Hostname: page-component-78c5997874-g7gxr Total loading time: 0 Render date: 2024-11-11T18:05:34.926Z Has data issue: false hasContentIssue false
  • English
  • Français

Amacrine and bipolar inputs to midget and parasol ganglion cells in marmoset retina

Published online by Cambridge University Press:  08 May 2012

CARLA J. ABBOTT ,
KUMIKO A. PERCIVAL ,
PAUL R. MARTIN  and
ULRIKE GRÜNERT
CARLA J. ABBOTT
Affiliation:
Department of Ophthalmology and Save Sight Institute, The University of Sydney, Sydney, New South Wales, Australia Australian Research Council Centre of Excellence in Vision Science, The University of Sydney, Sydney, New South Wales, Australia
KUMIKO A. PERCIVAL
Affiliation:
Department of Ophthalmology and Save Sight Institute, The University of Sydney, Sydney, New South Wales, Australia Australian Research Council Centre of Excellence in Vision Science, The University of Sydney, Sydney, New South Wales, Australia
PAUL R. MARTIN
Affiliation:
Department of Ophthalmology and Save Sight Institute, The University of Sydney, Sydney, New South Wales, Australia Australian Research Council Centre of Excellence in Vision Science, The University of Sydney, Sydney, New South Wales, Australia
ULRIKE GRÜNERT*
Affiliation:
Department of Ophthalmology and Save Sight Institute, The University of Sydney, Sydney, New South Wales, Australia Australian Research Council Centre of Excellence in Vision Science, The University of Sydney, Sydney, New South Wales, Australia
*
*Address correspondence and reprint requests to: Ulrike Grünert, Save Sight Institute, Sydney Eye Hospital Campus, GPO Box 4337, Sydney, NSW 2001, Australia, E-mail: ugrunert@sydney.edu.au
Get access Rights & Permissions [Opens in a new window]

Abstract

Retinal ganglion cells receive excitatory synapses from bipolar cells and inhibitory synapses from amacrine cells. Previous studies in primate suggest that the strength of inhibitory amacrine input is greater to cells in peripheral retina than to foveal (central) cells. A comprehensive study of a large number of ganglion cells at different eccentricities, however, is still lacking. Here, we compared the amacrine and bipolar input to midget and parasol ganglion cells in central and peripheral retina of marmosets (Callithrix jacchus). Ganglion cells were labeled by retrograde filling from the lateral geniculate nucleus or by intracellular injection. Presumed amacrine input was identified with antibodies against gephyrin; presumed bipolar input was identified with antibodies against the GluR4 subunit of the AMPA receptor. In vertical sections, about 40% of gephyrin immunoreactive (IR) puncta were colocalized with GABAA receptor subunits, whereas immunoreactivity for gephyrin and GluR4 was found at distinct sets of puncta. The density of gephyrin IR puncta associated with ganglion cell dendrites was comparable for midget and parasol cells at all eccentricities studied (up to 2 mm or about 16 degrees of visual angle for midget cells and up to 10 mm or >80 degrees of visual angle for parasol cells). In central retina, the densities of gephyrin IR and GluR4 IR puncta associated with the dendrites of midget and parasol cells are comparable, but the average density of GluR4 IR puncta decreased slightly in peripheral parasol cells. These anatomical results indicate that the ratio of amacrine to bipolar input does not account for the distinct functional properties of parasol and midget cells or for functional differences between cells of the same type in central and peripheral retina.

Keywords

Primate retinaInhibitory synapsesCallithrix jacchusExcitatory synapses
Type
Research Articles
Information
Visual Neuroscience , Volume 29 , Issue 3 , May 2012 , pp. 157 - 168
Copyright
Copyright © Cambridge University Press 2012

