Calcium-induced Transitions between the Spontaneous Miniature Outward and the Transient Outward Currents in Retinal Amacrine Cells

Spontaneous miniature outward currents (SMOCs) occur in a subset of retinal amacrine cells at membrane potentials between −60 and −40 mV. At more depolarized potentials, a transient outward current (I_to) appears and SMOCs disappear. Both SMOCs and the I_to are K⁺ currents carried by BK channels. They both arise from Ca²⁺ influx through high voltage–activated (HVA) Ca²⁺ channels, which stimulates release of internal Ca²⁺ from caffeine- and ryanodine-sensitive stores. An increase in Ca²⁺ influx resulted in an increase in SMOC frequency, but also led to a decline in SMOC mean amplitude. This reduction showed a temporal dependence: the effect being greater in the latter part of a voltage step. Thus, Ca²⁺ influx, although required to generate SMOCs, also produced a negative modulation of their amplitudes. Increasing Ca²⁺ influx also led to a decline in the first latency to SMOC occurrence. A combination of these effects resulted in the disappearance of SMOCs, along with the concomitant appearance of the I_to at high levels of Ca²⁺ influx. Therefore, low levels of Ca²⁺ influx, arising from low levels of activation of the HVA Ca²⁺ channels, produce randomly occurring SMOCs within the range of −60 to −40 mV. Further depolarization leads to greater activation of the HVA Ca²⁺ channels, larger Ca²⁺ influx, and the disappearance of discontinuous SMOCs, along with the appearance of the I_to. Based on their characteristics, SMOCs in retinal neurons may function as synaptic noise suppressors at quiescent glutamatergic synapses.