Summary
Computer-assisted neuroanatomical methods have been used to demonstrate unique identities of the glomeruli of the antennal lobes (ALs) in males of the sphinx moth Manduca sexta. The glomerular neuropil consists of the male-specific macroglomerular complex, which comprises two closely apposed bulky subunits, and 64±1 “ordinary” glomeruli arrayed in a shell around a central region of coarse neuropil. Computergenerated maps show the exact locations of all glomeruli and adjacent groups of neuronal somata in a constant Cartesian coordinate system, such that these can be accurately identified in any individual. The glomeruli belong to three classes according to the number and type of identification criteria they satisfy. The larger class comprises glomeruli (n=44) identified only in the computer-generated maps on the basis of their relative positions. The other two classes include glomeruli that were also identified in sections, either directly from their proximity to readily identifiable structures and their shape and size (n=10, including the labial-palp-pit-organ (LPO) glomerulus), or indirectly from their positions relative to the former (n=9). Two very small glomeruli were present in only one AL, demonstrating the existence of anomalous glomeruli, whereas another glomerulus had no homologue in both ALs of one individual. The true number of ordinary glomeruli (per male AL) was thus estimated to be 64. The uncertainty in delineating some glomeruli might affect this number without implying modification of the homologies proposed. The locations of tracts and cell groups, both within and near the AL, are also invariant with respect to glomeruli, as shown in the computer maps. The methods employed are general and might be useful to researchers in related fields. The results obtained call for more attention to the precise geometry of neural structures.
Article PDF
Similar content being viewed by others
Avoid common mistakes on your manuscript.
References
Arnold G, Masson C, Budharugsa S (1985) Comparative study of the antennal afferent pathway of the workerbee and the drone (Apis mellifera L). Cell Tissue Res 242:593–605
Boeckh J, Ernst KD (1987) Contribution of single cell analysis in insects to an understanding of olfactory function. J Comp Physiol [A] 161:549–565
Bogner FM, Boppré M, Ernst KD, Boeckh J (1986) CO2 sensitive receptors on labial palps of Rhodogastria moths (Lepidoptera: Arctiidae): physiology, fine structure and central projection. J Comp Physiol [A] 158:741–749
Chambille I, Rospars JP (1981) Le deutocérébron de la blatte Blaberuc craniifer Burm (Dictyoptera: Blaberidae): étude qualitative et identification visuelle des glomérules. Int J Insect Morphol Embryol 10:141–165
Chambille I, Rospars JP (1985) Neurons and identified glomeruli of antennal lobes during postembryonic development in the cockroach Blaberuc craniifer Burm. (Dictyoptera: Blaberidae). Int J Insect Morphol Embryol 14:203–226
Chambille I, Rospars JP, Masson C (1980) The deutocerebrum of the cockroach Blaberuc craniifer Burm: spatial organization of the sensory glomeruli. J Neurobiol 11:135–157
Christensen TA, Hildebrand JG (1987a) Male-specific, sex pheromone-selective projection neurons in the antennal lobes of the moth Manduca sexta. J Comp Physiol [A] 160:553–569
Christensen TA, Hildebrand JG (1987b) Functions, organization, and physiology of the olfactory pathways in the Lepidopteran brain. In: Gupta AP (ed) Arthropod brain, its evolution, development, structure and functions. Wiley, New York, pp 457–484
Ernst KD, Boeckh J (1983) A neuroanatomical study on the organization of the central antennal pathways in insects. II. Neuroanatomical characterization of physiologically defined response types of deutocerebral neurons in Periplaneta americana. Cell Tissue Res 229:1–22
Fischbach KF, Heisenberg M (1984) Neurogenesis and behavior in insects. J Exp Biol 112:65–93
Flanagan D, Mercer AR (1988) An atlas and 3-D reconstruction of the antennal lobes in the worker honey bee, Apis mellifera L (Hymenopera: Apidae). Int J Insect Morphol Embryol 18:145–159
Goll W (1967) Strukturuntersuchungen am Gehirn von Formica. Z Morphol Ökol Tiere 59:143–210
Gregory GE (1980) The Bodian protargol techinque. In: Strausfeld NJ, Miller TA (eds) Neuroanatomical techniques. Springer, Berlin Heidelberg New York, pp 75–95
Hansson B, Christensen TA, Hildebrand JG (1991) Functionally distinct subdivisions of the macroglomerular complex in the antennal lobes of the sphinx moth Manduca sexta. J Comp Neurol 312:264–278
Heisenberg M, Borst A, Wagner S, Byers D (1985) Drosophila mushroom body mutants are deficient in olfactory learning. J Neurogenet 2:1–30
Hildebrand JG, Montague RA (1986) Functional organization of olfactory pathways in the central nervous system of Manduca sexta. In: Payne T, Birch M, Kennedy J (eds) Mechanisms of insect olfaction. Oxford University Press, Oxford, pp 279–285
Hildebrand JG, Matsumoto SG, Camazine SG, Tolbert LP, Blank S, Ferguson H, Ecker V (1980) Organisation and physiology of antennal centres in the brain of the moth Manduca sexta. In: Insect neurobiology and pesticide action (Neurotox 79). Society of Chemical Industry, London, pp 101–107
