Inhibitory neurotransmission and olfactory memory in honeybees

Neurobiology of Learning and Memory

Volumn 90, Issue 4, 2008, Pages 589-595

  El Hassani, Abdessalam Kacimi ^a   Giurfa, Martin ^a   Gauthier, Monique ^a   Armengaud, Catherine ^a  

^a Université Paul Sabatier   (France)

Author keywords

Apis mellifera; GABA; GluCl; Honeybee; Ligand gated chloride channels; Olfactory memory

Indexed keywords

4 AMINOBUTYRIC ACID; 4 AMINOBUTYRIC ACID RECEPTOR STIMULATING AGENT; CHLORIDE CHANNEL; GLUTAMATE RECEPTOR; GLUTAMATE TRANSPORTER; IVERMECTIN; TACA; UNCLASSIFIED DRUG;

ARTICLE; CONTROLLED STUDY; HONEYBEE; LEARNING; LONG TERM MEMORY; MEMORY CONSOLIDATION; NEUROTRANSMISSION; NONHUMAN; OLFACTORY MEMORY;

ANIMALS; BEES; CHLORIDE CHANNELS; DICARBOXYLIC ACIDS; GAMMA-AMINOBUTYRIC ACID; GLUTAMIC ACID; IVERMECTIN; MANDIBLE; MEMORY; PYRROLIDINES; SMELL; SYNAPTIC TRANSMISSION;

EID: 55149107864     PISSN: 10747427     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.nlm.2008.07.018     Document Type: Article

References (50)

