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Passive electrical cable properties and synaptic excitation of tiger salamander retinal ganglion cells

Published online by Cambridge University Press:  02 June 2009

W. Rowland Taylor ,
Scott Mittman  and
David R. Copenhagen
W. Rowland Taylor
Affiliation:
Departments of Ophthalmology and Physiology and Program in Neurosciences, UCSF School of Medicine, San Francisco
Scott Mittman
Affiliation:
Departments of Ophthalmology and Physiology and Program in Neurosciences, UCSF School of Medicine, San Francisco
David R. Copenhagen
Affiliation:
Departments of Ophthalmology and Physiology and Program in Neurosciences, UCSF School of Medicine, San Francisco
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Abstract

The passive electrical properties of 17 ON-OFF retinal ganglion cells were derived from electrophysiological recordings. The parameters for each cells' equivalent model were obtained from the transient current responses to small step changes in clamp potential. Thirteen of the cells could be adequately approximated by a spherical soma connected to an equivalent dendritic cable. Estimates for the cell input conductance (GN), membrane time constant (τm), the dendritic-to-soma conductance ratio (ρ), and the normalized electrotonic length (L) were obtained (mean ± standard deviation, n = 13): GN = 580 ± 530 pS, τm = 97 ±72 ms, ρ = 2.8 ± 2.8, and L = 0.34 ± 0.13. Series resistance averaged 32 ± 11 MΩ The mean of the derived soma diameters was 18 ± 6 μm and the mean diameter and length of the equivalent cables were 1.4 ± 0.6 and 470 ± 90 μm, respectively. The average of the specific membrane conductances, 1.67 ± 1.08 S/cm2, corresponded to a membrane resistivity of 60 kΩ-cm2. Computer simulations of synaptic inputs were performed on a representative model, with an electrode at the soma and using the worst-case configuration, in which all synaptic inputs were confined to the tips of the dendrites. We draw three conclusions from the modeling: (1) Under voltage clamp, fast, spontaneous EPSCs would be significantly attenuated and slowed while the time course of the slower, light-evoked non-NMDA and NMDA EPSCs would be minimally distorted by dendritic filtering. (2) Excitatory synaptic reversal potentials can be accurately determined under voltage clamp. (3) In the absence of GABAergic and glycinergic inhibition, the efficacy at the soma of excitatory conductance changes is essentially independent of their dendritic location. The specific membrane resistivity appears to represent a good compromise between having a small membrane time constant and minimal EPSP attenuation.

Keywords

NMDAEPSCPassive electrotonic propertiesDendriteFiltering
Type
Research Articles
Information
Visual Neuroscience , Volume 13 , Issue 5 , September 1996 , pp. 979 - 990
Copyright
Copyright © Cambridge University Press 1996

