Advertisement

Cell and Tissue Research

, Volume 262, Issue 1, pp 9–34 | Cite as

Neuronal architecture of the antennal lobe in Drosophila melanogaster

  • R. F. Stocker
  • M. C. Lienhard
  • A. Borst
  • K. F. Fischbach
Article

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.

Key words

Antennal lobes Antennal glomeruli Antennal afferents Maxillary afferents Antennal interneurons Computer reconstruction Golgi impregnation Backfilling Drosophila melanogaster (Insecta) 

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

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. 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 97–130Google Scholar
  2. 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 132:235–242Google Scholar
  3. Boeckh J, Sandri C, Akert K (1970) Sensorische Eingänge und synaptische Verbindungen in Zentralnervensystem von Insekten. Z Zellforsch 103:429–446Google Scholar
  4. 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 30:15–26Google Scholar
  5. 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 HeidelbergGoogle Scholar
  6. 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 158:741–749Google Scholar
  7. Borst A (1983) Computation of olfactory signals in Drosophila melanogaster. J Comp Physiol A 152:373–383Google Scholar
  8. Borst A, Fischbach KF (1987) Golgi-and degeneration studies of the antennal lobes of Drosophila melanogaster. J Neurogenet 4:115–117Google Scholar
  9. Borst A, Heisenberg M (1982) Osmotropotaxis in Drosophila melanogaster. J Comp Physiol A 147:479–484Google Scholar
  10. 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 253:357–370Google Scholar
  11. 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 145:447–457Google Scholar
  12. 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 10:141–165Google Scholar
  13. Chapman RF (1982) Chemoreception. The significance of receptor numbers. Adv Insect Physiol 16:247–356Google Scholar
  14. 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 457–484Google Scholar
  15. Colonnier M (1964) The tangential organization of the visual cortex. J Anat 98:327–344Google Scholar
  16. Distler P (1989) Histochemical demonstration of GABA-like immunoreactivity in cobalt labeled neuron individuals in the insect olfactory pathway. Histochemistry 91:245–249Google Scholar
  17. 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 229:1–22Google Scholar
  18. 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 176:285–308Google Scholar
  19. Fischbach KF, Dittrich APM (1989) The optic lobe of Drosophila melanogaster. I. A Golgi analysis of wild-type structure. Cell Tissue Res 258:441–475Google Scholar
  20. Fischbach KF, Götz CR (1981) Das Experiment. Ein Blick ins Fliegengehirn-Golgi gefärbte Nervenzellen bei Drosophila. BIUZ 11:183–187Google Scholar
  21. Fischbach KF, Heisenberg M (1984) Neurogenetics and behaviour in insects. J Exp Biol 112:65–93Google Scholar
  22. 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: 277–287Google Scholar
  23. Ghysen A, O'Kane CJ (1989) Neural enhancer-like elements as specific cell markers in Drosophila. Development 105:35–52Google Scholar
  24. Hanesch U, Fischbach KF, Heisenberg M (1989) Neuronal architecture of the central complex in Drosophila melanogaster. Cell Tissue Res 257: 343–366Google Scholar
  25. Hardie RC (1983) Projection and connectivity of sex-specific photoreceptors in the compound eye of the male housefly (Musca domestica). Cell Tissue Res 233:1–21Google Scholar
  26. Heisenberg M, Borst A, Wagner S, Byers D (1985) Drosophila mushroom body mutants are deficient in olfactory learning. J Neurogenet 2:1–30Google Scholar
  27. Helfand SL, Carlson JR (1989) Isolation and characterization of an olfactory mutant in Drosophila with a chemically specific defect. Proc Natl Acad Sci USA 86:2908–2912Google Scholar
  28. Homberg U (1984) Processing of antennal information in extrinsic mushroom body neurons of the bee brain. J Comp Physiol A 154:825–836Google Scholar
  29. Homberg U, Montague RA, Hildebrand JG (1988) Anatomy of antenno-cerebral pathways in the brain of the sphinx moth Manduca sexta. Cell Tissue Res 254:255–281Google Scholar
