Integration of the antennal lobe glomeruli and three projection neurons in the standard brain atlas of the moth Heliothis virescens

Frontiers in Systems Neuroscience

Volumn 4, Issue FEB, 2010, Pages

  Løfaldli, Bjarte Bye ^a   Kvello, Pål ^a   Mustaparta, Hanna ^a  

^a NORWEGIAN UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Norway)

Author keywords

Insect; Lateral protocerebrum; Mushroom body calyces; Olfaction; Three dimensional reconstruction

Indexed keywords

EID: 79957919271     PISSN: 16625137     EISSN: None     Source Type: Journal    
DOI: 10.3389/neuro.06.005.2010     Document Type: Article

References (63)

1. Anton, S., and Hansson, B. S. (1999). Physiological mismatching between neurons innervating olfactory glomeruli in a moth. Proc. R. Soc. Lond., B, Biol. Sci. 266, 1813-1820.
2. Anton, S., and Homberg, U. (1999). Antennal lobe structure. In Insect Olfaction, B. S. Hansson, ed. (Berlin, Springer), pp. 97-124.
3. Axel, R. (1995). The molecular logic of smell. Sci. Am. 273, 154-159.
4. Berg, B. G., Almaas, T. J., Bjaalie, J. G., and Mustaparta, H. (1998). The macroglomerular complex of the antennal lobe in the tobacco budworm moth Heliothis virescens: specified subdivision in four compartments according to information about biologically significant compounds. J. Comp. Physiol. A 183, 669-682.
5. Berg, B. G., Galizia, C. G., Brandt, R., and Mustaparta, H. (2002). Digital atlases of the antennal lobe in two species of tobacco budworm moths, the oriental Helicoverpa assulta (male) and the American Heliothis virescens (male and female). J. Comp. Neurol. 446, 123-134.
6. Brandt, R., Rohlfing, T., Rybak, J., Krofczik, S., Maye, A., Westerhoff, M., Hege, H. C., and Menzel, R. (2005). Treedimensional average-shape atlas of the honeybee brain and its applications. J. Comp. Neurol. 492, 1-19.
7. Buck, L. B. (2000). The molecular architecture of odor and pheromone sensing in mammals. Cell 100, 611-618.
8. Chiang, A.-S., Liu, Y.-C., Chiu, S.-L., Hu, S. H., Huang, C.-Y., and Hsieh, C.-H. (2001). Three-dimensional mapping of brain neuropils in the cockroach, Diploptera punctata. J. Comp. Neurol. 440, 1-11.
9. Christensen, T. A., and Hildebrand, J. G. (2002). Pheromonal and host-odor processing in the insect antennal lobe: how different? Curr. Opin. Neurobiol. 12, 393-399.
10. Clyne, P. J., Warr, C. G., Freeman, M. R., Lessing, D., Kim, J., and Carlson, J. R. (1999). A novel family of divergent seven-transmembrane proteins: candidate odorant receptors in Drosophila. Neuron 22, 327-338.
11. El Jundi, B., Heinze, S., Lenschow, C., Kurylas, A., Rohlfing, T., and Homberg, U. (2010). The locust standard brain: a 3D standard of the central complex as a platform for neural network analysis. Front. Syst. Neurosci. 3:21. doi: 10.3389/neuro.06.021.2009.
12. El Jundi, B., Huetteroth, W., Kurylas, A. E., and Schachtner, J. (2009). Anisometric brain dimorphism revisited: implementation of a volumetric 3D standard brain in Manduca sexta. J. Comp. Neurol. 517, 210-225.
13. Evers, J. F., Schmitt, S., Sibila, M., and Duch, C. (2004). Progress in functional neuroanatomy: precise automatic geometric reconstruction of neuronal morphology from confocal image stacks. J. Neurophysiol. 93, 2331-2342.
14. Flanagan, D., and Mercer, A. R. (1989). 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. 18, 145-159.
15. Galizia, C. G., McIlwrath, S. L., and 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. Galizia, C. G., and Menzel, R. (2000). Probing the olfactory code. Nat. Neurosci. 3, 853-854.
17. Galizia, C. G., Sachse, S., and Mustaparta, H. (2000). Calcium responses to pheromones and plant odours in the antennal lobe of the male and female moth Heliothis virescens. J. Comp. Physiol. A 186, 1049-1063.
18. Greiner, B., Gadenne, C., and Anton, S. (2004). Three-dimensional antennal lobe atlas of the male moth, Agrotis ipsilon: a tool to study structure- function correlation. J. Comp. Neurol. 475, 202-210.
