A Hopf-like bifurcation produces depolarization block that expands the peripheral encoding of odors

Animals identify odors based on the combinatorial activation of olfactory sensory neurons having distinct chemical receptive fields. However, as the dose response of any olfactory sensory neuron is believed to follow a sigmoidal function that grows monotonically until it reaches a plateau, the subset of olfactory sensory neurons activated by an odor is expected to scale up with the odor concentration, undercutting the efficiency of combinatorial coding. Here we show that olfactory sensory neurons can in fact undergo a silent state upon strong and prolonged excitation called depolarization block, as part of their normal physiological function at ethologically-relevant odor concentrations. This silencing typically occurs at odor concentrations three orders of magnitude above the detection threshold of the olfactory sensory neuron. Using a data-driven model of the olfactory transduction cascade paired with a conductance-based spike generation model, we present a plausible biophysical mechanism that explains the emergence of depolarization block as a dynamical Hopf-like bifurcation. Quantitative predictions related to the history dependence and timescale of depolarization block are validated experimentally, allowing us to predict and simulate the activity of olfactory sensory neurons during larval navigation in odor gradients. We find that the same odor can induce depolarization block in distinct types of olfactory sensory neurons according to a concentration sequence matching their relative sensitivities to the odor, which fractionates the odor concentration space into domains corresponding to different subsets of active olfactory sensory neurons. We argue that depolarization block might facilitate perceptual recognition and discrimination over a large odor concentration range by maintaining sparsity in neural representations. While the role of depolarization block has been largely overlooked in chemosensory systems, our results suggest that this phenomenon creates a new dimension that expands the coding capacity of the peripheral encoding of odors.