Hostname: page-component-cd9895bd7-gvvz8 Total loading time: 0 Render date: 2024-12-27T14:00:00.182Z Has data issue: false hasContentIssue false
  • English
  • Français

Bipolar input to melanopsin containing ganglion cells in primate retina

Published online by Cambridge University Press:  18 October 2010

ULRIKE GRÜNERT ,
PATRICIA R. JUSUF ,
SAMMY C.S. LEE  and
DUNG THAN NGUYEN
ULRIKE GRÜNERT*
Affiliation:
Department of Ophthalmology Save Sight Institute, The University of Sydney, Eye Hospital Campus, Sydney, Australia Department of Optometry and Vision Sciences, The University of Melbourne, Parkville, Australia Australian Research Council Centre of Excellence in Vision Science, University of Sydney, Australia
PATRICIA R. JUSUF
Affiliation:
Department of Optometry and Vision Sciences, The University of Melbourne, Parkville, Australia
SAMMY C.S. LEE
Affiliation:
Department of Optometry and Vision Sciences, The University of Melbourne, Parkville, Australia
DUNG THAN NGUYEN
Affiliation:
Department of Optometry and Vision Sciences, The University of Melbourne, Parkville, Australia
*
*Address correspondence and reprint requests to: Ulrike Grünert, Save Sight Institute, The University of Sydney, Eye Hospital Campus, Sydney, NSW 2001, Australia. E-mail: ugrunert@sydney.edu.au
Get access Rights & Permissions [Opens in a new window]

Abstract

Two morphological types of melanopsin-expressing ganglion cells have been described in primate retina. Both types show intrinsic light responses as well as rod- and cone-driven ON-type responses. Outer stratifying cells have their dendrites close to the inner nuclear layer (OFF sublamina); inner stratifying cells have their dendrites close to the ganglion cell layer (ON sublamina). Both inner and outer stratifying cells receive synaptic input via ribbon synapses, but the bipolar cell types providing this input have not been identified. Here, we addressed the question whether the diffuse (ON) cone bipolar type DB6 and/or rod bipolar cells contact melanopsin-expressing ganglion cells. Melanopsin containing ganglion cells in marmoset (Callithrix jacchus) and macaque (Macaca fascicularis) retinas were identified immunohistochemically; DB6 cells were labeled with antibodies against the carbohydrate epitope CD15, rod bipolar cells were labeled with antibodies against protein kinase C, and putative synapses between the two cells types were identified with antibodies against piccolo. For one inner cell, nearly all of the DB6 axon terminals that overlap with its dendrites in the two-dimensional space show areas of close contact. In vertical sections, the large majority of the areas of close contact also contain a synaptic punctum, suggesting that DB6 cells contact inner melanopsin cells. The output from DB6 cells accounts for about 30% of synapses onto inner melanopsin cells. Synaptic contacts between rod bipolar axons and inner dendrites were not observed. In the OFF sublamina, about 10% of the DB6 axons are closely associated with dendrites of outer cells, and in about a third of these areas, axonal en passant synapses are detected. This result suggests that DB6 cells may also provide input to outer melanopsin cells.

Keywords

Bipolar synapsesIntrinsically photosensitive ganglion cellsCallithrix jacchusMacaca fascicularis
Type
Research Article
Information
Visual Neuroscience , Volume 28 , Issue 1 , January 2011 , pp. 39 - 50
Copyright
Copyright © Cambridge University Press 2010

