Skip to main content
SpringerLink
Log in

Acetylcholine, GABA and glutamate induce ionic currents in cultured antennal lobe neurons of the honeybee, Apis mellifera

  • Original Paper
  • Published:
Journal of Comparative Physiology A Aims and scope Submit manuscript

Abstract

The honeybee, Apis mellifera, is a valuable model system for the study of olfactory coding and its learning and memory capabilities. In order to understand the synaptic organisation of olfactory information processing, the transmitter receptors of the antennal lobe need to be characterized. Using whole-cell patch-clamp recordings, we analysed the ligand-gated ionic currents of antennal lobe neurons in primary cell culture. Pressure applications of acetylcholine (ACh), γ-amino butyric acid (GABA) or glutamate induced rapidly activating ionic currents. The ACh-induced current flows through a cation-selective ionotropic receptor with a nicotinic profile. The ACh-induced current is partially blocked by α-bungarotoxin. Epibatidine and imidacloprid are partial agonists. Our data indicate the existence of an ionotropic GABA receptor which is permeable to chloride ions and sensitive to picrotoxin (PTX) and the insecticide fipronil. We also identified the existence of a chloride current activated by pressure applications of glutamate. The glutamate-induced current is sensitive to PTX. Thus, within the honeybee antennal lobe, an excitatory cholinergic transmitter system and two inhibitory networks that use GABA or glutamate as their neurotransmitter were identified.

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

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

Abbreviations

AMPA:

Amino-hydroxy-5-methyl-4-isoxazol-propionic acid

BGT:

α-Bungarotoxin

ACh:

Acetylcholine

ATR:

Atropine

BIC:

Bicuculline

CACA:

4-Amino-cis-butenoic acid

CCh:

Carbamylcholine

DHE:

Dihydroxy-β-erythroidine

DTC:

D-tubocurarine

EPI:

Epibatidine

GABA:

γ-Aminobutyric acid

IMI:

Imidacloprid

MEC:

Mecamylamine

MLA:

Methyllycaconitine

NIC:

Nicotine

NMDG-Cl:

N-methyl-D-glucamine chloride

PTX:

Picrotoxin

TTX:

Tetrodotoxin

References

  • Albert JL, Lingle CJ (1993) Activation of nicotinic acetylcholine receptors on cultured Drosophila and other insect neurones. J Physiol 463:605–630

    PubMed  CAS  Google Scholar 

  • Alkondon M, Albuquerque EX (1993) Diversity of nicotinic acetylcholine receptors in rat hippocampal neurons. I. Pharmacological and functional evidence for distinct structural subtypes. J Pharmacol Exp Ther 265:1455–1473

    PubMed  CAS  Google Scholar 

  • Alkondon M, Pereira EF, Albuquerque EX (1998) Alpha-bungarotoxin- and methyllycaconitine-sensitive nicotinic receptors mediate fast synaptic transmission in interneurons of rat hippocampal slices. Brain Res 810:257–263

    Article  PubMed  CAS  Google Scholar 

  • Anthony NM, Harrison JB, Sattelle DB (1993) GABA receptor molecules of insects. Exs 63:172–209

    PubMed  CAS  Google Scholar 

  • Aydar E, Beadle DJ (1999) The pharmacological profile of GABA receptors on cultured insect neurones. J Insect Physiol 45:213–219

    Article  PubMed  CAS  Google Scholar 

  • Bazhenov M, Stopfer M, Rabinovich M, Abarbanel HD, Sejnowski TJ, Laurent G (2001a) Model of cellular and network mechanisms for odor-evoked temporal patterning in the locust antennal lobe. Neuron 30:569–581

    Article  PubMed  CAS  Google Scholar 

  • Bazhenov M, Stopfer M, Rabinovich M, Huerta R, Abarbanel HD, Sejnowski TJ, Laurent G (2001b) Model of transient oscillatory synchronization in the locust antennal lobe. Neuron 30:553–567

    Article  PubMed  CAS  Google Scholar 

  • Ben-Ari Y (2002) Excitatory actions of gaba during development: the nature of the nurture. Nat Rev Neurosci 3:728–739

    Article  PubMed  CAS  Google Scholar 

  • Benson JA (1988) Bicuculline blocks the response to acetylcholine and nicotine but not to muscarine or GABA in isolated insect neuronal somata. Brain Res 458:65–71

    Article  PubMed  CAS  Google Scholar 

  • Benson JA (1992) Electrophysiological pharmacology of the nicotinic and muscarinic cholinergic responses of isolated neuronal somata from locust thoracic ganglia. J Exp Biol 170:230–233

