Skip to main content
SpringerLink
Log in

GABA and glutamate-like immunoreactivity at synapses received by dorsal unpaired median neurones in the abdominal nerve cord of the locust

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

Abstract

Dorsal unpaired median (DUM) neurones in the abdominal ganglia of the locust were impaled with microelectrodes and some were injected intracellularly with horseradish peroxidase so that their synapses could be identified in the electron microscope. Simultaneous recordings from DUM neurones in different abdominal ganglia revealed that they received common postsynaptic potentials from descending interneurones. Post-embedding immunocytochemistry using antibodies against GABA and glutamate was carried out on ganglia containing HRP-stained neurones. GABA-like immunoreactivity was found in 39% (n=82) of processes presynaptic to abdominal DUM neurones and glutamate-like immunoreactivity in 21% (n=42) of presynaptic processes. Output synapses from the DUM neurites were rarely observed within the neuropile. Structures resembling presynaptic dense bars but not associated with synaptic vesicles, were seen in some large diameter neurites.

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

Access this article

Log in via an institution

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

  • Bicker G, Schäfer S, Ottersen OP, Storm-Mathisen J (1988) Glutamate-like immunoreactivity in identified neuronal populations of insect nervous systems. J Neurosci 8:2108–2122

    Google Scholar 

  • Brookes SHJ, Weevers R de G (1988) Unpaired median neurones in a Lepidopteran larva (Antherea pernyi). I. Anatomy and physiology. J Exp Biol 136:311–332

    Google Scholar 

  • Bräunig P (1991) Suboesophageal DUM neurones innervate the principal neuropiles of the locust brain. Phil Trans R Soc Lond [Biol] 332:221–240

    Google Scholar 

  • Buma P, Roubos EW (1986) Ultrastructural demonstration of non-synaptic release sites in the central nervous system of the snail Lymnaea stagnalis, and the insect Periplaneta americana, and the rat. Neuroscience 17:867–879

    Google Scholar 

  • Burrows M, Watson AHD, Brunn DE (1989) Physiological and ultrastructural characterization of a central synaptic connection between identified motor neurones in the locust. Eur J Neurosci 1:111–126

    Google Scholar 

  • Christensen TA, Carlson AD (1981) Symmetrically organised dorsal unpaired median (DUM) neurones and flash control in the male firefly, Photuris versicolor. J Exp Biol 93:133–147

    Google Scholar 

  • Christenson J, Cullheim S, Grillner S, Hökfelt T (1990) 5-Hydroxytryptamine immunoreactive varicosities in the lamprey spinal cord have no synaptic specializations — an ultrastructural study. Brain Res 512:201–109

    Google Scholar 

  • Crossman AR, Kerkut GA, Walker RJ (1971) Axon pathways of electrically excitable cell bodies in the insect nervous system. J Physiol 218:55–56

    Google Scholar 

  • Davis NT, Alanis J (1979) Morphological and electrophysiological characteristics of a dorsal unpaired median neurone of the cricket, Acheta domesticus. Comp Biochem Physiol [A] 62:777–788

    Google Scholar 

  • Dubas F (1990) Inhibitory effect of L-glutamate on the neuropile arborizations of flight motoneurones in locusts. J Exp Biol 148:501–508

    Google Scholar 

  • Dubas F (1991) Actions of putative amino-acid transmitters on the neuropile arborisations of locust flight motoneurones. J Exp Biol 155:337–356

    Google Scholar 

  • Eckert M, Rapus J, Nürnberger A, Penzlin H (1992) A new specific antibody reveals octopamine-like immunoreactivity in cockroach ventral nerve cord. J Comp Neurol 322:1–15

    Google Scholar 

  • Evans PD, O'Shea M (1978) The identification of an octopaminergic neurone and the modulation of a myogenic rhythm in the locust. J Exp Biol 73:235–260

    Google Scholar 

  • Ferber M, Pflüger H-J (1990) Bilaterally projecting neurones in pregenital abdominal ganglia of the locust: anatomy and peripheral targets. J Comp Neurol 302:447–460

