Abstract
Although inhibition has often been proposed as a central mechanism for coordinating activity in the olfactory system, relatively little is known about how activation of different inhibitory local circuit pathways can generate coincident inhibition of principal cells. We used serotonin (5-HT) as a pharmacological tool to induce spiking in ensembles of mitral cells (MCs), a primary output neuron in the olfactory bulb, and recorded intracellularly from pairs of MCs to directly assay coincident inhibitory input. We find that 5-HT disynaptically depolarized granule cells (GCs) only slightly but robustly increased the frequency of inhibitory postsynaptic inhibitory currents in MCs. Serotonin also triggered more coincident IPSCs in pairs of nearby MCs than expected by chance, including in MCs with truncated apical dendrites that lack glomerular synapses. That serotonin-triggered coincident inhibition in the absence of elevated GC somatic firing rates suggested that synchronized MC inhibition arose from glutamate receptor-mediated depolarization of GC dendrites or other (non-GC) interneurons outside the glomerular layer. Tetanic stimulation of GCL afferents to GCs triggered robust GC spiking, coincident inhibition in pairs of MCs, and recruited large-amplitude IPSCs in MCs. Enhancing neurotransmission through NMDARs by lowering the external Mg2+ concentration also increased inhibitory tone onto MCs but failed to promote synchronized inhibition. These results demonstrate that coincident MC inhibition can occur through multiple circuit pathways and suggests that the functional coordination between different GABAergic synapses in individual GCs can be dynamically regulated.