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Test of the paired-flash electroretinographic method in mice lacking b-waves

Published online by Cambridge University Press:  19 July 2007

JENNIFER J. KANG DERWENT
Affiliation:
Lions of Illinois Eye Research Institute, Department of Ophthalmology and Visual Sciences, University of Illinois at Chicago, College of Medicine, Chicago, Illinois Department of Biomedical Engineering, Pritzker Institute of Biomedical Science and Engineering, Illinois Institute of Technology, Chicago, Illinois
SHANNON M. SASZIK
Affiliation:
College of Optometry, University of Houston, Houston, Texas Department of Ophthalmology, Northwestern University School of Medicine, Chicago, Illinois
HIDETAKA MAEDA
Affiliation:
College of Optometry, University of Houston, Houston, Texas Kobe University Medical School, Kobe, Japan
DEBORAH M. LITTLE
Affiliation:
Department of Neurology and Rehabilitation, and Center for Cognitive Medicine, University of Illinois at Chicago, College of Medicine, Chicago, Illinois
MACHELLE T. PARDUE
Affiliation:
Atlanta VA Medical Center, Decatur, Georgia Department of Ophthalmology, Emory University, Atlanta, Georgia
LAURA J. FRISHMAN
Affiliation:
College of Optometry, University of Houston, Houston, Texas
DAVID R. PEPPERBERG
Affiliation:
Lions of Illinois Eye Research Institute, Department of Ophthalmology and Visual Sciences, University of Illinois at Chicago, College of Medicine, Chicago, Illinois

Abstract

Previous studies of rod photoreceptors in vivo have employed a paired-flash electroretinographic (ERG) technique to determine rod response properties. To test whether absence versus presence of the ERG b-wave affects the photoreceptor response derived by the paired-flash method, we examined paired-flash-derived responses obtained from nob mice, a mutant strain with a defect in signal transduction between photoreceptors and ON bipolar cells that causes a lack of the b-wave. Normal littermates of the nob mice served as controls. The normalized amplitude-intensity relation of the derived response determined in nob mice at the near-peak time of 86 ms was similar to that determined for the controls. The full time course of the derived rod response was obtained for test flash strengths ranging from 0.11 to 17.38 scotopic cd s m−2 (sc cd s m−2). Time-course data obtained from nob and control mice exhibited significant but generally modest differences. With saturating test flash strengths, half-recovery times for the derived response of nobversus control mice differed by ∼60 ms or less about the combined (nob and control) average respective values. Time course data also were obtained before versus after intravitreal injection of l-2-amino-4-phosphonobutyrate (APB) (which blocks transmission from photoreceptors to depolarizing bipolar cells) and of cis 2,3-piperidine dicarboxylic acid (PDA) (which blocks transmission to OFF bipolar cells, and to horizontal, amacrine and ganglion cells). Neither APB nor PDA substantially affected derived responses obtained from nob or control mice. The results provide quantitative information on the effect of b-wave removal on the paired-flash-derived response in mouse. They argue against a substantial skewing effect of the b-wave on the paired-flash-derived response obtained in normal mice and are consistent with the notion that, to good approximation, this derived response represents the isolated flash response of the photoreceptors in both nob and normal mice.

