Hostname: page-component-cd9895bd7-jkksz Total loading time: 0 Render date: 2024-12-27T08:36:39.690Z Has data issue: false hasContentIssue false
  • English
  • Français

Inhibitory network properties shaping the light evoked responses of cat alpha retinal ganglion cells

Published online by Cambridge University Press:  18 November 2003

BRENDAN J. O'BRIEN ,
RANDAL C. RICHARDSON  and
DAVID M. BERSON
BRENDAN J. O'BRIEN
Affiliation:
Department of Neuroscience, Brown University, Box 1953, Providence Present address: Department of Optometry and Visual Science, University of Auckland, Private Bag 92019, Auckland, New Zealand.
RANDAL C. RICHARDSON
Affiliation:
Department of Neuroscience, Brown University, Box 1953, Providence
DAVID M. BERSON
Affiliation:
Department of Neuroscience, Brown University, Box 1953, Providence
Get access Rights & Permissions [Opens in a new window]

Abstract

Cat retinal ganglion cells of the Y (or alpha) type respond to luminance changes opposite those preferred by their receptive-field centers with a transient hyperpolarization. Here, we examine the spatial organization and synaptic basis of this light response by means of whole-cell current-clamp recordings made in vitro. The hyperpolarization was largest when stimulus spots approximated the size of the receptive-field center, and diminished substantially for larger spots. The hyperpolarization was largely abolished by bath application of strychnine, a blocker of glycinergic inhibition. Picrotoxin, an antagonist of ionotropic GABA receptors, greatly reduced the attenuation of the hyperpolarizing response for large spots. The data are consistent with a model in which (1) the hyperpolarization reflects inhibition by glycinergic amacrine cells of bipolar terminals presynaptic to the alpha cells, and perhaps direct inhibition of the alpha cell as well; and (2) the attenuation of the hyperpolarization by large spots reflects surround inhibition of the glycinergic amacrine by GABAergic amacrine cells. This circuitry may moderate nonlinearities in the alpha-cell light response and could account for some excitatory and inhibitory influences on alpha cells known to arise from outside the classical receptive field.

Keywords

RetinaRetinal ganglion cellGamma amino butyric acid (GABA)GlycineAmacrine cell
Type
Research Article
Information
Visual Neuroscience , Volume 20 , Issue 4 , July 2003 , pp. 351 - 361
Copyright
2003 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

