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Melanopsin and calbindin immunoreactivity in the inner retina of humans and marmosets

Published online by Cambridge University Press:  18 June 2019

Ashleigh J. Chandra ,
Sammy C.S. Lee  and
Ulrike Grünert Open the ORCID record for Ulrike Grünert [Opens in a new window]
Ashleigh J. Chandra
Affiliation:
Save Sight Institute, Discipline of Clinical Ophthalmology, Sydney Medical School, The University of Sydney, Sydney, NSW 2000, Australia Australian Research Council Centre of Excellence for Integrative Brain Function, Sydney Node, The University of Sydney, Sydney, NSW 2000, Australia
Sammy C.S. Lee
Affiliation:
Save Sight Institute, Discipline of Clinical Ophthalmology, Sydney Medical School, The University of Sydney, Sydney, NSW 2000, Australia Australian Research Council Centre of Excellence for Integrative Brain Function, Sydney Node, The University of Sydney, Sydney, NSW 2000, Australia
Ulrike Grünert*
Affiliation:
Save Sight Institute, Discipline of Clinical Ophthalmology, Sydney Medical School, The University of Sydney, Sydney, NSW 2000, Australia Australian Research Council Centre of Excellence for Integrative Brain Function, Sydney Node, The University of Sydney, Sydney, NSW 2000, Australia
*
*Address correspondence to: Ulrike Grünert, Email: [email protected]
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Abstract

In primate retina, the calcium-binding protein calbindin is expressed by a variety of neurons including cones, bipolar cells, and amacrine cells but it is not known which type(s) of cell express calbindin in the ganglion cell layer. The present study aimed to identify calbindin-positive cell type(s) in the amacrine and ganglion cell layer of human and marmoset retina using immunohistochemical markers for ganglion cells (RBPMS and melanopsin) and cholinergic amacrine (ChAT) cells. Intracellular injections following immunolabeling was used to reveal the morphology of calbindin-positive cells. In human retina, calbindin-labeled cells in the ganglion cell layer were identified as inner and outer stratifying melanopsin-expressing ganglion cells, and ON ChAT (starburst amacrine) cells. In marmoset, calbindin immunoreactivity in the ganglion cell layer was absent from ganglion cells but present in ON ChAT cells. In the inner nuclear layer of human retina, calbindin was found in melanopsin-expressing displaced ganglion cells and in at least two populations of amacrine cells including about a quarter of the OFF ChAT cells. In marmoset, a very low proportion of OFF ChAT cells was calbindin-positive. These results suggest that in both species there may be two types of OFF ChAT cells. Consistent with previous studies, the ratio of ON to OFF ChAT cells was about 70 to 30 in human and 30 to 70 in marmoset. Our results show that there are species-related differences between different primates with respect to the expression of calbindin.

Keywords

Calcium-binding proteinCholinergic amacrine cellsMelanopsin-expressing ganglion cellsPrimate retina
Type
Research Article
Information
Visual Neuroscience , Volume 36 , 2019 , E009
Copyright
Copyright © Cambridge University Press 2019 

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References

Baden, T., Berens, P., Franke, K., Roman Roson, M., Bethge, M. & Euler, T. (2016). The functional diversity of retinal ganglion cells in the mouse. Nature 529, 345–350.CrossRefGoogle ScholarPubMed
Baimbridge, K.G., Celio, M.R. & Rogers, J.H. (1992). Calcium-binding proteins in the nervous system. Trends in Neurosciences 15, 303–308.CrossRefGoogle Scholar
