Hostname: page-component-586b7cd67f-rdxmf Total loading time: 0 Render date: 2024-11-24T03:27:43.691Z Has data issue: false hasContentIssue false
  • English
  • Français

Multiple pathways of inhibition shape bipolar cell responses in the retina

Published online by Cambridge University Press:  08 October 2010

ERIKA D. EGGERS  and
PETER D. LUKASIEWICZ
ERIKA D. EGGERS*
Affiliation:
Department of Physiology, University of Arizona, Tucson, Arizona Department of Biomedical Engineering, University of Arizona, Tucson, Arizona
PETER D. LUKASIEWICZ
Affiliation:
Department of Ophthalmology and Visual Sciences, Washington University, St. Louis, Missouri Department of Anatomy and Neurobiology, Washington University, St. Louis, Missouri
*
*Address correspondence and reprint requests to: Erika D. Eggers, Department of Physiology, P.O. Box 245051, University of Arizona, Tucson, AZ 85724. E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Bipolar cells (BCs) are critical relay neurons in the retina that are organized into parallel signaling pathways. The three main signaling pathways in the mammalian retina are the rod, ON cone, and OFF cone BCs. Rod BCs mediate incrementing dim light signals from rods, and ON cone and OFF cone BCs mediate incrementing and decrementing brighter light signals from cones, respectively. The outputs of BCs are shaped by inhibitory inputs from GABAergic and glycinergic amacrine cells in the inner plexiform layer, mediated by three distinct types of inhibitory receptors: GABAA, GABAC, and glycine receptors. The three main BC pathways receive distinct forms of inhibition from these three receptors that shape their light-evoked inhibitory signals. Rod BC inhibition is dominated by slow GABAC receptor inhibition, while OFF cone BCs are dominated by glycinergic inhibition. The inhibitory inputs to BCs are also shaped by serial inhibitory connections between GABAergic amacrine cells that limit the spatial profile of BC inhibition. We discuss our recent studies on how inhibitory inputs to BCs are shaped by receptor expression, receptor properties, and neurotransmitter release properties and how these affect the output of BCs.

Keywords

GABAGlycineLightGABAA receptorGABAC receptorglycine receptorpatch-clamp
Type
Review Article
Information
Visual Neuroscience , Volume 28 , Issue 1 , January 2011 , pp. 95 - 108
Copyright
Copyright © Cambridge University Press 2010