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

Bordt, A.S., Hoshi, H., Yamada, E.S., Perryman-Stout, W.C. & Marshak, D.W. (2006). Synaptic input to OFF parasol ganglion cells in macaque retina. The Journal of Comparative Neurology 498, 46–57.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.Google Scholar
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. & Sterling, P. (1996). Absence of spectrally specific lateral inputs to midget ganglion cells in primate retina. Nature 381, 613–615.CrossRefGoogle ScholarPubMed
Calkins, D.J. & Sterling, P. (2007). Microcircuitry for two types of achromatic ganglion cell in primate fovea. The Journal of Neuroscience 27, 2646–2653.Google Scholar
Chichilnisky, E.J. & Kalmar, R.S. (2002). Functional asymmetries in ON and OFF ganglion cells of primate retina. The Journal of Neuroscience 22, 2737–2747.CrossRefGoogle Scholar
Dacey, D.M. (1993). The mosaic of midget ganglion cells in the human retina. Journal of Neuroscience 13, 5334–5355.CrossRefGoogle ScholarPubMed
Dacey, D.M. (1999). Primate retina: Cell types, circuits and color opponency. Progress in Retinal and Eye Research 18, 737–763.CrossRefGoogle ScholarPubMed
Dacey, D.M. & Lee, B.B. (1994). The ‘blue-on’ opponent pathway in primate retina originates from a distinct bistratified ganglion cell type. Nature 367, 731–735.Google Scholar
Dacey, D.M. & Petersen, M.R. (1992). Dendritic field size and morphology of midget and parasol ganglion cells of the human retina. Proceedings of the National Academy of Sciences of the U.S.A. 89, 9666–9670.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
DeVries, S.H. (2000). Bipolar cells use kainate and AMPA receptors to filter visual information into separate channels. Neuron 28, 847–856.Google Scholar
DeVries, S.H., Li, W. & Saszik, S. (2006). Parallel processing in two transmitter microenvironments at the cone photoreceptor synapse. Neuron 50, 735–748.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
Eriköz, B., Jusuf, P.R., Percival, K.A. & Grünert, U. (2008). Distribution of bipolar input to midget and parasol ganglion cells in marmoset retina. Visual Neuroscience 25, 67–76.Google Scholar
Fischer, F., Kneussel, M., Tintrup, H., Haverkamp, S., Rauen, T., Betz, H. & Wässle, H. (2000). Reduced synaptic clustering of GABA and glycine receptors in the retina of the gephyrin null mutant mouse. The Journal of Comparative Neurology 427, 634–648.Google Scholar
Freed, M.A. (2000). Parallel cone bipolar pathways to a ganglion cell use different rates and amplitudes of quantal excitation. The Journal of Neuroscience 20, 3956–3963.Google Scholar
Ghosh, K.K., Goodchild, A.K., Sefton, A.E. & Martin, P.R. (1996). Morphology of retinal ganglion cells in a New World monkey, the marmoset Callithrix jacchus. The Journal of Comparative Neurology 366, 76–92.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. & Wässle, H. (1993). Immunocytochemical localization of glycine receptors in the mammalian retina. The Journal of Comparative Neurology 335, 523–537.CrossRefGoogle ScholarPubMed
Harlow, E. & Lane, D. (1988). Antibodies. A laboratory manual. Cold Spring Harbor: Cold Spring Harbor Laboratory.Google Scholar
Haverkamp, S., Grünert, U. & Wässle, H. (2000). The cone pedicle, a complex synapse in the retina. Neuron 27, 85–95.Google Scholar
Haverkamp, S., Grünert, U. & Wässle, H. (2001). The synaptic architecture of AMPA receptors at the cone pedicle of the primate retina. The Journal of Neuroscience 21, 2488–2500.Google Scholar
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.CrossRefGoogle Scholar
Jacoby, R., Stafford, D., Kouyama, N. & Marshak, D. (1996). Synaptic inputs to ON parasol ganglion cells in the primate retina. The Journal of Neuroscience 16, 8041–8056.Google Scholar
Jakobs, T.C., Koizumi, A. & Masland, R.H. (2008). The spatial distribution of glutamatergic inputs to dendrites of retinal ganglion cells. The Journal of Comparative Neurology 510, 221–236.Google Scholar
Jeon, C.-J., Kong, J.-H., Strettoi, E., Rockhill, R., Stasheff, S.F. & Masland, R.H. (2002). Pattern of synaptic excitation and inhibition upon direction-selective retinal ganglion cells. The Journal of Comparative Neurology 449, 195–205.CrossRefGoogle ScholarPubMed
