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Horizontal cell sensitivity in the cat retina during prolonged dark adaptation

Published online by Cambridge University Press:  02 June 2009

M. J. M. Lankheet ,
M. H. Rowe ,
R. J. A. van Wezel  and
W. A. van de Grind
M. J. M. Lankheet
Affiliation:
Neuroethology, Helmholtz Institute and Comparative Physiology, Universiteit Utrecht, Padualaan 8, 3584 CH Utrecht, The Netherlands
M. H. Rowe
Affiliation:
Neuroethology, Helmholtz Institute and Comparative Physiology, Universiteit Utrecht, Padualaan 8, 3584 CH Utrecht, The Netherlands
R. J. A. van Wezel
Affiliation:
Neuroethology, Helmholtz Institute and Comparative Physiology, Universiteit Utrecht, Padualaan 8, 3584 CH Utrecht, The Netherlands
W. A. van de Grind
Affiliation:
Neuroethology, Helmholtz Institute and Comparative Physiology, Universiteit Utrecht, Padualaan 8, 3584 CH Utrecht, The Netherlands
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Abstract

The effects of dark adaptation on the response properties of ganglion cells have been documented extensively in the cat retina. To pinpoint the different retinal mechanisms that underlie these effects, we studied the response characteristics of cat horizontal (H) cells during prolonged dark adaptation. H-cell responses were recorded intracellularly in the optically intact, in vivo eye. To disentangle rod and cone contributions, sensitivity changes during dark adaptation were tracked with white light and with monochromatic lights that favored either rod or cone excitation. Stable, long-lasting recordings allowed us to measure changes of sensitivity for adaptation periods up to 45 min. Thresholds for white light and 503-nm monochromatic light decreased steadily and in parallel. The maximum increase of sensitivity, after extinguishing a photopic adaptation light, was 1.8 log units only, reached after about 35 min. Sensitivity for 581-nm lights also increased steadily, but at a shallower slope. The steady increase of sensitivity was concomitant with a linear shift in resting membrane potential and with an increase in relative rod contribution to the threshold responses. Even though small-amplitude responses were rod dominated after prolonged dark adaptation, sensitivity to rod signals remained relatively low, compared to sensitivity of cone responses or to the absolute sensitivity of ganglion cells. This suggests that the cone-H-cell pathway plays no role in the dark-adapted cat retina.

Keywords

Horizontal cellDark adaptationCat retinaRod and cone input
Type
Research Articles
Information
Visual Neuroscience , Volume 13 , Issue 5 , September 1996 , pp. 885 - 896
Copyright
Copyright © Cambridge University Press 1996

