Functional and topographic segregation of glomeruli revealed by local staining of antennal sensory neurons in the honeybee Apis mellifera

Journal of Comparative Neurology

Volumn 515, Issue 2, 2009, Pages 161-180

  Nishino, Hiroshi ^a   Nishikawa, Michiko ^b   Mizunami, Makoto ^c   Yokohari, Fumio ^b  

^a HOKKAIDO UNIVERSITY   (Japan)

^b FUKUOKA UNIVERSITY   (Japan)

^c TOHOKU UNIVERSITY   (Japan)

Author keywords

Antennal lobe; Central projection; Insect; Receptive field; Sensory afferents; Somatotopic organization

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTENNA; ARTICLE; CELL LABELING; CONFOCAL MICROSCOPY; DENDRITE; FLAGELLUM; HONEYBEE; IMAGE RECONSTRUCTION; NERVE ENDING; NERVE FIBER; NONHUMAN; OLFACTORY RECEPTOR; OLFACTORY SYSTEM; PATTERN RECOGNITION; PRIORITY JOURNAL; RECEPTIVE FIELD; SENSORY NERVE CELL; SOMATOSENSORY SYSTEM; SPATIAL DISCRIMINATION; STAINING; THERMORECEPTOR; THREE DIMENSIONAL IMAGING; ANIMAL; BEE; FEMALE; HISTOLOGY; IMAGE PROCESSING; MALE; MECHANORECEPTOR; PHYSIOLOGY; SCANNING ELECTRON MICROSCOPY; SENSE ORGAN; SENSORY RECEPTOR; SEXUAL DEVELOPMENT; SYNAPTOSOME; TASTE; ULTRASTRUCTURE;

ANIMALS; BEES; FEMALE; IMAGE PROCESSING, COMPUTER-ASSISTED; MALE; MECHANORECEPTORS; MICROSCOPY, CONFOCAL; MICROSCOPY, ELECTRON, SCANNING; PRESYNAPTIC TERMINALS; SENSE ORGANS; SENSORY RECEPTOR CELLS; SEX CHARACTERISTICS; TASTE;

EID: 67650341513     PISSN: 00219967     EISSN: 10969861     Source Type: Journal    
DOI: 10.1002/cne.22064     Document Type: Article

References (59)

