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 Ca(2+) 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 GABA(C) responses in these cells. Bipolar cells of both groups displayed low-voltage-activated (LVA) Ca(2+) currents with similar voltage dependence of activation and steady-state inactivation. However, the activation, inactivation, and deactivation kinetics of the LVA Ca(2+) currents between rod and cone bipolar cells differed. Particularly, the LVA Ca(2+) currents of rod bipolar cells displayed both transient and sustained components. In contrast, the LVA Ca(2+) currents of cone bipolar cells were mainly transient. In addition, the LVA Ca(2+) channels of rod bipolar cells were more permeable to Ba(2+) than to Ca(2+), whereas those of cone bipolar cells were equally or less permeable to Ba(2+) than to Ca(2+). The LVA Ca(2+) currents of both rod and cone bipolar cells were antagonized by high concentrations of nimodipine with IC(50) of 17 and 23 microM, respectively, but largely resistant to Cd(2+) and Ni(2+). Bipolar cells of both groups also displayed high-voltage-activated (HVA) Ca(2+) currents. The HVA Ca(2+) currents were, at least in part, to be L-type that were potentiated by BayK-8644 (1 microM) and largely antagonized by low concentrations of nimodipine (5 microM). The L-type Ca(2+) 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 Ca(2+) channels. Rod and cone bipolar cells also show different spatial distribution of L-type Ca(2+) channels.

Regulation of ON bipolar cell activity

“…The large degree of convergence of photoreceptor input onto bipolar cells, particularly in lower vertebrates, may require that the voltage response from local portions of the dendritic tree be "reset" so that illumination detected elsewhere in the receptive field is able to further depolarize the bipolar cell. L-type Ca 2+ channels expressed in ON bipolar cell terminals begin to turn on at around −50 mV, and the activation curve is steepest 23 between −45 mV and −35 mV (Protti, 1998;Pan, 2000). In darkness, bipolar cell membrane potential is at the foot of the L-type channel activation curve.…”

“…In the mouse (Tsukamoto et al, 2001), as in other mammalian retinas (reviewed in Bloomfield and Dacheux, 2001), rod bipolar cells synapse onto the AII amacrine cell (Kolb and Famiglietti, 1974). At the rod bipolar cell terminal, the predominant Ca 2+ channel, the L-type channel (Protti, 1998;Satoh et al, 1998;Hartveit, 1999;Pan, 2000), begins to activate between −40 mV and −45 mV (Protti, 1998;Hartveit, 1999;Singer and Diamond, 2003). In darkness, when rod bipolar cell synaptic channels are mostly closed, the resting potential of the rod bipolar cell has been measured to be between −59 mV and −47 mV (Berntson and Taylor, 2000;Euler and Masland, 2000;Pang et al, 2004;Wu et al, 2004).…”

Synchronizing multiphasic circadian rhythms of rhodopsin promoter expression in rod photoreceptor cells

“…To determine whether the decrease of cytoplasmic Ca 2+ concentration after dopamine treatment is due to an effect of dopamine on cGMP-gated cation channels, we measured the Ca 2+ concentration in rod cells in response to 8-pCPT-cGMP (a membrane permeable cGMP analog) and dopamine in the absence or presence of Co 2+ , which is known to block voltagegated Ca 2+ channels (Pan, 2000). The application of 8-pCPTcGMP (500·mol·l -1 ) increased cytoplasmic Ca 2+ concentration by 21.3±2.8% (P<0.001; Fig.·6C).…”

Mammalian Retinal Bipolar Cells Express Inwardly Rectifying K+ Currents (IKir) With a Different Distribution Than That of Ih

“…Bipolar cells were isolated from approximately 6-to 8-wk-old Long Evans rats by dissociation methods previously described (Pan 2000). All animal handling procedures were approved by the Institutional Animal Care Committee at Wayne State University and were in accordance with the National Institutes of Health Guide for the Care and Use of Laboratory Animals.…”

“…The resulting cell suspension was plated onto culture dishes. RBCs and CBCs were identified based on their characteristic morphology (Karschin and Wässle 1990;Pan 2000).…”