    Google Scholar 

  • Bicker G (1999) Histochemistry of classical neurotransmitters in antennal lobes and mushroom bodies of the honeybee. Microsc Res Tech 45:174–183

    Article  PubMed  CAS  Google Scholar 

  • Bicker G, Schäfer S, Kingan TG (1985) Mushroom body feedback interneurones in the honeybee show GABA-like immunoreactivity. Brain Res 360:394–397

    Article  PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Bidaut M (1980) Pharmacological dissection of pyloric network of the lobster stomatogastric ganglion using picrotoxin. J Neurophysiol 44:1089–1101

    PubMed  CAS  Google Scholar 

  • Bornhauser BC, Meyer EP (1997) Histamine-like immunoreactivity in the visual system and brain of an orthopteran and a hymenopteran insect. Cell Tissue Res 287:211–221

    Article  PubMed  CAS  Google Scholar 

  • Buckingham SD, Hosie AM, Roush RL, Sattelle DB (1994a) Actions of agonists and convulsant antagonists on a Drosophila melanogaster GABA receptor (Rdl) homo-oligomer expressed in Xenopus oocytes. Neurosci Lett 181:137–140

    Article  PubMed  CAS  Google Scholar 

  • Buckingham SD, Hue B, Sattelle DB (1994b) Actions of bicuculline on cell body and neuropilar membranes of identified insect neurones. J Exp Biol 186:235–244

    PubMed  CAS  Google Scholar 

  • Chiang AS, Lin WY, Liu HP, Pszczolkowski MA, Fu TF, Chiu SL, Holbrook GL (2002a) Insect NMDA receptors mediate juvenile hormone biosynthesis. Proc Natl Acad Sci USA 99:37–42

    Article  PubMed  CAS  Google Scholar 

  • Chiang AS, Pszczolkowski MA, Liu HP, Lin SC (2002b) Ionotropic glutamate receptors mediate juvenile hormone synthesis in the cockroach, Diploptera punctata. Insect Biochem Mol Biol 32:669–678

    Article  PubMed  CAS  Google Scholar 

  • Christensen TA, Waldrop BR, Hildebrand JG (1998) Multitasking in the olfactory system: context-dependent responses to odors reveal dual GABA-regulated coding mechanisms in single olfactory projection neurons. J Neurosci 18:5999–6008

    PubMed  CAS  Google Scholar 

  • Cleland TA (1996) Inhibitory glutamate receptor channels. Mol Neurobiol 13:97–136

    PubMed  CAS  Google Scholar 

  • Cleland TA, Selverston AI (1995) Glutamate-gated inhibitory currents of central pattern generator neurons in the lobster stomatogastric ganglion. J Neurosci 15:6631–6639

    PubMed  CAS  Google Scholar 

  • Cleland TA, Selverston AI (1998) Inhibitory glutamate receptor channels in cultured lobster stomatogastric neurons. J Neurophysiol 79:3189–3196

    PubMed  CAS  Google Scholar 

  • Courjaret R, Lapied B (2001) Complex intracellular messenger pathways regulate one type of neuronal alpha-bungarotoxin-resistant nicotinic acetylcholine receptors expressed in insect neurosecretory cells (dorsal unpaired median neurons). Mol Pharmacol 60:80–91

    PubMed  CAS  Google Scholar 

  • Cull-Candy SG (1976) Two types of extrajunctional L-glutamate receptors in locust muscle fibres. J Physiol 255:449–464

    PubMed  CAS  Google Scholar 

  • Cull-Candy SG, Usherwood PN (1973) Two populations of L-glutamate receptors on locust muscle fibres. Nat New Biol 246:62–64

    PubMed  CAS  Google Scholar 

  • Cully DF, Vassilatis DK, Liu KK, Paress PS, Van der Ploeg LH, Schaeffer JM, Arena JP (1994) Cloning of an avermectin-sensitive glutamate-gated chloride channel from Caenorhabditis elegans. Nature 371:707–711

    Article  PubMed  CAS  Google Scholar 

  • Cully DF, Paress PS, Liu KK, Schaeffer JM, Arena JP (1996) Identification of a Drosophila melanogaster glutamate-gated chloride channel sensitive to the antiparasitic agent avermectin. J Biol Chem 271:20187–20191

    Article  PubMed  CAS  Google Scholar 

  • Dacher M, Lagarrigue A, Gauthier M (2005) Antennal tactile learning in the honeybee: effect of nicotinic antagonists on memory dynamics. Neuroscience 130:37–50

