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Journal ArticleDOI

Pushing the limit: masticatory stress and adaptive plasticity in mammalian craniomandibular joints

TL;DR: It is argued that a critical component of current and future research on adaptive plasticity in the skull, and especially cranial joints, should employ a multifaceted characterization of a functional system, one that incorporates data on myriad tissues so as to evaluate the role of altered load versus differential tissue response on the anatomical, cellular and molecular processes that contribute to the strength of such composite structures.
Abstract: Excessive, repetitive and altered loading have been implicated in the initiation of a series of soft- and hard-tissue responses or ;functional adaptations' of masticatory and locomotor elements. Such adaptive plasticity in tissue types appears designed to maintain a sufficient safety factor, and thus the integrity of given element or system, for a predominant loading environment(s). Employing a mammalian species for which considerable in vivo data on masticatory behaviors are available, genetically similar domestic white rabbits were raised on diets of different mechanical properties so as to develop an experimental model of joint function in a normal range of physiological loads. These integrative experiments are used to unravel the dynamic inter-relationships among mechanical loading, tissue adaptive plasticity, norms of reaction and performance in two cranial joint systems: the mandibular symphysis and temporomandibular joint (TMJ). Here, we argue that a critical component of current and future research on adaptive plasticity in the skull, and especially cranial joints, should employ a multifaceted characterization of a functional system, one that incorporates data on myriad tissues so as to evaluate the role of altered load versus differential tissue response on the anatomical, cellular and molecular processes that contribute to the strength of such composite structures. Our study also suggests that the short-term duration of earlier analyses of cranial joint tissues may offer a limited notion of the complex process of developmental plasticity, especially as it relates to the effects of long-term variation in mechanical loads, when a joint is increasingly characterized by adaptive and degradative changes in tissue structure and composition. Indeed, it is likely that a component of the adaptive increases in rabbit TMJ and symphyseal proportions and biomineralization represent a compensatory mechanism to cartilage degradation that serves to maintain the overall functional integrity of each joint system. Therefore, while variation in cranial joint anatomy and performance among sister taxa is, in part, an epiphenomenon of interspecific differences in diet-induced masticatory stresses characterizing the individual ontogenies of the members of a species, this behavioral signal may be increasingly mitigated in over-loaded and perhaps older organisms by the interplay between adaptive and degradative tissue responses.

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TL;DR: In this article, the authors highlight recent advances in X-ray microcomputed tomography (microCT) as applied to materials, specifically advances made since the first materials microCT review appeared in Internati...
Abstract: This review highlights recent advances in X-ray microcomputed tomography (microCT) as applied to materials, specifically advances made since the first materials microCT review appeared in Internati...

470 citations

Journal ArticleDOI
TL;DR: Novel findings in biomedicine and developments in imaging and computer technologies are beginning to provide a vision of future innovations in the diagnostics and therapeutics of TMJ disorders, and the identification and use of local or systemic biomarkers to diagnose disease or monitor improvements in therapy.
Abstract: Because their etiologies and pathogenesis are poorly understood, temporomandibular joint (TMJ) diseases are difficult to diagnose and manage. All current approaches to treatments of TMJ diseases are largely palliative. Definitive and rational diagnoses or treatments can only be achieved through a comprehensive understanding of the etiologies, predisposing factors, and pathogenesis of TMJ diseases. While much work remains to be done in this field, novel findings in biomedicine and developments in imaging and computer technologies are beginning to provide us with a vision of future innovations in the diagnostics and therapeutics of TMJ disorders. These advances include the identification and use of local or systemic biomarkers to diagnose disease or monitor improvements in therapy; the use of imaging technologies for earlier and more sensitive diagnostics; and the use of biomedicine, biomimetics, and imaging to design and manufacture bioengineered joints. Such advances are likely to help to customize and enhance the quality of care we provide to patients with TMJ disorders.

