Spatio-temporal activity patterns of odor-induced synchronized potentials revealed by voltage-sensitive dye imaging and intracellular recording in the antennal lobe of the cockroach

In animals, odor qualities are represented as both spatial activity patterns of glomeruli and temporal patterns of synchronized oscillatory signals in the primary olfactory centers. By optical imaging of a voltage-sensitive dye (VSD) and intracellular recording from secondary olfactory interneurons, we examined possible neural correlates of the spatial and temporal odor representations in the primary olfactory center, the antennal lobe (AL), of the cockroach Periplaneta americana. Voltage-sensitive dye imaging revealed that all used odorants induced odor-specific temporal patterns of depolarizing potentials in specific combinations of anterior glomeruli of the AL. The depolarizing potentials evoked by different odorants were temporally synchronized across glomeruli and were termed “synchronized potentials.” These observations suggest that odor qualities are represented by spatio-temporal activity patterns of the synchronized potentials across glomeruli. We also performed intracellular recordings and stainings from secondary olfactory interneurons, namely projection neurons and local interneurons. We analyzed the temporal structures of enanthic acid-induced action potentials of secondary olfactory interneurons using simultaneous paired intracellular recording from two given neurons. Our results indicated that the multiple local interneurons synchronously fired in response to the olfactory stimulus. In addition, all stained enanthic acid-responsive projection neurons exhibited dendritic arborizations within the glomeruli where the synchronized potentials were evoked. Since multiple local interneurons are known to synapse to a projection neuron in each glomerulus in the cockroach AL, converging inputs from local interneurons to the projection neurons appear to contribute the odorant specific spatio-temporal activity patterns of the synchronized potentials.