Dual olfactory pathway in the honeybee, Apis mellifera

Journal of Comparative Neurology

Volumn 499, Issue 6, 2006, Pages 933-952

  Kirschner, Sebastian ^a   Kleineidam, Christoph Johannes ^a   Zube, Christina ^a   Rybak, Jürgen ^b   Grünewald, Bernd ^b   Rössler, Wolfgang ^a  

^a UNIVERSITY OF WÜRZBURG   (Germany)

^b FREIE UNIVERSITÄT BERLIN   (Germany)

Author keywords

3D reconstruction; Antennal lobe; Antenno cerebral tract; Lateral horn; Mushroom bodies; Olfactory glomeruli; Projection neurons

Indexed keywords

ANTENNA; ANTENNA LOBE; ANTENNAL SENSORY TRACT; ANTENNO CEREBRAL TRACT; ARTICLE; CELL LABELING; CONFOCAL MICROSCOPY; EFFERENT NERVE; FLUORESCENCE HISTOCHEMISTRY; GLOMERULUS; HONEYBEE; INNERVATION; MUSHROOM BODY; NERVE CELL; NERVE CELL NETWORK; NERVE CONDUCTION; NERVE FIBER; NEUROPHYSIOLOGY; NEUROPIL; NONHUMAN; OLFACTORY BULB; OLFACTORY CORTEX; OLFACTORY GLOMERULUS; OLFACTORY NERVE; OLFACTORY SYSTEM; OLFACTORY TRACT; PRIORITY JOURNAL; PROJECTION NEURON; SENSORY NERVE; SMELLING; SPINAL CORD; TELENCEPHALON; THREE DIMENSIONAL IMAGING;

EID: 33845449967     PISSN: 00219967     EISSN: 10969861     Source Type: Journal    
DOI: 10.1002/cne.21158     Document Type: Article

References (67)

