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Spiking and nonspiking models of starburst amacrine cells in the rabbit retina

  • T. J. Velte (a1) and R. F. Miller (a1)
Abstract
Abstract

The integrative properties of starburst amacrine cells in the rabbit retina were studied with compartmental models and computer-simulation techniques. The anatomical basis for these simulations was provided by computer reconstructions of intracellularly stained starburst amacrine cells and published data on dendritic diameter and biophysical properties. Passive and active membrane properties were included to simulate spiking and nonspiking behavior. Simulated synaptic inputs into one or more compartments consisted of a bipolar-like conductance change with peak and steady-state components provided by the sum of two Gaussian responses. Simulated impulse generation was achieved by using a model of impulse generation that included five nonlinear channels (INa, ICa, Ia,. Ik. Ik.Ca). The magnitude of the sodium channel conductance change was altered to meet several different types of impulse generation and propagation behaviors. We studied a range of model constraints which included variations in membrane resistance (Rm) from 4,000 Ω.cm2 to 100,000 Ω.cm2, and dendritic diameter from 0.1 to 0.3 μm. In a separate series of simulations, we studied the feasibility of voltage-clamping starburst amacrine cells using a soma-applied, single-electrode voltage clamp, based on models with and without dendritic and somatic spiking behavior. Our simulation studies suggest that single dendrites of starburst amacrine cells can behave as independent functional subunits when the Rm is high, provided that one or a small number of dendrites is synaptically co-activated. However, as the number of co-activated dendrites increases, the starburst cell behavior becomes more uniform and independent dendritic function is less prevalent. The presence of impulse activity in the dendrites raises new questions about dendritic function. However, dendritic impulses do not necessarily eliminate independent dendritic function, because dendritic impulses commonly fail as they propagate toward the soma, where they contribute EPSP-like responses which summate with conventional synaptic currents.

