Correlated firing in tufted cells of mouse olfactory bulb

Temporally correlated spike discharges are proposed to be important for the coding of olfactory stimuli. In the olfactory bulb, correlated spiking is known in two classes of output neurons, the mitral cells and external tufted cells. We studied a third major class of bulb output neurons, the middle tufted cells, analyzing their bursting and spike timing correlations, and their relation to mitral cells. Using patch-clamp and fluorescent tracing, we recorded spontaneous spiking from tufted-tufted or mitral-tufted cell pairs with visualized dendritic projections in mouse olfactory bulb slices. We found peaks in spike cross-correlograms indicating correlated activity on both fast (peak width 1-50 ms) and slow (peak width>50 ms) time scales, only in pairs with convergent glomerular projections. Coupling appeared tighter in tufted-tufted pairs, which showed correlated firing patterns and smaller mean width and lag of narrow peaks. Some narrow peaks resolved into 2-3 sub-peaks (width 1-12 ms), indicating multiple modes of fast correlation. Slow correlations were related to bursting activity, while fast correlations were independent of slow correlations, occurring in both bursting and non-bursting cells. The AMPA receptor antagonist NBQX (20 microM) failed to abolish broad or narrow peaks in either tufted-tufted or mitral-tufted pairs, and changes of peak height and width in NBQX were not significantly different from spontaneous drift. Thus, AMPA-receptors are not required for fast and slow spike correlations. Electrical coupling was observed in all convergent tufted-tufted and mitral-tufted pairs tested, suggesting a potential role for gap junctions in concerted firing. Glomerulus-specific correlation of spiking offers a useful mechanism for binding the output signals of diverse neurons processing and transmitting different sensory information encoded by common olfactory receptors.