Type
Research Article
Copyright
2007 Cambridge University Press

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References

REFERENCES

Bader, C.R., Bertrand, D. & Schwartz, E.A. (1982). Voltage-activated and calcium-activated currents studied in solitary rod inner segments from the salamander retina. Journal of Physiology 331, 253284.CrossRefGoogle Scholar
Bech-Hansen, N.T., Naylor, M.J., Maybaum, T.A., Sparkes, R.L., Koop, B., Birch, D.G., Bergen, A.A., Prinsen, C.F., Polomeno, R.C., Gal, A., Drack, A.V., Musarella, M.A., Jacobson, S.G., Young, R.S. & Weleber, R.G. (2000). Mutations in NYX, encoding the leucine-rich proteoglycan nyctalopin, cause X-linked complete congenital stationary night blindness. Nature Genetics 26, 319323.CrossRefGoogle Scholar
Birch, D.G., Hood, D.C., Nusinowitz, S. & Pepperberg, D.R. (1995). Abnormal activation and inactivation mechanisms of rod transduction in patients with autosomal dominant retinitis pigmentosa and the pro-23-his mutation. Investigative Ophthalmology & Visual Science 36, 16031614.Google Scholar
Bush, R.A. & Sieving, P.A. (1994). A proximal retinal component in the primate photopic ERG a-wave. Investigative Ophthalmology & Visual Science 35, 635645.Google Scholar
Calvert, P.D., Govardovskii, V.I., Krasnoperova, N., Anderson, R.E., Lem, J. & Makino, C.L. (2001). Membrane protein diffusion sets the speed of rod phototransduction. Nature 411, 9094.CrossRefGoogle Scholar
Candille, S.I., Pardue, M.T., McCall, M.A., Peachey, N.S. & Gregg, R.G. (1999). Localization of the mouse nob (no b-wave) gene to the centromeric regions of the X chromosome. Investigative Ophthalmology & Visual Science 40, 27482751.Google Scholar
Chen, C.K., Burns, M.E., He, W., Wensel, T.G., Baylor, D.A. & Simon, M.I. (2000). Slowed recovery of rod photoresponse in mice lacking the GTPase accelerating protein RGS9-1. Nature 403, 557560.CrossRefGoogle Scholar
Dawson, W.W., Trick, G.L. & Litzkow, C.A. (1979). Improved electrode for electroretinography. Investigative Ophthalmology & Visual Science 18, 988991.Google Scholar
Dong, C.-J. & Hare, W.A. (2000). Contribution to the kinetics and amplitude of the electroretinogram b-wave by third-order retinal neurons in the rabbit retina. Vision Research 40, 579589.CrossRefGoogle Scholar
Friedburg, C., Thomas, M.M. & Lamb, T.D. (2001). Time course of the flash response of dark- and light-adapted human rod photoreceptors derived from the electroretinogram. Journal of Physiology 534, 217242.CrossRefGoogle Scholar
Frishman, L.J. (2006). Origins of the electroretinogram. In Principles and Practice of Clinical Electrophysiology of Vision, 2nd edition, ed. Heckenlively, J.R. & Arden, G.B., pp. 139183. Cambridge, MA: MIT Press.
Gregg, R.G., Mukhopadhyay, S., Candille, S.I., Ball, S.L., Pardue, M.T., McCall, M.A. & Peachey, N.S. (2003). Identification of the gene and the mutation responsible for the mouse nob phenotype. Investigative Ophthalmology & Visual Science 44, 378384.CrossRefGoogle Scholar
Hetling, J.R. & Pepperberg, D.R. (1999). Sensitivity and kinetics of mouse rod flash responses determined in vivo from paired-flash electroretinograms. Journal of Physiology 516, 593609.CrossRefGoogle Scholar
Kang Derwent, J.J. & Linsenmeier, R.A. (2001). Intraretinal analysis of the a-wave of the electroretinogram (ERG) in dark-adapted intact cat retina. Visual Neuroscience 18, 353363.CrossRefGoogle Scholar
Kang Derwent, J.J., Qtaishat, N.M. & Pepperberg, D.R. (2002). Excitation and desensitization of mouse rod photoreceptors in vivo following bright adapting light. Journal of Physiology 541, 201218.CrossRefGoogle Scholar
Krishna, V.R., Alexander, K.R. & Peachey, N.S. (2002). Temporal properties of the mouse cone electroretinogram. Journal of Neurophysiology 87, 4248.CrossRefGoogle Scholar
Krispel, C.M., Chen, C.K., Simon, M.I. & Burns, M.E. (2003). Novel form of adaptation in mouse retinal rods speeds recovery of phototransduction. Journal of General Physiology 122, 703712.CrossRefGoogle Scholar
Lyubarsky, A.L. & Pugh, E.N., Jr. (1996). Recovery phase of the murine rod photoresponse reconstructed from electroretinographic recordings. Journal of Neuroscience 16, 563571.Google Scholar
