Skip to main content
Log in

The organization of giant horizontal-motion-sensitive neurons and their synaptic relationships in the lateral deutocerebrum of Calliphora erythrocephala and Musca domestica

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

Summary

Three giant horizontal-motion-sensitive (HS) neurons arise in the lobula plate. Their axons terminate ipsilaterally in the medial deutocerebrum and suboesophageal ganglion. Both Golgi impregnations and cobalt fills demonstrate that endings of the two HS cells, representing the upper and middle third of the retina, differ in shape and location from that of the HS cell subtending the lower third of the eye. This dichotomy is reflected by the terminals of a pair of centrifugal horizontal cells (CH), one of which invades lobula plate neuropil subtending the upper two-thirds of the retina. The other overlaps the dendrites of the HS cell subtending the lower one-third of the retina.

The HS cells are cobalt-coupled to a variety of complexly arborizing descending neurons. In Musca domestica, gap-junction-like apposition areas have been observed between HS axon collaterals and descending neuron dendrites. The three HS cells also share conventional chemical synapses with postsynaptic elements, which include the dendritic spines of descending neurons. Unlike the giant vertical-motion-sensitive neurons of the lobula plate, whose relationships with descending neurons appear to be relatively simple, the horizontal cells end on a large number of descending neurons where they comprise one of several different populations of terminals. These descending neurons terminate within various centres of the thoracic ganglia, including neuropil supplying leg, neck, and flight muscle.

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.

Institutional subscriptions

Similar content being viewed by others

References

  • Bacon JP, Altman JS (1977) A silver intensification method for cobalt-filled neurones in wholemount preparations. Brain Res 138:359–363

    Google Scholar 

  • Bassemir UK, Strausfeld NJ (1983a) Cytology of cobalt-filled neurons in flies: Cobalt deposits at presynaptic and postsynaptic sites, mitochondria and the cytoskeleton. J Neurocytol 12:949–970

    Google Scholar 

  • Bassemir UK, Strausfeld NJ (1983b) Block intensification and X-ray microanalysis of cobalt-filled neurons for electron microscopy. In: Strausfeld NJ (ed) Functional neuroanatomy. Springer, Berlin, pp 19–43

    Google Scholar 

  • Beersma DGH, Stavenga DG, Kuiper JW (1977) Retinal lattice, visual field and binocularities in flies. J Comp Physiol 119:207–220

    Google Scholar 

  • Blondeau J (1981) Electrically evoked course control in the fly Calliphora erythrocephala. J Exp Biol 92:143–153

    Google Scholar 

  • Cajal SR, Castro F de (1933) Elementos de tecnica micrografica del sistema nervioso. Tipografia Artistica, Madrid

    Google Scholar 

  • Eckert H (1978) Response properties of dipteran giant visual interneurones involved in control of optomotor behaviour. Nature 271:358–360

    Google Scholar 

  • Eckert H (1981) The horizontal cells in the lobula plate of the blowfly Phaenicia sericata. J Comp Physiol 149:195–205

    Google Scholar 

  • Eckert H (1983) The centrifugal horizontal cells in the lobula plate of the blowfly Phaenicia sericata. Insect Physiol 29:547–560

    Google Scholar 

  • Geiger G, Nässel DR (1981) Visual orientation behaviour of flies after selective laser beam ablation of interneurons. Nature 293:398–399

    Google Scholar 

  • Hausen K (1976) Functional characterization and anatomical identification of motion sensitive neurons in the lobula plate of the blowfly Calliphora erythrocephala. Z Naturforsch 31c:629–633

    Google Scholar 

  • Hausen K (1981) Monocular and binocular computation of motion in the lobula plate of the fly. Verh Dtsch Zool Ges 1981:49–70

    Google Scholar 

  • Hausen K (1982a) Motion sensitive interneurons in the optomotor system of the fly. I. The horizontal cells: Structure and signals. Biol Cybern 45:143–156

