A slowly inactivating potassium current truncates spike activity in ganglion cells of 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 yielded 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 IA reported by Connor and Stevens (1971a, b). A slower current labeled IB inactivated with a time constant of 339 msec at 0 mV. The current with slowest inactivation is labeled IC here, inactivating with a time constant of 4.03 sec at 0 mV. An additional outward current was sustained and calcium dependent labeled IK(Ca). IB was the largest of these currents. It was slower than IA, was not blocked by 4AP, and inactivated over a much more positive potential range. IB appears to play an important role in spike generation, different from that of IA: 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.

Sodium Channels in Transient Retinal Bipolar Cells Enhance Visual Responses in Ganglion Cells

“…3) than that reported for amacrine cells or ganglion cells (Barnes and Werblin, 1986;Lukasiewicz and Werblin, 1988). The enhancement of the slow, light-evoked EPSCs in bipolar cells is consistent with these currents being persistent.…”

Evoked membrane potential change in rat optic nerve fiber: Computer simulation

“…The AP depolarization is due to fast Na + channels, and the repolarization is due to a 4-AP-sensitive K + current similar to the A-current found in other experiments [3,4] . In the presence of 4-AP, AP is broadened (approximately doubled), then followed by a depolarizing afterpotential (DAP) (dozens of milliseconds) and a late, TEA-sensitive, hyperpolarizing afterpotential (AHP) (several hundreds of milliseconds).…”

“…This is coherent with the supposed delaying role of the A-current of other mammalian neurons [25] . And it is the opposite of the A-current in salamander retinal ganglion cells [4] , where 4-AP decreases spike frequency. In the presence of both 4-AP and TEA, i.e.…”

Spike-Dependent GABA Inputs to Bipolar Cell Axon Terminals Contribute to Lateral Inhibition of Retinal Ganglion Cells

“…In the salamander, these channels have been observed on ganglion and amacrine cells but never on other retinal neurons (Barnes and Werblin 1986;Lukasiewicz and Werblin 1988). Our results suggest inhibitory, lateral transmission in the IPL depended on spiking in wide-field amacrine cells and not on sodium channel activity in photoreceptors, horizontal cells, or bipolar cells, as we detail in the following text.…”