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Immuocytochemical analysis of spatial organization of photoreceptors and amacrine and ganglion cells in the tiger salamander retina

Published online by Cambridge University Press:  23 June 2004

JIAN ZHANG ,
ZHUO YANG  and
SAMUEL M. WU
JIAN ZHANG
Affiliation:
Cullen Eye Institute, Baylor College of Medicine, One Baylor Plaza, Houston
ZHUO YANG
Affiliation:
Cullen Eye Institute, Baylor College of Medicine, One Baylor Plaza, Houston
SAMUEL M. WU
Affiliation:
Cullen Eye Institute, Baylor College of Medicine, One Baylor Plaza, Houston
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Abstract

In the present study, using double- or triple-label immunocytochemistry in conjunction with confocal microscopy, we aimed to examine the population and distribution of photoreceptors, GABAergic and glycinergic amacrine cells, and ganglion cells, which are basic but important parameters for studying the structure–function relationship of the salamander retina. We found that the outer nuclear layer (ONL) contained 82,019 ± 3203 photoreceptors, of which 52% were rods and 48% were cones. The density of photoreceptors peaked at ∼8000 cells/mm2 in the ventral and dropped to ∼4000 cells/mm2 in the dorsal retina. In addition, the rod/cone ratio was less than 1 in the central retina but larger than 1 in the periphery. Moreover, in the proximal region of the inner nuclear layer (INL3), the total number of cells was 50,576 ± 8400. GABAergic and glycinergic amacrine cells made up approximately 78% of all cells in this layer, including 43% GABAergic, 32% glycinergic, and 3% GABA/glycine colocalized amacrine cells. The density of these amacrine cells was ∼6500 cells/mm2 in the ventral and ∼3200 cells/mm2 in the dorsal area. The ratio of GABAergic to glycinergic amacrine cells was larger than 1. Furthermore, in the ganglion cell layer (GCL), among a total of 36,007 ± 2010 cells, ganglion cells accounted for 65.7 ± 1.5% of the total cells, whereas displaced GABAergic and glycinergic amacrine cells comprised about 4% of the cells in this layer. The ganglion cell density was ∼1800 cells/mm2 in the ventral and ∼600 cells/mm2 in the dorsal retina. Our data demonstrate that all three major cell types are not uniformly distributed across the salamander retina. Instead, they exhibit a higher density in the ventral than in the dorsal retina and their spatial arrangement is associated with the retinal topography. These findings provide a basic anatomical reference for the electrophysiological study of this species.

Keywords

PhotoreceptorsAmacrine cellsGanglion cellsTopographyAmphibian retina
Type
Research Article
Information
Visual Neuroscience , Volume 21 , Issue 2 , March 2004 , pp. 157 - 166
Copyright
2004 Cambridge University Press

