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Parvalbumin-immunoreactive amacrine cells of macaque retina

Published online by Cambridge University Press:  01 May 2009

KATHRYN E. KLUMP ,
AI-JUN ZHANG ,
SAMUEL M. WU  and
DAVID W. MARSHAK
KATHRYN E. KLUMP
Affiliation:
Department of Neurobiology and Anatomy, University of Texas Medical School at Houston, Houston, Texas
AI-JUN ZHANG
Affiliation:
Cullen Eye Institute, Baylor College of Medicine, Houston, Texas
SAMUEL M. WU
Affiliation:
Cullen Eye Institute, Baylor College of Medicine, Houston, Texas
DAVID W. MARSHAK*
Affiliation:
Department of Neurobiology and Anatomy, University of Texas Medical School at Houston, Houston, Texas
*
*Address correspondence and reprint requests to: David W. Marshak, Department of Neurobiology and Anatomy, University of Texas Medical School at Houston, PO Box 20708, Houston, TX 77225. E-mail: [email protected]
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Abstract

A number of authors have observed amacrine cells containing high levels of immunoreactive parvalbumin in primate retinas. The experiments described here were designed to identify these cells morphologically, to determine their neurotransmitter, to record their light responses, and to describe the other cells that they contact. Macaque retinas were fixed in paraformaldehyde and labeled with antibodies to parvalbumin and one or two other markers, and this double- and triple-labeled material was analyzed by confocal microscopy. In their morphology and dendritic stratification patterns, the parvalbumin-positive cells closely resembled the knotty type 2 amacrine cells described using the Golgi method in macaques. They contained immunoreactive glycine transporter, but not immunoreactive γ-aminobutyric acid, and therefore, they use glycine as their neurotransmitter. Their spatial density was relatively high, roughly half that of AII amacrine cells. They contacted lobular dendrites of AII cells, and they are expected to be presynaptic to AII cells based on earlier ultrastructural studies. They also made extensive contacts with axon terminals of OFF midget bipolar cells whose polarity cannot be predicted with certainty. A macaque amacrine cell of the same morphological type depolarized at the onset of increments in light intensity, and it was well coupled to other amacrine cells. Previously, we described amacrine cells like these that contacted OFF parasol ganglion cells and OFF starburst amacrine cells. Taken together, these findings suggest that one function of these amacrine cells is to inhibit the transmission of signals from rods to OFF bipolar cells via AII amacrine cells. Another function may be inhibition of the OFF pathway following increments in light intensity.

Keywords

MonkeyBipolarGlycineMidgetParasol
Type
Research Articles
Information
Visual Neuroscience , Volume 26 , Issue 3 , May 2009 , pp. 287 - 296
Copyright
Copyright © Cambridge University Press 2009

