Vocal tract dynamics shape the formant structure of conditioned vocalizations in a harbor seal.

Phoca vitulina articulation formants source‐filter theory vocal communication vocal tract

Journal

Annals of the New York Academy of Sciences
ISSN: 1749-6632
Titre abrégé: Ann N Y Acad Sci
Pays: United States
ID NLM: 7506858

Informations de publication

Date de publication:
01 Aug 2024
Historique:
medline: 2 8 2024
pubmed: 2 8 2024
entrez: 2 8 2024
Statut: aheadofprint

Résumé

Formants, or resonance frequencies of the upper vocal tract, are an essential part of acoustic communication. Articulatory gestures-such as jaw, tongue, lip, and soft palate movements-shape formant structure in human vocalizations, but little is known about how nonhuman mammals use those gestures to modify formant frequencies. Here, we report a case study with an adult male harbor seal trained to produce an arbitrary vocalization composed of multiple repetitions of the sound wa. We analyzed jaw movements frame-by-frame and matched them to the tracked formant modulation in the corresponding vocalizations. We found that the jaw opening angle was strongly correlated with the first (F1) and, to a lesser degree, with the second formant (F2). F2 variation was better explained by the jaw angle opening when the seal was lying on his back rather than on the belly, which might derive from soft tissue displacement due to gravity. These results show that harbor seals share some common articulatory traits with humans, where the F1 depends more on the jaw position than F2. We propose further in vivo investigations of seals to further test the role of the tongue on formant modulation in mammalian sound production.

Identifiants

pubmed: 39091036
doi: 10.1111/nyas.15189
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Subventions

Organisme : European Research Council
ID : Advanced Grant SOMACCA
Pays : International
Organisme : Austrian Science Foundation Grant
ID : (#W1262-B29)
Organisme : Danmarks Grundforskningsfond
ID : DNRF117
Organisme : Office of Naval Research
ID : N00014-04-1-0284
Organisme : Max-Planck-Gesellschaft
ID : Independent Max Planck Research Group Leader funding

Informations de copyright

© 2024 The Author(s). Annals of the New York Academy of Sciences published by Wiley Periodicals LLC on behalf of The New York Academy of Sciences.

