Skip to main content
Log in

Interneuronal and glial-neuronal gap junctions in the lamina ganglionaris of the compound eye of the housefly, Musca domestics

  • Published:
Cell and Tissue Research Aims and scope Submit manuscript

Summary

The cell-body layer of the lamina ganglionaris of the housefly, Musca domestica, contains the perikarya of five types of monopolar interneuron (L1–L5) along with their enveloping neuroglia (Strausfeld 1971). We confirm previous reports (Trujillo-Cenóz 1965; Boschek 1971) that monopolar cell bodies in the lamina form three structural classes: Class I, Class II, and midget monopolar cells. Class-I cells (L1 and L2) have large (8–15 μm) often crescentshaped cell bodies, much perinuclear cytoplasm and deep glial invaginations. Class-II cells (L3 and L4) have smaller perikarya (4–8 μm) with little perinuclear cytoplasm and no glial invaginations. The ‘midget’ monopolar cell (L5) resides at the base of the cell-body layer and has a cubshaped cell body. Though embedded within a reticulum of satellite glia, the L1–L4 monopolar perikarya and their immediately proximal neurites frequently appose each other directly. Typical arthropod (β-type) gap junctions are routinely observed at these interfaces. These junctions can span up to 0.8 μm with an intercellular space of 2–4 nm. The surrounding nonspecialized interspace is 12–20 nm. Freezefracture replicas of monopolar appositions confirm the presence of β-type gap junctions, i.e., circular plaques (0.15–0.7 μm diam.) of large (10–15 nm) E-face particles. Gap junctions are present between Class I somata and their proximal neurites, between Class I and Class II somata and proximal neurites, and between Class II somata. Intercartridge coupling may exist between such monopolar somata. The cell body and proximal neurite of L5 were not examined. We also find that Class I and Class II somata are extensively linked to their satellite glia via gap junctions. The gap width and nonjunctional interspace between neuron and glia are the same as those found between neurons. The particular arrangement and morphology of lamina monopolar neurons suggest that coupling or low resistance pathways between functionally distinct neurons and between neuron and glia are probably related to the metabolic requirements of the “nuclear” layer and may play a role in wide field signal averaging and light adaptation.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Bennett MVL (1978) Junctional permeability. In: Gilula NB Pitts JD (eds) Receptors and recognition, Ser B. Chapman & Hall, London pp 23–26

    Google Scholar 

  • Bennett MVL, Goodenough DA (1978) Gap junctions, electrotonic coupling and intercellular communication. Neurosci Res Progr Bull 16(8):373–486

    Google Scholar 

  • Boschek CB (1971) On the fine structure of the peripheral retina and lamina ganglionaris of the fly, Musca domestica. Z Zellforsch 118:369–409

    Google Scholar 

  • Braitenberg V (1967) Patterns of projection in the visual system of the fly. 1. Retina-lamina projections. Exp Brain Res 3:271–298

    Google Scholar 

  • Brightman MW, Reese TS (1969) Junctions between intimately apposed cell membranes in the vertebrate brain. J Cell Biol 40:648–677

    Google Scholar 

  • Carlson SD, Saint Marie RL, Chi C (1983) Interpretation of freeze fracture replicas of insect nervous tissue. In: Strausfeld, NJ (ed) Functional neuroanatomy Springer, Berlin pp 339–375

    Google Scholar 

  • Carlson SD, Saint Marie RL, Chi C (1984) The photoreceptor cells. In: King RC, Akai H (eds) Insect ultrastructure Vol. II, Plenum Press, New York pp 397–433

    Google Scholar 

  • Chi C, Carlson SD (1976) Close apposition of photoreceptor cell axons in the housefly. J Insect Phys 22:1153–1157

    Google Scholar 

  • Chi C, Carlson SD (1980a) Membrane specializations in the first optic neuropil of the housefly, Musca domestica L. I. Junctions between neurons. J. Neurocytol 9:429–449

    Google Scholar 

  • Chi C, Carlson SD (1980b) Membrane specializations in the first optic neuropil of the housefly, Musca domestica L. II. Junctions between glial cells. J Neurocytol 9:451–469

    Google Scholar 

  • Chi C, Carlson SD (1981) The perineurium of the adult housefly: ultrastructure and permeability to lanthanum. Cell Tissue Res 217:373–386