1. Abel R, Rybak J, Menzel R. 2001, Structure and response patterns of olfactory interneurons in the honeybee, Apis mellifera. J Comp Neurol 437:363-383
2. Anton S, Homberg U. 1999. Antennal lobe structures. In: Hansson BS, editor. Insect olfaction. Heidelberg: Springer, p 97-124.
3. Anton S, van Loon JJA, Meijerink J, Smid HM, Takken W, Rospars J-P. 2003. Central projections of olfactory receptor neurons from single antennal and palpal sensilla in mosquitoes. Arthropod Struct Dev 32:319.
4. Arnold G, Masson C, Budharugsa S. 1985. Comparative study of the antennal lobes and their afferent pathways in the worker bee and the drone (Apis mellifera). Cell Tissue Res 242:593-605.
5. Bicker G, Kreissl S, Hofbauer A. 1993. Monoclonal-antibody labels olfactory and visual pathways in Drosophila and Apis brains. J Comp Neurol 335:413-424.
6. Brandt R, Rohlfing T, Rybak J, Krofczik S, Maye A, Westerhoff M, Hege HC, Menzel R. 2005. Three-dimensional average-shape atlas of the honeybee brain and its applications. J Comp Neurol 492:1-19.
7. Carlsson MA, Galizia CG, Hansson BS. 2002. Spatial representation of odours in the antennal lobe of the moth Spodoptera littoralis (Lepidoptera: Noctuidae). Chem Senses 27:231-244.
8. Christensen TA, White J. 2000. Representation of olfactory information in the brain. In: Finger TE, Silver WL, Restrepo D, editors. The neurobiology of taste and smell, 2nd ed. New York: Wiley-Liss. p 201-232.
9. Engel MS, Grimaldi DA. 2005. Primitive new ants in cretaceous amber from Myanmar, New Jersey, and Canada (Hymenoptera: Formicidae). Am Mus Novit 3485:1-23.
10. Ernst KD, Boeckh J, Boeckh V. 1977. Neuroanatomical study on organization of central antennal pathways in insects. 2. Deutocerebral connections in Locusta migratoria and Periplaneta americana. Cell Tissue Res 176:285-308.
11. Fahrbach SE. 2006. Structure of the mushroom bodies of the insect brain. Annu Rev Entomol 51:209-232.
12. Farris SM, Strausfeld NJ. 2003. A unique mushroom body substructure common to basal cockroaches and to termites. J Comp Neurol 456:305-320.
13. Flanagan D, Mercer AR. 1989. An atlas and 3-D reconstruction of the antennal lobes in the worker honey bee, Apis mellifera (Hymenoptera, Apidae). Int J Insect Morphol Embryol 18:145-159.
14. Fonta C, Sun XJ, Masson C. 1993. Morphology and spatial-distribution of bee antennal lobe interneurons responsive to odors. Chem Senses 18:101-119.
15. Frambach I, Rössler W, Winkler M, Schürmann FW. 2004. F-actin at identified synapses in the mushroom body neuropil of the insect brain. J Comp Neurol 475:303-314.
16. Galizia CG, Kimmerle B. 2004. Physiological and morphological characterization of honeybee olfactory neurons combining electrophysiology, calcium imaging and confocal microscopy. J Comp Physiol [A] 190:21-38.
17. Galizia CG, Menzel R. 2000. Odour perception in honeybees: coding information in glomerular patterns. Curr Opin Neurobiol 10:504-510.
18. Galizia CG, Sachse S, Rappert A, Menzel R. 1999a. The glomerular code for odor representation is species specific in the honeybee Apis mellifera. Nat Neurosci 2:473-478.
19. Galizia GC, McIlwrath SL, Menzel R. 1999b. A digital three-dimensional atlas of the honeybee antennal lobe based on optical sections acquired by confocal microscopy. Cell Tissue Res 295:383-394.
20. Gebhardt S, Homberg U. 2004. Immunocytochemistry of histamine in the brain of the locust Schistocerca gregaria. Cell Tissue Res 317:195.
21. Groh C, Tautz J, Rössler W. 2004. Synaptic organization in the adult honey bee brain is influenced by brood-temperature control during pupal development. Proc Natl Acad Sci U S A 101:4268-4273.
22. Groh C, Ahrens D, Rössler W. 2006. Environment- and age-dependent plasticity of synaptic complexes in the mushroom bodies of honeybee queens. Brain Behav Evol 68:1-14.
23. Gronenberg W. 2001. Subdivisions of hymenopteran mushroom body calyces by their afferent supply. J Comp Neurol 435:474-489.
24. 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.
25. Hansson BS, Anton S. 2000. Function and morphology of the antennal lobe: new developments. Annu Rev Entomol 45:203-231.
26. Hansson BS, Christensen TA. 1999. Functional characteristics of the antennal lobe. In: Hansson BS, editor. Insect olfaction. Heidelberg: Springer. p 125-161.
27. Heisenberg M. 2003. Mushroom body memoir: from maps to models. Nat Rev Neurosci 4:266.
28. Hildebrand JG, Shepherd GM. 1997. Mechanisms of olfactory discrimination: converging evidence for common principles across phyla. Annu Rev Neurosci 20:595-631.
29. Homberg U, Montague RA, Hildebrand JG. 1988. Anatomy of antenno-cerebral pathways in the brain of the sphinx moth Manduca sexta. Cell Tissue Res 254:255-281.
30. Homberg U, Christensen T, Hildebrand JG. 1989. Structure and function of the deuterocerebrum in insects. Annu Rev Entomol 34:477-501.
31. Ignell R. 2001. Monoamines and neuropeptides in antennal lobe interneurons of the desert locust, Schistocerca gregaria: an immunocytochemical study. Cell Tissue Res 306:143-156.
32. Ignell R, Hansson BS. 2005. Projection patterns of gustatory neurons in the suboesophageal ganglion and tritocerebrum of mosquitoes. J Comp Neurol 492:214-233.
33. Ignell R, Anton S, Hansson BS. 2000. The maxillary palp sensory pathway of Orthoptera. Arthropod Struct Dev 29:295.
34. Itoh T, Yokohari F, Tominaga Y. 1991. Response to humidity change of deutocerebral interneurons of the honeybee, Apis mellifera L. Naturwissenschaften 78:320-322.
