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Brainstem control of vocalization and its coordination with respiration
Phonation critically depends on precise controls of laryngeal muscles in coordination with ongoing respiration. However, the neural mechanisms governing these processes remain unclear. We identified excitatory vocalization-specific laryngeal premotor neurons located in the retroambiguus nucleus (RAm...
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| Published in: | Science (American Association for the Advancement of Science) 2024-03, Vol.383 (6687), p.eadi8081-eadi8081 |
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| container_end_page | eadi8081 |
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| container_title | Science (American Association for the Advancement of Science) |
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| creator | Park, Jaehong Choi, Seonmi Takatoh, Jun Zhao, Shengli Harrahill, Andrew Han, Bao-Xia Wang, Fan |
| description | Phonation critically depends on precise controls of laryngeal muscles in coordination with ongoing respiration. However, the neural mechanisms governing these processes remain unclear. We identified excitatory vocalization-specific laryngeal premotor neurons located in the retroambiguus nucleus (RAm
) in adult mice as being both necessary and sufficient for driving vocal cord closure and eliciting mouse ultrasonic vocalizations (USVs). The duration of RAm
activation can determine the lengths of both USV syllables and concurrent expiration periods, with the impact of RAm
activation depending on respiration phases. RAm
neurons receive inhibition from the preBötzinger complex, and inspiration needs override RAm
-mediated vocal cord closure. Ablating inhibitory synapses in RAm
neurons compromised this inspiration gating of laryngeal adduction, resulting in discoordination of vocalization with respiration. Our study reveals the circuits for vocal production and vocal-respiratory coordination. |
| doi_str_mv | 10.1126/science.adi8081 |
| format | article |
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) in adult mice as being both necessary and sufficient for driving vocal cord closure and eliciting mouse ultrasonic vocalizations (USVs). The duration of RAm
activation can determine the lengths of both USV syllables and concurrent expiration periods, with the impact of RAm
activation depending on respiration phases. RAm
neurons receive inhibition from the preBötzinger complex, and inspiration needs override RAm
-mediated vocal cord closure. Ablating inhibitory synapses in RAm
neurons compromised this inspiration gating of laryngeal adduction, resulting in discoordination of vocalization with respiration. Our study reveals the circuits for vocal production and vocal-respiratory coordination.</description><identifier>ISSN: 0036-8075</identifier><identifier>ISSN: 1095-9203</identifier><identifier>EISSN: 1095-9203</identifier><identifier>DOI: 10.1126/science.adi8081</identifier><identifier>PMID: 38452069</identifier><language>eng</language><publisher>United States: The American Association for the Advancement of Science</publisher><subject>Ablation ; Animals ; Brain Stem ; Breathing ; Coordination ; Courtship ; Expiration ; Fear of Success ; Gating ; Heterogeneity ; Hindbrain ; Inhalation ; Inspiration ; Larynx ; Lyssavirus ; Male ; Medulla Oblongata - physiology ; Mesencephalon ; Mice ; Motor neurons ; Muscle function ; Muscles ; Neurogenesis ; Neurons ; Neurons - physiology ; Nodes ; Periaqueductal gray area ; Phonation ; Rabies ; Respiration ; Rhythms ; Sheep ; Social Environment ; Sound production ; Speech ; Stimulation ; Syllables ; Synapses ; Tetanus ; Tetanus toxin ; Toxins ; Vocal cords ; Vocal organs ; Vocalization behavior ; Vocalization, Animal - physiology ; Volatile Organic Compounds</subject><ispartof>Science (American Association for the Advancement of Science), 2024-03, Vol.383 (6687), p.eadi8081-eadi8081</ispartof><rights>Copyright © 2024 The Authors, some rights reserved; exclusive licensee American Association for the Advancement of Science. No claim to original U.S. Government Works</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c422t-bef3f77e18cf78835fef694e39a36444aab104710bb012398fe6280e03313c6d3</citedby><cites>FETCH-LOGICAL-c422t-bef3f77e18cf78835fef694e39a36444aab104710bb012398fe6280e03313c6d3</cites><orcidid>0000-0002-0976-7684 ; 0000-0002-3133-6493 ; 0000-0003-2988-0614 ; 0009-0004-3189-3830 ; 