Action Potential Backpropagation and Multiglomerular Signaling in the Rat Vomeronasal System

Abstract

In the accessory olfactory bulb (AOB), sensory neurons expressing a given vomeronasal receptor (VR) gene send divergent projections to many glomeruli, and second-order neurons (mitral cells) link to multiple glomeruli via branched primary dendrites. We used calcium imaging and paired somadendritic patch-clamp recording to track backpropagated action potentials (APs) in rat AOB primary dendrites. In cells loaded with 150 microm Calcium Orange, somatic spikes elicited fluorescence transients over the entire primary dendritic tree, and the relative fluorescence increment DeltaF/F(0) increased along all branches from soma to glomeruli. Backpropagation was reliant on Na+ channels: in 1 microm TTX, somatic AP commands evoked dendritic Ca2+ transients that declined steeply with distance. In paired soma- dendritic whole-cell recordings, backpropagated APs were unattenuated up to approximately 200 microm from the soma, whereas subthreshold voltage transients decayed markedly. Computational modeling indicated that the large distal Ca2+ transients are consistent with active, not passive, backpropagation. Genetic tracing in the AOB has suggested homotypic connectivity with individual mitral cell dendritic arbors projecting only to glomeruli targeted by sensory neurons expressing the same VR gene. Non-decremental, non-dichotomous backpropagation in AOB primary dendrites ensures fast, reliable communication between mitral cells and their homotypic glomeruli, binding them into functional modules in accordance with their VR-coded inputs.