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      Aerodynamics and motor control of ultrasonic vocalizations for social communication in mice and rats

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          Abstract

          Background

          Rodent ultrasonic vocalizations (USVs) are crucial to their social communication and a widely used translational tool for linking gene mutations to behavior. To maximize the causal interpretation of experimental treatments, we need to understand how neural control affects USV production. However, both the aerodynamics of USV production and its neural control remain poorly understood.

          Results

          Here, we test three intralaryngeal whistle mechanisms—the wall and alar edge impingement, and shallow cavity tone—by combining in vitro larynx physiology and individual-based 3D airway reconstructions with fluid dynamics simulations. Our results show that in the mouse and rat larynx, USVs are produced by a glottal jet impinging on the thyroid inner wall. Furthermore, we implemented an empirically based motor control model that predicts motor gesture trajectories of USV call types.

          Conclusions

          Our results identify wall impingement as the aerodynamic mechanism of USV production in rats and mice. Furthermore, our empirically based motor control model shows that both neural and anatomical components contribute to USV production, which suggests that changes in strain specific USVs or USV changes in disease models can result from both altered motor programs and laryngeal geometry. Our work provides a quantitative neuromechanical framework to evaluate the contributions of brain and body in shaping USVs and a first step in linking descending motor control to USV production.

          Supplementary Information

          The online version contains supplementary material available at 10.1186/s12915-021-01185-z.

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          Most cited references64

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          Behavioural phenotyping assays for mouse models of autism.

          Autism is a heterogeneous neurodevelopmental disorder of unknown aetiology that affects 1 in 100-150 individuals. Diagnosis is based on three categories of behavioural criteria: abnormal social interactions, communication deficits and repetitive behaviours. Strong evidence for a genetic basis has prompted the development of mouse models with targeted mutations in candidate genes for autism. As the diagnostic criteria for autism are behavioural, phenotyping these mouse models requires behavioural assays with high relevance to each category of the diagnostic symptoms. Behavioural neuroscientists are generating a comprehensive set of assays for social interaction, communication and repetitive behaviours to test hypotheses about the causes of autism. Robust phenotypes in mouse models hold great promise as translational tools for discovering effective treatments for components of autism spectrum disorders.
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            Self-organization, embodiment, and biologically inspired robotics.

            Robotics researchers increasingly agree that ideas from biology and self-organization can strongly benefit the design of autonomous robots. Biological organisms have evolved to perform and survive in a world characterized by rapid changes, high uncertainty, indefinite richness, and limited availability of information. Industrial robots, in contrast, operate in highly controlled environments with no or very little uncertainty. Although many challenges remain, concepts from biologically inspired (bio-inspired) robotics will eventually enable researchers to engineer machines for the real world that possess at least some of the desirable properties of biological organisms, such as adaptivity, robustness, versatility, and agility.
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              How many species are there on Earth?

              R M May (1988)
              This article surveys current answers to the factual question posed in the title and reviews the kinds of information that are needed to make these answers more precise. Various factors affecting diversity are also reviewed. These include the structure of food webs, the relative abundance of species, the number of species and of individuals in different categories of body size, along with other determinants of the commonness and rarity of organisms.
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                Author and article information

                Contributors
                coen@biology.sdu.dk
                Journal
                BMC Biol
                BMC Biol
                BMC Biology
                BioMed Central (London )
                1741-7007
                7 January 2022
                7 January 2022
                2022
                : 20
                : 3
                Affiliations
                [1 ]GRID grid.10825.3e, ISNI 0000 0001 0728 0170, Department of Biology, , University of Southern Denmark, ; 5230 Odense M, Denmark
                [2 ]GRID grid.21106.34, ISNI 0000000121820794, Department of Mechanical Engineering, , University of Maine, ; Orono, ME 04469 USA
                [3 ]GRID grid.7143.1, ISNI 0000 0004 0512 5013, Department of Orthopaedic Surgery and Traumatology, , Odense University Hospital, ; 5000 Odense C, Denmark
                [4 ]GRID grid.10825.3e, ISNI 0000 0001 0728 0170, Department of Clinical Research, , University of Southern Denmark, ; 5000 Odense C, Denmark
                [5 ]GRID grid.5335.0, ISNI 0000000121885934, Department of Engineering, , University of Cambridge, ; Cambridge, CB2 1TN UK
                Author information
                https://orcid.org/0000-0002-1247-5586
                https://orcid.org/0000-0002-7576-9653
                https://orcid.org/0000-0002-8462-1271
                https://orcid.org/0000-0001-5403-8862
                https://orcid.org/0000-0002-6610-8079
                https://orcid.org/0000-0002-0332-2166
                http://orcid.org/0000-0001-6306-5715
                Article
                1185
                10.1186/s12915-021-01185-z
                8742360
                34996429
                2ab02e8c-5b05-4ccf-a0a0-45300739246e
                © The Author(s) 2021

                Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data.

                History
                : 13 January 2021
                : 7 November 2021
                Funding
                Funded by: FundRef http://dx.doi.org/10.13039/100008394, Natur og Univers, Det Frie Forskningsråd;
                Award ID: 7014-00270B
                Categories
                Research Article
                Custom metadata
                © The Author(s) 2022

                Life sciences
                bioacoustics,vocal production,acoustic communication,speech,rodents
                Life sciences
                bioacoustics, vocal production, acoustic communication, speech, rodents

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