separation of receptor and lamina potentials in the electroretinogram of normal and mutantDrosophila. J Exp Biol 55:85–100Google Scholar
  14. Hotta Y, Benzer S (1970) Genetic dissection of theDrosophila nervous sysem by means of mosaics. Proc Natl Acad Sci USA 73:4154–4158Google Scholar
  15. Järvilehto M, Zettler F (1973) Electrophysiological-histological studies on some functional properties of visual cells and second order neurons of an insect retina. Z Zellforsch 136:291–306Google Scholar
  16. Klingman A, Chappell RL (1978) Feedback synaptic interaction in the dragonfly ocellar retina. J Gen Physiol 71:157–175Google Scholar
  17. Konopka RJ (1972) Abnormal concentrations of dopamine in aDrosophila mutant. Nature (Lond) 239:281–282Google Scholar
  18. Laughlin SB (1974a) Resistance changes associated with the response of insect monopolar neurons. Z Naturforsch 29c:449–450Google Scholar
  19. Laughlin SB (1974b) Neural integration in the first optic neuropile of dragonflies II. Receptor signal interactions in the lamina. J Comp Physiol 92:357–375Google Scholar
  20. Laughlin SB (1981) Neural principles in the peripheral visual system of invertebrates. In: Autrum H (ed) Vision in invertebrates (Handbook of sensory physiology, vol VII/6B). Springer, Berlin Heidelberg New York, pp 133–280Google Scholar
  21. Laughlin SB, Hardie RC (1978) Common strategies for light adaptation in the peripheral visual systems of fly and dragonfly. J Comp Physiol 128:319–340Google Scholar
  22. Laughlin SB, Howard J, Blakeslee B (1987) Synaptic limitations to contrast coding in the retina of the blowflyCalliphora. Proc R Soc Lond B (in press)Google Scholar
  23. McCaman RE, Weinreich D (1985) Histaminergic synaptic transmission in the cerebral ganglion ofAplysia. J Neurophysiol 53:1016–1037Google Scholar
  24. Meyer EP, Matute C, Streit P, Nässel DR (1986) Insect optic lobe neurons identifiable with monoclonal antibodies to GABA. Histochemistry 84:207–216Google Scholar
  25. Misgeld U, Deisz RA, Dodt HU, Lux HD (1986) The role of chloride transport in postsynaptic inhibition of hippocampal neurons. Science 232:1413–1415Google Scholar
  26. Muijser H (1979) The receptor potential of retinular cells of the blowflyCalliphora: the role of sodium, potassium and calcium ions. J Comp Physiol 132:87–95Google Scholar
  27. Nicol D, Meinertzhagen IA (1982) An analysis of the number and composition of the synaptic populations formed by photoreceptors of the fly. J Comp Neurol 207:29–44Google Scholar
  28. Pelhate M, Sattelle DB (1982) Pharmacological properties of insect axons: a review. J Insect Physiol 28:889–893Google Scholar
  29. Prell GD, Green JP (1986) Histamine as a neuroregulator. Annu Rev Neurosci 9:209–254Google Scholar
  30. Purves RD (1979) The physics of iontophoretic pipettes. J Neurosci Methods 1:165–178Google Scholar
  31. Roberts F (1981) The in vitro iontophoretic release of radiolabelled histamine, N2-methyl-histamine and GABA from 7-barrelled glass micropipettes. Neuropharmacol 20:711–714Google Scholar
  32. Saint Marie RL, Carlson SD (1983) Glial membrane specializations and the compartmentalization of the lamina ganglionaris of the housefly compound eye. J Neurocytol 12:234–275Google Scholar
  33. Sattelle D, Pinnock RD, Wafford KA, David JA (in press) GABA receptors on the cell body membrane of an identified insect motorneuron. Proc R Soc Lond BGoogle Scholar
  34. 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 124:203–224Google Scholar
  35. Shaw SR (1984) Early visual processing in insects. J Exp Biol 112:225–251Google Scholar
  36. Strausfeld NJ, Nässel DR (1981) Neuroarchitecture of brain regions that subserve the compound eyes of Crustacea and insects. In: Autrum H (ed) Vision in invertebrates. (Handbook of sensory physiology, vol VII/6B). Springer, Berlin Heidelberg New York, pp 1–134Google Scholar
  37. Weinreich D, Weiner C, McCaman R (1975) Endogenous levels of histamine in single neurons isolated from CNS ofAplysia californica. Brain Res 84:341–345Google Scholar
  38. Wilson M, Garrard P, McGiness S (1978) The unit structure of the locust compound eye. Cell Tissue Res 195:205–226Google Scholar
  39. Zimmerman RP (1978) Field potential analysis and the physiology of second-order neurons in the visual system.Google Scholar

Copyright information

© Springer-Verlag 1987

Authors and Affiliations

  • R. C. Hardie
    • 1
  1. 1.Max-Planck Institut für Biologische KybernetikTübingenFederal Republic of Germany

Personalised recommendations