Hostname: page-component-cd9895bd7-jn8rn Total loading time: 0 Render date: 2024-12-26T07:06:51.789Z Has data issue: false hasContentIssue false
  • English
  • Français

Receptive field properties of ON- and OFF-ganglion cells in the mouse retina

Published online by Cambridge University Press:  01 May 2009

MICHIEL VAN WYK ,
HEINZ WÄSSLE  and
W. ROWLAND TAYLOR
MICHIEL VAN WYK*
Affiliation:
Max Planck Institute for Brain Research, Department of Neuroanatomy Frankfurt am Main, Germany
HEINZ WÄSSLE
Affiliation:
Max Planck Institute for Brain Research, Department of Neuroanatomy Frankfurt am Main, Germany
W. ROWLAND TAYLOR
Affiliation:
Casey Eye Institute, Department of Ophthalmology, Oregon Health & Science University, Portland, Oregon
*
*Address correspondence and reprint requests to: Dr. Michiel van Wyk, Max Planck Institute for Brain Research, Deutschorden Str. 46, Frankfurt am Main, Germany. E-mail: mvanwyk@mpih-frankfurt.mpg.de
Get access Rights & Permissions [Opens in a new window]

Abstract

There are two subclasses of alpha cell in the mammalian retina, which are morphologically identical in plain view but have opposite responses to a luminance change: one is ON center and the other is OFF center. Recent studies have shown that the neural circuitries, which underlie light responses in such ON- and OFF-ganglion cell pairs, are not mirror symmetric with respect to the ON and OFF pathways (Pang et al., 2003; Zaghloul et al., 2003; Murphy & Rieke, 2006). This study examines alpha-cell homologues in the mouse retina and elucidates the synaptic mechanisms that generate their light responses. Morphological analysis of recorded cells revealed three subclasses that were essentially identical in plan view but had distinct vertical stratification levels. We refer to these cells as the sustained ON (ON-S), sustained OFF (OFF-S), and transient OFF (OFF-T) cells (Murphy & Rieke, 2006; Margolis & Detwiler, 2007). Both ON-S and OFF-S cells were largely driven through the ON pathway via changes in excitatory and inhibitory inputs, respectively. Light responses of OFF-T cells were driven by transient changes in excitatory and inhibitory inputs. Light responses of OFF-S cells were also measured in connexin 36 knockout mice in order to dissect glycinergic input arising from AII amacrine cells. At photopic/mesopic intensities, peak glycinergic input to OFF-S cells in the connexin 36 knockout mouse was reduced by ~85% compared to OFF-S cells in the wild-type retina. This is consistent with the idea that AII cells receive their input from ON-cone bipolar cells through gap junctions and in turn provide glycinergic inhibition to OFF-S cells.

Keywords

Alpha ganglion cellA-type ganglion cellAII amacrine cellconnexin36
Type
Research Articles
Information
Visual Neuroscience , Volume 26 , Issue 3 , May 2009 , pp. 297 - 308
Copyright
Copyright © Cambridge University Press 2009