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

Ashmore, J.F. & Copenhagen, D.R. (1980). Different postsynaptic events in two types of retinal bipolar cell. Nature 288, 84–86.CrossRefGoogle ScholarPubMed
Awatramani, G.B. & Slaughter, M.M. (2000). Origin of transient and sustained responses in ganglion cells of the retina. The Journal of Neuroscience 20, 7087–7095.CrossRefGoogle ScholarPubMed
Cadetti, L., Tranchina, D. & Thoreson, W.B. (2005). A comparison of release kinetics and glutamate receptor properties in shaping rod-cone differences in EPSC kinetics in the salamander retina. The Journal of Physiology 569, 773–788.CrossRefGoogle ScholarPubMed
Chang, Y. & Weiss, D.S. (1999). Channel opening locks agonist onto the GABAC receptor. Nature Neuroscience 2, 219–225.CrossRefGoogle ScholarPubMed
Chavez, A.E. & Diamond, J.S. (2008). Diverse mechanisms underlie glycinergic feedback transmission onto rod bipolar cells in rat retina. The Journal of Neuroscience 28, 7919–7928.CrossRefGoogle ScholarPubMed
Chavez, A.E., Grimes, W.N. & Diamond, J.S. (2010). Mechanisms underlying lateral GABAergic feedback onto rod bipolar cells in rat retina. The Journal of Neuroscience 30, 2330–2339.CrossRefGoogle ScholarPubMed
Chavez, A.E., Singer, J.H. & Diamond, J.S. (2006). Fast neurotransmitter release triggered by Ca influx through AMPA-type glutamate receptors. Nature 443, 705–708.CrossRefGoogle ScholarPubMed
Cook, P.B. & McReynolds, J.S. (1998). Lateral inhibition in the inner retina is important for spatial tuning of ganglion cells. Nature Neuroscience 1, 714–719.CrossRefGoogle ScholarPubMed
DeVries, S.H. (2000). Bipolar cells use kainate and AMPA receptors to filter visual information into separate channels. Neuron 28, 847–856.CrossRefGoogle ScholarPubMed
Devries, S.H. & Schwartz, E.A. (1999). Kainate receptors mediate synaptic transmission between cones and ‘Off’ bipolar cells in a mammalian retina. Nature 397, 157–160.CrossRefGoogle Scholar
Diamond, J.S. & Jahr, C.E. (1995). Asynchronous release of synaptic vesicles determines the time course of the AMPA receptor-mediated EPSC. Neuron 15, 1097–1107.CrossRefGoogle ScholarPubMed
Dong, C.J. & Hare, W.A. (2003). Temporal modulation of scotopic visual signals by A17 amacrine cells in mammalian retina in vivo. Journal of Neurophysiology 89, 2159–2166.CrossRefGoogle ScholarPubMed
Dong, C.J. & Werblin, F.S. (1998). Temporal contrast enhancement via GABAC feedback at bipolar terminals in the tiger salamander retina. Journal of Neurophysiology 79, 2171–2180.CrossRefGoogle ScholarPubMed
Eggers, E.D. & Lukasiewicz, P.D. (2006 a). GABA(A), GABA(C) and glycine receptor-mediated inhibition differentially affects light-evoked signalling from mouse retinal rod bipolar cells. The Journal of Physiology 572, 215–225.CrossRefGoogle Scholar
Eggers, E.D. & Lukasiewicz, P.D. (2006 b). Receptor and transmitter release properties set the time course of retinal inhibition. The Journal of Neuroscience 26, 9413–9425.CrossRefGoogle ScholarPubMed
Eggers, E.D. & Lukasiewicz, P.D. (2010). Interneuron circuits tune inhibition in retinal bipolar cells. Journal of Neurophysiology 103, 25–37.CrossRefGoogle ScholarPubMed
Eggers, E.D., McCall, M.A. & Lukasiewicz, P.D. (2007). Presynaptic inhibition differentially shapes transmission in distinct circuits in the mouse retina. The Journal of Physiology 582, 569–582.CrossRefGoogle ScholarPubMed
Euler, T. & Masland, R.H. (2000). Light-evoked responses of bipolar cells in mammalian retina. Journal of Neurophysiology 83, 1817–1829.CrossRefGoogle ScholarPubMed
Euler, T. & Wässle, H. (1998). Different contributions of GABAA and GABAC receptors to rod and cone bipolar cells in a rat retinal slice preparation. Journal of Neurophysiology 79, 1384–1395.CrossRefGoogle Scholar
Famiglietti, E.V. Jr & Kolb, H. (1976). Structural basis for ON-and OFF-center responses in retinal ganglion cells. Science 194, 193–195.CrossRefGoogle ScholarPubMed
Feigenspan, A. & Bormann, J. (1994). Differential pharmacology of GABA-A and GABA-C receptors on rat retinal bipolar cells. European Journal of Pharmacology 288, 97–104.CrossRefGoogle ScholarPubMed
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
Ghosh, K.K., Bujan, S., Haverkamp, S., Feigenspan, A. & Wässle, H. (2004). Types of bipolar cells in the mouse retina. The Journal of Comparative Neurology 469, 70–82.CrossRefGoogle ScholarPubMed
Hartveit, E. (1999). Reciprocal synaptic interactions between rod bipolar cells and amacrine cells in the rat retina. Journal of Neurophysiology 81, 2923–2936.CrossRefGoogle ScholarPubMed
Hefft, S. & Jonas, P. (2005). Asynchronous GABA release generates long-lasting inhibition at a hippocampal interneuron-principal neuron synapse. Nature Neuroscience 8, 1319–1328.CrossRefGoogle Scholar
Ivanova, E., Muller, U. & Wässle, H. (2006). Characterization of the glycinergic input to bipolar cells of the mouse retina. The European Journal of Neuroscience 23, 350–364.CrossRefGoogle ScholarPubMed
Jones, M.V. & Westbrook, G.L. (1996). The impact of receptor desensitization on fast synaptic transmission. Trends in Neuroscience 19, 96–101.CrossRefGoogle ScholarPubMed
