Anatomical basis of lingual hydrostatic deformation

SUMMARY The mammalian tongue is believed to fall into a class of organs known as muscular hydrostats, organs for which muscle contraction both generates and provides the skeletal support for motion. We propose that the myoarchitecture of the tongue, consisting of intricate arrays of muscular fibers, forms the structural basis for hydrostatic deformation. Owing to the fact that maximal diffusion of the ubiquitous water molecule occurs orthogonal to the short axis of most fiber-type cells, diffusion-weighted magnetic resonance imaging (MRI) measurements can be used to derive information regarding 3-D fiber orientation in situ. Image data obtained in this manner suggest that the tongue consists of a complex juxtaposition of muscle fibers oriented in orthogonal arrays, which provide the basis for multidirectional contraction and isovolemic deformation. From a mechanical perspective, the lingual tissue may be considered as set of continuous coupled units of compression and expansion from which 3-D strain maps may be derived. Such functional data demonstrate that during physiological movements, such as protrusion, bending and swallowing, hydrostatic deformation occurs via synergistic contractions of orthogonally aligned intrinsic and extrinsic fibers. Lingual deformation can thus be represented in terms of models demonstrating that synergistic contraction of fibers at orthogonal or near-orthogonal directions to each other is a necessary condition for volume-conserving deformation. Evidence is provided in support of the supposition that hydrostatic deformation is based on the contraction of orthogonally aligned intramural fibers functioning as a mechanical continuum.

[1]  Thomas Benner,et al.  Mapping complex myoarchitecture in the bovine tongue with diffusion-spectrum magnetic resonance imaging. , 2006, Biophysical journal.

[2]  I. Sanders,et al.  Neuromuscular organization of the canine tongue , 1999, The Anatomical record.

[3]  R. Fregosi,et al.  Coordination of intrinsic and extrinsic tongue muscles during spontaneous breathing in the rat. , 2004, Journal of applied physiology.

[4]  Wolf-Jürgen Beyn,et al.  Simulating the motion of the leech: A biomechanical application of DAEs , 1998, Numerical Algorithms.

[5]  W. Beyn,et al.  Computer simulation of the hydrostatic skeleton. The physical equivalent, mathematics and application to worm-like forms. , 1989, Journal of theoretical biology.

[6]  R. Gilbert,et al.  Patterns of lingual tissue deformation associated with bolus containment and propulsion during deglutition as determined by echo‐planar MRI , 1998, Journal of magnetic resonance imaging : JMRI.

[7]  V. Wedeen,et al.  Determination of lingual myoarchitecture in whole tissue by NMR imaging of anisotropic water diffusion. , 1998, American journal of physiology. Gastrointestinal and liver physiology.

[8]  W. Kristan,et al.  A model of the hydrostatic skeleton of the leech. , 1996, Journal of theoretical biology.

[9]  V. Wedeen,et al.  Diffusion MRI of Complex Neural Architecture , 2003, Neuron.

[10]  V J Napadow,et al.  Demonstration of primary and secondary muscle fiber architecture of the bovine tongue by diffusion tensor magnetic resonance imaging. , 2001, Biophysical journal.

[11]  R. Wilhelms-Tricarico Physiological modeling of speech production: methods for modeling soft-tissue articulators. , 1995, The Journal of the Acoustical Society of America.

[12]  A. Thexton,et al.  The electromyographic activities of jaw and hyoid musculature in different ingestive behaviours in the cat. , 1994, Archives of oral biology.

[13]  K. Nishikawa Neuromuscular control of prey capture in frogs. , 1999, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[14]  H. Takemoto,et al.  Morphological analyses of the human tongue musculature for three-dimensional modeling. , 2001, Journal of speech, language, and hearing research : JSLHR.

[15]  Tamar Flash,et al.  Dynamic model of the octopus arm. I. Biomechanics of the octopus reaching movement. , 2005, Journal of neurophysiology.

[16]  K. Hiiemae,et al.  The Effect of Food Consistency upon Jaw Movement in the Macaque: A Cineradiographic Study , 1997, Journal of dental research.

[17]  E. Stejskal Use of Spin Echoes in a Pulsed Magnetic‐Field Gradient to Study Anisotropic, Restricted Diffusion and Flow , 1965 .

[18]  A. Thexton,et al.  Tongue movement of the cat during lapping. , 1988, Archives of oral biology.

[19]  Yohan Payan,et al.  A control model of human tongue movements in speech , 1997, Biological Cybernetics.

[20]  C G Peterfy,et al.  MR imaging. , 1996, Bailliere's clinical rheumatology.

[21]  Herrel,et al.  Kinematics of feeding in the lizard Agama stellio , 1996, The Journal of experimental biology.

[22]  J Prothero,et al.  Determination of relative fiber orientation in heart muscle: Methodological problems , 1992, The Anatomical record.

