Abstract
The primary olfactory centres share striking similarities across the animal kingdom. The most conspicuous is their subdivision into glomeruli, which are spherical neuropil masses in which synaptic contacts between sensory and central neurons occur. Glomeruli have both an anatomical identity (being invariant in location, size and shape) and a functional identity (each glomerulus receiving afferents from olfactory receptor neurons that express the same olfactory receptor). Identified glomeruli offer a favourable system for analysing quantitatively the constancy and variability of the neuronal circuits, an important issue for understanding their function, development and evolution. The noctuid moth Spodoptera littoralis with its well-studied pheromone communication system has become a model species for olfaction research. We analyse here its glomerular organisation based on ethyl-gallate-stained and synapsin-stained preparations. Although we have confirmed that the majority of glomeruli can be individually identified in various antennal lobes, we have recognised several types of biological variability. Some glomeruli are absent, possibly indicating the lack of the corresponding receptor neuron type or its misrouting during development. The antennal lobes vary in global shape and, consequently, the spatial location of the glomerular changes. Although they do not prevent glomerulus identification when quantitative analysis methods are used, these variations place limits on the straightforward identification of glomeruli in functional studies, e.g. calcium-imaging or single-cell staining, when using conventional three-dimensional maps of individual antennal lobes.
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References
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
Anton S, Homberg U (1999) Antennal lobe structure. In: Hansson BS (ed) Insect olfaction. Springer, Berlin, pp 98–125
Anton S, Rospars JP (2004) Quantitative analysis of olfactory receptor neuron projections in the antennal lobe of the malaria mosquito, Anopheles gambiae. J Comp Neurol 475:315–326
Anton S, Ignell R, Hansson BS (2002) Developmental changes in the structure and function of the central olfactory system in gregarious and solitary desert locusts. Microsc Res Tech 56:281–291
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
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
Boeckh J, Boeckh V (1979) Threshold and odor specificity of pheromone-sensitive neurons in the deutocerebrum of Antheraea pernyi and A. polyphemus (Saturnidae). J Comp Physiol 132:235–242
Boissonnat JD, Geiger B (1993) Three dimensional reconstruction of complex shapes based on the Delaunay triangulation. In: Acharya RS, Goldgof DB (eds) Biomedical image processing and biomedical visualization. SPIE, Bellingham, Washington
Bucher D, Scholz M, Stetter M, Obermayer K, Pfluger HJ (2000) Correction methods for three-dimensional reconstructions from confocal images. I. Tissue shrinking and axial scaling. J Neurosci Methods 100:135–143
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
Chambille I, Masson C, Rospars JP (1980) The deutocerebrum of the cockroach Blaberus craniifer Burm. Spatial organization of the sensory glomeruli. J Neurobiol 11:135–157
Couto A, Alenius M, Dickson BJ (2005) Molecular, anatomical, and functional organization of the Drosophila olfactory system. Curr Biol 15:1535–1547
Devaud JM, Acebes A, Ramaswami M, Ferrus A (2003) Structural and functional changes in the olfactory pathway of adult Drosophila take place at a critical age. J Neurobiol 56:13–23
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
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
Ernst KD, Boeckh J, Boeckh V (1977) A neuroanatomical study on the organization of the central antennal pathways in insects. Cell Tissue Res 176:285–306
Fiala JC (2005) Reconstruct: a free editor for serial section microscopy. J Microsc 218:52–61
Fishilevich E, Vosshall LB (2005) Genetic and functional subdivision of the Drosophila antennal lobe. Curr Biol 15:1548–1553
Flanagan D, Mercer AR (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
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
Gao Q, Yuan B, Chess A (2000) Convergent projections of Drosophila olfactory neurons to specific glomeruli in the antennal lobe. Nat Neurosci 3:780–785
Ghaninia M, Hansson BS, Ignell R (2007) The antennal lobe of the African malaria mosquito, Anopheles gambiae—innervation and three-dimensional reconstruction. Arthropod Struct Dev 36:23–39
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
Guerenstein PG, Hildebrand JG (2007) Roles and effects of environmental carbon dioxide in insect life. Annu Rev Entomol 53:20–40
Guerenstein PG, Christensen TA, Hildebrand JG (2004) Sensory processing of ambient CO2 information in the brain of the moth Manduca sexta. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 190:707–725
Hallem EA, Dahanukar A, Carlson JR (2006) Insect odor and taste receptors. Annu Rev Entomol 51:113–135
Hansson BS, Anton S (2000) Function and morphology of the antennal lobe: new developments. Annu Rev Entomol 45:203–231
Hansson BS, Christensen TA (1999) Functional characteristics of the antennal lobe. In: Hansson BS (ed) Insect olfaction. Springer, Berlin, pp 125–161
Hanström B (1928) Vergleichende Anatomie des Nervensystems der wirbellosen Tiere. Springer, Berlin
Heisenberg M (2003) Mushroom body memoir: from maps to models. Nat Rev Neurosci 4:266–275
Hildebrand JG, Shepherd GM (1997) Mechanisms of olfactory discrimination: converging evidence for common principles across phyla. Annu Rev Neurosci 20:595–631
Huetteroth W, 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
Ignell R, Anton S, Hansson BS (2001) The antennal lobe of orthoptera—anatomy and evolution.Brain Behav Evol 57:1-17
