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Voltage-gated Ca 2+  channels are composed of a pore-forming α 1  subunit and auxiliary β and α 2 δ subunits, which modulate Ca 2+  current properties and channel trafficking. So far, the partial redundancy and specificity of α 1  for α 2 δ subunits in the CNS have remained largely elusive. Mature spiral ganglion (SG) neurons express α 2 δ subunit isoforms 1, 2, and 3 and multiple Ca 2+  channel subtypes. Differentiation and  in vivo  functions of their endbulb of Held synapses, which rely on presynaptic P/Q channels ( Lin et al., 2011 ), require the α 2 δ3 subunit ( Pirone et al., 2014 ). This led us to hypothesize that P/Q channels may preferentially co-assemble with α 2 δ3. Using a dissociated primary culture, we analyzed the effects of α 2 δ3 deletion on somatic Ca 2+  currents ( I Ca  ) of SG neurons isolated at postnatal day 20 (P20), when the cochlea is regarded to be mature. P/Q currents were the dominating steady-state Ca 2+  currents (54% of total) followed by T-type, L-type, N-type, and R-type currents. Deletion of α 2 δ3 reduced P/Q- and R-type currents by 60 and 38%, respectively, whereas L-type, N-type, and T-type currents were not altered. A subset of  I Ca   types was also analyzed in SG neurons isolated at P5, i.e., before the onset of hearing (P12). Both L-type and N-type current amplitudes of wildtype SG neurons were larger at P5 compared with P20. Deletion of α 2 δ3 reduced L-type and N-type currents by 23 and 44%, respectively. In contrast, small P/Q currents, which were just being up-regulated at P5, were unaffected by the lack of α 2 δ3. In summary, α 2 δ3 regulates amplitudes of L- and N-type currents of immature cultured SG neurons, whereas it regulates P/Q- and R-type currents at P20. Our data indicate a developmental switch from dominating somatic N- to P/Q-type currents in cultured SG neurons. A switch from N- to P/Q-type channels, which has been observed at several central synapses, may also occur at developing endbulbs of Held. In this case, reduction of both neonatal N- (P5) and more mature P/Q-type currents (around/after hearing onset) may contribute to the impaired morphology and function of endbulb synapses in α 2 δ3-deficient mice.

frontiers in cellular neuroscience

Deletion of the Ca2+ Channel Subunit α2δ3 Differentially Affects Cav2.1 and Cav2.2 Currents in Cultured Spiral Ganglion Neurons Before and After the Onset of Hearing