Intrinsic physiological properties of cat retinal ganglion cells.

Abstract

Retinal ganglion cells (RGCs) are the output neurons of the retina, sending their signals via the optic nerve to many different targets in the thalamus and brainstem. These cells are divisible into more than a dozen types, differing in receptive field properties and morphology. Light responses of individual RGCs are in large part determined by the exact nature of the retinal synaptic network in which they participate. Synaptic inputs, however, are greatly influenced by the intrinsic membrane properties of each cell. While it has been demonstrated clearly that RGCs vary in their intrinsic properties, it remains unclear whether this variation is systematically related to RGC type. To learn whether membrane properties contribute to the functional differentiation of RGC types, we made whole-cell current clamp recordings of RGC responses to injected current of identified cat RGCs. The data collected demonstrated that RGC types clearly differed from one another in their intrinsic properties. One of the most striking differences we observed was that individual cell types had membrane time constants that varied widely from approximately 4 ms (alpha cells) to more than 80 ms (zeta cells). Perhaps not surprisingly, we also observed that RGCs varied greatly in their maximum spike frequencies (kappa cells 48 Hz-alpha cells 262 Hz) and sustained spike frequencies (kappa cells 23 Hz-alpha cells 67 Hz). Interestingly, however, most RGC types exhibited similar amounts of spike frequency adaptation. Finally, RGC types also differed in their responses to injection of hyperpolarizing current. Most cell types exhibited anomalous rectification in response to sufficiently strong hyperpolarization, although alpha and beta RGCs showed only minimal, if any, rectification under similar conditions. The differences we observed in RGC intrinsic properties were striking and robust. Such differences are certain to affect how each type responds to synaptic input and may help tune each cell type appropriately for their individual roles in visual processing.