Stimulus-selective lateral signaling between olfactory afferents enables parallel encoding of distinct CO2 dynamics

Abstract

An important problem in sensory processing is how lateral interactions that mediate the integration of information across sensory channels function with respect to stimulus tuning. We demonstrate a novel form of selective crosstalk between specific olfactory channels that occurs between primary olfactory receptor neurons (ORNs). Neurotransmitter release from ORNs can be driven by two distinct sources of excitation, feedforward activity derived from the odorant receptor and lateral input originating from specific subsets of other ORNs. Consequently, levels of presynaptic release can become dissociated from firing rate. Stimulus-selective lateral signaling results in the distributed representation of CO2, a behaviorally important environmental cue that elicits spiking in only a single ORN class, in multiple olfactory channels. Different CO2-responsive channels preferentially transmit distinct stimulus dynamics, thereby expanding the coding bandwidth for CO2. These results generalize to additional odors and olfactory channels, revealing a subnetwork of lateral interactions between ORNs that reshape the spatial and temporal structure of odor representations in a stimulus-specific manner. One Sentence SummaryA novel subnetwork of stimulus-selective lateral interactions between primary olfactory sensory neurons enables new sensory computations.