Hostname: page-component-cd9895bd7-gvvz8 Total loading time: 0 Render date: 2024-12-25T04:22:36.608Z Has data issue: false hasContentIssue false
  • English
  • Français

Characterization of inhibitory postsynaptic currents in rod bipolar cells of the mouse retina

Published online by Cambridge University Press:  01 July 2004

MORITZ J. FRECH  and
KURT H. BACKUS
MORITZ J. FRECH
Affiliation:
Max-Planck-Institut für Hirnforschung, Neuroanatomical Department, Frankfurt am Main, Germany Institute of Physiology II, Cellular Neurophysiology, University of Frankfurt, Frankfurt, Germany
KURT H. BACKUS
Affiliation:
Max-Planck-Institut für Hirnforschung, Neuroanatomical Department, Frankfurt am Main, Germany Institute of Physiology II, Cellular Neurophysiology, University of Frankfurt, Frankfurt, Germany
Get access Rights & Permissions [Opens in a new window]

Abstract

The synaptic terminals of mammalian rod bipolar cells are the targets of multiple presynaptic inhibitory inputs arriving from glycinergic and GABAergic amacrine cells. To investigate the contribution of these different inhibitory receptor types, we have applied the patch-clamp technique in acutely isolated slices of the adult mouse retina. By using the whole-cell configuration, we measured and analyzed the spontaneous postsynaptic currents (PSCs) in rod bipolar cells. The spontaneous synaptic activity of rod bipolar cells was very low. However, when amacrine cells were depolarized by AMPA or kainate, the PSC frequency in rod bipolar cells increased significantly. These PSCs comprised several types that could be distinguished by pharmacological and kinetic criteria. Strychnine-sensitive, glycinergic PSCs were characterized by a mean peak amplitude of −43.5 pA and a weighted decay time constant (τw) of 10.9 ms. PSCs that persisted in the presence of strychnine, but were completely inhibited by bicuculline, were mediated by GABAARs. They had a mean peak amplitude of −20.0 pA and a significantly faster τw of 5.8 ms. Few PSCs remained in the presence of strychnine and bicuculline, suggesting that they were mediated by GABACRs. These PSCs were characterized by much smaller amplitudes (−6.2 pA) and a significantly slower decay kinetics (τw = 51.0 ms). We conclude that rod bipolar cells express at least three types of functionally different inhibitory receptors, namely GABAARs, GABACRs, and GlyRs that may ultimately regulate the Ca2+ influx into rod bipolar cell terminals, thereby modulating their glutamate release.

Keywords

Patch-clampPostsynaptic currentsGABAA receptorGABAC receptorGlycine receptor
Type
Research Article
Information
Visual Neuroscience , Volume 21 , Issue 4 , July 2004 , pp. 645 - 652
Copyright
2004 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