    Article  PubMed  CAS  Google Scholar 

  • Déglise P, Grünewald B, Gauthier M (2002) The insecticide imidacloprid is a partial agonist of the nicotinic receptor of honeybee Kenyon cells. Neurosci Lett 321:13–16

    Article  PubMed  Google Scholar 

  • Delgado R, Barla R, Latorre R, Labarca P (1989) L-glutamate activates excitatory and inhibitory channels in Drosophila larval muscle. FEBS Lett 243:337–342

    Article  PubMed  CAS  Google Scholar 

  • Devaud JM, Quenet B, Gascuel J, Masson C (1994) A morphometric classification of pupal honeybee antennal lobe neurones in culture. Neuroreport 6:214–218

    PubMed  CAS  Google Scholar 

  • Distler P (1989) Histochemical demonstration of GABA-like immunoreactivity in cobalt labeled neuron individuals in the insect olfactory pathway. Histochemistry 91:245–249

    Article  PubMed  CAS  Google Scholar 

  • Distler P (1990a) GABA-immunohistochemistry as a label for identifying types of local interneurons and their synaptic contacts in the antennal lobes of the American cockroach. Histochemistry 93:617–626

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Distler PG, Boeckh J (1996) Synaptic connection between olfactory receptor cells and uniglomerular projection neurons in the antennal lobe of the American cockroach, Periplaneta americana. J Comp Neurol 370:35–46

    Article  PubMed  CAS  Google Scholar 

  • Distler PG, Boeckh J (1997a) Synaptic connections between identified neuron types in the antennal lobe glomeruli of the cockroach, Periplaneta americana: I. Uniglomerular projection neurons. J Comp Neurol 378:307–319

    Article  PubMed  CAS  Google Scholar 

  • Distler PG, Boeckh J (1997b) Synaptic connections between identified neuron types in the antennal lobe glomeruli of the cockroach, Periplaneta americana: II. Local multiglomerular interneurons. J Comp Neurol 383:529–540

    Article  PubMed  CAS  Google Scholar 

  • Distler PG, Boeckh J (1998) An improved model of the synaptic organization of insect olfactory glomeruli. Ann N Y Acad Sci 855:508–510

    PubMed  CAS  Google Scholar 

  • Duan S, Cooke IM (2000) Glutamate and GABA activate different receptors and Cl(−) conductances in crab peptide-secretory neurons. J Neurophysiol 83:31–37

    PubMed  CAS  Google Scholar 

  • Dubas F (1991) Actions of putative amino acid neurotransmitters in the neuropile arborizations of locust flight motoneurones. J Exp Biol 155:337–356

    CAS  Google Scholar 

  • Dwoskin LP, Crooks PA (2001) Competitive neuronal nicotinic receptor antagonists: a new direction for drug discovery. J Pharmacol Exp Ther 298:395–402

    PubMed  CAS  Google Scholar 

  • Esslen J, Kaissling K-E (1976) Zahl und Verteilung antennaler Sensillen bei der Honigbiene (Apis mellifera L.). Zoomorphology 83:227–251

    Article  Google Scholar 

  • Etter A, Cully DF, Liu KK, Reiss B, Vassilatis DK, Schaeffer JM, Arena JP (1999) Picrotoxin blockade of invertebrate glutamate-gated chloride channels: subunit dependence and evidence for binding within the pore. J Neurochem 72:318–326

    PubMed  CAS  Google Scholar 

  • Ffrench-Constant RH, Mortlock DP, Shaffer CD, MacIntyre RJ, Roush RT (1991) Molecular cloning and transformation of cyclodiene resistance in Drosophila: an invertebrate gamma-aminobutyric acid subtype A receptor locus. Proc Natl Acad Sci USA 88:7209–7213

    PubMed  CAS  Google Scholar 

  • Fiala A, Spall T, Diegelmann S, Eisermann B, Sachse S, Devaud JM, Buchner E, Galizia CG (2002) Genetically expressed cameleon in Drosophila melanogaster is used to visualize olfactory information in projection neurons. Curr Biol 12:1877–1884

    Article  PubMed  CAS  Google Scholar 

  • Gallo V, Haydar T (2003) GABA: exciting again in its own right. J Physiol 550:665

    Article  PubMed  CAS  Google Scholar 

  • Gascuel J, Masson C (1991) A quantitative ultrastructural study of the honeybee antennal lobe. Tissue Cell 23:341–355

    Article  PubMed  CAS  Google Scholar 

  • Goldberg F, Grünewald B, Rosenboom H, Menzel R (1999) Nicotinic acetylcholine currents of cultured Kenyon cells from the mushroom bodies of the honey bee Apis mellifera. J Physiol 514:759–768

