SUMMARY Single channel properties of Ca²⁺-activated K⁺ (BK or Maxi-K) channels have been investigated in presynaptic membranes in Xenopus motoneuron-muscle cell cultures. The occurrence and density of BK channels increased with maturation/synaptogenesis and was not uniform: highest at the release face of bouton-like synaptic varicosities in contact with muscle cells, and lowest in varicosities that did not contact muscle cells. The Ca²⁺ affinity of the channel (Kd = 7.7 µM at a membrane potential of +20 mV) was lower than those of BK channels that have been characterized in other terminals. Hill coefficients varied between 1.5 and 2.8 at different potentials and open probability increased e-fold per 16 mV change in membrane potential over a range of [Ca²⁺]_i from 1 µM to 1 mM. The maximal activation rate of ensembled single BK channel currents was in the sub-millisecond range at +20 mV. The activation rate increased ~ 10-fold in response to a [Ca²⁺]_i increase from 1 to 100 µM, but increased only ~ 2-fold with a voltage change from +20 to +130 mV. The fastest activation kinetics of BK channels in cell-attached patches resembled that in inside-out patches with [Ca²⁺]_i of 100 µM or more, suggesting that many BK channels are located very close to calcium channels. Given the low Ca2+ affinity and rapid Ca²⁺ binding/unbinding properties, we conclude that BK channels in this preparation are adapted to play an important role in regulation of neurotransmitter release, and that they are ideal reporters of local [Ca²⁺] at the inner membrane surface.