Hostname: page-component-78c5997874-fbnjt Total loading time: 0 Render date: 2024-11-05T01:00:34.081Z Has data issue: false hasContentIssue false

Localization of ionotropic glutamate receptors to invaginating dendrites at the cone synapse in primate retina

Published online by Cambridge University Press:  06 October 2005

DAVID J. CALKINS
Affiliation:
Department of Ophthalmology and Visual Sciences, The Vanderbilt Eye Institute and Vanderbilt Vision Research Center, Vanderbilt University Medical Center, Nashville

Abstract

The separation of OFF pathways that signal light decrements from ON pathways that signal light increments occurs at the first retinal synapse. The dendrites of OFF bipolar cells abut the cone pedicle at basal positions distal to the site of glutamate release and express ligand-gated or ionotropic glutamate receptors (GluR). The dendrites of ON bipolar cells penetrate narrow invaginations of the cone pedicle proximal to the site of release and express the G-protein-coupled, metabotropic glutamate receptor, mGluR6. However, recent studies demonstrating the expression of GluR subunits in the rodent rod bipolar cell, known to yield an ON response to light, call this basic segregation of receptors into question. The light-microscopic distribution of many glutamate receptors in the primate retina is now well established. We reexamined their ultrastructural localization in the outer retina of Macaca fascicularis to test systematically whether invaginating dendrites at the cone synapse, presumably from ON bipolar cells, also express one or more ionotropic subunits. Using preembedding immunocytochemistry for electron microscopy, we quantified the distribution of the AMPA-sensitive subunits GluR2/3 and GluR4 and of the kainate-sensitive subunits GluR6/7 across 207 labeled dendrites occupying specific morphological loci at the cone pedicle. We report, in agreement with published investigations, that the majority of labeled processes for GluR2/3 (70%) and GluR4 (67%) either occupy basal positions or arise from horizontal cells. For GluR6/7, we find a significantly lower fraction of labeled processes at these positions (47%). We also find a considerable number of labeled dendrites for GluR2/3 (10%), GluR4 (21%), and GluR6/7 (18%) at invaginating positions. Surprisingly, for each subunit, the remainder of labeled processes corresponds to “fingers” of presynaptic cytoplasm within the cone invagination.

