A slowly inactivating potassium current truncates spike activity in ganglion cells the tiger salamander retina

Abstract

Voltage-gated ganglion cell membrane currents were studied under whole-cell patch clamp in isolation and in retinal slices. The cells were identified by (1) backfilling their axons with rhodamine and later identifying them by their fluorescence in the slice or the mix of isolated cells or (2) by filling them with Lucifer yellow during recording in retinal slices. Both methods yieled cells with similar currents. In some cases, isolated cells lacked processes yet showed currents similar to other cells, suggesting that voltage-gated currents in all cells were located primarily at the soma. Both a conventional inactivating sodium current and a sustained calcium current were found. We describe 3 inactivating outward currents, ordered in their rate of inactivation. The fastest current resembled I(A) reported by Connor and Stevens (1971a,b). A slower current labeled I(B) inactivated with a time constant of 339 msec at 0 mV. The current with slowest inactivation is labeled I(C) here, inactivating with a time constant of 4.03 sec at 0 mV. An additional outward current was sustained and calcium dependent, labeled I(K(Ca)). I(B) was the largest of these currents. It was slower than I(A), was not blocked by 4AP, and inactivated over a much more positive potential range. I(B) appears to play an important role in spike generation, different from that of I(A): Its inactivation leads to a slow depolarizing shift of the membrane during a current step, truncating spike activity after about 300-700 msec as the membrane potential enters the region of sodium inactivation. We analyze how the inactivating outward current acts to ensure a graded spiking response and to truncate the spiking output in the presence of large excitatory inputs.