Hostname: page-component-8448b6f56d-gtxcr Total loading time: 0 Render date: 2024-04-23T17:14:46.284Z Has data issue: false hasContentIssue false
  • English
  • Français

The nob2 mouse, a null mutation in Cacna1f: Anatomical and functional abnormalities in the outer retina and their consequences on ganglion cell visual responses

Published online by Cambridge University Press:  09 March 2006

BO CHANG ,
JOHN R. HECKENLIVELY ,
PHILIPPA R. BAYLEY ,
NICHOLAS C. BRECHA ,
MURIEL T. DAVISSON ,
NORM L. HAWES ,
ARLENE A. HIRANO ,
RONALD E. HURD ,
AKIHIRO IKEDA  and
BRITT A. JOHNSON
...Show all authors
BO CHANG
Affiliation:
The Jackson Laboratory, Bar Harbor, Maine
JOHN R. HECKENLIVELY
Affiliation:
Jules Stein Eye Institute, University of California at Los Angeles, Los Angeles, California W.K. Kellogg Eye Center, University of Michigan, Ann Arbor, Michigan
PHILIPPA R. BAYLEY
Affiliation:
Neurological Sciences Institute, Oregon Health and Science University, Beaverton, Oregon
NICHOLAS C. BRECHA
Affiliation:
Jules Stein Eye Institute, University of California at Los Angeles, Los Angeles, California Departments of Neurobiology and Medicine, Geffen School of Medicine, University of California at Los Angeles, Los Angeles, California Research Service, VAGLAHS, Los Angeles, California
MURIEL T. DAVISSON
Affiliation:
The Jackson Laboratory, Bar Harbor, Maine
NORM L. HAWES
Affiliation:
The Jackson Laboratory, Bar Harbor, Maine
ARLENE A. HIRANO
Affiliation:
Jules Stein Eye Institute, University of California at Los Angeles, Los Angeles, California Departments of Neurobiology and Medicine, Geffen School of Medicine, University of California at Los Angeles, Los Angeles, California Research Service, VAGLAHS, Los Angeles, California
RONALD E. HURD
Affiliation:
The Jackson Laboratory, Bar Harbor, Maine
AKIHIRO IKEDA
Affiliation:
Department of Genetics, University of Wisconsin, Madison, Wisconsin
BRITT A. JOHNSON
Affiliation:
Department of Genetics, University of Wisconsin, Madison, Wisconsin
MAUREEN A. MCCALL
Affiliation:
Department of Psychological and Brain Sciences, University of Louisville, Louisville, Kentucky The Center for Genetics and Molecular Medicine, University of Louisville, Louisville, Kentucky
CATHERINE W. MORGANS
Affiliation:
Neurological Sciences Institute, Oregon Health and Science University, Beaverton, Oregon
STEVE NUSINOWITZ
Affiliation:
Jules Stein Eye Institute, University of California at Los Angeles, Los Angeles, California
NEAL S. PEACHEY
Affiliation:
Research Service, Cleveland VAMC, Cleveland, Ohio Cole Eye Institute, Cleveland Clinic Foundation, Cleveland, Ohio
DENNIS S. RICE
Affiliation:
Lexicon Genetics, The Woodlands, Texas
KIRSTAN A. VESSEY
Affiliation:
Department of Psychological and Brain Sciences, University of Louisville, Louisville, Kentucky
RONALD G. GREGG
Affiliation:
The Center for Genetics and Molecular Medicine, University of Louisville, Louisville, Kentucky Department of Biochemistry and Molecular Biology, University of Louisville, Louisville, Kentucky
Get access Rights & Permissions [Opens in a new window]

Abstract

Glutamate release from photoreceptor terminals is controlled by voltage-dependent calcium channels (VDCCs). In humans, mutations in the Cacna1f gene, encoding the α1F subunit of VDCCs, underlie the incomplete form of X-linked congenital stationary night blindness (CSNB2). These mutations impair synaptic transmission from rod and cone photoreceptors to bipolar cells. Here, we report anatomical and functional characterizations of the retina in the nob2 (no b-wave 2) mouse, a naturally occurring mutant caused by a null mutation in Cacna1f. Not surprisingly, the b-waves of both the light- and dark-adapted electroretinogram are abnormal in nob2 mice. The outer plexiform layer (OPL) is disorganized, with extension of ectopic neurites through the outer nuclear layer that originate from rod bipolar and horizontal cells, but not from hyperpolarizing bipolar cells. These ectopic neurites continue to express mGluR6, which is frequently associated with profiles that label with the presynaptic marker Ribeye, indicating potential points of ectopic synapse formation. However, the morphology of the presynaptic Ribeye-positive profiles is abnormal. While cone pedicles are present their morphology also appears compromised. Characterizations of visual responses in retinal ganglion cells in vivo, under photopic conditions, demonstrate that ON-center cells have a reduced dynamic range, although their basic center-surround organization is retained; no alteration in the responses of OFF-center cells was evident. These results indicate that nob2 mice are a valuable model in which to explore the pathophysiological mechanisms associated with Cacna1f mutations causing CSNB2, and the subsequent effects on visual information processing. Further, the nob2 mouse represents a model system in which to define the signals that guide synapse formation and/or maintenance in the OPL.