1. Aydar E., and Beadle D.J. The pharmacological profile of GABA receptors on cultured insect neurones. Journal of Insect Physiology 45 (1999) 213-219
2. Barbara G.S., Zube C., Rybak J., Gauthier M., and Grunewald B. Acetylcholine, GABA and glutamate induce ionic currents in cultured antennal lobe neurons of the honeybee, Apis mellifera. Journal of Comparative Physiology A 191 (2005) 823-836
3. Bicker G. Histochemistry of classical neurotransmitters in antennal lobes and mushroom bodies of the honeybee. Microscopy Research and Technique 45 (1999) 174-183
4. Bicker G., Schafer S., and Kingan G.T. Mushroom body feedback interneurones in the honeybee show GABA-like immunoreactivity. Brain Research 360 (1985) 394-397
5. Bicker G., Schafer S., Ottersen O.P., and Storm-Mathisen J. Glutamate-like immunoreactivity in identified neuronal populations of insect nervous systems. Journal of Neurosciences 8 (1988) 2108-2122
6. Bitterman M.E., Menzel R., Fietz A., and Schäfer S. Classical conditioning of proboscis extension in honeybees (Apis mellifera). Journal of Comparative Psychology 97 (1983) 107-119
7. Cleland T. Inhibitory glutamate receptor channels. Molecular Neurobiology 13 (1996) 97-136
8. Cole L.M., Nicholson R.A., and Casida J.E. Action of phenylpyrazole insecticides at the GABA-gated chloride channel. Pesticide Biochemistry and Physiology 46 (1993) 47-54
9. Cully D.F., Paress P.S., Liu K.K., Schaeffer J.M., and Arena J.P. Identification of a Drosophila melanogaster glutamate-gated chloride channel sensitive to the antiparasitic agent avermectin. Journal of Biological Chemistry 271 (1996) 20187-20191
10. Dent J.A., Smith M.M., Vassilatis D.K., and Avery L. The genetics of avermectin resistance in Caenorhabditis elegans. Proceedings of the National Academy of Sciences of the United States of America 97 (2000) 2674-2679
11. El Hassani A.K., Dacher M., Gauthier M., and Armengaud C. Effects of sublethal doses of fipronil on the behavior of the honeybee (Apis mellifera). Pharmacology Biochemistry and Behavior 82 (2005) 30-39
12. Fairman W.A., Vandenberg R.J., Arriza J.L., Kavanaugh M.P., and Amara S.G. An excitatory amino-acid transporter with properties of a ligand-gated chloride channel. Nature 375 (1995) 599-603
13. Ferguson H.J., Cobey S., and Smith B. Sensitivity to a change in reward is heritable in the honeybee, Apis mellifera. Animal Behavior 61 (2001) 527-532
14. Funada M., Yasuo S., Yoshimura T., Ebihara S., Sasagawa H., Kitagawa Y., et al. Characterization of the two distinct subtypes of metabotropic glutamate receptors from honeybee, Apis mellifera. Neuroscience Letters 359 (2004) 190-194
15. Ganeshina O., and Menzel R. GABA-immunoreactive neurons in the mushroom bodies of the honeybee: An electron microscopic study. Journal of Comparative Neurology 27 (2001) 335-349
16. Gerber B., Wüstenberg D., Schütz A., and Menzel R. Temporal determinants of olfactory long-term retention in honeybee classical conditioning: Nonmonotonous effects of the training trial interval. Neurobiology of Learning and Memory 69 (1998) 71-78
17. Giurfa M. Behavioral and neural analysis of associative learning in the honeybee: A taste from the magic well. Journal of Comparative Physiology A 193 (2007) 801-824
18. Guerrieri F., Schubert M., Sandoz J.-C., and Giurfa M. Perceptual and neural olfactory similarity in honeybees. PLoS Biology 3 (2005) e60
19. Horoszok L., Raymond V., Sattelle D.B., and Wolstenholme A.J. GLC-3: A novel fipronil and BIDN-sensitive, but picrotoxin-insensitive, l-glutamate-gated chloride channel subunit from Caenorhabditis elegans. British Journal of Pharmacology 132 (2001) 1247-1254
20. Hosie A.M., and Sattelle D.B. Allosteric modulation of an expressed homo-oligomeric GABA-gated chloride channel of Drosophila melanogaster. British Journal of Pharmacology 117 (1996) 1229-1237
21. Hosler J., Buxton K., and Smith B. Impairment of olfactory discrimination by blockade of GABA and nitric oxide activity in the honeybee antennal lobes. Behavioral Neuroscience 114 (2000) 514-525
22. Ikeda T., Zhao X., Kono Y., Yeh J., and Narahashi T. Fipronil modulation of glutamate-induced chloride currents in cockroach thoracic ganglion neurons. Neurotoxicology 24 (2003) 807-815
23. Janssen D., Derst C., Buckinx R., Van den Eynden J., Rigo J.M., and Van Kerkhove E. Dorsal unpaired median neurons of Locusta migratoria express ivermectin- and fipronil-sensitive glutamate-gated chloride channels. Journal of Neurophysiology 97 (2007) 2642-2650
24. Jones A.K., and Sattelle D. The cys-loop ligand-gated ion channel superfamily of the honeybee, Apis mellifera. Invertebrate Neuroscience 6 (2006) 123-132
25. Kane N.S., Hirschberg B., Qian S., Hunt D., Thomas B., Brochu R., et al. Drug-resistant Drosophila indicate glutamate-gated chloride channels are targets for the antiparasitic nodulisporic acid and ivermectin. Proceedings of the National Academy of Sciences of the United States of America 97 (2000) 13949-13954
