T-Type Ca 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 channels serve as a crucial link for the coding of membrane potential variations into neurotransmitter release. Ca1.4 L-type Ca channels are expressed in photoreceptor terminals, but the complete pool of Ca 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 currents are composed of low- (T-type Ca channels) and high- (L-type Ca channels) voltage-activated components. Furthermore, Ca 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 chelators revealed that T-type Ca 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 Ca3.2 T-type Ca channels in cone photoreceptors but not in rod photoreceptors. Altogether, we found several crucial functions of T-type Ca 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 levels, and boost synaptic transmission. Photoreceptors provide the first synapse for coding light information. The key elements in synaptic transmission are the voltage-sensitive Ca channels. Here, we provide evidence that mouse cone photoreceptors express low-voltage-activated Ca3.2 T-type Ca channels in addition to high-voltage-activated L-type Ca channels. The presence of T-type Ca channels in cone photoreceptors appears to extend their light-responsive membrane potential range, amplify dark response, generate spikes, increase intracellular Ca levels, and boost synaptic transmission. By these functions, Ca3.2 T-type Ca channels increase the functional repertoire of cone photoreceptors.