Chan, T.L., Martin, P.R., Clunas, N. & Grünert, U. (2001). Bipolar cell diversity in the primate retina: Morphologic and immunocytochemical analysis of a New World monkey, the marmoset Callithrix jacchus. Journal of Comparative Neurology 437, 219–239.CrossRefGoogle ScholarPubMed
Chandra, A.J., Lee, S.C.S. & Grünert, U. (2017). Thorny ganglion cells in marmoset retina: Morphological and neurochemical characterization with antibodies against calretinin. Journal of Comparative Neurology 525, 3962–3974.CrossRefGoogle ScholarPubMed
Chen, S.K., Badea, T.C. & Hattar, S. (2011). Photoentrainment and pupillary light reflex are mediated by distinct populations of ipRGCs. Nature 476, 92–95.CrossRefGoogle ScholarPubMed
Chiquet, C., Dkhissi-Benyahya, O. & Cooper, H.M. (2005). Calcium-binding protein distribution in the retina of strepsirhine and haplorhine primates. Brain Research Bulletin 68, 185–194.CrossRefGoogle ScholarPubMed
Cuenca, N., Deng, P., Linberg, K.A., Fisher, S.K. & Kolb, H. (2003). Choline acetyltransferase is expressed by non-starburst amacrine cells in the ground squirrel retina. Brain Research 964, 21–30.CrossRefGoogle ScholarPubMed
Curcio, C.A. & Allen, K.A. (1990). Topography of ganglion cells in human retina. Journal of Comparative Neurology 300, 5–25.CrossRefGoogle ScholarPubMed
Dacey, D.M. (2004). Origins of perception: Retinal ganglion cell diversity and the creation of parallel visual pathways. In The Cognitive Neurosciences, ed. Gazzaniga, M.S., pp. 281–301. Cambridge: MIT Press.Google Scholar
Dacey, D.M., Liao, H.-W., Peterson, B.B., Robinson, F.R., Smith, V.C., Pokorny, J., Yau, K.-W. & Gamlin, P.D. (2005). Melanopsin-expressing ganglion cells in primate retina signal colour irradiance and project to the LGN. Nature 433, 749–754.CrossRefGoogle ScholarPubMed
Dacey, D.M., Peterson, B.B., Robinson, F.R. & Gamlin, P.D. (2003). Fireworks in the primate retina: In vitro photodynamics reveals diverse LGN-projecting ganglion cell types. Neuron 37, 15–27.CrossRefGoogle ScholarPubMed
de Souza, C.F., Nivison-Smith, L., Christie, D.L., Polkinghorne, P., McGhee, C., Kalloniatis, M. & Acosta, M.L. (2016). Macromolecular markers in normal human retina and applications to human retinal disease. Experimental Eye Research 150, 135–148.CrossRefGoogle ScholarPubMed
Ford, K.J. & Feller, M.B. (2012). Assembly and disassembly of a retinal cholinergic network. Visual Neuroscience 29, 61–71.CrossRefGoogle ScholarPubMed
Gábriel, R. & Witkovsky, P. (1998). Cholinergic, but not the rod pathway-related glycinergic (AII) amacrine cells contain calretinin in the rat retina. Neuroscience Letters 247, 179–182.CrossRefGoogle Scholar
Gu, Y.N., Lee, E.S. & Jeon, C.J. (2016). Types and density of calbindin D28k-immunoreactive ganglion cells in mouse retina. Experimental Eye Research 145, 327–336.CrossRefGoogle ScholarPubMed
Haley, T.L., Pochet, R., Baizer, L., Burton, M.D., Crabb, J.W., Parmentier, M. & Polans, A.S. (1995). Calbindin D-28k immunoreactivity of human cone cells varies with retinal position. Visual Neuroscience 12, 301–307.CrossRefGoogle ScholarPubMed
Hamano, K., Kiyama, H., Emson, P.C., Manabe, R., Nakauchi, M. & Tohyama, M. (1990). Localization of two calcium binding proteins, calbindin (28 kD) and parvalbumin (12 kD), in the vertebrate retina. Journal of Comparative Neurology 302, 417–424.CrossRefGoogle Scholar
Hannibal, J., Christiansen, A.T., Heegaard, S., Fahrenkrug, J. & Kiilgaard, J.F. (2017). Melanopsin expressing human retinal ganglion cells: Subtypes, distribution, and intraretinal connectivity. Journal of Comparative Neurology 525, 1934–1961.CrossRefGoogle ScholarPubMed
