Differential expression of voltage-sensitive K+ and Ca2+ currents in neurons of the honeybee olfactory pathway

Journal of Experimental Biology

Volumn 206, Issue 1, 2003, Pages 117-129

  Grünewald, Bernd ^a  

^a FREIE UNIVERSITÄT BERLIN   (Germany)

Author keywords

Antennal lobe; Apis mellifera; Calcium dependent K+ current; Honeybee; Insect; Mushroom body; Neuron; Olfactory; Patch clamp

Indexed keywords

CALCIUM; CALCIUM CHANNEL; POTASSIUM; POTASSIUM CHANNEL;

ANIMAL; ARTICLE; BEE; CELL MEMBRANE POTENTIAL; CYTOLOGY; IN VITRO STUDY; ION TRANSPORT; METABOLISM; OLFACTORY RECEPTOR; OLFACTORY SYSTEM;

ANIMALS; BEES; CALCIUM; CALCIUM CHANNELS; ION TRANSPORT; MEMBRANE POTENTIALS; OLFACTORY PATHWAYS; OLFACTORY RECEPTOR NEURONS; POTASSIUM; POTASSIUM CHANNELS;

ANIMALIA; APIS MELLIFERA; APOIDEA; BASIDIOMYCOTA; INSECTA;

EID: 0037235517     PISSN: 00220949     EISSN: None     Source Type: Journal    
DOI: 10.1242/jeb.00053     Document Type: Article

References (78)

