Distinct Ca2+ Channels Mediate Transmitter Release at Excitatory Synapses Displaying Different Dynamic Properties in Rat Neocortex

Abstract

To study the type of presynaptic calcium channels controlling transmitter release at synaptic connections displaying depression or facilitation, dual whole cell recordings combined with biocytin labelling were performed in acute slices from motor cortex of 17- to 22-day-old rats. Layer V postsynaptic interneurons displayed either fast spiking (FS) (n = 12) or burst firing (BF) (n = 12) behaviour. The axons of FS cells ramified preferentially around pyramidal cell somata, while BF cell axons ramified predominately around pyramidal cell dendrites. Synapses between pyramidal cells and FS cells displayed brief train depression (n = 12). Bath application of ω-Agatoxin IVA (0.5 μM), blocking P/Q-type calcium channels, decreased mean peak amplitudes of the EPSPs to 40% of control EPSPs (n = 8). Failure rate of the EPSPs after the first presynaptic action potential increased from 9 ± 11 to 28 ± 15%. This was associated with an increase in paired pulse ratio of 152 ± 44%. ω-Conotoxin GVIA (1-10 μM), selectively blocking N-type calcium channels, had no effect on peak amplitudes or frequency dependent properties of these connections (n = 5). Synapses from pyramidal cells to BF cells displayed brief train facilitation (n = 8). Application of ω-Conotoxin in these connections decreased peak amplitudes of the EPSPs to 15% of control EPSPs (n = 6) and decreased the paired pulse ratio by 41 ± 30%. ω-Agatoxin did not have any significant effect on the EPSPs elicited in BF cells. This study indicates that P/Q-type calcium channels are associated with transmitter release at connections displaying synaptic depression, whereas N-type channels are predominantly associated with connections displaying facilitation.