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

Andressen, C. & Mai, J.K. (1997). Localization of the CD15 carbohydrate epitope in the vertebrate retina. Visual Neuroscience 14, 253–262.Google Scholar
Baver, S.B., Pickard, G.E., Sollars, P.J. & Pickard, G.E. (2008). Two types of melanopsin retinal ganglion cell differentially innervate the hypothalamic suprachiasmatic nucleus and the olivary pretectal nucleus. The European Journal of Neuroscience 27, 1763–1770.Google Scholar
Belenky, M.A., Smeraski, C.A., Provencio, I., Sollars, P.J. & Pickard, G.E. (2003). Melanopsin retinal ganglion cells receive bipolar and amacrine cell synapses. The Journal of Comparative Neurology 460, 380–393.Google Scholar
Berson, D.M., Castrucci, A.M. & Provencio, I. (2010). Morphology and mosaics of melanopsin-expressing retinal ganglion cell types in mice. The Journal of Comparative Neurology 518, 2405–2422.CrossRefGoogle ScholarPubMed
Boycott, B.B. & Wässle, H. (1991). Morphological classification of bipolar cells of the primate retina. The European Journal of Neuroscience 3, 1069–1088.CrossRefGoogle ScholarPubMed
Calkins, D.J., Schein, S.J., Tsukamoto, Y. & Sterling, P. (1994). M and L cones in macaque fovea connect to midget ganglion cells by different numbers of excitatory synapses. Nature 371, 70–72.Google Scholar
Calkins, D.J., Tsukamoto, Y. & Sterling, P. (1998). Microcircuitry and mosaic of a blue-yellow ganglion cell in the primate retina. The Journal of Neuroscience 18, 3373–3385.CrossRefGoogle ScholarPubMed
Cases-Langhoff, C., Voss, B., Garner, A.M., Appeltauer, U., Takei, K., Kindler, S., Veh, R.W., De Camilli, P., Gundelfinger, E.D. & Garner, C.C. (1996). Piccolo, a novel 420 kDa protein associated with the presynaptic cytomatrix. European Journal of Cell Biology 69, 214–223.Google 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. The Journal of Comparative Neurology 437, 219–239.CrossRefGoogle ScholarPubMed
Chan, T.L., Martin, P.R. & Grünert, U. (2001). Immunocytochemical identification and analysis of the diffuse bipolar cell type DB6 in macaque monkey retina. The European Journal of Neuroscience 13, 829–832.CrossRefGoogle ScholarPubMed
Contini, M., Lin, B., Kobayashi, K., Okano, H., Masland, R.H. & Raviola, E. (2010). Synaptic input of ON-bipolar cells onto the dopaminergic neurons of the mouse retina. The Journal of Comparative Neurology 518, 2035–2050.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 Scholar
Dick, O., Hack, I., Altrock, W.D., Garner, C.C., Gundelfinger, E.D. & Brandstätter, J.H. (2001). Localization of the presynaptic cytomatrix protein piccolo at ribbon and conventional synapses in the rat retina: Comparison with bassoon. The Journal of Comparative Neurology 439, 224–234.Google Scholar
Dumitrescu, O.N., Pucci, F.G., Wong, K.Y. & Berson, D.M. (2009). Ectopic retinal ON bipolar cell synapses in the OFF inner plexiform layer: Contacts with dopaminergic amacrine cells and melanopsin ganglion cells. The Journal of Comparative Neurology 517, 226–244.Google Scholar
Famiglietti, E.V. & Kolb, H. (1976). Structural basis for ON- and OFF-center responses in retinal ganglion cells. Science 194, 193–195.Google Scholar
Ghosh, K.K. & Grünert, U. (1999). Synaptic input to small bistratified (blue-on) ganglion cells in the retina of a New World monkey, the marmoset Callithrix jacchus. The Journal of Comparative Neurology 413, 417–428.3.0.CO;2-H>CrossRefGoogle ScholarPubMed
Ghosh, K.K., Martin, P.R. & Grünert, U. (1997). Morphological analysis of the blue cone pathway in the retina of a New World monkey, the marmoset Callithrix jacchus. The Journal of Comparative Neurology 379, 211–225.3.0.CO;2-6>CrossRefGoogle ScholarPubMed
Greferath, U., Grünert, U. & Wässle, H. (1990). Rod bipolar cells in the mammalian retina show protein kinase C-like immunoreactivity. The Journal of Comparative Neurology 301, 433–442.Google Scholar
Grünert, U., Haverkamp, S., Fletcher, E.L. & Wässle, H. (2002). Synaptic distribution of ionotropic glutamate receptors in the inner plexiform layer of the primate retina. The Journal of Comparative Neurology 447, 138–151.CrossRefGoogle ScholarPubMed
Grünert, U., Lin, B. & Martin, P.R. (2003). Glutamate receptors at bipolar synapses in the inner plexiform layer of primate retina: Light microscopic analysis. The Journal of Comparative Neurology 466, 136–147.CrossRefGoogle ScholarPubMed
Grünert, U. & Martin, P.R. (1991). Rod bipolar cells in the macaque monkey retina: Immunoreactivity and connectivity. The Journal of Neuroscience 11, 2742–2758.CrossRefGoogle ScholarPubMed
