Adapted to Roar: Functional Morphology of Tiger and Lion Vocal Folds
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{"title"=>"Adapted to roar: Functional morphology of tiger and lion vocal folds", "type"=>"journal", "authors"=>[{"first_name"=>"Sarah A.", "last_name"=>"Klemuk", "scopus_author_id"=>"6508202541"}, {"first_name"=>"Tobias", "last_name"=>"Riede", "scopus_author_id"=>"6701515719"}, {"first_name"=>"Edward J.", "last_name"=>"Walsh", "scopus_author_id"=>"16187659400"}, {"first_name"=>"Ingo R.", "last_name"=>"Titze", "scopus_author_id"=>"35838594900"}], "year"=>2011, "source"=>"PLoS ONE", "identifiers"=>{"isbn"=>"19326203 (ISSN)", "pmid"=>"22073246", "doi"=>"10.1371/journal.pone.0027029", "pui"=>"362861826", "issn"=>"19326203", "sgr"=>"80355143394", "scopus"=>"2-s2.0-80355143394"}, "id"=>"b5ff002c-204a-3b56-aa53-32555f7dd3fa", "abstract"=>"Vocal production requires active control of the respiratory system, larynx and vocal tract. Vocal sounds in mammals are produced by flow-induced vocal fold oscillation, which requires vocal fold tissue that can sustain the mechanical stress during phonation. Our understanding of the relationship between morphology and vocal function of vocal folds is very limited. Here we tested the hypothesis that vocal fold morphology and viscoelastic properties allow a prediction of fundamental frequency range of sounds that can be produced, and minimal lung pressure necessary to initiate phonation. We tested the hypothesis in lions and tigers who are well-known for producing low frequency and very loud roaring sounds that expose vocal folds to large stresses. In histological sections, we found that the Panthera vocal fold lamina propria consists of a lateral region with adipocytes embedded in a network of collagen and elastin fibers and hyaluronan. There is also a medial region that contains only fibrous proteins and hyaluronan but no fat cells. Young's moduli range between 10 and 2000 kPa for strains up to 60%. Shear moduli ranged between 0.1 and 2 kPa and differed between layers. Biomechanical and morphological data were used to make predictions of fundamental frequency and subglottal pressure ranges. Such predictions agreed well with measurements from natural phonation and phonation of excised larynges, respectively. We assume that fat shapes Panthera vocal folds into an advantageous geometry for phonation and it protects vocal folds. Its primary function is probably not to increase vocal fold mass as suggested previously. The large square-shaped Panthera vocal fold eases phonation onset and thereby extends the dynamic range of the voice.", "link"=>"http://www.mendeley.com/research/adapted-roar-functional-morphology-tiger-lion-vocal-folds", "reader_count"=>45, "reader_count_by_academic_status"=>{"Professor > Associate Professor"=>3, "Researcher"=>9, "Student > Ph. D. Student"=>10, "Student > Postgraduate"=>1, "Student > Master"=>9, "Other"=>4, "Student > Bachelor"=>2, "Lecturer"=>2, "Professor"=>4, "Unspecified"=>1}, "reader_count_by_user_role"=>{"Professor > Associate Professor"=>3, "Researcher"=>9, "Student > Ph. D. Student"=>10, "Student > Postgraduate"=>1, "Student > Master"=>9, "Other"=>4, "Student > Bachelor"=>2, "Lecturer"=>2, "Professor"=>4, "Unspecified"=>1}, "reader_count_by_subject_area"=>{"Engineering"=>3, "Environmental Science"=>4, "Agricultural and Biological Sciences"=>26, "Medicine and Dentistry"=>4, "Neuroscience"=>1, "Business, Management and Accounting"=>1, "Physics and Astronomy"=>1, "Social Sciences"=>1, "Computer Science"=>3, "Unspecified"=>1}, "reader_count_by_subdiscipline"=>{"Engineering"=>{"Engineering"=>3}, "Medicine and Dentistry"=>{"Medicine and Dentistry"=>4}, "Neuroscience"=>{"Neuroscience"=>1}, "Social Sciences"=>{"Social Sciences"=>1}, "Physics and Astronomy"=>{"Physics and Astronomy"=>1}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>26}, "Computer Science"=>{"Computer Science"=>3}, "Business, Management and Accounting"=>{"Business, Management and Accounting"=>1}, "Environmental Science"=>{"Environmental Science"=>4}, "Unspecified"=>{"Unspecified"=>1}}, "reader_count_by_country"=>{"Hungary"=>1, "United Kingdom"=>2, "India"=>1}, "group_count"=>0}