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.Google Scholar
Kier, C.K., Buchsbaum, G. & Sterling, P. (1995). How retinal microcircuits scale for ganglion cells of different size. The Journal of Neuroscience 15, 7673–7683.CrossRefGoogle ScholarPubMed
Kneussel, M. & Betz, H. (2000). Receptors, gephyrin and gephyrin-associated proteins: Novel insights into the assembly of inhibitory postsynaptic membrane specializations. The Journal of Physiology 525, 1–9.CrossRefGoogle ScholarPubMed
Koizumi, A., Jakobs, T.C. & Masland, R.H. (2011). Regular mosaic of synaptic contacts among three retinal neurons. The Journal of Comparative Neurology 519, 341–357.Google Scholar
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., Linberg, K.A. & Fisher, S.K. (1992). Neurons of the human retina: A Golgi study. The Journal of Comparative Neurology 318, 146–187.Google Scholar
Kolb, H. & Marshak, D.W. (2003). The midget pathways of the primate retina. Documenta Ophthalmologica 106, 67–81.Google Scholar
Koontz, M.A. & Hendrickson, A.E. (1987). Stratified distribution of synapses in the inner plexiform layer of primate retina. The Journal of Comparative Neurology 263, 581–592.Google Scholar
Lebedev, D.S. & Marshak, D.W. (2007). Amacrine cell contributions to red-green color opponency in central primate retina: A model study. Visual Neuroscience 24, 535–547.CrossRefGoogle ScholarPubMed
Lee, B.B., Martin, P.R. & Grünert, U. (2010). Retinal connectivity and primate vision. Progress in Retinal and Eye Research 29, 622–639.CrossRefGoogle ScholarPubMed
Leventhal, A.G., Rodieck, R.W. & Dreher, B. (1981). Retinal ganglion cell classes in the Old World monkey: Morphology and central projections. Science 213, 1139–1142.CrossRefGoogle ScholarPubMed
Lin, B., Martin, P.R. & Grünert, U. (2002). Expression and distribution of ionotropic glutamate receptor subunits on parasol ganglion cells in the primate retina. Visual Neuroscience 19, 453–465.Google Scholar
Lin, B., Martin, P.R., Solomon, S.G. & Grünert, U. (2000). Distribution of glycine receptor subunits on primate retinal ganglion cells: A quantitative analysis. The European Journal of Neuroscience 12, 4155–4170.Google Scholar
Macri, J., Martin, P.R. & Grünert, U. (2000). Distribution of the α1 subunit of the GABAA receptor on midget and parasol ganglion cells in the retina of the common marmoset Callithrix jacchus. Visual Neuroscience 17, 437–448.Google Scholar
Majumdar, S., Heinze, L., Haverkamp, S., Ivanova, E. & Wässle, H. (2007). Glycine receptors of A-type ganglion cells of the mouse retina. Visual Neuroscience 24, 471–487.Google Scholar
Marshak, D.W., Yamada, E.S., Bordt, A.S. & Perryman, W.C. (2002). Synaptic input to an ON parasol ganglion cell in the macaque retina: A serial section analysis. Visual Neuroscience 19, 299–305.Google Scholar
Morgan, J.L., Schubert, T. & Wong, R.O. (2008). Developmental patterning of glutamatergic synapses onto retinal ganglion cells. Neural Development 3, 8.Google Scholar
Percival, K.A., Jusuf, P.R., Martin, P.R. & Grünert, U. (2009). Synaptic inputs onto small bistratified (blue-ON/yellow-OFF) ganglion cells in marmoset retina. The Journal of Comparative Neurology 517, 655–669.CrossRefGoogle ScholarPubMed
Percival, K.A., Martin, P.R. & Grünert, U. (2011). Synaptic inputs to two types of koniocellular pathway ganglion cells in marmoset retina. The Journal of Comparative Neurology 519, 2135–2153.Google Scholar
Perry, V.H., Oehler, R. & Cowey, A. (1984). Retinal ganglion cells that project to the dorsal lateral geniculate nucleus in the macaque monkey. Neuroscience 12, 1101–1123.CrossRefGoogle Scholar
Pfeiffer, F., Simler, R., Grenningloh, G. & Betz, H. (1984). Monoclonal antibodies and peptide mapping reveal structural similarities between the subunits of the glycine receptor of rat spinal cord. Proceedings of the National Academy of Sciences of the United States of America 81, 7224–7227.CrossRefGoogle ScholarPubMed
Pourcho, R.G. & Owczarzak, M.T. (1991). Glycine receptor immunoreactivity is localized at amacrine synapses in cat retina. Visual Neuroscience 7, 611–618.Google Scholar
