Hostname: page-component-586b7cd67f-g8jcs Total loading time: 0 Render date: 2024-11-23T11:12:04.111Z Has data issue: false hasContentIssue false

Origin of electroretinogram amplitude growth during light adaptation in pigmented rats

Published online by Cambridge University Press:  24 April 2006

BANG V. BUI
Affiliation:
Discoveries in Sight, Devers Eye Institute, Legacy Health System, Portland, Oregon Current Address: Department of Optometry and Vision Sciences, University of Melbourne, 3010, Victoria, Australia
BRAD FORTUNE
Affiliation:
Discoveries in Sight, Devers Eye Institute, Legacy Health System, Portland, Oregon

Abstract

We assessed the growth of the rat photopic electroretinogram (ERG) during light adaptation and the mechanisms underlying this process. Full field ERG responses were recorded from anesthetized adult Brown–Norway rats at each minute for 20 min of light adaptation (backgrounds: 1.8, 2.1, 2.4 log scotopic cd m−2). The rat photopic b-wave amplitude increased with duration of light adaptation and its width at 33% maximal amplitude narrowed (by ∼ 40 ms). These effects peaked 12–15 min after background onset. The narrowing of the b-wave reflected steepening of the b-wave recovery phase, with little change in the rising phase. OP amplitudes grew in proportion to the b-wave. Inhibition of inner retinal responses using TTX resulted in a greater relative growth of b-wave and OP amplitude compared with fellow control eyes, and delayed the change in recovery phase by ∼ 5 min. Inhibition of all ionotropic glutamate receptors with CNQX/D-AP7 delayed both rising and recovery phases equally (∼ 12 ms) without altering b-wave width or the time course of adaptation changes. These outcomes suggest that inner retinal light responses are not directly responsible for b-wave amplitude growth, but may contribute to the change in its recovery phase during adaptation. A TTX-sensitive mechanism may help to hasten this process. The cone a-wave was isolated using PDA/L-AP4 or CNQX/L-AP4. A-wave amplitude (35 ms after stimulus onset) also increased with time during light adaptation and reached a maximum (130 ± 29% above baseline) 12–15 min after background onset. B-wave amplitude growth in fellow control eyes closely followed the course and relative magnitude of cone a-wave amplitude growth. Hence, the increase of the cone response during light adaptation is sufficient to explain b-wave amplitude growth.