Keywords

Bipolar and horizontal cellsCongenital stationary night blindnessElectroretinogramON- and OFF-pathwaysVoltage-dependent calcium channel
Type
Research Article
Information
Visual Neuroscience , Volume 23 , Issue 1 , January 2006 , pp. 11 - 24
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

Ball, S.L., McEnery, M., & Gregg, R.G. (2004). Voltage gated calcium channel subunit composition and distribution in the retina. Investigative Ophthalmology and Visual Science 45, E-abstract 5423.Google Scholar
Ball, S.L., Pardue, M.T., McCall, M.A., Gregg, R.G., & Peachey, N.S. (2003). Immunohistochemical analysis of the outer plexiform layer in the nob mouse shows no abnormalities. Visual Neuroscience 20, 267–272.CrossRefGoogle Scholar
Ball, S.L., Powers, P.A., Shin, H.S., Morgans, C.W., Peachey, N.S., & Gregg, R.G. (2002). Role of the β2 subunit of voltage-dependent calcium channels in the retinal outer plexiform layer. Investigative Ophthalmology and Visual Science 43, 1595–1603.Google Scholar
Barthel, L. & Raymond, P.A. (1990). Improved method for obtaining 3 μm cryosections for immunocytochemistry. Journal of Histochemistry and Cytochemistry 38, 1383–1388.CrossRefGoogle Scholar
Baumann, L., Gerstner, A., Zong, X., Biel, M., & Wahl-Schott, C. (2004). Functional characterization of the L-type Ca2+ channel Cav1.4 from mouse retina. Investigative Ophthalmology and Visual Science 45, 708–713.Google Scholar
Bech-Hansen, N.T., Naylor, M.J., Maybaum, T.A., Pearce, W.G., Koop, B., Fishman, G.A., Mets, M., Musarella, M.A., & Boycott, K.M. (1998). Loss-of-function mutations in a calcium-channel α1-subunit gene in Xp11.23 cause incomplete X-linked congenital stationary night blindness. Nature Genetics 19, 264–267.Google Scholar
Blanks, J.C., Adinolfi, A.M., & Lolley, R.N. (1974). Synaptogenesis in the photoreceptor terminal of the mouse retina. Journal of Comparative Neurology 156, 81–93.CrossRefGoogle Scholar
Blanks, J.C. & Johnson, L.V. (1983). Selective lectin binding of the developing mouse retina. Journal of Comparative Neurology 221, 31–41.CrossRefGoogle Scholar
Boycott, K.M., Maybaum, T.A., Naylor, M.J., Weleber, R.G., Robitaille, J., Miyake, Y., Bergen, A.A.B., Pierpont, M.E., Pearce, W.G., & Bech-Hansen, N.T. (2001). A summary of 20 CACNA1F mutations identified in 36 families with incomplete X-linked congenital stationary night blindness, and characterization of splice variants. Human Genetics 108, 91–97.CrossRefGoogle Scholar
Buffone, G.J. & Darlington, G.J. (1985). Isolation of DNA from biological specimens without extraction with phenol. Clinical Chemistry 31, 164–165.Google Scholar
Chang, B., Hawes, N.L., Hurd, R.E., Davisson, M.T., Nusinowitz, S., & Heckenlively, J.R. (2002). Retinal degeneration mutants in the mouse. Vision Research 42, 517–525.CrossRefGoogle Scholar
Chang, S. & De Camilli, P. (2001). Glutamate regulates actin-based motility in axonal filopodia. Nature Neuroscience 4, 787–793.CrossRefGoogle Scholar
Claes, E., Seeliger, M., Michalakis, S., Biel, M., Humphries, P., & Haverkamp, S. (2004). Morphological characterization of the retina of the CNGA3(-/-)Rho(-/-) mutant mouse lacking functional cones and rods. Investigative Ophthalmology and Visual Science 45, 2039–2048.CrossRefGoogle Scholar