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

Abramoff, M.D., Magelhaes, P.J. & Ram, S.J. (2004). Image processing with ImageJ. Biophotonics International 11, 36–42.Google Scholar
Belgum, J.H., Dvorak, D.R. & McReynolds, J.S. (1982). Sustained synaptic input to ganglion cells of mudpuppy retina. The Journal of Physiology 326, 91–108.Google Scholar
Borg-Graham, L.J. (2001). The computation of directional selectivity in the retina occurs presynaptic to the ganglion cell. Nature Neuroscience 4, 176–183.CrossRefGoogle ScholarPubMed
Bormann, J., Hamill, O.P. & Sakmann, B. (1987). Mechanism of anion permeation through channels gated by glycine and g-aminobutyric acid in mouse cultured spinal neurones. The Journal of Physiology 385, 243–286.CrossRefGoogle Scholar
Boycott, B.B. & Wässle, H. (1974). The morphological types of ganglion cells of the domestic cat’s retina. The Journal of Physiology 240, 397–419.Google Scholar
Chun, M.H., Han, S.H., Chung, J.W. & Wässle, H. (1993). Electron microscopic analysis of the rod pathway of the rat retina. The Journal of Comparative Neurology 332, 421–432.CrossRefGoogle ScholarPubMed
Crook, J.D., Peterson, B.B., Packer, O.S., Robinson, F.R., Gamlin, P.D., Troy, J.B. & Dacey, D.M. (2008). The smooth monostratified ganglion cell: Evidence for spatial diversity in the Y-cell pathway to the lateral geniculate nucleus and superior colliculus in the macaque monkey. The Journal of Neuroscience 28, 12654–12671.CrossRefGoogle Scholar
Davenport, C.M., Detwiler, P.B. & Dacey, D.M. (2008). Effects of pH buffering on horizontal and ganglion cell light responses in primate retina: Evidence for the proton hypothesis of surround formation. The Journal of Neuroscience 28, 456–464.Google Scholar
Deans, M.R., Völgyi, B., Goodenough, D.A., Bloomfield, S.A. & Paul, D.L. (2002). Connexin36 is essential for transmission of rod-mediated visual signals in the mammalian retina. Neuron 36, 703–712.Google Scholar
DeVries, S.H. (2000). Bipolar cells use kainate and AMPA receptors to filter visual information into separate channels. Neuron 28, 847–856.CrossRefGoogle ScholarPubMed
Famiglietti, E.V. Jr & Kolb, H., (1975). A bistratified amacrine cell and synaptic circuitry in the inner plexiform layer of the retina. Brain Research 84, 293–300.Google Scholar
Flores-Herr, N., Protti, D.A. & Wässle, H. (2001). Synaptic currents generating the inhibitory surround of ganglion cells in the mammalian retina. The Journal of Neuroscience 21, 4852–4863.CrossRefGoogle ScholarPubMed
Güldenagel, M., Ammermuller, J., Feigenspan, A., Teubner, B., Degen, J., Sohl, G., Willecke, K. & Weiler, R. (2001). Visual transmission deficits in mice with targeted disruption of the gap junction gene connexin36. The Journal of Neuroscience 21, 6036–6044.CrossRefGoogle ScholarPubMed
Hirasawa, H. & Kaneko, A. (2003). External proton mediates the feedback from horizontal cells to cones in the newt retina. In Neural Basis of Early Vision, ed. Kaneko, A., pp. 108–109. Tokyo, Japan: Springer Verlag.CrossRefGoogle Scholar
Kamermans, M., Fahrenfort, I., Schultz, K., Janssen-Bienhold, U., Sjoerdsma, T. & Weiler, R. (2001). Hemichannel-mediated inhibition in the outer retina. Science 292, 1178–1180.Google Scholar
Kao, Y.H., Lassova, L., Bar-Yehuda, T., Edwards, R.H., Sterling, P. & Vardi, N. (2004). Evidence that certain retinal bipolar cells use both glutamate and GABA. The Journal of Comparative Neurology 478, 207–218.CrossRefGoogle ScholarPubMed
Kolb, H. (1979). The inner plexiform layer in the retina of the cat: Electron microscopic observations. Journal of Neurocytology 8, 295–329.Google Scholar
Kolb, H. & Famiglietti, E.V. (1976). Rod and cone pathways in the retina of the cat. Investigative Ophthalmology & Visual Science 15, 935–946.Google Scholar
