The Journal of Neurophysiology Vol. 78 No. 4 October 1997, pp. 1935-1947
Copyright ©1997 The American Physiological Society

Impulse Encoding Mechanisms of Ganglion Cells in the Tiger Salamander Retina

J. F. Fohlmeister and R. F. Miller

Department of Physiology, University of Minnesota, Minneapolis, Minnesota 55455

Fohlmeister, J. F. and R. F. Miller. Impulse encoding mechanisms of ganglion cells in the tiger salamander retina. J. Neurophysiol. 78: 1935-1947, 1997. A study of nerve impulse generation in ganglion cells of the tiger salamander retina is carried out through a combination of experimental and analytic approaches, including computer simulations based on a single-compartment model. Whole cell recordings from ganglion cells were obtained using a superfused retina-eyecup preparation and studied with pharmacological and electrophysiological techniques, including phase plot analysis. Experimental efforts were guided by computer simulation studies of an excitability model consisting of five voltage- or ion-gated channels, which were identified from earlier voltage-clamp data. The ion channels include sodium, calcium, and three types of potassium channels, namely the A type (I_K,A), Ca-activated potassium (I_K,Ca), and the delayed rectifier (I_K). A leakage channel was included to preserve input resistance continuity between model and experiment. Ion channel densities of Na and Ca currents (I_Na and I_Ca) for the single-compartment model were independently determined from phase plot analysis. The I_K and I_K,A current densities were determined from the measured width of impulses. The I_K,Ca was modeled to respond to Ca influx, and a variable-rate Ca-sequestering mechanism was implemented to remove cytoplasmic calcium. Impulse frequency increases when either I_Ca or I_K,Ca is eliminated from the model or blocked pharmacologically in whole cell recording experiments. Faithful simulations of experimental data show that the ionic currents may be grouped into small (I_K,Ca, leakage, and stimulus), and large (I_Na, I_K, I_A, I_Ca) on the basis of their peak magnitudes throughout the impulse train. This division of the currents is reflected in their function of controlling the interspike interval (small currents) and impulse generation (large currents). Although the single-compartmental model is qualitatively successful in simulating impulse frequency behavior and its controlling mechanisms, limitations were found that specifically suggest the need to include morphological details. The spike train analysis points to a role for electrotonic currents in the control of the duration of the interspike intervals, which can be compensated by prolonged activation of g_K,Ca in the single-compartment model. A detailed, multicompartmental model of the ganglion cell is presented in the companion paper.

This article has been cited by other articles:

				L. Sirovich Populations of Tightly Coupled Neurons: The RGC/LGN System Neural Comput., May 1, 2008; 20(5): 1179 - 1210. [Abstract] [Full Text] [PDF]

				R. F. Miller, N. P. Staff, and T. J. Velte Form and Function of ON-OFF Amacrine Cells in the Amphibian Retina J Neurophysiol, May 1, 2006; 95(5): 3171 - 3190. [Abstract] [Full Text] [PDF]

				N. K. Dhingra, M. A. Freed, and R. G. Smith Voltage-Gated Sodium Channels Improve Contrast Sensitivity of a Retinal Ganglion Cell J. Neurosci., August 31, 2005; 25(35): 8097 - 8103. [Abstract] [Full Text] [PDF]

				R. M. Glantz and J. P. Schroeter Encoder Adaptation Modulates the Visual Responses of Crayfish Interneurons J Neurophysiol, July 1, 2004; 92(1): 327 - 340. [Abstract] [Full Text] [PDF]

				N. K. Dhingra and R. G. Smith Spike Generator Limits Efficiency of Information Transfer in a Retinal Ganglion Cell J. Neurosci., March 24, 2004; 24(12): 2914 - 2922. [Abstract] [Full Text] [PDF]

				S. C. Lee, Y. Hayashida, and A. T. Ishida Availability of Low-Threshold Ca2+ Current in Retinal Ganglion Cells J Neurophysiol, December 1, 2003; 90(6): 3888 - 3901. [Abstract] [Full Text] [PDF]

				M.C.W. van Rossum, B. J. O'Brien, and R. G. Smith Effects of Noise on the Spike Timing Precision of Retinal Ganglion Cells J Neurophysiol, May 1, 2003; 89(5): 2406 - 2419. [Abstract] [Full Text] [PDF]

				K. J. Kim and F. Rieke Slow Na+ Inactivation and Variance Adaptation in Salamander Retinal Ganglion Cells J. Neurosci., February 15, 2003; 23(4): 1506 - 1516. [Abstract] [Full Text] [PDF]

				T. Tabata and M. Kano Heterogeneous Intrinsic Firing Properties of Vertebrate Retinal Ganglion Cells J Neurophysiol, January 1, 2002; 87(1): 30 - 41. [Abstract] [Full Text] [PDF]

				B. W. Sheasby and J. F. Fohlmeister Impulse Encoding Across the Dendritic Morphologies of Retinal Ganglion Cells J Neurophysiol, April 1, 1999; 81(4): 1685 - 1698. [Abstract] [Full Text] [PDF]

				J. F. Fohlmeister and R. F. Miller Mechanisms by Which Cell Geometry Controls Repetitive Impulse Firing in Retinal Ganglion Cells J Neurophysiol, October 1, 1997; 78(4): 1948 - 1964. [Abstract] [Full Text] [PDF]