Puller, C. & Haverkamp, S. (2011). Cell-type-specific localization of protocadherin beta16 at AMPA and AMPA/Kainate receptor-containing synapses in the primate retina. The Journal of Comparative Neurology 519, 467–479.Google Scholar
Rodieck, R.W., Binmoeller, K.F. & Dineen, J. (1985). Parasol and midget ganglion cells of the human retina. Journal of Comparative Neurology 233, 115–132.CrossRefGoogle ScholarPubMed
Sassoè-Pognetto, M. & Fritschy, J.-M. (2000). Gephyrin, a major postsynaptic protein of GABAergic synapses. The European Journal of Neuroscience 12, 2205–2210.Google Scholar
Sassoè-Pognetto, M., Kirsch, J., Grünert, U., Greferath, U., Fritschy, J.M., Möhler, H., Betz, H. & Wässle, H. (1995). Colocalization of gephyrin and GABAA receptor subunits in the rat retina. The Journal of Comparative Neurology 357, 1–14.Google Scholar
Schmitt, B., Knaus, P., Becker, C.-M. & Betz, H. (1987). The Mr 93000 polypeptide of the postsynaptic glycine receptor complex is a peripheral membrane protein. Biochemistry 26, 805–811.Google Scholar
Silveira, L.C., Saito, C.A., Lee, B.B., Kremers, J., da Silva Filho, M., Kilavik, B.E., Yamada, E.S. & Perry, V.H. (2004). Morphology and physiology of primate M- and P-cells. Progress in Brain Research 144, 21–46.Google Scholar
Silveira, L.C.L., Yamada, E.S., Perry, V.H. & Picanço-Diniz, C.W. (1994). M and P retinal ganglion cells of diurnal and nocturnal New-World monkeys. Neuroreport 5, 2077–2081.CrossRefGoogle ScholarPubMed
Solomon, S.G., Martin, P.R., White, A.J.R., Rüttiger, L. & Lee, B.B. (2002). Modulation sensitivity of ganglion cells in peripheral retina of macaque. Vision Research 42, 2893–2898.Google Scholar
Soto, F., Bleckert, A., Lewis, R., Kang, Y.H., Kerschensteiner, D., Craig, A.M. & Wong, R.O.L. (2011). Coordinated increase in inhibitory and excitatory synapses onto retinal ganglion cells during development. Neural Development 6, 31.Google Scholar
Szmajda, B.A., Grünert, U. & Martin, P.R. (2005). Mosaic properties of midget and parasol ganglion cells in the marmoset retina. Visual Neuroscience 22, 395–404.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
Troilo, D., Howland, H.C. & Judge, S.J. (1993). Visual optics and retinal cone topography in the common marmoset (Callithrix jacchus). Vision Research 33, 1301–1310.Google Scholar
Trong, P.K. & Rieke, F. (2008). Origin of correlated activity between parasol retinal ganglion cells. Nature Neuroscience 11, 1343–1351.CrossRefGoogle ScholarPubMed
Tse, Y.C., Lai, C.H., Lai, S.K., Liu, J.X., Yung, K.K., Shum, D.K. & Chan, Y.S. (2008). Developmental expression of NMDA and AMPA receptor subunits in vestibular nuclear neurons that encode gravity-related horizontal orientations. The Journal of Comparative Neurology 508, 343–364.CrossRefGoogle ScholarPubMed
Tyagarajan, S.K. & Fritschy, J.M. (2010). GABA(A) receptors, gephyrin and homeostatic synaptic plasticity. The Journal of Physiology 588, 101–106.CrossRefGoogle ScholarPubMed
Watanabe, M. & Rodieck, R.W. (1989). Parasol and midget ganglion cells of the primate retina. Journal of Comparative Neurology 289, 434–454.Google Scholar
Wilder, H.D., Grünert, U., Lee, B.B. & Martin, P.R. (1996). Topography of ganglion cells and photoreceptors in the retina of a New World monkey: The marmoset Callithrix jacchus. Visual Neuroscience 13, 335–352.CrossRefGoogle ScholarPubMed
Xu, Y., Vasudeva, V., Vardi, N., Sterling, P. & Freed, M.A. (2008). Different types of ganglion cell share a synaptic pattern. The Journal of Comparative Neurology 507, 1871–1878.CrossRefGoogle Scholar
Yamada, E.S., Silveira, L.C.L., Gomes, F.L. & Lee, B.B. (1996a). The retinal ganglion cell classes of New World primates. Revista Brasileira de Biologia 56, 381–396.Google Scholar
Yamada, E.S., Silveira, L.C.L. & Perry, V.H. (1996b). Morphology, dendriticfield size, somal size, density, and coverage of M and P retinal ganglioncells of dichromatic Cebus monkeys. Visual Neuroscience 13, 1011–1029.Google Scholar
Yamada, E.S., Silveira, L.C.L., Perry, V.H. & Franco, E.C.S. (2001). M and P retinal ganglion cells of the owl monkey: morphology, size and photoreceptor convergence. Vision Research 41, 119–131.Google Scholar