Références

Fant, G. (1970). Acoustic theory of speech production. Walter de Gruyter.
Titze, I. R., & Martin, D. W. (1998). Principles of voice production. Acoustical Society of America.
Charlton, B. D., & Reby, D. (2016). The evolution of acoustic size exaggeration in terrestrial mammals. Nature Communications, 7(1), Article 1. https://doi.org/10.1038/ncomms12739
Fitch, W. T. (1997). Vocal tract length and formant frequency dispersion correlate with body size in rhesus macaques. Journal of the Acoustical Society of America, 102(2), 1213–1222. https://doi.org/10.1121/1.421048
Reby, D., McComb, K., Cargnelutti, B., Darwin, C., Fitch, W. T., & Clutton‐Brock, T. (2005). Red deer stags use formants as assessment cues during intrasexual agonistic interactions. Proceedings of the Royal Society B: Biological Sciences, 272(1566), 941–947. https://doi.org/10.1098/rspb.2004.2954
Fitch, W. T. (1999). Acoustic exaggeration of size in birds via tracheal elongation: Comparative and theoretical analyses. Journal of Zoology, 248(1), 31–48. https://doi.org/10.1111/j.1469‐7998.1999.tb01020.x
Reber, S. A., Janisch, J., Torregrosa, K., Darlington, J., Vliet, K. A., & Fitch, W. T. (2017). Formants provide honest acoustic cues to body size in American alligators. Scientific Reports, 7(1), 1816. https://doi.org/10.1038/s41598‐017‐01948‐1
Fitch, W. T., & Hauser, M. D. (2003). Unpacking “honesty”: Vertebrate vocal production and the evolution of acoustic signals. In A. M. Simmons, R. R. Fay, & A. N. Popper (Eds.), Acoustic communication. (pp. 65–137). Springer. https://doi.org/10.1007/0‐387‐22762‐8_3
Beeck, V. C., Heilmann, G., Kerscher, M., & Stoeger, A. S. (2022). Sound visualization demonstrates velopharyngeal coupling and complex spectral variability in Asian elephants. Animals, 12(16), Article 16. https://doi.org/10.3390/ani12162119
Briefer, E. F. (2012). Vocal expression of emotions in mammals: Mechanisms of production and evidence. Journal of Zoology, 288(1), 1–20. https://doi.org/10.1111/j.1469‐7998.2012.00920.x
Taylor, A. M., & Reby, D. (2010). The contribution of source–filter theory to mammal vocal communication research. Journal of Zoology, 280(3), 221–236. https://doi.org/10.1111/j.1469‐7998.2009.00661.x
Mefferd, A. S., & Green, J. R. (2010). Articulatory‐to‐acoustic relations in response to speaking rate and loudness manipulations. Journal of Speech, Language, and Hearing Research, 53(5), 1206–1219. https://doi.org/10.1044/1092‐4388(2010/09‐0083)
Zlegler, W., & Cramon, D. V. (1983). Vowel distortion in traumatic dysarthria: A formant study. Phonetica, 40(1), 63–78. https://doi.org/10.1159/000261681
Roth, G., & Wake, D. (1989). Evolution of feeding in vertebrates. In D. B. Wake & G. Roth (Eds.), Complex organismal functions: Integration and evolution in vertebrates. (pp. 7–21). New York: Wiley‐Interscience.
Carterette, E., Shipley, C., & Buchwald, J. (1979). Linear prediction theory of vocalization in cat and kitten. In B. Lindblom & S. Öhman (Eds.), Frontiers in speech communication research (pp. 245–257).
Fitch, W. T. (2000). The phonetic potential of nonhuman vocal tracts: Comparative cineradiographic observations of vocalizing animals. Phonetica, 57(2–4), 205–218. https://doi.org/10.1159/000028474
Hauser, M. D., Evans, C. S., & Marler, P. (1993). The role of articulation in the production of rhesus monkey, Macaca mulatta, vocalizations. Animal Behaviour, 45(3), 423–433. https://doi.org/10.1006/anbe.1993.1054
Riede, T., Bronson, E., Hatzikirou, H., & Zuberbühler, K. (2005). Vocal production mechanisms in a non‐human primate: Morphological data and a model. Journal of Human Evolution, 48(1), 85–96. https://doi.org/10.1016/j.jhevol.2004.10.002
Shipley, C., Carterette, E. C., & Buchwald, J. S. (1991). The effects of articulation on the acoustical structure of feline vocalizations. Journal of the Acoustical Society of America, 89(2), 902–909. https://doi.org/10.1121/1.1894652
Elemans, C. P. H., Jiang, W., Jensen, M. H., Pichler, H., Mussman, B. R., Nattestad, J., Wahlberg, M., Zheng, X., Xue, Q., & Fitch, W. T. (2024). Evolutionary novelties underlie sound production in baleen whales. Nature, 627(8002), 123–129. https://doi.org/10.1038/s41586‐024‐07080‐1
Madsen, P. T., Siebert, U., & Elemans, C. P. H. (2023). Toothed whales use distinct vocal registers for echolocation and communication. Science, 379(6635), 928–933. https://doi.org/10.1126/science.adc9570
Fitch, W. T., & Reby, D. (2001). The descended larynx is not uniquely human. Proceedings of the Royal Society of London. Series B: Biological Sciences, 268(1477), 1669–1675. https://doi.org/10.1098/rspb.2001.1704