    Google Scholar 

  • Hausen K (1982b) Motion sensitive interneurons in the optomotor system of the fly. II. The horizontal cells: Receptive field organization and response characteristics. Biol Cybern 46:67–79

    Google Scholar 

  • Hausen K (1984) The lobula-complex of the fly: Structure, function and significance in visual behaviour. In: Ali MA (ed) Photoreception and vision in invertebrates. Plenum, New York, pp 523–559

    Google Scholar 

  • Hausen K, Wehrhahn C (1983) Microsurgical lesion of horizontal cells change optomotor yaw responses in the blowfly Calliphora erythrocephala. Proc R Soc Lond B219:211–216

    Google Scholar 

  • Hausen K, Wolburg-Buchholz K, Ribi WA (1980) The synaptic organization of visual interneurons in the lobula complex of flies. Cell Tissue Res 208:371–387

    Google Scholar 

  • Heisenberg M, Wonneberger R, Wolf R (1978) Optomotor-blind H31 — a Drosophila mutant of the lobula plate giant neurons. J Comp Physiol 124:287–296

    Google Scholar 

  • Hengstenberg R (1982) Common visual response properties of giant vertical cells in the lobula plate of the blowfly Calliphora. J Comp Physiol 149:179–193

    Google Scholar 

  • Pierantoni R (1976) A look into the cockpit of the fly. The architecture of the lobular plate. Cell Tissue Res 171:101–122

    Google Scholar 

  • Ribi WA (1983) Electron microscopy of Golgi-impregnated neurons. In: Strausfeld NJ (ed) Functional neuroanatomy. Springer, Berlin, pp 1–18

    Google Scholar 

  • Rowell CHF, Reichert H, Bacon JP (1985) How locusts fly straight. In: Barnes WJP, Gladden MH (eds) Feedback and motor control. Croom Helm, London

    Google Scholar 

  • Seyan HS, Bassemir UK, Strausfeld NJ (1983) Double marking for light and electron microscopy. In: Strausfeld NJ (ed) Functional neuroanatomy. Springer, Berlin, pp 112–131

    Google Scholar 

  • Simmons P (1980) A locust wind and ocellar brain neurone. J Exp Biol 85:281–294

    Google Scholar 

  • Speck PT, Strausfeld NJ (1983) Portraying the third dimension in neuroanatomy. In: Strausfeld NJ (ed) Functional neuroanatomy. Springer, Berlin, pp 156–182

    Google Scholar 

  • Strausfeld NJ (1984) Functional neuroanatomy of the blowfly's visual system. In: Ali MA (ed) Photoreception and vision in invertebrates. Plenum, New York, pp 483–522

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

  • Strausfeld NJ, Bassemir UK (1985) Lobula plate and ocellar interneurons converge onto a cluster of descending neurons leading to neck and leg neuropil in Calliphora erythrocephala. Cell Tissue Res 240:617–640

    Google Scholar 

  • Strausfeld NJ, Seyan HS (1985) Convergence of visual, haltere and prosternal inputs at neck motor neurons of Calliphora erythrocephala. Cell Tissue Res 240:601–615

    Google Scholar 

  • Strausfeld NJ, Wunderer H (1985) Optic lobe projections of marginal ommatidia in Calliphora erythrocephala specialized for detecting polarized light. Cell Tissue Res 242:163–178

    Google Scholar 

  • Tanouye MA, Wyman RJ (1980) Motor outputs of giant nerve fibres in Drosophila. J Neurophysiol 44:405–421

    Google Scholar 

  • Venable JH, Coggeshall R (1965) A simplified lead citrate stain for use in electron microscopy. J Cell Biol 25:407–408

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Strausfeld, N.J., Bassemir, U.K. The organization of giant horizontal-motion-sensitive neurons and their synaptic relationships in the lateral deutocerebrum of Calliphora erythrocephala and Musca domestica . Cell Tissue Res. 242, 531–550 (1985). https://doi.org/10.1007/BF00225419

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00225419

Key words

Navigation