Type
Research Article
Copyright
2006 Cambridge University Press

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

Akula, J.D., Lybarsky, A.L., & Naarendorp, F. (2003). The sensitiy and spectral identity of the cones driving the b-wave of the rat electroretinogram. Visual Neuroscience 20, 109117.CrossRefGoogle Scholar
Arden, G.B. & Frumkes, T.E. (1986). Stimulation of rods can increase cone flicker ERGs in man. Vision Research 26, 711721.CrossRefGoogle Scholar
Armington, J.C. & Biersdorf, W.R. (1958). Long-term light adaptation of the human electroretinogram. Journal of Comparative Physiology and Psychology 51, 15.CrossRefGoogle Scholar
Biel, M., Seeliger, M., Pfeifer, A., Kohler, K., Gerstner, A., Ludwig, A., Jaissle, G., Fauser, S., Zrenner, E., & Hofmann, F. (1999). Selective loss of cone function in mice lacking the cyclic nucleotide-gated channel CNG3. Proceedings of the National Academy of Sciences of the U.S.A 96, 75537557.CrossRefGoogle Scholar
Boos, R., Schneider, H., & Wassle, H. (1993). Voltage- and transmitter-gated currents of AII-amacrine cells in a slice preparation of the rat retina. Journal of Neuroscience 13, 28742888.Google Scholar
Bui, B.V. & Fortune, B. (2004). Ganglion cell contributions to the rat full-field electroretinogram. Journal of Physiology 555(Pt 1), 153173.Google Scholar
Burian, H.M. (1954). Electric responses of the human visual system. Ama Arch Opthalmol 51, 509524.CrossRefGoogle Scholar
Burkhardt, D.A. (1994). Light adaptation and photopigment bleaching in cone photoreceptors in situ in the retina of the turtle. Journal of Neuroscience 14, 10911105.Google Scholar
Burns, M.E. & Baylor, D.A. (2001). Activation, deactivation, and adaptation in vertebrate photoreceptor cells. Annual Review of Neuroscience 24, 779805.CrossRefGoogle Scholar
Bush, R.A. & Sieving, P.A. (1994). A proximal retinal component in the primate photopic ERG a-wave. Investigative Ophthalmology and Visual Science 35, 635645.Google Scholar
Calvert, P.D., Govardovskii, V.I., Arshavsky, V.Y., & Makino, C.L. (2002). Two temporal phases of light adaptation in retinal rods. Journal of General Physiology 119, 129145.CrossRefGoogle Scholar
Calvert, P.D., Ho, T.W., LeFebvre, Y.M., & Arshavsky, V.Y. (1998). Onset of feedback reactions underlying vertebrate rod photoreceptor light adaptation. Journal of General Physiology 111, 3951.CrossRefGoogle Scholar
Djamgoz, M.B., Sekaran, S., Angotzi, A.R., Haamedi, S., Vallerga, S., Hirano, J., & Yamada, M. (2000). Light-adaptive role of nitric oxide in the outer retina of lower vertebrates: A brief review. Philos Transactions of the Royal Society B (London) 355, 11991203.CrossRefGoogle Scholar
Dowling, J.E. (1987). The Retina: An Approachable Part of the Brain. Cambridge, Mass.: Belknap-Harvard.
Dureau, P., Bonnel, S., Menasche, M., Dufier, J.L., & Abitbol, M. (2001). Quantitative analysis of intravitreal injections in the rat. Current Eye Research 22, 7477.CrossRefGoogle Scholar
Elias, R.V., Sezate, S.S., Cao, W., & McGinnis, J.F. (2004). Temporal kinetics of the light/dark translocation and compartmentation of arrestin and alpha-transducin in mouse photoreceptor cells. Molecular Vision 10, 672681.Google Scholar
Euler, T., Schneider, H., & Wassle, H. (1996). Glutamate responses of bipolar cells in a slice preparation of the rat retina. Journal of Neuroscience 16, 29342944.Google Scholar
Euler, T. & Wassle, H. (1995). Immunocytochemical identification of cone bipolar cells in the rat retina. Journal of Comparative Neurology 361, 461478.CrossRefGoogle Scholar
Fain, G.L., Matthews, H.R., Cornwall, M.C., & Koutalos, Y. (2001). Adaptation in vertebrate photoreceptors. Physiological Reviews 81, 117151.Google Scholar
Goto, Y., Tobimatsu, S., Shigematsu, J., Akazawa, K., & Kato, M. (1999). Properties of rat cone-mediated electroretinograms during light adaptation. Current Eye Research 19, 248253.CrossRefGoogle Scholar
Gouras, P. & MacKay, C.J. (1989). Growth in amplitude of the human cone electroretinogram with light adaptation. Investigative Ophthalmology and Visual Science 30, 625630.Google Scholar
Green, C.B. & Besharse, J.C. (2004). Retinal circadian clocks and control of retinal physiology. Journal of Biological Rhythms 19, 91102.CrossRefGoogle Scholar
Green, D.G. & Kapousta-Bruneau, N.V. (1999). A dissection of the electroretinogram from the isolated rat retina with microelectrodes and drugs. Visual Neuroscience 16, 727741.Google Scholar
