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Neuronal architecture of the antennal lobe in Drosophila melanogaster

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Summary

Computer reconstruction of the antennal lobe of Drosophila melanogaster has revealed a total of 35 glomeruli, of which 30 are located in the periphery of the lobe and 5 in its center. Several prominent glomeruli are recognizable by their location, size, and shape; others are identifiable only by their positions relative to prominent glomeruli. No obvious sexual dimorphism of the glomerular architecture was observed. Golgi impregnations revealed: (1) Five of the glomeruli are exclusive targets for ipsilateral antennal input, whereas all others receive afferents from both antennae. Unilateral amputation of the third antennal segment led to a loss of about 1000 fibers in the antennal commissure. Hence, about 5/6 of the approximately 1200 antennal afferents per side have a process that extends into the contralateral lobe. (2) Afferents from maxillary palps (most likely from basiconic sensilla) project into both ipsi-and contralateral antennal lobes, yet their target glomeruli are apparently not the same as those of antennal basiconic sensilla. (3) Afferents in the antennal lobe may also stem from pharyngeal sensilla. (4) The most prominent types of interneurons with arborizations in the antennal lobe are: (i) local interneurons ramifying in the entire lobe, (ii) unilateral relay interneurons that extend from single glomeruli into the calyx and the lateral protocerebrum (LPR), (iii) unilateral interneurons that connect several glomeruli with the LPR only, (iv) bilateral interneurons that link a small number of glomeruli in both antennal lobes with the calyx and LPR, (v) giant bilateral interneurons characterized by extensive ramifications in both antennal lobes and the posterior brain and a cell body situated in the midline of the suboesophageal ganglion, and (vi) a unilateral interneuron with extensive arborization in one antennal lobe and the posterior brain and a process that extends into the thorax. These structural results are discussed in the context of the available functional and behavioral data.

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Abbreviations

AC :

antennal commissure

AMMC :

antennal mechanosensory and motor center

iACT, mACT, oACT :

inner/middle/outer antenno-cerebral tract

bACTI, uACTI :

bilateral/unilateral ACT relay interneuron

AN :

antennal nerve

AST :

antenno-suboesophageal tract

FAI :

fine arborization relay interneuron

GSI :

giant symmetric relay interneuron

LI :

local interneuron

LPR :

lateral protocerebrum

SOG :

suboesophageal ganglion

TI :

thoracic relay interneuron

bVI :

bilateral V-relay interneuron

References

  • Blest AD, Davie PS (1980) Reduced silver impregnations derived from the Holmes technique. In: Strausfeld NJ, Miller TA (eds) Neuroanatomical techniques: insect nervous system. Springer, New York Berlin Heidelberg, pp 97–130

    Google Scholar 

  • 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 A 132:235–242

    Google Scholar 

  • Boeckh J, Sandri C, Akert K (1970) Sensorische Eingänge und synaptische Verbindungen in Zentralnervensystem von Insekten. Z Zellforsch 103:429–446

    Google Scholar 

  • Boeckh J, Ernst KD, Sass H, Waldow U (1984) Anatomical and physiological characteristics of individual neurones in the central antennal pathway of insects. J Insect Physiol 30:15–26

    Google Scholar 

  • Boeckh J, Distler P, Ernst KD, Hösl M, Malun D (1990) Olfactory bulb and antennal lobe. In: Schild D (ed) Information processing of chemical sensory stimuli. Springer, New York Berlin Heidelberg

    Google Scholar 

  • Bogner F, 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

    Google Scholar 

  • Borst A (1983) Computation of olfactory signals in Drosophila melanogaster. J Comp Physiol A 152:373–383

    Google Scholar 

  • Borst A, Fischbach KF (1987) Golgi-and degeneration studies of the antennal lobes of Drosophila melanogaster. J Neurogenet 4:115–117

    Google Scholar 

  • Borst A, Heisenberg M (1982) Osmotropotaxis in Drosophila melanogaster. J Comp Physiol A 147:479–484

