Role of hyperpolarization-activated currents for the intrinsic dynamics of isolated retinal neurons

The intrinsic dynamics of bipolar cells and rod photoreceptors isolated from tiger salamanders were studied by a patch-clamp technique combined with estimation of effective impulse responses across a range of mean membrane voltages. An increase in external K⁺ reduces the gain and speeds the response in bipolar cells near and below resting potential. High external K⁺ enhances the inward rectification of membrane potential, an effect mediated by a fast, hyperpolarization-activated, inwardly rectifying potassium current (K_IR). External Cs⁺ suppresses the inward-rectifying effect of external K⁺. The reversal potential of the current, estimated by a novel method from a family of impulse responses below resting potential, indicates a channel that is permeable predominantly to K⁺. Its permeability to Na⁺, estimated from Goldman-Hodgkin-Katz voltage equation, was negligible. Whereas the activation of the delayed-rectifier K⁺ current causes bandpass behavior (i.e., undershoots in the impulse responses) in bipolar cells, activation of the K_IR current does not. In contrast, a slow hyperpolarization-activated current (I_h) in rod photoreceptors leads to pronounced, slow undershoots near resting potential. Differences in the kinetics and ion selectivity of hyperpolarization-activated currents in bipolar cells (K_IR) and in rod photoreceptors (I_h) confer different dynamical behavior onto the two types of neurons.