Haamedi, S.N. & Djamgoz, M.B. (2002). Dopamine and nitric oxide control both flickering and steady-light-induced cone contraction and horizontal cell spinule formation in the teleost (carp) retina: Serial interaction of dopamine and nitric oxide. Journal of Comparative Neurology 449, 120128.CrossRefGoogle Scholar
Hartveit, E. (1999). Reciprocal synaptic interactions between rod bipolar cells and amacrine cells in the rat retina. Journal of Neurophysiology 81, 29232936.Google Scholar
He, S., Weiler, R., & Vaney, D.I. (2000). Endogenous dopaminergic regulation of horizontal cell coupling in the mammalian retina. Journal of Comparative Neurology 418, 3340.3.0.CO;2-J>CrossRefGoogle Scholar
Heynen, H., Wachtmeister, L., & van Norren, D. (1985). Origin of the oscillatory potentials in the primate retina. Vision Research 25, 13651373.CrossRefGoogle Scholar
Higgs, M.H. & Lukasiewicz, P.D. (2002). Activation of group II metabotropic glutamate receptors inhibits glutamate release from salamander retinal photoreceptors. Visual Neuroscience 19, 275281.CrossRefGoogle Scholar
Hood, D.C. (1972). Adaptational changes in the cone system of the isolated frog retina. Vision Research 12, 875888.CrossRefGoogle Scholar
Hood, D.C. & Birch, D.G. (1993). Human cone receptor activity: The leading edge of the a-wave and models of receptor activity. Visual Neuroscience 10, 857871.CrossRefGoogle Scholar
Hood, D.C. & Birch, D.G. (1995). Phototransduction in human cones measured using the a-wave of the ERG. Vision Research 35, 28012810.CrossRefGoogle Scholar
Hughes, A. (1979). A schematic eye for the rat. Vision Research 19, 569588.CrossRefGoogle Scholar
Jacobs, G.H., Fenwick, J.A., & Williams, G.A. (2001). Cone-based vision of rats for ultraviolet and visible lights. The Journal of Experimental Biology 204, 24392446.Google Scholar
Kennedy, M.J., Dunn, F.A., & Hurley, J.B. (2004). Visual pigment phosphorylation but not transducin translocation can contribute to light adaptation in zebrafish cones. Neuron 41, 915928.CrossRefGoogle Scholar
Kohl, S., Baumann, B., Broghammer, M., Jagle, H., Sieving, P., Kellner, U., Spegal, R., Anastasi, M., Zrenner, E., Sharpe, L.T., & Wissinger, B. (2000). Mutations in the CNGB3 gene encoding the beta-subunit of the cone photoreceptor cGMP-gated channel are responsible for achromatopsia (ACHM3) linked to chromosome 8q21. Human Molecular Genetics 9, 21072116.CrossRefGoogle Scholar
Kohl, S., Marx, T., Giddings, I., Jagle, H., Jacobson, S.G., Apfelstedt-Sylla, E., Zrenner, E., Sharpe, L.T., & Wissinger, B. (1998). Total colourblindness is caused by mutations in the gene encoding the alpha-subunit of the cone photoreceptor cGMP-gated cation channel. Nature Genetics 19, 257259.Google Scholar
Kondo, M., Miyake, Y., Piao, C.H., Tanikawa, A., Horiguchi, M., & Terasaki, H. (1999). Amplitude increase of the multifocal electroretinogram during light adaptation. Investigative Ophthalmology and Visual Science 40, 26332637.Google Scholar
Kondo, M. & Sieving, P.A. (2002). Post-photoreceptoral activity dominates primate photopic 32-Hz ERG for sine-, square-, and pulsed stimuli. Investigative Ophthalmology and Visual Science 43, 25002507.Google Scholar
Koulen, P., Kuhn, R., Wassle, H., & Brandstatter, J.H. (1999). Modulation of the intracellular calcium concentration in photoreceptor terminals by a presynaptic metabotropic glutamate receptor. Proceedings of the National Academy of Sciences of the U.S.A. 96, 99099914.CrossRefGoogle Scholar
Marshak, D.W. (2001). Synaptic inputs to dopaminergic neurons in mammalian retinas. In Progress in Brain Research: Concepts and Challenges in Retinal Biology; A Tribute to John E. Dowling, vol. 131, ed. Kolb, H., Ripps, H. & Wu, S., pp. 8391. Amsterdam: Elsevier.CrossRef
Miyake, Y., Horiguchi, M., Ota, I., & Shiroyama, N. (1987). Characteristic ERG-flicker anomaly in incomplete congenital stationary night blindness. Investigative Ophthalmology and Visual Science 28, 18161823.Google Scholar
Murayama, K. & Sieving, P.A. (1992). Different rates of growth of monkey and human photopic a-, b-, and d-waves suggest two sites of ERG light adaptation. Clinical Vision Sciences 7, 385392.Google Scholar
Nakatani, K., Tamura, T., & Yau, K.W. (1991). Light adaptation in retinal rods of the rabbit and two other nonprimate mammals. The Journal of General Physiology 97, 413435.CrossRefGoogle Scholar
Normann, R.A. & Perlman, I. (1979). The effects of background illumination on the photoresponses of red and green cones. Journal of Physiology 286, 491507.CrossRefGoogle Scholar