    Google Scholar 

  • Järvilehto M, Zettler F (1971) Localized intracellular potentials from pre- and postsynaptic components in the external plexiform layer of an insect retina. Z vergl Physiol 75:422–440

    Google Scholar 

  • Järvilehto M, Zettler F (1973) Electrophysiological-histological studies on some functional properties of visual cells and secondorder neurons of an insect retina. Z Zellforsch 136:291–306

    Google Scholar 

  • Landolt AM, Ris H (1966) Electron microscope studies on somasomatic interneuronal junctions in the corpus pedunculatum of the wood ant (Formica lugubris Zett). J Cell Biol 28:391–403

    Google Scholar 

  • Lane NJ (1978) Intercellular junctions and cell contacts in invertebrates. In: Sturgess JM (ed) Proceedings of the Ninth International Congress on Electron Microscopy, Toronto Vol. 3. Microscopical Society of Canada, Toronto, pp 673–691

    Google Scholar 

  • Lane NJ (1981) Vertebrate-like tight junctions in the insect eye. Exp Cell Res 132:482–488

    Google Scholar 

  • Lane NJ, Skaer HleB (1980) Intercellular junctions in insect tissues. In: Berridge MJ, Treherne JE, Wigglesworth VB (ed) Advances in insect physiology Vol. 15. Academic Press London pp 35–213

    Google Scholar 

  • Laughlin S (1981) Neural principles in the peripheral visual systems of invertebrates In: Autrum H (ed) Handbook of sensory physiology, vol. VII/6B. Springer, Berlin Heidelberg New York, pp 133–280

    Google Scholar 

  • Ribi W (1978) Gap junctions coupling photoreceptor axons in the first optic ganglion of the fly. Cell Tissue Res 195:299–308

    Google Scholar 

  • Saint Marie RL (1981) A thin-section and freeze-fracture study of intercellular junctions and synaptic vesicle activity in the first optic neuropil of the housefly compound eye. Doctoral Thesis, University of Wisconsin-Madison

  • Saint Marie RL, Carlson SD (1983a) The fine structure of neuroglia in the lamina ganglionaris of the housefly, Musca domestica L. J Neurocytol 12:23–241

    Google Scholar 

  • Saint Marie RL, Carlson SD (1983b) Glial membrane specializations and the compartmentalization of the lamina ganglionaris of the housefly compound eye. J Neurocytol 12:243–275

    Google Scholar 

  • Saint Marie RL, Carlson SD, Chi C (1984) Glial cells. In: King RC, Akai H (eds) Insect ultrastructure, vol. II Plenum Press New York pp 435–475

    Google Scholar 

  • Shaw SR (1981) Anatomy and physiology of identified non-spiking cells in the photoreceptor-lamina complex of the compound eye of insects, especially Diptera. In: Roberts A, Bush BMH (eds) Neurones without impulses Cambridge University Press, Cambridge pp 61–116

    Google Scholar 

  • Shaw SR, Stowe S (1982) Freeze-fracture evidence for gap junctions connecting the axon terminals of dipteran photoreceptors. J Cell Sci 53:115–141

    Google Scholar 

  • Strausfeld NJ (1971) The organization of the insect visual system (light microscopy). I. Projections and arrangements of neurons in the lamina ganglionaris of Diptera. Z Zellforsch 121:377–441

    Google Scholar 

  • Strausfeld NJ, Bassemir V (1983) Cobalt-coupled neurons of a giant fibre system in Diptera. J Neurocytol 12:971–991

    Google Scholar 

  • Trujillo-Cenóz O (1965) Some aspects of the structural organization of the intermediate retina of dipterous. J Ultrastruct Res 13:1–33

    Google Scholar 

  • Zettler F, Järvilehto M (1971) Decrement-free conduction of graded potentials along the axon of a monopolar neuron. Z vergl Physiol 75:402–421

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Saint Marie, R.L., Carlson, S.D. Interneuronal and glial-neuronal gap junctions in the lamina ganglionaris of the compound eye of the housefly, Musca domestics . Cell Tissue Res. 241, 43–52 (1985). https://doi.org/10.1007/BF00214624

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00214624

Key words

Navigation