Hostname: page-component-8448b6f56d-cfpbc Total loading time: 0 Render date: 2024-04-24T00:05:01.364Z Has data issue: false hasContentIssue false

Signal integration at the pedicle of turtle cone photoreceptors: An anatomical and electrophysiological study

Published online by Cambridge University Press:  02 June 2009

Eric M. Lasater
Affiliation:
Departments of Physiology and Ophthalmology, University of Utah, School of Medicine, Salt Lake City
Richard A. Normann
Affiliation:
Departments of Bioengineering, Physiology, and Ophthalmology, University of Utah, School of Medicine, Salt Lake City
Helga Kolb
Affiliation:
Departments of Physiology and Ophthalmology, University of Utah, School of Medicine, Salt Lake City

Abstract

The morphology of the axon which connects the cell body and pedicle of turtle cone photoreceptors was studied by light and electron microscopy. The axon which contains numerous synaptic vesicles, some endoplasmic reticulum, and a few cisternae is basically filled with cytoplasm. The length of the axon is related to the class of cone and varies slightly with retinal location, with axons as short as 3–6 μm found in red cones, and as long as 60 μm in cones containing colorless oil droplets. By simultaneously voltage clamping the cell body and pedicle regions of single isolated cones, we measured the longitudinal axonal resistance and the cell body and pedicle membrane resistances. For each cell studied, the axonal resistance of cones with short axons was lower than the cell and pedicle membrane resistances. Thus, the cell can be considered to be an isopotential structure. However, in some cones with long axons, the axonal, cell body, and pedicle resistances were comparable. The pedicles of these cones, therefore, could act like summing points and may provide a locus for spatial signal integration. Electrical coupling between the principal and accessory members of double cones was also studied. Electron-microscopic observation of the membrane junction between the apposed inner segments of the double cones in the intact retina show narrow segments which resemble gap junctions. However, in every double cone studied in culture, passing currents into one member of the double cone did not result in measurable current flow in the adjacent cell. Thus, the two members of the double cone, isolated from the turtle retina, are not electrically coupled.

