Cell type-specific and activity-dependent dynamics of action potential-evoked Ca2+ signals in dendrites of...

In most central neurons, action potentials (APs), generated in the initial axon segment, propagate back into dendrites and trigger considerable Ca(2+) entry via activation of voltage-sensitive calcium channels (VSCCs). Despite the similarity in its underlying mechanisms, however, AP-evoked dendritic Ca(2+) signalling often demonstrates a cell type-specific profile that is determined by the neuron dendritic properties. Using two-photon Ca(2+) imaging in combination with patch-clamp whole-cell recordings,we found that in distinct types of hippocampal inhibitory interneurons Ca(2+) transients evoked by backpropagating APs not only were shaped by the interneuron-specific properties of dendritic Ca(2+) handling but also involved specific Ca(2+) mechanisms that were regulated dynamically by distinct activity patterns. In dendrites of regularly spiking basket cells, AP-evoked Ca(2+) rises were of large amplitude and fast kinetics; however, they decreased with membrane hyperpolarization or following high-frequency firing episodes. In contrast, AP-evoked Ca(2+) elevations in dendrites of Schaffer collateral-associated cells exhibited significantly smaller amplitude and slower kinetics, but increased with membrane hyperpolarization. These cell type-specific properties of AP-evoked dendritic Ca(2+) signalling were determined by distinct endogenous buffer capacities of the interneurons examined and by specific types of VSCCs recruited by APs during different patterns of activity. Furthermore, AP-evoked Ca(2+) transients summated efficiently during theta-like bursting and were associated with the induction of long-term potentiation at inhibitory synapses onto both types of interneurons. Therefore, the cell type-specific profile of AP-evoked dendritic Ca(2+) signalling is shaped in an activity-dependent manner, such that the same pattern of hippocampal activity can be differentially translated into dendritic Ca(2+) signals in different cell types. However, Cell type-specific differences in Ca(2+) signals can be 'smoothed out' by changes in neuronal activity, providing a means for common, cell-type-independent forms of synaptic plasticity.