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A spectral model for signal elements isolated from zebrafish photopic electroretinogram

Published online by Cambridge University Press:  02 September 2009

RALPH F. NELSON  and
NIRMISH SINGLA
RALPH F. NELSON*
Affiliation:
Basic Neurosciences Program, National Institute of Neurological Disorders and Stroke, National Institutes of Health, Rockville, Maryland 20892
NIRMISH SINGLA
Affiliation:
Basic Neurosciences Program, National Institute of Neurological Disorders and Stroke, National Institutes of Health, Rockville, Maryland 20892
*
†Address correspondence and reprint requests to: Ralph F. Nelson, Basic Neurosciences Program, National Institute of Neurological Disorders and Stroke, National Institutes of Health, 5625 Fisher’s Lane, Room TS-09, Rockville, MD 20892-9406. E-mail: [email protected]
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Abstract

The zebrafish photopic electroretinogram (ERG) sums isolatable elements. In each element, red-, blue-, green-, and UV- (r, g, b, and u) cone signals combine in a way that reflects retinal organization. ERG responses to monochromatic stimuli of different wavelengths and irradiances were recorded on a white rod suppressing background using superfused eyecups. Onset elements were isolated with glutamatergic blockers and response subtractions. CNQX-blocked ionotropic (AMPA/kainate) glutamate receptors; l-AP4 or CPPG-blocked metabotropic (mGluR6) glutamate receptors; TBOA-blocked glutamate transporters; and l-aspartate inactivated all glutamatergic mechanisms. Seven elements emerged: photopic PIII, the l-aspartate-isolated cone response; b1, a CNQX-sensitive early b-wave element of inner retinal origin; PII, a photopic, CNQX-insensitive composite b-wave element from ON bipolar cells; PIIm, an l-AP4/CPPG-sensitive, CNQX-insensitive, metabotropic subelement of PII; PIInm, an l-AP4/CPPG/CNQX-insensitive nonmetabotropic subelement of PII; a1nm, a TBOA-sensitive, CNQX/l-AP4/CPPG-insensitive, nonmetabotropic, postphotoreceptor a-wave element; and a2, a CNQX-sensitive a-wave element linked to OFF bipolar cells. The first five elements were fit with a spectral model that demonstrates independence of cone–color pathways. From this, Vmax and half-saturation values (k) for the contributing r-, g-, b-, and u-cone signals were calculated. Two signal patterns emerged. For PIII or PIInm, the Vmax order was Vr > Vg >> Vb ≈ Vu. For b1, PII, and PIIm, the Vmax order was Vr ≈ Vb > Vg > Vu. In either pattern, u-cone amplitude (Vu) was smallest, but u-cone sensitivity (ku362) was greatest, some 10–30 times greater than r cone (kr570). The spectra of b1/PII/PIIm elements peaked near b- and u-cone absorbance maxima regardless of criteria, but the spectra of PIII/PIInm elements shifted from b- toward r-cone absorbance maxima as criterion levels increased. The greatest gains in Vmax relative to PIII occurred for the b- and u-cone signals in the b1/PII/PIIm b-wave elements. This suggests a high-gain prolific metabotropic circuitry for b- and u-cone bipolar cells.

Keywords

ZebrafishSpectral sensitivityb-wavePIIION cone bipolar cells
Type
Research Articles
Information
Visual Neuroscience , Volume 26 , Issue 4 , July 2009 , pp. 349 - 363
Copyright
Copyright © Cambridge University Press 2009