Ignell R, Dekker T, Ghaninia M, Hansson BS (2005) Neuronal architecture of the mosquito deutocerebrum. J Comp Neurol 493:207–240
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
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 doi:10.1007/s00441-009-0756-3
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
Kent KS, Harrow ID, Quartararo P, Hildebrand JG (1986) An accessory olfactory pathway in Lepidoptera: the labial pit organ and its central projections in Manduca sexta and certain other sphinx moths and silk moths. Cell Tissue Res 245:237–245
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
Kurylas AE, Rohlfing T, Krofczik S, Jenett A, Homberg U (2008) Standardized atlas of the brain of the desert locust, Schistocerca gregaria. Cell Tissue Res 333:125–145
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
Leise EM, Mulloney B (1986) The osmium-ethyl gallate procedure is superior to silver impregnations for mapping neuronal pathways. Brain Res 367:265–272
Linster C, Sachse S, Galizia G (2005) Computational modeling suggests that response properties rather than spatial position determine connectivity between olfactory glomeruli. J Neurophysiology 93:3410–3417
Masante-Roca I, Gadenne C, 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
Ochieng SA, Anderson P, Hansson BS (1995) Antennal lobe projection patterns of olfactory receptor neurons involved in sex pheromone detection in Spodoptera littoralis (Lepidoptera: Noctuidae). Tissue Cell 27:221–232
Pinto L, Stocker RF, Rodrigues V (1988) Anatomical and neurochemical classification of the antennal glomeruli in Drosophila melanogaster Meigen (Diptera: Drosophilidae). Int J Insect Morphol Embryol 17:335–344
Ray A, Goes van Naters W van der, Shiraiwa T, Carlson JR (2007) Mechanisms of odor receptor gene choice in Drosophila. Neuron 53:353–369
Rein K, Zöckler M, Mader M, Grübel C, Heisenberg M (2002) The Drosophila standard brain. Curr Biol 12:227–231
Reisenman CE, Christensen TA, Hildebrand JG (2005) Chemosensory selectivity of output neurons innervating an identified, sexually isomorphic olfactory glomerulus. J Neurosci 25:8017–8026
Reisenman CE, Heinbockel T, Hildebrand JG (2008) Inhibitory interactions among olfactory glomeruli do not necessarily reflect spatial proximity. J Neurophysiol 100:554–564
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
Rospars JP (1988) Structure and development of the insect antennodeutocerebral system. Int J Insect Morphol Embryol 17:243–294
Rospars JP, Chambille I (1981) Deutocerebrum of the cockroach Blaberus craniifer Burm. Quantitative study and automated identification of the glomeruli. J Neurobiol 12:221–247
Rospars JP, Chambille I (1986) Postembryonic growth of antennal lobes in the cockroach Blaberus craniifer: a morphometric study. Int J Insect Morphol Embryol 15:393–415
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
Rospars JP, Hildebrand JG (2000) Sexually dimorphic and isomorphic glomeruli in the antennal lobes of the sphinx moth Manduca sexta. Chem Senses 25:119–129
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
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
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
Silbering AF, Galizia CG (2007) Processing of odor mixtures in the Drosophila antennal lobe reveals both global inhibition and glomerulus-specific interactions. J Neurosci 27:11966–11977
Skiri HT, Ro H, Berg BG, Mustaparta H (2005) Consistent organization of glomeruli in the antennal lobes of related species of heliothine moths. J Comp Neurol 491(4):367–380
Snedecor GW, Cochran WG (1967) Statistical methods, 6th edn. Iowa State University Press, Iowa
Stocker RF, Lienhard MC, Borst A, Fischbach KF (1990) Neuronal architecture of the antennal lobe in Drosophila melanogaster. Cell Tissue Res 262:9–34
Strausfeld NJ (1976) Atlas of an insect brain. Springer, Berlin Heidelberg New York
Strausfeld NJ, Hildebrand JG (1999) Olfactory systems: common design, uncommon origins? Curr Opin Neurobiol 9:634–639
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
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 (in press)
Vosshall LB, Wong AM, Axel R (2000) An olfactory sensory map in the fly brain. Cell 102:147–159
Wilson RI, Laurent G (2005) Role of GABAergic inhibition in shaping odor-evoked spatiotemporal patterns in the Drosophila antennal lobe. J Neurosci 25:9069–9079
Wilson RI, Turner GC, Laurent G (2004) Transformation of olfactory representations in the Drosophila antennal lobe. Nature 303:366–370
Zube C, Kleineidam CJ, Kirschner S, Neef J, Roessler W (2008) Organization of the olfactory pathway and odor processing in the antennal lobe of the ant Camponotus floridanus. J Comp Neurol 506:425–441
Acknowledgments
We thank J.-M. Nichols, L. Lloris, C. Chauvet and C. Gaertner for help with insect rearing and technical assistance. R. Barrozo's assistance with the preparation of the figures is greatly acknowledged. We are also grateful to C. Gadenne, N. Varela and D. Jarriault for critically reading an earlier version of the manuscript.
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This work was supported by research grants from INRA (Projet Jeune Equipe and Projet S.P.E.) to S.A. and J.P.R. and from ANR-BBSRC 07 BSYS 006 (Pherosys) to J.P.R. and S.A. and by a PhD grant from INRA Departments M.I.A. and S.P.E. to L.C.
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Couton, L., Minoli, S., Kiêu, K. et al. Constancy and variability of identified glomeruli in antennal lobes: computational approach in Spodoptera littoralis . Cell Tissue Res 337, 491–511 (2009). https://doi.org/10.1007/s00441-009-0831-9
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DOI: https://doi.org/10.1007/s00441-009-0831-9