[23]  S. Herring,et al.  Somatotopic Organization of Perioral Musculature Innervation within the Pig Facial Motor Nucleus , 2005, Brain, Behavior and Evolution.

[24]  W. Kier,et al.  Morphology and mechanics of tongue movement in the African pig-nosed frog Hemisus marmoratum: a muscular hydrostatic model. , 1999, The Journal of experimental biology.

[25]  C. E. Jordan Coupling Internal and External Mechanics to Predict Swimming Behavior: A General Approach , 1996 .

[26]  Ching Yao,et al.  Validation of diffusion spectrum magnetic resonance imaging with manganese-enhanced rat optic tracts and ex vivo phantoms , 2003, NeuroImage.

[27]  D Paydarfar,et al.  Respiratory phase resetting and airflow changes induced by swallowing in humans. , 1995, The Journal of physiology.

[28]  V. Wedeen,et al.  Mapping fiber orientation spectra in cerebral white matter with Fourier-transform diffusion MRI , 2000 .

[29]  W. Kier,et al.  Tongues, tentacles and trunks: the biomechanics of movement in muscular‐hydrostats , 1985 .

[30]  J. Wilson,et al.  A continuum model of elephant trunks. , 1991, Journal of biomechanical engineering.

[31]  W. Kier,et al.  Functional design of tentacles in squid : Linking sarcomere ultrastructure to gross morphological dynamics , 1997 .

[32]  Tamar Flash,et al.  Dynamic model of the octopus arm. II. Control of reaching movements. , 2005, Journal of neurophysiology.

[33]  R. Gilbert,et al.  Quantitative relationship between liquid bolus flow and laryngeal closure during deglutition. , 1993, The American journal of physiology.

[34]  R M Weisskoff,et al.  Dynamic magnetic resonance imaging of vocal cord closure during deglutition. , 1995, Gastroenterology.

[35]  K. K. Smith,et al.  Morphology and function of the tongue and hyoid apparatus in Varanus (varanidae, lacertilia) , 1986, Journal of morphology.

[36]  J. Kellow Mastication and Swallowing , 1996 .

[37]  Universitiit Konstanz Computer Simulation of the Hydrostatic Skeleton. The Physical Equivalent, Mathematics and Application to Worm-like Forms , 1989 .

[38]  J Prothero,et al.  Coordinated three‐dimensional reconstruction from serial sections at macroscopic and microscopic levels of resolution: The human heart , 1987, The Anatomical record.

[39]  V J Napadow,et al.  Intramural mechanics of the human tongue in association with physiological deformations. , 1999, Journal of biomechanics.

[40]  W. Kier,et al.  Trunks, Tongues, and Tentacles: Moving with Skeletons of Muscle , 1989 .

[41]  P. Basser,et al.  MR diffusion tensor spectroscopy and imaging. , 1994, Biophysical journal.

[42]  A. Crompton,et al.  Coordination of mastication and swallowing , 1992, Dysphagia.

[43]  P J Kahrilas,et al.  Pharyngeal clearance during swallowing: a combined manometric and videofluoroscopic study. , 1992, Gastroenterology.

[44]  A. Thexton Mastication and swallowing: an overview , 1992, British Dental Journal.

[45]  J. Abbs,et al.  Quantitative morphology and histochemistry of intrinsic lingual muscle fibers in Macaca fascicularis. , 1996, Acta anatomica.

[46]  V. Napadow,et al.  A biomechanical model of sagittal tongue bending. , 2002, Journal of biomechanical engineering.

[47]  E C Wong,et al.  In vivo determination of the anisotropic diffusion of water and the T1 and T2 times in the rabbit lens by high-resolution magnetic resonance imaging. , 1993, Investigative ophthalmology & visual science.

[48]  J V Hajnal,et al.  MR imaging of anisotropically restricted diffusion of water in the nervous system: technical, anatomic, and pathologic considerations. , 1991, Journal of computer assisted tomography.

[49]  J. Kucharczyk,et al.  Anisotropy in diffusion‐weighted MRI , 1991, Magnetic resonance in medicine.

[50]  K. Hiiemae,et al.  Food Transport and Bolus Formation during Complete Feeding Sequences on Foods of Different Initial Consistency , 1999, Dysphagia.

[51]  A F Gmitro,et al.  Use of a projection reconstruction method to decrease motion sensitivity in diffusion‐weighted MRI , 1993, Magnetic resonance in medicine.

[52]  Maria Beatriz Duarte Gavião,et al.  MASTICATION AND SWALLOWING: INFLUENCE OF FLUID ADDITION TO FOODS , 2007, Journal of applied oral science : revista FOB.

[53]  J R McClung,et al.  Functional anatomy of the hypoglossal innervated muscles of the rat tongue: A model for elongation and protrusion of the mammalian tongue , 2000, The Anatomical record.

[54]  W. Kier,et al.  Functional morphology of the cephalopod buccal mass: A novel joint type , 2005, Journal of morphology.