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/717034"], "description"=>"<p>A: Schematic frontal section through a larynx. The square indicates where the histological sections (Haematoxylin-eosin stain) in B, C and D were taken from. The mid-membraneous sections of the vocal fold are from Bengal tiger (<b>B</b>), Siberian tiger (<b>C</b>), and Lion (<b>D</b>). The terms ‘lateral’ and ‘medial’ are used in reference to the body axis and are indicated in D to explain how they apply to the vocal fold. In all three species, the vocal fold consists of epithelium, lamina propria and the thyroarytenoid muscle. LP: lamina propria; E: epiglottis; T: thyroid cartilage; TA: thyroarytenoid muscle; CT: cricothyroid muscle; C: cricoid cartilage; B: tracheal ring. Arrows in A indicate the airflow during expiration. Horizontal arrows in LP of B indicate medio-lateral depth. Vertical arrows in LP of B indicate cranio-caudal thickness.</p>", "links"=>[], "tags"=>["folds"], "article_id"=>387390, "categories"=>["Physiology", "Biophysics"], "users"=>["Sarah A. Klemuk", "Tobias Riede", "Edward J. Walsh", "Ingo R. Titze"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0027029.g001", "stats"=>{"downloads"=>1, "page_views"=>12, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Panthera_vocal_folds_possess_a_large_lamina_propria_/387390", "title"=>"Panthera vocal folds possess a large <i>lamina propria</i>.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-20 12:05:03"}
  • {"files"=>["https://ndownloader.figshare.com/files/717185"], "description"=>"<p>Haematoxylin-eosin stain of a Bengal tiger vocal fold. <b>A</b>: Overview of a midmembraneous section indicating a densely packed lamina propria without fat cells medially (LP<sub>2</sub>) and with fat cells laterally (LP<sub>1</sub>). The approximate border between both regions is indicated by a dotted line. Bar indicates a 5 mm distance. Larger magnification of an area in LP<sub>1</sub> region (<b>B</b>) and in LP<sub>2</sub> region (<b>C</b>) are shown. Bars in <b>B</b> and <b>C</b> indicate a 100 µm distance. TA: thyroarytenoid muscle; LP: lamina propria; BV: blood vessel; FC: fat cells.</p>", "links"=>[], "tags"=>["cells"], "article_id"=>387547, "categories"=>["Physiology", "Biophysics"], "users"=>["Sarah A. Klemuk", "Tobias Riede", "Edward J. Walsh", "Ingo R. Titze"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0027029.g002", "stats"=>{"downloads"=>1, "page_views"=>3, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Fat_cells_are_only_found_in_a_deep_portion_of_the_lamina_propria_/387547", "title"=>"Fat cells are only found in a deep portion of the <i>lamina propria</i>.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-20 12:05:54"}
  • {"files"=>["https://ndownloader.figshare.com/files/718684"], "description"=>"<p>E, Young's modulus (in kPa) between the linear strain limit and 50% strain. F<sub>0</sub>, fundamental frequency (in Hz) implementing the linear and exponential model in Eq. 1.</p>", "links"=>[], "tags"=>["linear", "curve-fitting", "empirical", "stress-strain", "lamina", "parameters", "exponential"], "article_id"=>389036, "categories"=>["Physiology", "Biophysics"], "users"=>["Sarah A. Klemuk", "Tobias Riede", "Edward J. Walsh", "Ingo R. Titze"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0027029.t002", "stats"=>{"downloads"=>0, "page_views"=>4, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Parameters_of_the_linear_model_Eq_6_for_curve_fitting_the_empirical_stress_strain_response_of_the_lamina_propria_linear_strain_limit_1_in_and_parameters_of_the_exponential_model_Eq_7_for_curve_fitting_the_empirical_stress_strain_response_of_the_lamina_pr/389036", "title"=>"Parameters of the linear model (Eq. 6) for curve-fitting the empirical stress-strain response of the lamina propria; linear strain limit (ε<sub>1</sub>) in %; and parameters of the exponential model (Eq. 7) for curve-fitting the empirical stress-strain response of the lamina propria.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2013-02-20 12:13:38"}
