Role of histamine as a putative inhibitory transmitter in the honeybee antennal lobe

Frontiers in Zoology - Tập 3 Số 1 - 2006
Silke Sachse1, Philipp Peele1, Ana F. Silbering1, Martin Gühmann1, C. Giovanni Galizia1
1Institut für Biologie – Neurobiologie, Freie Universität Berlin, Königin-Luise Str. 28-30, D-14195, Berlin, Germany

Tóm tắt

Abstract Background Odors are represented by specific spatio-temporal activity patterns in the olfactory bulb of vertebrates and its insect analogue, the antennal lobe. In honeybees inhibitory circuits in the AL are involved in the processing of odors to shape afferent odor responses. GABA is known as an inhibitory transmitter in the antennal lobe, but not all interneurons are GABAergic. Therefore we sought to analyze the functional role of the inhibitory transmitter histamine for the processing of odors in the honeybee AL. Results We optically recorded the representation of odors before, during and after histamine application at the input level (estimated from a compound signal), and at the output level (by selectively measuring the projection neurons). For both, histamine led to a strong and reversible reduction of odor-evoked responses. Conclusion We propose that histamine, in addition to GABA, acts as an inhibitory transmitter in the honeybee AL and is therefore likely to play a role in odor processing.

Từ khóa


Tài liệu tham khảo

Wilson RI, Laurent G: Role of GABAergic inhibition in shaping odor-evoked spatiotemporal patterns in the Drosophila antennal lobe. J Neurosci. 2005, 25: 9069-9079. 10.1523/JNEUROSCI.2070-05.2005.

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

Yokoi M, Mori K, Nakanishi S: Refinement of odor molecule tuning by dendrodendritic synaptic inhibition in the olfactory bulb. Proc Natl Acad Sci U S A. 1995, 92: 3371-3375. 10.1073/pnas.92.8.3371.

Christensen TA, Waldrop BR, Harrow ID, Hildebrand JG: Local interneurons and information processing in the olfactory glomeruli of the moth Manduca sexta. J Comp Physiol A Neuroethol Sens Neural Behav Physiol. 1993, 173: 385-399.

Esslen J, Kaissling KE: Number and distribution of sensilla on antennal flagellum of honeybee (Apis mellifera L). Zoomorphologie. 1976, 83: 227-251. 10.1007/BF00993511.

Witthöft W: Absolute Anzahl und Verteilung der Zellen im Hirn der Honigbiene [Absolute number and distribution of cells in the brain of honeybees]. Z Morphol Tiere. 1967, 61: 160-184. 10.1007/BF00298776.

Bicker G, Kreissl S, Hofbauer A: Monoclonal antibody labels olfactory and visual pathways in Drosophila and Apis brains. J Comp Neurol. 1993, 335: 413-424. 10.1002/cne.903350310.

Kirschner S, Kleineidam CJ, Zube C, Rybak J, Grunewald B, Rossler W: Dual olfactory pathway in the honeybee, Apis mellifera. J Comp Neurol. 2006, 499: 933-952. 10.1002/cne.21158.

Gascuel J, Masson C: A quantitative ultrastructural study of the honeybee antennal lobe. Tissue and Cell. 1991, 23: 341-355. 10.1016/0040-8166(91)90052-U.

Flanagan D, Mercer AR: An atlas and 3-D reconstruction of the antennal lobes in the worker honey bee, Apis mellifera L. (Hymenoptera: Apidae). Int J Insect Morphol Embryol. 1989, 18: 145-159. 10.1016/0020-7322(89)90023-8.

Galizia CG, McIlwrath SL, Menzel R: A digital three-dimensional atlas of the honeybee antennal lobe based on optical sections acquired by confocal microscopy. Cell Tissue Res. 1999, 295: 383-394. 10.1007/s004410051245.

Schmidt M, Ache BW: Processing of antennular input in the brain of the spiny lobster, Panulirus argus II. The olfactory pathway. J Comp Physiol A Neuroethol Sens Neural Behav Physiol. 1996, 178: 605-628.

Fonta C, Sun XJ, Masson C: Morphology and spatial distribution of bee antennal lobe interneurones responsive to odours. Chemical Senses. 1993, 18: 101-119. 10.1093/chemse/18.2.101.

Mori K, Yoshihara Y: Molecular recognition and olfactory processing in the mammalian olfactory system. Prog Neurobiol. 1995, 45: 585-619. 10.1016/0301-0082(94)00058-P.

Wachowiak M, Ache BW: Dual inhibitory pathways mediated by GABA- and histaminergic interneurons in the lobster olfactory lobe. J Comp Physiol A Neuroethol Sens Neural Behav Physiol. 1997, 180: 357-372. 10.1007/s003590050055.

Wachowiak M, Cohen LB: Presynaptic afferent inhibition of lobster olfactory receptor cells: reduced action-potential propagation into axon terminals. J Neurophysiol. 1998, 80: 1011-1015.

Wachowiak M, Cohen LB, Ache BW: Presynaptic inhibition of olfactory receptor neurons in crustaceans. Microsc Res Tech. 2002, 58: 365-375. 10.1002/jemt.10144.

Shipley MT, Ennis M: Functional organization of olfactory system. J Neurobiol. 1996, 30: 123-176. 10.1002/(SICI)1097-4695(199605)30:1<123::AID-NEU11>3.0.CO;2-N.

Distler PG: Histochemical demonstration of GABA-like immunoreactivity in cobalt labeled neuron individuals in the insect olfactory pathway. Histochemistry. 1989, 91: 245-249. 10.1007/BF00490139.

