Characterization of a Cone Bipolar Cell in the Rat Retina with Prominent Na+ Current: Predominant Expression of Inwardly Rectifying K+ Current and Terminal Stratification

Abstract

Abstract: : Purpose: A subset of retinal cone bipolar cells in the rat has been reported to express voltage–dependent Na⁺ current. To understand the functional role of expressing Na⁺ channels in bipolar cells, we investigated the physiological and morphological properties of Na⁺ current–bearing cone bipolar cells. Methods: Whole–cell patch–clamp recordings were performed to examine voltage–dependent currents of cone bipolar cells in retinal slices and isolated cells from the rat. The morphology of the recorded cells in slices was examined by filling fluorescent dye, Alexa 488. Antibody staining against Alexa 488 and acetylcholine transferase was performed to determine the terminal stratification of recorded cone bipolar cells. Results: A population of cone bipolar cells was found to show large voltage–dependent Na⁺ current. These cells also showed relatively large low–voltage–activated T–type Ca²⁺ current. Unlike many other cone bipolar cells which displayed large h–current (I_h), these cone bipolar cells displayed no or small I_h but inwardly rectifying K⁺ current (I_Kir). In current clamp, a prominent action potential could be evoked in the cells by current injection. Multiple action potential–like membrane oscillations were observed in some of the cells. The axon terminals of these cone bipolar cells were found to ramify in the middle of the inner plexiform layer, slightly distal to the inner cholinergic band. Some of their synapses appeared to overlap with the inner cholinergic band. We also observed another population of cone bipolar cells that had a similar terminal stratification level but a different terminal ramification pattern. Cone bipolar cells of this latter group, however, showed no apparent Na⁺ current but did show large I_h as well as I_Kir. Conclusions: We identified a subtype of retinal cone bipolar cells in the rat that express large Na⁺ and relatively large T–type Ca²⁺ currents and are capable of generating prominent action potentials and/or membrane oscillations. These cone bipolar cells express mainly I_Kir. Their terminals ramify in the middle of the inner plexiform layer and appear to share this stratification level with another group of physiologically distinct cone bipolar cells.

Keywords: bipolar cells • ion channels • electrophysiology: non–clinical