Hostname: page-component-78c5997874-t5tsf Total loading time: 0 Render date: 2024-11-10T16:50:27.877Z Has data issue: false hasContentIssue false
  • English
  • Français

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

Published online by Cambridge University Press:  02 June 2009

T. J. Velte  and
R. F. Miller
T. J. Velte
Affiliation:
University of Minnesota, Department of Physiology and Graduate Program in Neuroscience, Minneapolis
R. F. Miller
Affiliation:
University of Minnesota, Department of Physiology and Graduate Program in Neuroscience, Minneapolis
Get access Rights & Permissions [Opens in a new window]

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.

Keywords

Voltage clampModelingDendritic isolationRealistic morphologySpace clampInput resistance
Type
Research Articles
Information
Visual Neuroscience , Volume 14 , Issue 6 , November 1997 , pp. 1073 - 1088
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. (1981). Heavy metal intensification of DAB-based HRP reaction products. Journal of Histochemical Cytochemistry 29, 775.CrossRefGoogle Scholar
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, 135–160.CrossRefGoogle ScholarPubMed
Ariel, M. & Daw, N.W. (1982 b). Pharmacological analysis of directionally selective rabbit retinal ganglion cells. Journal of Physiology (London) 324, 161–185.CrossRefGoogle Scholar
Bloomfield, S.A. & Miller, R.F. (1986). A functional organization of ON and OFF pathways in rabbit retina. Journal of Neuroscience 6, 1–13.CrossRefGoogle Scholar
Bloomfield, S.A. (1991). Two types of orientation-sensitive responses of amacrine cells in the mammalian retina. Nature (London) 350, 347–350.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. (1996). Effect of spike blockade on the receptive-field size of amacrine and ganglion cells in the rabbit. Journal of Neurophysiology 75, 1878–1893.CrossRefGoogle ScholarPubMed
Burke, R.E. & Bruggencate, G. (1971). Electrotonic characteristics of alpha motoneurones of varying size. Journal of Physiology (London) 212, 1–20.CrossRefGoogle ScholarPubMed
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, 277–298.CrossRefGoogle ScholarPubMed
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, 518–532.CrossRefGoogle ScholarPubMed
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, 1127–1131.CrossRefGoogle ScholarPubMed
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).Google Scholar
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, 218–230.CrossRefGoogle ScholarPubMed
Famiglietti, E.V. (1983). On and off pathways through amacrine cells in mammalian retina: The synaptic connections of "starburst" amacrine cells. Vision Research 23, 1265–1279.CrossRefGoogle ScholarPubMed
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, 40–70.CrossRefGoogle ScholarPubMed
Finkel, A.S. & Redman, S. (1984). Theory and operation of a single microelectrode voltage clamp. Journal of Neuroscience Methods 11, 101–127.CrossRefGoogle ScholarPubMed
Fohlmeister, J.F., Coleman, P.A. & Miller, R.F. (1990). Modeling the repetitive firing of retinal ganglion cells. Brain Research 510, 343–345.CrossRefGoogle ScholarPubMed
Hines, M. (1993). NEURON—A program for simulation of nerve equations. In Neural Systems: Analysis and Modeling, ed. Eeckman, F., pp. 127–136. Norwell, Massachusetts: Kluwer Academic Publishers.CrossRefGoogle Scholar
Marty, A. & Neher, E. (1983). Tight-seal whole-cell recording. In Single-Channel Recording, ed. Sakmann, B. & Neher, E., pp. 107–189. New York: Plenum Publishing Corporation.CrossRefGoogle Scholar
Masland, R.H. & Ames, A. III. (1976). Responses to acetylcholine of ganglion cells in an isolated mammalian retina. Journal of Neurophysiology 39, 1220–1235.CrossRefGoogle Scholar
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, 3069–3073.CrossRefGoogle ScholarPubMed
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. 221–234. Berlin: Springer-Verlag.CrossRefGoogle Scholar
Moore, J.W. & Westerfield, M. (1983). Action potential propagation and threshold parameters in inhomogeneous regions of squid axons. Journal of Physiology 336, 285–300.CrossRefGoogle ScholarPubMed
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, 3414–3418.CrossRefGoogle ScholarPubMed
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, 1394–1408.CrossRefGoogle ScholarPubMed
Peters, B.N. & Masland, R.H. (1996). Responses to light of starburst amacrine cells. Journal of Neurophysiology 75, 469–480.CrossRefGoogle ScholarPubMed
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, 905–928.CrossRefGoogle ScholarPubMed
Rall, W. (1959). Branching dendritic trees and motorneuron membrane resistivity. Experimental Neurology 1, 491–527.CrossRefGoogle Scholar
Rall, W. (1967). Distinguishing theoretical synaptic potentials computed for different soma-dendritic distributions of synaptic input. Journal of Neurophysiology 30, 1138–1168.CrossRefGoogle ScholarPubMed
Rall, W. (1969). Time constants and electrotonic length of membrane cylinders and neurons. Biophysical Journal 9, 1483–1508.CrossRefGoogle ScholarPubMed
Rall, W. (1978). Dendritic spines and synaptic potency. In Studies in Neurophysiology, ed. McIntyre, A.K., pp. 203–209. U.K.: Cambridge University Press.Google Scholar
Sholl, D.A. (1956). The Organization of the Cerebral Cortex. London: Metheun and Co., Ltd.Google ScholarPubMed
Taylor, W.R. & Wässle, H. (1995). Receptive field properties of cholinergic amacrine cells in the rabbit retina. European Journal of Neuroscience 7, 2308–2321.CrossRefGoogle ScholarPubMed
Vaney, D.I. (1990). The mosaic of amacrine cells in the mammalian retina. In Progress in Retinal Research, ed. Osborne, N. & Chader, G., pp. 49–100. New York: Pergamon.Google Scholar
Velte, T.J. & Miller, R.F. (1995). Dendritic integration of retinal ganglion cells in the mudpuppy. Visual Neuroscience 12, 165–175.CrossRefGoogle ScholarPubMed
Velte, T.J. & Miller, R.F. (1996). Computer simulations of voltage clamping retinal ganglion cells through whole-cell electrodes. Journal of Neurophysiology 75, 2129–2143.CrossRefGoogle ScholarPubMed
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, 233–247.CrossRefGoogle Scholar
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, 8057–8062.CrossRefGoogle Scholar