Skip to main content
Log in

Aminergic neurons in the brain of blowflies and Drosophila: dopamine- and tyrosine hydroxylase-immunoreactive neurons and their relationship with putative histaminergic neurons

  • Published:
Cell and Tissue Research Aims and scope Submit manuscript

Summary

The distribution and morphology of neurons reacting with antisera against dopamine (DA), tyrosine hydroxylase (TH) and histamine (HA) were analyzed in the blowflies Calliphora erythrocephala and Phormia terraenovae. TH-immunoreactive (THIR) and HA-immunoreactive (HAIR) neurons were also mapped in the fruitfly Drosophila melanogaster. The antisera against DA and TH specifically labeled the same neurons in the blowflies. About 300 neurons displayed DA immunoreactivity (DAIR) and THIR in the brain and subesophageal ganglion of the blowflies. Most of these neurons were located in bilateral clusters; some were distributed as bilateral pairs, and two ventral unpaired median (VUM) neurons were seen in the subesophageal ganglion. Immunoreactive processes were found in all compartments of the mushroom bodies except the calyces, in all divisions of the central body complex, in the medulla, lobula and lobula plate of the optic lobe, and in non-glomerular neuropil of protocerebrum, tritocerebrum and the subesophageal ganglion. No DA or TH immunoreactivity was seen in the antennal lobes. In Drosophila, neurons homologous to the blowfly neurons were detected with the TH antiserum. In Phormia and Drosophila, 18 HA-immunoreactive neurons were located in the protocerebrum and 2 in the subesophageal ganglion. The HAIR neurons arborized extensively, but except for processes in the lobula, all HAIR processes were seen in non-glomerular neuropil. The deuto- and tritocerebrum was devoid of HAIR processes. Double labeling experiments demonstrated that TH and HA immunoreactivity was not colocalized in any neuron. In some regions there wasm however, substantial superposition between the two systems. The morphology of the extensively arborizing aminergic neurons described suggests that they have modulatory functions in the brain and subesophageal ganglion.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Bayer TA, McClintock TS, Grünert U, Ache BW (1989) Histamine induced modulation of olfactory receptor neurones in two species of lobster, Panulirus argus and Homarus americanus. J Exp Biol 145:133–146

    Google Scholar 

  • Bicker G, Menzel R (1989) Chemical codes for the control of behaviour in arthropods. Nature 337:33–39

    Google Scholar 

  • Björklund A, Falck B, Klemm N (1970) Microspectrofluorometric and chemical investigation of catecholamine-containing structures in the thoracic ganglia of Trichoptera. J Insect Physiol 16:1147–1154

    Google Scholar 

  • Bodnaryk RP (1979) Identification of specific dopamine- and octopamine-sensitive adenylate cyclases in the brain of Mamestra configurata Wlk. Insect Biochem 9:155–162

    Google Scholar 

  • Boer HH, Schot LPC, Roubos EW, Maat A, Lodder JC, Reicheld D (1979) ACTH-like immunoreactivity in two electronically coupled giant neurons in the pond snail Lymnea stagnalis. Cell Tissue Res 202:231–240

    Google Scholar 

  • Budnik V, White K (1987) Genetic dissection of dopamine and serotonin synthesis in the nervous system of Drosophila melanogaster. J Neurogenet 4:309–314

    Google Scholar 

  • Budnik V, White K (1988) Catecholamine-containing neurons in Drosophila melanogaster: distribution and development. J Comp Neurol 268:400–413

    Google Scholar 

  • Claiborne BJ, Selverston AI (1981) Histamine as a neurotransmitter in the stomatogastric nervous system of the spiny lobster. J Neurosci 4:708–721

    Google Scholar 

  • Distler P (1990) Synaptic connections of dopamine-immunoreactive neurons in the antennal lobes of Periplaneta americana. Colocalization with GABA-like immunoreactivity. Histochemistry 93:401–408

    Google Scholar 

  • Duve H, Thorpe A (1989) Distribution and functional significance of Met-enkephalin-Arg6-Phe7- and Met-enkephalin-Arg6-Gly7-Leu8-like peptides in the blowfly Calliphora vomitoria. I. Immunocytochemical mapping of neuronal pathways in the brain. Cell Tissue Res 258:147–161

    Google Scholar 

  • Elekes K, Hustert R, Geffard M (1987) Serotonin-immunoreactive and dopamine-immunoreactive neurones in the terminal ganglion of the cricket, Acheta domesticus: light and electronmicroscopic immunocytochemistry. Cell Tissue Res 250:167–180

