Summary
-
1.
An ionic equivalent circuit model is developed for the purpose of quantifying the strengths of electrical coupling existing between certain receptor cells in the compound eye ofCataglyphis bicolor which show wavelength dependence in the slopes of their ‘V logI’ relations and orientations of maximum PS (Mote and Wehner, 1980). It combines the pure electrical equivalent of the plasma membrane, as proposed by Finkelstein and Mauro (1963), and a closed series circuit such that Kirchhoff's laws are applicable.
-
2.
The model is applied to hypothetical pairs of cells with different sensitivities and different strengths of interaction. It predicts that cells are most strongly coupled when at rest and most weakly coupled when most active. When one is active and the second is not then “apparent rectification” can occur since the coupling strength is not symmetrical. This means that both “resting” and “dynamic” coupling coefficients must be considered. Transition between these modes causes irregularities in the ‘V logI’ relation of a weakly excited cell which is coupled to a strongly excited cell.
-
3.
The model is then applied to data obtained from photoreceptors in the compound eye ofCataglyphis. It adequately simulates the wavelength dependence of both the ‘V logI’ relation (Fig. 6) and the orientation of maximum PS (Fig. 7) measured in these cells. In its simplest form the model permits an estimate of the coupling coefficients which are greater than 0.6 for strongly coupled cells and less than 0.4 for weakly coupled cells.
-
4.
A hypothetical treatment of pairs of coupled cells under conditions approaching the natural situation in the animal's environment suggests that super-numerary analyzers of polarized light in the u.v. could arise through receptor coupling in certain ommatidial types found in the eye ofCataglyphis.
Similar content being viewed by others
Abbreviations
- UV, VIS, UV-VIS :
-
designations of receptor classes defined previously
- PS :
-
polarization sensitivity
- u.v. :
-
ultraviolet
- V log I :
-
response vs intensity function
References
Behrens, M.E., Wulff, V.J.: Light initiated responses of retinula and eccentric cells in theLimulus lateral eye. J. Gen. Physiol.48, 1081–1093 (1965)
Bennett, M.V.L.: Physiology of electrotonic junctions. Ann. N.Y. Acad. Sci.137, 509–539 (1966)
Butler, R., Horridge, G.A.: The electrophysiology of the retina ofPeriplaneta L. 1. Changes in receptor sensitivity upon light/dark adaptation. J. Comp. Physiol.83, 263–278 (1973)
Chi, C., Carlson, S.D.: Close apposition of photoreceptor cell axons in the housefly. J. Insect. Physiol.22, 1153–1157 (1976)
Duelli, P.: A fovea for e-vector orientation in the eye ofCataglyphis bicolor. J. Comp. Physiol.102, 43–56 (1975)
Duelli, P., Wehner, R.: The spectral sensitivity of polarized light orientation inCataglyphis bicolor. (Formicidae, Hymenoptera). J. Comp. Physiol.86, 37–53 (1973)
Fain, G.L.: Quantum sensitivity of rods in the toad retina. Science187, 838–841 (1975)
Finkelstein, A., Mauro, A.: Equivalent circuits as related to ionic systems. Biophys. J.3, 215–237 (1963)
Helversen, O. von, Edrich, W.: Der Polarisationsempfänger im Bienenauge: ein Ultraviolettrezeptor. J. Comp. Physiol.94, 33–47 (1974)
Herrling, P.L.: Regional distribution of three ultrastructural retinula types in the retina ofCataglyphis bicolor Fabr. (Formicidae, Hymenoptera). Cell Tissue Res.169, 247–266 (1976)
Kirschfeld, K.: Die notwendige Anzahl von Rezeptoren zur Bestimmung der Richtung des elektrischen Vektors linear polarisation Lichtes. Z. Naturforsch.27b, 578–579 (1972)
Laughlin, S.B.: Receptor function in the apposition eye — an electrophysiological approach. In: Photoreceptor optics. Snyder, A.W., Menzel, R. (eds.), pp. 479–498. Berlin, Heidelberg, New York: Springer 1975
Lillywhite, P.G.: Coupling between locust photoreceptors revealed by a study of quantum bumps. J. Comp. Physiol.125, 13–27 (1978)
Menzel, R., Blakers, M.: Colour receptors in the bee eye. Morphology and spectral sensitivity. J. Comp. Physiol.108, 11–33 (1976)
Meyer, E.P.: Golgi-EM-study of the first and second order neurons in the visual system ofCataglyphis bicolor Fabricius (Hymenoptera, Formicidae). Zoomorphologie92, 115–139 (1979)
Mimura, K.: Electrophysiological evidence for interaction between retinula cells in the flesh fly. J. Comp. Physiol.125, 209–216 (1978)
Mote, M.I., Goldsmith, T.H.: Spectral sensitivities of color receptors in the compound eye of the cockroachPeriplaneta. J. Exp. Zool.173, 137–146 (1970)
Mote, M.I., Wehner, R.: Functional properties of photoreceptors in the compound eye and ocellus of the Desert Ant,Cataglyphis bicolor. J. Comp. Physiol.137, 63–71 (1980)
Muller, K.: Photoreceptors in the crayfish compound eye: electrical interactions between cells as related to polarized light sensitivity. J. Physiol. (London)232, 573–595 (1973)
Ribi, W.A.: Gap junctions coupling photoreceptor axons in the first optic ganglion of the fly. Cell Tissue Res.195, 299–308 (1978)
Ribi, W.A.: Do the rhabdomeric structures in bees and flies really twist? J. Comp. Physiol.134, 109–112 (1979)
Shaw, S.R.: Interreceptor coupling in ommatidia of drone honeybee and locust compound eyes. Vision Res.9, 999–1029 (1969)
Tsukahara, T., Horridge, G.A.: Interaction between two retinula cell types in the anterior eye of the droneflyEristalis. J. Comp. Physiol.115, 287–298 (1977)
Wehner, R.: Space constancy of the visual world of insects. Fortschr. Zool.23, 148–160 (1975)
Wehner, R., Bernard, G., Geiger, E.: Twisted and non-twisted rhabdoms and their significance for polarization detection in bees. J. Comp. Physiol.164, 225–245 (1975)
Author information
Authors and Affiliations
Additional information
The experiments were performed while MIM was a guest of Professor R. Wehner at the Zoological Institute of the University of Zürich and on a study leave granted by Temple University. MIM was supported by Grant 3.529-0.75 from the Swiss National Science Foundation to Prof. Wehner, by a fellowship from the Roch Research Foundation (Basel), and by NIH Grant EY-00784 from the National Eye Institute, USA.
Rights and permissions
About this article
Cite this article
Martin, F.G., Mote, M.I. An equivalent circuit for the quantitative description of inter-receptor coupling in the retina of the desert antCataglyphis bicolor . J. Comp. Physiol. 139, 277–285 (1980). https://doi.org/10.1007/BF00610459
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00610459