Heterogeneity in dendritic morphology of moth antennal lobe projection neurons

Journal of Comparative Neurology

Volumn 519, Issue 17, 2011, Pages 3367-3386

  Namiki, Shigehiro ^a   Kanzaki, Ryohei ^a  

^a UNIVERSITY OF TOKYO   (Japan)

Author keywords

Bombyx mori; Digital atlas; Glomeruli; Neuronal diversity; Olfaction; Pheromone

Indexed keywords

ANIMAL ANATOMY; ANIMAL CELL; ANTENNAL LOBE; ANTENNOCEREBRAL TRACT; ARTICLE; BRAIN GLOMERULUS; BRAIN NERVE CELL; BRAIN REGION; CELL HETEROGENEITY; CONTROLLED STUDY; DENDRITE; INNERVATION; NERVE PROJECTION; NERVE TRACT; NEUROANATOMY; NONHUMAN; PRIORITY JOURNAL; PROJECTION NEURON; PROTOCEREBRUM; SILKWORM;

ANIMALS; ARTHROPOD ANTENNAE; BOMBYX; DENDRITES; MALE; MOTHS; NEURAL PATHWAYS; NEURONS; OLFACTORY PATHWAYS;

EID: 80053274888     PISSN: 00219967     EISSN: 10969861     Source Type: Journal    
DOI: 10.1002/cne.22754     Document Type: Article

References (101)

