Hostname: page-component-78c5997874-s2hrs Total loading time: 0 Render date: 2024-11-13T04:38:25.769Z Has data issue: false hasContentIssue false

Wavelength-dependent temporal properties of retinal horizontal cells in turtles

Published online by Cambridge University Press:  02 June 2009

C.A. Dvorak
Affiliation:
Program in Neurosciences, School of Life Sciences, University of Delawarer, Newark
A.M. Granda
Affiliation:
Program in Neurosciences, School of Life Sciences, University of Delawarer, Newark

Abstract

Electrical reponses of luminosity horizontal cells (L cells) to monochromatic stimuli were analyzed by intracellular recordings in the retinas of the freshwater turtle (Pseudemys scripta elegans) and of the sea turtle (Chelonia mydas mydas). Light intensity, duration, and wavelength were varied to assess temporal effects. For a given intensity of monochromatic light, response amplitude increased with stimulus duration until maximum amplitude occurred at a specific duration. This suprathreshold metric of temporal integration is called here summation time, and it is wavelength-dependent.

L cells always had some level of red-sensitive cone input, although in some cells inputs from green- and blue-sensitive cones were also observed. For these latter cells, summation times were shorter for 640-nm than for 540-nm or 450-nm lights. These results were most evident in cells that received dominant inputs from blue- or green-sensitive cones.

Responses of some other L cells were almost completely dominated by inputs from red-sensitive cones. Summation times of these cells were not wavelength-dependent. But when these inputs also included green-sensitive cones, shorter summation times were obtained to 640-nm light than to 540-nm light, even though dominant inputs were still from red-sensitive cones. These results, obtained from both retinal and 3,4-dehydroretinal photopigment systems, are consistent with reported observations in Pseudemys scripta elegans that show linear responses of red-sensitive cones to have shorter integration times and times-to-peak than green-sensitive cones.

Responses from horizontal cells dominated by blue-sensitive cone inputs were the most sensitive of all; they also had the longest summation times. These results support the hypothesis that a gain in sensitivity occurs from the integration of absorbed photons over longer periods of time.

These intracellular responses are of particular importance because behavioral critical durations in turtle, as defined by Bloch&'s law, are similarly wavelength-dependent.