1. Abel, R., Rybak, J. and Menzel, R. (2001). Structure and response patterns of olfactory interneurons in the honeybee, Apis mellifera. J. Comp. Neurol. 437, 363-383.
2. + currents in lamina cells of the desert locust Schistocerca gregaria. J. Exp. Biol. 202, 1939-1951.
3. Bicker, G., Schäfer, S. and Kingan, T. G. (1985). Mushroom body feedback interneurons in the honeybee show GABA-like immunoreactivity. Brain Res. 360, 394-397.
4. Byerly, L. and Leung, H.-T. (1988). Ionic currents of Drosophila neurons in embryonic cultures. J. Neurosci. 8, 4379-4393.
5. David, J. A. and Pitman, R. M. (1995). Calcium and potassium currents in the fast coxal depressor motor neuron of the cockroach Periplaneta americana. J. Neurophysiol. 74, 2043-2050.
6. Deglise, P., Grünewald, B. and Gauthier, M. (2002). The insecticide imidacloprid is a partial agonist of the nicotinic receptor of honeybee Kenyon cells. Neurosci. Lett. 321, 13-16.
7. Delgado, R., Davis, R. L., Bono, M. R., Latorre, R. and Labarca, P. (1998). Outward currents in Drosophila larval neurons: dunce lacks a maintained outward current component downregulated by cAMP. J. Neurosci. 18, 1399-1407.
8. Devaud, J. M., Quenet, B., Gascuel, J. and Masson, C. (1994). A morphometric classification of pupal honeybee antennal lobe neurones in culture. NeuroRep. 6, 214-218.
9. Dugladze, T., Heinemann, U. and Gloveli, T. (2001). Entorhinal cortex projection cells to the hippocampal formation in vitro. Brain Res. 905, 224-231.
10. Erber, J., Homberg, U. and Gronenberg, W. (1987). Functional roles of the mushroom bodies in insects. In Arthropod brain: Its Evolution, Development, Structure and Functions (ed. A. P. Gupta), pp. 485-511. New York: John Wiley and Sons.
11. Erber, J., Masuhr, T. and Menzel, R. (1980). Localization of short-term memory in the brain of the bee, Apis mellifera. Physiol. Entomol. 5, 343-358.
12. Fiala, A., Müller, U. and Menzel, R. (1999). Reversible downregulation of protein kinase A during olfactory learning using antisense technique impairs long-term memory formation in the honeybee, Apis mellifera. J. Neurosci. 19, 10125-10134.
13. Fonta, C., Sun, X.-J. and Masson, C. (1993). Morphology and spatial distribution of bee antennal lobe interneurones responsive to odours. Chem. Senses 18, 101-119.
14. Gascuel, J. and Masson, C. (1991a). A quantitative ultrastructural study of the honeybee antennal lobe. Tissue Cell 23, 341-355.
15. Gascuel, J. and Masson, C. (1991b). Developmental study of afferented and deafferented bee antennal lobes. J. Neurobiol. 22, 795-810.
16. Goldberg, F., Grünewald, B., Rosenboom, H. and 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.
17. Grolleau, F. and Lapied, B. (1995). Separation and identification of multiple potassium currents regulating the pacemaker activity of insect neurosecretory cells (DUM neurons). J. Neurophysiol. 73, 160-171.
18. 2+ currents contribute to the pacemaker mechanism in cockroach dorsal unpaired median neurons. J. Neurophysiol. 76, 963-976.
19. Grolleau, F. and Lapied, B. (2000). Dorsal unpaired median neurones in the insect central nervous system: towards a better understanding of the ionic mechanisms underlying spontaneous electrical activity. J. Exp. Biol. 203, 1633-1648.
20. Grünbaum, L. and Müller, U. (1998). Induction of a specific olfactory memory leads to a long-lasting activation of protein kinase C in the antennal lobe of the honeybee. J. Neurosci. 18, 4384-4392.
21. Grünewald, B. (1999a). Morphology of feedback neurons in the mushroom body of the honeybee, Apis mellifera. J. Comp. Neurol. 404, 114-126.
22. Grünewald, B. (1999b). Physiological properties and response modulations of mushroom body feedback neurons during olfactory learning in the honeybee, Apis mellifera. J. Comp. Physiol. A 185, 565-576.
23. Hamill, O. P., Neher, E., Marty, A., Sakman, B. and Sigworth, F. J. (1981). Improved patch-clamp techniques for high-resolution current recording from cells and cell-free membrane patches. Pflügers Arch. Eur. J. Physiol. 391, 85-100.
24. Hammer, M. (1993). An identified neuron mediates the unconditioned stimulus in associative olfactory learning in honeybees. Nature 366, 59-63.
25. Hammer, M. (1997). The neural basis of associative reward learning in honeybees. Trends Neurosci. 20, 245-252.
26. Hammer, M. and Menzel, R. (1995). Learning and memory in the honeybee. J. Neurosci. 15, 1617-1630.