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 voltage-sensitive dye imaging. J Exp Biol 207: 633-644.
3. Anton S, Hansson BS. 1994. Central processing of sex pheromone, host odour, and oviposition deterrent information by interneurons in the antennal lobe of female Spodoptera littoralis (Lepidoptera: Noctuidae). J Comp Neurol 350: 199-214.
4. Anton S, Hansson BS. 1995. Sex pheromone and plant-associated odour processing in antennal lobe interneurons of male Spodoptera littoralis (Lepidoptera: Noctuidae). J Comp Physiol A 176: 773-789.
5. Anton S, Homberg U. 1999. Antennal lobe structure. In: Hansson BS, editor. Insect olfaction. Berlin: Springer. p 97-124.
6. Ascoli GA, Alonso-Nanclares L, Anderson SA, Barrionuevo G, Benavides-Piccione R, Burkhalter A, Buzsaki G, Cauli B, Defelipe J, Fairen A, Feldmeyer D, Fishell G, Fregnac Y, Freund TF, Gardner D, Gardner EP, Goldberg JH, Helmstaedter M, Hestrin S, Karube F, Kisvarday ZF, Lambolez B, Lewis DA, Marin O, Markram H, Munoz A, Packer A, Petersen CC, Rockland KS, Rossier J, Rudy B, Somogyi P, Staiger JF, Tamas G, Thomson AM, Toledo-Rodriguez M, Wang Y, West DC, Yuste R. 2008. Petilla terminology: nomenclature of features of GABAergic interneurons of the cerebral cortex. Nat Rev Neurosci 9: 557-568.
7. Berdnik D, Chihara T, Couto A, Luo L. 2006. Wiring stability of the adult Drosophila olfactory circuit after lesion. J Neurosci 26: 3367-3376.
8. Berg BG, Galizia CG, Brandt R, 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.
9. 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.
10. Chelaru MI, Dragoi V. 2008. Efficient coding in heterogeneous neuronal populations. Proc Natl Acad Sci U S A 105: 16344-16349.
11. Chen CC, Abrams S, Pinhas A, Brumberg JC. 2009. Morphological heterogeneity of layer VI neurons in mouse barrel cortex. J Comp Neurol 512: 726-746.
12. Chou YH, Spletter ML, Yaksi E, Leong JCS, Wilson RI, Luo L. 2010. Diversity and wiring variability of olfactory local interneurons in the Drosophila antennal lobe. Nat Neurosci 13: 439-449.
13. Christensen TA, Hildebrand JG. 1987. Male-specific, sex pheromone-sensitive projection neurons in the antennal lobes of the moth Manduca sexta. J Comp Physiol A 160: 553-569.
14. Christensen TA, Hildebrand JG. 2002. Pheromonal and host-odor processing in the insect antennal lobe: how different? Curr Opin Neurobiol 12: 393-399.
15. Christensen TA, Waldrop BR, Harrow ID, Hildebrand JG. 1993. Local interneurons and information processing in the olfactory glomeruli of the moth Manduca sexta. J Comp Physiol A 173: 385-399.
16. Christensen TA, Waldrop BR, Hildebrand JG. 1998. Multitasking in the olfactory system: context-dependent odors reveal dual GABA-regulated coding mechanisms in single olfactory projection neurons. J Neurosci 18: 5999-6008.
17. Clyne PJ, Warr CG, Freeman MR, Lessing D, Kim J, Carlson JR. 1999. A novel family of divergent seven-transmembrane proteins: candidate odorant receptors in Drosophila. Neuron 22: 327-338.
18. Couton L, Minoli S, Kiêu K, Anton S, Rospars JP. 2009. Constancy and variability of identified glomeruli in antennal lobes: computational approach in Spodoptera littoralis. Cell Tissue Res 337: 491-511.
19. Datta SR, Vasconcelos ML, Ruta V, Luo S, Wong A, Demir E, Flores J, Balonze K, Dickson BJ, Axel R. 2008. The Drosophila pheromone cVA activates a sexually dimorphic neural circuit. Nature 452: 473-477.
20. Distler PG, Boeckh J. 1996. Synaptic connection between olfactory receptor cells and uniglomerular projection neurons in the antennal lobe of the American cockroach, Periplaneta americana. J Comp Neurol 370: 35-46.
21. Distler PG, Boeckh J. 1997. Synaptic connections between identified neuron types in the antennal lobe glomeruli of the cockroach, Periplaneta americana: I. Uniglomerular projection neurons. J Comp Neurol 378: 307-319.
22. Distler PG, Gruber C, Boeckh J. 1998. Synaptic connections between GABA-immunoreactive neurons and uniglomerular projection neurons within the antennal lobe of the cockroach, Periplaneta americana. Synapse 29: 1-13.
23. Fonta C, Sun XJ, Masson C. 1993. Morphology and spatial distribution of bee antennal lobe interneurones responsive to odours. Chem Senses 18: 101-119.
