Skip to main content
Log in

The neurons of the ground squirrel retina as revealed by immunostains for calcium binding proteins and neurotransmitters

  • Published:
Journal of Neurocytology

Abstract

Ground squirrel retinas were immunostained with antibodies against calcium binding proteins (CBPs) and classical neurotransmitters in order to describe neuronal phenotypes in a diurnal mammalian retina and to then compare these neurons with those of more commonly studied nocturnal retinas like cats' and rabbits'. Double immunostained tissue was examined by confocal microscopy using antibodies against the following: rhodopsin and the CBPs, calbindin, calretinin, parvalbumin, calmodulin and recoverin (CB, CR, PV, CM, RV), glycine, GABA, choline acetyltransferase (CHAT) and tyrosine hydroxylase (TOH).

In ground squirrel retina, the traditional cholinergic mirror symmetric amacrine cells colocalize CHAT with PV and GABA and faintly with glycine. A second cholinergic amacrine cell type colocalizes glycine alone. CR is found in at least 3 different amacrine cell types. The CR-immunoreactive (IR) cell population is a mixture of glycinergic and GABAergic types. The dopamine cell type IR to tyrosine hydroxylase has the typical morphology of a wide field cell with dendrites in S1 but the “rings” seen in cat or rabbit retina are not as numerous. TOH-IR amacrine cells send large club-shaped processes to the outer plexiform layer. CB and CR are in bipolar cells, A- and B-type horizontal cells and several amacrine cell types. Anti-rhodopsin labels the low density rod photoreceptor population in this species. Anti-recoverin labels cones and some bipolar cells while PKC is found in several different bipolar cell types. One ganglion cell with dendritic branching in S3 is strongly CR-IR.

We find no evidence for an AII amacrine cell in the ground squirrel, with either anti-CR or anti-PV. An amacrine cell with similarity to the DAP1-3 cell of rabbit is CR-IR and glycine-IR. We discuss this labeling pattern in relationship to other mammalian species. The differences in staining patterns and phenotypes revealed suggest a functional diversity in the populations of amacrine cells according to whether the retinas are rod or cone dominated.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Ahnelt, P. K. (1985) Characterization of the color related receptor mosaic in the ground squirrel retina. Vision Research 25, 1557–1567.

    PubMed  Google Scholar 

  • Amthor, F. R., Takahashi, E.S. & Oyster, C. W. (1989a) Morphologies of rabbit retinal ganglion cells with complex receptive fields. Journal of Comparative Neurology 280, 97–121.

    PubMed  Google Scholar 

  • Amthor, F. R., Takahashi, E. S. & Oyster, C. W. (1989b) Morphologies of rabbit retinal ganglion cells with concentric receptive fields. Journal of Comparative Neurology 280, 72–96.

    PubMed  Google Scholar 

  • Berger, S. J. & Devries, G. W. (1982) The distribution of enzymes which synthesize nicotinamide adenine dinucleotide and nicotinamide adenine dinucleotide phosphate in monkey, rabbit, and ground squirrel retinas. Journal of Neurochemistry 38, 821–826.

    PubMed  Google Scholar 

  • Bloomfield, S. A. (2001) Plasticity of AII amacrine cell circuitry in the mammalian retina. In “Concepts and Challenges in Retinal Biology:ATribute to John E. Dowling,” Brain Research Reviews (edited by Kolb, H., Ripps, H. & Wu, S.) pp. 185–200. Elsevier Press.

  • Casini, G., Rickman, D. W. & Brecha, N. C. (1995) AII amacrine cell population in the rabbit retina: Identification by parvalbumin immunoreactivity. Journal of Comparative Neurology 356, 132–142.

    PubMed  Google Scholar 

  • Cuenca, N., Haverkamp, S. & Kolb, H. (2000) Choline acetyltransferase is found in terminals of horizontal cells that label for GABA, nitric oxide synthase and calcium binding proteins in the turtle retina. Brain Research 878, 228–239.