Copenhagen, D.R. & Jahr, C.E. (1989). Release of endogenous excitatory amino acids from turtle photoreceptors. Nature 341, 536–539.CrossRefGoogle Scholar
Curtis, J. & Finkbeiner, S. (1999). Sending signals from the synapse to the nucleus: Possible roles for CaMK, Ras/ERK, and SAPK pathways in the regulation of synaptic plasticity and neuronal growth. Journal of Neuroscience Research 58, 88–95.3.0.CO;2-R>CrossRefGoogle Scholar
Dhingra, A., Jiang, M., Wang, T.L., Lyubarsky, A., Savchenko, A., Bar-Yehuda, T., Sterling, P., Birnbaumer, L., & Vardi, N. (2002). Light response of retinal ON bipolar cells requires a specific splice variant of GαO. Journal of Neuroscience 22, 4878–4884.Google Scholar
Dhingra, A., Lyubarsky, A., Jiang, M., Pugh, E.N., Jr., Birnbaumer, L., Sterling, P., & Vardi, N. (2000). The light response of ON bipolar neurons requires GαO. Journal of Neuroscience 20, 9053–9058.Google Scholar
Dick, O., tom Dieck, S., Altrock, W.D., Ammermüller, J., Weiler, R., Garner, C.C., Gundelfinger, E.D., & Brandstätter, J.H. (2003). The presynaptic active zone protein bassoon is essential for photoreceptor ribbon synapse formation in the retina. Neuron 37, 775–786.CrossRefGoogle Scholar
Engert, F. & Bonhoeffer, T. (1999). Dendritic spine changes associated with hippocampal long-term synaptic plasticity. Nature 399, 66–70.Google Scholar
Fishman, G.A., Birch, D.G., Holder, G.E., & Brigell, M.G. (2001). Electrophysiologic Testing in Disorders of the Retina, Optic Nerve and Visual Pathway. Second edition. San Francisco, California: American Academy of Ophthalmology.
Ghosh, A. & Greenberg, M.E. (1995). Calcium signaling in neurons: Molecular mechanisms and cellular consequences. Science 268, 239–247.CrossRefGoogle Scholar
Grady, E.F., Baluk, P., Böhm, S., Gamp, P.D., Wong, H., Payan, D.G., Ansel, J., Portbury, A.L., Furness, J.B., McDonald, D.M., & Bunnett, N.W. (1996). Characterization of antisera specific to NK1, NK2, and NK3 neurokinin receptors and their utilization to localize receptors in the rat gastrointestinal tract. Journal of Neuroscience 16, 6975–6986.Google Scholar
Greenstein, V.C., Hood, D.C., Siegel, I.M., & Carr, R.E. (1988). A possible use of rod–cone interaction in congenital stationary nightblindness. Clinical Vision Sciences 3, 69–74.Google Scholar
Greferath, U., Grünert, U., & Wässle, H. (1990). Rod bipolar cells in the mammalian retina show protein kinase C-like immunoreactivity. Journal of Comparative Neurology 301, 433–442.CrossRefGoogle Scholar
Gregg, R.G., Lukasiewicz, P.D., Peachey, N.S., Sagdullaev, B.T., & McCall, M.A. (2003b). Nyctalopin is required for signaling through depolarizing bipolar cells in the murine retina. Investigative Ophthalmology and Visual Science 44, ARVO E-abstract 4180.Google Scholar
Gregg, R.G., McCall, M.A., & Peachey, N.S. (2005). Bipolar specific expression of nyctalopin fusion gene rescues no b-wave phenotype in nob mice. Investigative Ophthalmology and Visual Science 46, ARVO E-abstract 3554.Google Scholar
Gregg, R.G., Mukhopadhyay, S., Candille, S.I., Ball, S.L., Pardue, M.T., McCall, M.A., & Peachey, N.S. (2003a). Identification of the gene and the mutation responsible for the nob (no b-wave) phenotype. Investigative Ophthalmology and Visual Science 44, 378–384.Google Scholar
