Hair cell identity establishes labeled lines of directional mechanosensation
Directional mechanoreception by hair cells is transmitted to the brain via afferent neurons to enable postural control and rheotaxis. Neuronal tuning to individual directions of mechanical flow occurs when each peripheral axon selectively synapses with multiple hair cells of identical planar polariz...
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| Veröffentlicht in: | PLoS biology 2018-07, Vol.16 (7), p.e2004404-e2004404 |
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| creator | Lozano-Ortega, Marta Valera, Gema Xiao, Yan Faucherre, Adèle López-Schier, Hernán |
| description | Directional mechanoreception by hair cells is transmitted to the brain via afferent neurons to enable postural control and rheotaxis. Neuronal tuning to individual directions of mechanical flow occurs when each peripheral axon selectively synapses with multiple hair cells of identical planar polarization. How such mechanosensory labeled lines are established and maintained remains unsolved. Here, we use the zebrafish lateral line to reveal that asymmetric activity of the transcription factor Emx2 diversifies hair cell identity to instruct polarity-selective synaptogenesis. Unexpectedly, presynaptic scaffolds and coherent hair cell orientation are dispensable for synaptic selectivity, indicating that epithelial planar polarity and synaptic partner matching are separable. Moreover, regenerating axons recapitulate synapses with hair cells according to Emx2 expression but not global orientation. Our results identify a simple cellular algorithm that solves the selectivity task even in the presence of noise generated by the frequent receptor cell turnover. They also suggest that coupling connectivity patterns to cellular identity rather than polarity relaxes developmental and evolutionary constraints to innervation of organs with differing orientation. |
| doi_str_mv | 10.1371/journal.pbio.2004404 |
| format | Article |
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Neuronal tuning to individual directions of mechanical flow occurs when each peripheral axon selectively synapses with multiple hair cells of identical planar polarization. How such mechanosensory labeled lines are established and maintained remains unsolved. Here, we use the zebrafish lateral line to reveal that asymmetric activity of the transcription factor Emx2 diversifies hair cell identity to instruct polarity-selective synaptogenesis. Unexpectedly, presynaptic scaffolds and coherent hair cell orientation are dispensable for synaptic selectivity, indicating that epithelial planar polarity and synaptic partner matching are separable. Moreover, regenerating axons recapitulate synapses with hair cells according to Emx2 expression but not global orientation. Our results identify a simple cellular algorithm that solves the selectivity task even in the presence of noise generated by the frequent receptor cell turnover. 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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>Distributed under a Creative Commons Attribution 4.0 International License</rights><rights>2018 Lozano-Ortega et al 2018 Lozano-Ortega et al</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c780t-a560fadba22bc7e6e77ac3e2e99d2f2a5349a849d05620aecb76290cb3b5358f3</citedby><cites>FETCH-LOGICAL-c780t-a560fadba22bc7e6e77ac3e2e99d2f2a5349a849d05620aecb76290cb3b5358f3</cites><orcidid>0000-0001-7925-7439 ; 0000-0002-6099-3898</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/PMC6067750/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC6067750/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,723,776,780,860,881,2095,2914,23846,27903,27904,53769,53771,79346,79347</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/30024872$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink><backlink>$$Uhttps://hal.science/hal-02990255$$DView record in HAL$$Hfree_for_read</backlink></links><search><contributor>Chitnis, Ajay</contributor><creatorcontrib>Lozano-Ortega, Marta</creatorcontrib><creatorcontrib>Valera, Gema</creatorcontrib><creatorcontrib>Xiao, Yan</creatorcontrib><creatorcontrib>Faucherre, Adèle</creatorcontrib><creatorcontrib>López-Schier, Hernán</creatorcontrib><title>Hair cell identity establishes labeled lines of directional mechanosensation</title><title>PLoS biology</title><addtitle>PLoS Biol</addtitle><description>Directional mechanoreception by hair cells is transmitted to the brain via afferent neurons to enable postural control and rheotaxis. Neuronal tuning to individual directions of mechanical flow occurs when each peripheral axon selectively