    Google Scholar 

  • Goodman CS, Heitler WJ (1979) Electrical properties of insect neurones with spiking and non-spiking somata: normal, axotomised and colchicine treated neurones. J Exp Biol 83:95–121

    Google Scholar 

  • Goodman CS, Spitzer NC (1979) Embryonic development of identified neurones: differentiation from neuroblast to neurone. Nature 280:208–214

    Google Scholar 

  • Goodman CS, Spitzer NC (1981) The mature electrical properties of identified neurones in grasshopper embryos. J Physiol 313:369–384

    Google Scholar 

  • Goodman CS, Bate M, Spitzer NC (1981) Embryonic development of identified neurones: origin and transformation of the H cell. J Neurosci 1:94–102

    Google Scholar 

  • Gras H, Hörner M, Runge L, Schürmann F-W (1990) Prothoracic DUM neurons of the cricket Gryllus bimaculatus respond to natural stimuli activie in walking behaviour. J Comp Physiol [A] 166:901–904

    Google Scholar 

  • Heitler WJ, Burrows M (1977a) The locust jump. I. The motor programme. J Exp Biol 66:203–219

    Google Scholar 

  • Heitler WJ, Burrows M (1977b) The locust jump. II. Neural circuits of the motor programme. J Exp Biol 66:221–241

    Google Scholar 

  • Heitler WJ, Goodman CS (1978) Multiple sites of spike initiation in a bifurcating locust neurone. J Exp Biol 76:63–84

    Google Scholar 

  • Horseman BG, Seymour C, Bermudez I, Beadle DJ (1988) The effect of L-glutamate on cultured insect neurons. Neurosc Letts 85:65–70

    Google Scholar 

  • Hoyle G (1975) Evidence that insect dorsal unpaired median (DUM) neurones are octopaminergic. J Exp Zool 193:425–431

    Google Scholar 

  • Hoyle G (1978) The dorsal unpaired median neurons of the locust metathoracic ganglion. J Neurobiol 9:43–57

    Google Scholar 

  • Hoyle G, Barker L (1975) Synthesis of octopamine by insect dorsal median unpaired neurons. J Exp Zool 193:433–439

    Google Scholar 

  • Hoyle G, Burrows M (1973) Neural mechanisms underlying behavior in the locust Schistocerca gregaria. I. Physiology of identified motorneurons in the metathoracic ganglion. J Neurobiol 4:3–41

    Google Scholar 

  • Hoyle G, Dagan D (1978) Physiological characteristics and reflex activation of DUM (octopaminergic) neurones of locust metathoracic ganglion. J Neurobiol 9:59–79

    Google Scholar 

  • Hoyle G, Colquhoun W, Williams M (1980) Fine structure of an octopaminergic neuron and its terminals. J Neurobiol 11:103–126

    Google Scholar 

  • Kalogianni E, Pflüger H-J (1992) The identification of motor and unpaired median neurones innervating the locust oviduct. J Exp Biol 168:177–198

    Google Scholar 

  • Kalogianni E, Theophilidis G (1993) Centrally generated rhythmic activity and modulatory function of the oviductal dorsal unpaired median (DUM) neurones in two Orthopteran species (Calliptamus sp. and Decticus albifrons). J Exp Biol 174:123–138

    Google Scholar 

  • Kiss T, Varanka I, Benedekzy I (1984) Neuromuscular transmission in the visceral muscle of locust oviduct. Neuroscience 12:309–322

    Google Scholar 

  • Konings PNM, Vullings HGB, GeffardM, Buijs RM, Diederen JHB, Jansen WF (1988) Immunocytochemical demonstration of octopamine-immunoreactive cells in the nervous system of Locusta migratoria and Schistocerca gregaria. Cell Tissue Res 251:371–379

    Google Scholar 

  • Lange AB, Orchard I (1984) Dorsal unpaired neurones and ventral bilaterally paired neurones project to a visceral muscle in an insect. J Neurobiol 15:441–453

