Summary
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1.
Colour coding in the retina of the honey bee,Apis mellifera, is examined by single unit recording and intracellular marking with the fluorescence dye Procion yellow.
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2.
The three receptor types (UV, blue, green receptors) are dominated by three rhodopsin — like pigments with absorbance maxima at 350 nm, 440 nm and 540 nm. This is in general agreement with the first discription of the bee's colour receptors by Autrum and v. Zwehl, 1964.
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3.
The UV-receptors were found to be those cells which form the long visual fibres. These penetrate the lamina with differing patterns of short arborisations and spines and project to the 1. or more often to the 2. medullary layer.
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4.
Most green receptors we have marked from the deep lamina axons which reach the internal (most proximal) lamina layer and end in several branches. The shallow lamina fibres come from blue or from green receptors.
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The majority of cells have secondary sensitivities at wavelength regions where the other receptor types absorb maximally. We show with spectral adaptation experiments that this linkage is caused by a positive electrical coupling. We give arguments which exclude the artificial nature of the electrical coupling.
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6.
There is also evidence for negative electrical coupling between different colour receptors. We have recorded from several UV-receptors, which responded with a hyperpolarising potential to long wavelength stimulation. The narrower spectral sensitivity functions when compared with Dartnall resonance functions found in a smaller number of receptors are interpreted to reflect, too, negative electrical interactions between different colour receptors.
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7.
We propose a model of electrical interactions of densely packed colour receptors which postulates negative electrical coupling occurring within the retina and positive electrical coupling through the lamina cartridge. Further-more, we discuss our results on the basis of colour integration mechanisms within the lamina.
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References
Autrum, H., Zwehl, V.: Spektrale Empfindlichkeit einzelner Sehzellen des Bienenauges. Z. vergl. Physiol.48, 357–384 (1964)
Bertholf, L.M.: The distribution of stimulative efficiency in the ultraviolet spectrum for the honeybee. J. agr. Res.43, 703–713 (1931)
Cajal, S.R., Sanchez, D.: Contribucion al conocimiento de los centros nerviosos de los insectos. Trab. Lab. Invest. Biol. Univ. Madrid13, 1–168 (1915)
Dartnall, H.J.A.: The interpretation of spectral sensitivity curves. Brit. med. Bull.9, 24–30 (1952)
Daumer, K.: Reizmetrische Untersuchung des Farbensehens der Biene. Z. vergl. Physiol.38, 413–478 (1956)
Frisch, K. von: Der Farbensinn und Formensinn der Biene. Zool. Jb. Physiol.37, 1–238 (1914)
Gribakin, F.G.: Cellular basis of colour vision in the honey bee. Nature (Lond.)223, 639–641 (1969)
Gribakin, F.G.: The distribution of the long wave photoreceptors in the compound eye of the honeybee as revealed by selective osmic staining. Vision Res.12, 1225–1230 (1972)
Grundler, O.J.: Elektronenmikroskopische Untersuchungen am Auge der Honigbiene (Apis mellifica) I. Untersuchungen zur Morphologie und Anordnung der neun Retinulazellen in Ommatidien verschiedener Augenbereiche und zur Perzeption linear polarisierten Lichtes. Cytobiol.9, 203–220 (1974)
Hamdorf, K.: Primärprozesse beim Sehen der Wirbellosen. Rhein. Westf. Akad. Wiss. N 253, 1–42 (1975)
