{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,2,27]],"date-time":"2026-02-27T06:15:25Z","timestamp":1772172925200,"version":"3.50.1"},"update-to":[{"DOI":"10.1371\/journal.pcbi.1009054","type":"new_version","label":"New version","source":"publisher","updated":{"date-parts":[[2021,6,23]],"date-time":"2021-06-23T00:00:00Z","timestamp":1624406400000}}],"reference-count":94,"publisher":"Public Library of Science (PLoS)","issue":"6","license":[{"start":{"date-parts":[[2021,6,11]],"date-time":"2021-06-11T00:00:00Z","timestamp":1623369600000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/100000055","name":"National Institute on Deafness and Other Communication Disorders","doi-asserted-by":"publisher","award":["R01 DC014701"],"award-info":[{"award-number":["R01 DC014701"]}],"id":[{"id":"10.13039\/100000055","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000055","name":"National Institute on Deafness and Other Communication Disorders","doi-asserted-by":"publisher","award":["R01 DC014701"],"award-info":[{"award-number":["R01 DC014701"]}],"id":[{"id":"10.13039\/100000055","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["www.ploscompbiol.org"],"crossmark-restriction":false},"short-container-title":["PLoS Comput Biol"],"abstract":"<jats:p>We present a general physicochemical sampling model for olfaction, based on established pharmacological laws, in which arbitrary combinations of odorant ligands and receptors can be generated and their individual and collective effects on odor representations and olfactory performance measured. Individual odor ligands exhibit receptor-specific affinities and efficacies; that is, they may bind strongly or weakly to a given receptor, and can act as strong agonists, weak agonists, partial agonists, or antagonists. Ligands interacting with common receptors compete with one another for dwell time; these competitive interactions appropriately simulate the degeneracy that fundamentally defines the capacities and limitations of odorant sampling. The outcome of these competing ligand-receptor interactions yields a pattern of receptor activation levels, thereafter mapped to glomerular presynaptic activation levels based on the convergence of sensory neuron axons. The metric of greatest interest is the mean discrimination sensitivity, a measure of how effectively the olfactory system at this level is able to recognize a small change in the physicochemical quality of a stimulus. This model presents several significant outcomes, both expected and surprising. First, adding additional receptors reliably improves the system\u2019s discrimination sensitivity. Second, in contrast, adding additional ligands to an odorscene initially can improve discrimination sensitivity, but eventually will reduce it as the number of ligands increases. Third, the presence of antagonistic ligand-receptor interactions produced clear benefits for sensory system performance, generating higher absolute discrimination sensitivities and increasing the numbers of competing ligands that could be present before discrimination sensitivity began to be impaired. Finally, the model correctly reflects and explains the modest reduction in odor discrimination sensitivity exhibited by transgenic mice in which the specificity of glomerular targeting by primary olfactory neurons is partially disrupted.<\/jats:p>","DOI":"10.1371\/journal.pcbi.1009054","type":"journal-article","created":{"date-parts":[[2021,6,11]],"date-time":"2021-06-11T13:40:22Z","timestamp":1623418822000},"page":"e1009054","update-policy":"https:\/\/doi.org\/10.1371\/journal.pcbi.corrections_policy","source":"Crossref","is-referenced-by-count":12,"title":["A physicochemical model of odor sampling"],"prefix":"10.1371","volume":"17","author":[{"given":"Mitchell E.","family":"Gronowitz","sequence":"first","affiliation":[]},{"ORCID":"https:\/\/orcid.org\/0000-0003-1963-4612","authenticated-orcid":true,"given":"Adam","family":"Liu","sequence":"additional","affiliation":[]},{"ORCID":"https:\/\/orcid.org\/0000-0002-7280-1005","authenticated-orcid":true,"given":"Qiang","family":"Qiu","sequence":"additional","affiliation":[]},{"ORCID":"https:\/\/orcid.org\/0000-0003-1555-8683","authenticated-orcid":true,"given":"C. Ron","family":"Yu","sequence":"additional","affiliation":[]},{"ORCID":"https:\/\/orcid.org\/0000-0001-7506-1201","authenticated-orcid":true,"given":"Thomas