    Google Scholar 

  • Lapied B, Malecot CO, Oelhate M (1990) Patch clamp study of the properties of the sodium current in cockroach single isolated adult aminergic neurones. J Exp Biol 151:387–403

    Google Scholar 

  • Morton DB, Evans PD (1984) Octopamine release from an identified neurone in the locust. J Exp Biol 113:269–287

    Google Scholar 

  • Newland PL, Smith PJS, Howe EA (1993) Regenerating adult cockroach dorsal unpaired median neurones in vitro retain their in vivo membrane characteristics. J Exp Biol 179:323–329

    Google Scholar 

  • Oertal D, Linberg KA, Case JF (1975) Ultrastructure of the larval firefly light organ as related to control of light emission. Cell Tissue Res 164:27–44

    Google Scholar 

  • Orchard I, Lange AB (1985) Evidence for octopaminergic modulation of an insect visceral muscle. J Neurobiol 16:171–181

    Google Scholar 

  • Orchard I, Lange AB (1987) Cockroach oviducts: the presence and release of octopamine and proctolin. J Insect Physiol 33:265–268

    Google Scholar 

  • Ottersen OP (1987) Post-embedding light- and electron microscopic immunocytochemistry of amino-acids: description of a new model system allowing identical conditions for specificity testing and tissue processing. Exp Br Res 69:167–174

    Google Scholar 

  • Pflüger HJ, Watson AHD (1988) Structure and distribution of Dorsal Unpaired Median (DUM) neurones in the abdominal nerve cord of male and female locusts. J Comp Neurol 268:329–345

    Google Scholar 

  • Pflüger H-J, Witten JL, Levine RB (1993) Fate of abdominal ventral unpaired median cells during metamorphosis of the hawkmoth, Manduca sexta. J Comp Neurol 335:508–522

    Google Scholar 

  • Pitman RM (1971) Transmitter substances in insects: a review. Comp Gen Pharmacol 2:347–371

    Google Scholar 

  • Pitman RM (1985) Pharmacology: the insect nervous system. In: Kerkut GA, Gilbert LI (eds) Comprehensive insect physiology, biochemistry and pharmacology, vol. 11. Pergamon Press, Oxford New York, pp 5–54

    Google Scholar 

  • Plotnikova SI (1969) Effector neurones with several axons in the ventral nerve cord of the Asian grasshopper, Locusta migratoria. J Evol Biochem Physiol 5:276–278

    Google Scholar 

  • Ridet JL, Rajaofetra N, Teilhac JR, Geffard M, Privat A (1993) Evidence for nonsynaptic serotonergic and noradrenergic innervation of the rat dorsal horn and possible involvement of neuron-glia interactions. Neuroscience 52:143–157

    Google Scholar 

  • Sombati S, Hoyle G (1984a) Generation of specific behaviors in a locust by release into neuropil of the natural neuromodulator octopamine. J Neurobiol 15:481–506

    Google Scholar 

  • Sombati S, Hoyle G (1984b) Glutamatergic central nervous transmission in locusts. J Neurobiol 15:507–516

    Google Scholar 

  • Spörhase-Eichmann U, Vullings HGB, Buijs RM, Hörner M (1992) Octopamine-immunoreactive neurones in the central nervous system of the cricket, Gryllus bimaculatus. Cell Tissue Res 268:287–304

    Google Scholar 

  • Stevenson PA, Kutsch W (1986) Basic circuitry of an adult-specific motor program completed with embryogenesis. Naturwissenschaften 73:741–742

    Google Scholar 

  • Stevenson PA, Kutsch W (1987) A reconsideration of the central pattern generator concept for locust flight. J Comp Physiol 161:115–129

    Google Scholar 

  • Stevenson PA, Pflüger HJ, Eckert M, Rapus J (1992) Octopamine immunoreactive cell populations in the locust thoracic-abdominal nervous system. J Comp Neurol 315:382–397

    Google Scholar 

  • Stevenson PA, Pflüger H-J, Eckert M, Rapus J (1994) Octopamine-like immunoreactive neurones in locust genital ganglia. Cell Tissue Res 275:299–308