Type
Research Article
Copyright
2005 Cambridge University Press

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

REFERENCES

Agrawal, S.K. & Fehlings, M.G. (1997). Role of NMDA and non-NMDA ionotropic glutamate receptors in traumatic spinal cord axonal injury. Journal of Neuroscience 17(3), 10551063.Google Scholar
Blanco, R. & de la Villa, P. (1999). Ionotropic glutamate receptors in isolated horizontal cells of the rabbit retina. European Journal of Neuroscience 11, 867873.Google Scholar
Bloomfield, S.A. & Dacheux, R.F. (2001). Rod vision: Pathways and processing in the mammalian retina. [Review] [142 refs]. Progress in Retinal & Eye Research 20, 351384.Google Scholar
Boycott, B.B. & Hopkins, J.M. (1997). The cone synapses of cone bipolar cells of primate retina. Journal of Neurocytology 26, 313325.Google Scholar
Boycott, B. & Wässle, H. (1999). Parallel processing in the mammalian retina. Investigative Ophthalmology & Visual Science 40, 13131327.Google Scholar
Brandstätter, J.H., Koulen, P., & Wassle, H. (1997). Selective synaptic distribution of kainate receptor subunits in the two plexiform layers of the rat retina. Journal of Neuroscience 17, 92989307.Google Scholar
Cai, W. & Pourcho, R.G. (1999). Localization of metabotropic glutamate receptors mGluR1α and mGluR2/3 in the cat retina. Journal of Comparative Neurology 407, 427437.Google Scholar
Calkins, D., Tsukamoto, Y., & Sterling, P. (1996). Foveal cones form basal as well as invaginating junctions with diffuse ON bipolar cells. Vision Research 36, 33733381.Google Scholar
Calkins, D.J., Tsukamoto, Y., & Sterling, P. (1998). Microcircuitry and mosaic of a blue-yellow ganglion cell in the primate retina. Journal of Neuroscience 18(9), 33733385.Google Scholar
Calkins, D.J. (2001). Seeing with S cones. Progress in Retinal & Eye Research 20, 255287.Google Scholar
Chun, M., Grünert, U., Martin, P., & Wässle, H. (1996). The synaptic complex of cones in the fovea and the periphery of the macaque monkey retina. Vision Research 36, 33733381.Google Scholar
de la Villa, P., Kurahashi, T., & Kaneko, A. (1995). L-glutamate-induced responses and cGMP-activated channels in retinal bipolar cells dissociated from the cat. Journal of Neuroscience 15, 35713582.Google Scholar
DeVries, S.H. & Schwartz, E.A. (1999). Kainate receptors mediate synaptic transmission between cones and ‘off’ bipolar cells in a mammalian retina. Nature 397, 157160.Google Scholar
DeVries, S.H. (2000). Bipolar cells use kainate and AMPA receptors to filter visual information into separate channels. Neuron 28, 847856.Google Scholar
Dhingra, A., Lyubarsky, A., Jiang, M., Pugh, E.N., Birnbaumer, L., Sterling, P., & Vardi, N. (2000). The Light Response of ON Bipolar Neurons Requires Gαo. Journal of Neuroscience 20, 90539058.Google Scholar
Dhingra, A., Jiang, M., Wang, T.-L., Lyubarsky, A., Savchenko, A., Bar-Yehuda, T., Sterling, P., Birnbaumer, L., & Vardi, N. (2002). Light Response of Retinal ON Bipolar Cells Requires a Specific Splice Variant of Gαo. Journal of Neuroscience 22, 48784884.Google Scholar
Euler, T., Schneider, H., & Wässle, H. (1996). Glutamate responses of bipolar cells in a slice preparation of the rat retina. Journal of Neuroscience 16, 29342944.Google Scholar
Euler, T. & Masland, R.H. (2000). Light-evoked responses of bipolar cells in a mammalian retina. Journal of Neurophysiology 83, 18171829.Google Scholar
Fletcher, E.L., Hack, I., Brandstätter, J.H., & Wässle, H. (2000). Synaptic localization of NMDA receptor subunits in the rat retina. Journal of Comparative Neurology 420, 98112.Google Scholar
Hack, I., Peichl, L., & Brandstätter, J.H. (1999). An alternative pathway for rod signals in the rodent retina: Rod photoreceptors, cone bipolar cells, and the localization of glutamate receptors. Proceedings of the National Academy of Sciences of the United States of America 96, 1413014135.Google Scholar
Hack, I., Frech, M., Dick, O., Peichl, L., & Brandstätter, J.H. (2001). Heterogeneous distribution of AMPA glutamate receptor subunits at the photoreceptor synapses of rodent retina. European Journal of Neuroscience 13, 1524.Google Scholar
Hartveit, E. (1997). Functional organization of cone bipolar cells in the rat retina. Journal of Neurophysiology 77, 17261730.Google Scholar
Harvey, D.M. (2001). Localization and expression of kainate receptors in the outer plexiform layer of the primate retina. Doctoral dissertation, University of Rochester.
Harvey, D.M & Calkins, D.J. (2002). Localization of kainate receptors to the presynaptic active zone of the rod photoreceptor in primate retina. Visual Neuroscience 19, 681692.Google Scholar
Haverkamp, S., Grünert, U., & Wässle, H. (2000). The cone pedicle, a complex synapse in the retina. Neuron 27, 8595.Google Scholar
Haverkamp, S., Grünert, U., & Wässle, H. (2001a). The synaptic architecture of AMPA receptors at the cone pedicle of the primate retina. The Journal of Neuroscience 21, 24882500.Google Scholar
Haverkamp, S., Grünert, U., & Wässle, H. (2001b). Localization of kainate receptors at the cone pedicles of the primate retina. Journal of Comparative Neurology 436, 471486.Google Scholar