Frey, R., Volodin, I., Volodina, E., Soldatova, N. V., & Juldaschev, E. T. (2011). Descended and mobile larynx, vocal tract elongation and rutting roars in male goitred gazelles (Gazella subgutturosa Güldenstaedt, 1780). Journal of Anatomy, 218(5), 566–585. https://doi.org/10.1111/j.1469‐7580.2011.01361.x
Frey, R., Volodin, I., Volodina, E., Carranza, J., & Torres‐Porras, J. (2012). Vocal anatomy, tongue protrusion behaviour and the acoustics of rutting roars in free‐ranging Iberian red deer stags (Cervus elaphus hispanicus). Journal of Anatomy, 220(3), 271–292. https://doi.org/10.1111/j.1469‐7580.2011.01467.x
Frey, R., Volodin, I. A., Volodina, E. V., Efremova, K. O., Menges, V., Portas, R., Melzheimer, J., Fritsch, G., Gerlach, C., & von Dörnberg, K. (2020). Savannah roars: The vocal anatomy and the impressive rutting calls of male impala (Aepyceros melampus)—Highlighting the acoustic correlates of a mobile larynx. Journal of Anatomy, 236(3), 398–424. https://doi.org/10.1111/joa.13114
Riede, T. (2011). Subglottal pressure, tracheal airflow, and intrinsic laryngeal muscle activity during rat ultrasound vocalization. Journal of Neurophysiology, 106(5), 2580–2592. https://doi.org/10.1152/jn.00478.2011
Volodin, I., Volodina, E., Frey, R., Carranza, J., & Torres‐Porras, J. (2013). Spectrographic analysis points to source–filter coupling in rutting roars of Iberian red deer. Acta Ethologica, 16(1), 57–63. https://doi.org/10.1007/s10211‐012‐0133‐1
Hauser, M. D., & Schön Ybarra, M. S. (1994). The role of lip configuration in monkey vocalizations: Experiments using xylocaine as a nerve block. Brain and Language, 46(2), 232–244. https://doi.org/10.1006/brln.1994.1014
Titze, I. (1994). Fluctuations and perturbations in vocal output. In I. Titze (Ed.), Principles of voice production (pp. 209–306).
Fahlman, A., Moore, M. J., & Garcia‐Parraga, D. (2017). Respiratory function and mechanics in pinnipeds and cetaceans. Journal of Experimental Biology, 220(10), 1761–1773.
Parisi, I., De Vincenzi, G., Torri, M., Papale, E., Mazzola, S., Bonanno, A., & Buscaino, G. (2017). Underwater vocal complexity of Arctic seal Erignathus barbatus in Kongsfjorden (Svalbard). Journal of the Acoustical Society of America, 142(5), 3104–3115. https://doi.org/10.1121/1.5010887
Reichmuth, C., & Casey, C. (2014). Vocal learning in seals, sea lions, and walruses. Current Opinion in Neurobiology, 28, 66–71. https://doi.org/10.1016/j.conb.2014.06.011
Stansbury, A. L., & Janik, V. M. (2019). Formant modification through vocal production learning in gray seals. Current Biology, 29(13), 2244–2249.
Schusterman, R. J. (2008). Vocal learning in mammals with special emphasis on pinnipeds. In D. K. Oller, & U. Griebel (Eds.), Evolution of communicative flexibility: Complexity, creativity, and adaptability in human and animal communication. (pp. 41–70). MIT Press. https://doi.org/10.7551/mitpress/9780262151214.003.0003
Shapiro, A. D., Slater, P. J. B., & Janik, V. M. (2004). Call usage learning in gray seals (Halichoerus grypus). Journal of Comparative Psychology, 118(4), 447–454. https://doi.org/10.1037/0735‐7036.118.4.447
Michaelis, H., & Jones, D. (2003). A phonetic dictionary of the English language (Vol. 2). Psychology Press.
Casey, C., Sills, J. M., Knaub, S., Sotolotto, K., & Reichmuth, C. (2021). Lifelong patterns of sound production in two seals. Aquatic Mammals, 47(5), 499–514.
Reichmuth, C. (2023). The life semi‐aquatic: Harbor seal sprouts and milestones in marine bioacoustics. Journal of the Acoustical Society of America, 153, (3_supplement), A308. https://doi.org/10.1121/10.0018953
Sills, J. M., Southall, B. L., & Reichmuth, C. (2014). Amphibious hearing in spotted seals (Phoca largha): Underwater audiograms, aerial audiograms and critical ratio measurements. Journal of Experimental Biology, 217(5), 726–734. https://doi.org/10.1242/jeb.097469
Hanggi, E. B., & Schusterman, R. J. (1994). Underwater acoustic displays and individual variation in male harbour seals, Phoca vitulina. Animal Behaviour, 48(6), 1275–1283.
Nowak, L. J. (2021). Observations on mechanisms and phenomena underlying underwater and surface vocalisations of grey seals. Bioacoustics, 30(6), 696–715. https://doi.org/10.1080/09524622.2020.1851298
Buschmeier, H., & Wlodarczak, M. (2013). TextGridTools: A TextGrid processing and analysis toolkit for Python. Tagungsband Der 24. Konferenz Zur Elektronischen Sprachsignalverarbeitung (ESSV 2013).
Boersma, P., & Weenik, D. (2022). Praat: Doing phonetics by computer [Computer program]. (6.2.06) [Computer software]. https://www.praat.org
Jadoul, Y., Thompson, B., & Boer, B. (2018). Introducing Parselmouth: A Python interface to Praat. Journal of Phonetics, 71, 1–15. https://doi.org/10.1016/j.wocn.2018.07.001