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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.CrossRefGoogle ScholarPubMed
Barrett, J.N. & Crill, W.E. (1974). Specific membrane properties of cat motoneurones. Journal of Physiology 239, 301–324.CrossRefGoogle ScholarPubMed
Clements, J.D. & Redman, S.J. (1989). Cable properties of cat spinal motoneurones measured by combining voltage clamp, current clamp and intracellular staining. Journal of Physiology 409, 63–87.CrossRefGoogle ScholarPubMed
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
Diamond, J.S. & Copenhagen, D.R. (1993). The contribution of NMDA and non-NMDA receptors to the light-evoked input-output characteristics of retinal ganglion cell. Neuron 11, 725–738.CrossRefGoogle Scholar
Eliasof, S., Barnes, S. & Werblin, F. (1987). The interaction of ionic currents mediating single spike activity in retinal amacrine cells of the tiger salamander. Journal of Neuroscience 7, 3512–3524.CrossRefGoogle ScholarPubMed
Glenn, L.L. (1988). Overestimation of the electrical length of neuron dendrites and synaptic electrotonic attenuation. Neuroscience Letters 91, 112–119.CrossRefGoogle ScholarPubMed
Hines, M.A. (1989). A program for simulation of nerve equations with branching geometries. International Journal of Bioinedical Computing 24, 55–68.Google ScholarPubMed
Holmes, W.R. & Rall, W. (1992 a). Electrotonic length estimates in neurons with dendritic tapering or somatic shunt. Journal of Neuro-physiology 68, 1421–1437.CrossRefGoogle ScholarPubMed
Holmes, W.R. & Rall, W. (1992 b). Estimating the electrotonic structure of neurons with compartmental models. Journal of Neurophysiology 68, 1438–1452.CrossRefGoogle ScholarPubMed
Holmes, W.R., Segev, I. & Rall, W. (1992). Interpretation of time constant and electrotonic length estimates in multicylinder or branched neuronal structures. Journal of Neurophysiology 68, 1401–1420.CrossRefGoogle ScholarPubMed
Jackson, M.B. (1992). Cable analysis with whole-cell patch clamp. Theory and experiment. Biophysical Journal 61, 756–766.CrossRefGoogle ScholarPubMed
Johnston, D. & Brown, T.H. (1983). Interpretation of voltage-clamp measurements in hippocampal neurons. Journal of Neurophysiology 50, 464–486.CrossRefGoogle ScholarPubMed
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
Lukasiewicz, P. & Werblin, F. (1988). A slowly inactivating potassium current truncates spike activity in ganglion cells of the tiger salamander retina. Journal of Neuroscience 8, 4470–4481.CrossRefGoogle ScholarPubMed
Lukasiewicz, P. & Werblin, F. (1994). A novel GABA receptor modulates synaptic transmission from bipolar to ganglion and amacrine cells in the tiger salamander retina. Journal of Neuroscience 14, 1213–1223.CrossRefGoogle ScholarPubMed
Major, G., Larkman, A.U., Jonas, P., Sakmann, B. & Jack, J.I. (1994). Detailed passive cable models of whole-cell recorded CA3 pyramidal neurons in rat hippocampal slices. Journal of Neuroscience 14, 4613–4638.CrossRefGoogle ScholarPubMed
Mittman, S. (1990). Excitation of retinal ganglion cells. Pharmacological and voltage-clamp analysis of the roles of N-methyl-D-aspartate (NMDA) and non-NMDA receptors. Ph.D. Dissertation, University of California, San Francisco.Google Scholar
Mittman, S., Taylor, W.R. & Copenhagen, D.R. (1990). Concomitant activation of two types of glulamate receptor mediates excitation of salamander retinal ganglion cells. Journal of Physiology 428, 175–197.CrossRefGoogle Scholar
Peichl, L. & Wässle, H. (1983). The structural correlate of the receptive field centre of alpha ganglion cells in the cat retina. Journal of Physiology 341, 309–324.CrossRefGoogle ScholarPubMed
Perkel, D.H. & Mulloney, B. (1978). Electrotonic properties of neurons: Steady-state compartmental models. Journal of Neurophysiology 41, 621–639.CrossRefGoogle 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.CrossRefGoogle ScholarPubMed
Press, W.H., Flannery, B.P., Teukolsky, S.A. & Vetterling, W.T. (1988). Numerical Recipes in C. Cambridge, Cambridge University Press.Google Scholar
Rall, W. (1962). Theory of physiological properties of dendrites. Annals of the New York Academy of Science 96, 1071–1092.CrossRefGoogle ScholarPubMed
Rall, W. (1964). Theoretical significance of dendritic trees for neuronal input-output relations. In Neural Theory and Modeling, ed. Reiss, R.F., pp. 73–97. Stanford, California: Stanford University Press.Google Scholar
Rall, W. (1977). Core conductor theory and cable properties of neurons. In Handbook of Physiology. The Nervous System. Cellular Biology of Neurons, ed. Kandell, E.R., pp. 39–97. Bethesda, Maryland: American Physiological Society.Google Scholar
Rapp, M., Segev, I. & Yarom, Y. (1994). Physiology, morphology and detailed passive models of guinea-pig cerebellar Purkinje cells. Journal of Physiology 474, 101–118.CrossRefGoogle ScholarPubMed
Rose, P.K. & Dagum, A. (1988). Nonequivalent cylinder models of neurons: Interpretation of voltage transients generated by somatic current injection. Journal of Neurophysiology 60, 125–148.CrossRefGoogle ScholarPubMed
Spruston, N., Jaffe, D.B., Williams, S.H. & Johnston, D. (1993). Voltage- and space-clamp errors associated with the measurement of electrotonically remote synaptic events. Journal of Neurophysiology 70, 781–802.CrossRefGoogle ScholarPubMed
Spruston, N. & Johnston, D. (1992). Perforated patch-clamp analysis of the passive and membrane properties of three classes of hippocampal neurons. Journal of Neurophysiology 67, 509–529.CrossRefGoogle ScholarPubMed
Stampfli, R. & Hille, B. (1976). Electrophysiology of the peripheral myelinated nerve. In Frog Neurobiology, ed. Llinas, R. & Precht, W., pp. 3–32. New York: Springer-Verlag.CrossRefGoogle Scholar
Taylor, W.R., Chen, E.P. & Copenhagen, D.R. (1995). Characterization of spontaneous excitatory synaptic currents in Salamander retinal ganglion cells. Journal of Physiology 486, 207–221.CrossRefGoogle ScholarPubMed
Velte, T.J. & Miller, R.F. (1995). Dendritic integration in ganglion cells of the mudpuppy retina. Visual Neuroscience 12, 165–175.CrossRefGoogle ScholarPubMed
Wässle, H., Peichl, L. & Boycott, B.B. (1981). Dendritic territories of cat retinal ganglion cells. Nature 292, 344–345.CrossRefGoogle ScholarPubMed