Heterogeneous intrinsic firing properties of vertebrate retinal ganglion cells.

Abstract

Retinal ganglion cells (RGCs) use their characteristic firing patterns to encode various aspects of visual information and carry them to the brain. It has been thought that the firing pattern of an RGC's light response is determined primarily by the time course and spatiotemporal interaction of the synaptic inputs. However, it is unclear whether there is a difference in intrinsic firing properties among RGCs that could contribute to the cell-to-cell distinction of the light response firing pattern. We investigated the intrinsic firing properties of isolated goldfish RGCs, minimizing cytoplasmic disturbance with a perforated-patch, whole-cell recording technique. In response to a 1-s depolarizing current step, the majority of the examined RGCs (n = 84) displayed sustained firing that lasted over 800 ms (n = 24; tonic RGCs) or transient firing accommodated within 200 ms of the step onset (n = 47; phasic RGCs). Tonic and phasic RGCs also differed in their firing frequency-current intensity dynamics. There was a significant difference in the soma sizes of phasic and tonic RGCs, indicating that some parts of these groups originate from distinct morphological subtypes. In the presence of extracellular Ba(2+) (1 mM), phasic RGCs displayed sustained firing and firing frequency-current intensity dynamics similar to those of tonic RGCs. Thus a Ba(2+)-sensitive ion current (I(Ba-s)) underlies the firing characteristics of phasic RGCs. Under voltage-clamp conditions, I(Ba-s) was identified as a low-threshold, noninactivating voltage-dependent K(+) current. Because of its slow kinetics (time constant of activation, approximately 100 ms), I(Ba-s) may confer a gradually increasing hyperpolarizing driving force during maintained excitatory stimulus, which eventually would result in firing accommodation. These findings suggest that RGCs have heterogeneous intrinsic firing properties that could aid synaptic inputs in shaping light responses.