    Google Scholar 

  • Buchner E, Bader R, Buchner S, Cox J, Emson PC, Flory E, Heizmann CW, Hemm S, Hofbauer A, Oertel WH (1988) Cell specific immuno-probes for the brain of normal and mutant Drosophila melanogaster. I. Wildtype visual system. Cell Tissue Res 253:357–370

    Google Scholar 

  • Burrows M, Boeckh J, Esslen J (1982) Physiological and morphological properties of interneurons in the deutocerebrum of male cockroaches which respond to female pheromone. J Comp Physiol A 145:447–457

    Google Scholar 

  • Chambille I, Rospars JP (1981) Deutocérébron de la blatte Blaberus craniifer Burm. (Dictyotera: Blaberidae): étude qualitative et identification morphologique des glomérules. Int J Insect Morphol Embryol 10:141–165

    Google Scholar 

  • Chapman RF (1982) Chemoreception. The significance of receptor numbers. Adv Insect Physiol 16:247–356

    Google Scholar 

  • Christensen TA, Hildebrand JG (1987) Functions, organization, and physiology of the olfactory pathways in the lepidopteran brain. In: Gupta AP (ed) Arthropod brain: its evolution, development, structure, and function. John Wiley and Sons, New York, pp 457–484

    Google Scholar 

  • Colonnier M (1964) The tangential organization of the visual cortex. J Anat 98:327–344

    Google Scholar 

  • Distler P (1989) Histochemical demonstration of GABA-like immunoreactivity in cobalt labeled neuron individuals in the insect olfactory pathway. Histochemistry 91:245–249

    Google Scholar 

  • Ernst KD, Boeckh J (1983) A neuroanatomical study of the central antennal pathways in insects. III. Neuroanatomical characterization of physiologically defined response types of deutocerebral neurons in Periplanta americana. Cell Tissue Res 229:1–22

    Google Scholar 

  • Ernst KD, Boeckh J, Boeckh V (1977) A neuroanatomical study of the central antennal pathways in insects. II. Deutocerebral connections in Locusta migratoria and Periplaneta americana. Cell Tissue Res 176:285–308

    Google Scholar 

  • Fischbach KF, Dittrich APM (1989) The optic lobe of Drosophila melanogaster. I. A Golgi analysis of wild-type structure. Cell Tissue Res 258:441–475

    Google Scholar 

  • Fischbach KF, Götz CR (1981) Das Experiment. Ein Blick ins Fliegengehirn-Golgi gefärbte Nervenzellen bei Drosophila. BIUZ 11:183–187

    Google Scholar 

  • Fischbach KF, Heisenberg M (1984) Neurogenetics and behaviour in insects. J Exp Biol 112:65–93

    Google Scholar 

  • Foelix RF, Stocker RF, Steinbrecht RA (1989) Fine structure of a sensory organ in the arista of Drosophila melanogaster and some other dipterans. Cell Tissue Res 258: 277–287

    Google Scholar 

  • Ghysen A, O'Kane CJ (1989) Neural enhancer-like elements as specific cell markers in Drosophila. Development 105:35–52

    Google Scholar 

  • Hanesch U, Fischbach KF, Heisenberg M (1989) Neuronal architecture of the central complex in Drosophila melanogaster. Cell Tissue Res 257: 343–366

    Google Scholar 

  • Hardie RC (1983) Projection and connectivity of sex-specific photoreceptors in the compound eye of the male housefly (Musca domestica). Cell Tissue Res 233:1–21

    Google Scholar 

  • Heisenberg M, Borst A, Wagner S, Byers D (1985) Drosophila mushroom body mutants are deficient in olfactory learning. J Neurogenet 2:1–30

    Google Scholar 

  • Helfand SL, Carlson JR (1989) Isolation and characterization of an olfactory mutant in Drosophila with a chemically specific defect. Proc Natl Acad Sci USA 86:2908–2912

