The type of K(+) channels controlling the waveform of the presynaptic spike and synaptic transmission were examined in the lamprey spinal cord. Reticulospinal neuron somata displayed a transient K(+) current with a high voltage-activation and inactivation. This current was selectively blocked by catechol at 100 microM. Reticulospinal axons also displayed a high voltage-activated fast K(+) current sensitive to catechol. The function of this presynaptic high voltage-activated fast K(+) current in controlling synaptic transmission was investigated by using paired intracellular recordings from reticulospinal axons and their targets. Blockade of this current by catechol (100 microM) prolonged the presynaptic spike elicited by a single stimulus leading to a potentiation of the postsynaptic EPSP. Calcium imaging of reticulospinal axons showed an increase in presynaptic calcium transients after blockade of the presynaptic K(+) current by catechol. During high frequency firing, catechol revealed an activity-dependent decrease in the spike duration, which resulted in a depression of synaptic transmission. These results suggest that the presynaptic high voltage-activated transient K(+) current acts to optimize the temporal fidelity of synaptic transmission by minimizing activity-dependent changes in the presynaptic spike waveform and calcium dynamics.