Paupoo, A.A., Mahroo, O.A., Friedburg, C., & Lamb, T.D. (2000). Human cone photoreceptor responses measured by the electroretinogram [correction of electoretinogram] a-wave during and after exposure to intense illumination. Journal of Physiology 529 Pt 2, 469482.Google Scholar
Peachey, N.S., Alexander, K.R., Derlacki, D.J., & Fishman, G.A. (1992a). Light adaptation, rods, and the human cone flicker ERG. Visual Neuroscience 8, 145150.Google Scholar
Peachey, N.S., Arakawa, K., Alexander, K.R., & Marchese, A.L. (1992b). Rapid and slow changes in the human cone electroretinogram during light and dark adaptation. Vision Research 32, 20492053.Google Scholar
Peachey, N.S., Goto, Y., al-Ubaidi, M.R., & Naash, M.I. (1993). Properties of the mouse cone-mediated electroretinogram during light adaptation. Neuroscience Letters 162, 911.CrossRefGoogle Scholar
Schnapf, J.L., Nunn, B.J., Meister, M., & Baylor, D.A. (1990). Visual transduction in cones of the monkey Macaca fascicularis. Journal of Physiology 427, 681713.CrossRefGoogle Scholar
Shiells, R.A. & Falk, G. (1994). Responses of rod bipolar cells isolated from dogfish retinal slices to concentration-jumps of glutamate. Visual Neuroscience 11, 11751183.CrossRefGoogle Scholar
Sieving, P.A., Murayama, K., & Naarendorp, F. (1994). Push-pull model of the primate photopic electroretinogram: A role for hyperpolarizing neurons in shaping the b-wave. Visual Neuroscience 11, 519532.CrossRefGoogle Scholar
Slaughter, M.M. & Miller, R.F. (1981). 2-amino-4-phosphonobutyric acid: A new pharmacological tool for retina research. Science 211, 182185.CrossRefGoogle Scholar
Sokolov, M., Lyubarsky, A.L., Strissel, K.J., Savchenko, A.B., Govardovskii, V.I., Pugh, E.N., Jr., & Arshavsky, V.Y. (2002). Massive light-driven translocation of transducin between the two major compartments of rod cells: A novel mechanism of light adaptation. Neuron 34, 95106.CrossRefGoogle Scholar
Szel, A. & Rohlich, P. (1992). Two cone types of rat retina detected by anti-visual pigment antibodies. Experimental Eye Research 55, 4752.CrossRefGoogle Scholar
Thoreson, W.B. & Witkovsky, P. (1999). Glutamate receptors and circuits in the vertebrate retina. Progress in Retinal Eye Research 18, 765810.CrossRefGoogle Scholar
Viswanathan, S., Frishman, L.J., & Robson, J.G. (2002). Inner-retinal contributions to the photopic sinusoidal flicker electroretinogram of macaques. Macaque photopic sinusoidal flicker ERG. Documenta Ophthalmologica 105, 223242.CrossRefGoogle Scholar
Viswanathan, S., Frishman, L.J., Robson, J.G., Harwerth, R.S., & Smith, E.L., 3rd. (1999). The photopic negative response of the macaque electroretinogram: reduction by experimental glaucoma. Investigative Ophthalmology and Visual Science 40, 11241136.Google Scholar
Weiler, R., He, S., & Vaney, D.I. (1999). Retinoic acid modulates gap junctional permeability between horizontal cells of the mammalian retina. European Journal of Neuroscience 11, 33463350.CrossRefGoogle Scholar
Weiler, R., Pottek, M., He, S., & Vaney, D.I. (2000). Modulation of coupling between retinal horizontal cells by retinoic acid and endogenous dopamine. Brain Research. Brain Research Reviews 32, 121129.CrossRefGoogle Scholar
Witkovsky, P. (2004). Dopamine and retinal function. Documenta Ophthalmologica 108, 1740.CrossRefGoogle Scholar
Witkovsky, P., Thoreson, W.B., & Tranchina, D. (2001). Transmission at the photoreceptor synapse. In Progress in Brain Research: Concepts and Challenges in Retinal Biology; A Tribute to John E. Dowling, vol. 131, ed. Kolb, H., Ripps, H. & Wu, S., pp. 145159. Amsterdam: Elsevier.CrossRef
Witkovsky, P., Veisenberger, E., Haycock, J.W., Akopian, A., Garcia-Espana, A., & Meller, E. (2004). Activity-dependent phosphorylation of tyrosine hydroxylase in dopaminergic neurons of the rat retina. Journal of Neuroscience 24, 42424249.Google Scholar
Xin, D. & Bloomfield, S.A. (1999). Dark- and light-induced changes in coupling between horizontal cells in mammalian retina. Journal of Comparative Neurology 405, 7587.3.0.CO;2-D>CrossRefGoogle Scholar
Xin, D. & Bloomfield, S.A. (2000). Effects of nitric oxide on horizontal cells in the rabbit retina. Visual Neuroscience 17, 799811.CrossRefGoogle Scholar
Xu, L., Ball, S.L., Alexander, K.R., & Peachey, N.S. (2003). Pharmacological analysis of the rat cone electroretinogram. Visual Neuroscience 20, 297306.CrossRefGoogle Scholar