218 citations

Journal Article
TL;DR: The data suggest that myostatin has direct effects on the proliferation and differentiation of osteoprogenitor cells, and that hisostatin antagonists and inhibitors are likely to enhance both muscle mass and bone strength.
Abstract: Myostatin (GDF-8) is a member of the transforming growth factor-beta (TGF-β) superfamily that is highly expressed in skeletal muscle, and myostatin loss-of-function leads to doubling of skeletal muscle mass. Myostatin-deficient mice have been used as a model for studying muscle-bone interactions, and here we review the skeletal phenotype associated with altered myostatin signaling. It is now known that myostatin is a key regulator of mesenchymal stem cell proliferation and differentiation, and mice lacking the myostatin gene show decreased body fat and a generalized increase in bone density and strength. The increase in bone density is observed in most anatomical regions, including the limbs, spine, and jaw, and myostatin inhibitors have been observed to significantly increase bone formation. Myostatin is also expressed in the early phases of fracture healing, and myostatin deficiency leads to increased fracture callus size and strength. Together, these data suggest that myostatin has direct effects on the proliferation and differentiation of osteoprogenitor cells, and that myostatin antagonists and inhibitors are likely to enhance both muscle mass and bone strength.

195 citations

Journal ArticleDOI
TL;DR: The osteological correlates and inferred soft tissue anatomy of the jaw muscles and relevant neurovasculature in the temporal region of the dinosaur head are presented to provide the anatomical foundation necessary for future analyses of skull function and evolution in an important vertebrate clade.
Abstract: Jaw muscles are key components of the head and critical to testing hypotheses of soft-tissue homology, skull function, and evolution. Dinosaurs evolved an extraordinary diversity of cranial forms adapted to a variety of feeding behaviors. However, disparate evolutionary transformations in head shape and function among dinosaurs and their living relatives, birds and crocodylians, impair straightforward reconstructions of muscles, and other important cephalic soft tissues. This study presents the osteological correlates and inferred soft tissue anatomy of the jaw muscles and relevant neurovasculature in the temporal region of the dinosaur head. Hypotheses of jaw muscle homology were tested across a broad range archosaur and sauropsid taxa to more accurately infer muscle attachments in the adductor chambers of non-avian dinosaurs. Many dinosaurs likely possessed m. levator pterygoideus, a trait shared with lepidosaurs but not extant archosaurs. Several major clades of dinosaurs (e.g., Ornithopoda, Ceratopsidae, Sauropoda) eliminated the epipterygoid, thus impacting interpretations of m. pseudotemporalis profundus. M. pseudotemporalis superficialis most likely attached to the caudoventral surface of the laterosphenoid, a trait shared with extant archosaurs. Although mm. adductor mandibulae externus profundus and medialis likely attached to the caudal half of the dorsotemporal fossa and coronoid process, clear osteological correlates separating the individual bellies are rare. Most dinosaur clades possess osteological correlates indicative of a pterygoideus ventralis muscle that attaches to the lateral surface of the mandible, although the muscle may have extended as far as the jugal in some taxa (e.g., hadrosaurs, tyrannosaurs). The cranial and mandibular attachments of mm adductor mandibulae externus superficialis and adductor mandibulae posterior were consistent across all taxa studied. These new data greatly increase the interpretive resolution of head anatomy in dinosaurs and provide the anatomical foundation necessary for future analyses of skull function and evolution in an important vertebrate clade.

148 citations


Cites background from "Pushing the limit: masticatory stre..."

  • ...Finally, feeding behavior and connective tissue adaptive plasticity are major factors involved in the structure and function of jaw muscles and the skull (Ravosa et al., 2007)....

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References
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Journal ArticleDOI

37 citations


"Pushing the limit: masticatory stre..." refers background in this paper

  • ...The mandibular symphysis and TMJ are highly specialized joints capable of both rotational and translational movements, and thus encounter multidirectional compressive, shear and tensile forces during biting and chewing (Rigler and Mlinsek, 1968; Beecher, 1977; Beecher, 1979; Hylander, 1979a; Hylander, 1979b; Hylander, 1979c; Hylander, 1992; Scapino, 1981; Ravosa and Hogue, 2004)....