Gregg, R.G., Read, D.S., Peachey, N.S., Pardue, M.T., & McCall, M.A. (2002). Photoreceptor voltage dependent calcium channels but not bipolar cell activity is required for normal ribbon synapse formation. Investigative Ophthalmology and Visual Science 43, ARVO E-abstract 831.Google Scholar
Haeseleer, F., Imanishi, Y., Maeda, T., Possin, D.E., Maeda, A., Lee, A., Rieke, F., & Palczewski, K. (2004). Essential role of Ca2+-binding protein 4, a Cav1.4 channel regulator, in photoreceptor synaptic function. Nature Neuroscience 7, 1079–1087.Google Scholar
Haverkamp, S., Ghosh, K.K., Hirano, A.A., & Wässle, H. (2003). Immunocytochemical description of five bipolar cell types of the mouse retina. Journal of Comparative Neurology 455, 463–476.CrossRefGoogle Scholar
Haverkamp, S. & Wässle, H. (2000). Immunocytochemical analysis of the mouse retina. Journal of Comparative Neurology 424, 1–23.Google Scholar
Hemara-Wahanui, A., Berjukow, S., Hope, C.I., Dearden, P.K., Wu, S.B., Wilson-Wheeler, J., Sharp, D.M., Lundon-Treweek, P., Clover, G.M., Hoda, J.C., Striessnig, J., Marksteiner, R., Hering, S., & Maw, M.A. (2005). A CACNA1F mutation identified in an X-linked retinal disorder shifts the voltage dependence of Cav1.4 channel activation. Proceedings of the National Academy of Sciences of the U.S.A. 102, 7553–7558.CrossRefGoogle Scholar
Hirano, A.A. & Brecha, N.C. (2002). Expression of the neurokinin-3 (NK3) receptor in off-type cone bipolar cells in mouse retina. Investigative Ophthalmology and Visual Science 43, ARVO E-abstract No. 736.Google Scholar
Hoda, J.-C., Zaghetto, F., Koschak, A., & Striessnig, J. (2005). Congenital stationary night blindness type 2 mutations S229P, G369D, L1068P, and W1440X alter channel gating or functional expression of Cav1.4 L-type Ca2+ channels. Journal of Neuroscience 25, 252–259.Google Scholar
Hood, D.C. & Birch, D.G. (1992). A computational model of the amplitude and implicit time of the b-wave of the human ERG. Visual Neuroscience 8, 107–126.CrossRefGoogle Scholar
Hope, C.I., Sharp, D.M., Hemara-Wahanui, A., Sissingh, J.I., Lundon, P., Mitchell, E.A., Maw, M.A., & Clover, G.M. (2005). Clinical manifestations of a unique X-linked retinal disorder in a large New Zealand family with a novel mutation in CACNA1F, the gene responsible for CSNB2. Clinical and Experimental Ophthalmology 33, 129–136.CrossRefGoogle Scholar
Jalkanen, R., Mantyjarvi, M., Tobias, R., Alitalo, T., & Bech-Hansen, N.T. (2004). X-linked cone–rod dystrophy (COD4) in a Finnish family is caused by mutation in CACNA1F. American Journal of Human Genetics 75, A2593.Google Scholar
Jeon, C.J., Strettoi, E., & Masland, R.H. (1998). The major cell populations of the mouse retina. Journal of Neuroscience 18, 8936–8946.Google Scholar
Kofuji, P., Ceelen, P., Zahs, K.R., Surbeck, L.W., Lester, H.A., & Newman, E.A. (2000). Genetic inactivation of an inwardly rectifying potassium channel (Kir4.1 subunit) in mice: Phenotypic impact in retina. Journal of Neuroscience 20, 5733–5740.Google Scholar
Koschak, A., Reimer, D., Walter, D., Hoda, J.C., Heinzle, T., Grabner, M., & Striessnig, J. (2003). Cav1.4 α1 subunits can form slowly inactivating dihydropyridine-sensitive L-type Ca2+ channels lacking Ca2+-dependent inactivation. Journal of Neuroscience 23, 6041–6049.Google Scholar
