Hostname: page-component-78c5997874-4rdpn Total loading time: 0 Render date: 2024-11-10T22:19:31.777Z Has data issue: false hasContentIssue false
  • English
  • Français

Light-dependent hydration of the space surrounding photoreceptors in the cat retina

Published online by Cambridge University Press:  02 June 2009

Jian-Dong Li ,
Victor I. Govardovskii  and
Roy H. Steinberg
Jian-Dong Li
Affiliation:
Departments of Physiology and Ophthalmology, University of California, San Francisco
Victor I. Govardovskii
Affiliation:
Institute of Evolutionary Physiology and Biochemistry, Russian Academy of Sciences, St. Petersburg, Russia
Roy H. Steinberg
Affiliation:
Departments of Physiology and Ophthalmology, University of California, San Francisco
Get access Rights & Permissions [Opens in a new window]

Abstract

We have studied the effect of retinal illumination on the concentration of the extracellular space marker tetramethylammonium (TMA+) in the dark-adapted cat retina using double-barreled ion-selective microelectrodes. The retina was loaded with TMA+ by a single intravitreal injection. Retinal illumination produced a slow decrease in , which was maximal in amplitude in the most distal portion of the space surrounding photoreceptors, the subretinal space. The light-evoked decrease in was considerably slower and of a different overall time course than the light-evoked decrease in , also recorded in the subretinal space. decreased to a peak at 38 s after the onset of illumination, then slowly recovered towards the baseline, and transiently increased following the offset of illumination. It resembled the light-evoked decreases previously recorded in the in vitro preparations of frog (Huang & Karwoski, 1990, 1992) and chick (Li et al., 1992, 1994) but was considerably larger in amplitude, 22% compared with 7%. As in frog, where it was first recorded, the light-evoked decrease is considered to originate from a light-evoked increase in the volume of the subretinal space (or subretinal hydration). A mathematical model accounting for diffusion predicted that the volume increase underlying the response was 63% on average and could be as large as 95% and last for minutes. The estimated volume increase was then used to examine its effect on K+ concentration in the subretinal space. We conclude that a light-dependent hydration of the subretinal space represents a significant physiological event in the intact cat eye, which should affect the organization of the interphotoreceptor matrix, and the concentrations of all ions and metabolites located in the subretinal space.

Keywords

Subretinal spaceTMA+PhotoreceptorRPEExtracellular volumeCat
Type
Research Articles
Information
Visual Neuroscience , Volume 11 , Issue 4 , July 1994 , pp. 743 - 752
Copyright
Copyright © Cambridge University Press 1994