    PubMed  Google Scholar 

  • Cuenca, N., Deng, P., Linberg, K., Fisher, S. K. & Kolb, H. (2003) Choline acetyl translerase is expressed The neurons of the ground squirrel retina 665 by non-starburst amacrine cells in the ground squirrel retina. Brain Research 964, 21–30.

    PubMed  Google Scholar 

  • Cueva, J. G., Haverkamp, S., Reimer, R. J., Edwards, R., WÄssle, H. & Brecha, N. C. (2002) Vesicular gamma-aminobutyric acid transporter expression in amacrine and horizontal cells. Journal of Comparative Neurology 445, 227–237.

    PubMed  Google Scholar 

  • Deng, P., Cuenca, N., Doerr, T., Pow, D., Miller, R. F. & Kolb, H. (2001) Localization of calcium binding proteins and neurotransmitters to neurons of salamander and mudpuppy retinas. Vision Research 41, 1771–1783.

    PubMed  Google Scholar 

  • Devries, S. H. & Baylor, D. A. (1995) An alternative pathway for signal flow from rod photoreceptors to ganglion cells in mammalian retina. Proceedings of National Academy of Sciences 92, 10658–10662.

    Google Scholar 

  • Devries, S. H. & Schwartz, E. R. (1999) Kainate receptors mediate synaptic transmission between cones and 'Off bipolar cells in a mammalian retina. Nature 397, 157–160.

    PubMed  Google Scholar 

  • Devries, S. H. (2000) Bipolar cells use kainate and AMPA receptors to filter visual information into separate channels. Neuron 28, 847–856.

    PubMed  Google Scholar 

  • Famiglietti, E. V. (1983) ‘Starburst’ amacrine cells and cholinergic neurons: Mirror-symmetric ON and OFF amacrine cells of rabbit retina. Brain Research 261, 138–144.

    PubMed  Google Scholar 

  • Famiglietti, E. V. & Kolb, H. (1975) A bistratified amacrine cell and synaptic circuitry in the inner plexiform layer of the retina. Brain Research 84, 293–300.

    PubMed  Google Scholar 

  • Galli-Resta, L., Novelli, E., Kryger, Z., Jacobs, G. H. & Reese, B. E. (1999) Modelling the mosaic organization of rod and cone photoreceptors with a minimal-spacing rule. European Journal of Neuroscience 11, 1461–1469.

    PubMed  Google Scholar 

  • Goebel, D. J. & Pourcho, R. G. (1997) Calretinin in the cat retina: Colocalizations with other calciumbinding proteins, GABA and glycine. Visual Neuroscience 14, 311–322.

    PubMed  Google Scholar 

  • Haverkamp, S., Kolb, H. & Cuenca, N. (1999) Endothelial nitric oxide (e-NOS) is localized to Muller cells in vertebrate retinas. Vision Research 39, 2299–2303.

    PubMed  Google Scholar 

  • He, S. & Masland, R. H. (1997) Retinal direction selectivity after targeted laser ablation of starburst amacrine cells. Nature 389, 378–382.

    PubMed  Google Scholar 

  • Jacobs, G. H. (1990) Duplicity theory and ground squirrels: Linkage between photoreceptors and visual function. Visual Neuroscience 5, 311–318.

    PubMed  Google Scholar 

  • Jacobs, G. H. & Tootell, R. B. H. (1980) Spectrally opponent responses in the ground squirrel optic nerve. Vision Research 20, 9–13.

    PubMed  Google Scholar 

  • Jacoby, R. A. & Marshak, D. W. (2000) Synaptic connections of DB3 diffuse bipolar cell axons in macaque retina. Journal of Comparative Neurology 416, 19–29.

    PubMed  Google Scholar 

  • Jacobs, G. H., Tootell, R. B. H., Fisher, S. K. & Anderson, D. H. (1980) Rod photoreceptors and scotopic vision in ground squirrels. Journal of Comparative Neurology 189, 113–125.

