Dendritic Calcium Plateau Potentials Modulate Input–Output Properties of Juxtaglomerular Cells in the Rat Olfactory Bulb

Abstract

Understanding the intrinsic membrane properties of juxtaglomerular (JG) cells is a necessary step toward understanding the neural basis of olfactory signal processing within the glomeruli. We used patch-clamp recordings and two-photon Ca2+imaging in rat olfactory bulb slices to analyze a long-lasting plateau potential generated in JG cells and characterize its functional input–output roles in the glomerular network. The plateau potentials were initially generated by dendritic calcium channels. Bath application of Ni2+(250 μM to 1 mM) totally blocked the plateau potential. A local puff of Ni2+on JG cell dendrites, but not on the soma, blocked the plateau potentials, indicating the critical contribution of dendritic Ca2+channels. Imaging studies with two-photon microscopy showed that a dendritic Ca2+increase was always correlated with a dendritic but not a somatic plateau potential. The dendritic Ca2+conductance contributed to boosting the initial excitatory postsynaptic potentials (EPSPs) to produce the plateau potential that shunted and reduced the amplitudes of the following EPSPs. This enables the JG cells to act as low-pass filters to convert high-frequency inputs to low-frequency outputs. The low frequency (2.6 ± 0.8 Hz) of rhythmic plateau potentials appeared to be determined by the intrinsic membrane properties of the JG cell. These properties of the plateau potential may enable JG cells to serve as pacemaker neurons in the synchronization and oscillation of the glomerular network.