Hostname: page-component-586b7cd67f-t7czq Total loading time: 0 Render date: 2024-11-26T11:14:17.678Z Has data issue: false hasContentIssue false
  • English
  • Français

A comparison of receptive-field and tracer-coupling size of amacrine and ganglion cells in the rabbit retina

Published online by Cambridge University Press:  02 June 2009

Stewart A. Bloomfield  and
Daiyan Xin
Stewart A. Bloomfield
Affiliation:
Department of Ophthalmology, New York University Medical Center, New York Department of Physiology and Neuroscience, New York University Medical Center, New York
Daiyan Xin
Affiliation:
Department of Ophthalmology, New York University Medical Center, New York
Get access Rights & Permissions [Opens in a new window]

Abstract

Recent studies have shown that amacrine and ganglion cells in the mammalian retina are extensively coupled as revealed by the intercellular movement of the biotinylated tracers biocytin and Neurobiotin. These demonstrations of tracer coupling suggest that electrical networks formed by proximal neurons (i.e. amacrine and ganglion cells) may underlie the lateral propagation of signals across the inner retina. We studied this question by comparing the receptive-field size, dendritic-field size, and extent of tracer coupling of amacrine and ganglion cells in the dark-adapted, supervised, isolated retina eyecup of the rabbit. Our results indicate that while the center-receptive fields of proximal neurons are approximately 15% larger than their corresponding dendritic diameters, this slight difference can be explained by factors other than electrical coupling such as tissue shrinkage associated with histological processing. However, the extent of tracer coupling of amacrine and ganglion cells was, on average, about twice the size of the corresponding receptive fields. Thus, the receptive field of an individual proximal neuron matched far more closely to its dendritic diameter than to the size of the tracer-coupled network of cells to which it belonged. The exception to this rule was the AII amacrine cells for which center-receptive fields were 2–3 times the size of their dendritic diameters but matched closely to the size of the tracer-coupled arrays. Thus, with the exception of AII cells, our data indicate that tracer coupling between proximal neurons is not associated with an enlargement of their receptive fields. Our results, then, provide no evidence for electrical coupling or, at least, indicate that extensive lateral spread of visual signals does not occur in the proximal mammalian retina.

Keywords

Amacrine cellsGanglion cellsGap junctionsElectrical couplingBiotinylated tracers
Type
Research Articles
Information
Visual Neuroscience , Volume 14 , Issue 6 , November 1997 , pp. 1153 - 1165
Copyright
Copyright © Cambridge University Press 1997