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References

REFERENCES

Attwell, D. & Wilson, M. (1980). Behaviour of the rod network in the tiger salamander retina mediated by membrane properties of individual rods. Journal of Physiology 309, 287–315.CrossRefGoogle Scholar
Attwell, D., Wilson, M., & Wu, S.M. (1984). A quantitative analysis of interactions between photoreceptors in the salamander (Ambystoma) retina. Journal of Physiology 352, 707–737.Google Scholar
Attwell, D., Wilson, M., & Wu, S.M. (1985). The effect of light on the spread of signals through the rod network of the salamander retina. Brain Research 343, 79–88.CrossRefGoogle Scholar
Barnes, S. & Hille, B. (1989). Ionic channels of the inner segment of tiger salamander cone photoreceptors. Journal of General Physiology 94, 719–743.CrossRefGoogle Scholar
Cook, P.B. & McReynolds, J.S. (1998). Lateral inhibition in the inner retina is important for spatial tuning of ganglion cells. Nature Neuroscience 1, 714–719.CrossRefGoogle Scholar
Cook, P.B., Lukasiewicz, P.D., & McReynolds, J.S. (1998). Action potentials are required for the lateral transmission of glycinergic transient inhibition in the amphibian retina. Journal of Neuroscience 18, 2301–2308.Google Scholar
Crevier, D.W. & Meister, M. (1998). Synchronous period-doubling in flicker vision of salamander and man. Journal of Neurophysiology 79, 1869–1878.Google Scholar
Deng, P., Cuenca, N., Doerr, T., Pow, D.V., Miller, R., & Kolb, H. (2001). Localization of neurotransmitters and calcium binding proteins to neurons of salamander and mudpuppy retinas. Vision Research 41, 1771–1783.CrossRefGoogle Scholar
Hestrin, S. (1987). The properties and function of inward rectification in rod photoreceptors of the tiger salamander. Journal of Physiology 390, 319–333.CrossRefGoogle Scholar
Hughes, A. (1977). The refractive state of the rat eye. Vision Research 17, 927–939.CrossRefGoogle 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
Lasansky, A. (1973). Organization of the outer synaptic layer in the retina of the larval tiger salamander. Philosophical Transactions Royal Society B (London) 265, 471–489.CrossRefGoogle Scholar
Lukasiewicz, P.D. & Werblin, F.S. (1994). A novel GABA receptor modulates synaptic transmission from bipolar to ganglion and amacrine cells in the tiger salamander retina. Journal of Neuroscience 14, 1213–1223.Google Scholar
Ma, J.X., Kono, M., Xu, L., Das, J., Ryan, J.C., Hazard, E.S., III, Oprian, D.D., & Crouch, R.K. (2001a). Salamander UV cone pigment: Sequence, expression, and spectral properties. Visual Neuroscience 18, 393–399.Google Scholar
Ma, J.X., Znoiko, S., Othersen, K.L., Ryan, J.C., Das, J., Isayama, T., Kono, M., Oprian, D.D., Corson, D.W., Cornwall, M.C., Cameron, D.A., Harosi, F.I., Makino, C.L., & Crouch, R.K. (2001b). A visual pigment expressed in both rod and cone photoreceptors. Neuron 32, 451–461.Google Scholar
Marc, R.E., Murry, R.F., & Basinger, S.F. (1995). Pattern recognition of amino acid signatures in retinal neurons. Journal of Neuroscience 15, 5106–5129.Google Scholar
Mariani, A.P. (1986). Photoreceptors of the larval tiger salamander retina. Proceedings of the Royal Society B (London) 227, 483–492.CrossRefGoogle Scholar
Packer, O., Hendrickson, A.E., & Curcio, C.A. (1989). Photoreceptor topography of the retina in the adult pigtail macaque (Macaca nemestrina). Journal of Comparative Neurology 288, 165–183.CrossRefGoogle Scholar
Pang, J.J., Gao, F., & Wu, S.M. (2002). Segregation and integration of visual channels: Layer-by-layer computation of ON-OFF signals by amacrine cell dendrites. Journal of Neuroscience 22, 4693–4701.Google Scholar
Perry, V.H. (1981). Evidence for an amacrine cell system in the ganglion cell layer of the rat retina. Neuroscience 6, 931–944.CrossRefGoogle Scholar
Roska, B., Nemeth, E., & Werblin, F.S. (1998). Response to change is facilitated by a three-neuron disinhibitory pathway in the tiger salamander retina. Journal of Neuroscience 18, 3451–3459.Google Scholar
Sherry, D.M. (2003). Neurochemical heterogeneity of retinal bipolar cells. Optometry 74, 429–442.Google Scholar
Sherry, D.M., Bui, D.D., Degrip, W.J. (1998). Identification and distribution of photoreceptor subtypes in the neotenic tiger salamander retina. Visual Neuroscience 15, 1175–1187.Google Scholar