Type
Research Articles
Copyright
Copyright © Cambridge University Press 1990

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

Baylor, D.A. & Fettiplace, R. (1975). Light path and photon capture in turtle photoreceptors. Journal of Physiology 248, 433464.Google Scholar
Baylor, D.A. & Fuortes, M.G.F. (1970). Electrical responses of single cones in the retina of the turtle. Journal of Physiology 207, 7792.Google Scholar
Baylor, D.A. & Hodgkin, A.L. (1973). Detection and resolution of visual stimuli by turtle photoreceptors. Journal of Physiology 234, 163198.Google Scholar
Baylor, D.A., Hodgkin, A.L. & Lamb, T.D. (1974). The electrical responses of turtle cones to flashes and steps of light. Journal of Physiology 242, 685727.CrossRefGoogle ScholarPubMed
Baylor, D.A., Mathews, G. & Yau, K.-W. (1980). Two components of electrical dark noise in toad retinal rod outer segments. Journal of Physiology 309, 591621.Google Scholar
Carr, A. (1952). Handbook of Turtles. Ithaca, New York: Comstock Publishing Association.Google Scholar
Copenhagen, D.R. & Owen, W.G. (1976). Functional characteristics of lateral interactions between rods in the retina of the snapping turtle. Journal of Physiology 259, 251282.CrossRefGoogle ScholarPubMed
Detwiler, P.B., Hodgkin, A.L. & McNaughton, P.A. (1980). Temporal and spatial characteristics of the voltage response of rods in the retina of the snapping turtle. Journal of Physiology 300, 213250.Google Scholar
Fesenko, E.E., Kolesnikov, S.S. & Lyubarsky, A.L. (1985). Induction by cGMP of cationic conductance in plasma membrane of retinal rod outer segment. Nature 313, 310313.Google Scholar
Fuortes, M.G.F. & Hodgkin, A.L. (1964). Changes in time scale and sensitivity in the ommatidia of Limulus. Journal of Physiology 172,239263.Google Scholar
Fourtes, M.G.F. & Simon, E.J. (1974). Interactions leading to horizontal cell responses in the turtle retina. Journal of Physiology 240, 177198.Google Scholar
Fuortes, M.G.F., Schwartz, E.A. & Simon, E.J. (1973). Colour dependence of cone responses in the turtle retina. Journal of physiology 234, 199216.Google Scholar
Granda, A.M. & Dvorak, C.A. (1977). Vision in turtle. In: Handbook of Sensory Physiology, Vol. II/5, ed. Crescitelli, F., pp. 451495. Heidelberg: Springer-Verlag.Google Scholar
Granda, A.M. & Stirling, C.E. (1966). The spectral sensitivity of the turtle&'s eye to very dim lights. Vision Research 6, 143152.CrossRefGoogle ScholarPubMed
Granda, A.M., Maxwell, J.H. & Zwick, H. (1972). The temporal course of dark adaptation in the turtle Pseudemys using a behavioral avoidance paradigm. Vision Research 12, 653672.CrossRefGoogle ScholarPubMed
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.Google Scholar
Leeper, H.F. (1978 a). Horizontal cells of the turtle retina, I: Light microscopy of Golgi preparations. Journal of Comparative Neurology 182, 777794.Google Scholar
Leeper, H.F. (1978 b). Horizontal cells of the turtle retina, II: Analysis of interconnections between photoreceptors and horizontal cells by light microscopy. Journal of Comparative Neurology 182, 795810.Google Scholar
Liepman, P.A. & Granda, A.M. (1971). Microspectrophotometric measurements of visual pigments in two species of turtle,Pseudemys scripta and Chelonia mydas. Vision Research 11, 105114.CrossRefGoogle Scholar
Liebman, P.A. & Granda, A.M. (1975). Super dense carotenoid spectra resolved in single cone oil droplets. Nature 253, 370372.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
Marchiafava, P.L., Strettoi, E. & Alpigiani, V. (1985). Intracellular recording from single- and double-cone cells isolated from the fish retina (Tinca tinca). Experimental Biology 44, 173180.Google Scholar
Nakatani, K. & Yau, K.-W. (1985). cGMP opens the light-sensitive conductance in retinal rods. Biophysical Journal 47, 356a.Google Scholar
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, 875877.Google Scholar
Ohtsuka, T. (1985 b). Spectral sensitivities of seven morphological types of photoreceptors in the retina of the turtle, Geoclemys revesii. Journal of Comparative Neurology 237, 145154.Google Scholar
Ohtsuka, T. & Kouyama, N. (1986 a). Electron-microscopic study of synaptic contacts between photoreceptors and HRP-filled horizontal cells in the turtle retina. Journal of Comparative Neurology 250, 141156.Google Scholar
Ohtsuka, T. & Kouyama, N. (1986 b). Physiological and morphological studies of cone-horizontal cell connections in the turtle retina. Neuroscience Research (Suppl.) 4, S69–S84.Google Scholar
Ohtsuka, T. & Kouyama, N. (1990). Telodendrial contact of HRP-filled photoreceptors in the turtle retina: Pathways of photoreceptor coupling. Journal of Comparative Neurology 292, 599613.Google Scholar
Perlman, I., Normann, R.A., Itzaki, A. & Daly, S.J. (1985). Chromatic and spatial information processing by red cones and L-type horizontal cells in the turtle retina. Vision Research 25, 543549.Google Scholar
Richter, A. & Simon, E.J. (1974). Electrical responses of double cones in the turtle retina. Journal of Physiology 242, 673683.CrossRefGoogle ScholarPubMed
Simon, E.J. (1973). Two types of lumionsity horizontal cell in the retina of the turtle. Journal of physiology 230, 199211.Google Scholar
Wheeler, T.G & Naka, T.-I. (1977). The modes of chromatic interactions in the retina. Vision Research 17, 10151018.Google Scholar