A.","family":"Cleland","sequence":"additional","affiliation":[]}],"member":"340","published-online":{"date-parts":[[2021,6,11]]},"reference":[{"issue":"2","key":"pcbi.1009054.ref001","doi-asserted-by":"crossref","first-page":"222","DOI":"10.1037\/0735-7044.116.2.222","article-title":"Behavioral models of odor similarity","volume":"116","author":"TA Cleland","year":"2002","journal-title":"Behav Neurosci"},{"issue":"3","key":"pcbi.1009054.ref002","doi-asserted-by":"crossref","first-page":"497","DOI":"10.1016\/S0031-9384(98)00324-2","article-title":"Behavioral responses to aliphatic aldehydes can be predicted from known electrophysiological responses of mitral cells in the olfactory bulb","volume":"66","author":"C Linster","year":"1999","journal-title":"Physiol 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Sci"},{"issue":"4146","key":"pcbi.1009054.ref024","doi-asserted-by":"crossref","first-page":"112","DOI":"10.1126\/science.185.4146.112","article-title":"Physicochemical correlates of olfactory quality","volume":"185","author":"SS Schiffman","year":"1974","journal-title":"Science"},{"issue":"5","key":"pcbi.1009054.ref025","doi-asserted-by":"crossref","first-page":"425","DOI":"10.1038\/nmeth.1197","article-title":"A metric for odorant comparison","volume":"5","author":"R Haddad","year":"2008","journal-title":"Nat Methods"},{"issue":"14","key":"pcbi.1009054.ref026","doi-asserted-by":"crossref","first-page":"5481","DOI":"10.1073\/pnas.1117491109","article-title":"Distributed representation of chemical features and tunotopic organization of glomeruli in the mouse olfactory bulb","volume":"109","author":"L Ma","year":"2012","journal-title":"Proc Natl Acad Sci U S 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Liu","year":"2020","journal-title":"Chemistry"},{"issue":"60","key":"pcbi.1009054.ref030","doi-asserted-by":"crossref","first-page":"ra9","DOI":"10.1126\/scisignal.2000016","article-title":"Odor coding by a mammalian receptor repertoire","volume":"2","author":"H Saito","year":"2009","journal-title":"Sci Signal"},{"issue":"19","key":"pcbi.1009054.ref031","doi-asserted-by":"crossref","first-page":"9598","DOI":"10.1073\/pnas.1813230116","article-title":"Competitive binding predicts nonlinear responses of olfactory receptors to complex mixtures","volume":"116","author":"V Singh","year":"2019","journal-title":"Proc Natl Acad Sci U S A"},{"issue":"12","key":"pcbi.1009054.ref032","doi-asserted-by":"crossref","first-page":"1248","DOI":"10.1038\/81774","article-title":"The molecular receptive range of an odorant receptor","volume":"3","author":"RC Araneda","year":"2000","journal-title":"Nat Neurosci"},{"issue":"Pt 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Kurahashi","year":"1994","journal-title":"Science"},{"issue":"10","key":"pcbi.1009054.ref036","doi-asserted-by":"crossref","first-page":"2659","DOI":"10.1523\/JNEUROSCI.4670-07.2008","article-title":"Competitive and noncompetitive odorant interactions in the early neural coding of odorant mixtures","volume":"28","author":"JP Rospars","year":"2008","journal-title":"J Neurosci"},{"key":"pcbi.1009054.ref037","doi-asserted-by":"crossref","first-page":"103469","DOI":"10.1016\/j.mcn.2020.103469","article-title":"Modulation of the combinatorial code of odorant receptor response patterns in odorant mixtures","volume":"104","author":"CA de March","year":"2020","journal-title":"Mol Cell Neurosci"},{"issue":"13","key":"pcbi.1009054.ref038","doi-asserted-by":"crossref","first-page":"107814","DOI":"10.1016\/j.celrep.2020.107814","article-title":"Widespread inhibition, antagonism, and synergy in mouse olfactory sensory neurons in vivo","volume":"31","author":"S Inagaki","year":"2020","journal-title":"Cell Rep."},{"issue":"13","key":"pcbi.1009054.ref039","doi-asserted-by":"crossref","first-page":"2574","DOI":"10.1016\/j.cub.2020.04.086","article-title":"Odorant receptor inhibition is fundamental to odor encoding","volume":"30","author":"P Pfister","year":"2020","journal-title":"Curr Biol"},{"key":"pcbi.1009054.ref040","first-page":"7","article-title":"Antagonism in olfactory receptor neurons and its implications for the perception of odor mixtures","author":"G Reddy","year":"2018","journal-title":"Elife"},{"issue":"6487","key":"pcbi.1009054.ref041","article-title":"Widespread receptor-driven modulation in peripheral olfactory coding","volume":"368","author":"L Xu","year":"2020","journal-title":"Science"},{"issue":"1","key":"pcbi.1009054.ref042","doi-asserted-by":"crossref","first-page":"3350","DOI":"10.1038\/s41467-020-17124-5","article-title":"Antagonistic odor interactions in olfactory sensory neurons are widespread in freely breathing mice","volume":"11","author":"JD Zak","year":"2020","journal-title":"Nat Commun."