T-Type Ca 2+ Channels Boost Neurotransmission in Mammalian Cone Photoreceptors.

It is a commonly accepted view that light stimulation of mammalian photoreceptors causes a graded change in membrane potential instead of developing a spike. The presynaptic Ca 2+ channels serve as a crucial link for the coding of membrane potential variations into neurotransmitter release. Ca v 1.4 L-type Ca 2+ channels are expressed in photoreceptor terminals, but the complete pool of Ca 2+ channels in cone photoreceptors appears to be more diverse. Here, we discovered, employing whole-cell patch-clamp recording from cone photoreceptor terminals in both sexes of mice, that their Ca 2+ currents are composed of low- (T-type Ca 2+ channels) and high- (L-type Ca 2+ channels) voltage-activated components. Furthermore, Ca 2+ channels exerted self-generated spike behavior in dark membrane potentials, and spikes were generated in response to light/dark transition. The application of fast and slow Ca 2+ chelators revealed that T-type Ca 2+ channels are located close to the release machinery. Furthermore, capacitance measurements indicated that they are involved in evoked vesicle release. Additionally, RT-PCR experiments showed the presence of Ca v 3.2 T-type Ca 2+ channels in cone photoreceptors but not in rod photoreceptors. Altogether, we found several crucial functions of T-type Ca 2+ channels, which increase the functional repertoire of cone photoreceptors. Namely, they extend cone photoreceptor light-responsive membrane potential range, amplify dark responses, generate spikes, increase intracellular Ca 2+ levels, and boost synaptic transmission. SIGNIFICANCE STATEMENT Photoreceptors provide the first synapse for coding light information. The key elements in synaptic transmission are the voltage-sensitive Ca 2+ channels. Here, we provide evidence that mouse cone photoreceptors express low-voltage-activated Ca v 3.2 T-type Ca 2+ channels in addition to high-voltage-activated L-type Ca 2+ channels. The presence of T-type Ca 2+ channels in cone photoreceptors appears to extend their light-responsive membrane potential range, amplify dark response, generate spikes, increase intracellular Ca 2+ levels, and boost synaptic transmission. By these functions, Ca v 3.2 T-type Ca 2+ channels increase the functional repertoire of cone photoreceptors.