Type
Research Article
Copyright
Copyright © Cambridge University Press 1989

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Attwell, D., Werblin, F.S. & Wilson, M. (1982). The properties of single cones isolated from the tiger salamander retina. Journal of Physiology (London) 328, 259283.CrossRefGoogle ScholarPubMed
Attwell, D., Wilson, M. & Wu, S.M. (1984). A quantitative analysis of interactions between photoreceptors in salamander (ambystoma) retina. Journal of Physiology (London) 352, 703737.CrossRefGoogle ScholarPubMed
Baylor, D.A., Fuortes, M.G.F. & O'Bryan, P.M. (1971). Receptive field of cones in the retina of the turtle. Journal of Physiology (London) 214, 265294.CrossRefGoogle ScholarPubMed
Borwein, B., Borwein, D., Medieros, J. & McGowan, J.W. (1980). The ultrastructure of monkey foveal photoreceptors, with special reference to the structure, shape, size, and spacing of the foveal cones. American Journal of Anatomy 159, 125146.CrossRefGoogle Scholar
Boycott, B.B., Hopkins, J.M. & Sperling, H.G. (1986). Cone connections of the horizontal cells of the rhesus monkey. Proceedings of the Royal Society B 229, 345379.Google Scholar
Dalton, A.J. (1955). A chrome-osmium fixative for electron microscopy. Anatomical Record 121, 281287.Google Scholar
Hagins, W.A., Penn, R.D. & Yoshlkami, S. (1970). Dark current and photocurrent in retinal rods. Biophysical Journal 10, 380412.CrossRefGoogle ScholarPubMed
Hamill, O.P., Morty, A., Neher, E., Sakmann, B. & Segworth, F.J. (1981). Improved patch-clamp techniques for high-resolution recording from cells and cell-free membrane patches. Pfluegers Archiv 391, 85100.CrossRefGoogle ScholarPubMed
Kaneko, A. (1973). Receptive-field organization of bipolar and ama-crine cells in the goldfish retina. Journal of Physiology (London) 235, 133153.CrossRefGoogle ScholarPubMed
Kolb, H. & Jones, J. (1982). Light and electron microscopy of the photoreceptors in the retina of the red-eared slider (Pseudemys scripta elegans). Journal of Comparative Neurology 209, 331338.CrossRefGoogle ScholarPubMed
Kolb, H. & Jones, J. (1984). Synaptic organization of the outer plexi-form layer of the turtle retina: an electron microscope study of serial sections. Journal of Neurocytology 13, 567591.CrossRefGoogle Scholar
Kolb, H. & Jones, J. (1985). Electron microscopy of Golgi-impregnated photoreceptors reveals connections between red and green cones in the turtle retina. Journal of Neurophysiology 54, 304317.CrossRefGoogle ScholarPubMed
Kolb, H. & Jones, J. (1987). The distinction by light and electron microscopy of two types of cone containing colorless oil droplets in the retina of the turtle. Vision Research 27, 14451458.CrossRefGoogle ScholarPubMed
Kraft, T.W. & Burkhardt, D.A. (1986). Telodendrites of cone photoreceptors: structure and probable function. Journal of Comparative Neurology 249, 1327.CrossRefGoogle ScholarPubMed
Lasater, E.M. & Dowling, J.E. (1985). Dopamine decreases conductance of the electrical junctions between cultured retinal horizontal cells. Proceedings of the National Academy of Sciences of the U.S.A. 82, 3025–2029.CrossRefGoogle ScholarPubMed
Liebman, P.A. & Granda, A.M. (1971). Microspectrophotometric measurements of visual pigments of two species of turtle, Pseudemys scripta and Chelonia mydas. Vision Research 11, 105114.CrossRefGoogle ScholarPubMed
Lipetz, L.E. (1985). Some neuronal circuits of the turtle retina. In The Visual System, ed. Fein, A. & Levine, J.S., pp. 107132. New York: Alan R. Liss.Google Scholar
Lipetz, L.E. & Macnichol, E.F. Jr, (1982). Photoreceptors of freshwater turtles: cell types and visual pigments. Biological Bulletin 163, 396.Google Scholar
Lipetz, L.E. & Macnichol, E.F. Jr, (1983). Visual pigments of two freshwater turtles. Biophysical Journal 41 (2/2), 26a.Google Scholar
Loewenstein, W.E. (1964). Permeability of the nuclear membrane as determined with electrical methods. Protoplasmatologia 54, 2634.Google Scholar
Naka, K-I. & Nye, P.W. (1971). Role of horizontal cells in the organization of the catfish retinal receptive field. Journal of Neurophys-iology 34, 785801.CrossRefGoogle ScholarPubMed
Normann, R.A., Perlman, I., Kolb, H., Jones, J. & Daly, S.J. (1984). Direct excitatory interactions between cones of different spectral types in the turtle retina. Science 224, 625627.CrossRefGoogle ScholarPubMed
Normann, R.A., Perlman, I. & Daly, S.J. (1985). Mixing of color signals by turtle cone photoreceptors. Journal of Neurophysiology 54, 293303.CrossRefGoogle ScholarPubMed
Ohtsuka, T. (1985 a). Relation of spectral types to oil droplets in cones of turtle retina. Science 229, 874877.CrossRefGoogle ScholarPubMed
Ohtsuka, T. (1985 b). Spectral sensitivities of seven morphological types of photoreceptors in the retina of the turtle (Geoclemys reevesii). Journal of Comparative Neurology 237, 145154.CrossRefGoogle ScholarPubMed
Ohtsuka, T. & Kouyama, N. (1986). Electron-microscopic study of synaptic contacts between photoreceptors and HRP-filled horizontal cells in the turtle retina. Journal of Comparative Neurology 250, 141156.CrossRefGoogle ScholarPubMed
Richter, A. & Simon, E.J. (1974). Electrical responses of double cones in the turtle retina. Journal of Physiology (London) 242, 673683.CrossRefGoogle ScholarPubMed
Schanne, O.F. & Ruiz, P.-Ceretti E. (1978). Impedance Measurements in Biological Cells. Wiley Interscience.Google Scholar
Schnapf, J.L. & McBurney, R.N. (1980). Light-induced changes in membrane current in cone outer segments of tiger salamander and turtle. Nature 287, 239241.CrossRefGoogle ScholarPubMed
Spray, D.C., White, R.L., Campos De Carvalho, A., Harris, A.L. & Bennett, M.V.L. (1984). Gating of gap junction channels. Biophysical Journal 45, 219230.CrossRefGoogle ScholarPubMed
Toyoda, J.-I. & Kujiraoka, T. (1982). Analysis of bipolar cell responses elicited by polarization of horizontal cells. Journal of General Physiology 79, 131145.CrossRefGoogle Scholar
Werblin, F.S. & Dowling, J.E. (1969). Organization of the retina of the mudpuppy, Necturus maculosus. II. Intracellular recording. Journal of Neurophysiology 32, 339355.CrossRefGoogle ScholarPubMed