    PubMed  Google Scholar 

  • Jacobs, G. H., Neitz, J. & Crognale, M. (1985) Spectral sensitivity of ground squirrel cones measured with ERG flicker photometry. Journal of Comparative Neurology 156, 503–509.

    Google Scholar 

  • Jacobs, G. H., Calderone, J. B., Sakai, T., Lewis, G. P. & Fisher, S. K. (2002)Ananimal model for studying cone function in retinal detachment. Documenta Ophthalmologica 104, 119–132.

    PubMed  Google Scholar 

  • Kolb, H. & Famiglietti, E. V. (1974) Rodand cone pathways in the inner plexiform layer of the cat retina. Science 186, 47–49.

    PubMed  Google Scholar 

  • Kolb, H. & Nelson, R. (1984) Neural architecture of the cat retina. Progress in Retinal Research 3, 21–60.

    Article  Google Scholar 

  • Kolb, H. & Zhang, L. (1997) Immunostaining with antibodies against Protein Kinase C isoforms in the fovea of the monkey retina. Microscope Research Techniques 36, 57–75.

    Article  Google Scholar 

  • Kolb, H., Cuenca, N. & Dekorver, L. (1991) Postembedding immunocytochemistry for GABA and glycine reveals the synaptic relationships of the dopaminergic amacrine cell of the cat retina. Journal of Comparative Neurology 310, 267–284.

    PubMed  Google Scholar 

  • Kolb, H., Deng, P., Linberg, K., Lewis, G., Fisher, S. & Cuenca, N. (1999) The ground squirrel compared to the rat retina: An immunocytochemical study using calcium binding proteins and neurotransmitter candidates. InvestigativeOphthalmology & Visual Science 40, S438.

    Google Scholar 

  • Kolb, H., Zhang, L., Dekorver, L. & Cuenca, N. (2002) A new look at calretinin-immunoreactive amacrine cell types in the monkey retina. Journal of Comparative Neurology 453, 168–184.

    PubMed  Google Scholar 

  • Kouyama, N. & Marshak, D. W. (1992) Bipolar cells specific for blue cones in the macaque retina. Journal of Neuroscience 12, 1233–1252.

    PubMed  Google Scholar 

  • Kryger, Z., Galli-Resta, L., Jacobs, G. H. & Reese, B. E. (1998) The topography of rod and cone photoreceptors in the retina of the ground squirrel. Visual Neuroscience 15, 685–691.

    PubMed  Google Scholar 

  • Linberg, K. A., Suemune, S. & Fisher, S. K. (1996) Retinal neurons of the California ground squirrel, Spermophilus beecheyi: A Golgi study. Journal of Comparative Neurology 365, 173–216.

    PubMed  Google Scholar 

  • Linberg, K. A., Cuenca, N., Ahnelt, P., Fisher, S.K. & Kolb, H. (2001) Comparative anatomy of major retinal pathways in the eyes of nocturnal and diurnal mammals. In “Concepts and Challenges in Retinal Biology:A Tribute to John E. Dowling,” Brain Research Reviews (edited by Kolb, H., Ripps, H. & Wu, S.) pp. 27–52. Elsevier Press.

  • Long, K. O. & Fisher, S. K. (1983) The distributions of photoreceptors and ganglion cells in the California ground squirrel, Spermophilus beecheyi. Journal of Comparative Neurology 221, 329–340.

    Article  Google Scholar 

  • Lugo-Garcia, N. & Blanco, R. E. (1991) Localization of GAD-and GABA-like immunoreactivity in ground squirrel retina: Retrograde labeling demonstrates GADpositive ganglion cells. Brain Research 8(564), 19–26.

    Article  Google Scholar 

  • Lugo-Garcia, N. & Blanco, R. E. (1993) Dopaminergic neurons in the cone-dominated ground squirrel retina: A light and electron microscopy study. Journal fur Hirnforsuchung 34, 561–569.