26. Komischke B., Giurfa M., Lachnit H., and Malun D. Successive olfactory reversal learning in honeybees. Learning & Memory 9 (2002) 122-129
27. Kucharski R., Mitri C., Grau Y., and Maleszka R. Characterization of a metabotropic glutamate receptor in the honeybee (Apis mellifera): Implications for memory formation. Invertebrate Neuroscience 7 (2007) 99-108
28. Le Corronc H., Alix H., and Hue B. Differential sensitivity of two insect GABA-gated chloride channels to dieldrin, fipronil and picrotoxin. Journal of Insect Physiology 48 (2002) 419-431
29. Leal S., Kumar N., and Neckameyer W. GABAergic modulation of motor-driven behaviors in juvenile Drosophila and evidence for a non behavioral role for GABA transport. Journal of Neurobiology 61 (2004) 189-208
30. Liu X., Krause W.C., and Davis R.L. GABAA receptor RDL inhibits Drosophila olfactory associative learning. Neuron 56 (2007) 1090-1120
31. Liu H.P., Lin S.C., Lin C.Y., Yeh S.R., and Chiang A.S. Glutamate-gated chloride channels inhibit juvenile hormone biosynthesis in the cockroach, Diploptera punctata. Insect Biochemistry and Molecular Biology 35 (2005) 1260-1268
32. Locatelli F., Bundrock G., and Muller U. Focal and temporal release of glutamate in the mushroom bodies improves olfactory memory in Apis mellifera. Journal of Neuroscience 25 (2005) 11614-11618
33. Ludmerer S.W., Warren V.A., Williams B.S., Zheng Y., Hunt D.C., Ayer M.B., et al. Ivermectin and nodulisporic acid receptors in Drosophila melanogaster contain both gamma-aminobutyric acid-gated Rdl and glutamate-gated GluCl alpha chloride channel subunits. Biochemistry 41 (2002) 6548-6560
34. Maleszka R., Helliwell P., and Kucharski R. Pharmacological interference with glutamate re-uptake impairs long-term memory in the honeybee, Apis mellifera. Behavioural Brain Research 115 (2000) 49-53
35. Menzel R. Memory dynamics in the honeybee. Journal of Comparative Physiology A 185 (1999) 323-340
36. Okada R., Rybak J., Manz G., and Menzel R. Learning-related plasticity in PE1 and other mushroom body-extrinsic neurons in the honeybee brain. Journal of Neuroscience 27 (2007) 11736-11747
37. Oleskevich S. Cholinergic synaptic transmission in insect mushroom bodies in vitro. Journal of Neurophysiology 82 (1999) 1091-1096
38. Pérez-Orive J., Mazor O., Turner G.C., Cassenaer S., Wilson R.I., and Laurent G. Oscillations and sparsening of odor representations in the mushroom body. Science 297 (2002) 359-365
39. Portillo V., Jagannathan S., and Wolstenholmehe A.J. Distribution of glutamate-gated chloride channel subunits in the parasitic nematode Haemonchus contortus. The Journal of Comparative Neurology 462 (2003) 213-222
40. Rohrer S.P., Birzin E.T., Costa S.D., Arena J.P., Hayes E.C., and Schaeffer J.M. Identification of neuron-specific ivermectin binding sites in Drosophila melanogaster and Schistocerca americana. Insect Biochemistry and Molecular Biology 25 (1995) 11-17
41. Sachse S., and Galizia C.G. Role of inhibition for temporal and spatial odor representation in olfactory output neurons: A calcium imaging study. Journal of Neurophysiology 87 (2002) 1106-1117
42. Si A., Helliwell P., and Maleszka R. Effects of NMDA receptor antagonists on olfactory learning and memory in the honeybee (Apis mellifera). Pharmacology, Biochemistry, and Behavior 77 (2004) 191-197
43. Sinakevitch I., Farris S.M., and Strausfeld N.J. Taurine-, aspartate- and glutamate-like immunoreactivity identifies chemically distinct subdivisions of Kenyon cells in the cockroach mushroom body. The Journal of Comparative Neurology 439 (2001) 352-367
44. Smith M.M., Warren V.A., Thomas B.S., Brochu R.M., Ertel E.A., Rohrer S., et al. Nodulisporic acid opens insect glutamate-gated chloride channels: Identification of a new high affinity modulator. Biochemistry 18 (2000) 5543-5554
45. Stopfer M., Bhagavan S., Smith B., and Laurent G. Impaired odour discrimination on desynchronisation of odour-encoding neural assemblies. Nature 390 (1997) 70-74
46. Wilson R.I., and Laurent G. Role of GABAergic inhibition in shaping odor-evoked spatiotemporal patterns in the Drosophila antennal lobe. Journal of Neuroscience 5 (2005) 9069-9079
47. Wolstenholme A.J., and Rogers A.T. Glutamate-gated chloride channels and the mode of action of the avermectin/milbemycin anthelmintics. Parasitology 131 (2005) 85-95
48. Xia S., Miyashita T., Fu T.U., Lin W.Y., Wu C.L., Pyzocha L., et al. NMDA receptors mediate olfactory learning and memory in Drosophila. Current Biology 15 (2005) 603-615
49. Zannat M.T., Locatelli F., Rybak J., Menzel R., and Leboulle G. Identification and localisation of the NR1 sub-unit homologue of the NMDA glutamate receptor in the honeybee brain. Neuroscience Letters 398 (2006) 274-279
50. Zhao X., Salgado V.L., Yeh J.Z., and Narahashi T. Kinetic and pharmacological characterization of desensitizing and non-desensitizing glutamate-gated chloride channels in cockroach neurons. Neurotoxicology 25 (2004) 967-980