Lamb, T.D. (1996). Ida Mann Lecture. Transduction in human photoreceptors. Australian and New Zealand Journal of Ophthalmology 24, 105–110.CrossRefGoogle Scholar
Li, C., Cheng, M., Yang, H., Peachey, N.S., & Naash, M.I. (2001). Age-related changes in the mouse outer retina. Optometry and Vision Science 78, 425–430.CrossRefGoogle Scholar
Maletic-Savatic, M., Malinow, R., & Svoboda, K. (1999). Rapid dendritic morphogenesis in CA1 hippocampal dendrites induced by synaptic activity. Science 283, 1923–1927.CrossRefGoogle Scholar
Mansergh, F., Orton, N.C., Vessey, J.P., Lalonde, M.R., Stell, W.K., Tremblay, F., Barnes, S., Rancourt, D.E., & Hansen, N.T. (2005). Mutation of the calcium channel gene Cacna1f disrupts calcium signaling, synaptic transmission and cellular organization in mouse retina. Human Molecular Genetics 14, 3035–3046.CrossRefGoogle Scholar
Massey, S.C. (1990). Cell types using glutamate as a neurotransmitter in the vertebrate retina. Progress in Retinal Research 9, 399–425.CrossRefGoogle Scholar
Masu, M., Iwakabe, H., Tagawa, Y., Miyoshi, T., Yamashita, M., Fukuda, Y., Sasaki, H., Hiroi, K., Nakamura, Y., Shigemoto, R., Takada, M., Nakamura, K., Nakao, K., Katsuki, M., & Nakanishi, S. (1995). Specific deficit of the ON response in visual transmission by targeted disruption of the mGluR6 gene. Cell 80, 757–765.CrossRefGoogle Scholar
McCall, M.A., Lukasiewicz, P.D., Gregg, R.G., & Peachey, N.S. (2002). Elimination of the ρ1 subunit abolishes GABA(C) receptor expression and alters visual processing in the mouse retina. Journal of Neuroscience 22, 4163–4174.Google Scholar
McRory, J., Hamid, J., Doering, C., Garcia, E., Parker, R., Hamming, K., Chen, L., Hildebrand, M., Beedle, A., Feldcamp, L., Zamponi, G., & Snutch, T. (2004). The CACNA1F gene encodes an L-type calcium channel with unique biophysical properties and tissue distribution. Journal of Neuroscience 24, 1707–1718.Google Scholar
Miyake, Y., Yagasaki, K., Horiguchi, M., Kawase, Y., & Kanda, T. (1986). Congenital stationary night blindness with negative electroretinogram. A new classification. Archives of Ophthalmology 104, 1013–1020.Google Scholar
Morgans, C.W. (1999). Calcium channel heterogeneity among cone photoreceptors in the tree shrew retina. European Journal of Neuroscience 11, 2989–2993.CrossRefGoogle Scholar
Morgans, C.W., Bayley, P.R., Oesch, N.W., Ren, G., Akileswaran, L., & Taylor, W.R. (2005). Photoreceptor calcium channels: Insight from night blindness. Visual Neuroscience 22, 561–568.CrossRefGoogle Scholar
Morgans, C.W., Gaughwin, P., & Maleszka, R. (2001). Expression of the α1F calcium channel subunit by photoreceptors in the rat retina. Molecular Vision 7, 202–209.Google Scholar
Mumm, J.S., Godinho, L., Morgan, J.L., Oakley, D.M., Schroeter, E.H., & Wong, R.O. (2005). Laminar circuit formation in the vertebrate retina. Progress in Brain Research 147, 155–169.CrossRefGoogle Scholar
Nachman-Clewner, M., St. Jules, R., & Townes-Anderson, E. (1999). L-type calcium channels in the photoreceptor ribbon synapse: Localization and role in plasticity. Journal of Comparative Neurology 415, 1–16.Google Scholar
Nakamura, M., Ito, S., Piao, C.-H., Terasaki, H., & Miyake, Y. (2003). Retinal and optic disc atrophy associated with a CACNA1F mutation in a Japanese family. Archives of Ophthalmology 121, 1028–1033.CrossRefGoogle Scholar