    Google Scholar 

  • Lugo-Garcia, N. & Blanco, R. E. (1997) Somatostatinlike immunoreactive cells in the ground squirrel retina. Cell Biology International 21, 447–453.

    PubMed  Google Scholar 

  • Masland, R. H. & Tauchi, M. (1986) The cholinergic amacrine cell. Trends in Neuroscience 9, 218–223.

    Article  Google Scholar 

  • Massey, S. C. & Mills, S. L. (1996) A calbindinimmunoreactive cone bipolar cell type in the rabbit retina. Journal of Comparative Neurology 366, 15–33.

    PubMed  Google Scholar 

  • Massey, S. C. & Mills, S. L. (1999) An antibody to calretinin stains AII amacrine cells in the rabbit retina: Double label and confocal analysis. Journal of Comparative Neurology 411, 3–18.

    PubMed  Google Scholar 

  • Michael, C. R. (1968a) Receptive fields of single optic nerve fibers in a mammal with an allcone retina. I. Contrast-sensitive units. Journal of Neurophysiology 31, 249–256.

    PubMed  Google Scholar 

  • Michael, C. R. (1968b) Receptive fields of single optic nerve fibers in a mammal with an allcone retina. II. Directionally selective units. Journal of Neurophysiology 31, 257–267.

    PubMed  Google Scholar 

  • Michael, C. R. (1968c) Receptive fields of single optic nerve fibers in a mammal with an allcone retina. III. Opponent color units. Journal of Neurophysiology 31, 268–282.

    PubMed  Google Scholar 

  • Mills, S. L. & Massey, S. C. (1999) AII amacrine cells limit scotopic acuity in the central macaque retina: An analysis with calretinin labeling, confocal microscopy and intracellular dye injection. Journal of Comparative Neurology 1(411), 19–34.

    Article  Google Scholar 

  • Mills, S. L. & Massey, S. C. (1995) Differential properties of two gap junctional pathways made by AII amacrine cells. Nature 377, 734–737.

    PubMed  Google Scholar 

  • Mitchell, C. K. & Redburn, D. A. (1996) GABA and GABA-A receptors are maximally expressed in association with cone synaptogenesis in neonatal rabbit retina. Developmental Brain Research 95, 63–71.

    PubMed  Google Scholar 

  • Pasteels, B., Rogers, J., Blachier, F. & Pochet, P. (1990) Calbindin and calretinin localization in retina from different species. Visual Neurosciences 5, 1–16.

    Google Scholar 

  • Pochet, R., Pasteels, B., Seto-Ohshima, A., Bastianelli, E., Kitajima, S. & van Eldik, L. J. (1991) Calmodulin and calbindin localization in retina from six vertebrate species. Journal of Comparative Neurology 314, 750–762.

    PubMed  Google Scholar 

  • Polans, A., Baehr, W. & Palcsewski, K. (1996) Turned on by Ca2+: The physiology and pathology of Ca2+-binding proteins in the retina. Trends in Neuroscience 19, 547–554.

    Article  Google Scholar 

  • Pourcho, R. G. (1982) Dopaminergic amacrine cells in the cat retina. Brain Research 252, 101–109.

    PubMed  Google Scholar 

  • Pourcho, R. G. & Goebel, D. J. (1985) A combined Golgi and autoradiographic study of 3(H)glycineaccumulating amacrine cells in the cat retina. Journal of Comparative Neurology 233, 473–480.

    PubMed  Google Scholar 

  • RÖhrenbeck, J., WÄ ssle, H. & Boycott, B. B. (1989) Horizontal cells in themonkeyretina:Immunocytochemical staining with antibodies against calcium binding proteins European Journal of Neuroscience 1, 407–420.

    Google Scholar 

  • Sanna, P. P., Keyser, K. T., Celio, M. R., Karten, H. J. & Bloom, F. E. (1993) Distribution of parvalbumin immunoreactivity in the vertebrate retina. Brain Research 600, 141–150.