    Google Scholar 

  • Erber J, Homberg U, Gronenberg W (1987) Functional roles of the mushroom bodies in insects. In: Gupta AP (ed) Arthropod brain: its evolution, development, structure and functions. Wiley, New York, pp 485–512

    Google Scholar 

  • Evans PD (1980) Biogenic amines in the insect nervous system. Adv Insect Physiol 15:317–473

    Google Scholar 

  • Flanagan TRJ (1984) Wholemount histofluorescence of catecholamine-containing neurons in a hemipteran brain. J Insect Physiol 30:796–804

    Google Scholar 

  • Haas HL, Greene RW, Reiner PB (1989) The brain histamine system in vitro. J Neurosci Methods 28:71–75

    Google Scholar 

  • HÃ¥kanson R, Böttcher G, Ekblad E, Panula P, Simonsson M, Dohlsten M, Hallberg T, Sundler F (1986) Histamine in endocrine cells in the stomach. A survey of several species using a panel of histamine antibodies. Histochemistry 86:5–17

    Google Scholar 

  • Hanesch U, Fischbach KF, Heisenberg M (1989) Neuronal architecture of the central complex in Drosophila melanogaster. Cell Tissue Res 257:343–366

    Google Scholar 

  • Hardie RC (1987) Is histamine a neurotransmitter in insect photoreceptors? J Comp Physiol 161:201–213

    Google Scholar 

  • Hardie RC (1989) A histamine-activated chloride channel involved in neurotransmission at a photoreceptor synapse. Nature 339:704–706

    Google Scholar 

  • Heisenberg M, Borst A, Wagner S, Byers D (1985) Drosophila mushroom body mutants are deficient in olfactory learning. J Neurogenet 2:1–30

    Google Scholar 

  • Hiripi L, Rózsa KS (1979) Adenylate cyclase as a receptor for monoamines and a peptide transmitter proctolin in the insect brain. In: Vizi ES, Wolleman M (eds) Aminergic and peptidergic receptors. Adv Pharmacol Res Pract 7:57–69

  • Homberg U (1987) Structure and functions of the central complex of insects. In: gupta AP (ed) Arthropod brain. Its evolution, development, structure and functions. Wiley, New York, pp 347–367

    Google Scholar 

  • Homberg U (1991) Neuroarchitecture of the central complex in the brain of the locust Schistocerca gregaria and S. americana as revealed by serotonin immunocytochemistry. J Comp Neurol 303:245–254

    Google Scholar 

  • Klemm N (1974) Vergleichend-histochemistche Untersuchungen über die Verteilung monoaminhaltiger Strukturen im Oberschlundganlion von Angehörigen verschiedener Insekten-Ordnungen. Entomol Germ 1:21–49

    Google Scholar 

  • Klemm N (1976) Histochemistry of putative transmitter substances in the insect brain. Progr Neurobiol 7:99–169

    Google Scholar 

  • Klemm N (1983a) Organization of catecholamine and serotonin-immunoreactive neurons in the corpora pedunculata of the desert locust, Schistocerca greagaria Fors. Neurosci Lett 36:13–17

    Google Scholar 

  • Klemm N (1983b) Monoamine containing neurons and their projections in the brain (supraoesophageal ganglion) of cockroaches. An aldehyde fluorescence study. Cell Tissue Res 229:379–402

    Google Scholar 

  • Klemm N, Axelsson S (1973) Determination of dopamine, noradrenaline and 5-hydroxytryptamine in the brain of the desert locust Schistocerca gregaria Forsk. (Insecta, Orthoptera). Brain Res 57:289–298

    Google Scholar 

  • Klemm N, Nässel DR, Osborne NN (1985) Dopamine-β-hydroxylase-like immunoreactive neurons in two insect species, Calliphora erythrocephala and Periplaneta americana. Histochemistry 85:159–164

    Google Scholar 

  • Konrad KD, Marsh JL (1987) Developmental expression of and spatial distribution of dopa decarboxylase in Drosophila. Dev Biol 122:172–185

    Google Scholar 

  • Livingstone MS, Tempel BL (1983) Genetic dissection of monoamine neurotransmitter synthesis in Drosophila. Nature 303:67–70

    Google Scholar 

  • Lundquist CT, Nässel DR (1990) Substance P-, FMRFamide-, and gastrin/cholecystokinin-like immunoreactive neurons in the thoraco-abdominal ganglia of the flies Drosophila and Calliphora. Comp Neurol 294:161–178

    Google Scholar 

  • Lundquist T, Rökaeus Ã…, Nässel DR (1991) Galanin immunoreactivity in the blowfly nervous system: localization and chromatographic analysis. J Comp Neurol 312:314–333