0009-0007-9432-0070</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>230,314,780,784,885,2884,2885,27924,27925</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/38452069$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Park, Jaehong</creatorcontrib><creatorcontrib>Choi, Seonmi</creatorcontrib><creatorcontrib>Takatoh, Jun</creatorcontrib><creatorcontrib>Zhao, Shengli</creatorcontrib><creatorcontrib>Harrahill, Andrew</creatorcontrib><creatorcontrib>Han, Bao-Xia</creatorcontrib><creatorcontrib>Wang, Fan</creatorcontrib><title>Brainstem control of vocalization and its coordination with respiration</title><title>Science (American Association for the Advancement of Science)</title><addtitle>Science</addtitle><description>Phonation critically depends on precise controls of laryngeal muscles in coordination with ongoing respiration. However, the neural mechanisms governing these processes remain unclear. We identified excitatory vocalization-specific laryngeal premotor neurons located in the retroambiguus nucleus (RAm
) in adult mice as being both necessary and sufficient for driving vocal cord closure and eliciting mouse ultrasonic vocalizations (USVs). The duration of RAm
activation can determine the lengths of both USV syllables and concurrent expiration periods, with the impact of RAm
activation depending on respiration phases. RAm
neurons receive inhibition from the preBötzinger complex, and inspiration needs override RAm
-mediated vocal cord closure. Ablating inhibitory synapses in RAm
neurons compromised this inspiration gating of laryngeal adduction, resulting in discoordination of vocalization with respiration. Our study reveals the circuits for vocal production and vocal-respiratory coordination.</description><subject>Ablation</subject><subject>Animals</subject><subject>Brain Stem</subject><subject>Breathing</subject><subject>Coordination</subject><subject>Courtship</subject><subject>Expiration</subject><subject>Fear of Success</subject><subject>Gating</subject><subject>Heterogeneity</subject><subject>Hindbrain</subject><subject>Inhalation</subject><subject>Inspiration</subject><subject>Larynx</subject><subject>Lyssavirus</subject><subject>Male</subject><subject>Medulla Oblongata - physiology</subject><subject>Mesencephalon</subject><subject>Mice</subject><subject>Motor neurons</subject><subject>Muscle function</subject><subject>Muscles</subject><subject>Neurogenesis</subject><subject>Neurons</subject><subject>Neurons - physiology</subject><subject>Nodes</subject><subject>Periaqueductal gray area</subject><subject>Phonation</subject><subject>Rabies</subject><subject>Respiration</subject><subject>Rhythms</subject><subject>Sheep</subject><subject>Social Environment</subject><subject>Sound production</subject><subject>Speech</subject><subject>Stimulation</subject><subject>Syllables</subject><subject>Synapses</subject><subject>Tetanus</subject><subject>Tetanus toxin</subject><subject>Toxins</subject><subject>Vocal cords</subject><subject>Vocal organs</subject><subject>Vocalization behavior</subject><subject>Vocalization, Animal - 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physiology</topic><topic>Mesencephalon</topic><topic>Mice</topic><topic>Motor neurons</topic><topic>Muscle function</topic><topic>Muscles</topic><topic>Neurogenesis</topic><topic>Neurons</topic><topic>Neurons - physiology</topic><topic>Nodes</topic><topic>Periaqueductal gray area</topic><topic>Phonation</topic><topic>Rabies</topic><topic>Respiration</topic><topic>Rhythms</topic><topic>Sheep</topic><topic>Social Environment</topic><topic>Sound production</topic><topic>Speech</topic><topic>Stimulation</topic><topic>Syllables</topic><topic>Synapses</topic><topic>Tetanus</topic><topic>Tetanus toxin</topic><topic>Toxins</topic><topic>Vocal cords</topic><topic>Vocal organs</topic><topic>Vocalization behavior</topic><topic>Vocalization, Animal - physiology</topic><topic>Volatile Organic Compounds</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Park, Jaehong</creatorcontrib><creatorcontrib>Choi, Seonmi</creatorcontrib><creatorcontrib>Takatoh, Jun</creatorcontrib><creatorcontrib>Zhao, Shengli</creatorcontrib><creatorcontrib>Harrahill, Andrew</creatorcontrib><creatorcontrib>Han, Bao-Xia</creatorcontrib><creatorcontrib>Wang, Fan</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Aluminium Industry Abstracts</collection><collection>Animal Behavior Abstracts</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Calcium & Calcified Tissue Abstracts</collection><collection>Ceramic Abstracts</collection><collection>Chemoreception Abstracts</collection><collection>Computer and Information Systems Abstracts</collection><collection>Corrosion