Hostname: page-component-586b7cd67f-2plfb Total loading time: 0 Render date: 2024-11-23T22:33:39.390Z Has data issue: false hasContentIssue false
  • English
  • Français

Effects of adaptation level and hypoglycemia on function of the cat retina during hypoxemia

Published online by Cambridge University Press:  02 June 2009

M. A. McRipley ,
J. Ahmed ,
E. P. -C. Chen  and
R. A. Linsenmeier
M. A. McRipley
Affiliation:
Department of Biomedical Engineering, Northwestern University, Evanston
J. Ahmed
Affiliation:
Department of Biomedical Engineering, Northwestern University, Evanston
E. P. -C. Chen
Affiliation:
Department of Biomedical Engineering, Northwestern University, Evanston
R. A. Linsenmeier
Affiliation:
Department of Biomedical Engineering, Northwestern University, Evanston Department of Neurobiology and Physiology, Northwestern University, Evanston
Get access Rights & Permissions [Opens in a new window]

Abstract

Acute hypoxemia (low PaO2) leads to changes in oxygen consumption and electrical responses of the outer retina of cats, but inner retinal ERG components and ganglion cell responses have been shown to be quite resistant to hypoxemia. The purpose of this study was to determine whether the resistance of the inner retina depends on (1) the stimulus conditions, specifically the degree of light adaptation; and (2) the ability of the photoreceptors to increase glycolysis during hypoxemia. To address these issues, recordings of single ganglion cell action potentials and of the b-wave and scotopic threshold response (STR) of the electroretinogram (ERG) were made from the eyes of anesthetized cats during hypoxemia alone and hypoxemia plus hypoglycemia. Ganglion cells appeared to be equally resistant to hypoxemia at high and low backgrounds (3.3 to 9.7 log equivalent quanta(555 nm)-deg-2-s-1), and the STR, recorded with dim stimuli during dark adaptation, when photoreceptor oxygen consumption is most susceptible to hypoxemia, was unchanged until PaO2 was below 30 mm Hg. The amplitude of the b-wave was similarly resistant to hypoxemia when the animal was normoglycemic. During hypoglycemia, however, both the b-wave and the STR became more sensitive to hypoxemia, beginning to change at PaO2s as high as 50 mm Hg when blood glucose was 40–50 mg/dl. It is argued that hypoglycemia limits or prevents the increased glycolytic ATP production that would ordinarily occur when the photoreceptor oxygen supply decreases, and that increased photoreceptor glycolysis is essential in the protection of the retina against mild hypoxemia.

Keywords

HypoxiaHypoxemiaHypoglycemiaRetinaElectroretinogramRetinal ganglion cells
Type
Research Articles
Information
Visual Neuroscience , Volume 14 , Issue 2 , March 1997 , pp. 339 - 350
Copyright
Copyright © Cambridge University Press 1997

