Synaptic sodium spikes trigger long-lasting depolarizations and slow calcium entry in rat olfactory bulb granule cells

In the mammalian olfactory bulb, axonless granule cells mediate self- and lateral inhibitory interactions between mitral/tufted cells via reciprocal dendrodendritic synapses. Synaptic output from granule cells occurs on both fast and slow timescales, allowing for multiple granule cell functions during olfactory processing. We find that granule cell sodium action potentials evoked by synaptic activation of the sensory input via mitral/tufted cells are followed by a long-lasting depolarization that is not observed after current-evoked action potentials or large excitatory postsynaptic potentials in the same cell. Using two-photon imaging in acute rat brain slices, we demonstrate that this prolonged electrical response is paralleled by an unusual, long-lasting postsynaptic calcium signal. We find that this slow synaptic Ca²⁺ signal requires sequential activation of NMDA receptors, a nonselective cation conductance I_CAN and T-type voltage-dependent Ca²⁺ channels. Remarkably, T-type Ca²⁺ channels are of critical importance for the 'globalization' of Ca²⁺ transients. In individual active spines, the local synaptic Ca²⁺ signal summates at least linearly with the global spike-mediated Ca²⁺ signal. We suggest that this robust slow synaptic Ca²⁺ signal triggers dendritic transmitter release and thus contributes to slow synaptic output of the granule cell. Therefore, the synaptic sodium spike signal could represent a special adaptation of granule cells to the wide range of temporal requirements for their dendritic output. Our findings demonstrate with respect to neuronal communication in general that action potentials evoked by somatic current injection may lack some of the information content of 'true' synaptically evoked spikes.