Awatramani, G.B. & Slaughter, M.M. (2000). Origin of transient and sustained responses in ganglion cells of the retina. Journal of Neuroscience 20, 7087–7095.Google Scholar
Bishop, P.O., Kozak, W., & Vakkur, J. (1962). Some quantitative aspects of the cat's eye: Axis and plane of refrence, visual field co-ordinates and optics. Journal of Physiology (London) 163, 466–502.CrossRefGoogle Scholar
Bloomfield, S.A. (1992). Relationship between receptive and dendritic field size of amacrine cells in the rabbit retina. Journal of Neurophysiology 68, 711–725.Google Scholar
Bloomfield, S.A. & Miller, R.F. (1986). A functional organization of ON and OFF pathways in the rabbit retina. Journal of Neuroscience 6, 1–13.Google Scholar
Boycott, B.B. & Wässle, H. (1974). The morphological types of ganglion cells of the domestic cat's retina. Journal of Physiology (London) 240, 397–419.CrossRefGoogle Scholar
Brivanlou, I.H., Warland, D.K., & Meister, M. (1998). Mechanisms of concerted firing among retinal ganglion cells. Neuron 20(3), 527–539.CrossRefGoogle Scholar
Cohen, E.D., Zhou, Z.J., & Fain, G.L. (1994). Ligand-gated currents of alpha and beta ganglion cells in the cat retinal slice. Journal of Neurophysiology 72, 1260–1269.Google Scholar
Cook, J.E. (1997). Getting to grips with neuronal diversity: What is a neuronal type? In Development and Organization of the Retina: From Molecules to Function, ed. Chalupa, L.M. & Finlay, B.L., pp. 91–120. New York: Plenum Press.
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 Scholar
Cook, P.B., Lukasiewicz, P.D., & McReynolds, J.S. (1998). Action potentials are required for the lateral transmission of glycinergic transient inhibition in the amphibian retina. Journal of Neuroscience 18, 2301–2308.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
Dacey, D.M. (1999). Primate retina: Cell types, circuits and color opponency. Progress in Retinal and Eye Research 18, 737–763.CrossRefGoogle Scholar
Dacey, D.M. & Brace, S. (1992). A coupled network for parasol but not midget ganglion cells in the primate retina. Visual Neuroscience 9 (3–4), 279–290.CrossRefGoogle Scholar
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 Scholar
Demb, J.B., Haarsma, L., Freed, M.A., & Sterling, P. (1999). Functional circuitry of the retinal ganglion cell's nonlinear receptive field. Journal of Neuroscience 19, 9756–9767.Google Scholar
Demb, J.B., Zaghloul, K., & Sterling, P. (2001a). Cellular basis for the response to second-order motion cues in Y retinal ganglion cells. Neuron 32, 711–721.Google Scholar
Demb, J.B., Zaghloul, K., Haarsma, L., & Sterling, P. (2001b). Bipolar cells contribute to nonlinear spatial summation in the brisk-transient (Y) ganglion cell in mammalian retina. Journal of Neuroscience 21, 7447–7454.Google Scholar
Deng, P., Cuenca, N., Doerr, T., Pow, D.V., Miller, R., & Kolb, H. (2001). Localization of neurotransmitters and calcium binding proteins to neurons of salamander and mudpuppy retinas. Vision Research 41, 1771–1783.CrossRefGoogle Scholar
DeVries, S.H. (2000). Bipolar cells use kainate and AMPA receptors to filter visual information into separate channels. Neuron 28, 847–856.CrossRefGoogle Scholar
Enroth-Cugell, C. & Jakiela, H.G. (1980). Suppression of cat retinal ganglion cell responses by moving patterns. Journal of Physiology (London) 302, 49–72.CrossRefGoogle Scholar
Enroth-Cugell, C. & Robson, J.G. (1966). The contrast sensitivity of retinal ganglion cells of the cat. Journal of Physiology (London) 187, 517–552.CrossRefGoogle Scholar
Enroth-Cugell, C., Hertz, B.G., & Lennie, P. (1977). Convergence of rod and cone signals in the cat's retina. Journal of Physiology (London) 269, 297–318.CrossRefGoogle Scholar
Freed, M.A. (2000). Rate of quantal excitation to a retinal ganglion cell evoked by sensory input. Journal of Neurophysiology 83, 2956–2966.Google Scholar
Freed, M.A. & Sterling, P. (1988). The ON-alpha ganglion cell of the cat retina and its presynaptic cell types. Journal of Neuroscience 8, 2303–2320.Google Scholar
Hamill, O.P., Marty, A., Neher, E., Sakmann, B., & Sigworth, F.J. (1981). Improved patch-clamp techniques for high-resolution current recording from cells and cell-free membrane patches. Pflügers Archive 391, 85–100.CrossRefGoogle Scholar
Hochstein, S. & Shapley, R.M. (1976a). Quantitative analysis of retinal ganglion cell classifications. Journal of Physiology (London) 262, 237–264.Google Scholar
Hochstein, S. & Shapley, R.M. (1976b). Linear and nonlinear spatial subunits in Y cat retinal ganglion cells. Journal of Physiology (London) 262, 265–284.Google Scholar
Jacoby, R., Stafford, D., Kouyama, N., & Marshak, D. (1996) Synaptic inputs to ON parasol ganglion cells in the primate retina. Journal of Neuroscience 16(24), 8041–8056.Google 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.CrossRefGoogle Scholar
Kim, I.-B., Lee, E.-J., Oh, S.-J., Park, C.-B., Pow, D.V., & Chun, M.-H. (2002). Light- and electron-microscopic analysis of aquaporin 1-like immunoreactive amacrine cells in the rat retina. Journal of Comparative Neurology 452, 178–191.CrossRefGoogle Scholar
Koulen, P., Sassoe-Pognetto, M., Grünert, U., & Wässle, H. (1996). Selective clustering of GABA(A) and glycine receptors in the mammalian retina. Journal of Neuroscience 16, 2127–2140.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. Journal of Comparative Neurology 413, 305–326.3.0.CO;2-E>CrossRefGoogle Scholar
McIlwain, J.T. (1964). Receptive fields of optic tract axons and lateral geniculate cells: Peripheral extent and barbiturate sensitivity. Journal of Neurophysiology 27, 1154–1173.Google Scholar
