Abstract
In the olfactory system of male moths, a specialized subset of neurons detects and processes the main component of the sex pheromone emitted by females. It is composed of several thousand first-order olfactory receptor neurons (ORNs), all expressing the same pheromone receptor, that contact synaptically a few tens of second-order projection neurons (PNs) within a single restricted brain area. The functional simplicity of this system makes it a favorable model for studying the factors that contribute to its exquisite sensitivity and speed. Sensory information—primarily the identity and intensity of the stimulus—is encoded as the firing rate of the action potentials, and possibly as the latency of the neuron response. We found that over all their dynamic range, PNs respond with a shorter latency and a higher firing rate than most ORNs. Modelling showed that the increased sensitivity of PNs can be explained by the ORN-to-PN convergent architecture alone, whereas their faster response also requires cell-to-cell heterogeneity of the ORN population. So, far from being detrimental to signal detection, the ORN heterogeneity is exploited by PNs, and results in two different schemes of population coding based either on the response of a few extreme neurons (latency) or on the average response of many (firing rate). Moreover, ORN-to-PN transformations are linear for latency and nonlinear for firing rate, suggesting that latency could be involved in concentration-invariant coding of the pheromone blend and that sensitivity at low concentrations is achieved at the expense of precise encoding at high concentrations.
Highlights
In insects and vertebrates the first two neuronal layers of the olfactory system present the same organization where many olfactory receptor neurons (ORNs) in the first layer converge to a small number of output neurons in the second layer – projection neurons (PNs) in insects and mitral cells in vertebrates [1,2]
This is a significant advantage for experimental analysis with respect to glomeruli sensitive to general odors that receive both homotypic and heterotypic inputs because of the lack of specificity of generalist ORNs [7]. Apart from this difference, which allowed us to record responses with welldefined input, the isomorphic glomeruli involved in general odor processing and the cumulus share the same functional organization, so that the main properties found here for the pheromonal system should apply to the general odorant system. We found that both firing rates and latencies of ORNs and PNs are strongly dose-dependent, that PNs respond with a higher firing rate and a shorter latency than most ORNs, and that the sensitivity and speed of a given neuron are not correlated
The rare stained LNs we found (3 among 67 stained cells) were monophasic. These observations do not rule out the existence of LNs with a multiphasic response pattern, they support the contention that multiphasic LNs are rare in our recording conditions, which means that most if not all recorded neurons were PNs
Summary
In insects and vertebrates the first two neuronal layers of the olfactory system present the same organization where many ORNs in the first layer converge to a small number of output neurons in the second layer – PNs in insects and mitral cells in vertebrates [1,2]. The ORNs that project onto a single glomerulus express a single type of olfactory receptors They present heterogeneous dose–response properties [3]. Experiments in the fruit fly reveal that firing rates rise more rapidly in PNs than in ORNs and that weak odor inputs are more amplified than strong inputs [6,7,8]. Such a non-linear transformation leads to an efficient use of coding capacity [6] and a maximum preservation of information on odor quality [9]
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