In previous studies, some channels, called the “sleeper channels,” were reported to contribute to the shaping of the action potential (AP) only under non-physiological conditions. These channels have been hypothesized to play a role in providing a protective mechanism to prevent damage from neuronal hyperexcitation. Here we applied two-electrode current clamp at the primary branch point (1°BP) and the presynaptic terminal simultaneously on crayfish axons. Cadmium had minimal effects on AP shaping, suggesting the absence of calcium-activated potassium channels. Application of 1 mM TEA had minimal impact on AP waveform. In the presence of 4-Aminopyridine (4-AP), the same tetraethylammonium (TEA) concentration significantly prolonged AP duration, resembling the behaviors of sleeper channels. The kinetics of the TEA-sensitive channel (Kv(TEA)) is similar to the Kv2 family of mammalian K+ channels. TEA depolarized the potential after an AP and increased the AP duration in a dose-dependent manner, indicating that these channels contributed to maintaining AP waveform majorly during the hyperpolarization. The terminals were more sensitive to the blockers, suggesting a probability of regulation on neurotransmitter release. However, the TEA-sensitive channels at the crayfish axon had a higher affinity to TEA than the Kv2 channels. Pharmacological profiles, spatial distinction and function of the Kv(TEA) in the crayfish axon require further study.