Grünert, U., Martin, P.R. & Wässle, H. (1994). Immunocytochemical analysis of bipolar cells in the macaque monkey retina. The Journal of Comparative Neurology 348, 607–627.Google Scholar
Gustincich, S., Feigenspan, A., Wu, D.K., Koopman, L.J. & Raviola, E. (1997). Control of dopamine release in the retina: A transgenic approach to neural networks. Neuron 18, 723–736.Google Scholar
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.Google Scholar
Harlow, E. & Lane, D. (1988). Antibodies. A Laboratory Manual. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.Google Scholar
Hattar, S., Kumar, M., Park, A., Tong, P., Tung, J., Yau, K.W. & Berson, D.M. (2006). Central projections of melanopsin-expressing retinal ganglion cells in the mouse. The Journal of Comparative Neurology 497, 326–349.Google Scholar
Hendrickson, A., Troilo, D., Djajadi, H., Possin, D. & Springer, A. (2009). Expression of synaptic and phototransduction markers during photoreceptor development in the marmoset monkey Callithrix jacchus. The Journal of Comparative Neurology 512, 218–231.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. The Journal of Neuroscience 29, 8875–8883.Google Scholar
Jusuf, P.R., Lee, S.C.S. & Grünert, U. (2004). Synaptic connectivity of the diffuse bipolar cell type DB6 in the inner plexiform layer of primate retina. The Journal of Comparative Neurology 469, 494–506.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. The European Journal of Neuroscience 26, 2906–2921.Google Scholar
Jusuf, P.R., Martin, P.R. & Grünert, U. (2006). Synaptic connectivity in the midget-parvocellular pathway of primate central retina. The Journal of Comparative Neurology 494, 260–274.CrossRefGoogle ScholarPubMed
Kolb, H. & DeKorver, L. (1991). Midget ganglion cells of the parafovea of the human retina: A study by electron microscopy and serial section reconstructions. The Journal of Comparative Neurology 303, 617–636.CrossRefGoogle ScholarPubMed
Kolb, H. & Famiglietti, E.V. (1974). Rod and cone pathways in the inner plexiform layer of cat retina. Science 186, 47–49.Google Scholar
Kouyama, N. & Marshak, D.W. (1992). Bipolar cells specific for blue cones in the macaque retina. The Journal of Neuroscience 12, 1233–1252.Google Scholar
MacNeil, M.A., Heussy, J.K., Dacheux, R.F., Raviola, E. & Masland, R.H. (2004). The population of bipolar cells in the rabbit retina. The Journal of Comparative Neurology 472, 73–86.CrossRefGoogle ScholarPubMed
Marshak, D.W., Aldrich, L.B., Del Valle, J. & Yamada, T. (1990). Localization of immunoreactive cholecystokinin precursor to amacrine cells and bipolar cells of the macaque monkey retina. The Journal of Neuroscience 10, 3045–3055.CrossRefGoogle ScholarPubMed
Nelson, R., Famiglietti, E.V. & Kolb, H. (1978). Intracellular staining reveals different levels of stratification for On- and Off-center ganglion cells in cat retina. Journal of Neurophysiology 41, 472–483.Google Scholar
Østergaard, J., Hannibal, J. & Fahrenkrug, J. (2007). Synaptic contact between melanopsin-containing retinal ganglion cells and rod bipolar cells. Investigative Ophthalmology & Visual Science 48, 3812–3820.CrossRefGoogle ScholarPubMed
Provencio, I. (2008) Melanopsin cells. In The Senses. A Comprehensive Reference. Vol. 1, Vision I, ed. Basbaum, A., Kaneko, A., Shepherd, G. & Westheimer, G., pp. 423–431. San Diego, CA: Academic Press.Google Scholar
Schmidt, T.M. & Kofuji, P. (2009). Functional and morphological differences among intrinsically photosensitive retinal ganglion cells. The Journal of Neuroscience 29, 476–482.CrossRefGoogle ScholarPubMed
Schmitz, F., Königstorfer, A. & Südhof, 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.Google Scholar
Strettoi, E., Dacheux, R.F. & Raviola, E. (1990). Synaptic connections of rod bipolar cells in the inner plexiform layer of the rabbit retina. The Journal of Comparative Neurology 295, 449–466.CrossRefGoogle ScholarPubMed
Szmajda, B.A., Grünert, U. & Martin, P.R. (2008). Retinal ganglion cell inputs to the koniocellular pathway. The Journal of Comparative Neurology 510, 251–268.CrossRefGoogle Scholar
tom Dieck, S., Altrock, W.D., Kessels, M.M., Qualmann, B., Regus, H., Brauner, D., Fejtova, 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. The Journal of Cell Biology 168, 825–836.CrossRefGoogle ScholarPubMed
Viney, T.J., Balint, K., Hillier, D., Siegert, S., Boldogkoi, Z., Enquist, L.W., Meister, M., Cepko, C.L. & Roska, B. (2007). Local retinal circuits of melanopsin-containing ganglion cells identified by transsynaptic viral tracing. Current Biology 17, 981–988.Google Scholar