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  • ...In rabbits and other mammals, this results in elevated peak strains along the mandible and higher TMJ reaction forces (Weijs and de Jongh, 1977; Hylander, 1979a; Hylander, 1979b; Hylander, 1979c; Hylander, 1992; Hylander et al., 1998; Ravosa et al., 2000)....

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  • ...…and translational movements, and thus encounter multidirectional compressive, shear and tensile forces during biting and chewing (Rigler and Mlinsek, 1968; Beecher, 1977; Beecher, 1979; Hylander, 1979a; Hylander, 1979b; Hylander, 1979c; Hylander, 1992; Scapino, 1981; Ravosa and Hogue, 2004)....

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Journal ArticleDOI
TL;DR: The results suggest that during development the possibility of the system to generate large bite forces is increased at the cost of a restriction in the range of jaw excursion and that a restriction takes place in therange of possible force directions that can be exerted at the molars.
Abstract: Using dissection, biometry, and two three-dimensional mechanical models, the postnatal changes of the rabbit masticatory muscles were studied by analyzing their three-dimensional orientation, their strength and fiber lengths, and certain functional consequences of these changes. The first mechanical model uses length-tension relationships of the muscles and predicts the maximum bite force as a function of mandibular position. It shows that young rabbits are able to generate large bite forces at a wider gape than adult animals and that the forces are directed more vertically. In spite of the postnatal changes the mechanical advantage of the system remains about equal. However, the muscles are reoriented so that they exert a larger degree of parallel action, suggesting a larger bite force magnitude but a smaller range of bite force directions. The second model predicts this range. It shows that during postnatal development a relative gain occurs in the possibilities for the system to exert forces directed rostrodorsally. In all other directions the capability to exert force decreases. The results suggest that during development the possibility of the system to generate large bite forces is increased at the cost of a restriction in the range of jaw excursion and that a restriction takes place in the range of possible force directions that can be exerted at the molars.

36 citations


"Pushing the limit: masticatory stre..." refers background in this paper

  • ...Watts, 1985; Tarnaud, 2004) and develop ‘adult’ jaw-adductor activity patterns (Herring and Wineski, 1986; Weijs et al., 1987; Herring et al., 1991; Iinuma et al., 1991; Langenbach et al., 1991; Langenbach et al., 1992; Langenbach et al., 2001; Westneat and Hall, 1992; Huang et al., 1994), with associated skeletal and soft-tissue responses to ‘adult’ jaw-loading regimes (Ravosa, 1991a; Ravosa, 1992; Ravosa, 1996; Ravosa, 1999; Cole, 1992; Biknevicius and Leigh, 1997; Vinyard and Ravosa, 1998; Taylor et al....

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  • ...…2004) and develop ‘adult’ jaw-adductor activity patterns (Herring and Wineski, 1986; Weijs et al., 1987; Herring et al., 1991; Iinuma et al., 1991; Langenbach et al., 1991; Langenbach et al., 1992; Langenbach et al., 2001; Westneat and Hall, 1992; Huang et al., 1994), with associated skeletal…...

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  • ...…muscle activity, jaw-kinematic and jaw-loading patterns, masticatory function during ontogeny, and the link between masticatory behaviors and diet (Weijs et al., 1987; Weijs et al., 1989; Langenbach et al., 1991; Langenbach et al., 1992; Langenbach et al., 2001; Langenbach and van Eijden, 2001)....

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Journal ArticleDOI
TL;DR: In dogs the earlier teeth erupted, the earlier the dominant oral behavior was changed from suckling to mastication, and concomitantly the dominant muscle for the oral behaviorwas changed from the temporal to the masseter muscle.