  • {"files"=>["https://ndownloader.figshare.com/files/718136"], "description"=>"<p><b>A</b>: loading and unloading phase. The upper part of the “banana-shaped” curve is the loading phase (stretching). The lower part is the unloading phase (relaxation). The difference between both curves is due to hysteresis of the tissue, i.e., lower stress in the tissue during the unloading phase. The low strain region of the loading phase was fitted with a linear regression line (<b>B</b>), while the high-strain region was modeled with an exponential function (<b>C</b>). The limit of the linear region (‘Linear strain limit’) was determined by maximizing the sum of the two regression coefficients (‘sum of r<sup>2</sup>’). <b>D</b>: Tangents modulus versus strain for the high-strain (>Linear strain limit) region.</p>", "links"=>[], "tags"=>["linear", "followed", "nonlinear", "occurs", "subjected", "hz", "sinusoidal"], "article_id"=>388489, "categories"=>["Physiology", "Biophysics"], "users"=>["Sarah A. Klemuk", "Tobias Riede", "Edward J. Walsh", "Ingo R. Titze"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0027029.g007", "stats"=>{"downloads"=>1, "page_views"=>3, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_A_linear_followed_by_a_nonlinear_stress_response_at_about_15_strain_occurs_when_Lion_2_vocal_fold_lamina_propria_is_subjected_to_a_1_Hz_sinusoidal_elongation_/388489", "title"=>"A linear followed by a nonlinear stress response at about 15% strain occurs when Lion 2 vocal fold <i>lamina propria</i> is subjected to a 1 Hz sinusoidal elongation.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-20 12:10:55"}
  • {"files"=>["https://ndownloader.figshare.com/files/718378"], "description"=>"<p>Mean elastic modulus <i>G</i>′ (<b>A</b>), viscous modulus <i>G</i>″ (<b>B</b>), and loss tangent = <i>G</i>″/<i>G</i>′ (<b>C</b>) of the lion LP<sub>2</sub> and LP<sub>1</sub> as a function of frequency. Error bars correspond to ±1 standard error().</p>", "links"=>[], "tags"=>["modulus", "tangent", "diverge", "frequencies", "larger", "10", "hz", "fat-free", "fat-containing"], "article_id"=>388733, "categories"=>["Physiology", "Biophysics"], "users"=>["Sarah A. Klemuk", "Tobias Riede", "Edward J. Walsh", "Ingo R. Titze"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0027029.g009", "stats"=>{"downloads"=>3, "page_views"=>11, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Viscous_modulus_and_loss_tangent_diverge_at_frequencies_larger_10_Hz_indicating_different_behavior_between_the_fat_free_and_fat_containing_layer_/388733", "title"=>"Viscous modulus and loss tangent diverge at frequencies larger 10 Hz indicating different behavior between the fat-free and fat-containing layer.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-20 12:12:07"}
  • {"files"=>["https://ndownloader.figshare.com/files/717475"], "description"=>"<p>A: Overview of a midmembraneous section (Elastica-van-Gieson stain). Bar indicates a 5 mm distance. Larger magnifications indicated by four squares in the overview are shown in <b>B</b>–<b>E</b>. The black dots in <b>B</b> are cross sections of elastic fibers. They indicate that most of the elastic fibers are oriented dorso-ventrally. More laterally (<b>C</b>, <b>D</b> and <b>E</b>), fibers are cut along as well as perpendicular to their longitudinal axis suggesting that fibers are more variably oriented. Bars in <b>B</b> and <b>C</b> indicate a 100 µm distance. TA: thyroarytenoid muscle; BV: blood vessel; FC: fat cells; EP: epithelium.</p>", "links"=>[], "tags"=>["fibers", "densely", "packed", "medial"], "article_id"=>387838, "categories"=>["Physiology", "Biophysics"], "users"=>["Sarah A. Klemuk", "Tobias Riede", "Edward J. Walsh", "Ingo R. Titze"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0027029.g003", "stats"=>{"downloads"=>1, "page_views"=>6, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Elastic_fibers_are_densely_packed_in_the_medial_Lion_vocal_fold_/387838", "title"=>"Elastic fibers are densely packed in the medial Lion vocal fold.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-20 12:07:20"}
