Chemotaxis Behavior Mediated by Single Larval Olfactory Neurons in Drosophila
Odorant receptors (ORs) are thought to act in a combinatorial fashion, in which odor identity is encoded by the activation of a subset of ORs and the olfactory sensory neurons (OSNs) that express them. The extent to which a single OR contributes to chemotaxis behavior is not known. We investigated t...
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| Veröffentlicht in: | Current biology 2005-12, Vol.15 (23), p.2086-2096 |
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| creator | Fishilevich, Elane Domingos, Ana I. Asahina, Kenta Naef, Félix Vosshall, Leslie B. Louis, Matthieu |
| description | Odorant receptors (ORs) are thought to act in a combinatorial fashion, in which odor identity is encoded by the activation of a subset of ORs and the olfactory sensory neurons (OSNs) that express them. The extent to which a single OR contributes to chemotaxis behavior is not known. We investigated this question in
Drosophila larvae, which represent a powerful genetic system to analyze the contribution of individual OSNs to odor coding.
We identify 25 larval
OR genes expressed in 21 OSNs and generate genetic tools that allow us to engineer larvae missing a single OSN or having only a single or a pair of functional OSNs. Ablation of single OSNs disrupts chemotaxis behavior to a small subset of the odors tested. Larvae with only a single functional OSN are able to chemotax robustly, demonstrating that chemotaxis is possible in the absence of the remaining elements of the combinatorial code. We provide behavioral evidence that an OSN not sufficient to support chemotaxis behavior alone can act in a combinatorial fashion to enhance chemotaxis along with a second OSN.
We conclude that there is extensive functional redundancy in the olfactory system, such that a given OSN is necessary and sufficient for the perception of only a subset of odors. This study is the first behavioral demonstration that formation of olfactory percepts involves the combinatorial integration of information transmitted by multiple ORs. |
| doi_str_mv | 10.1016/j.cub.2005.11.016 |
| format | Article |
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Drosophila larvae, which represent a powerful genetic system to analyze the contribution of individual OSNs to odor coding.
We identify 25 larval
OR genes expressed in 21 OSNs and generate genetic tools that allow us to engineer larvae missing a single OSN or having only a single or a pair of functional OSNs. Ablation of single OSNs disrupts chemotaxis behavior to a small subset of the odors tested. Larvae with only a single functional OSN are able to chemotax robustly, demonstrating that chemotaxis is possible in the absence of the remaining elements of the combinatorial code. We provide behavioral evidence that an OSN not sufficient to support chemotaxis behavior alone can act in a combinatorial fashion to enhance chemotaxis along with a second OSN.
We conclude that there is extensive functional redundancy in the olfactory system, such that a given OSN is necessary and sufficient for the perception of only a subset of odors. This study is the first behavioral demonstration that formation of olfactory percepts involves the combinatorial integration of information transmitted by multiple ORs.</description><identifier>ISSN: 0960-9822</identifier><identifier>EISSN: 1879-0445</identifier><identifier>DOI: 10.1016/j.cub.2005.11.016</identifier><identifier>PMID: 16332533</identifier><language>eng</language><publisher>England: Elsevier Inc</publisher><subject>Animals ; Chemotaxis - physiology ; Drosophila ; Drosophila - physiology ; Fluorescent Antibody Technique ; Ganglia, Invertebrate - cytology ; Ganglia, Invertebrate - metabolism ; Gene Expression ; Green Fluorescent Proteins - metabolism ; In Situ Hybridization ; Larva - physiology ; Larva - ultrastructure ; Microscopy, Electron ; Odorants ; Olfactory Receptor Neurons - cytology ; Olfactory Receptor Neurons - metabolism ; Olfactory Receptor Neurons - physiology ; Promoter Regions, Genetic - genetics ; Receptors, Odorant - genetics ; Regression Analysis ; Transgenes - genetics</subject><ispartof>Current biology, 2005-12, Vol.15 (23), p.2086-2096</ispartof><rights>2005 Elsevier Ltd</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c491t-893db72fe050c5503790998a1725efe502c3ef181cdbab19dbad3ed94827d2133</citedby><cites>FETCH-LOGICAL-c491t-893db72fe050c5503790998a1725efe502c3ef181cdbab19dbad3ed94827d2133</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktohtml>$$Uhttps://dx.doi.org/10.1016/j.cub.2005.11.016$$EHTML$$P50$$Gelsevier$$Hfree_for_read</linktohtml><link.rule.ids>314,780,784,3548,27923,27924,45994</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/16332533$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Fishilevich, Elane</creatorcontrib><creatorcontrib>Domingos, Ana I.</creatorcontrib><creatorcontrib>Asahina, Kenta</creatorcontrib><creatorcontrib>Naef, Félix</creatorcontrib><creatorcontrib>Vosshall, Leslie B.</creatorcontrib><creatorcontrib>Louis, Matthieu</creatorcontrib><title>Chemotaxis Behavior Mediated by Single Larval Olfactory Neurons in Drosophila</title><title>Current biology</title><addtitle>Curr Biol</addtitle><description>Odorant receptors (ORs) are thought to act in a combinatorial fashion, in which odor identity is encoded by the activation of a subset of ORs and the olfactory sensory neurons (OSNs) that express them. The extent to which a single OR contributes to chemotaxis behavior is not known. We investigated this question in
Drosophila larvae, which represent a powerful genetic system to analyze the contribution of individual OSNs to odor coding.