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. Ai H, Kanzaki R. 2004. Modular organization of the silkmoth antennal lobe macroglomerular complex revealed by voltatge-sensitive dye imaging. J Exp Biol 207:633-644.
3. Ai H, Nishino H, Itoh T. 2007. Topographic organization of sensory afferents of Johnston's organ in the honeybee brain. J Comp Neurol 502: 1030-1046.
4. Altner H. Prillinger L. 1980. Ultrastructure of invertebrate chemo-, thermo-, and hygroreceptors and its functional significance. Int Rev Cytol 67: 69-139.
5. Arnold G, Masson C, Budharugsa S. 1985. Comparative study of the antennal lobes and their afferent pathway in the worker bee and the drone (Apis mellifera). Cell Tissue Res 242:593-605.
6. Berg BG, Almaas TJ, Bjaalie JG, Mustaparta H. 2005. Projections of male-specific receptor neurons in the antennal lobe of the oriental tobacco budworm moth, Helicoverpa assulta: a unique glomerular organization among related species. J Comp Neurol 486:209-220.
7. Boeckh J, Sandri C, Akert K. 1970. Sensorische Eingänge und synaptische Verbindungen im Zentralnervensystem von Insekten. Experimentelle Degeneration in der antennalen Sinnesbahn von Fliegen und Schaben. Z Zellforsch 103:429-446.
8. Burrows M, Boeckh J, Esslen J. 1982. Physiological and morphological properties of interneurones in the deutocerebrum of male cockroaches which respond to female pheromone. J Comp Physiol [A] 145:447-457.
9. Christensen TA, Harrow ID, Cuzzocrea C, Randolph PW, Hildebrand JG. 1995. Distinct projections of two populations of olfactory receptor axons in the antennal lobe of the sphinx moth Manduca sexta. Chem Senses 20:313-323.
10. Couto A, Alenius M, Dickson BJ. 2005. Molecular, anatomical and functional organization of the Drosophila olfactory system. Curr Biol 15: 1535-1547.
11. Esslen J, Kaissling KE. 1976. Zahl und Verteilun antennaler Sensillen bei der Honibiene (Apis melliifera L). Zoomorphology 83:227-251.
12. Fishilevich E, Vosshall LB. 2005. Genetic and functional subdivision of the Drosophila antennal lobe. Curr Biol 15:1548 -1553.
13. Flanagan D, Mercer AR. 1989. An atlas and 3-D reconstruction of the antennal lobe in the worker honey bee, Apis mellifera L (Hymenoptera: Apidae). Int 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 odours. Chem Senses 18:101-119.
15. Galizia CG, McIlwrath SL, Menzel R. 1999. A digital three-dimensional atlas of the honeybee antennal lobe based on optical sections acquired by confocal microscopy. Cell Tissue Res 295:383-394.
16. Gao Q, Yuan B, Chess A. 2000. Convergent projections of Drosophila olfactory neurons to specific glomeruli in the antennal lobe. Nat Neurosci 2:473-478.
17. Hansson BS, Christensen TA, Hildebrand JG. 1991. Functionally distinct subdivisions of the macroglomerular complex in the antennal lobe of the male sphinx moth Manduca sexta. J Comp Neurol 312:264-278.
18. Haupt S. 2007. Central gustatory projections and side-specificity of operant antennal muscle conditioning in the honeybee. J Comp Physiol A 193:523-535.
19. Hildebrand JG, Shepherd GM. 1997. Mechanisms of olfactory discrimination: converging evidence for common principles across phyla. Annu Rev Neurosci 20:595-631.
20. Hösl M. 1990. Pheromone-sensitive neurons in the deutocerebrum of Periplaneta americana: receptive fields on the antenna. J Comp Physiol [A] 167:321-327.
21. Ignell R, Dekker T, Ghaninia M, Hansson BS. 2005. Neuronal architecture of the mosquito deutocerebrum. J Comp Neurol 493:207-240.
22. Johnson BA, Leon M. 2007. Chemotopic odorant coding in a mammalian olfactory system. J Comp Neurol 503:1-34.
23. Kaissling KE, Renner M. 1968. Antennale Rezeptoren für Queen-Substance und Sterzelduft der Honigbiene. Z Vergl Physiol 59:357-361.
24. Kandel ER, Schwartz JH, Jessell TM 2000. Principles of neural science. New York: McGraw-Hill.
25. Kanzaki R, Soo K, Seki Y, Wada S. 2003. Projections to higher olfactory centers from subdivisions of the antennal lobe macroglomerular complex of the male silkmoth. Chem Senses 28:113-130.
26. Keil T. 1999. Morphology and development of the peripheral olfactory organs. In: Hannson BS, editor. Insect olfaction. Heidelberg: Springer. p 5-48.
27. Kelber C, Rössler W, Kleineidam J. 2006. Multiple olfactory receptor neurons and their axonal projections in the antennal lobe of the honeybee Apis mellifera. J Comp Neurol 496:395-405.
28. Kirschner S, Kleineidam CJ, Zube C, Rybak J, Grünewald B, Rössler W. 2006. Dual olfactory pathway in the honeybee, Apis mellifera. J Comp Neurol 499:933-952.
29. 2 sensitive sensillum ampullaceum in the leaf-cutting ant Atta sexdens. Arthropod Struct Dev 29:43-55.
