Optical manipulations reveal strong reciprocal inhibition but limited recurrent excitation within olfactory bulb glomeruli

Abstract

The local circuitry within olfactory bulb glomeruli filters, transforms, and facilitates information transfer from olfactory sensory neurons to bulb output neurons. Two key elements of this circuit are glutamatergic tufted cells (TCs) and GABAergic periglomerular (PG) cells, both of which actively shape mitral cell activity and bulb output. A subtype of TCs, the external tufted cells (eTCs), can synaptically excite PG cells, but there are unresolved questions about other aspects of the glomerular connections, including the extent of connectivity between eTCs and the precise nature of reciprocal interactions between eTCs and PG cells. We combined patch-clamp recordings in OB slices and optophysiological tools to investigate local functional connections within glomeruli. When TCs were optically suppressed, we found a large decrease in excitatory post-synaptic currents (EPSCs) in "uniglomerular" PG cells that extend dendrites to one glomerulus, indicating that TC activation was required for most excitation of these PG cells. However, TC suppression had no effect on EPSCs in eTCs, arguing that TCs make few, if any, direct excitatory synaptic connections onto eTCs. The absence of synaptic connections between eTCs was also supported by recordings in eTC pairs. Lastly, we show using similar optical suppression methods that PG cells that express GAD65, mainly uniglomerular PG cells, provide strong inhibition onto eTCs. Our results indicate that the local network of TCs form potent reciprocal synaptic connections with GAD65-expressing uniglomerular PG cells but not other TCs. This configuration favors local inhibition over recurrent excitation within a glomerulus, limiting information transfer to downstream cortical regions.