Hoskins SG, Homberg U, Kingan TG, Christensen TA, Hildebrand JG: Immunocytochemistry of GABA in the antennal lobes of the sphinx moth Manduca sexta. Cell Tissue Res. 1986, 244: 243-252. 10.1007/BF00219199.

Schäfer S, Bicker G: Distribution of GABA-like immunoreactivity in the brain of the honeybee. J Comp Neurol. 1986, 246: 287-300. 10.1002/cne.902460302.

Bornhauser BC, Meyer EP: Histamine-like immunoreactivity in the visual system and brain of an orthopteran and a hymenopteran insect. Cell Tissue Res. 1997, 287: 211-221. 10.1007/s004410050747.

Ignell R: Monoamines and neuropeptides in antennal lobe interneurons of the desert locust, Schistocerca gregana: an immunocytochemical study. Cell Tissue Res. 2001, 306: 143-156. 10.1007/s004410100434.

Nässel DR: Histamine in the brain of insects: a review. Microsc Res Tech. 1999, 44: 121-136. 10.1002/(SICI)1097-0029(19990115/01)44:2/3<121::AID-JEMT6>3.0.CO;2-F.

Pirvola U, Tuomisto L, Yamatodani A, Panula P: Distribution of histamine in the cockroach brain and visual system: an immunocytochemical and biochemical study. J Comp Neurol. 1988, 276: 514-526. 10.1002/cne.902760406.

Zheng Y, Hirschberg B, Yuan J, Wang AP, Hunt DC, Ludmerer SW, Schmatz DM, Cully DF: Identification of two novel Drosophila melanogaster histamine-gated chloride channel subunits expressed in the eye. J Biol Chem. 2002, 277: 2000-2005. 10.1074/jbc.M107635200.

Galizia CG, Vetter RS: Optical methods for analyzing odor-evoked activity in the insect brain. Advances in Insect Sensory Neuroscience. Edited by: Christensen TA. 2004, Boca Raton, CRC Press, 349-392.

Galizia CG, Nägler K, Hölldobler B, Menzel R: Odour coding is bilaterally symmetrical in the antennal lobes of honeybees (Apis mellifera). Eur J Neurosci. 1998, 10: 2964-2974. 10.1111/j.1460-9568.1998.00303.x.

Abel R, Rybak J, Menzel R: Structure and response patterns of olfactory interneurons in the honeybee, Apis mellifera. J Comp Neurol. 2001, 437: 363-383. 10.1002/cne.1289.

Müller D, Abel R, Brandt R, Zockler M, Menzel R: Differential parallel processing of olfactory information in the honeybee, Apis mellifera L. J Comp Physiol A Neuroethol Sens Neural Behav Physiol. 2002, 188: 359-370. 10.1007/s00359-002-0310-1.

Wachowiak M, Cohen LB: Presynaptic inhibition of primary olfactory afferents mediated by different mechanisms in lobster and turtle. J Neurosci. 1999, 19: 8808-8817.

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

Orona E, Battelle BA, Ache BW: Immunohistochemical and biochemical evidence for the putative inhibitory neurotransmitters histamine and GABA in lobster olfactory lobes. J Comp Neurol. 1990, 294: 633-646. 10.1002/cne.902940410.

Barbara GS, Zube C, Rybak J, Gauthier M, Grünewald B: Acetylcholine, GABA and glutamate induce ionic currents in cultured antennal lobe neurons of the honeybee, Apis mellifera. J Comp Physiol A Neuroethol Sens Neural Behav Physiol. 2005, 191: 823-836. 10.1007/s00359-005-0007-3.

Stuart AE: From fruit flies to barnacles, histamine is the neurotransmitter of arthropod photoreceptors. Neuron. 1999, 22: 431-433. 10.1016/S0896-6273(00)80699-6.

Gisselmann G, Pusch H, Hovemann BT, Hatt H: Two cDNAs coding for histamine-gated ion channels in D. melanogaster. Nat Neurosci. 2002, 5: 11-12. 10.1038/nn787.

McClintock TS, Ache BW: Histamine directly gates a chloride channel in lobster olfactory receptor neurons. Proc Natl Acad Sci U S A. 1989, 86: 8137-8141. 10.1073/pnas.86.20.8137.

Roeder T: Metabotropic histamine receptors--nothing for invertebrates?. Eur J Pharmacol. 2003, 466: 85-90. 10.1016/S0014-2999(03)01553-X.

Iovchev M, Boutanaev A, Ivanov I, Wolstenholme A, Nurminsky D, Semenov E: Phylogenetic shadowing of a histamine-gated chloride channel involved in insect vision. Insect Biochem Mol Biol. 2006, 36: 10-17. 10.1016/j.ibmb.2005.09.002.

Nässel DR, Homberg U: Neuropeptides in interneurons of the insect brain. Cell Tissue Res. 2006, 326: 1-24. 10.1007/s00441-006-0210-8.

Schachtner J, Trosowski B, D'Hanis W, Stubner S, Homberg U: Development and steroid regulation of RFamide inummoreactivity in antennal lobe neurons of the sphinx moth Manduca sexta. J Exp Biol. 2004, 207: 2389-2400. 10.1242/jeb.01036.

Galizia CG, Joerges J, Küttner A, Faber T, Menzel R: A semi in-vivo preparation for optical recording of the insect brain. J Neurosci Methods. 1997, 76: 61-69. 10.1016/S0165-0270(97)00080-0.

Galizia CG, Sachse S, Rappert A, Menzel R: The glomerular code for odor representation is species specific in the honeybee Apis mellifera. Nat Neurosci. 1999, 2: 473-478. 10.1038/8144.

Thông tin
Thông tin xuất bản

Frontiers in Zoology

Tập 3 Số 1

Thông tin tác giả