    Google Scholar 

  • Homberg U (1984) Processing of antennal information in extrinsic mushroom body neurons of the bee brain. J Comp Physiol A 154:825–836

    Google Scholar 

  • 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

    Google Scholar 

  • Homberg U, Christensen TA, Hildebrand JG (1989) Structure and function of the deutocerebrum in insects. Annu Rev Entomol 34:477–501

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • Kent KS, Harrow ID, Quartaro 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

    Google Scholar 

  • Kent KS, Hoskins SG, Hildebrand JG (1987) A novel serotonin-immunoreactive neuron in the antennal lobe of the sphinx moth Manduca sexta persists throughout postembryonic life. J Neurobiol 18:451–465

    Google Scholar 

  • 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

    Google Scholar 

  • Koto M, Tanouye MA, Ferrus A, Thomas JB, Wyman RJ (1981) The morphology of the cervical giant fiber neuron of Drosophila. Brain Res 221:213–217

    Google Scholar 

  • Kraus D, Malun D, Waldow U, Boeckh J (1988) Tracts between the deuto- and the protocerebrum in male Periplaneta americana, and distribution, fine structure, and connections of terminals of identified deurocerebral projection neurons. Proc 16th Göttingen Neurobiol Conf, p 62

  • 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 15:439–488

    Google Scholar 

  • Lee JK, Selzer R, Altner H (1985) Lamellated outer dendritic segments of a chemoreceptor within wall-pore sensilla in the labial palp pit organ in the butterfly, Pieris rapae L. (Insecta, Lepidoptera). Cell Tissue Res 240:333–342

    Google Scholar 

  • Lienhard MC, Stocker RF (1987) Sensory projection patterns of supernumerary legs and aristae in D. melanogaster. J Exp Zool 244:187–201

    Google Scholar 

  • Light DM (1986) Central integration of sensory signals: an exploration of processing of pheromonal and multimodal information in lepidopteran brains. In: Payne TL, Birch MC, Kennedy CEJ (eds) Mechanisms in insect olfaction. Clarendon, Oxford, pp 287–301

    Google Scholar 

  • 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

    Google Scholar 

  • McKenna M, Monte P, Helfand SL, Woodard C, Carlson JR (1989) A simple chemosensory response in Drosophila and the isolation of acj mutations in which it is affected. Proc Natl Acad Sci USA 86:8118–8122

    Google Scholar 

  • Miller A (1950) The internal anatomy and histology of the imago of Drosophila melanogaster. In: Demerec M (ed) Biology of Drosophila. Hafner, New York, pp 420–534

    Google Scholar 

  • 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

    Google Scholar 

  • Nässel DR (1987) Neuroactive substances in the insect CNS. In: Ali MA (ed) Nervous systems in invertebrates. Plenum, New York, pp 171–212

    Google Scholar 

  • Nässel DR, Högmo O, Hallberg E (1984) Antennal receptors in the blowfly Calliphora erythrocephala. I. The gigantic central projection of the pedicellar campaniform sensillum. J Morphol 180:159–169

    Google Scholar 

  • Nayak SV, Singh RN (1983) Sensilla on the tarsal segments and mouthparts of adult Drosophila melanogaster Meigen (Diptera: Drosophilidae). Int J Insect Morphol Embryol 12:273–291

    Google Scholar 

  • Nayak SV, Singh RN (1985) Primary sensory projections from the labella to the brain of Drosophila melanogaster Meigen (Diptera: Drosophilidae). Int J Insect Morphol Embryol 14:115–129

    Google Scholar 

  • Oland LA, Tolbert LP (1987) Glial patterns during early development of antennal lobes of Manduca sexta: a comparison between normal lobes and lobes deprived of antennal neurons. J Comp Neurol 255:196–207

    Google Scholar 

  • Oland LA, Tolbert LP (1989) Patterns of glial proliferation during formation of olfactory glomeruli in an insect. Glia 2:10–24