Abstracts</collection><collection>Ecology Abstracts</collection><collection>Electronics & Communications Abstracts</collection><collection>Engineered Materials Abstracts</collection><collection>Entomology Abstracts (Full archive)</collection><collection>Industrial and Applied Microbiology Abstracts (Microbiology A)</collection><collection>Materials Business File</collection><collection>Mechanical & Transportation Engineering Abstracts</collection><collection>Neurosciences Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>Solid State and Superconductivity Abstracts</collection><collection>Virology and AIDS Abstracts</collection><collection>METADEX</collection><collection>Technology Research Database</collection><collection>Environmental Sciences and Pollution Management</collection><collection>ANTE: Abstracts in New Technology & Engineering</collection><collection>Engineering Research Database</collection><collection>Aerospace Database</collection><collection>Copper Technical Reference Library</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>Materials Research Database</collection><collection>ProQuest Computer Science Collection</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>Civil Engineering Abstracts</collection><collection>Advanced Technologies Database with Aerospace</collection><collection>Computer and Information Systems Abstracts Academic</collection><collection>Computer and Information Systems Abstracts Professional</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Science (American Association for the Advancement of Science)</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Park, Jaehong</au><au>Choi, Seonmi</au><au>Takatoh, Jun</au><au>Zhao, Shengli</au><au>Harrahill, Andrew</au><au>Han, Bao-Xia</au><au>Wang, Fan</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Brainstem control of vocalization and its coordination with respiration</atitle><jtitle>Science (American Association for the Advancement of Science)</jtitle><addtitle>Science</addtitle><date>2024-03-08</date><risdate>2024</risdate><volume>383</volume><issue>6687</issue><spage>eadi8081</spage><epage>eadi8081</epage><pages>eadi8081-eadi8081</pages><issn>0036-8075</issn><issn>1095-9203</issn><eissn>1095-9203</eissn><abstract>Phonation critically depends on precise controls of laryngeal muscles in coordination with ongoing respiration. However, the neural mechanisms governing these processes remain unclear. We identified excitatory vocalization-specific laryngeal premotor neurons located in the retroambiguus nucleus (RAm
) in adult mice as being both necessary and sufficient for driving vocal cord closure and eliciting mouse ultrasonic vocalizations (USVs). The duration of RAm
activation can determine the lengths of both USV syllables and concurrent expiration periods, with the impact of RAm
activation depending on respiration phases. RAm
neurons receive inhibition from the preBötzinger complex, and inspiration needs override RAm
-mediated vocal cord closure. Ablating inhibitory synapses in RAm
neurons compromised this inspiration gating of laryngeal adduction, resulting in discoordination of vocalization with respiration. Our study reveals the circuits for vocal production and vocal-respiratory coordination.</abstract><cop>United States</cop><pub>The American Association for the Advancement of Science</pub><pmid>38452069</pmid><doi>10.1126/science.adi8081</doi><orcidid>https://orcid.org/0000-0002-0976-7684</orcidid><orcidid>https://orcid.org/0000-0002-3133-6493</orcidid><orcidid>https://orcid.org/0000-0003-2988-0614</orcidid><orcidid>https://orcid.org/0009-0004-3189-3830</orcidid><orcidid>https://orcid.org/0009-0007-9432-0070</orcidid><oa>free_for_read</oa></addata></record> |
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| source | American Association for the Advancement of Science; Alma/SFX Local Collection |
| subjects | Ablation Animals Brain Stem Breathing Coordination Courtship Expiration Fear of Success Gating Heterogeneity Hindbrain Inhalation Inspiration Larynx Lyssavirus Male Medulla Oblongata - physiology Mesencephalon Mice Motor neurons Muscle function Muscles Neurogenesis Neurons Neurons - physiology Nodes Periaqueductal gray area Phonation Rabies Respiration Rhythms Sheep Social Environment Sound production Speech Stimulation Syllables Synapses Tetanus Tetanus toxin Toxins Vocal cords Vocal organs Vocalization behavior Vocalization, Animal - physiology Volatile Organic Compounds |
| title | Brainstem control of vocalization and its coordination with respiration |
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