    Google Scholar 

  • Macmillan CS, Mercer AR (1987) An investigation of the role of dopamine in the antennal lobes of the honey bee, Apis mellifera. J Comp Physiol 160:359–366

    Google Scholar 

  • McClintock TS, Ache BW (1989) Histamine directly gates a chloride channel in lobster olfactory receptor neurons. Proc Natl Acad Sci USA 86:8137–8141

    Google Scholar 

  • Mercer AR (1982) The effects of amines on behaviour and neuronal activity in the honey bee. In: Breed MD, Mitchener CD, Evans HE (eds) The biology of social insects. Westview Press, Boulder, pp 360–363

    Google Scholar 

  • Mercer AR (1987) Biogenic amines in the insect brain. In: Gupta AP (ed) Arthropod brain: its evolution, development, structure and functions. Wiley, New York, pp 399–414

    Google Scholar 

  • Mercer AR, Menzel R (1982) The effects of biogenic amines on conditioned and unconditioned responses to olfactory stimuli in the honey bee Apis mellifera. J Comp Physiol 145:363–368

    Google Scholar 

  • Mercer AR, Mobbs PG, Davenport AP, Evans PD (1983) Biogenic amines in the brain of the honey Apis mellifica. Cell Tissue Res 234:655–677

    Google Scholar 

  • Meyer EP, Matute C, Streit P, Nässel DR (1986) Insect optic lobe neurons identifiable with monoclonal antibodies to GABA. Histochemistry 84:207–216

    Google Scholar 

  • Nässel DR (1987) Aspects of the functional and chemical anatomy of the insect brain. In: MA Ali (ed) Nervous systems of invertebrates. Plenum, New York, pp 353–392

    Google Scholar 

  • Nässel DR (1988) Serotonin and serotonin-immunoreactive neurons in the insect nervous system. Progr Neurobiol 30:1–85

    Google Scholar 

  • 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 

  • Nässel DR, Lundquist CT (1989) Substance P-like immunoreactivity in a subpopulation of the FMRFamide-like immunoreactive neurons in Drosophila and Calliphora. Soc Neurosci Abstr 15:364

    Google Scholar 

  • Nässel DR, Lundquist CT (1991) Insect tachykinin-like peptide: distribution of leucokinin immunoreactive neurons in the cockroach and blowfly brains. Neurosci Lett 130:225–228

    Google Scholar 

  • Nässel DR, O'Shea M (1987) Proctolin-like immunoreactive neurons in the blowfly central nervous system. J Comp Neurol 265:437–454

    Google Scholar 

  • Nässel DR, Elekes K, Johansson KUI (1988a) Dopamine immunoreactive neurons in the blowfly visual system: light and electron microscopic immunocytochemistry. J Chem Neuroanat 1:311–325

    Google Scholar 

  • Nässel DR, Holmqvist MH, Hardie RC, HÃ¥kanson R, Sundler F (1988b) Histamine-like immunoreactivity in photoreceptors of the compound eyes and ocelli of the flies Calliphora erythrocephala and Musca domestica. Cell Tissue Res 253:639–646

    Google Scholar 

  • Nässel DR, Pirvola U, Panula P (1990) Histamine-like immunoreactive neurons innervating putative neurohaemal areas and central neuropil in the thoraco-abdominal ganglia of the flies Calliphora and Drosophila. J Comp Neurol 297:525–536

    Google Scholar 

  • Neckameyer WS, Quinn WG (1989) Isolation and characterization of the gene for Drosophila tyrosine hydroxylase. Neuron 2:1167–1175

    Google Scholar 

  • Orchard I (1991) Tyrosine hydroxylase-like immunoreactivity in previously described catecholamine-containing neurons in the ventral nerve chord of Rhodnius prolixus. J Insect Physiol 36:593–600

    Google Scholar 

  • Orchard I, Gole WD, Downer RGH (1983) Pharmacology of aminergic receptors mediating an elevation in cyclic AMP and release of hormone from locust neurosecretory cells. Brain Res 288:349–353

    Google Scholar 

  • Orona E, Battelle BA, Ache BW (1990) Immunohistochemical and biochemical evidence for the putative inhibitory neurotransmitters histamine and GABA in lobster olfactory lobes. Comp Neurol 294:633–646

    Google Scholar 

  • Orr GL, Gole JWD, Notman HJ, Downer RGH (1987) Pharmacological characterization of the dopamine sensitive adenylate cyclase in cockroach brain: evidence for a distinct dopamine receptor. Life Sci 41:2705–2715

    Google Scholar 

  • Panula P, Yang HYT, Costa E (1984) Histamine-containing neurons in the rat hypothalamus. Proc Natl Acad Sci USA 81:2572–2576

