The Journal of Neurophysiology Vol. 80 No. 6 December 1998, pp. 3047-3061
Copyright ©1998 The American Physiological Society

Development of Ionic Currents Underlying Changes in Action Potential Waveforms in Rat Spinal Motoneurons

Bao-Xi Gao and Lea Ziskind-Conhaim

Department of Physiology and Center for Neuroscience, University of Wisconsin Medical School, Madison, Wisconsin 53706

Gao, Bao-Xi and Lea Ziskind-Conhaim. Development of ionic currents underlying changes in action potential waveforms in rat spinal motoneurons. J. Neurophysiol. 80: 3047-3061, 1998. Differentiation of the ionic mechanism underlying changes in action potential properties was investigated in spinal motoneurons of embryonic and postnatal rats using whole cell voltage- and current-clamp recordings. Relatively slow-rising, prolonged, largely Na⁺-dependent action potentials were recorded in embryonic motoneurons, and afterdepolarizing potentials were elicited in response to prolonged intracellular injections of depolarizing currents. Action potential amplitude, as well as its rates of rise and repolarization significantly increased, and an afterhyperpolarizing potential (AHP) became apparent immediately after birth. Concurrently, repetitive action potential firing was elicited in response to a prolonged current injection. To determine the ionic mechanism underlying these changes, the properties of voltage-gated macroscopic Na⁺, Ca²⁺, and K⁺ currents were examined. Fast-rising Na⁺ currents (I_Na) and slow-rising Ca²⁺ currents (I_Ca) were expressed early in embryonic development, but only I_Na was necessary and sufficient to trigger an action potential. I_Na and I_Ca densities significantly increased while the time to peak I_Na and I_Ca decreased after birth. The postnatal increase in I_Na resulted in overshooting action potential with significantly faster rate of rise than that recorded before birth. Properties of three types of outward K⁺ currents were examined: transient type-A current (I_A), noninactivating delayed rectifier-type current (I_K), and Ca²⁺-dependent K⁺ current (I_K(Ca)). The twofold postnatal increase in I_K and I_K(Ca) densities resulted in shorter duration action potential and the generation of AHP. Relatively large I_A was expressed early in neuronal development, but unlike I_K and I_K(Ca) its density did not increase after birth. The three types of K⁺ channels had opposite modulatory actions on action potential firing behavior: I_K and I_A increased the firing rate, whereas I_K(Ca) decreased it. Our findings demonstrated that the developmental changes in action potential waveforms and the onset of repetitive firing were correlated with large increases in the densities of existing voltage-gated ion channels rather than the expression of new channel types.

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