Lyubarsky, A.L., Falsini, B., Pennesi, M.E., Valentini, P. & Pugh, E.N., Jr. (1999). UV- and midwave-sensitive cone-driven retinal responses of the mouse: A possible phenotype for coexpression of cone photopigments. Journal of Neuroscience 19, 442455.Google Scholar
Pardue, M.T., McCall, M.A., LaVail, M.M., Gregg, R.G. & Peachey, N.S. (1998). A naturally occurring mouse model of X-linked congenital stationary night blindness. Investigative Ophthalmology & Visual Science 39, 24432449.Google Scholar
Pardue, M.T., Ball, S.L., Mukhopadhyay, S., Candille, S.I., McCall, M.A., Gregg, R.G. & Peachey, N.S. (2001). nob, A mouse model of CSNB1. In New Insights into Retinal Degenerative Diseases, eds. Hollyfield, J.G., Anderson, R.E. & LaVail, M.M., pp. 319328. New York: Kluwer/Plenum Press.CrossRef
Pepperberg, D.R. (2006). Paired-flash ERG analysis of rod phototransduction and adaptation. In Principles and Practice of Clinical Electrophysiology of Vision, 2nd edition, ed. Heckenlively, J.R. & Arden, G.B., pp. 519532. Cambridge, MA: MIT Press.
Pepperberg, D.R., Birch, D.G. & Hood, D.C. (1997). Photoresponses of human rods in vivo derived from paired-flash electroretinograms. Visual Neuroscience 14, 7382.CrossRefGoogle Scholar
Pugh, E.N., Jr., Falsini, B. & Lyubarsky, A. (1998). The origin of the major rod- and cone-driven components of the rodent electroretinogram and the effects of age and light-rearing history on the magnitude of these components. In Photostasis and Related Phenomena, ed. Williams, T.P. & Thistle, A.B., pp. 93128. New York: Plenum Press.CrossRef
Pusch, C.M., Zeitz, C., Brandau, O., Pesch, K., Achatz, H., Feil, S., Scharfe, C., Maurer, J., Jacobi, F.K., Pinckers, A., Andreasson, S., Hardcastle, A., Wissinger, B., Berger, W. & Meindl, A. (2000). The complete form of X-linked congenital stationary night blindness is caused by mutations in a gene encoding a leucine-rich repeat protein. Nature Genetics 26, 324327.CrossRefGoogle Scholar
Reiser, M.A., Williams, T.P. & Pugh, E.N., Jr. (1996). The effect of light history on the aspartate-isolated fast-PIII responses of the albino rat retina. Investigative Ophthalmology & Visual Science 37, 221229.Google Scholar
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, 837850.CrossRefGoogle Scholar
Robson, J.G. & Frishman, L.J. (1996). Photoreceptor and bipolar-cell contributions to the cat electroretinogram: A kinetic model for the early part of the flash response. Journal of the Optical Society of America A 13, 613622.CrossRefGoogle Scholar
Robson, J.G. & Frishman, L.J. (1999). Dissecting the dark-adapted electroretinogram. Documenta Ophthalmologica 95, 187215.Google Scholar
Robson, J.G. & Frishman, L.J. (2004). Sampling and interpolation of the a-wave of the electroretinogram. Documenta Ophthalmologica 108, 171179.CrossRefGoogle Scholar
Robson, J.G., Saszik, S.M., Ahmed, J. & Frishman, L.J. (2003). Rod and cone contributions to the a-wave of the electroretinogram of the macaque. Journal of Physiology 547, 509530.CrossRefGoogle Scholar
Saszik, S.M., Robson, J.G. & Frishman, L.J. (2002). The scotopic threshold response of the dark-adapted electroretinogram of the mouse. Journal of Physiology 543, 899916.CrossRefGoogle Scholar
Schneeweis, D.M. & Schnapf, J.L. (2000). Noise and light adaptation in rods of the macaque monkey. Visual Neuroscience 17, 659666.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
Silva, G.A., Hetling, J.R. & Pepperberg, D.R. (2001). Dynamic and steady-state light adaptation of mouse rod photoreceptors in vivo. Journal of Physiology 534, 203216.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
Wakabayashi, K., Gieser, J. & Sieving, P.A. (1988). Aspartate separation of the scotopic threshold response (STR) from the photoreceptor a-wave of the cat and monkey ERG. Investigative Ophthalmology & Visual Science 29, 16151622.Google Scholar
Wu, J., Marmorstein, A.D., Kofuji, P. & Peachey, N.S. (2004a). Contribution of Kir4.1 to the mouse electroretinogram. Molecular Vision 10, 650654.Google Scholar
Wu, J., Peachey, N.S. & Marmorstein, A.D. (2004b). Light-evoked responses of the mouse retinal pigment epithelium. Journal of Neurophysiology 91, 11341142.Google Scholar
Xu, J., Dodd, R.L., Makino, C.L., Simon, M.I., Baylor, D.A. & Chen, J. (1997). Prolonged photoresponses in transgenic mouse rods lacking arrestin. Nature 389, 505509.CrossRefGoogle Scholar