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

Adorante, J.S. & Miller, S.S. (1990). Potassium-dependent volume regulation in retinal pigment epithelium is mediated by Na, K, Cl cotransport. Journal of General Physiology 96, 1153–1176.Google Scholar
Ballanyi, K., Grafe, P., Serve, G. & Schlue, W.-R. (1990). Electro physiological measurements of volume changes in leech neuropile glial cells. Glia 3, 151–158.CrossRefGoogle Scholar
Bialek, S. & Miller, S.S. (1994). K and Cl transport in bovine retinal pigment epithelium: Mechanisms that modulate subretinal space volume and composition. Journal of Physiology 472, 401–417.CrossRefGoogle Scholar
Blair, N.P., Baker, D.S., Rhode, J.P. & Solomon, M. (1989). Vitreoperfusion, a new approach to ocular ischemia. Archive für Ophthalmologic 107, 417–423.CrossRefGoogle ScholarPubMed
Dietzel, I., Heinemann, U., Hofmeier, G. & Lux, H.D. (1980). Transient changes in the size of the extracellular space in the sensorimotor cortex of cats in relation to stimulus-induced changes in potassium concentration. Experimental Brain Research 40, 432–439.Google Scholar
Frambach, D.A. & Misfeldt, D.S. (1983). Furosemide-sensitive Cl transport in embryonic chicken retinal pigment epithelium. American Journal of Physiology 244, F679–685.Google ScholarPubMed
Frishman, L.J. & Steinberg, R.H. (1989 a). Intraretinal analysis of the threshold dark-adapted ERG of cat retina. Journal of Neurophysiology 61, 1221–1232.Google Scholar
Frishman, L.J. & Steinberg, R.H. (1989 b). Light-evoked changes in in proximal portion of the dark-adapted cat retina. Journal of Neurophysiology 61, 1233–1243.CrossRefGoogle ScholarPubMed
Gallemore, R.P., Li, J.-D., Govardovskii, V.I. & Steinberg, R.H. (1994). Calcium gradients and light-evoked calcium changes outside rods in the intact cat retina. Visual Neuroscience 11, 753–761.Google Scholar
Govardovskii, V.J., Li, J.-D., Dmitriev, A.V. & Steinberg, R.H. (1994). Mathematical model of TMA+ diffusion and prediction of light-dependent subretinal hydration in chick retina. Investigative Ophthalmology and Visual Science 35 (in press).Google Scholar
Huang, B. & Karwoski, C. (1989). Changes in extracellular space in the frog retina. Investigative Ophthalmology and Visual Science 30, 64.Google Scholar
Huang, B. & Karwoski, C. (1990). Light-evoked increase in subretinal space (SRS) in frog retina. Investigative Ophthalmology and Visual Science 31, 71.Google Scholar
Huang, B. & Karwoski, C. (1992). Light-evoked expansion of subretinal space volume in the retina of the frog. Journal of Neuroscience 12(11), 4243–4252.CrossRefGoogle ScholarPubMed
Joseph, D.P. & Miller, S.S. (1991). Apical and basal membrane ion transport mechanisms in bovine retinal pigment epithelium. Journal of Physiology 435, 439–463.CrossRefGoogle ScholarPubMed
Karwoski, C.J., Frambach, D.A. & Proenza, L.M. (1985). Laminar profile of resistivity in frog retina. Journal of Neurophysiology 54, 1607–1619.Google Scholar
Kennedy, B.B. (1990). Na+-K+-Cl−cotransport in cultured ceils derived from human pigment epithelium. American Journal of Physiology 25, C29–C34.Google Scholar
Kennedy, B.B. (1992). Rubidium transport in cultured monkey retinal pigment epithelium. Experimental Eye Research 55, 289–296.Google Scholar
Li, J.-D. & Steinberg, R.H. (1993). Light-dependent hydration of the space surrounding photoreceptors in the cat retina. Investigative Ophthalmology and Visual Science (Suppl.) 34, 1204.Google Scholar
Li, J.-D., Gallemore, R.P. & Steinberg, R.H. (1992). Light-induced increase in subretinal space volume in chick retina. Investigative Ophthalmology and Visual Science (Suppl.) 33, 913.Google Scholar
Li, J.-D., Gallemore, R.P., Dmitriev, A.V. & Steinberg, R.H. (1994). Light-dependent hydration of the space surrounding photoreceptors in chick retina. Investigative Ophthalmology and Visual Science 35 (in press).Google ScholarPubMed
Linsenmeier, R.A. (1986). Effects of light and darkness on oxygen distribution and consumption in the cat retina. Journal of General Physiology 88, 521–542.CrossRefGoogle ScholarPubMed
Linsenmeier, R.A. & Steinberg, R.H. (1982). Origin and sensitivity of the light peak in the intact cat eye. Journal of Physiology (London) 331, 653–673.Google Scholar
Linsenmeier, R.A. & Steinberg, R.H. (1984). Effects of hypoxia on potassium homeostasis and pigment epithelial cells in the cat retina. Journal of General Physiology 84, 945–970.CrossRefGoogle ScholarPubMed
Miller, S.S. & Edelman, J.L. (1990). Active ion transport pathways in the bovine retinal pigment epithelium. Journal of Physiology 424, 283–300.Google Scholar
Newman, E.A. (1980). Current source-density analysis of the b–wave of the frog retina. Neurophysiology 43, 1355–1366.Google Scholar
Ogden, T.E. & Ito, H. (1971). Avian retina. II. An evaluation of retinal electrical anisotropy. Neurophysiology 34, 367–373.CrossRefGoogle Scholar
Steinberg, R.H. (1969). The rod after-effect in S potentials from the cat retina. Vision Research 9, 1345–1355.CrossRefGoogle Scholar
Steinberg, R.H., Li, J.-D. & Govardovskii, V. (1993). Effects of a light-evoked increase in volume on ion concentrations in the subretinal space of chick retina. Investigative Ophthalmology and Visual Science (Suppl.) 34, 1204.Google Scholar
Steinberg, R.H., IIOakley, B. & Niemeyer, G. (1980). Light-evoked changes in in retina of intact cat eye. Journal of Neurophysiology 44, 897–921.CrossRefGoogle ScholarPubMed
Tsuboi, S., Manabe, R. & Iizuka, S. (1986). Aspects of electrolyte transport across isolated dog retinal pigment epithelium. American Journal of Physiology 250, F781–784.Google Scholar
Wiederholt, M. & Zadunaisky, J.A. (1984). Decrease of intracellular chloride activity by furosemide in frog retinal pigment epithelium. Current Eye Research 3, 673–675.Google Scholar
Yamamoto, F., Borgula, G.A. & Steinberg, R.H. (1992). Effects of light and darkness on pH outside rod photoreceptors in the cat retina. Experimental Eye Research 54, 685–697.Google Scholar