Tight temporal coupling between synaptic rewiring of olfactory glomeruli and the emergence of odor‐guided behavior in Xenopus tadpoles
Olfactory sensory neurons (OSNs) are chemoreceptors that establish excitatory synapses within glomeruli of the olfactory bulb. OSNs undergo continuous turnover throughout life, causing the constant replacement of their synaptic contacts. Using Xenopus tadpoles as an experimental system to investigat...
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| Veröffentlicht in: | Journal of comparative neurology (1911) 2017-12, Vol.525 (17), p.3769-3783 |
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| creator | Terni, Beatrice Pacciolla, Paolo Masanas, Helena Gorostiza, Pau Llobet, Artur |
| description | Olfactory sensory neurons (OSNs) are chemoreceptors that establish excitatory synapses within glomeruli of the olfactory bulb. OSNs undergo continuous turnover throughout life, causing the constant replacement of their synaptic contacts. Using Xenopus tadpoles as an experimental system to investigate rewiring of glomerular connectivity, we show that novel OSN synapses can transfer information immediately after formation, mediating olfactory‐guided behavior. Tadpoles recover the ability to detect amino acids 4 days after bilateral olfactory nerve transection. Restoration of olfactory‐guided behavior depends on the efficient reinsertion of OSNs to the olfactory bulb. Presynaptic terminals of incipient synaptic contacts generate calcium transients in response to odors, triggering long lasting depolarization of olfactory glomeruli. The functionality of reconnected terminals relies on well‐defined readily releasable and cytoplasmic vesicle pools. The continuous growth of non‐compartmentalized axonal processes provides a vesicle reservoir to nascent release sites, which contrasts to the gradual development of cytoplasmic vesicle pools in conventional excitatory synapses. The immediate availability of fully functional synapses upon formation supports an age‐independent contribution of OSNs to the generation of odor maps.
Olfactory sensory neurons are chemoreceptors that establish excitatory synapses within glomeruli of the olfactory bulb and undergo continuous turnover throughout life. In Xenopus tadpoles novel olfactory sensory neuron synapses contain well‐structured synaptic vesicle pools that allow the transfer information immediately after formation, mediating an olfactory‐guided behavior. |
| doi_str_mv | 10.1002/cne.24303 |
| format | Article |
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Olfactory sensory neurons are chemoreceptors that establish excitatory synapses within glomeruli of the olfactory bulb and undergo continuous turnover throughout life. In Xenopus tadpoles novel olfactory sensory neuron synapses contain well‐structured synaptic vesicle pools that allow the transfer information immediately after formation, mediating an olfactory‐guided behavior.</description><identifier>ISSN: 0021-9967</identifier><identifier>EISSN: 1096-9861</identifier><identifier>DOI: 10.1002/cne.24303</identifier><identifier>PMID: 28815589</identifier><language>eng</language><publisher>United States: Wiley Subscription Services, Inc</publisher><subject>Age ; Age Factors ; Amino Acids - metabolism ; Animals ; Animals, Genetically Modified ; Calcium ; Chemoreceptors ; Depolarization ; Electrophysiology ; Evoked Potentials - physiology ; Fisiologia ; Green Fluorescent Proteins - genetics ; Green Fluorescent Proteins - metabolism ; Larva ; Metabolism ; Metabolisme ; Microscopy, Electron ; Neural networks ; Odor ; Odorants ; Olfacte ; Olfactory bulb ; Olfactory Bulb - metabolism ; Olfactory glomeruli ; Olfactory nerve ; Olfactory Nerve Injuries - physiopathology ; Olfactory pathways ; Olfactory receptor neurons ; Olfactory Receptor Neurons - physiology ; Olfactory Receptor Neurons - ultrastructure ; Physiology ; presynaptic terminals ; Recovery of Function - physiology ; RRID: AB‐221570 ; RRID: AB‐887824 ; RRID:SCR_007164 ; RRID:SCR_013731 ; Sensory evaluation ; Sensory neurons ; Sinapsi ; Smell ; Swimming - physiology ; Synapses ; Synapses - metabolism ; Synapses - ultrastructure ; synaptic vesicles ; Synaptogenesis ; Synaptophysin - metabolism ; Time Factors ; Tubulin - genetics ; Tubulin - metabolism ; Xenopus ; Xenopus laevis - physiology</subject><ispartof>Journal of comparative neurology (1911), 2017-12, Vol.525 (17), p.3769-3783</ispartof><rights>2017 Wiley Periodicals, Inc.