Gain modulation and odor concentration invariance in early olfactory networks
The broad receptive field of the olfactory receptors constitutes the basis of a combinatorial code that allows animals to detect and discriminate many more odorants than the actual number of receptor types that they express. One drawback is that high odor concentrations recruit lower affinity recept...
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description | The broad receptive field of the olfactory receptors constitutes the basis of a combinatorial code that allows animals to detect and discriminate many more odorants than the actual number of receptor types that they express. One drawback is that high odor concentrations recruit lower affinity receptors which can lead to the perception of qualitatively different odors. Here we addressed the contribution that signal-processing in the antennal lobe makes to reduce concentration dependence in odor representation. By means of calcium imaging and pharmacological approach we describe the contribution that GABA receptors play in terms of the amplitude and temporal profiles of the signals that convey odor information from the antennal lobes to higher brain centers. We found that GABA reduces the amplitude of odor elicited signals and the number of glomeruli that are recruited in an odor-concentration-dependent manner. Blocking GABA receptors decreases the correlation among glomerular activity patterns elicited by different concentrations of the same odor. In addition, we built a realistic mathematical model of the antennal lobe that was used to test the viability of the proposed mechanisms and to evaluate the processing properties of the AL network under conditions that cannot be achieved in physiology experiments. Interestingly, even though based on a rather simple topology and cell interactions solely mediated by GABAergic lateral inhibitions, the AL model reproduced key features of the AL response upon different odor concentrations and provides plausible solutions for concentration invariant recognition of odors by artificial sensors. |
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One drawback is that high odor concentrations recruit lower affinity receptors which can lead to the perception of qualitatively different odors. Here we addressed the contribution that signal-processing in the antennal lobe makes to reduce concentration dependence in odor representation. By means of calcium imaging and pharmacological approach we describe the contribution that GABA receptors play in terms of the amplitude and temporal profiles of the signals that convey odor information from the antennal lobes to higher brain centers. We found that GABA reduces the amplitude of odor elicited signals and the number of glomeruli that are recruited in an odor-concentration-dependent manner. Blocking GABA receptors decreases the correlation among glomerular activity patterns elicited by different concentrations of the same odor. In addition, we built a realistic mathematical model of the antennal lobe that was used to test the viability of the proposed mechanisms and to evaluate the processing properties of the AL network under conditions that cannot be achieved in physiology experiments. Interestingly, even though based on a rather simple topology and cell interactions solely mediated by GABAergic lateral inhibitions, the AL model reproduced key features of the AL response upon different odor concentrations and provides plausible solutions for concentration invariant recognition of odors by artificial sensors.</description><identifier>ISSN: 1553-7358</identifier><identifier>ISSN: 1553-734X</identifier><identifier>EISSN: 1553-7358</identifier><identifier>DOI: 10.1371/journal.pcbi.1011176</identifier><identifier>PMID: 37343029</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Activity patterns ; Amplitudes ; Animals ; Antennal lobe ; Bees ; Biology and Life Sciences ; Calcium imaging ; Cell interactions ; Combinatorial analysis ; GABA ; Mathematical models ; Network topologies ; Neuroimaging ; Neurons ; Odorant receptors ; Odorants ; Odors ; Olfactory Pathways - physiology ; Olfactory Receptor Neurons - physiology ; Physical Sciences ; Physiology ; Receptive field ; Receptors ; Receptors, GABA ; Receptors, Odorant - metabolism ; Signal processing ; Smell - physiology ; Social Sciences ; Topology ; γ-Aminobutyric acid ; γ-Aminobutyric acid receptors</subject><ispartof>PLoS computational biology, 2023-06, Vol.19 (6), p.e1011176-e1011176</ispartof><rights>Copyright: © 2023 Marachlian et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.</rights><rights>COPYRIGHT 2023 Public Library of Science</rights><rights>2023 Marachlian et al. 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>2023 Marachlian et al 2023 Marachlian et al</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><cites>FETCH-LOGICAL-c611t-9606a5e779efae7db84c29e38f7b368eca4654f425cfabcec77c2abf30c858033</cites><orcidid>0000-0001-9826-5696 ; 0000-0002-8415-8264</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/PMC10317235/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC10317235/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,727,780,784,864,885,2100,2926,23864,27922,27923,53789,53791,79370,79371</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/37343029$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>van Vugt, Marieke Karlijn</contributor><creatorcontrib>Marachlian, Emiliano</creatorcontrib><creatorcontrib>Huerta, Ramón</creatorcontrib><creatorcontrib>Locatelli, Fernando F</creatorcontrib><title>Gain modulation and odor concentration invariance in early olfactory networks</title><title>PLoS computational biology</title><addtitle>PLoS Comput Biol</addtitle><description>The broad receptive field of the olfactory receptors constitutes the basis of a combinatorial code that allows animals to detect and discriminate many more odorants than the actual number of receptor types that they express. One drawback is that high odor concentrations recruit lower affinity receptors which can lead to the perception of qualitatively different odors. Here we addressed the contribution that