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References

Arriza, J.L., Eliasof, S., Kavanaugh, M.P. & Amara, S.G. (1997). Excitatory amino acid transporter 5, a retinal glutamate transporter coupled to a chloride conductance. Proceedings of the National Academy of Sciences of the United States of America 94, 4155–4160.Google Scholar
Bird, R. & Riorden, C. (1986). Simple solar spectral model for direct and diffuse irradiance on horizontal and tilted planes at the Earth’s surface for cloudless atmospheres. Journal of Applied Meteorology 25, 87–97.Google Scholar
Bui, B.V. & Fortune, B. (2004). Ganglion cell contributions to the rat full-field electroretinogram. The Journal of Physiology 555, 153–173.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, 635–645.Google Scholar
Chappell, R.L., Naka, K. & Sakuranaga, M. (1985). Dynamics of turtle horizontal cell response. The Journal of General Physiology 86, 423–453.Google Scholar
Connaughton, V.P., Graham, D. & Nelson, R. (2004). Identification and morphological classification of horizontal, bipolar, and amacrine cells within the zebrafish retina. Journal of Comparative Neurology 477, 371–385.Google Scholar
Connaughton, V.P. & Nelson, R. (2000). Axonal stratification patterns and glutamate-gated conductance mechanisms in zebrafish retinal bipolar cells. The Journal of Physiology 524, 135–146.CrossRefGoogle Scholar
Connaughton, V.P., Nelson, R. & Bender, A.M. (2008). Electrophysiological evidence of GABAA and GABAC receptors on zebrafish retinal bipolar cells. Visual Neuroscience 25, 139–153.CrossRefGoogle Scholar
Dacheux, R.F. & Raviola, E. (1986). The rod pathway in the rabbit retina: A depolarizing bipolar and amacrine cell. The Journal of Neuroscience 6, 331–345.CrossRefGoogle Scholar
DeVries, S.H. (2000). Bipolar cells use kainate and AMPA receptors to filter visual information into separate channels. Neuron 28, 847–856.Google Scholar
Engstrom, K. (1960). Cone types and cone arrangement in the retina of some cyprinids. Acta Zoologica 41, 277–295.Google Scholar
Fadool, J.M. & Dowling, J.E. (2008). Zebrafish: A model system for the study of eye genetics. Progress in Retinal and Eye Research 27, 89–110.Google Scholar
Famiglietti, E.V. Jr, Kaneko, A. & Tachibana, M. (1977). Neuronal architecture of on and off pathways to ganglion cells in carp retina. Science 198, 1267–1269.Google Scholar
Granit, R. (1933). The components of the retinal action potential in mammals and their relation to the discharge in the optic nerve. The Journal of Physiology 77, 207–239.Google Scholar
Grant, G.B. & Dowling, J.E. (1995). A glutamate-activated chloride current in cone-driven ON bipolar cells of the white perch retina. The Journal of Neuroscience 15, 3852–3862.Google Scholar
Grant, G.B. & Dowling, J.E. (1996). On bipolar cell responses in the teleost retina are generated by two distinct mechanisms. Journal of Neurophysiology 76, 3842–3849.Google Scholar
Hankins, M.W. & Ikeda, H. (1991). Non-NMDA type excitatory amino acid receptors mediate rod input to horizontal cells in the isolated rat retina. Vision Research 31, 609–617.Google Scholar
Hensley, S.H., Yang, X.L. & Wu, S.M. (1993). Identification of glutamate receptor subtypes mediating inputs to bipolar cells and ganglion cells in the tiger salamander retina. Journal of Neurophysiology 69, 2099–2107.Google Scholar
Hughes, A., Saszik, S., Bilotta, J., Demarco, P.J. Jr & Patterson, W.F. II. (1998). Cone contributions to the photopic spectral sensitivity of the zebrafish ERG. Visual Neuroscience 15, 1029–1037.Google Scholar
Jeon, C.J., Strettoi, E. & Masland, R.H. (1998). The major cell populations of the mouse retina. The Journal of Neuroscience 18, 8936–8946.Google Scholar
Krizaj, D., Akopian, A. & Witkovsky, P. (1994). The effects of L-glutamate, AMPA, quisqualate, and kainate on retinal horizontal cells depend on adaptational state: Implications for rod-cone interactions. The Journal of Neuroscience 14, 5661–5671.Google 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.Google Scholar
Nelson, R. (1977). Cat cones have rod input: A comparison of the response properties of cones and horizontal cell bodies in the retina of the cat. The Journal of Comparative Neurology 172, 109–135.Google Scholar
