Differential Expression of High- and Two Types of Low-Voltage–Activated Calcium Currents in Rod and Cone Bipolar Cells of the Rat Retina

Abstract

Whole cell voltage-clamp recordings were performed to investigate voltage-activated Ca2+ currents in acutely isolated retinal bipolar cells of rats. Two groups of morphologically different bipolar cells were observed. Bipolar cells of the first group, which represent the majority of isolated bipolar cells, were immunoreactive to protein kinase C (PKC) and, therefore likely to be rod bipolar cells. Bipolar cells of the second group, which represent only a small population of isolated bipolar cells, did not show PKC immunoreactivity and were likely to be cone bipolar cells. The validity of morphological identification of bipolar cells was further confirmed by the presence of GABAC responses in these cells. Bipolar cells of both groups displayed low-voltage–activated (LVA) Ca2+ currents with similar voltage dependence of activation and steady-state inactivation. However, the activation, inactivation, and deactivation kinetics of the LVA Ca2+ currents between rod and cone bipolar cells differed. Particularly, the LVA Ca2+ currents of rod bipolar cells displayed both transient and sustained components. In contrast, the LVA Ca2+ currents of cone bipolar cells were mainly transient. In addition, the LVA Ca2+ channels of rod bipolar cells were more permeable to Ba2+ than to Ca2+, whereas those of cone bipolar cells were equally or less permeable to Ba2+ than to Ca2+. The LVA Ca2+ currents of both rod and cone bipolar cells were antagonized by high concentrations of nimodipine with IC50of 17 and 23 μM, respectively, but largely resistant to Cd2+ and Ni2+. Bipolar cells of both groups also displayed high-voltage–activated (HVA) Ca2+ currents. The HVA Ca2+ currents were, at least in part, to be L-type that were potentiated by BayK-8644 (1 μM) and largely antagonized by low concentrations of nimodipine (5 μM). The L-type Ca2+channels were almost exclusively located at the axon terminals of rod bipolar cells but expressed at least in the cell soma of cone bipolar cells. Results of this study indicate that rod and cone bipolar cells of the mammalian retina differentially express at least two types of LVA Ca2+ channels. Rod and cone bipolar cells also show different spatial distribution of L-type Ca2+channels.