Boos, R., Schneider, H., & Wässle H. (1993). Voltage- and transmitter-gated currents of All-amacrine cells in a slice preparation of the rat retina. Journal of Neuroscience 13, 2874–2888.Google Scholar
Bormann, J. & Feigenspan, A. (1995). GABAC receptors. Trends in Neuroscience 18, 515–519.Google Scholar
Bormann, J., Hamill, O.P., & Sakmann, B. (1987). Mechanism of anion permeation through channels gated by glycine and gamma-aminobutyric acid in mouse cultured spinal neurones. Journal of Physiology 385, 243–286.Google Scholar
Cook, P.B., Lukasiewicz, P.D., & McReynolds, J.S. (2000). GABA(C) receptors control adaptive changes in a glycinergic inhibitory pathway in salamander retina. Journal of Neuroscience 20, 806–812.Google Scholar
Enz, R., Brandstätter, J.H., Wässle, H., & Bormann, J. (1996). Immunocytochemical localization of the GABAC receptor rho subunits in the mammalian retina. Journal of Neuroscience 16, 4479–4490.Google Scholar
Euler, T., Detwiler, P.B., & Denk, W. (2002). Directionally selective calcium signals in dendrites of starburst amacrine cells. Nature 418, 845–852.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, 2934–2944.Google Scholar
Feigenspan, A. & Bormann, J. (1994). Differential pharmacology of GABAA and GABAC receptors on rat retinal bipolar cells. European Journal of Pharmacology 288, 97–104.Google Scholar
Feigenspan, A. & Bormann, J. (1998). GABA-gated Cl− channels in the rat retina. Progress in Retinal and Eye Research 17, 99–126.Google Scholar
Feigenspan, A., Wässle, H., & Bormann, J. (1993). Pharmacology of GABA receptor Cl− channels in rat retinal bipolar cells. Nature 361, 159–162.Google Scholar
Fletcher, E.L., Koulen, P., & Wässle, H. (1998). GABAA and GABAC receptors on mammalian rod bipolar cells. Journal of Comparative Neurology 396, 351–365.Google Scholar
Frech, M.F., Perez-Leon, J., & Backus, K.H. (1999). Inhibitory synapses on retinal bipolar cells. Zoology 102 (Suppl. II), 51.Google Scholar
Frech, M.J., Perez-Leon, J., Wässle, H., & Backus, K.H. (2001). Characterization of the spontaneous synaptic activity of amacrine cells in the mouse retina. Journal of Neurophysiology 86, 1632–1643.Google Scholar
Gingrich, K.J., Roberts, W.A., & Kass, R.S. (1995). Dependence of the GABAA receptor gating kinetics on the alpha-subunit isoform: Implications for structure–function relations and synaptic transmission. Journal of Physiology (London) 489, 529–543.Google Scholar
Gleason, E., Borges, S., & Wilson, M. (1993). Synaptic transmission between pairs of retinal amacrine cells in culture. Journal of Neuroscience 13, 2359–2370.Google Scholar
Greferath, U., Brandstätter, J.H., Wässle, H., Kirsch, J., Kuhse, J., & Grünert, U. (1994). Differential expression of glycine receptor subunits in the retina of the rat: A study using immunohistochemistry and in situ hybridization. Visual Neuroscience 11, 721–729.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, 15–24.Google Scholar
Kamphuis, W., Dijk, F., & O'Brien, B.J. (2003a). Gene expression of AMPA-type glutamate receptor subunits in rod-type ON bipolar cells of rat retina. European Journal of Neuroscience 18, 1085–1092.Google Scholar
Kamphuis, W., Klooster, J., & Dijk, F. (2003b). Expression of AMPA-type glutamate receptor subunit (GluR2) in ON-bipolar neurons in the rat retina. Journal of Comparative Neurology 455, 172–186.Google Scholar
Karschin, A. & Wässle, H. (1990). Voltage- and transmitter-gated currents in isolated rod bipolar cells of rat retina. Journal of Neurophysiology 63, 860–876.Google Scholar
Koulen, P., Sassoè-Pognetto, M., Grünert, U., & Wässle, H. (1996). Selective clustering of GABAA and glycine receptors in the mammalian retina. Journal of Neuroscience 16, 2127–2140.Google Scholar
Langosch, D., Becker, C.M., & Betz, H. (1990). The inhibitory glycine receptor: A ligand-gated chloride channel of the central nervous system. European Journal of Biochemistry 194, 1–8.Google Scholar
Lavoie, A.M., Tingey, J.J., Harrison, N.L., Pritchett, D.B., & Twyman, R.E. (1997). Activation and deactivation rates of recombinant GABA(A) receptor channels are dependent on alpha-subunit isoform. Biophysical Journal 73, 2518–2526.Google Scholar
Lukasiewicz, P.D. & Werblin, F.S. (1994). A novel GABA receptor modulates synaptic transmission from bipolar to ganglion and amacrine cells in the tiger salamander retina. Journal of Neuroscience 14, 1213–1223.Google Scholar
MacNeil, M.A. & Masland, R.H. (1998). Extreme diversity among amacrine cells: implications for function. Neuron 20, 971–982.Google Scholar
McKernan, R.M., Quirk, K., Prince, R., Cox, P.A., Gillard, N.P., Ragan, C.I., & Whiting, P. (1991). GABAA receptor subtypes immunopurified from rat brain with alpha subunit-specific antibodies have unique pharmacological properties. Neuron 7, 667–676.Google Scholar
Möhler, H., Fritschy, J.M., Lüscher, B., Rudolph, U., Benson, J., & Benke, D. (1996). The GABAA receptors. From subunits to diverse functions. Ion Channels 4, 89–113.Google Scholar
Nusser, Z., Cull-Candy, S., & Farrant, M. (1997). Differences in synaptic GABA(A) receptor number underlie variation in GABA mini amplitude. Neuron 19, 697–709.Google Scholar
Pan, Z.H. & Lipton, S.A. (1995). Multiple GABA receptor subtypes mediate inhibition of calcium influx at rat retinal bipolar cell terminals. Journal of Neuroscience 15, 2668–2679.Google Scholar
Perez-Leon, J., Frech, M.J., Schröder, J.E., Fischer, F., Kneussel, M., Wässle, H., & Backus, K.H. (2003). Spontaneous synaptic activity in an organotypic culture of the mouse retina. Investigative Ophthalmology and Visual Science 44, 1376–1387.Google Scholar
Persohn, E., Malherbe, P., & Richards, J.G. (1992). Comparative molecular neuroanatomy of cloned GABAA receptor subunits in the rat CNS. Journal of Comparative Neurology 326, 193–216.Google Scholar
Protti, D.A., Gerschenfeld, H.M., & Llano, I. (1997). GABAergic and glycinergic IPSCs in ganglion cells of rat retinal slices. Journal of Neuroscience 17, 6075–6085.Google Scholar
Protti, D.A. & Llano, I. (1998). Calcium currents and calcium signaling in rod bipolar cells of rat retinal slices. Journal of Neuroscience 18, 3715–3724.Google Scholar
Satoh, H., Aoki, K., Watanabe, S.I., & Kaneko, A. (1998). L-type calcium channels in the axon terminal of mouse bipolar cells. Neuroreport 9, 2161–2165.Google Scholar
Somogyi, P., Fritschy, J.M., Benke, D., Roberts, J.D., & Sieghart, W. (1996). The gamma 2 subunit of the GABAA receptor is concentrated in synaptic junctions containing the alpha 1 and beta 2/3 subunits in hippocampus, cerebellum and globus pallidus. Neuropharmacology 35, 1425–1444.Google Scholar
Taylor, W.R., He, S., Levick, W.R., & Vaney, D.I. (2000). Dendritic computation of direction selectivity by retinal ganglion cells. Science 289, 2347–2350.Google Scholar
Vaney, D. (1990). The mosaic of amacrine cells in the mammalian retina. Progress in Retinal Research 9, 49–100.Google Scholar
Wässle, H. & Boycott, B.B. (1991). Functional architecture of the mammalian retina. Physiological Review 71, 447–480.Google Scholar
Wässle, H., Koulen, P., Brandstätter, J.H., Fletcher, E.L., & Becker, C.M. (1998). Glycine and GABA receptors in the mammalian retina. Vision Research 38, 1411–1430.Google Scholar