Hannibal, J., Hindersson, P., Østergaard, J., Georg, B., Heegaard, S., Larsen, P.J. & Fahrenkrug, J. (2004). Melanopsin is expressed in PACAP-containing retinal ganglion cells of the human retinohypothalamic tract. Investigative Ophthalmology & Visual Science 45, 4202–4209.CrossRefGoogle ScholarPubMed
Haverkamp, S., Haeseleer, F. & Hendrickson, A. (2003). A comparison of immunocytochemical markers to identify bipolar cell types in human and monkey retina. Visual Neuroscience 20, 589–600.CrossRefGoogle ScholarPubMed
Haverkamp, S. & Wässle, H. (2000). Immunocytochemical analysis of the mouse retina. Journal of Comparative Neurology 424, 1–23.3.0.CO;2-V>CrossRefGoogle ScholarPubMed
Heizmann, C.W. & Hunziker, W. (1991). Intracellular calcium-binding proteins: More sites than insights. Trends in Biochemical Sciences 16, 98–103.CrossRefGoogle ScholarPubMed
Hoshi, H., Liu, W.L., Massey, S.C. & Mills, S.L. (2009). ON inputs to the OFF layer: Bipolar cells that break the stratification rules of the retina. Journal of Neuroscience 29, 8875–8883.CrossRefGoogle ScholarPubMed
Jacoby, R.A. & Marshak, D.W. (2000). Synaptic connections of DB3 diffuse bipolar cell axons in macaque retina. Journal of Comparative Neurology 416, 19–29.3.0.CO;2-H>CrossRefGoogle ScholarPubMed
Jacoby, R.A., Wiechmann, A.F., Amara, S.G., Leighton, B.H. & Marshak, D.W. (2000). Diffuse bipolar cells provide input to OFF parasol ganglion cells in the macaque retina. Journal of Comparative Neurology 416, 6–18.3.0.CO;2-X>CrossRefGoogle ScholarPubMed
Jeong, M.J. & Jeon, C.J. (2015). Localization of melanopsin-immunoreactive cells in the Mongolian gerbil retina. Neuroscience Research 100, 6–16.CrossRefGoogle ScholarPubMed
Johnson, E.N., Westbrook, T., Shayesteh, R., Chen, E.L., Schumacher, J.W., Fitzpatrick, D. & Field, G.D. (2019). Distribution and diversity of intrinsically photosensitive retinal ganglion cells in tree shrew. Journal of Comparative Neurology 527, 328–344.CrossRefGoogle ScholarPubMed
Jusuf, P.R., Lee, S.C.S., Hannibal, J. & Grünert, U. (2007). Characterization and synaptic connectivity of melanopsin-containing ganglion cells in the primate retina. European Journal of Neuroscience 26, 2906–2921.CrossRefGoogle ScholarPubMed
Kántor, O., Mezey, S., Adeghate, J., Naumann, A., Nitschke, R., Enzsoly, A., Szabó, A., Lukats, A., Nemeth, J., Somogyvari, Z. & Völgyi, B. (2016). Calcium buffer proteins are specific markers of human retinal neurons. Cell and Tissue Research 365, 29–50.CrossRefGoogle ScholarPubMed
Kao, Y.H. & Sterling, P. (2003). Matching neural morphology to molecular expression: Single cell injection following immunostaining. Journal of Neurocytology 32, 245–251.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle Scholar
Kolb, H., Linberg, K.A. & Fisher, S.K. (1992). Neurons of the human retina: A Golgi study. Journal of Comparative Neurology 318, 146–187.Google ScholarPubMed
Kriegsfeld, L.J., Mei, D.F., Yan, L., Witkovsky, P., Lesauter, J., Hamada, T. & Silver, R. (2008). Targeted mutation of the calbindin D28K gene disrupts circadian rhythmicity and entrainment. European Journal of Neuroscience 27, 2907–2921.CrossRefGoogle ScholarPubMed
Kwong, J.M., Caprioli, J. & Piri, N. (2010). RNA binding protein with multiple splicing: A new marker for retinal ganglion cells. Investigative Ophthalmology & Visual Science 51, 1052–1058.CrossRefGoogle ScholarPubMed
Lee, E.S. & Jeon, C.J. (2013). Starburst amacrine cells express parvalbumin but not calbindin and calretinin in rabbit retina. NeuroReport 24, 918–923.CrossRefGoogle Scholar
