Adaptation of olfactory receptor abundances for efficient coding
Abstract
Olfactory receptor usage is highly heterogeneous, with some receptor types being orders of magnitude more abundant than others. We propose an explanation for this striking fact: the receptor distribution is tuned to maximally represent information about the olfactory environment in a regime of efficient coding that is sensitive to the global context of correlated sensor responses. This model predicts that in mammals, where olfactory sensory neurons are replaced regularly, receptor abundances should continuously adapt to odor statistics. Experimentally, increased exposure to odorants leads variously, but reproducibly, to increased, decreased, or unchanged abundances of different activated receptors. We demonstrate that this diversity of effects is required for efficient coding when sensors are broadly correlated, and provide an algorithm for predicting which olfactory receptors should increase or decrease in abundance following specific environmental changes. Finally, we give simple dynamical rules for neural birth and death processes that might underlie this adaptation.
Data availability
All the code necessary to reproduce our results and the figures from the paper is available on GitHub, at https://github.com/ttesileanu/OlfactoryReceptorDistribution. The olfactory receptor affinity data were originally published in Hallem et al. (2006) and Saito et al. (2009), and the olfactory receptor expression levels in mouse were originally published in Ibarra-Soria et al. (2017).
-
Coding of odors by a receptor repertoiredoi:10.1016/j.cell.2006.01.050.
-
Odor Coding by a Mammalian Receptor Repertoiredoi:10.1126/scisignal.2000016.
Article and author information
Author details
Funding
Simons Foundation (400425)
- Vijay Balasubramanian
Aspen Center for Physics (PHY-160761)
- Vijay Balasubramanian
Swartz Foundation
- Tiberiu Tesileanu
National Science Foundation (PHY-1734030)
- Tiberiu Tesileanu
- Vijay Balasubramanian
US-Israel Binational Science Foundation (2011058)
- Vijay Balasubramanian
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Copyright
© 2019, Tesileanu et al.
This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.
Metrics
-
- 4,761
- views
-
- 471
- downloads
-
- 27
- citations
Views, downloads and citations are aggregated across all versions of this paper published by eLife.
Download links
Downloads (link to download the article as PDF)
Open citations (links to open the citations from this article in various online reference manager services)
Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)
Further reading
-
- Cell Biology
- Physics of Living Systems
Cell mechanical properties determine many physiological functions, such as cell fate specification, migration, or circulation through vasculature. Identifying factors that govern the mechanical properties is therefore a subject of great interest. Here, we present a mechanomics approach for establishing links between single-cell mechanical phenotype changes and the genes involved in driving them. We combine mechanical characterization of cells across a variety of mouse and human systems with machine learning-based discriminative network analysis of associated transcriptomic profiles to infer a conserved network module of five genes with putative roles in cell mechanics regulation. We validate in silico that the identified gene markers are universal, trustworthy, and specific to the mechanical phenotype across the studied mouse and human systems, and demonstrate experimentally that a selected target, CAV1, changes the mechanical phenotype of cells accordingly when silenced or overexpressed. Our data-driven approach paves the way toward engineering cell mechanical properties on demand to explore their impact on physiological and pathological cell functions.
-
- Physics of Living Systems
Proteins containing prion-like low complexity domains (PLDs) are common drivers of the formation of biomolecular condensates and are prone to misregulation due to amino acid mutations. Here, we exploit the accuracy of our residue-resolution coarse-grained model, Mpipi, to quantify the impact of amino acid mutations on the stability of 140 PLD mutants from six proteins (hnRNPA1, TDP43, FUS, EWSR1, RBM14, and TIA1). Our simulations reveal the existence of scaling laws that quantify the range of change in the critical solution temperature of PLDs as a function of the number and type of amino acid sequence mutations. These rules are consistent with the physicochemical properties of the mutations and extend across the entire family tested, suggesting that scaling laws can be used as tools to predict changes in the stability of PLD condensates. Our work offers a quantitative lens into how the emergent behavior of PLD solutions vary in response to physicochemical changes of single PLD molecules.