    Article  PubMed  CAS  Google Scholar 

  • Grolleau F, Sattelle DB (2000) Single channel analysis of the blocking actions of BIDN and fipronil on a Drosophila melanogaster GABA receptor (RDL) stably expressed in a Drosophila cell line. Br J Pharmacol 130:1833–1842

    Article  PubMed  CAS  Google Scholar 

  • Grünewald B (2003) Differential expression of voltage-sensitive K+ and Ca2+ currents in neurons of the honeybee olfactory pathway. J Exp Biol 206:117–129

    Article  PubMed  CAS  Google Scholar 

  • Guez D, Belzunces LP, Maleszka R (2003) Effects of imidacloprid metabolites on habituation in honeybees suggest the existence of two subtypes of nicotinic receptors differentially expressed during adult development. Pharmacol Biochem Behav 75:217–222

    Article  PubMed  CAS  Google Scholar 

  • Gundelfinger ED, Schulz R (2000) Insect nicotinic acetylcholine receptors: genes, structure, physiological and pharmacological properties. In: Handbook of experimental pharmacology, Neuronal nicotinic receptors 144:496–521

  • Hamill OP, Marty A, Neher E, Sakmann B, Sigworth FJ (1981) Improved patch-clamp techniques for high-resolution current recording from cells and cell-free membrane patches. Pflugers Arch 391:85–100

    Article  PubMed  CAS  Google Scholar 

  • Harvey RJ, Schmitt B, Hermans-Borgmeyer I, Gundelfinger ED, Betz H, Darlison MG (1994) Sequence of a Drosophila ligand-gated ion-channel polypeptide with an unusual amino-terminal extracellular domain. J Neurochem 62:2480–2483

    Article  PubMed  CAS  Google Scholar 

  • Henderson JE, Soderlund DM, Knipple DC (1993) Characterization of a putative gamma-aminobutyric acid (GABA) receptor beta subunit gene from Drosophila melanogaster. Biochem Biophys Res Commun 193:474–482

    Article  PubMed  CAS  Google Scholar 

  • Hermsen B, Stetzer E, Thees R, Heiermann R, Schrattenholz A, Ebbinghaus U, Kretschmer A, Methfessel C, Reinhardt S, Maelicke A (1998) Neuronal nicotinic receptors in the locust Locusta migratoria. Cloning and expression. J Biol Chem 273:18394–18404

    Article  PubMed  CAS  Google Scholar 

  • Homberg U (1984) Processing of antennal information in extrinsic mushroom body neurons of the bee brain. J Comp Phys 154:825–836

    Article  Google Scholar 

  • Homberg U (2002) Neurotransmitters and neuropeptides in the brain of the locust. Microsc Res Tech 56:189–209

    Article  PubMed  CAS  Google Scholar 

  • Homberg U, Hildebrand JG (1991) Histamine-immunoreactive neurons in the midbrain and suboesophageal ganglion of sphinx moth Manduca sexta. J Comp Neurol 307:647–657

    Article  PubMed  CAS  Google Scholar 

  • Homberg U, Kingan TG, Hildebrand JG (1987) Immunocytochemistry of GABA in the brain and suboesophageal ganglion of Manduca sexta. Cell Tissue Res 248:1–24

    Article  PubMed  CAS  Google Scholar 

  • Horoszok L, Raymond V, Sattelle DB, Wolstenholme AJ (2001) GLC-3: a novel fipronil and BIDN-sensitive, but picrotoxinin-insensitive, L-glutamate-gated chloride channel subunit from Caenorhabditis elegans. Br J Pharmacol 132:1247–1254

    Article  PubMed  CAS  Google Scholar 

  • Hosie AM, Sattelle DB (1996) Agonist pharmacology of two Drosophila GABA receptor splice variants. Br J Pharmacol 119:1577–1585

    PubMed  CAS  Google Scholar 

  • Hosie AM, Baylis HA, Buckingham SD, Sattelle DB (1995) Actions of the insecticide fipronil, on dieldrin-sensitive and -resistant GABA receptors of Drosophila melanogaster. Br J Pharmacol 115:909–912

    PubMed  CAS  Google Scholar 

  • Hosie AM, Aronstein K, Sattelle DB, ffrench-Constant RH (1997) Molecular biology of insect neuronal GABA receptors. Trends Neurosci 20:578–583

