Developmental changes in the inward current of the action potential of Rohon-Beard neurones

Abstract

1. Rohon-Beard cells in the spinal cord of Xenopus tadpoles have been studied in animals from early neural tube to free-swimming larval stages. The onset and further development of electrical excitability of these neurones has been investigated in different ionic environments, to determine the ionic species carrying the inward current of the action potential.2. The cells appear inexcitable at early stages (Nieuwkoop & Faber stages 18-20) and do not give action potentials to depolarizing current pulses.3. The action potential is first recorded at stage 20. (A) The inward current is carried by Ca(2+) at stages 20-25, since it is blocked by mm quantitites of La(3+), Co(2+) or Mn(2+) and is unaffected by removal of Na(+) or the addition of tetrodotoxin (TTX). (B) The action potential is an elevated plateau of long duration (mean 190 msec at stages 20-22). The duration decreases exponentially with repetitive stimulation. (C) The specific Ca(2+) conductance (g(Ca)) at the onset of the plateau of the action potential is 2.6 x 10(-4) mho/cm(2). Calculations show that a single action potential raises [Ca(2+)](1) by more than 100-fold.4. At later times (stages 25-40), the inward current of the action potential is carried by both Na(+) and Ca(2+): the action potential has two components, an initial spike which is blocked by removal of Na(+) or addition of TTX, followed by a plateau which is blocked by La(3+), Co(2+) or Mn(2+).5. Finally (stages 40-51), the inward current is primarily carried by Na(+), since the action potential is blocked only by removal of Na(+) or addition of TTX, and the overshoot agrees with the prediction of the Nernst equation for a Na-selective membrane. When the outward current channel is blocked and cells exposed to Na-free solutions, 67% of cells at the latest stages studied were incapable of producing action potentials in which the inward current is carried by divalent cations.6. The duration of the action potential decreases from a maximum of about 1000 msec to about 1 msec during development. The maximum input resistance (R(in)) decreases from ca. 1000 to 100 MOmega.7. The calcium action potential may play a role in the development of excitability and the growth of the neurones.