    Google Scholar 

  • Olberg RM (1983) Interneurons sensitive to female pheromone in the deutocerebrum of the male silkworm moth, Bombyx mori. Physiol Entomol 8:419–428

    Google Scholar 

  • 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

    Google Scholar 

  • Possidente DR, Murphey RK (1989) Genetic control of sexually dimorphic axon morphology in Drosophila sensory neurons. Dev Biol 132:448–457

    Google Scholar 

  • Power ME (1943) The brain of Drosophila melanogaster. J Morphol 72:517–559

    Google Scholar 

  • Power ME (1946) The antennal centers and their connections within the brain of Drosophila melanogaster. J Comp Neurol 85:485–517

    Google Scholar 

  • Rane N, Jithra L, Pinto L, Rodrigues V, Krishnan KS (1987) Monoclonal antibodies to synaptic macromolecules of Drosophila melanogaster. J Neuroimmunol 16:331–344

    Google Scholar 

  • Rodrigues V (1988) Spatial coding of olfactory information in the antennal lobe of Drosophila melanogaster. Brain Res 453:299–307

    Google Scholar 

  • Rodrigues V, Buchner E (1984) 2-Deoxyglucose mapping of odorinduced neuronal activity in the antennal lobes of Drosophila melanogaster. Brain Res 324:374–378

    Google Scholar 

  • 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

    Google Scholar 

  • Rodrigues V, Siddiqi O (1978) Genetic analysis of chemosensory pathway. Proc Indian Acad Sci 87B:147–160

    Google Scholar 

  • 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

    Google Scholar 

  • Rospars JP (1988) Structure and development of the insect antennodeutocerebral system. Int J Insect Morphol Embryol 17:243–294

    Google Scholar 

  • 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

    Google Scholar 

  • Rospars JP, Chambille I (1989) Identified glomeruli in the antennal lobes of insects: invariance, sexual variation and postembryonic development. In: Singh RN, Strausfeld NJ (eds) Neurobiology of sensory systems. Plenum, New York, pp 355–375

    Google Scholar 

  • Schaller-Selzer L (1984) Physiology and morphology of the larval sexual pheromone-sensitive neurones in the olfactory, lobe of the cockroach, Periplaneta americana. J Insect Physiol 30:537–546

    Google Scholar 

  • Schildberger K (1983) Local interneurons associated, with the mushroom bodies and the central body in the brain of Acheta domesticus. Cell Tissue Res 230:573–586

    Google Scholar 

  • Schildberger K (1984) Multimodal interneurons in the cricket brain: properties of identified extrinsic mushroom body cells. J Comp Physiol A 154:71–79

    Google Scholar 

  • Schmid H, Gendre N, Stocker RF (1986) Surgical generation of supernumerary appendages for studying neuronal specificity in Drosophila melanogaster. Dev Biol 113:160–173

    Google Scholar 

  • Selzer R (1979) Morphological and physiological identification of food odor specific neurones in the deutocerebrum of Periplaneta americana. J Comp Physiol A 134:159–163

    Google Scholar 

  • Siddiqi O (1984) Olfactory neurogenetics of Drosophila. In: Chopra VL, Joshi BC, Sharma RP, Bausal HC (eds) Genetics: new frontiers, Vol III. Oxford and IBH Publ Co., New Delhi, Bombay, Calcutta, pp 243–261

    Google Scholar 

  • Siddiqi O (1987) Neurogenetics of olfaction in Drosophila melanogaster. Trends Genet 3:137–141

    Google Scholar 

  • 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

    Google Scholar 

  • Stocker RF (1979) Fine structural comparison of the antennal nerve in the homeotic mutant Antennapedia with the wild-type antennal and second leg nerves of Drosophila melanogaster. J Morphol 160:209–222

    Google Scholar 

  • Stocker RF (1982) Genetically displaced sensory neurons in the head of Drosophila melanogaster project via different pathways into the same specific brain regions. Dev Biol 94:31–40