24. Galizia CG, Rössler W. 2010. Parallel olfactory systems in insects: anatomy and function. Annu Rev Entomol 55: 399-420.
25. Galizia CG, McIlwrath SL, Menzel R. 1999. Digital three-dimensional atlas of the honeybee antennal lobe based on optical sections acquired by confocal microscopy. Cell Tissue Res 295: 383-394.
26. Greiner B, Gadenne C, 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.
27. 2 information in the brain of the moth Manduca sexta. J Comp Physiol A 190: 707-725.
28. Han Q, Hansson BS, Anton S. 2005. Interactions of mechanical stimuli and sex pheromone information in antennal lobe neurons of a male moth, Spodoptera littoralis. J Comp Physiol A 191: 521-528.
29. Hansson BS, Anton S, Christensen TA. 1994. Structure and function of antennal lobe neurons in the male turnip moth, Agrotis segetum (Lepidoptera: Noctuidae). J Comp Physiol A 175: 547-562.
30. Heinbockel T, Hildebrand JG. 1998. Antennal receptive fields of pheromone-responsive projection neurons in the antennal lobes of the male sphinx moth Manduca sexta. J Comp Physiol A 183: 121-133.
31. Hildebrand JG, Shepherd GM. 1997. Mechanisms of olfactory discrimination: converging evidence for common principles across phyla. Annu Rev Neurosci 20: 595-631.
32. Hill ES, Okada K, Kanzaki R. 2003. Visualization of modulatory effects of serotonin in the silkmoth antennal lobe. J Exp Biol 206: 345-352.
33. 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.
34. Homberg U, Christensen TA, Hildebrand JG. 1989. Structure and function of the deutocerebrum in insects. Annu Rev Entomol 34: 477-501.
35. Hösl M. 1990. Pheromone-sensitive neurons in the deutocerebrum of Periplaneta americana: receptive fields on the antenna. J Comp Physiol A 167: 321-327.
36. Iwano M, Kanzaki R. 2005. Immunocytochemical identification of neuroactive substances in the antennal lobe of the male silkworm moth Bombyx mori. Zool Sci 22: 199-211.
37. Jarriault D, Gadenne C, Lucas P, Rospars JP, Anton S. 2010. Transformation of the sex pheromone signal in the noctuid moth Agrotis ipsilon: from peripheral input to antennal lobe output. Chem Senses doi:10.1093/chemse/bjq069.
38. Jayaraman V, Laurent G. 2007. Evaluating a genetically encoded optical sensor of neural activity using electrophysiology in intact adult fruit flies. Front Neural Circuits 1: 3.
39. Jefferis GS, Potter CJ, Chan AM, Marin EC, Rohlfing T, Maurer CR Jr, Luo L. 2007. Comprehensive maps of Drosophila higher olfactory centers: spatially segregated fruit and pheromone representation. Cell 128: 1187-1203.
40. Kaissling KE. 2009. Olfactory perireceptor and receptor events in moths: a kinetic model revised. J Comp Physiol A 195: 895-922.
41. Kanzaki R, Shibuya T. 1983. Olfactory neural pathway and sexual pheromone responses in the deutocerebrum of the male silkworm moth, Bombyx mori (Lepidoptera: Bombycidae). Appl Entomol Zool 18: 131-133.
42. Kanzaki R, Shibuya T. 1986. Identification of the deutocerebral neurons responding to the sexual pheromone in the male silkworm moth brain. Zool Sci 3: 409-418.
43. Kanzaki R, Arbas EA, Strausfeld NJ, Hildebrand JG. 1989. Physiology and morphology of projection neurons in the antennal lobe of the male moth Manduca sexta. J Comp Physiol A 165: 427-453.
44. 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.
45. Kazama H, Wilson RI. 2009. Origins of correlated activity in an olfactory circuit. Nat Neurosci 12: 1136-1144.
46. Kazawa T, Ikeno H, Kanzaki R. 2008. Development and application of a neuroinformatics environment for neuroscience and neuroethology. Neural Networks 21: 1047-1055.
47. Kazawa T, Namiki S, Fukushima R, Terada M, Soo K, Kanzaki R. 2009. Constancy and variability of glomerular organization in the antennal lobe of the silkmoth. Cell Tissue Res 336: 119-136.
48. Kent KS, Harrow ID, Quartararo P, Hildebrand JG. 1986. An accessory olfactory pathway in Lepidoptera: the labial pit organ and its central projections in the Manduca sexta and certain other sphinx moths and silk moths. Cell Tissue Res 245: 237-245.