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

Adams, J.C. (1977). Technical considerations on the use of horseradish peroxidase as a neuronal marker. Neuwscience 2, 141–145.Google ScholarPubMed
Amthor, F.R., Takahashi, E.S. & Oyster, C.W. (1989). Morphologies of rabbit retinal ganglion cells with concentric receptive fields. Journal of Comparative Neurology 280, 72–96.CrossRefGoogle ScholarPubMed
Bloomfield, S.A. (1992). Relationship between receptive and dendritic field size of amacrine cells in the rabbit retina. Journal of Neurophysiology 68, 711–725.CrossRefGoogle ScholarPubMed
Bloomfield, S.A. & Miller, R.F. (1982). A physiological and morphological study of the horizontal cell types of the rabbit retina. Journal of Comparative Neurology 208, 288–303.CrossRefGoogle ScholarPubMed
Bloomfield, S.A. & Miller, R.F. (1986). A functional organization of ON and OFF pathways in the rabbit retina. Journal Neuwscience 6, 1–13.Google Scholar
Bloomfield, S.A., Xin, D. & Osborne, T. (1997). Light-induced modulation of coupling between AII amacrine cells in rabbit retina. Visual Neuwscience 14, 565–576.Google ScholarPubMed
Bloomfield, S.A., Xin, D. & Persky, S.E. (1995). A comparison of receptive field and tracer coupling size of horizontal cells in the rabbit retina. Visual Neuroscience 12, 985–999.CrossRefGoogle ScholarPubMed
Cook, J.E. & Becker, D.L. (1995). Gap junctions in the vertebrate retina. Microscopy Research and Technique 31, 408–419.CrossRefGoogle ScholarPubMed
Dacev, D.M. & Brace, S. (1992). A coupled network for parasol but not midget ganglion cells in the primate retina. Visual Neuroscience 9, 279–290.Google Scholar
Dacheux, R.F. & Raviola, E. (1982). Horizontal cells in the retina of the rabbit. Journal of Neuroscience 2, 1486–1493.CrossRefGoogle ScholarPubMed
Dacheux, R.F. & Raviola, E. (1986). The rod pathway in the rabbit retina: A depolarizing bipolar and amacrine cell. Journal of Neuroscience 6. 331–345.CrossRefGoogle ScholarPubMed
Famiglietti, E.V. & Kolb, H. (1975). A bistratified amacrine cell and synaptic circuitry in the inner plexiform layer of the retina. Brain Research 84, 293–300.CrossRefGoogle Scholar
Freed, M.A., Smith, R.G. & Sterling, P. (1992). Computational model of the on-alpha ganglion cell receptive field based on bipolar cell circuitry. Proceedings of the National Academy of Sciences of the U.S.A. 89. 236–240.CrossRefGoogle ScholarPubMed
Hampson, E.C.G.M., Vaney, D.I. & Weiler, R. (1992). Dopaminergic modulation of gap junction permeability between amacrine cells in mammalian retina. Journal of Neuroscience 12, 4911–4922.CrossRefGoogle ScholarPubMed
Hidaka, S., Maehara, M., Umino, O., Lu, Y. & Hashimoto, Y. (1993). Lateral gap junction connections between retinal amacrine cells sum-mating sustained responses. NeuroReport 5, 29–32.CrossRefGoogle ScholarPubMed
Kaneko, A. (1971). Electrical connexions between horizontal cells in the dogfish retina. Journal of Physiology (London) 213, 95–105.CrossRefGoogle ScholarPubMed
Kaneko, A. & Stuart, A.E. (1984). Coupling between horizontal cells in carp retina revealed by diffusion of Lucifer yellow. Neuroscience Letters 47, 1–7.CrossRefGoogle ScholarPubMed
Kolb, H. (1979). The inner plexiform layer in the retina of the cat: Electron microscopic observations. Journal of Neurocytology 8, 295–329.CrossRefGoogle ScholarPubMed
Kolb, H. & Famiglietti, E.V. (1974). Rod and cone pathways in the inner plexiform layer of the cat retina. Science 186, 47–49.CrossRefGoogle ScholarPubMed
Mangel, S.C. (1991). Analysis of the horizontal cell contribution to the receptive field surround of ganglion cells in the rabbit retina. Journal of Physiology 442, 211–234.CrossRefGoogle Scholar
Mastronarde, D. (1983). Interactions between ganglion cells in cat retina. Journal of Neurophysiology 49, 350–365.CrossRefGoogle ScholarPubMed
Meister, M., Lagnado, L. & Baylor, D.A. (1995). Concerted signaling by retinal ganglion cells. Science 270, 1207–1210.CrossRefGoogle ScholarPubMed
Mills, S.L. & Massey, S.C. (1991). Labeling and distribution of AII amacrine cells in the rabbit retina. Journal of Comparative Neurology 304, 491–501.CrossRefGoogle ScholarPubMed
Naka, K.-l. & Nye, P.W. (1971). Roles of horizontal cells in organization of the catfish retinal receptive field. Journal of Neurophysiology 34, 785–801.CrossRefGoogle ScholarPubMed
Naka, K.-I. & Rushton, W.A.H. (1967). The generation and spread of S-potentials in fish (Cyprinidae). Journal of Physiology 192, 437–461.CrossRefGoogle ScholarPubMed
Naka, K.-I. & Witkovsky, P. (1972). Dogfish ganglion cells discharges resulting from extrinsic polarization of the horizontal cells. Journal of Physiology 223, 449–460.CrossRefGoogle ScholarPubMed
Negishi, K. & Teranishi, T. (1990). Close tip-to-tip contacts between dendrites of transient amacrine cells in carp retina. Neuroscience Letters 115, 1–6.CrossRefGoogle ScholarPubMed
Nelson, R. & Kolb, H. (1985). A17: A broad-field amacrine cell in the rod system of the cat retina. Journal of Neurophysiology 54, 592–614.CrossRefGoogle ScholarPubMed
