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Fold-change detection and scalar symmetry of sensory input fields

Shoval, Oren and Goentoro, Lea and Hart, Yuval and Mayo, Avi and Sontag, Eduardo and Alon, Uri (2010) Fold-change detection and scalar symmetry of sensory input fields. Proceedings of the National Academy of Sciences of the United States of America, 107 (36). pp. 15995-16000. ISSN 1091-6490. PMCID PMC2936624. http://resolver.caltech.edu/CaltechAUTHORS:20150616-090521744

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Abstract

Recent studies suggest that certain cellular sensory systems display fold-change detection (FCD): a response whose entire shape, including amplitude and duration, depends only on fold changes in input and not on absolute levels. Thus, a step change in input from, for example, level 1 to 2 gives precisely the same dynamical output as a step from level 2 to 4, because the steps have the same fold change. We ask what the benefit of FCD is and show that FCD is necessary and sufficient for sensory search to be independent of multiplying the input field by a scalar. Thus, the FCD search pattern depends only on the spatial profile of the input and not on its amplitude. Such scalar symmetry occurs in a wide range of sensory inputs, such as source strength multiplying diffusing/convecting chemical fields sensed in chemotaxis, ambient light multiplying the contrast field in vision, and protein concentrations multiplying the output in cellular signaling systems. Furthermore, we show that FCD entails two features found across sensory systems, exact adaptation and Weber's law, but that these two features are not sufficient for FCD. Finally, we present a wide class of mechanisms that have FCD, including certain nonlinear feedback and feed-forward loops. We find that bacterial chemotaxis displays feedback within the present class and hence, is expected to show FCD. This can explain experiments in which chemotaxis searches are insensitive to attractant source levels. This study, thus, suggests a connection between properties of biological sensory systems and scalar symmetry stemming from physical properties of their input fields.


Item Type:Article
Related URLs:
URLURL TypeDescription
http://dx.doi.org/10.1073/pnas.1002352107DOIArticle
http://www.pnas.org/content/107/36/15995.longPublisherArticle
http://www.pnas.org/lookup/suppl/doi:10.1073/pnas.1002352107/-/DCSupplementalPublisherSupporting Material
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC2936624/PubMed CentralArticle
ORCID:
AuthorORCID
Goentoro, Lea0000-0002-3904-0195
Additional Information:© 2010 National Academy of Sciences. Freely available online through the PNAS open access option. Edited by Curtis G. Callan, Princeton University, Princeton, NJ, and approved July 2, 2010 (received for review February 26, 2010). Published online before print August 20, 2010, doi: 10.1073/pnas.1002352107. We thank M. Kirschner, J. J. E. Slotine, H. Berg, Y. Tu, and T. Shimizu for useful discussions. O.S. is grateful to the Azrieli Foundation for the award of an Azrieli Fellowship. O.S. and U.A. thank the Department of Systems Biology at Harvard Medical School for hospitality. L.G. is a Robert Black Fellow of the Damon Runyon Foundation (DRG-1958-07). This work was supported by the US National Institutes of Health (E.S.), the Air Force Office of Scientific Research (E.S.), the Kahn Family Foundation (U.A.), and the Israel Science Foundation (U.A.). Author contributions: O.S., L.G., Y.H., A.M., E.S., and U.A. designed research, performed research, contributed analytic tools, analyzed data, and wrote the paper. The authors declare no conflict of interest. This article is a PNAS Direct Submission. This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1002352107/-/DCSupplemental.
Funders:
Funding AgencyGrant Number
Azrieli FoundationUNSPECIFIED
Damon Runyon Cancer Research FoundationDRG-1958-07
NIHUNSPECIFIED
Air Force Office of Scientific Research (AFOSR)UNSPECIFIED
Kahn Family FoundationUNSPECIFIED
Israel Science FoundationUNSPECIFIED
Subject Keywords:adaptation; sensory response; spatial search
PubMed Central ID:PMC2936624
Record Number:CaltechAUTHORS:20150616-090521744
Persistent URL:http://resolver.caltech.edu/CaltechAUTHORS:20150616-090521744
Official Citation:Oren Shoval, Lea Goentoro, Yuval Hart, Avi Mayo, Eduardo Sontag, and Uri Alon Fold-change detection and scalar symmetry of sensory input fields PNAS 2010 107 (36) 15995-16000; published ahead of print August 20, 2010, doi:10.1073/pnas.1002352107
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:58274
Collection:CaltechAUTHORS
Deposited By: George Porter
Deposited On:16 Jun 2015 16:18
Last Modified:24 Feb 2016 02:52

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