Li, G.L., Vigh, J. & von Gersdorff, H. (2007). Short-term depression at the reciprocal synapses between a retinal bipolar cell terminal and amacrine cells. The Journal of Neuroscience 27, 7377–7385.CrossRefGoogle ScholarPubMed
Li, W. & DeVries, S.H. (2004). Separate blue and green cone networks in the mammalian retina. Nature Neuroscience 7, 751–756.CrossRefGoogle ScholarPubMed
Li, W. & DeVries, S.H. (2006). Bipolar cell pathways for color and luminance vision in a dichromatic mammalian retina. Nature Neuroscience 9, 669–675.CrossRefGoogle 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. The Journal of Neuroscience 14, 1213–1223.CrossRefGoogle ScholarPubMed
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
McCall, M.A., Lukasiewicz, P.D., Gregg, R.G. & Peachey, N.S. (2002). Elimination of the ρ1 subunit abolishes GABAC receptor expression and alters visual processing in the mouse retina. The Journal of Neuroscience 22, 4163–4174.CrossRefGoogle ScholarPubMed
Menger, N., Pow, D.V. & Wässle, H. (1998). Glycinergic amacrine cells of the rat retina. The Journal of Comparative Neurology 401, 34–46.3.0.CO;2-P>CrossRefGoogle ScholarPubMed
Molnar, A., Hsueh, H.A., Roska, B. & Werblin, F.S. (2009). Crossover inhibition in the retina: Circuitry that compensates for nonlinear rectifying synaptic transmission. Journal of Computational Neuroscience 27, 569–590.CrossRefGoogle ScholarPubMed
Morgans, C.W., Zhang, J., Jeffrey, B.G., Nelson, S.M., Burke, N.S., Duvoisin, R.M. & Brown, R.L. (2009). TRPM1 is required for the depolarizing light response in retinal ON-bipolar cells. Proceedings of the National Academy of Sciences of the United States of America 106, 19174–19178.CrossRefGoogle ScholarPubMed
Morkve, S.H. & Hartveit, E. (2009). Properties of glycine receptors underlying synaptic currents in presynaptic axon terminals of rod bipolar cells in the rat retina. The Journal of Physiology 587, 3813–3830.CrossRefGoogle ScholarPubMed
Palmer, M.J. (2006). Functional segregation of synaptic GABAA and GABAC receptors in goldfish bipolar cell terminals. The Journal of Physiology 577, 45–53.CrossRefGoogle ScholarPubMed
Pan, Z.-H. & Lipton, S.A. (1995). Multiple GABA receptor subtypes mediate inhibition of calcium influx at rat retinal bipolar cell terminals. The Journal of Neuroscience 15, 2668–2679.CrossRefGoogle ScholarPubMed
Pourcho, R.G. & Goebel, D.J. (1983). Neuronal subpopulations in cat retina which accumulate the GABA agonist, (3H)muscimol: A combined Golgi and autoradiographic study. The Journal of Comparative Neurology 219, 25–35.CrossRefGoogle ScholarPubMed
Roska, B., Molnar, A. & Werblin, F.S. (2006). Parallel processing in retinal ganglion cells: How integration of space-time patterns of excitation and inhibition form the spiking output. Journal of Neurophysiology 95, 3810–3822.CrossRefGoogle ScholarPubMed
Roska, B., Nemeth, E. & Werblin, F.S. (1998). Response to change is facilitated by a three-neuron disinhibitory pathway in the tiger salamander retina. The Journal of Neuroscience 18, 3451–3459.CrossRefGoogle ScholarPubMed
Sagdullaev, B.T., McCall, M.A. & Lukasiewicz, P.D. (2006). Presynaptic inhibition modulates spillover, creating distinct dynamic response ranges of sensory output. Neuron 50, 923–935.CrossRefGoogle ScholarPubMed
Schnapf, J.L. & Copenhagen, D.R. (1982). Differences in the kinetics of rod and cone synaptic transmission. Nature 296, 862–864.CrossRefGoogle ScholarPubMed
Shen, Y., Heimel, J.A., Kamermans, M., Peachey, N.S., Gregg, R.G. & Nawy, S. (2009). A transient receptor potential-like channel mediates synaptic transmission in rod bipolar cells. The Journal of Neuroscience 29, 6088–6093.CrossRefGoogle ScholarPubMed
Shields, C.R., Tran, M.N., Wong, R.O. & Lukasiewicz, P.D. (2000). Distinct ionotropic GABA receptors mediate presynaptic and postsynaptic inhibition in retinal bipolar cells. The Journal of Neuroscience 20, 2673–2682.CrossRefGoogle ScholarPubMed
Singer, J.H. & Diamond, J.S. (2003). Sustained Ca2+ entry elicits transient postsynaptic currents at a retinal ribbon synapse. The Journal of Neuroscience 23, 10923–10933.CrossRefGoogle Scholar
van Genderen, M.M., Bijveld, M.M., Claassen, Y.B., Florijn, R.J., Pearring, J.N., Meire, F.M., McCall, M.A., Riemslag, F.C., Gregg, R.G., Bergen, A.A. & Kamermans, M. (2009). Mutations in TRPM1 are a common cause of complete congenital stationary night blindness. American Journal of Human Genetics 85, 730–736.CrossRefGoogle ScholarPubMed
Vaney, D.I. (1990). The mosaic of amacrine cells in the mammalian retina. Progress in Retinal Research 9, 49–100.CrossRefGoogle Scholar
Wässle, H. (2004). Parallel processing in the mammalian retina. Nature Reviews. Neuroscience 5, 747–757.CrossRefGoogle ScholarPubMed
Werblin, F., Roska, B. & Balya, D. (2001). Parallel processing in the mammalian retina: Lateral and vertical interactions across stacked representations. Progress in Brain Research 131, 229–238.CrossRefGoogle ScholarPubMed
Werblin, F.S. (2010). Six different roles for crossover inhibition in the retina: Correcting the nonlinearities of synaptic transmission. Visual Neuroscience 27, 1–8.CrossRefGoogle ScholarPubMed
Zhang, J., Chang-Sub, J. & Slaughter, M.M. (1997). Serial inhibitory synapses in retina. Visual Neuroscience 14, 553–563.CrossRefGoogle ScholarPubMed