Lee, S.C., Weltzien, F., Madigan, M.C., Martin, P.R. & Grünert, U. (2016). Identification of AII amacrine, displaced amacrine and bistratified ganglion cell types in human retina with antibodies against calretinin. Journal of Comparative Neurology 524, 39–53.CrossRefGoogle Scholar
Li, J.Y. & Schmidt, T.M. (2018). Divergent projection patterns of M1 ipRGC subtypes. Journal of Comparative Neurology 526, 2010–2018.CrossRefGoogle ScholarPubMed
Liao, H.W., Ren, X., Peterson, B.B., Marshak, D.W., Yau, K.W., Gamlin, P.D. & Dacey, D.M. (2016). Melanopsin-expressing ganglion cells in macaque and human retinas form two morphologically distinct populations. Journal of Comparative Neurology 524, 2845–2872.CrossRefGoogle ScholarPubMed
Luo, X., Ghosh, K.K., Martin, P.R. & Grünert, U. (1999). Analysis of two types of cone bipolar cells in the retina of a New World monkey, the marmoset, Callithrix jacchus. Visual Neuroscience 16, 709–719.CrossRefGoogle ScholarPubMed
Martin, P.R. & Grünert, U. (1992). Spatial density and immunoreactivity of bipolar cells in the macaque monkey retina. Journal of Comparative Neurology 323, 269–287.CrossRefGoogle ScholarPubMed
Martínez-Navarrete, G.C., Angulo, A., Martín-Nieto, J. & Cuenca, N. (2008). Gradual morphogenesis of retinal neurons in the peripheral retinal margin of adult monkeys and humans. Journal of Comparative Neurology 511, 557–580.CrossRefGoogle ScholarPubMed
Masri, R.A., Percival, K.A., Koizumi, A., Martin, P.R. & Grünert, U. (2019). Survey of retinal ganglion cell morphology in marmoset. Journal of Comparative Neurology 527, 236–258.CrossRefGoogle ScholarPubMed
Milam, A.H., Dacey, D.M. & Dizhoor, A.M. (1993). Recoverin immunoreactivity in mammalian cone bipolar cells. Visual Neuroscience 10, 1–12.CrossRefGoogle ScholarPubMed
Moritoh, S., Komatsu, Y., Yamamori, T. & Koizumi, A. (2013). Diversity of retinal ganglion cells identified by transient GFP transfection in organotypic tissue culture of adult marmoset monkey retina. PLoS One 8, e54667.CrossRefGoogle ScholarPubMed
Nasir-Ahmad, S., Lee, S.C.S., Martin, P.R. & Grünert, U. (2019). Melanopsin-expressing ganglion cells in human retina: Morphology, distribution, and synaptic connections. Journal of Comparative Neurology 527, 312–327.CrossRefGoogle ScholarPubMed
Pasteels, B., Rogers, J., Blachier, F. & Pochet, R. (1990). Calbindin and calretinin localization in retina from different species. Visual Neuroscience 5, 1–16.CrossRefGoogle ScholarPubMed
Peterson, B.B. & Dacey, D.M. (1999). Morphology of wide-field, monostratified ganglion cells of the human retina. Visual Neuroscience 16, 107–120.CrossRefGoogle ScholarPubMed
Pinol, M.R., Kägi, U., Heizmann, C.W., Vogel, B., Séquier, J.-M., Haas, W. & Hunziker, W. (1990). Poly- and monoclonal antibodies against recombinant rat brain calbindin D-28k were produced to map its selective distribution in the central nervous system. Journal of Neurochemistry 54, 1827–1833.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Puthussery, T, Gayet-Primo, J, Taylor, WR, Haverkamp, S. (2011). Immunohistochemical identification and synaptic inputs to the diffuse bipolar cell type DB1 in macaque retina. Journal of Comparative Neurology 519, 3640–3656.CrossRefGoogle ScholarPubMed
Rodieck, R.W. (1989). Starburst amacrine cells in the primate retina. Journal of Comparative Neurology 285, 18–37.CrossRefGoogle ScholarPubMed
Rodieck, R.W. & Marshak, D.W. (1992). Spatial density and distribution of choline acetyltransferase immunoreactive cells in human, macaque, and baboon retinas. Journal of Comparative Neurology 321, 46–64.CrossRefGoogle ScholarPubMed