signal-processing in the antennal lobe makes to reduce concentration dependence in odor representation. By means of calcium imaging and pharmacological approach we describe the contribution that GABA receptors play in terms of the amplitude and temporal profiles of the signals that convey odor information from the antennal lobes to higher brain centers. We found that GABA reduces the amplitude of odor elicited signals and the number of glomeruli that are recruited in an odor-concentration-dependent manner. Blocking GABA receptors decreases the correlation among glomerular activity patterns elicited by different concentrations of the same odor. In addition, we built a realistic mathematical model of the antennal lobe that was used to test the viability of the proposed mechanisms and to evaluate the processing properties of the AL network under conditions that cannot be achieved in physiology experiments. Interestingly, even though based on a rather simple topology and cell interactions solely mediated by GABAergic lateral inhibitions, the AL model reproduced key features of the AL response upon different odor concentrations and provides plausible solutions for concentration invariant recognition of odors by artificial sensors.</description><subject>Activity patterns</subject><subject>Amplitudes</subject><subject>Animals</subject><subject>Antennal lobe</subject><subject>Bees</subject><subject>Biology and Life Sciences</subject><subject>Calcium imaging</subject><subject>Cell interactions</subject><subject>Combinatorial analysis</subject><subject>GABA</subject><subject>Mathematical models</subject><subject>Network topologies</subject><subject>Neuroimaging</subject><subject>Neurons</subject><subject>Odorant receptors</subject><subject>Odorants</subject><subject>Odors</subject><subject>Olfactory Pathways - physiology</subject><subject>Olfactory Receptor Neurons - physiology</subject><subject>Physical Sciences</subject><subject>Physiology</subject><subject>Receptive field</subject><subject>Receptors</subject><subject>Receptors, GABA</subject><subject>Receptors, Odorant - 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physiology</topic><topic>Olfactory Receptor Neurons - physiology</topic><topic>Physical Sciences</topic><topic>Physiology</topic><topic>Receptive field</topic><topic>Receptors</topic><topic>Receptors, GABA</topic><topic>Receptors, Odorant - metabolism</topic><topic>Signal processing</topic><topic>Smell - physiology</topic><topic>Social Sciences</topic><topic>Topology</topic><topic>γ-Aminobutyric acid</topic><topic>γ-Aminobutyric acid receptors</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Marachlian, Emiliano</creatorcontrib><creatorcontrib>Huerta, Ramón</creatorcontrib><creatorcontrib>Locatelli, Fernando F</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 (ProQuest)</collection><collection>Natural Science Collection (ProQuest)</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 China</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>Marachlian, Emiliano</au><au>Huerta, Ramón</au><au>Locatelli, Fernando F</au><au>van Vugt, Marieke Karlijn</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Gain modulation and odor concentration invariance in early olfactory networks</atitle><jtitle>PLoS computational biology</jtitle><addtitle>PLoS Comput Biol</addtitle><date>2023-06-01</date><risdate>2023</risdate><volume>19</volume><issue>6</issue><spage>e1011176</spage><epage>e1011176</epage><pages>e1011176-e1011176</pages><issn>1553-7358</issn><issn>1553-734X</issn><eissn>1553-7358</eissn><abstract>The broad receptive field of the olfactory receptors constitutes the basis of a combinatorial code that allows animals to detect and discriminate many more odorants than the actual number of receptor types that they express. One drawback is that high odor concentrations recruit lower affinity receptors which can lead to the perception of qualitatively different odors. Here we addressed the contribution that signal-processing in the antennal lobe makes to reduce concentration dependence in odor representation. By means of calcium imaging and pharmacological approach we describe the contribution that GABA receptors play in terms of the amplitude and temporal profiles of the signals that convey odor information from the antennal lobes to higher brain centers. We found that GABA reduces the amplitude of odor elicited signals and the number of glomeruli that are recruited in an odor-concentration-dependent manner. Blocking GABA receptors decreases the correlation among glomerular activity patterns elicited by different concentrations of the same odor. In addition, we built a realistic mathematical model of the antennal lobe that was used to test the viability of the proposed mechanisms and to evaluate the processing properties of the AL network under conditions that cannot be achieved in physiology experiments. Interestingly, even though based on a rather simple topology and cell interactions solely mediated by GABAergic lateral inhibitions, the AL model reproduced key features of the AL response upon different odor concentrations and provides plausible solutions for concentration invariant recognition of odors by artificial sensors.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>37343029</pmid><doi>10.1371/journal.pcbi.1011176</doi><tpages>e1011176</tpages><orcidid>https://orcid.org/0000-0001-9826-5696</orcidid><orcidid>https://orcid.org/0000-0002-8415-8264</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Activity patterns Amplitudes Animals Antennal lobe Bees Biology and Life Sciences Calcium imaging Cell interactions Combinatorial analysis GABA Mathematical models Network topologies Neuroimaging Neurons Odorant receptors Odorants Odors Olfactory Pathways - physiology Olfactory Receptor Neurons - physiology Physical Sciences Physiology Receptive field Receptors Receptors, GABA Receptors, Odorant - metabolism Signal processing Smell - physiology Social Sciences Topology γ-Aminobutyric acid γ-Aminobutyric acid receptors |
title | Gain modulation and odor concentration invariance in early olfactory networks |
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