Kolb, H. & Nelson, R. (1993). OFF-alpha and OFF-beta ganglion cells in cat retina: II. Neural circuitry as revealed by electron microscopy of HRP stains. The Journal of Comparative Neurology 329, 85–110.Google Scholar
Kong, J.H., Fish, D.R., Rockhill, R.L. & Masland, R.H. (2005). Diversity of ganglion cells in the mouse retina: Unsupervised morphological classification and its limits. The Journal of Comparative Neurology 489, 293–310.Google Scholar
MacNeil, M.A., Heussy, J.K., Dacheux, R.F., Raviola, E. & Masland, R.H. (1999). The shapes and numbers of amacrine cells: Matching of photofilled with Golgi-stained cells in the rabbit retina and comparison with other mammalian species. The Journal of Comparative Neurology 413, 305–326.Google Scholar
Manookin, M.B., Beaudoin, D.L., Ernst, Z.R., Flagel, L.J. & 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
Margolis, D.J. & Detwiler, P.B. (2007). Different mechanisms generate maintained activity in ON and OFF retinal ganglion cells. The Journal of Neuroscience 27, 5994–6005.Google Scholar
Massey, S.C. & Mills, S.L. (1999). Gap junctions between AII amacrine cells and calbindin-positive bipolar cells in the rabbit retina. Visual Neuroscience 16, 1181–1189.CrossRefGoogle ScholarPubMed
McGuire, B.A., Stevens, J.K. & Sterling, P. (1986). Microcircuitry of beta ganglion cells in cat retina. The Journal of Neuroscience 6, 907–918.CrossRefGoogle ScholarPubMed
Menger, N., Pow, D.V. & Wässle, H. (1998). Glycinergic amacrine cells of the rat retina. The Journal of Comparative Neurology 401, 34–46.Google Scholar
Münch, T.A., da Silveira, R.A., Siegert, S. & Roska, B. (2008). A Functional Role of AII Amacrine Cells in Light-Adapted Retina. Arvo Annual Meeting, 1415/A603 (27 April to 1 May, Fort Lauderdale, FL, USA; Association for Research in Vision and Ophthalmology).Google Scholar
Murphy, G.J. & Rieke, F. (2006). Network variability limits stimulus-evoked spike timing precision in retinal ganglion cells. Neuron 52, 511–524.CrossRefGoogle ScholarPubMed
Murphy, G.J. & Rieke, F. (2008). Signals and noise in an inhibitory interneuron diverge to control activity in nearby retinal ganglion cells. Nature Neuroscience 11, 318–326.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. The Journal of Biological Chemistry 268, 11868–11873.CrossRefGoogle ScholarPubMed
Nomura, A., Shigemoto, R., Nakamura, Y., Okamoto, N., Mizuno, N. & Nakanishi, S. (1994). Developmentally regulated postsynaptic localization of a metabotropic glutamate receptor in rat rod bipolar cells. Cell 77, 361–369.Google Scholar
O’Brien, B.J., Isayama, T., Richardson, R. & Berson, D.M. (2002). Intrinsic physiological properties of cat retinal ganglion cells. The Journal of Physiology 538, 787–802.CrossRefGoogle ScholarPubMed
O’Brien, B.J., Richardson, R.C. & Berson, D.M. (2003). Inhibitory network properties shaping the light evoked responses of cat alpha retinal ganglion cells. Visual Neuroscience 20, 351–361.Google Scholar
Pang, J.J., Abd-El-Barr, M.M., Gao, F., Bramblett, D.E., Paul, D.L. & Wu, S.M. (2007). Relative contributions of rod and cone bipolar cell inputs to AII amacrine cell light responses in the mouse retina. The Journal of Physiology 580, 397–410.Google Scholar
Pang, J.J., Gao, F. & Wu, S.M. (2003). Light-evoked excitatory and inhibitory synaptic inputs to ON and OFF alpha ganglion cells in the mouse retina. The Journal of Neuroscience 23, 6063–6073.Google Scholar
Pang, J.J., Gao, F. & Wu, S.M. (2004). Light-evoked current responses in rod bipolar cells, cone depolarizing bipolar cells and AII amacrine cells in dark-adapted mouse retina. The Journal of Physiology 558, 897–912.CrossRefGoogle ScholarPubMed
Peichl, L. (1989). Alpha and delta ganglion cells in the rat retina. The Journal of Comparative Neurology 286, 120–139.Google Scholar