19. Gurenstein P. G., Christensen T. A., and Hildebrand J. G. (2004). Sensory processing of ambient CO2 information in the brain of the moth Manduca sexta. J. Comp. Physiol. A. 190, 707-725.
20. Heisenberg, M. (2003). Mushroom body memoir: from maps to models. Nat. Rev. Neurosci. 4, 266-275.
21. Hildebrand, J. G., and Shepherd, G. M. (1997). Mechanisms of olfactory discrimination: converging evidence for common principles across phyla. Annu. Rev. Neurosci. 20, 595-631.
22. Homberg, U., Montague, R. A., and Hildebrand, J. G. (1988). Anatomy of antenno-cerebral pathways in the brain of the sphinx moth Manduca sexta. Cell Tissue Res. 254, 255-281.
23. Huetteroth, W., and Schachtner, J. (2005). Standard three-dimensional glomeruli of the Manduca sexta antennal lobe: a tool to study both developmental and adult neuronal plasticity. Cell Tissue Res. 319, 513-524.
24. Iyengar, B. G., Chou, C. J., Sharma, A., and Atwood, H. L. (2006). Modular neuropile organization in the Drosophila larval brain facilitates identification and mapping of central neurons. J. Comp. Neurol. 499, 583-602.
25. Jefferis, G. S. X. E., Potter, C. J., Chan A. I., Marin, E. C., Rohlfing, T., Maurer, C. R., and Luo, L. Q. (2007). Comprehensive maps of Drosophila higher olfactory centers: spatially segregated fruit and pheromone representation. Cell 128, 1187-1203.
26. Kanzaki, R., Soo, S., Seki, Y., and 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.
27. Kazawa, T., Namiki, S., Fukushima, R., Terada, M., Soo, K., and Kanzaki, R. (2009). Constancy and variability of glomerular organization in the antennal lobe of the silkmoth. Cell Tissue Res. 336, 119-136.
28. Kloppenburg, P., and Mercer, A. R. (2008). Serotonin modulation of moth central olfactory neurons. Annu. Rev. Entomol. 53, 179-190.
29. Kurylas, A. E., Rohlfing, T., Krofczik, S., Jenett, A., and Homberg, U. (2008). Standardized atlas of the brain of the desert locust, Schistocerca gregaria. Cell Tissue Res. 33, 125-145.
30. Kvello, P., Løfaldli, B. B., Rybak, J., Menzel, R., and Mustaparta, H. (2009). Digital, three-dimensional average shaped atlas of the Heliothis virescens brain with integrated gustatory and olfactory neurons. Front. Syst. Neurosci. 3:14. doi: 10.3389/neuro.06.014.2009.
31. Laissue, P. P., Reiter, C., Hiesinger, P. R., Halter, S., Fischbach, K. F., and Stocker, R. F. (1999). Three-dimensional reconstruction of the antennal lobe in Drosophila melanogaster. J. Comp. Neurol. 405, 543-552.
32. Laurent, G., Wehr, M., and Davidowitz, H. (1996). Temporal representations of odors in an olfactory network. J. Neurosci. 16, 3837-3847.
33. Lledo, P.-M., Gheusi, G., and Vincent, J.-D. (2005). Information processing in the mammalian olfactory system. Physiol. Rev. 85, 281-317.
34. Masante-Roca, I., Gadenne, C., and Anton, S. (2005). Three-dimensional antennal lobe atlas of male and female moths, Lobesia botrana (Lepidoptera: Tortricidae) and glomerular representation of plant volatiles in females. J. Exp. Biol. 208, 1147-1159.
35. Menzel, R. (2001). Searching for the memory trace in a mini-brain, the honeybee. Learn. Mem. 8, 53-62.
36. Mombaerts, P. (2001). How smell develops. Nat. Neurosci. 4, 1192-1198.
37. Müller, D., Abel, R., Brandt, R., Zöckler, M., and Menzel, R. (2002). Differential parallel processing of olfactory information in the honeybee, Apis mellifera L. J. Comp. Physiol. A. 188, 359-370.
38. Mustaparta, H. (2002). Encoding of plant odour information in insects: peripheral and central mechanisms. Entomol. Exp. Appl. 104, 1-13.
39. Mustaparta, H., and Stranden, M. (2005). Olfaction and learning in moths and weevils living on angiosperm and gymnosperm hosts. Recent Adv. Phytochem. 39, 269-292.
40. Rein, K., Zöckler, M., Mader, M. T., Grübel, C., and Heisenberg, M. (2002). The Drosophila standard brain. Curr. Biol. 12, 227-231.
41. Reischig, T., and Stengl, M. (2002). Optic lobe commissures in a three-dimensional brain model of the cockroach Leucophaea maderae: a search for the circadian coupling pathways. J. Comp. Neurol. 443, 388-400.