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

REFERENCES

Ames, A. III & Gurian, B.S. (1963). Effects of glucose and oxygen deprivation on function of isolated mammalian retina. Journal of Neurophysiology 26, 617–634.CrossRefGoogle ScholarPubMed
Bill, A. (1962). Aspects of physiological and pharmacological regulation of uveal blood flow. Acta Societas Medica Upsaliensis 67, 122–134.Google Scholar
Braun, R.D. & Linsenmeier, R.A. (1995). Retinal oxygen tension and the electroretinogram during retinal artery occlusion in the cat. Investigative Ophthalmology and Visual Science 36, 523–541.Google ScholarPubMed
Caldwell, G., Davies, E.G., Sullivan, P.M., Morris, A.H. & Kohner, E.M. (1990). A laser Doppler velocimetry study of the effect of hypoglycaemia on retinal blood flow in the minipig. Diabetologica 33, 262–265.CrossRefGoogle ScholarPubMed
Cao, W., Govardovskii, V., Li, J.-D. & Steinberg, R.H. (1996). Systemic hypoxia dehydrates the space surrounding photoreceptors in the cat retina. Investigative Ophthalmology and Visual Science 37, 586–596.Google ScholarPubMed
Chen, E.P.-C. & Linsenmeier, R. (1989) Effects of 2-amino-4-phos-phonobutyric acid on responsivity and spatial summation of X cells in the cat retina. Journal of Physiology 419, 59–75.CrossRefGoogle ScholarPubMed
Cohen, L.H. & Noell, W.K. (1965). Relationships between visual function and metabolism. In Biochemistry of the Retina, ed. Graymore, C.N., pp. 36–50. London, England: Academic Press.Google Scholar
Dawis, S., Hofmann, H. & Niemeyer, G. (1985). The electroretinogram, standing potential and light peak of the perfused cat eye during acid-base changes. Vision Research 25, 1163–1177.CrossRefGoogle ScholarPubMed
Derrer, S.A., Sieber, F.E., Saudek, C.D., Koehler, R.C. & Traystman, R.J. (1990). Cerebrovascular and metabolic responses to hypoxia during hypoglycemia in dogs. American Journal of Physiology 258, H400–H407.Google 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., Goldstick, T.K. & Linsenmeier, R.A. (1980). The contrast sensitivity of cat retinal ganglion cells at reduced oxygen tensions. Journal of Physiology 304, 59–81.CrossRefGoogle ScholarPubMed
Enroth-Cugell, C. & Robson, J.G. (1966). The contrast sensitivity of retinal ganglion cells of the cat. Journal of Physiology 187, 517–552.CrossRefGoogle ScholarPubMed
Eperon, G., Johnson, M. & David, N.J. (1975). The effect of arterial P02 on relative retinal blood flow in monkeys. Investigative Ophthalmology and Visual Science 4, 342–352.Google Scholar
Ferrendelli, J.A. (1974). Cerebral utilization of nonglucose substrates and their effect in hypoglycemia. In Brain Dysfunction and Metabolic Disorders, ed. Plum, F., pp. 113–123. New York: Raven Press.Google Scholar
Friedman, E. & Chandra, S.R. (1972). Choroidal blood flow, III. Effects of oxygen and carbon dioxide. Archives of Ophthalmology 87, 70–71.CrossRefGoogle Scholar
Frishman, L. & Steinberg, R.H. (1989 a). Intraretinal analysis of the threshold dark-adapted ERG of cat retina. Journal of Neurophysiology 61, 1233–1243.CrossRefGoogle ScholarPubMed
Frishman, L. & Steinberg, R.H. (1989 b). Light-evoked increases in [K+]0 in proximal portion of the dark-adapted cat retina. Journal of Neurophysiology 61, 1221–1232.CrossRefGoogle Scholar
Granit, R. (1933). The components of the retinal action potential and their relation to the discharge in the optic nerve. Journal of Physiology 77, 207–240.CrossRefGoogle Scholar
Graymore, C.N. (1959). Metabolism of the developing retina. I. Aerobic and anaerobic glycolysis. British Journal of Ophthalmology 43, 34–39.CrossRefGoogle ScholarPubMed
Hiroi, K., Yamamoto, F. & Honda, Y. (1994). Analysis of electroretinogram during systemic hypercapnia with intraretinal K+-microelectrodes in cats. Investigative Ophthalmology and Visual Science 35, 3957–3961.Google ScholarPubMed
