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Origins of correlated spiking in the mammalian olfactory bulb

Significance Neurons exhibit temporally correlated patterns of activity, and the brain is believed to process information in part by exploiting these correlations. Here we use new analytic tools to show that in the olfactory bulb, the first processing station for smell in mammals, these correlations emerge primarily from the animal’s own breathing pattern, and also from the sparse connectivity of the cells that ultimately transmit olfactory information to higher brain areas. These results inform our understanding of how, and how well, the brain can represent information about smell and provide insight into the importance of active sampling processes in sensory coding. Mitral/tufted (M/T) cells of the main olfactory bulb transmit odorant information to higher brain structures. The relative timing of action potentials across M/T cells has been proposed to encode this information and to be critical for the activation of downstream neurons. Using ensemble recordings from the mouse olfactory bulb in vivo, we measured how correlations between cells are shaped by stimulus (odor) identity, common respiratory drive, and other cells’ activity. The shared respiration cycle is the largest source of correlated firing, but even after accounting for all observable factors a residual positive noise correlation was observed. Noise correlation was maximal on a ∼100-ms timescale and was seen only in cells separated by <200 µm. This correlation is explained primarily by common activity in groups of nearby cells. Thus, M/T-cell correlation principally reflects respiratory modulation and sparse, local network connectivity, with odor identity accounting for a minor component.