Neurons respond to sensory stimuli by altering the rate and temporal pattern of action potentials. These spike trains both encode and propagate information that guides behavior. Local inhibitory networks can affect the information encoded and propagated by neurons by altering correlations between different spike trains. Correlations introduce redundancy that can reduce encoding but also facilitate propagation of activity to downstream targets. Given this trade-off, how can networks maximize both encoding and propagation efficacy? Here, we examine this problem by measuring the effects of olfactory bulb inhibition on the pairwise statistics of mitral cell spiking. We evoked spiking activity in the olfactory bulb in vitro and measured how lateral inhibition shapes correlations across timescales. We show that inhibitory circuits simultaneously increase fast correlation (i.e., synchrony increases) and decrease slow correlation (i.e., firing rates become less similar). Further, we use computational models to show the benefits of fast correlation/slow decorrelation in the context of odor coding. Olfactory bulb inhibition enhances population-level discrimination of similar inputs, while improving propagation of mitral cell activity to cortex. Our findings represent a targeted strategy by which a network can optimize the correlation structure of its output in a dynamic, activity-dependent manner. This trade-off is not specific to the olfactory system, but rather our work highlights mechanisms by which neurons can simultaneously accomplish multiple, and sometimes competing, aspects of sensory processing.

Inhibitory circuits are critical for shaping odor representations in the olfactory bulb. There, individual granule cells can respond to brief stimulation with extremely long (up to 1000 ms), input-specific latencies that are highly reliable. However, the mechanism and function of this long timescale activity remain unknown. We sought to elucidate the mechanism responsible for long-latency activity, and to understand the impact of widely distributed interneuron latencies on olfactory coding. We used a combination of electrophysiological, optical, and pharmacological techniques to show that long-latency inhibition is driven by late onset synaptic excitation to granule cells. This late excitation originates from tufted cells, which have intrinsic properties that favor longer latency spiking than mitral cells. Using computational modeling, we show that widely distributed interneuron latency increases the discriminability of similar stimuli. Thus, long-latency inhibition in the olfactory bulb requires a combination of circuit- and cellular-level mechanisms that function to improve stimulus representations.

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