Peichl, L., Ott, H. & Boycott, B.B. (1987). Alpha ganglion cells in mammalian retinae. Proceedings of the Royal Society of London. Series B. Biological Sciences 231, 169–197.Google ScholarPubMed
Quraishi, S., Gayet, J., Morgans, C.W. & Duvoisin, R.M. (2007). Distribution of group-III metabotropic glutamate receptors in the retina. The Journal of Comparative Neurology 501, 931–943.CrossRefGoogle ScholarPubMed
Schubert, T., Kerschensteiner, D., Eggers, E.D., Misgeld, T., Kerschensteiner, M., Lichtman, J.W., Lukasiewicz, P.D. & Wong, R.O. (2008). Development of presynaptic inhibition onto retinal bipolar cell axon terminals is subclass-specific. Journal of Neurophysiology 100, 304–316.Google Scholar
Slaughter, M.M. & Miller, R.F. (1985). Characterization of an extended glutamate receptor of the on bipolar neuron in the vertebrate retina. The Journal of Neuroscience 5, 224–233.Google Scholar
Snellman, J. & Nawy, S. (2004). cGMP-dependent kinase regulates response sensitivity of the mouse on bipolar cell. The Journal of Neuroscience 24, 6621–6628.CrossRefGoogle ScholarPubMed
Strettoi, E., Raviola, E. & Dacheux, R.F. (1992). Synaptic connections of the narrow-field, bistratified rod amacrine cell (AII) in the rabbit retina. The Journal of Comparative Neurology 325, 152–168.Google Scholar
Sun, W., Li, N. & He, S. (2002). Large-scale morphological survey of mouse retinal ganglion cells. The Journal of Comparative Neurology 451, 115–126.CrossRefGoogle ScholarPubMed
Taylor, W.R. (1999). TTX attenuates surround inhibition in rabbit retinal ganglion cells. Visual Neuroscience 16, 285–290.Google Scholar
Taylor, W.R. & Vaney, D.I. (2002). Diverse synaptic mechanisms generate direction selectivity in the rabbit retina. The Journal of Neuroscience 22, 7712–7720.CrossRefGoogle ScholarPubMed
Trexler, E.B., Li, W., Mills, S.L. & Massey, S.C. (2001). Coupling from AII amacrine cells to ON cone bipolar cells is bidirectional. The Journal of Comparative Neurology 437, 408–422.CrossRefGoogle Scholar
van Wyk, M., Taylor, W.R. & Vaney, D.I. (2006). Local edge detectors: A substrate for fine spatial vision at low temporal frequencies in rabbit retina. The Journal of Neuroscience 26, 13250–13263.Google Scholar
Veruki, M.L. & Hartveit, E. (2002). Electrical synapses mediate signal transmission in the rod pathway of the mammalian retina. The Journal of Neuroscience 22, 10558–10566.CrossRefGoogle ScholarPubMed
Völgyi, B., Deans, M.R., Paul, D.L. & Bloomfield, S.A. (2004). Convergence and segregation of the multiple rod pathways in mammalian retina. The Journal of Neuroscience 24, 11182–11192.Google Scholar
Wässle, H. (2004). Parallel processing in the mammalian retina. Nature Reviews. Neuroscience 5, 747–757.CrossRefGoogle ScholarPubMed
Werblin, F.S. & Dowling, J.E. (1969). Organization of the retina of the mudpuppy, Necturus maculosus. II. Intracellular recording. Journal of Neurophysiology 32, 339–355.CrossRefGoogle ScholarPubMed
Wunk, D.F. & Werblin, F.S. (1979). Synaptic inputs to the ganglion cells in the tiger salamander retina. The Journal of General Physiology 73, 265–286.CrossRefGoogle Scholar
Xin, D. & Bloomfield, S.A. (1999). Comparison of the responses of AII amacrine cells in the dark- and light-adapted rabbit retina. Visual Neuroscience 16, 653–665.Google Scholar
Yamashita, M. & Wässle, H. (1991). Responses of rod bipolar cells isolated from the rat retina to the glutamate agonist 2-amino-4-phosphonobutyric acid (APB). The Journal of Neuroscience 11, 2372–2382.Google Scholar
Zaghloul, K.A., Boahen, K. & Demb, J.B. (2003). Different circuits for ON and OFF retinal ganglion cells cause different contrast sensitivities. The Journal of Neuroscience 23, 2645–2654.Google Scholar