Hirsch-Hoffmann, C. & Niemeyer, G. (1993). Changes in plasma glucose level affect rod-, but not cone-ERG in the anesthetized cat. Clinical Vision Science 8, 489–501.Google Scholar
Hochstein, S. & Shapley, R. (1976). Linear and nonlinear spatial sub-units in Y cat retinal ganglion cells. Journal of Physiology 262, 265–284.CrossRefGoogle Scholar
Kogure, K., Scheinberg, P., Reinmuth, O.M., Fujishima, M. & Busto, R. (1970). Mechanisms of cerebral vasodilatation in hypoxia. Journal of Applied Physiology 29, 223–229.CrossRefGoogle ScholarPubMed
Krebs, H.A. (1972). The Pasteur effect and the relations between respiration and fermentation. Assays in Biochemistry 8, 1–34.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. (1990). Electrophysiological consequences of retinal hypoxia. Graefe's Archive for Clinical and Experimental Ophthalmology 228, 143–150.CrossRefGoogle ScholarPubMed
Linsenmeier, R.A. & Braun, R.D. (1992). Oxygen distribution and consumption in the cat retina during normoxia and hypoxemia. Journal of General Physiology 99, 177–197.CrossRefGoogle ScholarPubMed
Linsenmeier, R.A., Mines, A.H. & Steinberg, R.H. (1983). Effects of hypoxia and hypercapnia on the light peak and electroretinogram of the cat. Investigative Ophthalmology and Visual Science 24, 37–46.Google ScholarPubMed
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
Linsenmeier, R.A. & Steinberg, R.H. (1986). Mechanisms of hypoxic effects on the cat DC electroretinogram. Investigative Ophthalmology and Visual Science 27, 1385–1394.Google ScholarPubMed
Lovasik, J.V. & Kothe, A.C. (1989). Neural effects of transiently raised intraocular pressure: The scotopic and photopic flash electroretinogram. Clinical Vision Sciences 4, 313–321.Google Scholar
Lynch, R.M. & Paul, R.J. (1983). Compartmentalization of glycolytic and glycogenolytic metabolism in vascular smooth muscle. Science 222, 1344–1346.CrossRefGoogle ScholarPubMed
Macaluso, C., Onoe, S. & Niemeyer, G. (1992). Changes in glucose level affect rod function more than cone function in the isolated, perfused cat eye. Investigative Ophthalmology and Visual Science 33, 2798–2808.Google ScholarPubMed
Masland, R.H. & Ames, A. III. (1975). Dissociation of field potential from neuronal activity in the isolated retina: Failure of the b-wave with normal ganglion cell response. Journal of Neurobiology 6, 305–312.CrossRefGoogle ScholarPubMed
McFarland, R.A. (1972). Psychophysiological implications of life at altitude and including the role of oxygen in the process of aging. In Physiological Adaptations: Desert and Mountain, ed. Yousef, M.K., Horvath, S.M. & Bullard, R.W., pp. 157–181. London, England: Academic Press.CrossRefGoogle Scholar
McFarland, R.A. & Forbes, W.H. (1940). The effects of variations in the concentration of oxygen and of glucose on dark adaptation. Journal of General Physiology 24, 69–98.CrossRefGoogle ScholarPubMed
McFarland, R.A., Halperin, M.H. & Niven, J.I. (1944). Visual thresholds as an index of physiological imbalance during anoxia. American Journal of Physiology 142, 328–349.CrossRefGoogle Scholar
McFarland, R.A., Halperin, M.H. & Niven, J.I. (1945). Visual thresholds as an index of the modification of the effects of anoxia by glucose. American Journal of Physiology 144, 378–388.CrossRefGoogle Scholar
Newman, E.A. & Frishman, L.J. (1991). The b-wave. In Principles and Practice of Clinical Eiectrophysiology of Vision, ed. Heckenlively, J.R. & Arden, G.B., pp. 101–111. St. Louis, Missouri: Mosby.Google Scholar
Niemeyer, G. (1975). Function of the retina in the perfused eye. Documenta Ophthalmologica 39, 53–116.CrossRefGoogle ScholarPubMed
Niemeyer, G., Nagahara, K. & Demant, E. (1982). Effects of changes in arterial PO2 and PCO2 on the electroretinogram in the cat. Investigative Ophthalmology and Visual Science 23, 678–683.Google ScholarPubMed