  • {"files"=>["https://ndownloader.figshare.com/files/718734"], "description"=>"<p>Provided here is a single value for Young's modulus at 40% strain. At large strains the stress-strain curve of the lamina propria is exponential and therefore the Young's modulus is continuously changing.</p>", "links"=>[], "tags"=>["tangent", "moduli", "lamina", "propria", "folds", "males", "mammal"], "article_id"=>389086, "categories"=>["Physiology", "Biophysics"], "users"=>["Sarah A. Klemuk", "Tobias Riede", "Edward J. Walsh", "Ingo R. Titze"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0027029.t003", "stats"=>{"downloads"=>2, "page_views"=>10, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Mean_tangent_Young_s_moduli_of_lamina_propria_tissue_of_vocal_folds_from_males_of_different_mammal_species_/389086", "title"=>"Mean tangent Young's moduli of lamina propria tissue of vocal folds from males of different mammal species.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2013-02-20 12:13:52"}
  • {"files"=>["https://ndownloader.figshare.com/files/718222"], "description"=>"<p>Shear elastic modulus <i>G</i>′ (<b>A</b>), viscous modulus <i>G</i>″ (<b>B</b>) and loss tangent = <i>G</i>″/<i>G</i>′ (<b>C</b>) lion, Siberian tiger, and Sumatran tiger vocal fold tissue as a function of frequency.</p>", "links"=>[], "tags"=>["viscous", "moduli", "tiger", "tissues", "elastic", "modulus", "dominates", "oscillation", "tangent"], "article_id"=>388573, "categories"=>["Physiology", "Biophysics"], "users"=>["Sarah A. Klemuk", "Tobias Riede", "Edward J. Walsh", "Ingo R. Titze"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0027029.g008", "stats"=>{"downloads"=>2, "page_views"=>54, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Elastic_and_viscous_moduli_of_lion_and_tiger_vocal_fold_tissues_increase_with_frequency_where_elastic_modulus_dominates_material_response_to_oscillation_i_e_loss_tangent_values_are_0_1_8211_0_4_/388573", "title"=>"Elastic and viscous moduli of lion and tiger vocal fold tissues increase with frequency, where elastic modulus dominates material response to oscillation (i.e., loss tangent values are 0.1–0.4).", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-20 12:11:20"}
  • {"files"=>["https://ndownloader.figshare.com/files/718509"], "description"=>"<p>The values were calculated from biomechanical properties of lion and Sumatran tiger across frequency with varying glottal half-widths.</p>", "links"=>[], "tags"=>["panthera"], "article_id"=>388875, "categories"=>["Physiology", "Biophysics"], "users"=>["Sarah A. Klemuk", "Tobias Riede", "Edward J. Walsh", "Ingo R. Titze"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0027029.g010", "stats"=>{"downloads"=>1, "page_views"=>3, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Phonation_threshold_is_surprisingly_low_for_Panthera_vocal_folds_/388875", "title"=>"Phonation threshold is surprisingly low for Panthera vocal folds.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-20 12:12:49"}
  • {"files"=>["https://ndownloader.figshare.com/files/717842"], "description"=>"<p><b>A</b>: Overview of a midmembraneous section (Trichrome stain) of a lion vocal fold. Bar indicates a 5 mm distance. Larger magnifications indicated by four squares in the overview are shown in <b>B</b>–<b>E</b>. Bars in <b>B</b> to <b>E</b> indicate a 100 µm distance. TA: thyroarytenoid muscle; BV: blood vessel; FC: fat cells; EP: epithelium.</p>", "links"=>[], "tags"=>["fibers", "densely", "packed", "medial", "cells", "lateral"], "article_id"=>388197, "categories"=>["Physiology", "Biophysics"], "users"=>["Sarah A. Klemuk", "Tobias Riede", "Edward J. Walsh", "Ingo R. Titze"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0027029.g005", "stats"=>{"downloads"=>5, "page_views"=>8, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Collagen_fibers_are_densely_packed_in_the_medial_layer_and_provide_a_bed_for_fat_cells_in_the_lateral_portion_/388197", "title"=>"Collagen fibers are densely packed in the medial layer and provide a bed for fat cells in the lateral portion.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-20 12:09:16"}
