Heterogeneity and convergence of olfactory first-order neurons account for the high speed and sensitivity of second-order neurons

PLoS Comput Biol. 2014 Dec 4;10(12):e1003975. doi: 10.1371/journal.pcbi.1003975. eCollection 2014 Dec.

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.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Computational Biology
  • Male
  • Models, Neurological*
  • Moths / physiology
  • Neurons / physiology*
  • Olfactory Pathways / physiology*
  • Olfactory Receptor Neurons / metabolism
  • Olfactory Receptor Neurons / physiology*
  • Pheromones / metabolism

Substances

  • Pheromones

Grants and funding

This work was funded by the Agence Nationale de la Recherche within the French-British ANR BBSRC SysBio 006 01 “Pherosys” initiative (http://www.neurochem-project.org/), the European FP7-ICT 2007 STREP Bio-ICT convergence “Neurochem” (http://www.informatics.sussex.ac.uk/research/projects/PheroSys/) and the state program “Investissements d′avenir” managed by the Agence Nationale de la Recherche, grant ANR-10-BINF-05 “Pherotaxis” (http://www.agence-nationale-recherche.fr/investissements-d-avenir/appels-a-projets/2010/bioinformatique). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.