Skip to main content
Log in

Electrical coupling of neuro-ommatidial photoreceptor cells in the blowfly

  • Published:
Journal of Comparative Physiology A Aims and scope Submit manuscript

Summary

A new method of microstimulation of the blowfly eye using corneal neutralization was applied to the 6 peripheral photoreceptor cells (R1–R6) connected to one neuro-ommatidium (and thus looking into the same direction), whilst the receptor potential of a dark-adapted photoreceptor cell was recorded by means of an intracellular microelectrode. Stimulation of the photoreceptor cells not impaled elicited responses in the recorded cell of about 20% of the response elicited when stimulating the recorded cell. This is probably caused by gap junctions recently found between the axon terminals of these cells. Stimulation of all 6 cells together yielded responses that were larger and longer than those obtained with stimulation of just the recorded cell, and intensity-response curves that deviated more strongly from linearity. Evidence is presented that the resistance of the axon terminal of the photoreceptor cells quickly drops in response to a light flash, depending on the light intensity. Incorporating the cable properties of the cell body and the axon, the resistance of the gap junctions, and the (adapting) terminal resistance, a theoretical model is presented that explains the measurements well. Finally, it is argued that the gap junctions between the photoreceptor cells may effectively uncouple the synaptic responses of the cells by counteracting the influence of field potentials.

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

  • Attwell D, Wilson M, Wu SM (1984) A quantitative analysis of interactions between photoreceptors in the salamander (Ambystoma) retina. J Physiol 352:703–737

    Google Scholar 

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

    Google Scholar 

  • Detwiler PB, Hodgkin AL, McNaughton PA (1978) A surprising property of electrical spread in the network of rods in the turtle's retina. Nature 274:562–565

    Google Scholar 

  • Dubs A (1981) Non-linearity and light adaptation in the fly photoreceptor. J Comp Physiol 144:53–59

    Google Scholar 

  • Dubs A, Laughlin SB, Srinivasan MV (1981) Single photon signals in fly photoreceptors and first order interneurons at behavioural threshold. J Physiol 317:317–334

    Google Scholar 

  • Franceschini N (1975) Sampling of the visual environment by the compound eye of the fly: Fundamentals and appli cations. In: Snyder AW, Menzel R (eds) Photoreceptor Optics. Springer, Berlin Heidelberg New York, pp 98–125

    Google Scholar 

  • French AS, Kuster JE (1985) Nonlinearities in locust photoreceptors during transduction of small numbers of photons. J Comp Physiol A 156:645–652

    Google Scholar 

  • Hardie RC, Franceschini N, Ribi W, Kirschfeld K (1981) Distribution and properties of sex-specific photoreceptors in the flyMusca domestica. J Comp Physiol 145:139–152

    Google Scholar 

  • Hardie RC (1984) Functional organization of the fly retina. In: Ottoson D (ed) Progr sensory physiol, vol 5. Springer, Berlin Heidelberg New York Tokyo, pp 1–79

    Google Scholar 

  • Hateren JH van (1984) Waveguide theory applied to optically measured angular sensitivities of fly photoreceptors. J Comp Physiol A 154:761–771

    Google Scholar 

  • Hateren JH van (1985) The Stiles-Crawford effect in the eye of the blowfly,Calliphora erythrocephala. Vision Res 25:1305–1315

    Google Scholar 

  • Hateren JH van (1986) An efficient algorithm for cable theory, applied to blowfly photoreceptor cells and LMC's. Biol Cybern (in press)

  • Hirosawa K, Hotta Y (1982) Morphological analysis of photoreceptor membranes in mutantDrosophila eyes. In: Hollyfield JG (ed) The structure of the eye. Elsevier North Holland, Amsterdam, pp 45–53

    Google Scholar 

  • Jack JJB, Noble D, Tsien RW (1975) Electric current flow in excitable cells. Clarendon Press, Oxford

    Google Scholar 

  • Kirschfeld K, Franceschini N (1968) Optische Eigenschaften der Ommatidien im Komplexauge vonMusca. Kybernetik 5:47–52

    Google Scholar 

  • Koch C (1984) Cable theory in neurons with active, linearized membranes. Biol Cybern 50:15–33

    Google Scholar 

  • Koch C, Poggio T (1985) A simple algorithm for solving the cable equation in dendritic trees of arbitrary geometry. J Neurosci Meth 12:303–315

    Google Scholar 

  • Laughlin SB, Lillywhite PG (1982) Intrinsic noise in locust photoreceptors. J Physiol 332:25–45

    Google Scholar 

  • Loewenstein WR (1975) Permeable junctions. In: Cold Spring Harbour Symp Quant Biol XL:49–63

  • Matic T, Laughlin SB (1981) Changes in the intensity-response function of an insect's photoreceptor due to light adaptation. J Comp Physiol 145:169–177

    Google Scholar 

  • Muijser H (1979) A micro-electrode amplifier with an infinite resistance current source for intracellular measurements of membrane potential and resistance changes under current clamp. Experientia 35:912–913

    Google Scholar 

  • Pick B (1977) Specific misalignments of rhabdomere visual axes in the neural superposition eye of dipteran flies. Biol Cybern 26:215–224

    Google Scholar 

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

    Google Scholar 

  • Scholes J (1969) The electrical responses of the retinal receptors and the lamina in the visual system of the flyMusca. Kybernetik 6:149–162

    Google Scholar 

  • Shaw SR (1975) Retinal resistance barriers and electrical lateral inhibition. Nature 255:480–483

    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) Neurons without impulses. Cambridge University Press, Cambridge, pp 61–116

    Google Scholar 

  • Shaw SR (1984a) Asymmetric distribution of gap junctions amongst identified photoreceptor axons ofLucilia cuprina (Diptera). J Cell Sci 66:65–80

    Google Scholar 

  • Shaw SR (1984b) Early visual processing in insects. J Exp Biol 112:225–251

    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 

  • Smakman JGJ, Hateren JH van, Stavenga DG (1984) Angular sensitivity of blowfly photoreceptors: intracellular measurements and wave-optical predictions. J Comp Physiol A 155:239–247

    Google Scholar 

  • Smakman JGJ (1985) Angular and spectral sensitivity of blowfly photoreceptors. Thesis, Groningen University

  • Torre V, Owen WG (1983) High-pass filtering of small signals by the rod network in the retina of the toad,Bufo marinus. Biophys J 41:305–324

    Google Scholar 

  • Wunderer H, Smola U (1982) Morphological differentiation of the central visual cells R7/8 in various regions of the blowfly eye. Tissue Cell 14:341–358

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

van Hateren, J.H. Electrical coupling of neuro-ommatidial photoreceptor cells in the blowfly. J. Comp. Physiol. 158, 795–811 (1986). https://doi.org/10.1007/BF01324822

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF01324822

Keywords

Navigation