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References

Adelson, E.H. (1982). Saturation and adaptation in the rod system. Vision Research 22, 1299–1312.CrossRefGoogle ScholarPubMed
Alpern, M. & Pugh, E.N. Jr (1974). The density and photosensitivity of human rhodopsin in the living retina. Journal of Physiology 237, 341–370.CrossRefGoogle ScholarPubMed
Barlow, H.B., Fitzhugh, R. & Kuffler, S.W. (1957). Change of organization in the receptive fields of the cat's retina during dark adaptation. Journal of Physiology 137, 338–354.CrossRefGoogle ScholarPubMed
Barlow, H.B. & Levick, W.R. (1968). The Purkinje shift in the cat retina. Journal of Physiology 196, 2P–3P.Google Scholar
Barlow, H.B. & Levick, W.R. (1969). Three factors limiting the reliable detection of light by retinal ganglion cells of the cat. Journal of Physiology 200, 1–24.CrossRefGoogle ScholarPubMed
Barlow, H.B., Levick, W.R. & Yoon, M. (1971). Responses to single quanta of light in retinal ganglion cells of the cat. Vision Research (Suppl.) 3, 87–101.CrossRefGoogle Scholar
Bonds, A.B. & Enroth-Cugell, C. (1979). Recovery of cat retinal ganglion cell sensitivity following pigment bleaching. Journal of Physiology 295, 47–68.CrossRefGoogle ScholarPubMed
Bonds, A.B. & MacLeod, D.I.A. (1974). The bleaching and regeneration of rhodopsin in the cat. Journal of Physiology 242, 237–253.CrossRefGoogle ScholarPubMed
Brown, K.T. & Murakami, M. (1968). Rapid effects of light and dark adaptation upon the receptive field organization of S-potentials and late receptor potentials. Vision Research 8, 1145–1171.CrossRefGoogle ScholarPubMed
Chan, L.P., Freeman, A.W. & Cleland, B.G. (1992). The rod-cone shift and its effect on ganglion cells in the cat's retina. Vision Research 32, 2209–2219.CrossRefGoogle ScholarPubMed
Derrington, A.M. & Lennie, P. (1982). The influence of temporal frequency and adaptation level on receptive field organization of retinal ganglion cells in cat. Journal of Physiology 333, 343–366.CrossRefGoogle ScholarPubMed
Enroth-Cugell, C., Hertz, B.G. & Lennie, P. (1977). Cone signals in the cat's retina. Journal of Physiology 269, 273–296.CrossRefGoogle ScholarPubMed
Enroth-Cugell, C. & Lennie, P. (1975). The control of retinal ganglion cell discharge by receptive field surrounds. Journal of Physiology 247, 551–578.CrossRefGoogle ScholarPubMed
Goldberg, S.H., Frumkes, T.E. & Nygaard, R.W. (1983). Inhibitory influence of unstimulated rods in the human retina: Evidence provided by examining cone flicker. Science 221, 180–182.CrossRefGoogle ScholarPubMed
Kaplan, E., Marcus, S. & So, Y.T. (1979). Effects of dark adaptation on spatial and temporal properties of receptive fields in cat lateral geniculate nucleus. Journal of Physiology 294, 561–580.CrossRefGoogle ScholarPubMed
Kolb, H. (1977). The organization of the outer plexiform layer in the retina of the cat: Electron microscope observations. Journal of Neurocytology 6, 131–153.CrossRefGoogle Scholar
Kolb, H. & Famiglietti, E.V. (1974). Rod and cone pathways in the inner plexiform layer of the cat retina. Science 186, 47–49.CrossRefGoogle ScholarPubMed
Kolb, H. & Nelson, R. (1983). Rod pathways in the retina of the cat. Vision Research 23, 301–312.CrossRefGoogle ScholarPubMed
Kolb, H. & Nelson, R. (1984). Neural architecture of the cat retina. In Progress in Retinal Research Vol. 3, ed. Osborne, N.N. & Chader, G.J., pp. 21–60. Oxford, New York: Pergamon Press.Google Scholar
Lankheet, M.J.M., Frens, M.A. & Van De Grind, W.A. (1990). Spatial properties of horizontal cell responses in the cat retina. Vision Research 30, 1257–1275.CrossRefGoogle ScholarPubMed
Lankheet, M.J.M., Van Wezel, R.J.A. & Van De Grind, W.A. (1991). Effects of background illumination on cat horizontal cell responses. Vision Research 31, 919–932.CrossRefGoogle ScholarPubMed
