Odor encoding by fine-timescale spike synchronization patterns in the olfactory bulb

In the mammalian olfactory bulb (OB), gamma oscillations in the local field potential are generated endogenously during odor sampling. Such oscillations arise from dynamical systems that generate organized periodic behavior in neural circuits and correspond to spike timing constraints at millisecond timescales. Although the cellular and network mechanisms of gamma oscillogenesis in the OB are reasonably well established, it remains unclear how these fine-timescale dynamics serve to represent odors. Are patterns of spike synchronization on the gamma timescale replicable and odor-specific? Does the transformation to a spike-timing metric embed additional signal processing computations? To address these questions, we used OB slice recordings to examine the spike timing dynamics evoked by "fictive odorants" generated via spatiotemporally patterned optogenetic stimulation of olfactory sensory neuron axonal arbors. We found that a small proportion of mitral/tufted cells phase-lock strongly to the fast oscillations evoked by fictive odorants and exhibit tightly coupled spike-spike synchrony on the gamma timescale. Moreover, the specific population of synchronized neurons corresponded to the "quality," but not the "concentration" (intensity), of the fictive odorant presented, and was conserved across multiple presentations of the same fictive odorant. Given the established selectivity of piriform cortical pyramidal neurons for inputs synchronized on this timescale, we conclude that spike synchronization on a milliseconds timescale is a metric by which the OB encodes and exports afferent odor information in a concentration-invariant manner. As a corollary, mitral/tufted cell spikes that are not organized in time are unlikely to contribute meaningfully to the ensemble odor representation.NEW & NOTEWORTHY Neurophysiological activity patterns often are interpreted as simple mean spike rates, without consideration of the intrinsic representational timescales established by the dynamical systems of the brain. We here show that principal neuron spike timing in the olfactory bulb circuit is regulated by such fast internal network dynamics, and that these tightly synchronized spikes encode sensory information into a form interpretable by downstream target neurons.