    PubMed  Google Scholar 

  • Smith, R. G., Freed, M. A. & Sterling, P. (1986) Microcircuitry of the dark-adapted cat retina: Functional architecture of the rod-cone network. Journal of Neuroscience 6, 3503–3517.

    Google Scholar 

  • Strettoi, E., Raviola, E. & Dacheux, R. F. (1992) Synaptic connections of the narrow-field, bistratified rod amacrine cell (AII) in the rabbit retina. Journal of Comparative Neurology 325, 152–168.

    PubMed  Google Scholar 

  • Szel, A., Diamanstein, T. & Rohlich, P. (1988) Indentification of blue-sensitive cones in the mammalian retina by antivisual pigment antibody. Journal of Comparative Neurology 273, 593–602.

    PubMed  Google Scholar 

  • Taylor, W. R., He, S., Levick, W. R. & Vaney, D. I. (2000) Dendritic computation of direction selectivity by retinal ganglion cells. Science 289, 2347–2350.

    PubMed  Google Scholar 

  • Tsukamoto, Y., Morigiwa, K., Ueda, M. & sterling, P. (2001) Microcircuits for night vision in mouse retina. Journal of Neuroscience 21, 8616–8623.

    PubMed  Google Scholar 

  • Vaquero, C. F., Velasco, A. & Devilla, P. (1996) Protein kinase C localization in the synaptic terminal of rod bipolar cells. NeuroReport 7, 2176–2180.

    PubMed  Google Scholar 

  • WÄssle, H., GrÜnert, U. & RÖhrenbeck, J. (1995) Immunocytochemical staining of AII amacrine cells in the rat retina with antibodies against parvalbumin. Journal of Comparative Neurology 356, 132–142.

    PubMed  Google Scholar 

  • WÄssle, H., GrÜnert, U., Chun, M.-H. & Boycott, B. B. (1995) The rod pathway of the macaque monkey retina: Identification of AII-amacrine cells with antibodies against calretinin. Journal of Comparative Neurology 361, 537–551.

    PubMed  Google Scholar 

  • West, R. W. & Dowling, J. E. (1972) Synapses onto different morphological types of retinal ganglion cells. Science 178, 510–512.

    PubMed  Google Scholar 

  • West, R. W. (1976) Light and electron microscopy of the ground squirrel retina: Functional considerations. Journal of Comparative Neurology 168, 355–378.

    PubMed  Google Scholar 

  • West, R. W. (1978) Bipolar, and horizontal cells of the gray squirrel retina: Golgi morphology and receptor connections. Vision Research 18, 129–136.

    PubMed  Google Scholar 

  • Wright, L. L., Macqueen, C. L., Elston, G. N., Young, H. M., Pow, D. V. & Vaney, D. I. (1997) The DAPI-3 amacrine cells of the rabbit retina.Visual Neuroscience 14, 473–492.

    PubMed  Google Scholar 

  • Yoshida, K., Watanabe, D., Ishikane, H., Tachibana, M., Pastan, I. & Nakanishi, S. (2001) A key role of starburst amacrine cells in originating retinal directional selectivity and optokinetic eye movement. Neuron 30, 771–780.

    PubMed  Google Scholar 

  • Zhang, L., Dekorver, L. & Kolb, H. (1995) PKCαβ and PKC-β immunostaining in the cat retina. Investigative Ophthalmology & Visual Science 36, S282.

    Google Scholar 

  • Zucker, C. L. & Ehinger, B. (2001) Complexities of retinal circuitry revealed by neurotransmitter receptor localization. In “Concepts and Challenges in Retinal Biology: A Tribute to John E. Dowling, ” Brain Research Reviews (edited by Kolb, H., Ripps, H. & Wu, S.) pp. 71–81. Elsevier Press.

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Cuenca, N., Deng, P., Linberg, K.A. et al. The neurons of the ground squirrel retina as revealed by immunostains for calcium binding proteins and neurotransmitters. J Neurocytol 31, 649–666 (2002). https://doi.org/10.1023/A:1025791512555

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1025791512555

Keywords

Navigation