Steinberg, R.H., Reid, M., & Lacy, P.L. (1973). The distribution of rods and cones in the retina of the cat (Felis domesticus). Journal of Comparative Neurology 148, 229–248.CrossRefGoogle Scholar
Strettoi, E. & Masland, R.H. (1995). The organization of the inner nuclear layer of the rabbit retina. Journal of Neuroscience 15, 875–888.Google Scholar
Vaney, D.I., Peichi, L., & Boycott, B.B. (1981). Matching populations of amacrine cells in the inner nuclear and ganglion cell layers of the rabbit retina. Journal of Comparative Neurology 199, 373–391.CrossRefGoogle Scholar
Warland, D.K., Reinagel, P., & Meister, M. (1997). Decoding visual information from a population of retinal ganglion cells. Journal of Neurophysiology 78, 2336–2350.Google Scholar
Watt, C.B. & Florack, V.J. (1992). A double-label analysis demonstrating the non-coexistence of tyrosine hydroxylase-like and GABA-like immunoreactivities in amacrine cells of the larval tiger salamander retina. Neuroscience Letters 148, 47–50.CrossRefGoogle Scholar
Watt, C.B., Yang, S.Z., Lam, D.M., & Wu, S.M. (1988). Localization of tyrosine-hydroxylase-like-immunoreactive amacrine cells in the larval tiger salamander retina. Journal of Comparative Neurology 272, 114–126.CrossRefGoogle Scholar
Watt, C.B., Glazebrook, P.A., & Florack, V.J. (1994). Localization of substance P and GABA in retinotectal ganglion cells of the larval tiger salamander. Visual Neuroscience 11, 355–362.CrossRefGoogle Scholar
Werblin, F.S. (1978). Transmission along and between rods in the tiger salamander retina. Journal of Physiology 280, 449–470.CrossRefGoogle Scholar
Williams, R.W., Strom, R.C., Rice, D.S., & Goldowitz, D. (1996). Genetic and environmental control of variation in retinal ganglion cell number in mice. Journal of Neuroscience 16, 7193–7205.Google Scholar
Wong-Riley, M.T. (1974). Synaptic organization of the inner plexiform layer in the retina of the tiger salamander. Journal of Neurocytology 3, 1–33.Google Scholar
Wu, S.M. & Yang, X.L. (1988). Electrical coupling between rods and cones in the tiger salamander retina. Proceedings of the National Academy of Sciences of the U.S.A. 85, 275–278.CrossRefGoogle Scholar
Wu, S.M., Gao, F., & Maple, B.R. (2000). Functional architecture of synapses in the inner retina: segregation of visual signals by stratification of bipolar cell axon terminals. Journal of Neuroscience 20, 4462–4470.Google Scholar
Yang, C.Y. & Yazulla, S. (1988a). Light microscopic localization of putative glycinergic neurons in the larval tiger salamander retina by immunocytochemical and autoradiographical methods. Journal of Comparative Neurology 272, 343–357.Google Scholar
Yang, C.Y. & Yazulla, S. (1988b). Localization of putative GABAergic neurons in the larval tiger salamander retina by immunocytochemical and autoradiographic methods. Journal of Comparative Neurology 277, 96–108.Google Scholar
Yang, C.Y. & Yazulla, S. (1994). Glutamate-, GABA-, and GAD-immunoreactivities co-localize in bipolar cells of tiger salamander retina. Visual Neuroscience 11, 1193–1203.CrossRefGoogle Scholar
Yang, C.Y., Lukasiewicz, P., Maguire, G., Werblin, F.S., & Yazulla, S. (1991). Amacrine cells in the tiger salamander retina: Morphology, physiology, and neurotransmitter identification. Journal of Comparative Neurology 312, 19–32.CrossRefGoogle Scholar
Yazulla, S. & Yang, C.Y. (1988). Colocalization of GABA and glycine immunoreactivities in a subset of retinal neurons in tiger salamander. Neuroscience Letter 95, 37–41.CrossRefGoogle Scholar
Young, H.M. & Vaney, D.I. (1991). Rod-signal interneurons in the rabbit retina: 1. Rod bipolar cells Journal of Comparative Neurology 310, 139–153.Google Scholar
Zhan, X.J. & Troy, J.B. (1997). An efficient method that reveals both the dendrites and the soma mosaics of retinal ganglion cells. Journal of Neuroscience Methods 72, 109–116.CrossRefGoogle Scholar
Zhang, J. & Wu, S.M. (2001). Immunocytochemical analysis of cholinergic amacrine cells in the tiger salamander retina. Neuroreport 12, 1371–1375.CrossRefGoogle Scholar
Zhang, J.Wu, S.M. (2003). Synaptic contacts between photoreceptors and On bipolar cells in the tiger salamander retina. Journal of Comparative Neurology 461, 276–289.CrossRefGoogle Scholar
Zhang, J., Jung, C.S., & Slaughter, M.M. (1997). Serial inhibitory synapses in retina. Visual Neuroscience 14, 553–563.CrossRefGoogle Scholar