We identify 25 larval
OR genes expressed in 21 OSNs and generate genetic tools that allow us to engineer larvae missing a single OSN or having only a single or a pair of functional OSNs. Ablation of single OSNs disrupts chemotaxis behavior to a small subset of the odors tested. Larvae with only a single functional OSN are able to chemotax robustly, demonstrating that chemotaxis is possible in the absence of the remaining elements of the combinatorial code. We provide behavioral evidence that an OSN not sufficient to support chemotaxis behavior alone can act in a combinatorial fashion to enhance chemotaxis along with a second OSN.
We conclude that there is extensive functional redundancy in the olfactory system, such that a given OSN is necessary and sufficient for the perception of only a subset of odors. This study is the first behavioral demonstration that formation of olfactory percepts involves the combinatorial integration of information transmitted by multiple ORs.</description><subject>Animals</subject><subject>Chemotaxis - physiology</subject><subject>Drosophila</subject><subject>Drosophila - physiology</subject><subject>Fluorescent Antibody Technique</subject><subject>Ganglia, Invertebrate - cytology</subject><subject>Ganglia, Invertebrate - metabolism</subject><subject>Gene Expression</subject><subject>Green Fluorescent Proteins - metabolism</subject><subject>In Situ Hybridization</subject><subject>Larva - physiology</subject><subject>Larva - ultrastructure</subject><subject>Microscopy, Electron</subject><subject>Odorants</subject><subject>Olfactory Receptor Neurons - cytology</subject><subject>Olfactory Receptor Neurons - metabolism</subject><subject>Olfactory Receptor Neurons - physiology</subject><subject>Promoter Regions, Genetic - genetics</subject><subject>Receptors, Odorant - genetics</subject><subject>Regression Analysis</subject><subject>Transgenes - genetics</subject><issn>0960-9822</issn><issn>1879-0445</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2005</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqFkE1vEzEQhi1ERUPhB3BBPnHbrceOd21xgpSPSik9AGfLa88SR5t1sHej5t_jKpG4tZcZafS8rzQPIe-A1cCgud7Wbu5qzpisAepyeUEWoFpdseVSviQLphtWacX5JXmd85Yx4Eo3r8glNEJwKcSC3K02uIuTfQiZfsaNPYSY6B36YCf0tDvSn2H8MyBd23SwA70feuummI70B84pjpmGkd6kmON-Ewb7hlz0dsj49ryvyO-vX36tvlfr-2-3q0_ryi01TJXSwnct75FJ5qRkotVMa2Wh5RJ7lIw7gT0ocL6zHegyvUCvl4q3noMQV-TDqXef4t8Z82R2ITscBjtinLNplGqbhqtnQc6UkLxtCwgn0JVncsLe7FPY2XQ0wMyjbLM1RbZ5lG0ATLmUzPtz-dzt0P9PnO0W4OMJwOLiEDCZ7AKOruhN6CbjY3ii_h_imo75</recordid><startdate>20051206</startdate><enddate>20051206</enddate><creator>Fishilevich, Elane</creator><creator>Domingos, Ana I.</creator><creator>Asahina, Kenta</creator><creator>Naef, Félix</creator><creator>Vosshall, Leslie B.</creator><creator>Louis, Matthieu</creator><general>Elsevier Inc</general><scope>6I.</scope><scope>AAFTH</scope><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7QG</scope><scope>7QR</scope><scope>7SS</scope><scope>7TK</scope><scope>8FD</scope><scope>FR3</scope><scope>P64</scope><scope>RC3</scope><scope>7X8</scope></search><sort><creationdate>20051206</creationdate><title>Chemotaxis Behavior Mediated by Single Larval Olfactory Neurons in Drosophila</title><author>Fishilevich, Elane ; Domingos, Ana I. ; Asahina, Kenta ; Naef, Félix ; Vosshall, Leslie B. ; Louis, Matthieu</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c491t-893db72fe050c5503790998a1725efe502c3ef181cdbab19dbad3ed94827d2133</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2005</creationdate><topic>Animals</topic><topic>Chemotaxis - physiology</topic><topic>Drosophila</topic><topic>Drosophila - physiology</topic><topic>Fluorescent Antibody Technique</topic><topic>Ganglia, Invertebrate - cytology</topic><topic>Ganglia, Invertebrate - metabolism</topic><topic>Gene Expression</topic><topic>Green Fluorescent Proteins - metabolism</topic><topic>In Situ Hybridization</topic><topic>Larva - physiology</topic><topic>Larva - ultrastructure</topic><topic>Microscopy, Electron</topic><topic>Odorants</topic><topic>Olfactory Receptor Neurons - cytology</topic><topic>Olfactory Receptor Neurons - metabolism</topic><topic>Olfactory Receptor Neurons - physiology</topic><topic>Promoter Regions, Genetic - genetics</topic><topic>Receptors, Odorant - genetics</topic><topic>Regression Analysis</topic><topic>Transgenes - genetics</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Fishilevich, Elane</creatorcontrib><creatorcontrib>Domingos, Ana I.