Hostname: page-component-745bb68f8f-lrblm Total loading time: 0 Render date: 2025-01-11T17:38:04.193Z Has data issue: false hasContentIssue false
  • English
  • Français

Dendritic integration in ganglion cells of the mudpuppy 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

Computer simulations were carried out to evaluate the influence of varying the membrane resistance (Rm) on the dendritic integration capacity of three classes of ganglion cells in the mudpuppy (Necturus maculosus) retina. Three broadly different morphological classes of ganglion cells were selected for this study and represent the range of dendritic tree sizes found in the ganglion cell population of this species. Simulations were conducted on anatomical data obtained from cells stained with horseradish peroxidase; each cell was traced, using a computer as an entry device and later converted to a compartmental (electrical) representation of the cell. Computer-simulation analysis used a time-variant conductance change which was similar in waveform to light-activated bipolar cell input. The simulated membrane resistance for each cell varied between 5000 and 100,000 Ω cm2, and conductance changes were introduced into different regions of the soma-dendritic tree to evaluate dendritic integration efficiency. When higher values of Rm are used, even the largest cells become electrotonically compact and attenuation of voltage responses is minimized from distal to soma regions. Responses were less attenuated from proximal to distal regions of the cell because of the favorable impedance matching, and because less current is required to polarize small “sealed” dendritic terminations. Steady-state responses integrate more effectively than transient responses, particularly when Rm is high, since transient responses were more attenuated by the membrane capacitance. The possibility that Rm is a dynamic property of retinal ganglion cells is discussed in view of the functional organization of dendritic integration efficiency as Rm fluctuates from low to high values.

Keywords

RetinaDendritic integrationCompartmental modelingGanglion cellMembrane resistance
Type
Research Articles
Information
Visual Neuroscience , Volume 12 , Issue 1 , January 1995 , pp. 165 - 175
Copyright
Copyright © Cambridge University Press 1995

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

Arkin, M.S. & Miller, R.F. (1988). Mudpuppy retinal ganglion cell morphology revealed by an HRP impregnation technique which provides Golgi-like staining. Journal of Comparative Neurology 270, 185–208.Google Scholar
Brown, A.M., Schwindt, P.C. & Crill, W.E. (1993). Voltage dependence and activation kinetics of pharmacologically defined components of the high-threshold calcium current in rat neocortical neurons. Journal of Neurophysiology 70, 1530–1543.CrossRefGoogle ScholarPubMed
Carnevale, N.T., Woolf, T.B. & Shepherd, G.M. (1990). Neuron simulations with saber. Journal of Neuroscience Methods 33, 135–148.CrossRefGoogle ScholarPubMed
Carras, P.L., Coleman, P.A. & Miller, R.F. (1992). Site of action potential initiation in amphibian retinal ganglion cells. Journal of Neurophysiology 67, 292–304.Google Scholar
Cohen, E. & Sterling, P. (1991). Microcircuitry related to the receptive filed center of the on-beta ganglion cell. Journal of Neurophysiology 65, 352–359.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.Google Scholar
Doll, C.J., Hochachka, P.W. & Reiner, P.B. (1991). Channel arrest: Implications from membrane resistance in turtle neurons. American Journal of Physiology 261(5 Pt. 2), R1321–4.Google Scholar
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
Jack, J.J.B., Noble, D. & Tsien, R.W. (1975). Electric Current Flow in Excitable Cells. Oxford, UK: Claredon Press.Google Scholar
Koch, C., Poggio, T. & Torre, V. (1982). Retinal ganglion cells: A functional interpretation of dendritic morphology. Philosophical Transactions of the Royal Society B (London) 298, 227–264.Google ScholarPubMed
Lasater, E.M. & Witkovsky, P. (1990). Membrane currents of spiking cells isolated from turtle retina. Journal of Comparative Physiology A 167, 11–21.Google 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. & Dacheux, R.F. (1976). Synaptic organization and ionic basis of on and off channels in mudpuppy retina. I. Intracellular analysis of chloride-sensitive electrogenic properties of receptors, horizontal cells, bipolar cells, and amacrine cells. Journal of General Physiology 67, 639–659.Google Scholar
Miller, R.F., Dacheux, R.F. & Frumkes, T.E. (1977). Amacrine cells in necturus retina: Evidence for independent γ-aminobutyric acid-and glycine-releasing neurons. Science 198, 748–750.Google Scholar
Miller, R.F., Slaughter, M.M. & Dick, E. (1982). Excitatory, inhibitory and peptidergic pathways in the mudpuppy retina. In Neurotransmitter Interaction and Compartmentation, ed. Bradford, H.F., pp. 735–759. New York: Plenum Publishing Corporation.CrossRefGoogle Scholar
Nitzan, R., Segev, I. & Yarom, Y. (1990). Voltage behavior along the irregular dendritic structure of morphologically and physiologically characterized vagal motoneurons in the guinea pig. Journal of Neurophysiology 63, 333–346.Google Scholar
Pongracz, F., Firestein, S. & Shepherd, G.M. (1991). Electrotonic structure of olfactory sensory neurons analyzed by intracellular and whole-cell patch techniques. Journal of Neurophysiology 65, 747–758.Google Scholar
Rall, W. (1959). Branching dendritic trees and motorneuron membrane resistivity. Experimental Neurology 1, 491–527.Google 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. (1977). Core conductor theory and cable properties of neurons. In Handbook of Physiology: The Nervous System: Volume 1, Sect. 1, pp. 39–97. Bethesda, Maryland: American Physiological Society.Google Scholar
Rall, W. & Rinzel, J. (1973). Branch input resistance and steady attenuation for input to one branch of a dendritic model. Biophysical Journal 13, 648–688.CrossRefGoogle Scholar
Segev, I. (1992). Single neurone models: Oversimple, complex and reduced. Trends in Neuroscience 15(11), 414–421.Google Scholar
Segev, I., Fleshman, J.W. & Burke, R.E. (1989). Compartmental models of complex neurons. In Methods in Neuronal Modeling: From Synapses to Networks, ed. Koch, C. & Segev, I., pp. 63–96. Bradford, Massachusetts: MIT Press.Google Scholar
Sholl, D.A. (1956). The Organization of the Cerebral Cortex. London, England: Metheun & Co., Ltd.Google Scholar
Spruston, N., Jaffe, D.B. & Johnston, D. (1994). Dendritic attenuation of synaptic potentials and currents: The role of passive membrane. Trends in Neuroscience 17(4), 161–166.CrossRefGoogle ScholarPubMed
Spruston, N. & Johnston, D. (1992). Perforated patch-clamp analysis of the passive membrane properties of three classes of hippo-campal neurons. Journal of Neurophysiology 67, 508–529.CrossRefGoogle Scholar
Staley, K.J., Otis, T.S. & Mody, I. (1992). Membrane properties of dentate gyrus granule cells: Comparison of sharp microelectrodes and whole-cell recordings. Journal of Neurophysiology 67, 1346–1358.Google Scholar
Wunk, D.F. & Werblin, F.S. (1979). Synaptic inputs to the ganglion cells in the tiger salamander retina. Journal of General Physiology 73, 265–286.CrossRefGoogle Scholar