Niemeyer, G. & Steinberg, R.H. (1984). Differential effects of PC02 and pH on the ERG and light peak of the perfused cat eye. Vision Research 24, 275–280.CrossRefGoogle Scholar
Noell, W.K. (1951). Site of asphyxial block in mammalian retinae. Journal of Applied Physiology 3, 489–500.CrossRefGoogle ScholarPubMed
Park, T.S., Gonzales, E.R., Shah, A.R. & Gidday, J.M. (1995). Hypoglycemia selectively abolishes hypoxic reactivity of pial arterioles in piglets: Role of adenosine. American Journal of Physiology 268, H871–H878.Google ScholarPubMed
Robson, J.G. & Frishman, L.J. (1995). Response linearity and kinetics of the cat retina: The bipolar cell component of the dark-adapted electroretinogram. Visual Neuroscience 12, 837–850.CrossRefGoogle ScholarPubMed
Rodieck, R.W. (1972). Components of the electroretinogram—a reappraisal. Vision Research 12, 773–780.CrossRefGoogle ScholarPubMed
Sannita, W.G., Balestra, V., Bon, Di G., Gambaro, M., Malfatto, L. & Rosadini, G. (1993). Spontaneous variations of flash-elec-troretinogram and retinal oscillatory potentials in healthy volunteers are correlated to serum glucose. Clinical Vision Sciences 8, 147–158.Google Scholar
Sieving, P.A., Frishman, L.J. & Steinberg, R.H. (1986). Scotopic threshold response of proximal retina in cat. Journal of Neurophysiology 56, 1049–1061.CrossRefGoogle ScholarPubMed
Sponsel, W.E., DePaul, K.L. & Zetlan, S.R. (1992). Retinal hemodynamic effects of carbon dioxide, hyperoxia, and mild hypoxia. Investigative Ophthalmology and Visual Science 33, 1864–1869.Google ScholarPubMed
Steinberg, R.H. (1987). Monitoring communications between photoreceptors and pigment epithelial cells: Effects of mild systemic hypoxia. Investigative Ophthalmology and Visual Science 28, 1888–1904.Google ScholarPubMed
Steinberg, R.H., Frishman, L.J. & Sieving, P.A. (1991). Negative components of the electroretinogram from proximal retina and photoreceptor. Progress in Retinal Research 10, 121–160.CrossRefGoogle Scholar
Winkler, B.S. (1995). A quantitative assessment of glucose metabolism in the isolated rat retina. In Les Séminaires ophtalmologiques d′IPSEN 6 Vision et adaptation, ed. Christen, Y., Doly, M. & Droy-Lefaix, M.T., pp. 78–96. Paris, France: Elsevier.Google Scholar
Yamamoto, F. & Steinberg, R.S. (1992). Effects of systemic hypoxia on pH outside rod photoreceptors in the cat retina. Experimental Eye Research 54, 699–709.CrossRefGoogle ScholarPubMed
Zhu, Y. & Gidday, J.M. (1996). Hypoglycemic hyperemia in retina of newborn pigs. Involvement of adenosine. Investigative Ophthalmology and Visual Science 37, 86–92.Google ScholarPubMed
Tornquist, P. & Alm, A. (1979). Retinal and choroidal contributions to retinal metabolism in vivo. A study in pigs. Acta Physiologica Scandinavica 106, 351–357.CrossRefGoogle ScholarPubMed
Van den Bos, G.C. (1968). L'electroretinogramme du chat en cas d'hypoxie. Journal de Physiologie (Paris) 60, 199–216.Google Scholar
Weiss, J.N. & Lamp, S.T. (1987). Glycolysis preferentially inhibits ATP-sensitive K+ channels in isolated guinea pig cardiac myocytes. Science 238, 67–69.CrossRefGoogle ScholarPubMed
Winkler, B.S. (1981). Glycolytic and oxidative metabolism in relation to retinal function. Journal of General Physiology 77, 667–692.CrossRefGoogle ScholarPubMed
Winkler, B.S. (1995). A quantitative assessment of glucose metabolism in the isolated rat retina. In Lés Siminaires ophtalmologiques d'IPSEN 6 Vision et adaptation, ed Christen, Y., Doly, M. and Droy-Lefaix, M.T., pp. 78–96. Paris, France: Elsevier.Google Scholar
Yamamoto, F. & Steinberg, R. S. (1992). Effects of systemic hypoxia on pH outside rod photoreceptors in the cat retina. Experimental Eye Research 54, 699–709.CrossRefGoogle ScholarPubMed
Zhu, Y. & Gidday, J. M. (1996). Hypoglycemic hyperemia in retina of newborn pigs. Involvement of adenosine. Investigative Ophthalmology and Visual Science 37, 86–92.Google ScholarPubMed