35. Iwama A, Shibuya T. 1998. Physiology and morphology of olfactory neurons associating with the protocerebral lobe of the honeybee brain. J Insect Physiol 44:1191-1204.
36. Joerges J, Küttner A, Galizia GC, Menzel R. 1997. Representation of odours and odour mixtures visualized in the honeybee brain. Nature 387:285-288.
37. Kelber C, Rössler W, Kleineidam CJ. 2006. Multiple olfactory receptor neurons and their axonal projections in the antennal lobe of the honeybee Apis mellifera. J Comp Neurol 496:395-405.
38. Kent KS, Oland LA, Hildebrand JG. 1999. Development of the labial pit organ glomerulus in the antennal lobe of the moth Manduca sexta: the role of afferent projections in the formation of identifiable olfactory glomeruli. J Neurobiol 40:28-44.
39. Klagges BRE, Heimbeck G, Godenschwege TA, Hofbauer A, Pflugfelder GO, Reifegerste R, Reisch D, Schaupp M, Buchner S, Buchner E. 1996. Invertebrate synapsins: a single gene codes for several isoforms in Drosophila. J Neurosci 16:3154-3165.
40. Kreissl S, Bicker G. 1989. Histochemistry of acetylcholinesterase and immunohistochemistry of an acetylcholine receptor-like antigen in the brain of the honeybee. J Comp Neurol 286:71-84.
41. Malun D, Waldow U, Kraus D, Boeckh J. 1993. Connections between the deutocerebrum and the protocerebrum, and neuroanatomy of several classes of deutocerebral projection neurons in the brain of male periplaneta-americana. J Comp Neurol 329:143-162.
42. Marin EC, Jefferis G, Komiyama T, Zhu HT, Luo LQ. 2002. Representation of the glomerular olfactory map in the Drosophila brain. Cell 109:243-255.
43. Menzel R. 2001. Searching for the memory trace in a mini-brain, the honeybee. Learn Mem 8:53-62.
44. Menzel R, Manz G. 2005. Neural plasticity of mushroom body-extrinsic neurons in the honeybee brain. J Exp Biol 208:4317-4332.
45. Mobbs PG. 1982. The brain of the honeybee Apis mellifera. 1. The connections and spatial-organization of the mushroom bodies. Philos R Soc Lond B 298:309-354.
46. Müller D, Abel R, Brandt R, Zockler M, Menzel R. 2002. Differential parallel processing of olfactory information in the honeybee, Apis mellifera L. J Comp Physiol [A] 188:359-370.
47. Nishikawa M, Yokohari F, Ishibashi T. 1995. Central projections of the antennal cold receptor neurons and hygroreceptor neurons of the cockroach Periplaneta americana. J Comp Neurol 361:165-176.
48. Nishino H, Yamashita S, Yamazaki Y, Nishikawa M, Yokohari F, Mizunami M. 2003. Projection neurons originating from thermo- and hygrosensory glomeruli in the antennal lobe of the cockroach. J Comp Neurol 455:40-55.
49. Pareto A. 1972. Spatial-distribution of sensory antennal fibers in central nervous-system of worker bees. Z Zellforsch Mikrosk Anat 131:109.
50. Rospars JP, Hildebrand JG. 1992. Anatomical identification of glomeruli in the antennal lobes of the male sphinx moth Manduca sexta. Cell Tissue Res 270:205-227.
51. Rössler W, Randolph PW, Tolbert LP, Hildebrand JG. 1999. Axons of olfactory receptor cells of transsexually grafted antennae induce development of sexually dimorphic glomeruli in Manduca sexta. J Neurobiol 38:521-541.
52. Rybak J, Menzel R. 1993. Anatomy of the mushroom bodies in the honeybee brain - the neuronal connections of the alpha-lobe. J Comp Neurol 334:444-465.
53. 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.
54. Sachse S, Galizia CG. 2003. The coding of odour-intensity in the honeybee antennal lobe: local computation optimizes odour representation. Eur J Neurosci 18:2119-2132.
55. Schäfer S, Bicker G. 1986. Distribution of GABA-like immunoreactivity in the brain of the honeybee. J Comp Neurol 246:287-300.
56. Schneider D, Steinbrecht A. 1968. Checklist of insect olfactory sensilla. Symp Zool Soc Lond 23:279-297.
57. Schröter U, Menzel R. 2003. A new ascending sensory tract to the calyces of the honeybee mushroom body, the subesophageal-calycal tract. J Comp Neurol 465:168-178.
58. Stocker RF, Lienhard MC, Borst A, Fischbach KF. 1990. Neuronal architecture of the antennal lobe in Drosophila melanogaster. Cell Tissue Res 262:9-34.
59. Strausfeld NJ. 2002. Organization of the honey bee mushroom body: representation of the calyx within the vertical and gamma lobes. J Comp Neurol 450:4-33.
60. Strausfeld NJ, Hildebrand JG. 1999. Olfactory systems: common design, uncommon origins? Curr Opin Neurobiol 9:634-639.
61. Suzuki H. 1975. Antennal movements induced by odour and central projection of the antennal neurones in the honeybee. J Insect Physiol 21:831-847.
62. Tanaka NK, Awasaki T, Shimada T, Ito K. 2004. Integration of chemosensory pathways in the Drosophila second-order olfactory centers. Curr Biol 14:449-457.
63. Vosshall LB, Wong AM, Axel R. 2000. An olfactory sensory map in the fly brain. Cell 102:147-159.
64. Wang JW, Wong AM, Flores J, Vosshall LB, Axel R. 2003. Two-photon calcium imaging reveals an odor-evoked map of activity in the fly brain. Cell 112:271-282.
65. Wegerhoff R. 1999. GABA and serotonin immunoreactivity during postembryonic brain development in the beetle Tenebrio molitor. Microscopy Research and Technique 45:154-164.
66. Wong AM, Wang JW, Axel R. 2002. Spatial representation of the glomerular map in the Drosophila protocerebrum. Cell 109:229-241.
67. Xu FQ, Greer CA, Shepherd GM. 2000. Odor maps in the olfactory bulb. J Comp Neurol 422:489-495.