  30. Homberg U, Christensen TA, Hildebrand JG (1989) Structure and function of the deutocerebrum in insects. Annu Rev Entomol 34:477–501Google Scholar
  31. 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 244:243–252Google Scholar
  32. 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 165:427–453Google Scholar
  33. 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 245:237–245Google Scholar
  34. 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 18:451–465Google Scholar
  35. 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 249:39–50Google Scholar
  36. Koto M, Tanouye MA, Ferrus A, Thomas JB, Wyman RJ (1981) The morphology of the cervical giant fiber neuron of Drosophila. Brain Res 221:213–217Google Scholar
  37. 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 62Google Scholar
  38. 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 15:439–488Google Scholar
  39. 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 240:333–342Google Scholar
  40. Lienhard MC, Stocker RF (1987) Sensory projection patterns of supernumerary legs and aristae in D. melanogaster. J Exp Zool 244:187–201Google Scholar
  41. 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 287–301Google Scholar
  42. 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] 213:249–277Google Scholar
  43. 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 86:8118–8122Google Scholar
  44. 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 420–534Google Scholar
  45. 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] 298:309–354Google Scholar
  46. Nässel DR (1987) Neuroactive substances in the insect CNS. In: Ali MA (ed) Nervous systems in invertebrates. Plenum, New York, pp 171–212Google Scholar
  47. 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 180:159–169Google Scholar
  48. Nayak SV, Singh RN (1983) Sensilla on the tarsal segments and mouthparts of adult Drosophila melanogaster Meigen (Diptera: Drosophilidae). Int J Insect Morphol Embryol 12:273–291Google Scholar
  49. 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 14:115–129Google Scholar
  50. 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 255:196–207Google Scholar
  51. Oland LA, Tolbert LP (1989) Patterns of glial proliferation during formation of olfactory glomeruli in an insect. Glia 2:10–24Google Scholar
  52. Olberg RM (1983) Interneurons sensitive to female pheromone in the deutocerebrum of the male silkworm moth, Bombyx mori. Physiol Entomol 8:419–428Google Scholar
  53. 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 17:335–344Google Scholar
  54. Possidente DR, Murphey RK (1989) Genetic control of sexually dimorphic axon morphology in Drosophila sensory neurons. Dev Biol 132:448–457Google Scholar
  55. Power ME (1943) The brain of Drosophila melanogaster. J Morphol 72:517–559Google Scholar
  56. Power ME (1946) The antennal centers and their connections within the brain of Drosophila melanogaster. J Comp Neurol 85:485–517Google Scholar
  57. Rane N, Jithra L, Pinto L, Rodrigues V, Krishnan KS (1987) Monoclonal antibodies to synaptic macromolecules of Drosophila melanogaster. J Neuroimmunol 16:331–344Google Scholar
  58. Rodrigues V (1988) Spatial coding of olfactory information in the antennal lobe of Drosophila melanogaster. Brain Res 453:299–307Google Scholar
  59. Rodrigues V, Buchner E (1984) 2-Deoxyglucose mapping of odorinduced neuronal activity in the antennal lobes of Drosophila melanogaster. Brain Res 324:374–378Google Scholar
  60. 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 387–396Google Scholar
  61. Rodrigues V, Siddiqi O (1978) Genetic analysis of chemosensory pathway. Proc Indian Acad Sci 87B:147–160Google Scholar
  62. 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 220:80–96Google Scholar
  63. Rospars JP (1988) Structure and development of the insect antennodeutocerebral system. Int J Insect Morphol Embryol 17:243–294Google Scholar
  64. Rospars JP, Chambille I (1981) Deutocerebrum of the cockroach Blaberus craniifer Burm. Quantitative study and automated identification of the glomeruli. J Neurobiol 12:221–247Google Scholar
  65. 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 355–375Google Scholar
  66. 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 30:537–546Google Scholar