Rodieck, R.W. & Watanabe, M. (1993). Survey of the morphology of macaque retinal ganglion cells that project to the pretectum, superior colliculus, and parvicellular laminae of the lateral geniculate nucleus. Journal of Comparative Neurology 338, 289–303.CrossRefGoogle ScholarPubMed
Rodriguez, A.R., Pérez de Sevilla Müller, L. & Brecha, N.C. (2014). The RNA binding protein RBPMS is a selective marker of ganglion cells in the mammalian retina. Journal of Comparative Neurology 522, 1411–1443.CrossRefGoogle ScholarPubMed
Röhrenbeck, J., Wässle, H. & Boycott, B.B. (1989). Horizontal cells in the monkey retina: Immunocytochemical staining with antibodies against calcium binding proteins. European Journal of Neuroscience 1, 407–420.CrossRefGoogle ScholarPubMed
Roski, C., Langrock, C., Körber, N., Habermann, G., Buse, E., Reichenbach, A., Pannicke, T. & Francke, M. (2018). Comparison of cellular localisation of the Ca2+ -binding proteins calbindin, calretinin and parvalbumin in the retina of four different Macaca species. Anatomia Histologia Embryologia 47, 573–582.CrossRefGoogle ScholarPubMed
Sanes, J.R. & Masland, R.H. (2015). The types of retinal ganglion cells: Current status and implications for neuronal classification. Annual Review of Neuroscience 38, 221–246.CrossRefGoogle ScholarPubMed
Schindelin, J., Arganda-Carreras, I., Frise, E., Kaynig, V., Longair, M., Pietzsch, T., Preibisch, S., Rueden, C., Saalfeld, S., Schmid, B., Tinevez, J.Y., White, D.J., Hartenstein, V., Eliceiri, K., Tomancak, P. & Cardona, A. (2012). Fiji: An open-source platform for biological-image analysis. Nature Methods 9, 676–682.CrossRefGoogle ScholarPubMed
Schmidt, H. (2012). Three functional facets of calbindin D-28k. Frontiers in Molecular Neuroscience 5, 25.CrossRefGoogle ScholarPubMed
Schwaller, B., Meyer, M. & Schiffmann, S. (2002). ‘New’ functions for ‘old’ proteins: The role of the calcium-binding proteins calbindin D-28k, calretinin and parvalbumin, in cerebellar physiology. Studies with knockout mice. The Cerebellum 1, 241–258.CrossRefGoogle ScholarPubMed
Szmajda, B.A., Grünert, U. & Martin, P.R. (2008). Retinal ganglion cell inputs to the koniocellular pathway. Journal of Comparative Neurology 510, 251–268.CrossRefGoogle ScholarPubMed
Vaney, D.I., Sivyer, B. & Taylor, W.R. (2012). Direction selectivity in the retina: Symmetry and asymmetry in structure and function. Nature Reviews Neuroscience 13, 194–208.CrossRefGoogle ScholarPubMed
Wässle, H., Dacey, D., Haun, T., Haverkamp, S., Grünert, U. & Boycott, B.B. (2000). The mosaic of horizontal cells in the macaque monkey retina: With a comment on biplexiform ganglion cells. Visual Neuroscience 17, 591–608.CrossRefGoogle ScholarPubMed
Wässle, H., Peichl, L., Airaksinen, M.S. & Meyer, M. (1998). Calcium-binding proteins in the retina of a calbindin-null mutant mouse. Cell and Tissue Research 292, 211–218.Google ScholarPubMed
Weltzien, F., Dimarco, S., Protti, D.A., Daraio, T., Martin, P.R. & Grünert, U. (2014). Characterization of secretagogin immunoreactive amacrine cells in marmoset retina. Journal of Comparative Neurology 522, 435–455.CrossRefGoogle ScholarPubMed
Weltzien, F., Percival, K.A., Martin, P.R. & Grünert, U. (2015). Analysis of bipolar and amacrine populations in marmoset retina. Journal of Comparative Neurology 523, 313–334.CrossRefGoogle ScholarPubMed
Yamada, E.S., Bordt, A.S. & Marshak, D.W. (2005). Wide-field ganglion cells in macaque retinas. Visual Neuroscience 22, 383–393.CrossRefGoogle ScholarPubMed
Zhang, C., Yu, W.Q., Hoshino, A., Huang, J., Rieke, F., Reh, T.A. & Wong, R.O.L. (2019). Development of ON and OFF cholinergic amacrine cells in the human fetal retina. Journal of Comparative Neurology 527, 174–186.CrossRefGoogle Scholar