Hamdorf, K., Höglund, G., Langer, H.: Mikrophotometrische Untersuchungen an der Retinula des NachtschmetterlingsDeilephila elpenor. Verh. dtsch. zool. Ges.65, 276–280 (1972)
Hamdorf, K., Schwemer, J.: Photoregeneration and the adaptation in insect photoreceptors. In: Photoreceptor optics (eds. A.W. Snyder, R. Menzel), pp. 263–289. Berlin-Heidelberg-New York: Springer 1975
Helversen, O. von: Zur spektralen Unterschiedsempfindlichkeit der Honigbiene. J. comp. Physiol.80, 439–472 (1972)
Kaiser, W.: A preliminary report of the analysis of the optomotor system of the honey bee — single unit recordings during stimulation with spectral lights. In: Information processing in the visual systems of arthropods (ed. R. Wehner), pp. 166–170. Berlin-Heidelberg-New York: Springer 1972
Kaiser, W., Liske, E.: Die optomotorische Reaktion von fixiert fliegenden Bienen bei Reizung mit Spektrallicht. J. comp. Physiol.89, 391–408 (1974)
Labhart, T.: Behavioural analysis of light intensity discrimination and spectral sensitivity in the honey bee,Apis mellifera. J. comp. Physiol.95, 203–216 (1974)
Laughlin, S.B.: Neural integration in the first optic neuropile of dragonflies. II. The receptor signal in the lamina. J. comp. Physiol.92, 357–375 (1974)
Laughlin, S.B.: Receptor and interneuron light-adaptation in the dragonfly visual system. Z. Naturforsch.30c, 306–308 (1975)
Laughlin, S.B.: Neural integration in the first optic neuropile of the drangonflies. IV. Colour coding and polarized light sensitivity. (In press)
Menzel, R.: Feinstruktur des Komplexauges der Roten Waldameise,Formica polyctena (Hymenoptera, Formicidae). Z. Zellforsch.127, 356–373 (1972a)
Menzel, R.: Spectral response of moving detecting and “sustaining” fibres in the optic lobe of the bee. J. comp. Physiol.82, 135–150 (1973)
Menzel, R.: Spectral sensitivity of monopolar cells in the bee lamina. J. comp. Physiol.93, 337–346 (1974)
Menzel, R.: Insect colour receptors. In: The compound eye and vision of insects (ed. G.A. Horridge), pp. 121–153. Oxford: Oxford University Press 1975
Menzel, R., Blakers, M.: Functional organisation of an insect ommatidium with fused rhabdom. Cytobiol.11, 279–298 (1975)
Menzel, R., Snyder, A.W.: Polarized light detection in the bee,Apis mellifera. J. comp. Physiol.88, 247–270 (1974)
Perrelet, A.: The fine structure of the retina of the honey bee drone. An electron microscopical study. Z. Zellforsch.108, 530–562 (1970)
Ribi, W.A.: The neurons of the first optic ganglion of the bee,Apis mellifera. Adv. Anat. Embryol. Cell Biol.50, 6–43 (1975)
Shaw, S.R.: Retinal resistance barriers and electrical lateral inhibition. Nature (Lond.)255, 480–483 (1975)
Snyder, A.W., McIntyre, P.: Polarisation sensitivity of twisted fused rhabdoms. In: Photoreceptor optics (eds. A.W. Snyder, R. Menzel), pp. 388–391. Berlin-Heidelberg-New York: Springer 1975
Snyder, A.W., Menzel, R., Laughlin, S.B.: Structure and function of the fused rhabdom. J. comp. Physiol.87, 99–135 (1973)
Strausfeld, N.J.: Variations and invariants of cell arrangements in the nervous systems of insects. Verh. dtsch. zool. Ges.64, 97–107 (1970)
Varela, F.G.: Fine Structure of the visual system of the honey bee (Apis mellifera). J. Ultrastruct. Res.31, 178–194 (1970)
Wasserman, G.S.: Invertebrate colour vision and the tuned receptor paradigm. Science180, 268–275 (1973)
Zettler, F., Järvilehto, M.: Active and passive axonal propagation of non-spike signals in the retina ofCalliphora. J. comp. Physiol.85, 89–104 (1973)
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Supported by a grant from the Deutsche Forschungsgemeinschaft (Az. Me 365/4)
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Menzel, R., Blakers, M. Colour receptors in the bee eye — Morphology and spectral sensitivity. J. Comp. Physiol. 108, 11–13 (1976). https://doi.org/10.1007/BF00625437
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DOI: https://doi.org/10.1007/BF00625437