The well-documented role of neuromuscular activity as a regulator of motoneuron and muscle development raises important questions about the differentiation of excitability in motoneurons. We have recently described changes in expression of voltage-dependent calcium currents that take place during neuromuscular development in the chick embryo (McCobb et al., 1989). We now report similar analyses, using whole-cell patch-recording methods, of the major currents underlying action potential generation in the same motoneurons. Studies were conducted on identified hindlimb motoneurons isolated from the spinal cord at 3 very different stages of chick hindlimb development. Motoneurons could generate overshooting action potentials at the earliest stage studied [embryonic day 4 (E4)]. However, large changes in densities of several voltage-dependent ionic currents occurred thereafter. E6 and E11 motoneurons had progressively larger INa densities and, consequently, greater action potential amplitudes. Densities of 2 potassium currents, Ik and IA, increased on separate schedules. The relatively late and much larger increase in IA resulted in a substantial developmental decline in action potential duration. These changes, which will greatly affect motoneuron output to muscle by affecting Ca2+ entry through voltage-gated channels, occur at the same time that activity-dependent developmental changes occur in the neuromuscular system.