    Article  PubMed  CAS  Google Scholar 

  • Ikeda T, Zaho X, Salgado VL, Kono Y, Yeh JZ, Narahashi T (2003) Fipronil modulation of glutamate-induced chloride currents in cockroach thoracic ganglion neurons. NeuroToxicol 24:807–815

    Article  CAS  Google Scholar 

  • Jackson C, Bermudez I, Beadle DJ (2002) Pharmacological properties of nicotinic acetylcholine receptors in isolated Locusta migratoria neurones. Microsc Res Tech 56:249–255

    Article  PubMed  CAS  Google Scholar 

  • Joerges J, Küttner A, Galizia CG, Menzel R (1997) Representations of odours and odour mixtures visualized in the honeybee brain. Nature 387:285–288

    Article  CAS  Google Scholar 

  • Kehoe J (1994) Glutamate activates a K+ conductance increase in Aplysia neurons that appears to be independent of G proteins. Neuron 13:691–702

    Article  PubMed  CAS  Google Scholar 

  • Kirchhof BS, Mercer AR (1997) Antennal lobe neurons of the honey bee, Apis mellifera, express a D2-like dopamine receptor in vitro. J Comp Neurol 383:189–198

    Article  PubMed  CAS  Google Scholar 

  • Kloppenburg P, Kirchhof BS, Mercer AR (1999) Voltage-activated currents from adult honeybee (Apis mellifera) antennal motor neurons recorded in vitro and in situ. J Neurophysiol 81:39–48

    PubMed  CAS  Google Scholar 

  • Kreissl S, Bicker G (1989) Histochemistry of acetylcholinesterase and immunocytochemistry of an acetylcholine receptor-like antigen in the brain of the honeybee. J Comp Neurol 286:71–84

    Article  PubMed  CAS  Google Scholar 

  • Kreissl S, Bicker G (1992) Dissociated neurons of the pupal honeybee brain in cell culture. J Neurocytol 21:545–556

    Article  PubMed  CAS  Google Scholar 

  • Lapied B, Le Corronc H, Hue B (1990) Sensitive nicotinic and mixed nicotinic-muscarinic receptors in insect neurosecretory cells. Brain Res 533:132–136

    Article  PubMed  CAS  Google Scholar 

  • Laurent G, Davidowitz H (1994) Encoding of olfactory information with oscillating neural assemblies. Science 265:1872–1875

    PubMed  CAS  Google Scholar 

  • Laurent G, Naraghi M (1994) Odorant-induced oscillations in the mushroom bodies of the locust. J Neurosci 14:2993–3004

    PubMed  CAS  Google Scholar 

  • Laurent S, Masson C, Jakob I (2002) Whole-cell recording from honeybee olfactory receptor neurons: ionic currents, membrane excitability and odourant response in developing workerbee and drone. Eur J Neurosci 15:1139–1152

    Article  PubMed  Google Scholar 

  • Le Corronc H, Alix P, Hue B (2002) Differential sensitivity of two insect GABA-gated chloride channels to dieldrin, fipronil and picrotoxin. J Insect Physiol 48:419–431

    Article  PubMed  CAS  Google Scholar 

  • Le Novere N, Corringer PJ, Changeux JP (2002) The diversity of subunit composition in nAChRs: evolutionary origins, physiologic and pharmacologic consequences. J Neurobiol 53:447–456

    Article  PubMed  CAS  Google Scholar 

  • Leitch B, Laurent G (1996) GABAergic synapses in the antennal lobe and mushroom body of the locust olfactory system. J Comp Neurol 372:487–514

    Article  PubMed  CAS  Google Scholar 

  • Linster C, Smith BH (1997) A computational model of the response of honey bee antennal lobe circuitry to odor mixtures: overshadowing, blocking and unblocking can arise from lateral inhibition. Behav Brain Res 87:1–14

    Article  PubMed  CAS  Google Scholar 

  • Loesel R, Homberg U (1999) Histamine-immunoreactive neurons in the brain of the cockroach Leucophaea maderae. Brain Res 842:408–418

    Article  PubMed  CAS  Google Scholar 

  • Ludmerer SW, Warren VA, Williams BS, Zheng Y, Hunt DC, Ayer MB, Wallace MA, Chaudhary AG, Egan MA, Meinke PT, Dean DC, Garcia ML, Cully DF, Smith MM (2002) Ivermectin and nodulisporic acid receptors in Drosophila melanogaster contain both gamma-aminobutyric acid-gated Rdl, glutamate-gated GluCl alpha chloride channel subunits. Biochemistry 41:6548–6560

