Normal and rebound impulse firing in retinal ganglion cells

Abstract

Given that the action potential output of retinal ganglion cells (RGCs) determines the nature of the visual information that is transmitted from the retina, an understanding of their intrinsic impulse firing characteristics is critical for an appreciation of the overall processing of visual information. Recordings from RGCs within an isolated whole-mount retina preparation showed that their normal impulse firing from the resting membrane potential (RMP) was linearly correlated in its frequency with the stimulus intensity. In addition to describing the relationship between the magnitude of the current injection and the resulting impulse frequency (F/I relationship), we have characterized the properties of individual action potentials when they are elicited from the RMP. In contrast, hyperpolarizing below the RMP revealed that RGCs displayed a time dependent anomalous rectification, manifested by the appearance of a depolarizing sag in their voltage response. When an adequate period of hyperpolarization was terminated, a fast phasic period of “rebound excitation” was observed, characterized by a brief phasic burst of impulse activity. When compared to equivalent action potential firing evoked by depolarizing from the RMP, rebound spiking was associated with a lower threshold and shorter latency for impulse activation as well as a prominent, phasic, burst-like doublet, or triplet of impulses. The rebound action potential had a more positive voltage overshoot and displayed a higher peak rate of rise in its upstroke than those correspondingly generated by depolarizing current pulses from the RMP. Blocking sodium spikes with TTX confirmed that the preceding hyperpolarization led to the recruitment and subsequent generation of a transient depolarizing voltage overshoot, which we have termed the net depolarizing overshoot (NDO). We propose that the NDO boosts the generation of sodium spikes by triggering rebound spikes on its upstroke and crest, thus accounting for the observed voltage dependent change in the firing pattern of RGCs.