  67. Schildberger K (1983) Local interneurons associated, with the mushroom bodies and the central body in the brain of Acheta domesticus. Cell Tissue Res 230:573–586Google Scholar
  68. Schildberger K (1984) Multimodal interneurons in the cricket brain: properties of identified extrinsic mushroom body cells. J Comp Physiol A 154:71–79Google Scholar
  69. Schmid H, Gendre N, Stocker RF (1986) Surgical generation of supernumerary appendages for studying neuronal specificity in Drosophila melanogaster. Dev Biol 113:160–173Google Scholar
  70. Selzer R (1979) Morphological and physiological identification of food odor specific neurones in the deutocerebrum of Periplaneta americana. J Comp Physiol A 134:159–163Google Scholar
  71. 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 243–261Google Scholar
  72. Siddiqi O (1987) Neurogenetics of olfaction in Drosophila melanogaster. Trends Genet 3:137–141Google Scholar
  73. 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 14:291–306Google Scholar
  74. 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 160:209–222Google Scholar
  75. 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 94:31–40Google Scholar
  76. Stocker RF, Gendre N (1988) Peripheral and central nervous effects of lozenge 3, a Drosophila mutant lacking basiconic antennal sensilla. Dev Biol 127:12–27Google Scholar
  77. Stocker RF, Lawrence PA (1981) Sensory projections from normal and homoeotically transformed antennae in Drosophila. Dev Biol 82:224–237Google Scholar
  78. Stocker RF, Schorderet M (1981) Cobalt filling of sensory projections from internal and external mouthparts in Drosophila. Cell Tissue Res 216:513–523Google Scholar
  79. Stocker RF, Edwards JS, Palka J, Schubiger G (1976) Projection of sensory neurons from a homeotic mutant appendage, Antennapedia, in Drosophila melanogaster. Dev Biol 52:210–220Google Scholar
  80. 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 232:237–248Google Scholar
  81. Straufeld NJ (1976) Atlas of an insect brain. Springer, Berlin Heidelberg New YorkGoogle Scholar
  82. Strausfeld NJ (1980a) Male and female visual neurones in dipterous insects. Nature 283:381–383Google Scholar
  83. 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 131–203Google Scholar
  84. 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 319–353Google Scholar
  85. Strausfeld NJ (1989b) Cellular organization in male-specific olfactory neuropil in the moth Manduca sexta. Proc 17th Göttingen Neurobiol Conf, p 79Google Scholar
  86. 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 47–76Google Scholar
  87. Strausfeld NJ, Bassemir U, Singh RN, Bacon JP (1984) Organizational principles of outputs from dipteran brains. J Insect Physiol 30:73–93Google Scholar
  88. Technau GM (1984) Fiber number in the mushroom bodies of adult Drosophila melanogaster depends on age, sex and experience. J Neurogenet 1:113–126Google Scholar
  89. 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] 213:279–301Google Scholar
  90. Tolbert LP, Oland LA (1989) A rule for glia in the development of organized neuropilar structures. Trends Neurosci 12:70–75Google Scholar
  91. Tompkins L (1984) Genetic analysis of sex appeal in Drosophila. Behav Genet 14:411–440Google Scholar
  92. Venard R, Antony C, Jallon JM (1989) Drosophila chemoreceptors. In: Singh RN, Strausfeld NJ (eds) Neurobiology of sensory systems. Plenum, New York, pp 377–385Google Scholar
  93. Venkatesh S, Singh RN (1984) Sensilla on the third antennal segment of Drosophila melanogaster Meigen (Diptera: Drosophilidae). Int J Insect Morphol Embryol 13:51–63Google Scholar
  94. 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 123:315–326Google Scholar

Copyright information

© Springer-Verlag 1990

Authors and Affiliations

  • R. F. Stocker
    • 1
  • M. C. Lienhard
    • 1
  • A. Borst
    • 2
  • K. F. Fischbach
    • 3
  1. 1.Institut de ZoologieUniversité de FribourgFribourgSwitzerland
  2. 2.Max-Planck-Institut für Biologische KybernetikTübingenFederal Republic of Germany
  3. 3.Institut für Biologie IIIAlbert-Ludwigs-UniversitätFreiburg i. Br.Federal Republic of Germany

Personalised recommendations