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Adams J.C. (1981). Heavy metal intensification of DAB-based HRP reaction products. Journal of Histochemical Cytochemistry 29, 775.
Ariel M. & Daw N.W. (1982 a). Effect of cholinergic drugs on receptive field properties of rabbit retinal ganglion cells. Journal of Physiology (London) 324, 135160.
Ariel M. & Daw N.W. (1982 b). Pharmacological analysis of directionally selective rabbit retinal ganglion cells. Journal of Physiology (London) 324, 161185.
Bloomfield S.A. & Miller R.F. (1986). A functional organization of ON and OFF pathways in rabbit retina. Journal of Neuroscience 6, 113.
Bloomfield S.A. (1991). Two types of orientation-sensitive responses of amacrine cells in the mammalian retina. Nature (London) 350, 347350.
Bloomfield S.A. (1992). Relationship between receptive and dendritic field size of amacrine cells in the rabbit retina. Journal of Neurophysiology 68, 711725.
Bloomfield S.A. (1996). Effect of spike blockade on the receptive-field size of amacrine and ganglion cells in the rabbit. Journal of Neurophysiology 75, 18781893.
Burke R.E. & Bruggencate G. (1971). Electrotonic characteristics of alpha motoneurones of varying size. Journal of Physiology (London) 212, 120.
Caldwell J.H., Daw N.W. & Wyatt H.J. (1978). Effects of picrotoxin and strychnine on rabbit retinal ganglion cells: Lateral interactions for cells with more complex receptive fields. Journal of Physiology (London) 276, 277298.
Capowski J.J. & Sedivee M.J. (1981). Accurate computer reconstruction and graphics display of complex neurons utilizing state-of-the-art interactive techniques. Computational Biomedical Research 14, 518532.
Cohen E.D. & Miller R.F. (1995). Quinoxalines block the mechanism of directional selectivity in ganglion cells of the rabbit retina. Proceedings of the National Academy of Sciences of the U.S.A. 92, 11271131.
Cohen E.D., Honoré T. & Miller R.F. (1996). NBQX reveals a prominent NMDA response in the rabbit retina Society for Neuroscience 403.1 (Abstract).
Coleman P.A. & Miller R.F. (1989). Measurement of passive membrane parameters with whole-cell recording from neurons in the intact amphibian retina. Journal of Neurophysiology 61, 218230.
Famiglietti E.V. (1983). On and off pathways through amacrine cells in mammalian retina: The synaptic connections of "starburst" amacrine cells. Vision Research 23, 12651279.
Famiglietti E.V. (1991). Synaptic organization of starburst amacrine cells in rabbit retina: Analysis of serial thin sections by electron microscopy and graphic reconstruction. Journal of Comparative Neurology 309, 4070.
Finkel A.S. & Redman S. (1984). Theory and operation of a single microelectrode voltage clamp. Journal of Neuroscience Methods 11, 101127.
Fohlmeister J.F., Coleman P.A. & Miller R.F. (1990). Modeling the repetitive firing of retinal ganglion cells. Brain Research 510, 343345.
Hines M. (1993). NEURON—A program for simulation of nerve equations. In Neural Systems: Analysis and Modeling, ed. Eeckman F., pp. 127136. Norwell, Massachusetts: Kluwer Academic Publishers.
Marty A. & Neher E. (1983). Tight-seal whole-cell recording. In Single-Channel Recording, ed. Sakmann B. & Neher E., pp. 107189. New York: Plenum Publishing Corporation.
Masland R.H. & Ames A. III. (1976). Responses to acetylcholine of ganglion cells in an isolated mammalian retina. Journal of Neurophysiology 39, 12201235.
Miller R.F. & Bloomfield S.A. (1983). Electroanatomy of a unique amacrine cell in the rabbit retina. Proceedings of the National Academy of Sciences of the U.S.A. 80, 30693073.
Miller R.F, Coleman P. & Arkin M. (1989). Structure function relationships of sustained on ganglion cells of the mudpuppy retina. In NATO ASI Series, Vol H31, Neurobiology of the Inner Retina, ed. Weiler R. & Osborne N.N., pp. 221234. Berlin: Springer-Verlag.
Moore J.W. & Westerfield M. (1983). Action potential propagation and threshold parameters in inhomogeneous regions of squid axons. Journal of Physiology 336, 285300.
O'Malley D.M. & Masland R.H. (1989). Co-release of acetylcholine and gamma-aminobutyric acid by a retinal neuron. Proceedings of the National Academy of Sciences of the U.S.A. 86, 34143418.
O'Malley D.M., Sandell J.H. & Masland R.H. (1992). Co-release of acetylcholine and GABA by the starburst amacrine cells. Journal of Neuroscience 12, 13941408.
Peters B.N. & Masland R.H. (1996). Responses to light of starburst amacrine cells. Journal of Neurophysiology 75, 469480.
Poznanski R.R. (1992). Modelling the electrotonic structure of starburst amacrine cells in the rabbit retina: A functional interpretation of dendritic morphology. Bulletin of Mathematical Biology 54, 905928.
Rall W. (1959). Branching dendritic trees and motorneuron membrane resistivity. Experimental Neurology 1, 491527.
Rall W. (1967). Distinguishing theoretical synaptic potentials computed for different soma-dendritic distributions of synaptic input. Journal of Neurophysiology 30, 11381168.
Rall W. (1969). Time constants and electrotonic length of membrane cylinders and neurons. Biophysical Journal 9, 14831508.
Rall W. (1978). Dendritic spines and synaptic potency. In Studies in Neurophysiology, ed. McIntyre A.K., pp. 203209. U.K.: Cambridge University Press.
Sholl D.A. (1956). The Organization of the Cerebral Cortex. London: Metheun and Co., Ltd.
Taylor W.R. & Wässle H. (1995). Receptive field properties of cholinergic amacrine cells in the rabbit retina. European Journal of Neuroscience 7, 23082321.
Vaney D.I. (1990). The mosaic of amacrine cells in the mammalian retina. In Progress in Retinal Research, ed. Osborne N. & Chader G., pp. 49100. New York: Pergamon.
Velte T.J. & Miller R.F. (1995). Dendritic integration of retinal ganglion cells in the mudpuppy. Visual Neuroscience 12, 165175.
Velte T.J. & Miller R.F. (1996). Computer simulations of voltage clamping retinal ganglion cells through whole-cell electrodes. Journal of Neurophysiology 75, 21292143.
Wann D.F., Woolsey T.A., Dieker M.L. & Cowan W.M. (1973). An on-line digital computer system for the semi-automatic analysis of Golgi-impregnated neurons. IEEE Transactions of Biomedical Engineering 20, 233247.
Zhou Z.J. & Fain G.L. (1996). Starburst amacrine cells change from spiking to non-spiking neurons during retinal development. Proceedings of the National Academy of Sciences of the U.S.A. 93, 80578062.
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Visual Neuroscience
  • ISSN: 0952-5238
  • EISSN: 1469-8714
  • URL: /core/journals/visual-neuroscience
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