Primacy coding facilitates effective odor discrimination when receptor sensitivities are tuned
The olfactory system faces the difficult task of identifying an enormous variety of odors independent of their intensity. Primacy coding, where the odor identity is encoded by the receptor types that respond earliest, might provide a compact and informative representation that can be interpreted eff...
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description | The olfactory system faces the difficult task of identifying an enormous variety of odors independent of their intensity. Primacy coding, where the odor identity is encoded by the receptor types that respond earliest, might provide a compact and informative representation that can be interpreted efficiently by the brain. In this paper, we analyze the information transmitted by a simple model of primacy coding using numerical simulations and statistical descriptions. We show that the encoded information depends strongly on the number of receptor types included in the primacy representation, but only weakly on the size of the receptor repertoire. The representation is independent of the odor intensity and the transmitted information is useful to perform typical olfactory tasks with close to experimentally measured performance. Interestingly, we find situations in which a smaller receptor repertoire is advantageous for discriminating odors. The model also suggests that overly sensitive receptor types could dominate the entire response and make the whole array useless, which allows us to predict how receptor arrays need to adapt to stay useful during environmental changes. Taken together, we show that primacy coding is more useful than simple binary and normalized coding, essentially because the sparsity of the odor representations is independent of the odor statistics, in contrast to the alternatives. Primacy coding thus provides an efficient odor representation that is independent of the odor intensity and might thus help to identify odors in the olfactory cortex. |
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Primacy coding, where the odor identity is encoded by the receptor types that respond earliest, might provide a compact and informative representation that can be interpreted efficiently by the brain. In this paper, we analyze the information transmitted by a simple model of primacy coding using numerical simulations and statistical descriptions. We show that the encoded information depends strongly on the number of receptor types included in the primacy representation, but only weakly on the size of the receptor repertoire. The representation is independent of the odor intensity and the transmitted information is useful to perform typical olfactory tasks with close to experimentally measured performance. Interestingly, we find situations in which a smaller receptor repertoire is advantageous for discriminating odors. The model also suggests that overly sensitive receptor types could dominate the entire response and make the whole array useless, which allows us to predict how receptor arrays need to adapt to stay useful during environmental changes. Taken together, we show that primacy coding is more useful than simple binary and normalized coding, essentially because the sparsity of the odor representations is independent of the odor statistics, in contrast to the alternatives. Primacy coding thus provides an efficient odor representation that is independent of the odor intensity and might thus help to identify odors in the olfactory cortex.</description><identifier>ISSN: 1553-7358</identifier><identifier>ISSN: 1553-734X</identifier><identifier>EISSN: 1553-7358</identifier><identifier>DOI: 10.1371/journal.pcbi.1007188</identifier><identifier>PMID: 31323033</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Animals ; Arrays ; Binary codes ; Biology and Life Sciences ; Brain ; Coding ; Computational Biology ; Computer Simulation ; Cortex (olfactory) ; Environmental changes ; Experiments ; Humans ; Information management ; Ligands ; Mammals ; Mathematical models ; Medicine and Health Sciences ; Models, Neurological ; Neural coding ; Neurons ; Numerical analysis ; Odor intensity ; Odorant receptors ; Odorants ; Odors ; Olfactory Bulb - physiology ; Olfactory discrimination ; Olfactory discrimination learning ; Olfactory Pathways - physiology ; Olfactory Perception - physiology ; Olfactory Receptor Neurons - physiology ; Olfactory receptors ; Olfactory system ; Physical Sciences ; Physiological aspects ; Receptors, Odorant - physiology ; Representations ; Smell ; Smell - physiology ; Social Sciences</subject><ispartof>PLoS computational biology, 2019-07, Vol.15 (7), p.e1007188-e1007188</ispartof><rights>COPYRIGHT 2019 Public Library of Science</rights><rights>2019 David Zwicker. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><rights>2019 David Zwicker 2019 David Zwicker</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c633t-b78ddb8baf6350e8afcef8e6331bd29774b6c45e8353932a7f710e49ed8727de3</citedby><cites>FETCH-LOGICAL-c633t-b78ddb8baf6350e8afcef8e6331bd29774b6c45e8353932a7f710e49ed8727de3</cites><orcidid>0000-0002-3909-3334</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC6692051/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC6692051/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,723,776,780,860,881,2096,2915,23847,27903,27904,53769,53771,79346,79347</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/31323033$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>Latham, Peter E.</contributor><creatorcontrib>Zwicker, David</creatorcontrib><title>Primacy coding facilitates effective odor discrimination when receptor sensitivities are tuned</title><title>PLoS computational biology</title><addtitle>PLoS Comput Biol</addtitle><description>The olfactory system faces the difficult task of identifying an enormous variety of odors independent of their intensity. Primacy coding, where the odor identity is encoded by the receptor types that respond earliest, might provide a compact and informative representation that can be interpreted efficiently by the brain. In this paper, we analyze the information transmitted by a simple model of primacy coding using numerical simulations and statistical descriptions. We show that the encoded information depends strongly on the number of receptor types included in the primacy representation, but only weakly on the size of the receptor repertoire. The representation is independent of the odor intensity and the transmitted information is useful to perform typical olfactory tasks with close to experimentally measured performance. Interestingly, we find situations in which a smaller receptor repertoire is advantageous for discriminating odors. The model also suggests that overly sensitive receptor types could dominate the entire response and make the whole array useless, which allows us to predict how receptor arrays need to adapt to stay useful during environmental changes. Taken together, we show that primacy coding is more useful than simple binary and normalized coding, essentially because the sparsity of the odor representations is independent of the odor statistics, in contrast to the alternatives. Primacy coding thus provides an efficient odor representation that is independent of the odor intensity and might thus help to identify odors in the olfactory cortex.</description><subject>Animals</subject><subject>Arrays</subject><subject>Binary codes</subject><subject>Biology and Life Sciences</subject><subject>Brain</subject><subject>Coding</subject><subject>Computational Biology</subject><subject>Computer Simulation</subject><subject>Cortex (olfactory)</subject><subject>Environmental changes</subject><subject>Experiments</subject><subject>Humans</subject><subject>Information management</subject><subject>Ligands</subject><subject>Mammals</subject><subject>Mathematical models</subject><subject>Medicine and Health Sciences</subject><subject>Models, Neurological</subject><subject>Neural coding</subject><subject>Neurons</subject><subject>Numerical analysis</subject><subject>Odor intensity</subject><subject>Odorant receptors</subject><subject>Odorants</subject><subject>Odors</subject><subject>Olfactory Bulb - 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physiology</topic><topic>Olfactory discrimination</topic><topic>Olfactory discrimination learning</topic><topic>Olfactory Pathways - physiology</topic><topic>Olfactory Perception - physiology</topic><topic>Olfactory Receptor Neurons - physiology</topic><topic>Olfactory receptors</topic><topic>Olfactory system</topic><topic>Physical Sciences</topic><topic>Physiological aspects</topic><topic>Receptors, Odorant - physiology</topic><topic>Representations</topic><topic>Smell</topic><topic>Smell - physiology</topic><topic>Social Sciences</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Zwicker, David</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Gale In Context: Canada</collection><collection>Gale In Context: Science</collection><collection>ProQuest Central (Corporate)</collection><collection>Biotechnology Research Abstracts</collection><collection>Calcium & Calcified Tissue Abstracts</collection><collection>Neurosciences Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>Health & Medical Collection</collection><collection>ProQuest Central (purchase pre-March 2016)</collection><collection>Medical Database (Alumni Edition)</collection><collection>Computing Database (Alumni Edition)</collection><collection>Technology Research Database</collection><collection>ProQuest SciTech Collection</collection><collection>ProQuest Technology Collection</collection><collection>ProQuest Natural Science Collection</collection><collection>Hospital Premium Collection</collection><collection>Hospital Premium Collection (Alumni Edition)</collection><collection>ProQuest Central (Alumni) (purchase pre-March 2016)</collection><collection>ProQuest Central (Alumni Edition)</collection><collection>ProQuest One