Nelson, R., Kolb, H. & Freed, M.A. (1993). OFF-alpha and OFF-beta ganglion cells in cat retina. I. Intracellular electrophysiology and HRP stains. Journal of Comparative Neurology 329, 68–84.CrossRefGoogle ScholarPubMed
Peichl, L., Buhl, E.H. & Boycott, B.B. (1987). Alpha ganglion cells in the rabbit retina. Journal of Comparative Neurology 263, 25–41.CrossRefGoogle ScholarPubMed
Peichl, L. & Wässle, H. (1983). The structural correlate of the receptive field centre of alpha-ganglion cells in cat retina. Journal of Physiology 341, 309–324.CrossRefGoogle ScholarPubMed
Penn, A.A., Wong, R.O.L. & Shatz, C.J. (1994). Neuronal coupling in the developing mammalian retina. Journal of Neuroscience 14, 3805–3815.CrossRefGoogle ScholarPubMed
Peters, B.N. & Masland, R.H. (1996). Responses to light of starburst amacrine cells. Journal of Neurophysiology 75, 469–480.CrossRefGoogle ScholarPubMed
Piccolino, M., Neyton, J., Witkovsky, P. & Gerchenfeld, H.M. (1982). λ-aminobutyric acid antagonists decrease junctional communication between L-type horizontal cells of the retina. Proceedings of the National Academy of Sciences of the U.S.A. 79, 3671–3675.CrossRefGoogle 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 ScholarPubMed
Raviola, E. & Dacheux, R.F. (1987). Excitatory dyad synapse in rabbit retina. Proceedings of the National Academy of Sciences of the U.S.A. 84, 7324–7328.CrossRefGoogle ScholarPubMed
Sandell, J.H. & Masland, R.H. (1986). A system of indoleamine-accumulating neurons in the rabbit retina. Journal of Neuroscience 6, 411–428.CrossRefGoogle ScholarPubMed
Smith, R.G. & Vardi, N. (1995). Simulation of the AII amacrine cell of mammalian retina: Functional consequences of electrical coupling and regenerative membrane properties. Visual Neuroscience 12, 851–860.CrossRefGoogle ScholarPubMed
Stanford, L.R. (1987). X-cells in the cat retina: relationship between the morphology and physiology of a class of retinal ganglion cells. Journal of Neurophysiology 58, 940–964.CrossRefGoogle ScholarPubMed
Stewart, W.W. (1978). Functional connections between cells as revealed by dye-coupling with a highly fluorescent naphthalimide tracer. Cell 14, 741–759.CrossRefGoogle ScholarPubMed
Strettoi, E., Dacheux, R.F. & Raviola, E. (1990). Synaptic connections of rod bipolar cells in the inner plexiform layer of the rabbit retina. Journal of Comparative Neurology 295, 449–466.CrossRefGoogle ScholarPubMed
Taylor, W. R. (1996). Response properties of long-range axon-bearing amacrine cells in the dark-adapted rabbit retina. Visual Neuroscience 13, 599–604.CrossRefGoogle ScholarPubMed
Taylor, W. R. & Wässle, H. (1995). Receptive field properties of star-burst cholinergic amacrine cells in the rabbit retina. European Journal of Neuroscience 7, 2308–2321.CrossRefGoogle Scholar
Teranishi, T. & Negishi, K. (1994). Double-staining of horizontal and amacrine cells by intracellular injection with Lucifer yellow and bio-cytin in carp retina. Neuroscience 59, 217–226.CrossRefGoogle ScholarPubMed
Teranishi, T., Negishi, K. & Kato, S. (1983). Dopamine modulates S-potential amplitude and dye-coupling between external horizontal cells in carp retina. Nature (London) 301, 243–246.CrossRefGoogle ScholarPubMed
Teranishi, T., Negishi, K. & Kato, S. (1984). Regulatory effect of dopamine on spatial properties of horizontal cells in carp retina. Journal of Neuroscience 4, 1271–1280.CrossRefGoogle ScholarPubMed
Teranishi, T., Negishi, K. & Kato, S. (1987). Functional and morphological correlates of amacrine cells in carp retina. Neuroscience 20, 935–950.CrossRefGoogle ScholarPubMed
Tomita, T. (1965). Electrophysiological study of the mechanisms subserving color coding in the fish retina. Cold Spring Harbor Symposium on Quantitative Biology 30, 559–566.CrossRefGoogle ScholarPubMed
Vaney, D.I. (1985). The morphology and topographic distribution of AII amacrine cells in the cat retina. Proceedings of the Royal Society B (London) 224, 475–488.Google ScholarPubMed
Vaney, D.I. (1986). Morphological identification of serotonin-accumulating neurons in the living retina. Science 233, 444–446.CrossRefGoogle ScholarPubMed
Vaney, D.I. (1991). Many diverse types of retinal neurons show tracer coupling when injected with biocytin or neurobiotin. Neuroscience Letters 125, 187–190.CrossRefGoogle ScholarPubMed
Vaney, D.I. (1994). Patterns of neuronal coupling in the retina. Progress in Retinal Research 13, 301–355.CrossRefGoogle Scholar
Xin, D. & Bloomfield, S.A. (1997). The tracer coupling pattern of amacrine and ganglion cells in rabbit retina. Journal of Comparative Neurology 383, 512–528.3.0.CO;2-5>CrossRefGoogle ScholarPubMed
Yang, G. & Masland, R.H. (1992). Direct visualization of the dendritic and receptive fields of directionally selective retinal ganglion cells. Science 258, 1949–1952.CrossRefGoogle ScholarPubMed
Yang, G. & Masland, R.H. (1994). Receptive fields and dendritic structure of directionally selective retinal ganglion cells. Journal of Neuroscience 14, 5267–5280.CrossRefGoogle ScholarPubMed