Functional anatomy of the hypoglossal innervated muscles of the rat tongue: A model for elongation and protrusion of the mammalian tongue

McClung, J. Ross; Goldberg, Stephen J.

doi:10.1002/1097-0185(20001201)260:4<378::aid-ar70>3.0.co;2-a

Cited by 97 publications

(93 citation statements)

References 22 publications

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“…In mammalian tongues, the intrinsic musculature typically includes transverse muscle fibers in alternating sheets of parallel muscle fibers oriented more or less vertically and horizontally and longitudinal muscle fibers in bundles around the central core of transverse muscle fibers. Mammalian tongue deformations and many types of tongue movement are generated according to the general principles outlined above for muscular hydrostats (Bailey and Fregosi, 2004;Gilbert et al, 2007;Kier and Smith, 1985;McClung and Goldberg, 2000;Napadow et al, 1999). Muscular-hydrostatic mechanisms may also be important in the support and movement of many lizard tongues and some frog tongues (Chiel et al, 1992;Nishikawa et al, 1999;Smith and Mackay, 1990;Smith, 1986;van Leeuwen, 1997;van Leeuwen et al, 2000;Wainwright and Bennett, 1992a;Wainwright and Bennett, 1992b).…”

Section: W M Kiermentioning

confidence: 99%

The diversity of hydrostatic skeletons

Kier

2012

Journal of Experimental Biology

202

158

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Summary A remarkably diverse group of organisms rely on a hydrostatic skeleton for support, movement, muscular antagonism and the amplification of the force and displacement of muscle contraction. In hydrostatic skeletons, force is transmitted not through rigid skeletal elements but instead by internal pressure. Functioning of these systems depends on the fact that they are essentially constant in volume as they consist of relatively incompressible fluids and tissue. Contraction of muscle and the resulting decrease in one of the dimensions thus results in an increase in another dimension. By actively (with muscle) or passively (with connective tissue) controlling the various dimensions, a wide array of deformations, movements and changes in stiffness can be created. An amazing range of animals and animal structures rely on this form of skeletal support, including anemones and other polyps, the extremely diverse wormlike invertebrates, the tube feet of echinoderms, mammalian and turtle penises, the feet of burrowing bivalves and snails, and the legs of spiders. In addition, there are structures such as the arms and tentacles of cephalopods, the tongue of mammals and the trunk of the elephant that also rely on hydrostatic skeletal support but lack the fluid-filled cavities that characterize this skeletal type. Although we normally consider arthropods to rely on a rigid exoskeleton, a hydrostatic skeleton provides skeletal support immediately following molting and also during the larval stage for many insects. Thus, the majority of animals on earth rely on hydrostatic skeletons.

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Section: W M Kiermentioning

confidence: 99%

The diversity of hydrostatic skeletons

Kier

2012

Journal of Experimental Biology

202

158

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“…In order to achieve this function, the tissue must possess muscle fibers that are arrayed across a large spectrum of angles and exhibit the capacity for multidirectional contraction. Hydrostatic deformation has been inferred based on tissue anatomy (Uyeno and Kier, 2005;Marshall et al, 2005), gross motor behavior (Nishikawa, 1999;McClung and Goldberg, 2000) and electromyographic recordings (Bailey and Fregosi, 2001). We propose that lingual hydrostatic deformation is best considered mechanically if the tissue is portrayed as a set of coupled units of compression and expansion.…”

Section: Lingual Myoarchitecture and Hydrostatic Deformationmentioning

confidence: 99%

Anatomical basis of lingual hydrostatic deformation

Gilbert

Napadow

Gaige

et al. 2007

Journal of Experimental Biology

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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.

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“…The ability of the prion agent to establish infection in brain nuclei that contribute to, or synapse with, the four cranial nerves that innervate the tongue suggests that this could be a pathway for centrifugal prion agent spread. The tongue is one of the most densely innervated extraneural tissues in the human body, with a very high concentration of both motor and sensory axons (28,30,35,36,41). Anterograde prion transport within the hypoglossal nerve would be expected to result in prion infection of the lingual muscles, while transganglionic transport within the trigeminal, facial, and glossopharyngeal nerves could result in prion spread to the sensory fibers in the tongue.…”

Section: Fig 4 Confocal Microscopy Of Prpmentioning

confidence: 99%

Prion Infection of Skeletal Muscle Cells and Papillae in the Tongue

Mulcahy¹,

Bartz²,

Kincaid

et al. 2004

J Virol

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The presence of the prion agent in skeletal muscle is thought to be due to the infection of nerve fibers located within the muscle. We report here that the pathological isoform of the prion protein, PrP Sc , accumulates within skeletal muscle cells, in addition to axons, in the tongue of hamsters following intralingual and intracerebral inoculation of the HY strain of the transmissible mink encephalopathy agent. Localization of PrP Sc to the neuromuscular junction suggests that this synapse is a site for prion agent spread between motor axon terminals and muscle cells. Following intracerebral inoculation, the majority of PrP Sc in the tongue was found in the lamina propria, where it was associated with sensory nerve fibers in the core of the lingual papillae. PrP Sc staining was also identified in the stratified squamous epithelium of the lingual mucosa. These findings indicate that prion infection of skeletal muscle cells and the epithelial layer in the tongue can be established following the spread of the prion agent from nerve terminals and/or axons that innervate the tongue. Our data suggest that ingestion of meat products containing prion-infected tongue could result in human exposure to the prion agent, while sloughing of prion-infected epithelial cells at the mucosal surface of the tongue could be a mechanism for prion agent shedding and subsequent prion transmission in animals.

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Functional anatomy of the hypoglossal innervated muscles of the rat tongue: A model for elongation and protrusion of the mammalian tongue

Cited by 97 publications

References 22 publications

The diversity of hydrostatic skeletons

The diversity of hydrostatic skeletons

Anatomical basis of lingual hydrostatic deformation

Prion Infection of Skeletal Muscle Cells and Papillae in the Tongue

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