30. Lacher V. 1964. Electrophysiologische Untersuchungen an einzelnen Rezeptoren f_udsr Geruch, Kohlendioxid, Luftfeuchtigkeit und Temperatur auf den Antennen der Arbeitsbiene und der Drohne (Apis mellifica L.). Z Vergl Physiol 48:587-623.
31. Lipscomb BW, Tolbert L. 2006. Temporally staggered glomerulus development in the moth Manduca sexta. Chem Senses 31:237-247.
32. Michener CD. 1974. The social behavior of bees. A comparative study. Cambridge, MA: Belknap Press of Harvard University Press.
33. Müller D, Abel R, Brabndt 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.
34. 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.
35. Nishino H, Mizunami M. 2006. Termination profiles of insect chemosensory afferents in the antennal lobe are dependent on their origin on the flagellum. NeuroReport 17:1303-1307.
36. Nishino H, Mizunami M. 2007. Sensilla position on antennae influences afferent terminal location in glomeruli. NeuroReport 18:1765-1769.
37. 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.
38. Nishino H, Nishikawa M, Yokohari F, Mizunami M. 2005. Dual, multilayered somatosensory maps formed by antennal tactile and contact chemosensory afferents in an insect brain. J Comp Neurol 493:291-308.
39. Okada J, Toh Y. 2005. Active tactile sensing for localization of objects by the cockroach antenna. J Comp Physiol [A] 192:715-726.
40. Pareto A. 1972. Die zentrale Verteilung der Fühlerafferenz bei Arbeiterinnen der Honigbiene, Apis mellifera L. Z Zellforsch 131:109-140.
41. Ressler KJ, Sullivan SL, Buck LB. 1994. Information coding in the olfactory system: evidence for a stereotyped and highly organized epitope map in the olfactory bulb. Cell 79:1245-1225.
42. Robertson HM, Wanner KW. 2006. The chemoreceptor superfamily in the honey bee, Apis mellifera: expantion of the odorant, but not gustatory, receptor family. Genome Res 16:1395-1403
43. Sachse S, Rappert A, Galizia CG. 1999. The spatial representation of chemical structures in the antennal lobe of honeybees: steps towards the olfactory code. Eur J Neurosci 11:3970-3982.
44. Sandoz JC. 2006. Odour-evoked responses to queen pheromone components and to plant odours using optical imaging in the antennal lobe of the honey bee drone Apis mellifera L. J Exp Biol 209:3587-3598.
45. Sato K, Pellegrino M, Nakagawa T, Nakagawa T, Vosshall LB, Touhara K. 2008. Insect olfactory receptors are heteromeric ligand-gated ion channels. Nature 452:1002-1007
46. Schafer R, Sanchez TV. 1973. Antennal sensory system of the cockroach, Periplaneta americana: postembryonic development and morphology of the sense organs. J Comp Neurol 149:335-354.
47. Schaller D. 1978. Antennal sensory system of Periplaneta americana L. Distribution and frequency of morphologic types of sensilla and their sex-specific changes during postembryonic development. Cell Tissue Res 191:121-139.
48. Scheiner R, Schnitt S, Erber J. 2005. The functions of antennal mechanoreceptors and antennal joints in tactile discrimination of the honeybee (Apis meillilfera L.) J Comp Physiol [A] 191:857-864.
49. Schneider D, Steinbrecht RA. 1968. Checklist of insect olfactory sensilla. Symp Zool Soc Lond 23:279-297.
50. Takahashi YK, Kurosaki M, Hirono S, Mori K. 2004. Topographic representation of odorant molecular features in the rat olfactory bulb. J Neurophysiol 92:2413-2427.
51. Vassar R, Chao SK, Sicheran R, Nunez JM, Vosshakll LB, Axel R. 1994. Topographic organization of sensory projections to the olfactory bulb. Cell 79:981-991
52. Vosshall LB, Wong AM, Axel R. 2000. An olfactory sensory map in the fly brain. Cell 102:147-159.
53. Wanner KW, Nichols AS, Walden KKO, Brockmann A, Luetje CW, Robertson HM. 2007. A honey bee odorant receptor for the queen substance 9-oxo-2-decenoic acid. Proc Natl Acad Sci U S A 104:14383-14388.
54. Wicher D, Schäfer R, Bauernfeind R, Stensmyr MC, Heller R, Heinemann SH, Hansson BS. 2008. Drosophila odorant receptors are both ligand-gated and cyclic nucleotide-activated cation channels. Nature 452: 1007-1012
55. Willis MA, Avondet JL. 2005. Odor-modulated orientation in walking male cockroaches Periplaneta americana, and the effect of odor plumes of different structure. J Exp Biol 208:721-735.
56. Yao CA, Ignell R, Carlson JR. 2005. Chemosensory coding by neurons in the coeloconic sensilla of the Drosophila antenna. J Neurosci 25:8359-8367.
57. Yokohari F. 1981. The sensillum capitulum, an antennal hygro- and thermoreceptive sensillum of the cockroach, Periplaneta americana L. Cell Tissue Res 216:525-543
58. Yokohari F. 1983. The coleocapitular sensillum, an antennal hygro- and thermoreceptive sensillum of the honey bee, Apis mellifera L. Cell Tissue Res 233:355-365.
59. Yokohari F, Tominaga Y, Tateda H. 1982. Antennal hygroreceptors of the honey bee, Apis mellifera L. Cell Tissue Res 226:63-73.