49. 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.
50. Koontz MA, Schneider D. 1987. Sexual dimorphism in neuronal projections from the antennae of silk moths (Bombyx mori, Antheraea polyphemus) and the gypsy moth (Lymantria dispar). Cell Tissue Res 249: 39-50.
51. Krofczik S, Menzel R, Nawrot M. 2009. Rapid odor processing in the honeybee antennal lobe network. Front Comput Neurosci 2: 9.
52. Kvello P, Løfaldli BB, Rybak J, Menzel R, 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.
53. Laissue PP, Reiter C, Hiesinger PR, Halter S, Fischbach KF, Stocker RF. 1999. Three-dimensional reconstruction of the antennal lobe in Drosophila melanogaster. J Comp Neurol 405: 543-552.
54. Lin HH, Lai JS, Chin AL, Chen YC, Chiang AS. 2007. A map of olfactory representation in the Drosophila mushroom body. Cell 128: 1205-1217.
55. Lledo PM, Merkle FT, Alvarez-Buylla A. 2008. Origin and function of olfactory bulb interneuron diversity. Trends Neurosci 31: 392-400.
56. Løfaldli BB, Kvello P, Mustaparta H. 2010. Integration of the antennal lobe glomeruli and three projection neurons in the standard brain atlas of the moth Heliothis virescens. Front Syst Neurosci 4: 5.
57. 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.
58. Malun D, Oland LA, Tolbert LP. 1994. Uniglomerular projection neurons participate in early development of olfactory glomeruli in the moth Manduca sexta. J Comp Neurol 350: 1-22.
59. Marder E, Goaillard JM. 2006. Variability, compensation and homeostasis in neuron and network function. Nat Rev Neurosci 7: 563-574.
60. Marin EC, Jefferis GSXE, Komiyama T, Zhu H, Luo L. 2002. Representation of the glomerular olfactory map in the Drosophila brain. Cell 109: 243-255.
61. Masante-Roca I, Gadenne C, Anton S. 2002. Plant odour processing in the antennal lobe of the male and female grapevine moths, Lobesia botrana (Lepidoptera: Tortricidae). J Insect Physiol 48: 1111-1121.
62. Matsumoto SG, Hildebrand JG. 1981. Olfactory mechanisms in the moth Manduca sexta: response characteristics and morphology of central neurons in the antennal lobes. Proc R Soc Lond B Biol Sci 1192: 249-277.
63. 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.
64. Namiki S, Kanzaki R. 2008. Reconstructing the population activity of olfactory output neurons that innervate identifiable processing units. Front Neural Circuits 2: 1.
65. Namiki S, Iwabuchi S, Kanzaki R. 2008. Representation of a mixture of pheromone and host plant odor by antennal lobe projection neurons of the silkmoth Bombyx mori. J Comp Physiol A 194: 501-515.
66. Namiki S, Haupt SS, Kazawa T, Takashima A, Ikeno H, Kanzaki R. 2009. Reconstruction of virtual neural circuits in an insect brain. Front Neurosci 32: 1-9.
67. 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.
68. Padmanabhan K, Urban NN. 2010. Intrinsic biophysical diversity decorrelates neuronal firing while increasing information content. Nat Neurosci doi:10.1038/nn.2630.
69. Rall W, Shepherd GM, Reese TS, Brightman MW. 1966. Dendrodendritic synaptic pathway for inhibition in the olfactory bulb. Exp Neurol 14: 44-56.
70. Reisenman CE, Christensen TA, Francke W, Hildebrand JG. 2004. Enantioselectivity of projection neurons innervating identified olfactory glomeruli. J Neurosci 24: 2602-2611.
71. Reisenman CE, Christensen TA, Hildebrand JG. 2005. Chemosensory selectivity of output neurons innervating an identified, sexually isomorphic olfactory glomerulus. J Neurosci 25: 8017-8026.
72. Rø H, Müller D, Mustaparta H. 2007. Anatomical organization of antennal lobe projection neurons in the moth Heliothis virescens. J Comp Neurol 500: 658-675.
73. Rospars JP. 1983. Invariance and sex-specific variations of the glomerular organization in the antennal lobes of a moth, Mamestra brassicae, and a butterfly, Pieris brassicae. J Comp Neurol 220: 80-96.
74. Rospars JP, Hildebrand JG. 1992. Anatomical identification of glomeruli in the antennal lobes of the sphinx moth Manduca sexta. Cell Tissue Res 270: 205-227.
75. Rybak J, Kuß A, Lamcker H, Zachow S, Hege HC, Lienhard M, Singer J, Neubert K, Menzel R. 2010. The digital bee brain: integrating and managing neurons in a common 3D reference system. Front Syst Neurosci 4: 30.