Nusinowitz, S., Nguyen, L., Radu, R., Kashani, Z., Farber, D., & Danciger, M. (2003). Electroretinographic evidence for altered phototransduction gain and slowed recovery from photobleaches in albino mice with a MET450 variant in RPE65. Experimental Eye Research 77, 627–638.CrossRefGoogle Scholar
Pardue, M.T., Ball, S.L., 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, ed. Anderson, R.E., LaVail, M.M. & Hollyfield, J.G., pp. 319–328. New York: Kluwer Academic/Plenum.CrossRef
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 and Visual Science 39, 2443–2449.Google Scholar
Passafaro, M., Nakagawa, T., Sala, C., & Sheng, M. (2003). Induction of dendritic spines by an extracellular domain of AMPA receptor subunit GluR2. Nature 424, 677–681.CrossRefGoogle Scholar
Peichl, L. & González-Soriano, J. (1994). Morphological types of horizontal cell in rodent retinae: A comparison of rat, mouse, gerbil, and guinea pig. Visual Neuroscience 11, 501–517.CrossRefGoogle Scholar
Pugh, E.N., Jr. & Lamb, T.D. (1993). Amplification and kinetics of the activation steps in phototransduction. Biochimica Biophysica Acta 1141, 111–149.CrossRefGoogle Scholar
Redburn, D.A. & Rowe-Rendleman, C. (1996). Developmental neurotransmitters. Signals for shaping neuronal circuitry. Investigative Ophthalmology and Visual Science 37, 1479–1482.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, 837–850.CrossRefGoogle Scholar
Robson, J.G. & Frishman, L.J. (1998). Dissecting the dark-adapted electroretinogram. Documenta Ophthalmologica 95, 187–215.CrossRefGoogle Scholar
Rosen, L.B., Ginty, D.D., Weber, M.J., & Greenberg, M.E. (1994). Membrane depolarization and calcium influx stimulate MEK and MAP kinase via activation of Ras. Neuron 12, 1207–1221.CrossRefGoogle Scholar
Sagdullaev, B.T., DeMarco, P.J., & McCall, M.A. (2004). Improved contact lens electrode for corneal ERG recordings in mice. Documenta Ophthalmologica 108, 181–184.CrossRefGoogle Scholar
Sagdullaev, B.T. & McCall, M.A. (2005). Stimulus size and intensity alter fundamental response properties of mouse retinal ganglion cells in vivo. Visual Neuroscience 22, 649–659.CrossRefGoogle Scholar
Schmitz, F., Konigstorfer, A., & Sudhof, T.C. (2000). RIBEYE, a component of synaptic ribbons: A protein's journey through evolution provides insight into synaptic ribbon function. Neuron 28, 857–872.CrossRefGoogle Scholar
Schmitz, Y. & Witkovsky, P. (1997). Dependence of photoreceptor glutamate release on a dihydropyridine-sensitive Ca2+ channel. Neuroscience 78, 1209–1216.CrossRefGoogle Scholar
Sharma, S., Ball, S.L., & Peachey, N.S. (2005). Pharmacological studies of the mouse cone electroretinogram. Visual Neuroscience 22, 631–636.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, 519–532.CrossRefGoogle Scholar
Sterling, P. & Matthews, G. (2005). Structure and function of ribbon synapses. TINS 28, 20–29.CrossRefGoogle Scholar
Strom, T.M., Nyakatura, G., Apfelstedt-Sylla, E., Hellebrand, H., Lorenz, B., Weber, B.H., Wutz, K., Gutwillinger, N., Rüther, K., Drescher, B., Sauer, C., Zrenner, E., Meitinger, T., Rosenthal, A., & Meindl, A. (1998). An L-type calcium-channel gene mutated in incomplete X-linked congenital stationary night blindness. Nature Genetics 19, 260–263.Google Scholar