    Google Scholar 

  • Stocker RF, Gendre N (1988) Peripheral and central nervous effects of lozenge 3, a Drosophila mutant lacking basiconic antennal sensilla. Dev Biol 127:12–27

    Google Scholar 

  • Stocker RF, Lawrence PA (1981) Sensory projections from normal and homoeotically transformed antennae in Drosophila. Dev Biol 82:224–237

    Google Scholar 

  • Stocker RF, Schorderet M (1981) Cobalt filling of sensory projections from internal and external mouthparts in Drosophila. Cell Tissue Res 216:513–523

    Google Scholar 

  • Stocker RF, Edwards JS, Palka J, Schubiger G (1976) Projection of sensory neurons from a homeotic mutant appendage, Antennapedia, in Drosophila melanogaster. Dev Biol 52:210–220

    Google Scholar 

  • Stocker RF, Singh RN, Schorderet M, Siddiqi O (1983) Projection patterns of different types of antennal sensilla in the antennal glomeruli of Drosophila melanogaster. Cell Tissue Res 232:237–248

    Google Scholar 

  • Straufeld NJ (1976) Atlas of an insect brain. Springer, Berlin Heidelberg New York

    Google Scholar 

  • Strausfeld NJ (1980a) Male and female visual neurones in dipterous insects. Nature 283:381–383

    Google Scholar 

  • Strausfeld NJ (1980b) The Golgi method: its application to the insect nervous system and the phenomenon of stochastic impregnation. In: Strausfeld NJ, Miller TA (eds) Neuroanatomical techniques; insect nervous system. Springer, Berlin Heidelberg New York, pp 131–203

    Google Scholar 

  • Strausfeld NJ (1989a) Insect vision and olfaction: common design principles of neuronal organization. In: Singh RN, Strausfeld NJ (eds) Neurobiology of sensory systems. Plenum, New York, pp 319–353

    Google Scholar 

  • Strausfeld NJ (1989b) Cellular organization in male-specific olfactory neuropil in the moth Manduca sexta. Proc 17th Göttingen Neurobiol Conf, p 79

  • Straufeld NJ, Bacon JP (1983) Multimodal convergence in the central nervous system of dipterous insects. In: Horn E (ed) Multimodal convergences in sensory systems. G Fischer, Stuttgart, pp 47–76

    Google Scholar 

  • Strausfeld NJ, Bassemir U, Singh RN, Bacon JP (1984) Organizational principles of outputs from dipteran brains. J Insect Physiol 30:73–93

    Google Scholar 

  • Technau GM (1984) Fiber number in the mushroom bodies of adult Drosophila melanogaster depends on age, sex and experience. J Neurogenet 1:113–126

    Google Scholar 

  • Tolbert LP, Hildebrand 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

    Google Scholar 

  • Tolbert LP, Oland LA (1989) A rule for glia in the development of organized neuropilar structures. Trends Neurosci 12:70–75

    Google Scholar 

  • Tompkins L (1984) Genetic analysis of sex appeal in Drosophila. Behav Genet 14:411–440

    Google Scholar 

  • Venard R, Antony C, Jallon JM (1989) Drosophila chemoreceptors. In: Singh RN, Strausfeld NJ (eds) Neurobiology of sensory systems. Plenum, New York, pp 377–385

    Google Scholar 

  • Venkatesh S, Singh RN (1984) Sensilla on the third antennal segment of Drosophila melanogaster Meigen (Diptera: Drosophilidae). Int J Insect Morphol Embryol 13:51–63

    Google Scholar 

  • Woodard C, Huang T, Sun H, Helfand SL, Carlson JR (1989) Genetic analysis of olfactory behavior in Drosophila: a new screen yields the ota mutants. Genetics 123:315–326

    Google Scholar 

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Stocker, R.F., Lienhard, M.C., Borst, A. et al. Neuronal architecture of the antennal lobe in Drosophila melanogaster . Cell Tissue Res 262, 9–34 (1990). https://doi.org/10.1007/BF00327741

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