Sustainability</collection><collection>ProQuest Central UK/Ireland</collection><collection>Advanced Technologies & Aerospace Collection</collection><collection>ProQuest Central Essentials</collection><collection>Biological Science Collection</collection><collection>ProQuest Central</collection><collection>Technology Collection</collection><collection>Natural Science Collection</collection><collection>ProQuest One Community College</collection><collection>ProQuest Central Korea</collection><collection>Engineering Research Database</collection><collection>Health Research Premium Collection</collection><collection>Health Research Premium Collection (Alumni)</collection><collection>ProQuest Central Student</collection><collection>SciTech Premium Collection</collection><collection>ProQuest Computer Science Collection</collection><collection>Computer Science Database</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>ProQuest Biological Science Collection</collection><collection>Computing Database</collection><collection>Health & Medical Collection (Alumni Edition)</collection><collection>Medical Database</collection><collection>Biological Science Database</collection><collection>Advanced Technologies & Aerospace Database</collection><collection>ProQuest Advanced Technologies & Aerospace Collection</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Publicly Available Content Database</collection><collection>ProQuest One Academic Eastern Edition (DO NOT USE)</collection><collection>ProQuest One Academic</collection><collection>ProQuest One Academic UKI Edition</collection><collection>ProQuest Central Basic</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><collection>DOAJ Directory of Open Access Journals</collection><jtitle>PLoS computational biology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Zwicker, David</au><au>Latham, Peter E.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Primacy coding facilitates effective odor discrimination when receptor sensitivities are tuned</atitle><jtitle>PLoS computational biology</jtitle><addtitle>PLoS Comput Biol</addtitle><date>2019-07-01</date><risdate>2019</risdate><volume>15</volume><issue>7</issue><spage>e1007188</spage><epage>e1007188</epage><pages>e1007188-e1007188</pages><issn>1553-7358</issn><issn>1553-734X</issn><eissn>1553-7358</eissn><abstract>The olfactory system faces the difficult task of identifying an enormous variety of odors independent of their intensity. Primacy coding, where the odor identity is encoded by the receptor types that respond earliest, might provide a compact and informative representation that can be interpreted efficiently by the brain. In this paper, we analyze the information transmitted by a simple model of primacy coding using numerical simulations and statistical descriptions. We show that the encoded information depends strongly on the number of receptor types included in the primacy representation, but only weakly on the size of the receptor repertoire. The representation is independent of the odor intensity and the transmitted information is useful to perform typical olfactory tasks with close to experimentally measured performance. Interestingly, we find situations in which a smaller receptor repertoire is advantageous for discriminating odors. The model also suggests that overly sensitive receptor types could dominate the entire response and make the whole array useless, which allows us to predict how receptor arrays need to adapt to stay useful during environmental changes. Taken together, we show that primacy coding is more useful than simple binary and normalized coding, essentially because the sparsity of the odor representations is independent of the odor statistics, in contrast to the alternatives. Primacy coding thus provides an efficient odor representation that is independent of the odor intensity and might thus help to identify odors in the olfactory cortex.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>31323033</pmid><doi>10.1371/journal.pcbi.1007188</doi><orcidid>https://orcid.org/0000-0002-3909-3334</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Animals Arrays Binary codes Biology and Life Sciences Brain Coding Computational Biology Computer Simulation Cortex (olfactory) Environmental changes Experiments Humans Information management Ligands Mammals Mathematical models Medicine and Health Sciences Models, Neurological Neural coding Neurons Numerical analysis Odor intensity Odorant receptors Odorants Odors Olfactory Bulb - physiology Olfactory discrimination Olfactory discrimination learning Olfactory Pathways - physiology Olfactory Perception - physiology Olfactory Receptor Neurons - physiology Olfactory receptors Olfactory system Physical Sciences Physiological aspects Receptors, Odorant - physiology Representations Smell Smell - physiology Social Sciences |
title | Primacy coding facilitates effective odor discrimination when receptor sensitivities are tuned |
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