    Article  PubMed  CAS  Google Scholar 

  • MacLeod K, Laurent G (1996) Distinct mechanisms for synchronization and temporal patterning of odor-encoding neural assemblies. Science 274:976–979

    Article  PubMed  CAS  Google Scholar 

  • Malun D (1991a) Inventory and distribution of synapses of identified uniglomerular projection neurons in the antennal lobe of Periplaneta americana. J Comp Neurol 305:348–360

    Article  PubMed  CAS  Google Scholar 

  • Malun D (1991b) Synaptic relationships between GABA-immunoreactive neurons and an identified uniglomerular projection neuron in the antennal lobe of Periplaneta americana: a double-labeling electron microscopic study. Histochemistry 96:197–207

    Article  PubMed  CAS  Google Scholar 

  • Marder E, Eisen JS (1984) Transmitter identification of pyloric neurons: electrically coupled neurons use different transmitters. J Neurophysiol 51:1345–1361

    PubMed  CAS  Google Scholar 

  • Marder E, Paupardin-Tritsch D (1978) The pharmacological properties of some crustacean neuronal acetylcholine, gamma-aminobutyric acid, and L-glutamate responses. J Physiol 280:213–236

    PubMed  CAS  Google Scholar 

  • Matsuda K, Buckingham SD, Kleier D, Rauh JJ, Grauso M, Sattelle DB (2001) Neonicotinoids: insecticides acting on insect nicotinic acetylcholine receptors. Trends Pharmacol Sci 22:573–580

    Article  PubMed  CAS  Google Scholar 

  • Müller D, Abel R, Brandt R, Zöckler M (2002) Differential parallel processing of olfactory information in the honeybee, Apis mellifera L. J Comp Phys A 188:359–370

    Article  Google Scholar 

  • Nässel DR (1999) Histamine in the brain of insects: a review. Microsc Res Tech 44:121–136

    Article  PubMed  Google Scholar 

  • Nauen R, Ebbinghaus-Kintscher U, Schmuck R (2001) Toxicity and nicotinic acetylcholine receptor interaction of imidacloprid and its metabolites in Apis mellifera (Hymenoptera: Apidae). Pest Manag Sci 57:577–586

    Article  PubMed  CAS  Google Scholar 

  • Oleskevich S (1999) Cholinergic synaptic transmission in insect mushroom bodies in vitro. J Neurophysiol 82:1091–1096

    PubMed  CAS  Google Scholar 

  • Osborne RH (1996) Insect neurotransmission: neurotransmitters and their receptors. Pharmacol Ther 69:117–142

    Article  PubMed  CAS  Google Scholar 

  • Pelz C, Jander J, Rosenboom H, Hammer M, Menzel R (1999) IA in Kenyon cells of the mushroom body of honeybees resembles shaker currents: kinetics, modulation by K+, and simulation. J Neurophysiol 81:1749–1759

    PubMed  CAS  Google Scholar 

  • Pemberton DJ, Franks CJ, Walker RJ, Holden-Dye L (2001) Characterization of glutamate-gated chloride channels in the pharynx of wild-type and mutant Caenorhabditis elegans delineates the role of the subunit GluCl-alpha2 in the function of the native receptor. Mol Pharmacol 59:1037–1043

    PubMed  CAS  Google Scholar 

  • Pinnock RD, Lummis SC, Chiappinelli VA, Sattelle DB (1988) Kappa-bungarotoxin blocks an alpha-bungarotoxin-sensitive nicotinic receptor in the insect central nervous system. Brain Res 458:45–52

    Article  PubMed  CAS  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

    Article  PubMed  CAS  Google Scholar 

  • Rauh JJ, Lummis SC, Sattelle DB (1990) Pharmacological and biochemical properties of insect GABA receptors. Trends Pharmacol Sci 11:325–329

    Article  PubMed  CAS  Google Scholar 

  • Raymond V, Sattelle DB (2002) Novel animal-health drug targets from ligand-gated chloride channels. Nat Rev Drug Discov 1:427–436

    Article  PubMed  CAS  Google Scholar 

  • Raymond V, Sattelle DB, Lapied B (2000) Co-existence in DUM neurones of two GluCl channels that differ in their picrotoxin sensitivity. Neuroreport 11:2695–2701

    PubMed  CAS  Google Scholar 

  • Rybak J (1994) Die strukturelle Organisation der Pilzkörper und synaptische Konnektivität protocerebraler Interneurone im Gehirn der Honigbiene, Apis mellifera. Eine licht-und elektronenmikroskopische Studie. PhD Thesis, Freie Universität