Menger, N., Pow, D.V., & Wässle, H. (1998). Glycinergic amacrine cells of the rat retina. Journal of Comparative Neurology 401, 34–46.3.0.CO;2-P>CrossRefGoogle Scholar
Müller, F., Boos, R., & Wässle, H. (1992). Actions of GABAergic ligands on brisk ganglion cells in the cat retina. Visual Neuroscience 9, 415–425.CrossRefGoogle Scholar
Neher, E. (1992). Correction for liquid junction potentials in patch-clamp experiments. Methods in Enzymology 207, 123–131.CrossRefGoogle Scholar
Nelson, R. & Kolb, H. (1983). Synaptic patterns and response properties of bipolar and ganglion cells in the cat retina. Vision Research 23, 1183–1195.CrossRefGoogle Scholar
O'Brien, B.J., Isayama, T., Richardson, R., & Berson, D.M. (2002). Intrinsic physiological properties of cat retinal ganglion cells. Journal of Physiology (London) 538, 787–802.CrossRefGoogle Scholar
Owczarzak, M.T. & Pourcho, R.G. (1999). Transmitter-specific input to OFF-alpha ganglion cells in the cat retina. Anatomical Record 255, 363–373.3.0.CO;2-9>CrossRefGoogle Scholar
Passaglia, C.L., Enroth-Cugell, C., & Troy, J.B. (2001). Effects of remote stimulation on the mean firing rate of cat retinal ganglion cells. Journal of Neuroscience 21, 5794–5803.Google Scholar
Peichl, L. (1991). Alpha ganglion cells in mammalian retinae: Common properties, species differences, and some comments on other ganglion cells. Visual Neuroscience 7, 155–169.CrossRefGoogle Scholar
Penn, A.A., Wong, R.O., & Shatz, C.J. (1994). Neuronal coupling in the developing mammalian retina. Journal of Neuroscience 14(6), 3805–3815.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.Google Scholar
Pu, M. & Berson, D.M. (1992). A method for reliable and permanent intracellular staining of retinal ganglion cells. Journal of Neuroscience Methods 41, 45–51.CrossRefGoogle Scholar
Robinson, D.W. & Chalupa, L.M. (1997). The intrinsic temporal properties of alpha and beta retinal ganglion cells are equivalent. Current Biology 7, 366–374.CrossRefGoogle Scholar
Rodieck, R.W. (1998). The First Steps in Seeing. Sunderland, Massachusetts: Sinauer Associates.
Rodieck, R.W. & Brening, R.K. (1983). Retinal ganglion cells: Properties, types, genera, pathways and trans-species comparisons. Brain, Behavior, and Evolution 23, 121–164.Google Scholar
Roska, B. & Werblin, F. (2001). Vertical interactions across ten parallel, stacked representations in the mammalian retina. Nature 410, 583–587.CrossRefGoogle Scholar
Roska, B., Nemeth, E., & Werblin, F.S. (1998). Response to change is facilitated by a three-neuron disinhibitory pathway in the tiger salamander retina. Journal of Neuroscience 18, 3451–3459.Google Scholar
Rowe, M.H. & Stone, J. (1977). Naming of neurones. Classification and naming of cat retinal ganglion cells. Brain, Behavior, and Evolution 14, 185–216.Google Scholar
Schubert, T. & Weiler, R. (2002). Connexin36 is involved in the coupling pattern of alpha ganglion cells in the mouse retina. FENS Forum Abstracts 3, 60.Google Scholar
Stone, J. (1983) Parallel Processing in the Visual System. New York: Plenum Press.
Taylor, W.R. & Wässle, H. (1995). Receptive field properties of starburst cholinergic amacrine cells in the rabbit retina. European Journal of Neuroscience 7, 2308–2321.CrossRefGoogle Scholar
Thibos, L.N. & Werblin, F.S. (1978). The properties of surround antagonism elicited by spinning windmill patterns in the mudpuppy retina. Journal of Physiology (London) 278, 101–116.CrossRefGoogle Scholar
Troy, J.B. & Shou, T. (2002). The receptive fields of cat retinal ganglion cells in physiological and pathological states: Where we are after half a century of research? Progress in Retinal and Eye Research 21, 263–302.Google Scholar
Vaney, D.I. (1990). The mosaic of amacrine cells in the mammalian retina. In Progress in Retinal Research, ed. Osborne, J.J. & Chader, G., pp. 49–100. Oxford, UK: Pergamon.CrossRef
Vaney, D.I. (1991). Many diverse types of retinal neurons show tracer coupling when injected with biocytin or Neurobiotin. Neuroscience Letters 125(2), 187–190.CrossRefGoogle Scholar
Wässle, H. & Boycott, B.B. (1991). Functional architecture of the mammalian retina. Physiological Reviews 71, 447–480.Google Scholar
Wässle, H., Schafer-Trenkler, I., & Voigt, T. (1986). Analysis of a glycinergic inhibitory pathway in the cat retina. Journal of Neuroscience 6, 594–604.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.CrossRefGoogle Scholar
Wright, L.L., Macqueen, C.L., Elston, G.N., Young, H.M., Pow, D.V., & Vaney, D.I. (1997). The DAPI-3 amacrine cells of the rabbit retina. Visual Neuroscience 14, 473–492.CrossRefGoogle Scholar
Wu, S.M., Gao, F., & Maple, B.R. (2000). Functional architecture of synapses in the inner retina: Segregation of visual signals by stratification of bipolar cell axon terminals. Journal of Neuroscience 20, 4462–4470.Google Scholar
Xin, D. & Bloomfield, S.A. (1997). Tracer coupling pattern of amacrine and ganglion cells in the rabbit retina. Journal of Comparative Neurology 383(4), 512–528.3.0.CO;2-5>CrossRefGoogle Scholar
Yang, C-Y., Lukasiewicz, P., Maguire, G., Werblin, F.S., & Yazulla, S. (1991). Amacrine cells in the tiger salamander retina: Morphology, physiology, and neurotransmitter identification. Journal of Comparative Neurology 312, 19–32.CrossRefGoogle Scholar
Zhang, J., Jung, C-S., & Slaughter, M.M. (1997). Serial inhibitory synapses in retina. Visual Neuroscience 14, 553–563.CrossRefGoogle Scholar
Zucker, C.L. & Ehinger, B. (1998). Gamma-aminobutyric acid A receptors on a bistratified amacrine cell type in the rabbit retina. Journal of Comparative Neurology 393, 309–319.3.0.CO;2-5>CrossRefGoogle Scholar