27. Hammer, M. and Menzel, R. (1998). Multiple sites of associative odor learning as revealed by local brain microinjections of octopamine in honeybees. Learn. Mem. 5, 146-156.
28. Hayashi, J. H. and Hildebrand, J. G. (1990). Insect olfactory neurons in vitro: morphological and physiological characterization of cells from the developing antennal lobes of Manduca sexta. J. Neurosci. 10, 848-859.
29. Hayashi, J. H. and Levine, R. B. (1992). Calcium and potassium currents in leg motoneurons during postembryonic development in the hawkmoth Manduca sexta. J. Exp. Biol. 171, 15-42.
30. Hewes, R. S. (1999). Voltage-dependent ionic currents in the ventromedial eclosion hormone neurons of Manduca sexta. J. Exp. Biol. 202, 2371-2383.
31. Hildebrandt, H. and Müller, U. (1995). Octopamine mediates rapid stimulation of protein kinase A in the antennal lobe of honeybees. J. Neurobiol. 27, 44-50.
32. Homberg, U. (1984). Processing of antennal information in extrinsic mushroom body neurons of the bee brain. J. Comp. Physiol. A 154, 825-836.
33. + channels in glutamatergic hippocampal terminals and their role in spike repolarization and regulation of transmitter release. J. Neurosci. Meth. 21, 9585-9597.
34. Ikeno, H. and Usui, S. (1999). Mathematical description of ionic currents of the Kenyon cell in the mushroom body of honeybee. Neurocomputing 26-27, 177-184.
35. 2+ channels. J. Exp. Biol. 203, 841-856.
36. Joerges, J., Küttner, A., Galizia, C. G. and Menzel, R. (1997). Representations of odours and odour mixtures visualized in the honeybee brain. Nature 387, 285-288.
37. Kenyon, C. F. (1896). The brain of the bee. A preliminary contribution to the morphology of the nervous system of the arthropoda. J. Comp. Neurol. 6, 133-210.
38. Kirchhof, B. S. and Mercer, A. R. (1997). Antennal lobe neurons of the honey bee, Apis mellifera, express a D2-like dopamine receptor in vitro. J. Comp. Neurol. 383, 189-198.
39. Kloppenburg, P. and Hörner, M. (1998). Voltage-activated currents in identified giant interneurons isolated from adult crickets Gryllus bimaculatus. J. Exp. Biol. 201, 2529-2541.
40. Kloppenburg, P., Kirchhof, B. S. and Mercer, A. R. (1999a). Voltage-activated currents from adult honeybee (Apis mellifera) antennal motor neurons recorded in vitro and in situ. J. Neurophysiol. 81, 39-48.
41. Kloppenburg, P., Levini, R. M. and Harris-Warrick, R. M. (1999b). Dopamine modulates two potassium currents and inhibits the intrinsic firing properties of an identified motor neuron in a central pattern generator network. J. Neurophysiol. 81, 29-38.
42. Kreissl, S. and Bicker, G. (1992). Dissociated neurons of the pupal honeybee brain in cell culture. J. Neurocytol. 21, 545-556.
43. Kreissl, S., Eichmüller, S., Bicker, G., Rapus, J. and Eckert, M. (1994). Octopamine-like immunoreactivity in the brain and subesophageal ganglion of the honeybee. J. Comp. Neurol. 348, 583-595.
44. Lapied, B., Pelhate, M. and Pelhate, M. (1989). Ionic species involved in the electrical activity of single adult aminergic neurones isolated from the sixth abdominal ganglion of the cockroach Periplaneta americana. J. Exp. Biol. 144, 535-549.
45. Laurent, G., Seymour-Laurent, K. J. and Johnson, K. (1993). Dendritic excitability and a voltage-gated calcium current in locust nonspiking local interneurons. J. Neurophysiol. 69, 1484-1498.
46. Masuhr, T. and Menzel, R. (1972). Learning experiments on the use of sidespecific information in the olfactory and visual system in the honeybee (Apis mellifica). In Information Processing in the Visual Systems of Arthropods (ed. R. Wehner), pp. 315-322. Berlin-Heidelberg-New York: Springer.
47. Mauelshagen, J. (1993). Neural correlates of olfactory learning paradigms in an identified neuron in the honeybee brain. J. Neurophysiol. 69, 609-625.
48. Menzel, R. (1999). Memory dynamics in the honeybee. J. Comp. Physiol. A 185, 323-340.
49. Menzel, R. (2001). Searching for the memory trace in a mini-brain, the honeybee. Learn. Mem. 8, 53-62.
50. Menzel, R. and Müller, U. (1996). Learning and memory in honeybees: from behaviour to neural substrates. Ann. Rev. Neurosci. 19, 379-404.
51. Mercer, A. R. and Hildebrand, J. G. (2002a). Developmental changes in the density of ionic currents in antennal-lobe neurons of the sphinx moth, Manduca sexta. J. Neurophysiol. 87, 2664-2675.
52. Mercer, A. R. and Hildebrand, J. G. (2002b). Developmental changes in the electrophysiological properties and response characteristics of Manduca sexta antennal-lobe neurons. J. Neurophysiol. 87, 2650-2663.