</rights><rights>(c) Wiley, 2017 info:eu-repo/semantics/openAccess</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c4303-9c0030031ed598edba911d6ca38756908e30b6a47d1f51cef22271c79b30ea943</citedby><cites>FETCH-LOGICAL-c4303-9c0030031ed598edba911d6ca38756908e30b6a47d1f51cef22271c79b30ea943</cites><orcidid>0000-0002-7268-5577 ; 0000-0001-5797-6782</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://onlinelibrary.wiley.com/doi/pdf/10.1002%2Fcne.24303$$EPDF$$P50$$Gwiley$$H</linktopdf><linktohtml>$$Uhttps://onlinelibrary.wiley.com/doi/full/10.1002%2Fcne.24303$$EHTML$$P50$$Gwiley$$H</linktohtml><link.rule.ids>230,314,780,784,885,1417,26974,27924,27925,45574,45575</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/28815589$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Terni, Beatrice</creatorcontrib><creatorcontrib>Pacciolla, Paolo</creatorcontrib><creatorcontrib>Masanas, Helena</creatorcontrib><creatorcontrib>Gorostiza, Pau</creatorcontrib><creatorcontrib>Llobet, Artur</creatorcontrib><title>Tight temporal coupling between synaptic rewiring of olfactory glomeruli and the emergence of odor‐guided behavior in Xenopus tadpoles</title><title>Journal of comparative neurology (1911)</title><addtitle>J Comp Neurol</addtitle><description>Olfactory sensory neurons (OSNs) are chemoreceptors that establish excitatory synapses within glomeruli of the olfactory bulb. OSNs undergo continuous turnover throughout life, causing the constant replacement of their synaptic contacts. Using Xenopus tadpoles as an experimental system to investigate rewiring of glomerular connectivity, we show that novel OSN synapses can transfer information immediately after formation, mediating olfactory‐guided behavior. Tadpoles recover the ability to detect amino acids 4 days after bilateral olfactory nerve transection. Restoration of olfactory‐guided behavior depends on the efficient reinsertion of OSNs to the olfactory bulb. Presynaptic terminals of incipient synaptic contacts generate calcium transients in response to odors, triggering long lasting depolarization of olfactory glomeruli. The functionality of reconnected terminals relies on well‐defined readily releasable and cytoplasmic vesicle pools. The continuous growth of non‐compartmentalized axonal processes provides a vesicle reservoir to nascent release sites, which contrasts to the gradual development of cytoplasmic vesicle pools in conventional excitatory synapses. The immediate availability of fully functional synapses upon formation supports an age‐independent contribution of OSNs to the generation of odor maps.
Olfactory sensory neurons are chemoreceptors that establish excitatory synapses within glomeruli of the olfactory bulb and undergo continuous turnover throughout life. In Xenopus tadpoles novel olfactory sensory neuron synapses contain well‐structured synaptic vesicle pools that allow the transfer information immediately after formation, mediating an olfactory‐guided behavior.</description><subject>Age</subject><subject>Age Factors</subject><subject>Amino Acids - metabolism</subject><subject>Animals</subject><subject>Animals, Genetically Modified</subject><subject>Calcium</subject><subject>Chemoreceptors</subject><subject>Depolarization</subject><subject>Electrophysiology</subject><subject>Evoked Potentials - physiology</subject><subject>Fisiologia</subject><subject>Green Fluorescent Proteins - genetics</subject><subject>Green Fluorescent Proteins - metabolism</subject><subject>Larva</subject><subject>Metabolism</subject><subject>Metabolisme</subject><subject>Microscopy, Electron</subject><subject>Neural networks</subject><subject>Odor</subject><subject>Odorants</subject><subject>Olfacte</subject><subject>Olfactory bulb</subject><subject>Olfactory Bulb - metabolism</subject><subject>Olfactory glomeruli</subject><subject>Olfactory nerve</subject><subject>Olfactory Nerve Injuries - physiopathology</subject><subject>Olfactory pathways</subject><subject>Olfactory receptor neurons</subject><subject>Olfactory Receptor Neurons - physiology</subject><subject>Olfactory Receptor Neurons - ultrastructure</subject><subject>Physiology</subject><subject>presynaptic terminals</subject><subject>Recovery of Function - physiology</subject><subject>RRID: AB‐221570</subject><subject>RRID: AB‐887824</subject><subject>RRID:SCR_007164</subject><subject>RRID:SCR_013731</subject><subject>Sensory evaluation</subject><subject>Sensory neurons</subject><subject>Sinapsi</subject><subject>Smell</subject><subject>Swimming - physiology</subject><subject>Synapses</subject><subject>Synapses - metabolism</subject><subject>Synapses - ultrastructure</subject><subject>synaptic vesicles</subject><subject>Synaptogenesis</subject><subject>Synaptophysin - metabolism</subject><subject>Time Factors</subject><subject>Tubulin - genetics</subject><subject>Tubulin - metabolism</subject><subject>Xenopus</subject><subject>Xenopus laevis - physiology</subject><issn>0021-9967</issn><issn>1096-9861</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2017</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>XX2</sourceid><recordid>eNp1kU2LFDEQhoO4uLOrB_-ABLzooXeTTn_lKMP6Act6WcFbSCfVPVnSSZukd5ibR4_-Rn_JZnZGBUGoUBT11EtVXoReUnJBCSkvlYOLsmKEPUErSnhT8K6hT9Eq92jBedOeorMY7wghnLPuGTotu47WdcdX6MetGTcJJ5hmH6TFyi-zNW7EPaQtgMNx5-ScjMIBtibsO37A3g5SJR92eLR-grBYg6XTOG0AQ65HcAoeQe3Dr-8_x8Vo0FlzI--ND9g4_BWcn5eIk9SztxCfo5NB2ggvjvkcfXl_dbv-WFx__vBp_e66UPsDC64IYTko6Jp3oHvJKdWNkqxr64aTDhjpG1m1mg41VTCUZdlS1fKeEZC8YueIHnRVXJQIoCAomYSX5m-xfyVpS8GatqE0z7w5zMzBf1sgJjGZqMBa6cAvUVDOSJW_vGQZff0PeueX4PJFmarqirW0qzP19rhE8DEGGMQczCTDTlAi9paKbKl4tDSzr46KSz-B_kP-9jADlwdgayzs_q8k1jdXB8kHcKas0w</recordid><startdate>20171201</startdate><enddate>20171201</enddate><creator>Terni, Beatrice</creator><creator>Pacciolla, Paolo</creator><creator>Masanas, Helena</creator><creator>Gorostiza, Pau</creator><creator>Llobet, Artur</creator><general>Wiley Subscription Services, Inc</general><general>Wiley</general><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>7QR</scope><scope>7TK</scope><scope>8FD</scope><scope>FR3</scope><scope>K9.</scope><scope>P64</scope><scope>7X8</scope><scope>XX2</scope><orcidid>https://orcid.org/0000-0002-7268-5577</orcidid><orcidid>https://orcid.org/0000-0001-5797-6782</orcidid></search><sort><creationdate>20171201</creationdate><title>Tight temporal coupling between synaptic rewiring of olfactory glomeruli and the emergence of odor‐guided behavior in Xenopus tadpoles</title><author>Terni, Beatrice ; Pacciolla, Paolo ; Masanas, Helena ; Gorostiza, Pau ; Llobet, Artur</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c4303-9c0030031ed598edba911d6ca38756908e30b6a47d1f51cef22271c79b30ea943</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2017</creationdate><topic>Age</topic><topic>Age Factors</topic><topic>Amino Acids - metabolism</topic><topic>Animals</topic><topic>Animals, Genetically Modified</topic><topic>Calcium</topic><topic>Chemoreceptors</topic><topic>Depolarization</topic><topic>Electrophysiology</topic><topic>Evoked Potentials - physiology</topic><topic>Fisiologia</topic><topic>Green Fluorescent Proteins - genetics</topic><topic>Green Fluorescent Proteins - metabolism</topic><topic>Larva</topic><topic>Metabolism</topic><topic>Metabolisme</topic><topic>Microscopy, Electron</topic><topic>Neural networks</topic><topic>Odor</topic><topic>Odorants</topic><topic>Olfacte</topic><topic>Olfactory bulb</topic><topic>Olfactory Bulb - metabolism</topic><topic>Olfactory glomeruli</topic><topic>Olfactory nerve</topic><topic>Olfactory Nerve Injuries - physiopathology</topic><topic>Olfactory pathways</topic><topic>Olfactory receptor neurons</topic><topic>Olfactory Receptor Neurons - physiology</topic><topic>Olfactory Receptor Neurons - ultrastructure</topic><topic>Physiology</topic><topic>presynaptic terminals</topic><topic>Recovery of Function - physiology</topic><topic>RRID: AB‐221570</topic><topic>RRID: AB‐887824</topic><topic>RRID:SCR_007164</topic><topic>RRID:SCR_013731</topic><topic>Sensory evaluation</topic><topic>Sensory neurons</topic><topic>Sinapsi</topic><topic>Smell</topic><topic>Swimming - physiology</topic><topic>Synapses</topic><topic>Synapses - metabolism</topic><topic>Synapses - ultrastructure</topic><topic>synaptic vesicles</topic><topic>Synaptogenesis</topic><topic>Synaptophysin - metabolism</topic><topic>Time Factors</topic><topic>Tubulin - genetics</topic><topic>Tubulin - metabolism</topic><topic>Xenopus</topic><topic>Xenopus laevis - physiology</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Terni, Beatrice</creatorcontrib><creatorcontrib>Pacciolla, Paolo</creatorcontrib><creatorcontrib>Masanas, Helena</creatorcontrib><creatorcontrib>Gorostiza, Pau</creatorcontrib><creatorcontrib>Llobet, Artur</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Chemoreception