},{"issue":"9","key":"pcbi.1009054.ref043","doi-asserted-by":"crossref","first-page":"815","DOI":"10.1093\/chemse\/bjh247","article-title":"An odorant derivative as an antagonist for an olfactory receptor","volume":"29","author":"Y Oka","year":"2004","journal-title":"Chem Senses"},{"issue":"1","key":"pcbi.1009054.ref044","doi-asserted-by":"crossref","first-page":"120","DOI":"10.1038\/sj.emboj.7600032","article-title":"Olfactory receptor antagonism between odorants","volume":"23","author":"Y Oka","year":"2004","journal-title":"EMBO J"},{"issue":"49","key":"pcbi.1009054.ref045","doi-asserted-by":"crossref","first-page":"19959","DOI":"10.1073\/pnas.1208110109","article-title":"Perceptual convergence of multi-component mixtures in olfaction implies an olfactory white","volume":"109","author":"T Weiss","year":"2012","journal-title":"Proc Natl Acad Sci U S 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Physiol"},{"issue":"7","key":"pcbi.1009054.ref056","doi-asserted-by":"crossref","first-page":"1673","DOI":"10.1162\/089976699300016188","article-title":"Concentration tuning mediated by spare receptor capacity in olfactory sensory neurons: A theoretical study","volume":"11","author":"TA Cleland","year":"1999","journal-title":"Neural Comput"},{"issue":"5","key":"pcbi.1009054.ref057","doi-asserted-by":"crossref","first-page":"737","DOI":"10.1016\/S0896-6273(00)80314-1","article-title":"Combinatorial and chemotopic odorant coding in the zebrafish olfactory bulb visualized by optical imaging","volume":"18","author":"RW Friedrich","year":"1997","journal-title":"Neuron"},{"issue":"4","key":"pcbi.1009054.ref058","doi-asserted-by":"crossref","first-page":"1351","DOI":"10.1523\/JNEUROSCI.21-04-01351.2001","article-title":"Tuning and topography in an odor map on the rat olfactory bulb","volume":"21","author":"M Meister","year":"2001","journal-title":"J 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stimuli on the orientation selectivity of cells in primary visual cortex of the cat","volume":"30","author":"CD Gilbert","year":"1990","journal-title":"Vision Res"},{"issue":"22","key":"pcbi.1009054.ref063","doi-asserted-by":"crossref","first-page":"10749","DOI":"10.1073\/pnas.90.22.10749","article-title":"Simple models for reading neuronal population codes","volume":"90","author":"HS Seung","year":"1993","journal-title":"Proc Natl Acad Sci U S A"},{"issue":"3","key":"pcbi.1009054.ref064","doi-asserted-by":"crossref","first-page":"265","DOI":"10.1007\/BF00198480","article-title":"Population coding of visual stimuli by cortical neurons tuned to more than one dimension","volume":"66","author":"E Zohary","year":"1992","journal-title":"Biological Cybernetics"},{"key":"pcbi.1009054.ref065","doi-asserted-by":"crossref","first-page":"459","DOI":"10.1088\/0959-5309\/46\/3\/317","article-title":"Hue-discrimination in normal colour-vision","volume":"46","author":"WD Wright","year":"1934","journal-title":"Proceedings of the Physical Society"},{"issue":"2","key":"pcbi.1009054.ref066","doi-asserted-by":"crossref","first-page":"129","DOI":"10.1364\/JOSA.48.000129","article-title":"Wavelength discrimination for point sources","volume":"48","author":"RE Bedford","year":"1958","journal-title":"J Opt Soc Am"},{"key":"pcbi.1009054.ref067","doi-asserted-by":"crossref","first-page":"3","DOI":"10.1088\/0031-9155\/6\/1\/201","article-title":"Colour discrimination","volume":"6","author":"J Birch","year":"1961","journal-title":"Physics in Medicine and Biology"},{"issue":"43","key":"pcbi.1009054.ref068","doi-asserted-by":"crossref","first-page":"13454","DOI":"10.1523\/JNEUROSCI.2368-09.2009","article-title":"Control of on\/off glomerular signaling by a local gabaergic microcircuit in the olfactory bulb","volume":"29","author":"DH Gire","year":"2009","journal-title":"J 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