</creatorcontrib><creatorcontrib>Asahina, Kenta</creatorcontrib><creatorcontrib>Naef, Félix</creatorcontrib><creatorcontrib>Vosshall, Leslie B.</creatorcontrib><creatorcontrib>Louis, Matthieu</creatorcontrib><collection>ScienceDirect Open Access Titles</collection><collection>Elsevier:ScienceDirect:Open Access</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Animal Behavior Abstracts</collection><collection>Chemoreception Abstracts</collection><collection>Entomology Abstracts (Full archive)</collection><collection>Neurosciences Abstracts</collection><collection>Technology Research Database</collection><collection>Engineering Research Database</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><jtitle>Current biology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Fishilevich, Elane</au><au>Domingos, Ana I.</au><au>Asahina, Kenta</au><au>Naef, Félix</au><au>Vosshall, Leslie B.</au><au>Louis, Matthieu</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Chemotaxis Behavior Mediated by Single Larval Olfactory Neurons in Drosophila</atitle><jtitle>Current biology</jtitle><addtitle>Curr Biol</addtitle><date>2005-12-06</date><risdate>2005</risdate><volume>15</volume><issue>23</issue><spage>2086</spage><epage>2096</epage><pages>2086-2096</pages><issn>0960-9822</issn><eissn>1879-0445</eissn><abstract>Odorant receptors (ORs) are thought to act in a combinatorial fashion, in which odor identity is encoded by the activation of a subset of ORs and the olfactory sensory neurons (OSNs) that express them. The extent to which a single OR contributes to chemotaxis behavior is not known. We investigated this question in
Drosophila larvae, which represent a powerful genetic system to analyze the contribution of individual OSNs to odor coding.
We identify 25 larval
OR genes expressed in 21 OSNs and generate genetic tools that allow us to engineer larvae missing a single OSN or having only a single or a pair of functional OSNs. Ablation of single OSNs disrupts chemotaxis behavior to a small subset of the odors tested. Larvae with only a single functional OSN are able to chemotax robustly, demonstrating that chemotaxis is possible in the absence of the remaining elements of the combinatorial code. We provide behavioral evidence that an OSN not sufficient to support chemotaxis behavior alone can act in a combinatorial fashion to enhance chemotaxis along with a second OSN.
We conclude that there is extensive functional redundancy in the olfactory system, such that a given OSN is necessary and sufficient for the perception of only a subset of odors. This study is the first behavioral demonstration that formation of olfactory percepts involves the combinatorial integration of information transmitted by multiple ORs.</abstract><cop>England</cop><pub>Elsevier Inc</pub><pmid>16332533</pmid><doi>10.1016/j.cub.2005.11.016</doi><tpages>11</tpages><oa>free_for_read</oa></addata></record> |
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| source | MEDLINE; Cell Press Free Archives; ScienceDirect Journals (5 years ago - present); EZB-FREE-00999 freely available EZB journals |
| subjects | Animals Chemotaxis - physiology Drosophila Drosophila - physiology Fluorescent Antibody Technique Ganglia, Invertebrate - cytology Ganglia, Invertebrate - metabolism Gene Expression Green Fluorescent Proteins - metabolism In Situ Hybridization Larva - physiology Larva - ultrastructure Microscopy, Electron Odorants Olfactory Receptor Neurons - cytology Olfactory Receptor Neurons - metabolism Olfactory Receptor Neurons - physiology Promoter Regions, Genetic - genetics Receptors, Odorant - genetics Regression Analysis Transgenes - genetics |
| title | Chemotaxis Behavior Mediated by Single Larval Olfactory Neurons in Drosophila |
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