Harris, C. R., Millman, K. J., van der Walt, S. J., Gommers, R., Virtanen, P., Cournapeau, D., Wieser, E., Taylor, J., Berg, S., Smith, N. J., Kern, R., Picus, M., Hoyer, S., van Kerkwijk, M. H., Brett, M., Haldane, A., del Río, J. F., Wiebe, M., Peterson, P., … Oliphant, T. E. (2020). Array programming with NumPy. Nature, 585(7825), Article 7825. https://doi.org/10.1038/s41586‐020‐2649‐2
van Kemenade, H., Murray, A., Clark, J. A., Karpinsky, A., Baranovič, O., Gohlke, C., Dufresne, J., Schmidt, D., Kopachev, K., Houghton, A., Mani, S., Landey, S., Ware, J., Piolie, Douglas, J., … Base, M. (2022). python‐pillow/Pillow: 9.2.0. [Computer software]. Zenodo. https://doi.org/10.5281/zenodo.6788304
Silvester, S., Tanbakuchi, A., Müller, P., Nunez‐Iglesias, J., Harfouche, M., McCormick, M., Ladegaard, A., Rai, A., Smith, T. D., Konowalczyk, M., Lee, A., Klein, A., Nises, J., Vaillant, G. A., Barnes, C., Zulko, … Dusold, C. (2020). Imageio/imageio v2.8.0. [Computer software]. Zenodo. https://doi.org/10.5281/zenodo.3674133
Fry, D. B. (1979). The physics of speech. Cambridge University Press.
Vorperian, H. K., Kurtzweil, S. L., Fourakis, M., Kent, R. D., Tillman, K. K., & Austin, D. (2015). Effect of body position on vocal tract acoustics: Acoustic pharyngometry and vowel formants. Journal of the Acoustical Society of America, 138(2), 833–845. https://doi.org/10.1121/1.4926563
Lindblom, B. E. F., & Sundberg, J. E. F. (1971). Acoustical consequences of lip, tongue, jaw, and larynx movement. Journal of the Acoustical Society of America, 50(4B), 1166–1179. https://doi.org/10.1121/1.1912750
Litman, R. S., Wake, N., Chan, L.‐M. L., McDonough, J. M., Sin, S., Mahboubi, S., & Arens, R. (2005). Effect of lateral positioning on upper airway size and morphology in sedated children. Anesthesiology, 103(3), 484–488. https://doi.org/10.1097/00000542‐200509000‐00009
Ono, T., Otsuka, R., Kuroda, T., Honda, E., & Sasaki, T. (2000). Effects of head and body position on two‐ and three‐dimensional configurations of the upper airway. Journal of Dental Research, 79(11), 1879–1884. https://doi.org/10.1177/00220345000790111101
Pae, E.‐K., Lowe, A. A., Sasaki, K., Price, C., Tsuchiya, M., & Fleetham, J. A. (1994). A cephalometric and electromyographic study of upper airway structures in the upright and supine positions. American Journal of Orthodontics and Dentofacial Orthopedics, 106(1), 52–59. https://doi.org/10.1016/S0889‐5406(94)70021‐4
Pevernagie, D. A., Stanson, A. W., Sheedy, P. F., Daniels, B. K., & Shepard, J. W. (1995). Effects of body position on the upper airway of patients with obstructive sleep apnea. American Journal of Respiratory and Critical Care Medicine, 152(1), 179–185. https://doi.org/10.1164/ajrccm.152.1.7599821
Shiller, D. M., Ostry, D. J., & Gribble, P. L. (1999). Effects of gravitational load on jaw movements in speech. Journal of Neuroscience, 19(20), 9073–9080. https://doi.org/10.1523/JNEUROSCI.19‐20‐09073.1999
Van Holsbeke, C. S., Verhulst, S. L., Vos, W. G., De Backer, J. W., Vinchurkar, S. C., Verdonck, P. R., van Doorn, J. W. D., Nadjmi, N., & De Backer, W. A. (2014). Change in upper airway geometry between upright and supine position during tidal nasal breathing. Journal of Aerosol Medicine and Pulmonary Drug Delivery, 27(1), 51–57. https://doi.org/10.1089/jamp.2012.1010
Schneider, R., & Kükenthal, W. G. (1964). Der larynx der säugetiere. de Gruyter.
Lee, J., Shaiman, S., & Weismer, G. (2016). Relationship between tongue positions and formant frequencies in female speakers. Journal of the Acoustical Society of America, 139(1), 426–440. https://doi.org/10.1121/1.4939894
Fernandez, A. A., Burchardt, L. S., Nagy, M., & Knörnschild, M. (2021). Babbling in a vocal learning bat resembles human infant babbling. Science, 373(6557), 923–926. https://doi.org/10.1126/science.abf9279

Auteurs

Maria Goncharova (M)

Comparative Bioacoustics Research Group, Max Planck Institute for Psycholinguistics, Nijmegen, the Netherlands.

Yannick Jadoul (Y)

Comparative Bioacoustics Research Group, Max Planck Institute for Psycholinguistics, Nijmegen, the Netherlands.
Artificial Intelligence Lab, Vrije Universiteit Brussel, Brussels, Belgium.
Department of Human Neurosciences, Sapienza University of Rome, Rome, Italy.

Colleen Reichmuth (C)

Long Marine Laboratory, Institute of Marine Sciences, University of California Santa Cruz, Santa Cruz, California, USA.

W Tecumseh Fitch (WT)

Department of Behavioral and Cognitive Biology, Vienna CogSciHub, University of Vienna, Vienna, Austria.

Andrea Ravignani (A)

Comparative Bioacoustics Research Group, Max Planck Institute for Psycholinguistics, Nijmegen, the Netherlands.
Department of Human Neurosciences, Sapienza University of Rome, Rome, Italy.
Center for Music in the Brain, Department of Clinical Medicine, Aarhus University, Aarhus, Denmark.

Classifications MeSH