synapses with multiple hair cells of identical planar polarization. How such mechanosensory labeled lines are established and maintained remains unsolved. Here, we use the zebrafish lateral line to reveal that asymmetric activity of the transcription factor Emx2 diversifies hair cell identity to instruct polarity-selective synaptogenesis. Unexpectedly, presynaptic scaffolds and coherent hair cell orientation are dispensable for synaptic selectivity, indicating that epithelial planar polarity and synaptic partner matching are separable. Moreover, regenerating axons recapitulate synapses with hair cells according to Emx2 expression but not global orientation. Our results identify a simple cellular algorithm that solves the selectivity task even in the presence of noise generated by the frequent receptor cell turnover. They also suggest that coupling connectivity patterns to cellular identity rather than polarity relaxes developmental and evolutionary constraints to innervation of organs with differing orientation.</description><subject>Axons</subject><subject>Biology</subject><subject>Biology and Life Sciences</subject><subject>Brain</subject><subject>Fish</subject><subject>Hair</subject><subject>Hair cells</subject><subject>Hair cells (Mechanoreceptors)</subject><subject>Hearing protection</subject><subject>Innervation</subject><subject>Lateral line</subject><subject>Life Sciences</subject><subject>Mechanoreceptors</subject><subject>Mechanotransduction</subject><subject>Medicine and Health Sciences</subject><subject>Neural networks</subject><subject>Neurobiology</subject><subject>Neurons</subject><subject>Neurons and Cognition</subject><subject>Organs</subject><subject>Orientation</subject><subject>Physiological aspects</subject><subject>Polarity</subject><subject>Posture</subject><subject>Research 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biology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Lozano-Ortega, Marta</au><au>Valera, Gema</au><au>Xiao, Yan</au><au>Faucherre, Adèle</au><au>López-Schier, Hernán</au><au>Chitnis, Ajay</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Hair cell identity establishes labeled lines of directional mechanosensation</atitle><jtitle>PLoS biology</jtitle><addtitle>PLoS Biol</addtitle><date>2018-07-19</date><risdate>2018</risdate><volume>16</volume><issue>7</issue><spage>e2004404</spage><epage>e2004404</epage><pages>e2004404-e2004404</pages><issn>1545-7885</issn><issn>1544-9173</issn><eissn>1545-7885</eissn><abstract>Directional mechanoreception by hair cells is transmitted to the brain via afferent neurons to enable postural control and rheotaxis. Neuronal tuning to individual directions of mechanical flow occurs when each peripheral axon selectively synapses with multiple hair cells of identical planar polarization. How such mechanosensory labeled lines are established and maintained remains unsolved. Here, we use the zebrafish lateral line to reveal that asymmetric activity of the transcription factor Emx2 diversifies hair cell identity to instruct polarity-selective synaptogenesis. Unexpectedly, presynaptic scaffolds and coherent hair cell orientation are dispensable for synaptic selectivity, indicating that epithelial planar polarity and synaptic partner matching are separable. Moreover, regenerating axons recapitulate synapses with hair cells according to Emx2 expression but not global orientation. Our results identify a simple cellular algorithm that solves the selectivity task even in the presence of noise generated by the frequent receptor cell turnover. They also suggest that coupling connectivity patterns to cellular identity rather than polarity relaxes developmental and evolutionary constraints to innervation of organs with differing orientation.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>30024872</pmid><doi>10.1371/journal.pbio.2004404</doi><orcidid>https://orcid.org/0000-0001-7925-7439</orcidid><orcidid>https://orcid.org/0000-0002-6099-3898</orcidid><oa>free_for_read</oa></addata></record> |
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| subjects | Axons Biology Biology and Life Sciences Brain Fish Hair Hair cells Hair cells (Mechanoreceptors) Hearing protection Innervation Lateral line Life Sciences Mechanoreceptors Mechanotransduction Medicine and Health Sciences Neural networks Neurobiology Neurons Neurons and Cognition Organs Orientation Physiological aspects Polarity Posture Research and Analysis Methods Rheotaxis Selectivity Senses Sensory neurons Synapses Synaptogenesis Zebrafish |
| title | Hair cell identity establishes labeled lines of directional mechanosensation |
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