Lankheet, M.J.M., Van Wezel, R.J.A., Prickaerts, J.H.H.J. & Van De Grind, W.A. (1993). The dynamics of light adaptation in cat horizontal cell responses. Vision Research 33, 1153–1171.CrossRefGoogle ScholarPubMed
Lennie, P. (1979). Scotopic increment thresholds in retinal ganglion cells. Vision Research 19, 425–430.CrossRefGoogle ScholarPubMed
Molenaar, J., Voorhorst, R., Schreurs, A.W., Broekhuyzen, P., Nivard, J. & Van De Grind, W.A. (1980). A mechanical oscilloscope for vision research. Pflügers Archive für die gesamte Physiology 383, 173–179.CrossRefGoogle ScholarPubMed
Naka, K.I. & Rushton, W.A.H. (1968). S-potentials and dark adaptation in fish. Journal of Physiology 194, 259–269.CrossRefGoogle ScholarPubMed
Nelson, R. (1977). Cat cones have rod input: A comparison of the response properties of cones and horizontal cell bodies in the retina of the cat. Journal of Comparative Physiology 172, 109–136.Google ScholarPubMed
Nelson, R. (1985). Spectral properties of cat horizontal cells. Neuroscience Research (Suppl.) 2, S167–S183.Google ScholarPubMed
Nelson, R., Lützow, A., Kolb, H. & Gouras, P. (1975). Horizontal cells in cat retina with independent dendritic systems. Science 189, 137–139.CrossRefGoogle ScholarPubMed
Nelson, R., Lynn, T., Dickinson-Nelson, A. & Kolb, H. (1985). Spectral mechanisms in cat horizontal cells. In Neurocircuitry of the Retina, A Cajal Memorial, ed. Gallego, A. & Gouras, P., pp. 109–121. Amsterdam: Elsevier.Google Scholar
Nelson, R., Pflug, R. & Baer, S.M. (1990). Background-induced flicker enhancement in cat retinal horizontal cells. II Spatial properties. Journal of Neurophysiology 64, 326–340.CrossRefGoogle ScholarPubMed
Peichl, L. & Wässle, H. (1979). Size, scatter, and coverage of ganglion cell receptive field centers in the cat retina. Journal of Physiology 291, 117–141.CrossRefGoogle ScholarPubMed
Pflug, R., Nelson, R. & Ahnelt, P.K. (1990). Background-induced flicker enhancement in cat retinal horizontal cells. II Temporal and spectral properties. Journal of Neurophysiology 64, 313–325.CrossRefGoogle Scholar
Purkinje, J.E. (1825). Neue Beiträge zur Kenntniss des Sehens in subjectiver Hinsicht. Berlin: G. Reimer.CrossRefGoogle Scholar
Raviola, E. & Gilula, N.B. (1973). Gap junctions between photoreceptor cells in the vertebrate retina. Proceedings of the National Academy of Science of the U.S.A. 70, 1677–1681.CrossRefGoogle ScholarPubMed
Rushton, W.A.H. (1962). Visual pigments in man. Scientific American 139, 2–10.Google Scholar
Sakmann, B. & Creutzfeldt, O.D. (1969). Scotopic and mesopic light adaptation in the cat's retina. Pflugers Archive 313, 168–185.CrossRefGoogle ScholarPubMed
Shapley, R.M. & Enroth-Cugell, C. (1984). Visual adaptation and retinal gain controls. Progress in Retinal Research 3, 263–346.CrossRefGoogle Scholar
Smith, R.G., Freed, M.A. & Sterling, P. (1986). Microcircuitry of the dark-adapted cat retina: Functional architecture of the rod-cone network. Journal of Neuroscience 6, 3505–3517.CrossRefGoogle ScholarPubMed
Steinberg, R.H. (1969 a). Rod and cone contributions to S-potentials from the cat retina. Vision Research 9, 1319–1329.CrossRefGoogle ScholarPubMed
Steinberg, R.H. (1969 b). Rod-cone interaction in S-potentials from the cat retina. Vision Research 9, 1331–1344.CrossRefGoogle ScholarPubMed
Steinberg, R.H. (1969 c). The rod after-effect in S-potentials from the cat retina. Vision Research 9, 1345–1355.CrossRefGoogle ScholarPubMed
Steinberg, R.H. (1971). Incremental responses to light recorded from pigment epithelial cells and horizontal cells of the cat retina. Journal of Physiology 217, 93–110.CrossRefGoogle ScholarPubMed
Sterling, P. (1983). Microcircuitry of the cat retina. Annual Review of Neuroscience 6, 149–185.CrossRefGoogle ScholarPubMed
Yang, X.L. & Wu, S.M. (1989). Modulation of rod-cone coupling by light. Science 244, 352–354.CrossRefGoogle ScholarPubMed