  • Sachse S, Galizia CG (2002) Role of inhibition for temporal and spatial odor representation in olfactory output neurons: a calcium imaging study. J Neurophysiol 87:1106–1117

    PubMed  Google Scholar 

  • Sattelle DB (1992) Receptors for L-glutamate and GABA in the nervous system of an insect (Periplaneta americana). Comp Biochem Physiol C 103:429–438

    Article  PubMed  CAS  Google Scholar 

  • Sattelle DB, Lummis SC, Wong JF, Rauh JJ (1991) Pharmacology of insect GABA receptors. Neurochem Res 16:363–374

    Article  PubMed  CAS  Google Scholar 

  • Sattelle DB, Culetto E, Grauso M, Raymond V, Franks CJ, Towers P (2002) Functional genomics of ionotropic acetylcholine receptors in Caenorhabditis elegans and Drosophila melanogaster. Novartis Found Symp 245:240–257

    Article  PubMed  CAS  Google Scholar 

  • Schäfer S, Bicker G (1986) Distribution of GABA-like immunoreactivity in the brain of the honeybee. J Comp Neurol 246:287–300

    Article  PubMed  Google Scholar 

  • Schäfer S, Rosenboom H, Menzel R (1994) Ionic currents of Kenyon cells from the mushroom body of the honeybee. J Neurosci 14:4600–4612

    PubMed  Google Scholar 

  • Scheidler A, Kaulen P, Bruning G, Erber J (1990) Quantitative autoradiographic localization of [125I]alpha-bungarotoxin binding sites in the honeybee brain. Brain Res 534:332–335

    Article  PubMed  CAS  Google Scholar 

  • Schürmann FW, Ottersen OP, Honegger HW (2000) Glutamate-like immunoreactivity marks compartments of the mushroom bodies in the brain of the cricket. J Comp Neurol 418:227–239

    Article  PubMed  Google Scholar 

  • Stopfer M, Laurent G (1999) Short-term memory in olfactory network dynamics. Nature 402:664–668

    Article  PubMed  CAS  Google Scholar 

  • Stopfer M, Bhagavan S, Smith BH, Laurent G (1997) Impaired odour discrimination on desynchronization of odour-encoding neural assemblies. Nature 390:70–74

    Article  PubMed  CAS  Google Scholar 

  • Sun XJ, Tolbert LP, Hildebrand JG (1997) Synaptic organization of the uniglomerular projection neurons of the antennal lobe of the moth Manduca sexta: a laser scanning confocal and electron microscopic study. J Comp Neurol 379:2–20

    Article  PubMed  CAS  Google Scholar 

  • Tareilus E, Hanke W, Breer H (1990) Neuronal acetylcholine receptor channels from insects: a comparative electrophysiological study. J Comp Physiol A 167:521–526

    Article  PubMed  CAS  Google Scholar 

  • Thany SH, Crozatier M, Raymond-Delpech V, Gauthier M, Lenaers G (2005) Apisα2, Apisα7–1 and Apisα7–2 three new neuronal nicotinic acetylcholine receptor subunits in the brain of the honeybee Apis mellifera. Gene 344C:125–132

    Article  CAS  Google Scholar 

  • Tomizawa M, Casida JE (2001) Structure and diversity of insect nicotinic acetylcholine receptors. Pest Manag Sci 57:914–922

    Article  PubMed  CAS  Google Scholar 

  • Tornoe C, Bai D, Holden-Dye L, Abramson SN, Sattelle DB (1995) Actions of neurotoxins (bungarotoxins, neosurugatoxin and lophotoxins) on insect and nematode nicotinic acetylcholine receptors. Toxicon 33:411–424

    Article  PubMed  CAS  Google Scholar 

  • Van Eyseren I, Guillet JC, Le Guen J, Tiaho F, Pichon Y (1998) Effects of nicotinic and muscarinic ligands on embryonic neurones of Periplaneta americana in primary culture: a whole cell clamp study. J Insect Physiol 44:227–240

    Article  PubMed  CAS  Google Scholar 

  • Vassilatis DK, Arena JP, Plasterk RH, Wilkinson HA, Schaeffer JM, Cully DF, Van der Ploeg LH (1997) Genetic and biochemical evidence for a novel avermectin-sensitive chloride channel in Caenorhabditis elegans. Isolation and characterization. J Biol Chem 272:33167–33174

    Article  PubMed  CAS  Google Scholar 

  • Wafford KA, Bai D, Sepulveda MI, Sattelle B (1991) L-Glutamate receptors in the insect central nervous system. Excitatory amino acids 275–278