76. 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.
77. Sadek MM, Hansson BS, Rospars JP, Anton S. 2002. Glomerular representation of plant volatiles and sex pheromone components in the antennal lobe of the female Spodoptera littoralis. J Exp Biol 205: 1363-1376.
78. Sanes JR, Hildebrand JG. 1976a. Structure and development of antennae in a moth, Manduca sexta. Dev Biol 51: 280-299.
79. Sanes JR, Hildebrand JG. 1976b. Origin and morphogenesis of sensory neurons in an insect antenna. Dev Biol 51: 300-319.
80. Schachtner J, Schmidt M, Homberg U. 2005. Organization and evolutionary trends of primary olfactory brain centers in Tetraconata (Crustacea + Hexapoda). Arthropod Struct Dev 34: 257-299.
81. Seki Y, Kanzaki R. 2008. Comprehensive morphological identification and GABA immunocytochemistry of antennal lobe local interneurons in Bombyx mori. J Comp Neurol 506: 93-107.
82. Seki Y, Aonuma H, Kanzaki R. 2005. Pheromone processing center in the protocerebrum of Bombyx mori revealed by NO-induced anti-cGMP immunocytochemistry. J Comp Neurol 481: 340-351.
83. Seki Y, Rybak J, Wicher D, Sachse S, Hansson BS. 2010. Physiological and morphological characterization of local interneurons in the Drosophila antennal lobe. J Neurophysiol 104: 1007-1019.
84. Selzer R. 1979. Morphological and physiological identification of food odour specific neurones in the deutocerebrum of Periplaneta americana. J Comp Physiol A 134: 159-163.
85. Shepherd G, Chen WR, Greer CA. 2004. Olfactory bulb. In: Shepherd GM, editor. Synaptic organization of the brain, 5th ed. New York: Oxford University Press. p 165-216.
86. Skiri HT, Rø H, Berg BG, Mustaparta H. 2005. Consistent organization of glomeruli in the antennal lobes of related species of heliothine moths. J Comp Neurol 491: 367-380.
87. Smid HM, Bleeker MA, van Loon JJ, Vet LEM. 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.
88. Stocker RF, Lienhard MC, Borst A, Fischbach KF. 1990. Neuronal architecture of the antennal lobe in Drosophila melanogaster. Cell Tissue Res 262: 9-34.
89. Stopfer M, Jayaraman V, Laurent G. 2003. Intensity versus identity coding in an olfactory system. Neuron 39: 991-1004.
90. Sun XJ, Tolbert LP, Hildebrand JG. 1997. Synaptic organization of the uniglomerular projection neurons of the antennal lobe of the moth Manduca sexta: a laser scanning confocal and electron microscopic study. J Comp Neurol 379: 2-20.
91. 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.
92. Tolbert LP, Oland LA, Tucker ES, Gibson NJ, Higgins MR, Lipscomb BW. 2004. Bidirectional influences between neurons and glial cells in the developing olfactory system. Prog Neurobiol 73: 73-105.
93. Tripathy SJ, Peters OJ, Staudacher EM, Kalwar FR, Hatfield MN, Daly KC. 2010. Odors pulsed at wing beat frequencies are tracked by primary olfactory networks and enhance odor detection. Front Cell Neurosci 4: 1.
94. Varela N, Couton L, Gemeno C, Avilla J, Rospars JP, 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.
95. Vickers NJ, Christensen TA, Hildebrand JG. 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.
96. Vosshall LB, Amrein H, Morozov PS, Rzhetsky A, Axel R. 1999. A spatial map of olfactory receptor expression in the Drosophila antenna. Cell 96: 725-736.
97. Wilson RI, Turner GC, Laurent G. 2004. Transformation of olfactory representations in Drosophila antennal lobe. 303: 366-370.
98. Winnington AP, Napper RM, Mercer AR. 1996. Structural plasticity of identified glomeruli in the antennal lobes of the adult worker honey bee. J Comp Neurol 365: 479-490.
99. Wong AM, Wang JW, Axel R. 2002. Spatial representation of the glomerular map in the Drosophila protocerebrum. Cell 109: 229-241.
100. Yamagata N, Schmuker M, Szyszka P, Mizunami M, Menzel R. 2009. Differential odor processing in two olfactory pathways in the honeybee. Front Syst Neurosci 3: 16.
101. Zhao XC, Berg BG. 2010. Arrangement of output information from the three macroglomerular units in the Heliothine moth Helicoverpa assulta: morphological and physiological features of male-specific projection neurons. Chem Senses 35: 511-521.