42. Rø, H., Müller, D., and Mustaparta, H. (2007). Anatomical organization of antennal lobe projection neurons in the moth Heliothis virescens. J. Comp. Neurol. 500, 658-675.
43. Rospars, J. P., and Chambille, I. (1981). Deutocerebrum of the cockroach Blaberus craniifer burm. Quantitative study and automated identification of the glomeruli. J. Neurobiol. 12, 221-247.
44. Rospars, J. P., and Hildebrand, J. G. (2000). Sexually dimorphic and isomorphic glomeruli in the antennal lobes of the sphinx moth Manduca sexta. Chem. Senses 25, 119-129.
45. Røstelien, T., Stranden, M., Borg-Karlson, A.-K., and Mustaparta, H. (2005). Olfactory receptor neurones in two heliothine moth species responding selectively to aliphatic green leaf volatiles, aromatics, monoterpenes and sesquiterpenes of plant origin. Chem. Senses 30, 443-461.
46. Sadek, M. M., Hansson, B. S., Rospars, J. P., and Anton, S. (2002). Glomerular representation of plant volatiles and sex pheromone components in the antennal lobe of the female Spodoptera littoralis. J. Exp. Biology. 205, 1363-1376.
47. Schachtner, J., Schmidt, M., and Homberg, U. (2005). Organization and evolutionary trends of primary olfactory brain centers in Tetraconata (Crustacea + Hexapoda). Arthropod Struct. Dev. 34, 257-299.
48. Schmitt, S., Evers, J. F., Duch, C., Scholz, M., and Obermayer, K. (2004). New methods for the computer-assisted 3-D reconstruction of neurons from confocal image stacks. Neuroimage 23, 1283-1298.
49. Skiri, H. T., Rø, H., Berg, B. G., and Mustaparta, H. (2005). Consistent organization of glomeruli in the antennal lobes of related species of heliothine moths. J. Comp. Neurol. 491, 367-380.
50. Smid, H. M., Bleeker, M. A., Van Loon, J. J. A., and Vet, L. E. (2003). Three-dimensional organization of the glomeruli in the antennal lobe of the parasitoid wasps Cotesia glomerata and C. rubecula. Cell Tissue Res. 312, 237-248.
51. Stocker, R. F, Lienhard, M. C., Borst, A., and Fischbach, K. F. (1990). Neuronal architecture of the antennal lobe in Drosophila melanogaster. Cell Tissue Res. 262, 9-34.
52. Stopfer, M. (2007). Olfactory processing: massive convergence onto sparse codes. Curr. Biol. 17, 363-364.
53. Tanaka, N. K., Awasaki, T., Shimada, T., and Ito, K. (2004). Integration of chemosensory pathways in the Drosophila second-order olfactory centers. Curr. Biol. 14, 449-457.
54. Toga, A. W. (2002). Neuroimage databases: the good, the bad and the ugly. Nat. Rev. Neurosci. 3, 302-309.
55. Toga, A. W., and Thompson, P. M. (2001). Maps of the brain. Anat. Rec. 265, 37-53.
56. Van Essen, D. C. (2002). Windows on the brain: the emerging role of atlases and databases in neuroscience. Curr. Opin. Neurobiol. 12, 574-579.
57. Varela, N., Couton, L., Gemeno, C., Avilla, J., Rospars, J. P., and Anton, S. (2009). Three-dimensional antennal lobe atlas of the oriental fruit moth, Cydia molesta (Busck) (Lepidoptera: Tortricidae): comparison of male and female glomerular organization. Cell Tissue Res. 337, 513-526.
58. Vickers, N. J., and Christensen, T. A. (2003). Functional divergence of spatially conserved olfactory glomeruli in two related moth species. Chem. Senses 28, 325-338.
59. Vickers, N. J., Christensen, T. A., and Hildebrand, J. G. (1998). Combinatorial odor discrimination in the brain: Attractive and antagonist odor blends are represented in distinct combinations of uniquely identifiable glomeruli. J. Comp. Neurol. 400, 35-56.
60. Vosshall, L. B., Amrein, H., Morozov, P. S., Rzhetsky, A., and Axel, R. (1999). A spatial map of olfactory receptor expression in the Drosophila antenna. Cell 96, 725-736.
61. Vosshall, L. B., and Stocker, R. F. (2007). Molecular architecture of smell and taste in Drosophila. Annu. Rev. Neurosci. 30, 505-533.
62. Wilson, R. I., and Mainen, Z. F. (2006). Early events in olfactory processing. Annu. Rev. Neurosci. 29, 163-201.
63. Wong, A. M., Wang, J. W., and Axel, R. (2002). Spatial representation of the glomerular map in the Drosophila protocerebrum. Cell 109, 229-241.