53. Mills, A. and Pitman, R. M. (1997). Electrical properties of a cockroach motor neuron soma depend on different characteristics of individual Ca components. J. Physiol. 78, 2455-2466.
54. Mills, J. D. and Pitman, R. M. (1999). Contribution of potassium conductances to a time-dependent transition in electrical properties of a cockroach motoneuron soma. J. Neurophysiol. 81, 2253-2266.
55. Mobbs, P. G. (1982). The brain of the honeybee Apis mellifera. I. The connections and spatial organization of the mushroom bodies. Phil. Trans. R. Soc. Lond. B. 298, 309-354.
56. Mobbs, P. G. (1985). Brain structure. In Comprehensive Insect Physiology, Biochemistry, and Pharmacology, vol. 5 (ed. G. A. Kerkut and L. I. Gilbert), pp. 299-370. Oxford: Pergamon Press.
57. Müller, D., Abel, R., Brandt, R., and Zöckler, M. (2002). Differential parallel processing of olfactory information in the honeybee, Apis mellifera L. J. Comp. Physiol. A 188, 359-370.
58. Müller, U. (1996). Inhibition of nitric oxide synthase impairs a distinct form of long-term memory in the honeybee Apis mellifera. Neuron 16, 541-549.
59. Müller, U. (2000). Prolonged activation of cAMP-dependent protein kinase during conditioning induces long-term memory in honeybees. Neuron 27, 159-168.
60. Nightingale, W. D. and Pitman, R. M. (1989). Ionic currents in the soma of an identified cockroach motoneurone recorded under voltage-clamp. Comp. Biochem. Physiol. 93A, 85-93.
61. Oland, L. A. and Hayashi, J. H. (1993). Effects of the steroid hormone 20-hydroxyectysone and prior sensory input on the survival and growth of Moth central olfactory neurons in vitro. J. Neurobiol. 24, 1170-1186.
62. Oland, L. A., Müller, T., Kettenmann, H. and Hayashi, J. (1996). Preparation of primary cultures and acute slices of the nervous system of the moth Manduca sexta. J. Neurosci. Methods 69, 103-112.
63. Pearson, H. A., Lees, G. and Wray, D. (1993). Calcium channel currents in neurones from locust (Schistocerca gregaria) thoracalic ganglia. J. Exp. Biol. 177, 201-221.
64. +, and simulation. J. Neurophysiol. 81, 1749-1759.
65. Rogero, O., Hämmerle, B. and Tejedor, F. J. (1997). Diverse expression and distribution of Shaker potassium channels during the development of the Drosophila nervous system. J. Neurosci. 17, 5108-5118.
66. Rybak, J. and Menzel, R. (1993). Anatomy of the mushroom bodies in the honey bee brain: the neuronal connections of the alpha-lobe. J. Comp. Neurol. 334, 444-465.
67. Sachse, S., Rappert, A. and Galizia, C. G. (1999). The spatial representation of chemical structures in the antennal lobe of honeybees: steps towards the olfactory code. Eur. J. Neurosci. 11, 3970-3982.
68. Saito, M. and Wu, C.-F. (1991). Expression of ion channels and mutational effects in giant Drosophila neurons differentiated from cell division-arrested embryonic neuroblasts. J. Neurosci. 11, 2135-2150.
69. Saito, M. and Wu, C.-F. (1993). Ionic channels in cultured Drosophila neurons. EXS 63, 366-389.
70. Schäfer, S., Rosenboom, H. and Menzel, R. (1994). Ionic currents of Kenyon cells from the mushroom body of the honeybee. J. Neurosci. 14, 4600-4612.
71. Schmidt, H., Lüer, K., Hevers, W. and Technau, G. M. (2000). Ionic currents of Drosophila embryonic neurons derived from selectively cultured CNS midline precursors. J. Neurobiol. 44, 392-413.
72. Schröter, U. and Malun, D. (2000). Formation of antennal lobe and mushroom body neuropils during metamorphosis in the honeybee, Apis mellifera. J. Comp. Neurol. 422, 229-245.
73. Stopfer, M., Bhagavan, S., Smith, B. H., and Laurent, G. (1997). Impaired odour discrimination on desynchronization of odour-encoding neural assemblies. Nature 390, 70-74.
74. Tanouye, M. A. and Ferrus, A. (1985). Action potentials in normal and shaker mutant Drosophila. J. Neurogenet. 2, 253-271.
75. Thomas, M. V. (1984). Voltage-clamp analysis of a calcium-mediated potassium conductance in cockroach (Periplaneta americana) central neurones. J. Physiol. 350, 159-178.
76. Wei, A., Solaro, C., Lingle, C. and Salkoff, L. (1994). Calcium sensitivity of BK-type KCa channels determined by a separable domain. Neuron 13, 671-681.
77. 2+ currents in central insect neurons: electrophysiological and pharmacological properties. J. Neurophysiol. 77, 186-199.
78. Wicher, D., Walther, C. and Wicher, C. (2001). Non-synaptic ion channels in insects - basic properties of currents and their modulation in neurons and skeletal muscles. Prog. Neurobiol. 64, 431-525.