Tagawa, Y., Sawai, H., Ueda, Y., Tauchi, M., & Nakanishi, S. (1999). Immunohistological studies of metabotropic glutamate receptor subtype 6-deficient mice show no abnormality of retinal cell organization and ganglion cell maturation. Journal of Neuroscience 19, 2568–2579.Google Scholar
Taylor, B.A., Navin, A., & Phillips, S.J. (1994). PCR-amplification of simple sequence repeat variants from pooled DNA samples for rapidly mapping new mutations of the mouse. Genomics 21, 626–632.CrossRefGoogle Scholar
Taylor, W.R. & Morgans, C. (1998). Localization and properties of voltage-gated calcium channels in cone photoreceptors of Tupaia belangeri. Visual Neuroscience 15, 541–552.Google Scholar
tom Dieck, S., Altrock, W.D., Kessels, M.M., Qualmann, B., Regus, H., Brauner, D., Fejtová, A., Bracko, O., Gundelfinger, E.D., & Brandstätter, J.H. (2005). Molecular dissection of the photoreceptor ribbon synapse: Physical interaction of Bassoon and RIBEYE is essential for the assembly of the ribbon complex. Journal of Cell Biology 168, 825–836.CrossRefGoogle Scholar
von Gersdorff, H. (2001). Synaptic ribbons: Versatile signal transducers. Neuron 29, 7–10.CrossRefGoogle Scholar
Wachtmeister, L. (1998). Oscillatory potentials in the retina: What do they reveal. Progress in Retinal and Eye Research 17, 485–521.CrossRefGoogle Scholar
Wilkinson, M.F. & Barnes, S. (1996). The dihydropyridine-sensitive calcium channel subtype in cone photoreceptors. Journal of General Physiology 107, 621–630.CrossRefGoogle Scholar
Wollstein, G., Paunescu, L.A., Ko, T.H., Fujimoto, J.G., Kowalevicz, A., Hartl, I., Beaton, S., Ishikawa, H., Mattox, C., Singh, O., Duker, J., Drexler, W., & Schuman, J.S. (2005). Ultrahigh-resolution optical coherence tomography in glaucoma. Ophthalmology 112, 229–237.CrossRefGoogle Scholar
Wong, W.T., Faulkner-Jones, B.E., Sanes, J.R., & Wong, R.O. (2000). Rapid dendritic remodeling in the developing retina: Dependence on neurotransmission and reciprocal regulation by Rac and Rho. Journal of Neuroscience 20, 5024–5036.Google Scholar
Wong, W.T. & Wong, R.O. (2001). Changing specificity of neurotransmitter regulation of rapid dendritic remodeling during synaptogenesis. Nature Neuroscience 4, 351–352.CrossRefGoogle Scholar
Wutz, K., Sauer, C., Zrenner, E., Lorenz, B., Alitalo, T., Broghammer, M., Hergersberg, M., de la Chapelle, A., Weber, B.H., Wissinger, B., Meindl, A., & Pusch, C.M. (2002). Thirty distinct CACNA1F mutations in 33 families with incomplete type of XLCSNB and Cacna1f expression profiling in mouse retina. European Journal of Human Genetics 10, 449–456.CrossRefGoogle Scholar
Yang, X.L. (2004). Characterization of receptors for glutamate and GABA in retinal neurons. Progress in Neurobiology 73, 127–150.CrossRefGoogle Scholar
Zeitz, C., Minotti, R., Feil, S., Mátyás, G., Cremers, F.P.M., Hoyng, C.B., & Berger, W. (2005). Novel mutations in CACNA1F and NYX in Dutch families with X-linked congenital stationary night blindness. Molecular Vision 11, 179–183.Google Scholar
Zhang, N. & Townes-Anderson, E. (2002). Regulation of structural plasticity by different channel types in rod and cone photoreceptors. Journal of Neuroscience 22, 7065–7079.Google Scholar