    Google Scholar 

  • Panula P, Häppölä O, Airaksinen MS, Auvinen S, Virkamäki A (1988) Carbodiimide as a tissue fixation in histamine immunohistochemistry and its application to developmental biology. J Histochem Cytochem 36:259–269

    Google Scholar 

  • Panula P, Airaksinen MS, Pirvola U, Kotilainen E (1990) A histamine-containing neuronal system in human brain. Neuroscience 34:127–132

    Google Scholar 

  • Pearse AGE, Polak JM (1975) Bifunctional reagents as vapourand liquid phase fixatives for immunohistochemistry. Histochem J 7:179–186

    Google Scholar 

  • Pirvola U, Tuomisto L, Yamatodani A, Panula P (1988) Distribution of histamine in the cockroach brain and visual system: an immunocytochemical and biochemical study. J Comp Neurol 276:514–526

    Google Scholar 

  • Prell GD, Green JP (1986) Histamine as a neuroregulator. Ann Rev Neurosci 9:209–254

    Google Scholar 

  • Schäfer S, Rehder V (1989) Dopamine-like immunoreactivity in the brain and suboesophageal ganglion of the honey bee. J Comp Neurol 280:43–58

    Google Scholar 

  • Schürmann F-W (1987) The architecture of the mushroom bodies and related neuropils in the insect brain. In: Gupta AP (ed) Arthropod brain: its evolution, development, structure and functions. Wiley, New York, pp 231–264

    Google Scholar 

  • Schürmann F-W, Elekes K (1987) Synaptic connectivity in the mushroom bodies of the honey bee brain: electron microscopy and immunocytochemistry of neuroactive compounds. In: Menzel R, Mercer A (eds) Neurobiology and behaviour of honey bees. Springer, Berlin Heidelberg New York, pp 225–234

    Google Scholar 

  • Schürmann F-W, Elekes K, Geffard M (1989) Dopamine-like immunoreactivity in the bee brain. Cell Tissue Res 256:399–410

    Google Scholar 

  • Skiebe P, Corrette BJ, Wiese K (1990) Evidence that histamine is the inhibitory transmitter of the auditory interneuron ON1 of crickets. Neurosci Lett 116:361–366

    Google Scholar 

  • Steinbusch HWM, Tilders FJH (1987) Immunocytochemical techniques for light microscopical localization of dopamine, noradrenaline, adrenaline, serotonin and histamine in the central nervous system. In: Steinbusch HWM (ed) Monoaminergic neurons: light microscopy and ultrastructure. Wiley, Chichester, pp 125–166

    Google Scholar 

  • Steinbusch HWM, Bol JGJM, De vent J (1987) Development of dopamine antibodies raised against glutaraldehyde versus formaldehyde coupled dopamine and characterized in non-biological as well as biological models. Neuroscience [Suppl] 22:S373

  • Strausfeld NJ (1976) Atlas of an insect brain. Springer, Berlin Heidelberg New York

    Google Scholar 

  • Strausfeld NJ, Bacon JP (1983) Multimodal convergence in the central nervous system of insects. In: Horn E (ed) Multimodal convergence in sensory systems. Fischer, Stuttgart, pp 47–76

    Google Scholar 

  • Takeda S, Viellemaringe J, Geffard M, Rémy C (1986) Immunohistological evidence of dopamine cells in the cephalic nervous system of the silkworm Bombyx mori. Co-existence of dopamine and α-endorphin-like substance in neurosecretory cells of suboesophageal ganglion. Cell Tissue Res 243:125–128

    Google Scholar 

  • Tempel BL, Livingstone MS, Quinn WG (1984) Mutations in the dopa decarboxylase gene effects learning in Drosophila. Proc Natl Acad Sci USA 81:3577–3581

    Google Scholar 

  • Uzzan A, Dudai Y (1982) Aminergic receptors in Drosophila melanogaster: responsiveness of adenylate cyclase to putative neurotransmitters. J Neurochem 38:1542–1550

    Google Scholar 

  • Viellemaringe J, Duris P, Geffard M, LeMoal M, Delaage M, Bensch C, Girardie J (1984) Immunohistochemical localization of dopamine in the brain of the insect Locusta migratoria migratorioides in comparison with catecholamine distribution determined by the histofluorescence technique. Cell Tissue Res 237:391–394

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Nässel, D.R., Elekes, K. Aminergic neurons in the brain of blowflies and Drosophila: dopamine- and tyrosine hydroxylase-immunoreactive neurons and their relationship with putative histaminergic neurons. Cell Tissue Res 267, 147–167 (1992). https://doi.org/10.1007/BF00318701

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00318701

Key words

Navigation