  • {"files"=>["https://ndownloader.figshare.com/files/718645"], "description"=>"<p>Specimen details. vocal fold length measured between insertion at thyroid cartilage and ventral tip of processus vocalis of arytenoid cartilage.</p>", "links"=>[], "tags"=>["insertion", "thyroid", "cartilage", "ventral", "processus", "vocalis", "arytenoid"], "article_id"=>388997, "categories"=>["Physiology", "Biophysics"], "users"=>["Sarah A. Klemuk", "Tobias Riede", "Edward J. Walsh", "Ingo R. Titze"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0027029.t001", "stats"=>{"downloads"=>7, "page_views"=>10, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Specimen_details_vocal_fold_length_measured_between_insertion_at_thyroid_cartilage_and_ventral_tip_of_processus_vocalis_of_arytenoid_cartilage_/388997", "title"=>"Specimen details. vocal fold length measured between insertion at thyroid cartilage and ventral tip of processus vocalis of arytenoid cartilage.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2013-02-20 12:13:24"}
  • {"files"=>["https://ndownloader.figshare.com/files/717661"], "description"=>"<p>Elastin, collagen and fat distribution along a medio-lateral transect for Siberian Tiger (<b>A</b>) Lion (<b>B</b>) and Bengal Tiger (<b>C</b>). The area is the relative number of pixels stained positively (elastin, collagen) or representing empty fat cells. See <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0027029#pone-0027029-g001\" target=\"_blank\">Figure 1</a> for an explanation of ‘lateral’ and ‘medial’.</p>", "links"=>[], "tags"=>["cells", "distributed", "medial", "lateral"], "article_id"=>388018, "categories"=>["Physiology", "Biophysics"], "users"=>["Sarah A. Klemuk", "Tobias Riede", "Edward J. Walsh", "Ingo R. Titze"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0027029.g004", "stats"=>{"downloads"=>1, "page_views"=>12, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Proteins_and_fat_cells_are_distributed_differently_in_the_medial_and_lateral_lamina_propria_/388018", "title"=>"Proteins and fat cells are distributed differently in the medial and lateral <i>lamina propria</i>.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-20 12:08:20"}
  • {"files"=>["https://ndownloader.figshare.com/files/718020"], "description"=>"<p>Overview of an alcian blue stain (<b>A</b>) and an alcian blue stain after hyaluronidase treatment (<b>B</b>) of two consecutive midmembraneous sections of a Siberian tiger vocal fold. Sections in (<b>C</b>) to (<b>F</b>) are larger magnifications of two different locations of the lamina propria. The locations are indicated by little squares with the respective letter in (<b>A</b>) and (<b>B</b>). (<b>C</b>) and (<b>D</b>): locations in the densely packed lamina propria without fat cells medially (LP<sub>2</sub> in <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0027029#pone-0027029-g002\" target=\"_blank\">Figure 2</a>) and (<b>E</b>) and (<b>F</b>) are lamina propria locations with fat cells laterally (LP<sub>1</sub> in <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0027029#pone-0027029-g002\" target=\"_blank\">Figure 2</a>). Scale bar in <b>A</b> and <b>B</b> is 5 mm, scale bar in <b>C</b>–<b>F</b> is 100 µm. TA: thyroarytenoid muscle; LP: lamina propria; FC: fat cells; GL: glands; EP: epithelium.</p>", "links"=>[], "tags"=>["physiology", "biophysics"], "article_id"=>388383, "categories"=>["Physiology", "Biophysics"], "users"=>["Sarah A. Klemuk", "Tobias Riede", "Edward J. Walsh", "Ingo R. Titze"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0027029.g006", "stats"=>{"downloads"=>1, "page_views"=>4, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Hyaluronan_is_found_throughout_the_lamina_propria_/388383", "title"=>"Hyaluronan is found throughout the <i>lamina propria</i>.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-20 12:10:15"}

PMC Usage Stats | Further Information

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