Abstracts</collection><collection>Neurosciences Abstracts</collection><collection>Technology Research Database</collection><collection>Engineering Research Database</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>MEDLINE - Academic</collection><collection>Recercat</collection><jtitle>Journal of comparative neurology (1911)</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Terni, Beatrice</au><au>Pacciolla, Paolo</au><au>Masanas, Helena</au><au>Gorostiza, Pau</au><au>Llobet, Artur</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Tight temporal coupling between synaptic rewiring of olfactory glomeruli and the emergence of odor‐guided behavior in Xenopus tadpoles</atitle><jtitle>Journal of comparative neurology (1911)</jtitle><addtitle>J Comp Neurol</addtitle><date>2017-12-01</date><risdate>2017</risdate><volume>525</volume><issue>17</issue><spage>3769</spage><epage>3783</epage><pages>3769-3783</pages><issn>0021-9967</issn><eissn>1096-9861</eissn><abstract>Olfactory sensory neurons (OSNs) are chemoreceptors that establish excitatory synapses within glomeruli of the olfactory bulb. OSNs undergo continuous turnover throughout life, causing the constant replacement of their synaptic contacts. Using Xenopus tadpoles as an experimental system to investigate rewiring of glomerular connectivity, we show that novel OSN synapses can transfer information immediately after formation, mediating olfactory‐guided behavior. Tadpoles recover the ability to detect amino acids 4 days after bilateral olfactory nerve transection. Restoration of olfactory‐guided behavior depends on the efficient reinsertion of OSNs to the olfactory bulb. Presynaptic terminals of incipient synaptic contacts generate calcium transients in response to odors, triggering long lasting depolarization of olfactory glomeruli. The functionality of reconnected terminals relies on well‐defined readily releasable and cytoplasmic vesicle pools. The continuous growth of non‐compartmentalized axonal processes provides a vesicle reservoir to nascent release sites, which contrasts to the gradual development of cytoplasmic vesicle pools in conventional excitatory synapses. The immediate availability of fully functional synapses upon formation supports an age‐independent contribution of OSNs to the generation of odor maps.
Olfactory sensory neurons are chemoreceptors that establish excitatory synapses within glomeruli of the olfactory bulb and undergo continuous turnover throughout life. In Xenopus tadpoles novel olfactory sensory neuron synapses contain well‐structured synaptic vesicle pools that allow the transfer information immediately after formation, mediating an olfactory‐guided behavior.</abstract><cop>United States</cop><pub>Wiley Subscription Services, Inc</pub><pmid>28815589</pmid><doi>10.1002/cne.24303</doi><tpages>17</tpages><orcidid>https://orcid.org/0000-0002-7268-5577</orcidid><orcidid>https://orcid.org/0000-0001-5797-6782</orcidid><oa>free_for_read</oa></addata></record> |
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| subjects | Age Age Factors Amino Acids - metabolism Animals Animals, Genetically Modified Calcium Chemoreceptors Depolarization Electrophysiology Evoked Potentials - physiology Fisiologia Green Fluorescent Proteins - genetics Green Fluorescent Proteins - metabolism Larva Metabolism Metabolisme Microscopy, Electron Neural networks Odor Odorants Olfacte Olfactory bulb Olfactory Bulb - metabolism Olfactory glomeruli Olfactory nerve Olfactory Nerve Injuries - physiopathology Olfactory pathways Olfactory receptor neurons Olfactory Receptor Neurons - physiology Olfactory Receptor Neurons - ultrastructure Physiology presynaptic terminals Recovery of Function - physiology RRID: AB‐221570 RRID: AB‐887824 RRID:SCR_007164 RRID:SCR_013731 Sensory evaluation Sensory neurons Sinapsi Smell Swimming - physiology Synapses Synapses - metabolism Synapses - ultrastructure synaptic vesicles Synaptogenesis Synaptophysin - metabolism Time Factors Tubulin - genetics Tubulin - metabolism Xenopus Xenopus laevis - physiology |
| title | Tight temporal coupling between synaptic rewiring of olfactory glomeruli and the emergence of odor‐guided behavior in Xenopus tadpoles |
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