Nelson, R. (1982). AII amacrine cells quicken time course of rod signals in the cat retina. Journal of Neurophysiology 47, 928–947.Google Scholar
Nelson, R., Bender, A.M. & Connaughton, V.P. (2003). Stimulation of sodium pump restores membrane potential to neurons excited by glutamate in zebrafish distal retina. The Journal of Physiology 549, 787–800.Google Scholar
Nelson, R. & Connaughton, V.P. (2004). Glutamate transporter drives the b-wave in zebrafish retina. Investigative Ophthalmology and Visual Science 45, E-abstract 815.Google Scholar
Newman, E.A. (1980). Current source-density analysis of the b-wave of frog retina. Journal of Neurophysiology 43, 1355–1366.Google Scholar
Palacios, A.G., Goldsmith, T.H. & Bernard, G.D. (1996). Sensitivity of cones from a cyprinid fish (Danio aequipinnatus) to ultraviolet and visible light. Visual Neuroscience 13, 411–421.Google Scholar
Pflug, R., Nelson, R. & Ahnelt, P.K. (1990). Background-induced flicker enhancement in cat retinal horizontal cells. I. Temporal and spectral properties. Journal of Neurophysiology 64, 313–325.Google Scholar
Robinson, J., Schmitt, E.A., Harosi, F.I., Reece, R.J. & Dowling, J.E. (1993). Zebrafish ultraviolet visual pigment: Absorption spectrum, sequence, and localization. Proceedings of the National Academy of Sciences of the United States of America 90, 6009–6012.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.Google Scholar
Robson, J.G. & Frishman, L.J. (1998). Dissecting the dark-adapted electroretinogram. Documenta Ophthalmologica 95, 187–215.Google Scholar
Robson, J.G., Maeda, H., Saszik, S.M. & Frishman, L.J. (2004). In vivo studies of signaling in rod pathways of the mouse using the electroretinogram. Vision Research 44, 3253–3268.Google Scholar
Saszik, S., Alexander, A., Lawrence, T. & Bilotta, J. (2002 a). APB differentially affects the cone contributions to the zebrafish ERG. Visual Neuroscience 19, 521–529.Google Scholar
Saszik, S.M., Robson, J.G. & Frishman, L.J. (2002 b). The scotopic threshold response of the dark-adapted electroretinogram of the mouse. The Journal of Physiology 543, 899–916.Google Scholar
Shimamoto, K., Lebrun, B., Yasuda-Kamatani, Y., Sakaitani, M., Shigeri, Y., Yumoto, N. & Nakajima, T. (1998). DL-threo-beta-benzyloxyaspartate, a potent blocker of excitatory amino acid transporters. Molecular Pharmacology 53, 195–201.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.Google 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.Google Scholar
Sillman, A.J., Ito, H. & Tomita, T. (1969 a). Studies on the mass receptor potential of the isolated frog retina. I. General properties of the response. Vision Research 9, 1435–1442.Google Scholar
Sillman, A.J., Ito, H. & Tomita, T. (1969 b). Studies on the mass receptor potential of the isolated frog retina. II. On the basis of the ionic mechanism. Vision Research 9, 1443–1451.Google Scholar
Slaughter, M.M. & Miller, R.F. (1981). 2-amino-4-phosphonobutyric acid: A new pharmacological tool for retina research. Science 211, 182–185.Google Scholar
Stockton, R.A. & Slaughter, M.M. (1989). B-wave of the electroretinogram. A reflection of ON bipolar cell activity. The Journal of General Physiology 93, 101–122.Google Scholar
Strettoi, E. & Masland, R.H. (1995). The organization of the inner nuclear layer of the rabbit retina. The Journal of Neuroscience 15, 875–888.Google Scholar
Wesolowska, A., Nelson, R. & Connaughton, V. (2002). Glutamate mechanisms involved in the OFF pathway of zebrafish retina. Investigative Ophthalmology and Visual Science 43, E-abstract 1826.Google Scholar
Wong, K.Y. (2004). Glutamatergic mechanisms in the outer retina of larval zebrafish: Analysis of electroretinogram b- and d-waves using a novel preparation. Zebrafish 1, 121–131.Google Scholar
Wong, K.Y., Adolph, A.R. & Dowling, J.E. (2005 a). Retinal bipolar cell input mechanisms in giant danio. I. Electroretinographic analysis. Journal of Neurophysiology 93, 84–93.Google Scholar
Wong, K.Y., Cohen, E.D. & Dowling, J.E. (2005 b). Retinal bipolar cell input mechanisms in giant danio. II. Patch-clamp analysis of on bipolar cells. Journal of Neurophysiology 93, 94–107.Google Scholar