Huang, H., Luo, D.G., Shen, Y., Zhang, A.J., Yang, R., & Yang, X.L. (2004). AMPA receptor is involved in transmission of cone signal to ON bipolar cells in carp retina. Brain Research 1002(1–2), 8693.Google Scholar
Hughes, T.E. (1997). Are there ionotropic glutamate receptors on the rod bipolar cell of the mouse retina? Visual Neuroscience 14, 103109.Google Scholar
Kamermans, M. & Spekreijse, H. (1999). The feedback pathway from horizontal cells to cones—A mini review with a look ahead. Vision Research 39, 24492468.Google Scholar
Kamphuis, W., Klooster, J., & Dijk, F. (2003a). Expression of AMPA-type glutamate receptor subunit (GluR2) in ON-bipolar neurons in the rat retina. Journal of Comparative Neurology 455(2), 172186.Google Scholar
Kamphuis, W., Dijk, F., & O'brien, B.J. (2003b). Gene expression of AMPA-type glutamate receptor subunits in rod-type ON bipolar cells of rat retina. European Journal of Neuroscience 18(5), 10851092.Google Scholar
Klooster, J., Studholme, K.M., & Yazulla, S. (2001). Localization of the AMPA subunit GluR2 in the outer plexiform layer of goldfish retina. Journal of Comparative Neurology 441(2), 155167.Google Scholar
Kolb, H. & Nelson, R. (1995). The organization of photoreceptor to bipolar synapses in the outer plexiform layer. In Neurobiology and clinical aspects of the outer retina, ed. Djamgoz, M.B.A., Archer, S.N. & Vallerga, S., pp. 273296. London: Chapman & Hall.
Koulen, P., Kuhn, R., Wassle, H., & Brandstätter, J.H. (1999). Modulation of the intracellular calcium concentration in photoreceptor terminals by a presynaptic metabotropic glutamate receptor. Proceedings of the National Academy of Sciences USA 99, 99099914.Google Scholar
Koulen, P. & Brandstätter, J.H. (2002). Pre- and postsynaptic sites of action of mGluR8a in the mammalian retina. Investigative Ophthalmology and Visual Science 43, 19331940.Google Scholar
Koulen, P., Liu, J., Nixon, E., & Madry, C. (2005). Interaction between mGluR8 and calcium channels in photoreceptors is sensitive to pertussis toxin and occurs via G protein βγ subunit signaling. Investigative Ophthalmology and Visual Science 46, 287291.Google Scholar
Morigiwa, K. & Vardi, N. (1999). Differential expression of ionotropic glutamate receptor subunits in the outer retina. Journal of Comparative Neurology 405, 173184.Google Scholar
Nakajima, Y., Iwakabe, H., Akazawa, C., Nawa, H., Shigemoto, R., Mizuno, N., & Nakanishi, S. (1993). Molecular characterization of a novel retinal metabotropic glutamate receptor mGluR6 with a high agonist selectivity for L-2-amino-4-phosphonobutyrate. Journal of Biological Chemistry 268, 1186811873.Google Scholar
Nawy, S. (1999). The metabotropic receptor mGluR6 may signal through Go, but not phosphodiesterase, in retinal bipolar cells. Journal of Neuroscience 19, 29382944.Google Scholar
Peng, Y.-W., Blackstone, C.D., Huganir, R.L., & Yau, K.-W. (1995). Distribution of glutamate receptor subtypes in the vertebrate retina. Neuroscience 66, 483497.Google Scholar
Picaud, S., Larsson, H.P., Wellis, D.P., Lecar, H., & Werblin, F. (1995). Cone photoreceptors respond to their own glutamate release in tiger salamander. Proceedings of the National Academy of Sciences USA 92, 94179421.Google Scholar
Pourcho, R.G., Qin, P., & Goebel, D.J. (2001). Cellular and subcellular distribution of NMDA receptor subunit NR2B in the retina. Journal of Comparative Neurology 433, 7585.Google Scholar
Qin, P. & Pourcho, R.G. (1999). Localization of AMPA-selective glutamate receptor subunits in the cat retina: A light- and electron-microscope study. Visual Neuroscience 16, 169177.Google Scholar
Qin, P. & Pourcho, R.G. (2001). Immunocytochemical localization of kainate-selective glutamate receptor subunits GluR5, GluR6, GluR7 in the cat retina. Brain Research 890, 211221.Google Scholar
Rao-Mirotznik, R., Harkins, A., Buchsbaum, G., & Sterling, P. (1995). Mammalian rod terminal: Architecture of a binary synapse. Neuron 14, 561569.Google Scholar
Rodieck, R.W. (1998). The First Steps in Seeing. Sunderland, MA: Sinauer Associates, Inc.
Sassoè-Pognetto, M., Wassle, H., & Grunert, U. (1994). Glycinergic synapses in the rod pathway of the rat retina: Cone bipolar cells express the α1 subunit of the glycine receptor. Journal of Neuroscience 14, 51315146.Google Scholar
Schultz, K., Janssen-Bienhold, U., & Weiler, R. (2001). Selective synaptic distribution of AMPA and kainate receptor subunits in the outer plexiform layer of the carp retina. Journal of Comparative Neurology 435, 433449.Google Scholar
Shiells, R.A. & Falk, G. (1994). Responses of rod bipolar cells isolated from dogfish retinal slices to concentration-jumps of glutamate. Visual Neuroscience 11, 11751183.Google Scholar
Vardi, N., Morigiwa, K., Wang, T.-L., Shi, Y.-Y., & Sterling, P. (1998). Neurochemistry of the mammalian cone ‘synaptic complex’. Vision Research 38, 13591369.Google Scholar
Vardi, N., Duvoisin, R., Wu, G., & Sterling, P. (2000). Localization of mGluR6 to dendrites of ON bipolar cells in primate retina. Journal of Comparative Neurology 423, 402412.Google Scholar
Wässle, H. (2004). Parallel processing in the mammalian retina. Nature Reviews Neuroscience 5, 747757.Google Scholar