  • Waldrop B, Hildebrand JG (1989) Physiology and pharmacology of acetylcholinergic responses of interneurons in the antennal lobes of the moth Manduca sexta. J Comp Physiol A 164:433–441

    Article  PubMed  CAS  Google Scholar 

  • Waldrop B, Christensen TA, Hildebrand JG (1987) GABA-mediated synaptic inhibition of projection neurons in the antennal lobes of the sphinx moth, Manduca sexta. J Comp Physiol A 161:23–32

    Article  PubMed  CAS  Google Scholar 

  • Wang DD, Krueger DD, Bordey A (2003) GABA depolarizes neuronal progenitors of the postnatal subventricular zone via GABAA receptor activation. J Physiol 550:785–800

    Article  PubMed  CAS  Google Scholar 

  • Ward JM, Cockcroft VB, Lunt GG, Smillie FS, Wonnacott S (1990) Methyllycaconitine: a selective probe for neuronal alpha-bungarotoxin binding sites. FEBS Lett 270:45–48

    Article  PubMed  CAS  Google Scholar 

  • Watanabe S, Kawahara S, Kirino Y (1999) Glutamate induces Cl− and K+ currents in the olfactory interneurons of terrestrial slug. J Comp Physiol A 184:553–562

    Article  CAS  Google Scholar 

  • Wersing A, Grünewald B (2002) Ionotropic GABA and glutamate receptors in cultured honeybee Kenyon cells. Eur J Neurosci Abstr 1:216.11

    Google Scholar 

  • Witthöft W (1967) Absolute Anzahl und Verteilung der Zellen im Hirn der Honigbiene. Z Morph Tiere 61:160–184

    Article  Google Scholar 

  • Yasuyama K, Salvaterra PM (1999) Localization of choline acetyltransferase-expressing neurons in Drosophila nervous system. Microsc Res Tech 45:65–79

    Article  PubMed  CAS  Google Scholar 

  • Zhang HG, Lee HJ, Rocheleau T, ffrench-Constant RH, Jackson MB (1995) Subunit composition determines picrotoxin and bicuculline sensitivity of Drosophila gamma-aminobutyric acid receptors. Mol Pharmacol 48:835–840

    PubMed  CAS  Google Scholar 

  • Zhao X, Salgado VL, Yeh JZ, Narahashi T (2003) Differential actions of fipronil and dieldrin insecticides on GABA-gated chloride channels in cockroach neurons. J Pharmacol Exp Ther 206:914–924

    Article  CAS  Google Scholar 

  • Zhao X, Yeh JZ, Salgado VL, Narahashi T (2004) Fipronil is a potent open channel blocker of glutamate-activated chloride channels in cockroach neurons. J Pharmacol Exp Ther 310:192–201

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

We are grateful to Dr. Valerie Raymond for critically reading the manuscript, Dr. Randolf Menzel for fruitful discussions. The authors thank Marion Ganz for technical assistance with cell cultures of antennal lobe neurons; Dr. Martin Giurfa for financial support. Thanks to Marc Moreau and Catherine Leclerc for technical support. G. Barbara was supported by a doctoral grant from the French Ministry of Scientific Research and Education. This work was performed at the Freie Universität Berlin and was funded by PRESCOT, the Région Midi-Pyrénées and a DAAD/MAE PROCOPE grant D/9910368/00352UE.

Author information

Authors and Affiliations

  1. Institut für Biologie, AG Neurobiologie, Freie Universität Berlin, Königin-Luise-Str. 28-30, 14195, Berlin, Germany

    Guillaume Stephane Barbara, Christina Zube, Jürgen Rybak, Monique Gauthier & Bernd Grünewald

  2. Centre de Recherches sur la Cognition Animale-CNRS, Universite Paul Sabatier, 118 rte de Narbonne, 31062, Toulouse, France

    Guillaume Stephane Barbara & Monique Gauthier

  3. Department of Behavioural Physiology and Sociobiology (Zoologie II), Universität Würzburg Biozentrum, Am Hubland, 97074, Würzburg, Germany

    Christina Zube & Jürgen Rybak

Authors
  1. Guillaume Stephane Barbara
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Christina Zube
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jürgen Rybak
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Monique Gauthier
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Bernd Grünewald
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Bernd Grünewald.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Barbara, G.S., Zube, C., Rybak, J. et al. Acetylcholine, GABA and glutamate induce ionic currents in cultured antennal lobe neurons of the honeybee, Apis mellifera . J Comp Physiol A 191, 823–836 (2005). https://doi.org/10.1007/s00359-005-0007-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00359-005-0007-3

Keywords

Search

Navigation