    Google Scholar 

  • Storm-Mathisen J, Leknes AK, Bore AT, Vaaland JL, Edminson P, Haug F, Ottersen OP (1983) First visualisation of glutamate and GABA in neurones by immunocytochemistry. Nature 301:517–520

    Google Scholar 

  • Sun XJ, Tolbert LP, Hildebrand JG (1993) Ramification pattern and ultrastructural characteristics of the serotonin-immunoreactive neruron in the antennal lobe of the moth Manduca sexta: a laser scanning confocal and electron mocroscopic study. J Comp Neurol 338:5–16

    Google Scholar 

  • Thompson KJ, Siegler MVS (1989) Properties of the small dorsal unpaired median (DUM) neurons of the grasshopper. Soc Neurosci Abs 15:1296

    Google Scholar 

  • Thompson KJ, Siegler MVS (1991) Anatomy and physiology of spiking local and intersegmental interneurons in the median neuroblast lineage of the grasshopper. J Comp Neurol 305:659–675

    Google Scholar 

  • Usherwood PNR (1979) Glutamate receptors in eukaryotes. Adv Pharmacol Chemother 1:107–116

    Google Scholar 

  • Usherwood PNR, Machili P, Leaf G (1968) L-glutamate at insect nerve-muscle synapses. Nature 219:1169–1172

    Google Scholar 

  • Usherwood PNR, Giles D, Suter C (1980) Studies of the pharmacology of insect neurones in vitro. In: Insect neurobiology and pesticide action (Neurotox 79)'. Society of Chemical Industry, London, pp 115–128

    Google Scholar 

  • Wafford KA, Sattelle DB (1986) Effects of amino acid neurotransmitter candidates on an identified insect motoneurone. Neurosci Letts 63:135–140

    Google Scholar 

  • Watson AHD (1984) The dorsal unpaired median neurons of the locust metathoracic ganglion: neuronal structure and diversity, and synapse distribution. J Neurocytol 13:303–327

    Google Scholar 

  • Watson AHD (1986) The distribution of GABA-like immunoreactivity in the thoracic nervous system of the locust Schistocerca gregaria. Cell Tissue Res 246:331–341

    Google Scholar 

  • Watson AHD (1988) Antibodies against GABA and glutamate label neurones with morphologically distinct synaptic vesicles in locust central nervous system. Neuroscience 26:33–44

    Google Scholar 

  • Watson AHD, Burrows M (1981) Input and output synapses on identified motor neurones of a locust revealed by the intracellular injection of horseradish peroxidase. Cell Tissue Res 215:325–332

    Google Scholar 

  • Watson AHD, Burrows M (1987) Immunocytochemical and pharmacological evidence for GABAergic spiking local interneurones in the locust. J Neurosci 7:1741–1751

    Google Scholar 

  • Watson AHD, Pflüger HJ (1987) The distribution of GABA-like immunoreactivity in relation to ganglion structure in the abdominal nerve cord of the locust (Schistocerca gregaria). Cell Tissue Res 249:391–402

    Google Scholar 

  • Watson AHD, Seymour-Laurent KJ (1993) The distribution of glutamate-like immunoreactivity in the thoracic and abdominal ganglia of the locust (Schistocerca gregaria). Cell Tissue Res 273:557–570

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Institut für Neurobiologie, Freie Universität, Königin-Luise-Strasse 28-30, D-14195, Berlin, Germany

    H. -J. Pflüger

  2. Anatomy Unit, School of Molecular and Medical Biosciences, University of Wales College of Cardiff, Museum Avenue, PO Box 911, CF1 3US, Cardiff, UK

    A. H. D. Watson

Authors
  1. H. -J. Pflüger
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. A. H. D. Watson
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Pflüger, H.J., Watson, A.H.D. GABA and glutamate-like immunoreactivity at synapses received by dorsal unpaired median neurones in the abdominal nerve cord of the locust. Cell Tissue Res 280, 325–333 (1995). https://doi.org/10.1007/BF00307805

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00307805

Key words

Search

Navigation