Hildebrand JG, Christensen TA, Arbas EA, Hayashi JH, Homberg U, Kanzaki R, Stengl M (1992) Olfaction in Manduca sexta: cellular mechanisms of responses to sex pheromone. In: Duce IR (ed) Neurotox '91 — Molecular basis of drug and pesticide action. Elsevier, Amsterdam, pp 323–338
Homberg U (1984) Processing of antennal information in extrinsic mushroom body neurons of the bee brain. J Comp Physiol [A] 154:825–836
Homberg U, Kingan TG, Hildebrand JG (1987) Immunocytochemistry of GABA in the brain and suboesophageal ganglion of Manduca sexta. Cell Tissue Res 248:1–24
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
Homberg U, Christensen TA, Hildebrand JG (1989) Structure and function of the deutocerebrum in insects. Annu Rev Entomol 34:477–501
Hoskins SG, Homberg U, Kingan TG, Christensen TA, Hildebrand JG (1986) Immunocytochemistry of GABA in the antennal lobes of the sphinx moth Manduca sexta. Cell Tissue Res 244:243–252
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
Kanzaki R, Arbas EA, Hildebrand JG (1991a) Physiology and morphology and protocerebral olfactory neurons in the male moth Manduca sexta. J Comp Physiol [A] 168:281–298
Kanzaki R, Arbas EA, Hildebrand JG (1991b) Physiology and morphology of descending neurons in pheromone-processing olfactory pathways in the male moth Manduca sexta. J Comp Physiol [A] 169:1–14
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
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
Lee JK, Altner H (1986) Primary sensory projections of the labial palp-pit organ of Pieris rapae L (Lepidoptera:Pieridae). Int J Insect Morphol Embryol 15:439–448
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 (Biol) 213:249–277
Mobbs PG (1982) The brain of the honeybee Apis mellifera. I. The connections and spatial organization of the mushroom bodies. Philos Trans R Soc Lond (Biol) 298:309–354
Mustaparta A, Masson C (1990) Chemical information processing in the olfactory system of insects. Physiol Rev 70:199–245
Oland LA, Tolbert LP (1987) Glial patterns during early development of antennal lobes in Manduca sexta: a comparison between normal lobes and lobes deprived of antennal axons. J Comp Neurol 255:196–207
Oland LA, Tolbert LP (1989) Patterns of glial proliferation during formation of olfactory glomeruli in an insect. Glia 2:10–24
Olberg RM (1983) Pheromone-triggered flip-flopping interneurons in the ventral nerve cord of the silkworm moth, Bombyx mori. J Comp Physiol [A] 152:297–307
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
Rodrigues V, Pinto L (1989) The antennal glomerulus as a functional unit of odor coding in Drosophila melanogaster. In: Singh RN, Strausfeld NJ (eds) Neurobiology of sensory systems. Plenum, New York, pp 387–396
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 (1988a) Structure and development of the insect antennodeutocerebral system. Int J Insect Morphol Embryol 17:243–294
Rospars JP (1988b) Analyse de structures tridimensionnelles à partir de coupes sériées par un système informatique: application aux lobes antennaires. Ann Soc Entomol Fr 24:450
Rospars JP (1988c) Reconstruction, display and analysis of insect antennal lobes using a computerized digitizing system. Eur Chemorecept Res Org 8:123
Rospars JP, Chambille I (1981) The deutocerebrum of the cockroach Blaberuc 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 and their identified glomeruli in the cockroach Blaberuc craniifer Burm. (Dictyoptera: Blaberidae). Int J Insect Morphol Embryol 15:393–415
Rospars JP, Chambille I (1989) Identified glomeruli in the antennal lobes of insects: invariance, sexual variation and postembryonic development. In: Singh NR, Strausfeld N (eds) Neurobiology of sensory systems. Plenum, New York, pp 355–375
Sanes JR, Hildebrand JG (1976) Structure and development of antennae in a moth, Manduca sexta. Dev Biol 51:282–299
Schildberger K (1983) Multimodal interneurons in the cricket brain: properties of identified extrinsic mushroom body cells. J Comp Physiol [A] 154:71–79
Schneiderman AM, Hildebrand JG, Jacobs JJ (1983) Computeraided morphometry of developing and mature antennal lobes in the moth Manduca sexta. Soc Neurosci Abstr 9:834
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
Singh RN, Nayak SV (1985) Fine structure and primary sensory projections of sensilla on the maxillary palp of Drosophila melanogaster Meigen (Diptera: Drosophilidae). Int J Insect Morphol Embryol 14:291–306
Stocker RF, Singh RN, Shorderet M, Sidiqqi O (1983) Projection patterns of different types of antennal sensilla in the antennal glomeruli of Drosophila melanogaster. Cell Tissue Res 232:237–248
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, Heidelberg New York
tolbert LP, Hildebrandt JG (1981) Organization and synaptic ultrastructure of glomeruli in the antennal lobes of the moth Manduca sexta: a study using thin sections and freeze-fracture. Proc R Soc Lond (Biol) 213:279–301
Tolbert LP, Matsumoto SG, Hildebrand JG (1983) Development of synapses in the antennal lobes of the moth Manduca sexta during metamorphosis. J Neurosci 3:1158–1175
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Rospars, J.P., Hildebrand, J.G. Anatomical identification of glomeruli in the antennal lobes of the male sphinx moth Manduca sexta . Cell Tissue Res 270, 205–227 (1992). https://doi.org/10.1007/BF00328007
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00328007