Two types of cone bipolar cells express voltage-gated Na⁺ channels in the rat retina

Abstract

Two groups of retinal cone bipolar cells (CBCs) in rats were found to express voltage-gated Na + channels. The axon terminals of the first group stratify in sublamina 2 of the inner plexiform layer (IPL) and partially overlap with the OFF-cholinergic band. This group was identified as type 3 CBCs. The axon terminals of the second group stratify in sublamina 3 of the IPL, slightly distal to the ONcholinergic band. Cells of this second group resemble type 5 CBCs. In addition, we observed another group of ON-type CBCs with terminal stratification similar to that of the second group. However, this latter group did not show any Na + current, instead exhibiting a large hyperpolarization-activated cyclic nucleotide-gated cation current, suggesting the existence of two subclasses of physiologically distinct type 5 CBCs. Both groups of Na + -expressing bipolar cells were capable of generating a rapid TTX sensitive action potential as revealed by current injection. Multiple spike-like potentials were also observed in some of these cells. Results of this study provide valuable insights into the function of voltage-gated Na + channels of retinal bipolar cells in retinal processing.

Specific Wiring of Distinct Amacrine Cells in the Directionally Selective Retinal Circuit Permits Independent Coding of Direction and Size

“…SACs express predominantly TTX-insensitive Na + channels (Oesch and Taylor, 2010), excluding them as a target for TTX. On average, we did observe a mild decrease in excitation/inhibition evoked by small spots in the presence of TTX, which could be due to an effect on spiking AII amacrine cells, bipolar cells which express TTX-sensitive Na + channels (Cui and Pan, 2008), and/or noncanonical excitatory amacrine cells recently shown to contact DSGCs and express TTX-sensitive Na + channels (Grimes et al, 2011). However, the most striking effect was that TTX increased the amplitude of both EPSCs and IPSCs evoked by large spots (400-1,000 mm), clearly indicating a presynaptic inhibitory mechanism that relies on spiking.…”

Selective Activation of Neuronal Targets With Sinusoidal Electric Stimulation

“…Importantly, our work here suggests that voltage-gated sodium channels are not a necessary component for a neuron to respond to electric stimulation. In the physiological experiments, bipolar cells and photoreceptors were highly sensitive to LFSS, despite the fact that they are nonspiking, do not exhibit voltage-gated sodium currents (Kawai et al 2001(Kawai et al , 2002, and do not express dense regions of sodium channels (Cui and Pan 2008). This strongly suggests that other types of voltage gated ion channels underlie the response to electric stimulation in these cells; results from the computer simulation implicate voltage-gated calcium channels as a likely candidate.…”

Functional Circuitry of the Retina

“…Experiments combining light responses and current injection suggested that low-pass characteristics (i.e., suppression of high temporal frequencies) depended on intrinsic properties of the bipolar cells, whereas high-pass characteristics (i.e., suppression of low temporal frequencies) were generated through synaptic mechanisms. Electrophysiological and immunohistochemical analyses have demonstrated the expression of transient, voltage-gated conductances such as I h , I Na , and T-type Ca currents in different ON and OFF bipolar cells (de la Villa et al 1998, DeVries et al 2006, Cui & Pan 2008, Hu et al 2009); and some bipolar cell types generate Na or Ca channel–dependent spikes in response to photoreceptor input, which should make the output more transient (Protti et al 2000, Ichinose et al 2005, Baden et al 2011, Saszik & DeVries 2012). Thus, the postsynaptic responses of bipolar cells in the various parallel pathways are diverse and contribute to differential signaling by distinct pathways.…”