Isolated ascidian Halocynthia roretzi blastomeres of the muscle lineage exhibit muscle cell-like excitability upon differentiation despite the arrest of cell cleavage early in development. This characteristic provides a unique opportunity to track changes in ion channel expression during muscle cell differentiation. Here, we show that the intrinsic membrane property of ascidian cleavage-arrested muscle-type cells becomes oscillatory by expressing transient outward currents (I_to) activated by Ca²⁺-induced Ca²⁺ release (CICR) in a maturation-dependent manner. In current clamp mode, most day four (72-h after fertilization) cleavage-arrested muscle cells exhibited an oscillatory membrane potential of -20 mV at 15 Hz, whereas most day three (48-h after fertilization) cells exhibited a spiking pattern. In voltage-clamp mode, the day four cells exhibited prominent transient outward currents which were not present in day three cells. I_to was abolished by the application of 10 mM caffeine, implying that CICR was involved in I_to activation. I_to was based on K⁺ efflux and sensitive to TEA and some BK channel inhibitors. We found a 60-pS single channel conductance that was activated by local Ca²⁺ release in ascidian muscle. Voltage-clamp recording with an oscillatory waveform as a command pulse showed that CICR-activated K⁺ currents were activated during the falling phase of the membrane potential oscillation. These results suggest that developmental expression of CICR-activated K⁺ current plays a role in the maturation of larval locomotion by modifying the intrinsic membrane excitability of muscle cells.