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References

Bloomfield, S.A. & Dacheux, R. (2001). Rod vision: Pathways and processing in the mammalian retina. Progress in Retina and Eye Research 20, 351–384.CrossRefGoogle ScholarPubMed
Boos, R., Schneider, H. & Wässle, H. (1993). Voltage- and transmitter-gated currents of AII-amacrine cells in a slice preparation of the rat retina. The Journal of Neuroscience 13, 2874–2888.CrossRefGoogle Scholar
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. & Dowling, J.E. (1969). Organization of the primate retina: Light microscopy. Philosophical Transactions of the Royal Society of London 799, 109–184.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
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
Cohen, E.D. & Miller, R.F. (1994). The role of NMDA and non-NMDA excitatory amino acid receptors in the functional organization of primate retinal ganglion cells. Visual Neuroscience 11, 317–332.CrossRefGoogle ScholarPubMed
Dacey, D., Packer, O.S., Diller, L., Brainard, D., Peterson, B. & Lee, B. (2000). Center surround receptive field structure of cone bipolar cells in primate retina. Vision Research 40, 1801–1811.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
Dowling, J.E. & Boycott, B.B. (1966). Organization of the primate retina: Electron microscopy. Proceedings of the Royal Society B: Biological Sciences 166, 80–111.Google ScholarPubMed
Endo, T., Kobayashi, M., Kobayashi, S. & Onaya, T. (1986). Immunocytochemical and biochemical localization of parvalbumin in the retina. Cell and Tissue Research 234, 213–217.Google Scholar
Field, G.D., Sher, A., Gauthier, J.L., Greschner, M., Shlens, J., Litke, A.M. & Chichilinisky, E.J. (2007). Spatial properties and functional organization of small bistratified ganglion cells in primate retina. The Journal of Neuroscience 27, 13261–13272.CrossRefGoogle ScholarPubMed
Frederick, J.M., Rayborn, M.E. & Hollyfield, J.G. (1984) Glycinergic neurons in the human retina. The Journal of Comparative Neurology 227, 159–172.CrossRefGoogle ScholarPubMed
Grünert, U. & Wässle, H. (1996). Glycine receptors in the rod pathway of the macaque monkey retina. Visual Neuroscience 13, 101–115.CrossRefGoogle ScholarPubMed
Hendrickson, A., Yan, Y.H., Erickson, A., Possin, D. & Pow, D. (2007). Expression patterns of calretinin, calbindin and parvalbumin and their colocalizations in neurons during development of Macaca monkey retina. Experimental Eye Research 85, 587–601.CrossRefGoogle ScholarPubMed
Hendrickson, A.E., Koontz, M.A., Pourcho, R.G., Sarthy, P.V. & Goebel, D.J. (1988). Localization of glycine-containing neurons in the Macaca monkey retina. The Journal of Comparative Neurology 273, 473–487.CrossRefGoogle ScholarPubMed
Hokoc, J.N. & Mariani, A.P. (1987). Tyrosine hydroxylase immunoreactivity in the rhesus monkey retina reveals synapses from bipolar cells to dopaminergic amacrine cells. The Journal of Neuroscience 7, 2785–2793.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. The Journal of Comparative Neurology 416, 6–18.3.0.CO;2-X>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.CrossRefGoogle ScholarPubMed
Kalloniatis, M., Marc, R.E. & Murry, R.F. (1996). Amino acid signatures in the primate retina. The Journal of Neuroscience 16, 6807–6829.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, 147–187.CrossRefGoogle ScholarPubMed
Kolb, H. & Marshak, D. (2003). The midget pathways of the primate retina. Documenta Ophthalmologica 106, 67–81.CrossRefGoogle ScholarPubMed
Kolb, H., Zhang, L., Dekorver, L. & Cuenca, N. (2002). A new look at calretinin-immunoreactive amacrine cell types in the monkey retina. The Journal of Comparative Neurology 453, 168–184.CrossRefGoogle 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, 591–592.CrossRefGoogle ScholarPubMed
Koontz, M.A., Hendrickson, L.E., Brace, S.T. & Hendrickson, A.E. (1993). Immunocytochemical localization of GABA and glycine in amacrine and displaced amacrine cells of macaque monkey retina. Vision Research 33, 2617–2628.CrossRefGoogle ScholarPubMed
Li, W., Zhang, J. & Massey, S.C. (2002) Coupling pattern of S1 and S2 amacrine cells in the rabbit retina. Visual Neuroscience 19, 119–131.CrossRefGoogle ScholarPubMed
Manookin, M.B., Beaudoin, D.L., Ernst, Z.R., Flagel, L.I. & Demb, J.B. (2008). Disinhibition combines with excitation to extend the operating range of the OFF visual pathway in daylight. The Journal of Neuroscience 28, 4136–4150.CrossRefGoogle ScholarPubMed
Marc, R.E. & Liu, W.L. (1985). (3H) glycine-accumulating neurons of the human retina. The Journal of Comparative Neurology 232, 241–260.CrossRefGoogle ScholarPubMed
Mariani, A.P. (1990). Amacrine cells of the rhesus monkey retina. The Journal of Comparative Neurology 301, 382–400.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
Martin, P.R. & Grünert, U. (1992). Spatial density and immunoreactivity of bipolar cells in the macaque monkey retina. The Journal of Comparative Neurology 323, 269–287.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
Mills, S.L. & Massey, S.C. (1995). Differential properties of two gap junctional pathways made by AII amacrine cells. Nature 377, 734–737.CrossRefGoogle ScholarPubMed
Mills, S.L. & Massey, S.C. (1999). AII amacrine cells limit scotopic acuity in central macaque retina: A confocal analysis of calretinin labeling. The Journal of Comparative Neurology 411, 19–34.3.0.CO;2-4>CrossRefGoogle ScholarPubMed
Nishimura, Y., Schwartz, M.L. & Rakic, P. (1985). Localization of γ-aminobutyric acid and glutamic acid decarboxylase in rhesus monkey retina. Brain Research 359, 351–355.CrossRefGoogle ScholarPubMed
Polyak, S.L. (1941). The Retina. Chicago, IL: Chicago University Press.Google Scholar
Pow, D.V. & Hendrickson, A.E. (1999). Distribution of the glycine transporter glyt-1 in mammalian and nonmammalian retinae. Visual Neuroscience 16, 231–239.CrossRefGoogle ScholarPubMed
Rodieck, R.W. & Marshak, D.W. (1992). Spatial density and distribution of choline acetyltransferase immunoreactive cells in human, macaque and baboon retinas. The Journal of Comparative Neurology 321, 46–64.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Schiller, P.H. (1984). The connections of the retinal on and off pathways to the lateral geniculate nucleus of the monkey. Vision Research 24, 923–932.CrossRefGoogle Scholar
Steinberg, R.H. (1969). The rod after-effect in S-potentials from the cat retina. Vision Research 9, 1345–1355.CrossRefGoogle ScholarPubMed
Vaney, D.I. (2004). Type 1 nitrergic (ND1) cells of the rabbit retina: Comparison with other axon-bearing amacrine cells. The Journal of Comparative Neurology 474, 149–171.CrossRefGoogle ScholarPubMed
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. The Journal of Comparative Neurology 361, 537–551.CrossRefGoogle ScholarPubMed
Wässle, H., Grünert, U., Martin, P.R. & Boycott, B.B. (1994). Immunocytochemical characterization and spatial distribution of midget bipolar cells in the macaque monkey retina. Vision Research 34, 561–579.CrossRefGoogle ScholarPubMed
Yamada, E.S., Dmitrieva, N., Keyser, K.T., Lindstrom, J.M., Hersh, L.B. & Marshak, D.W. (2003). Synaptic connections of starburst amacrine cells and localization of acetylcholine receptors in primate retinas. The Journal of Comparative Neurology 461, 76–90.CrossRefGoogle ScholarPubMed
Zhang, A.J., Zhang, J. & Wu, S.M. (2006). Electrical coupling, receptive fields, and relative rod/cone inputs of horizontal cells in the tiger salamander retina. The Journal of Comparative Neurology 499, 422–431.CrossRefGoogle ScholarPubMed