36 citations


"Pushing the limit: masticatory stre..." refers background in this paper

  • ...Watts, 1985; Tarnaud, 2004) and develop ‘adult’ jaw-adductor activity patterns (Herring and Wineski, 1986; Weijs et al., 1987; Herring et al., 1991; Iinuma et al., 1991; Langenbach et al., 1991; Langenbach et al., 1992; Langenbach et al., 2001; Westneat and Hall, 1992; Huang et al., 1994), with associated skeletal and soft-tissue responses to ‘adult’ jaw-loading regimes (Ravosa, 1991a; Ravosa, 1992; Ravosa, 1996; Ravosa, 1999; Cole, 1992; Biknevicius and Leigh, 1997; Vinyard and Ravosa, 1998; Taylor et al....

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  • ...…Watts, 1985; Tarnaud, 2004) and develop ‘adult’ jaw-adductor activity patterns (Herring and Wineski, 1986; Weijs et al., 1987; Herring et al., 1991; Iinuma et al., 1991; Langenbach et al., 1991; Langenbach et al., 1992; Langenbach et al., 2001; Westneat and Hall, 1992; Huang et al., 1994),…...

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Journal ArticleDOI
TL;DR: Postnatal development enhances, but does not soley contribute to, the biomechanical differences in the jaws of these species; basic differences in jaw construction between Crocuta and Puma appear to develop prenatally as they are largely in place at birth.

35 citations


"Pushing the limit: masticatory stre..." refers background in this paper

  • ...…Langenbach et al., 2001; Westneat and Hall, 1992; Huang et al., 1994), with associated skeletal and soft-tissue responses to ‘adult’ jaw-loading regimes (Ravosa, 1991a; Ravosa, 1992; Ravosa, 1996; Ravosa, 1999; Cole, 1992; Biknevicius and Leigh, 1997; Vinyard and Ravosa, 1998; Taylor et al., 2006)....

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  • ...Once weaned, mammals ingest ‘adult’ food items (e.g. Watts, 1985; Tarnaud, 2004) and develop ‘adult’ jaw-adductor activity patterns (Herring and Wineski, 1986; Weijs et al., 1987; Herring et al., 1991; Iinuma et al., 1991; Langenbach et al., 1991; Langenbach et al., 1992; Langenbach et al., 2001; Westneat and Hall, 1992; Huang et al., 1994), with associated skeletal and soft-tissue responses to ‘adult’ jaw-loading regimes (Ravosa, 1991a; Ravosa, 1992; Ravosa, 1996; Ravosa, 1999; Cole, 1992; Biknevicius and Leigh, 1997; Vinyard and Ravosa, 1998; Taylor et al., 2006)....

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  • ...Cole, T. M. (1992)....

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Journal ArticleDOI
TL;DR: The change in PCSA but not fiber length suggests that variation in dietary consistency has an impact on maximum force production but not necessarily on excursion or contraction velocity.
Abstract: Dietary consistency has been shown to influence cross-sectional area and fiber type composition of the masticatory muscles. However, little is known about the effects of dietary consistency on masticatory muscle fiber architecture. In this study, we explore the effects of dietary consistency on the internal architecture of rabbit masseter muscle. Because activity patterns of the rabbit chewing muscles show inter- and intramuscular heterogeneity, we evaluate if alterations in fiber architecture are homogeneous across various portions of the superficial masseter muscle. We compared masseter muscle fiber architecture between two groups of weanling rabbits raised on different diets for 105 days. One group was raised on a diet of ground rabbit pellets to model underuse of the masticatory complex, while the other group was fed a diet of intact pellets and hay blocks to model an overuse diet. In all portions of the superficial masseter, physiological cross-sectional areas (PCSAs) are greater in the overuse compared to underuse diet rabbits. Thus, the mechanical demands for larger muscle and bite forces associated with early and prolonged exposure to a tough diet are met by an increase in PCSA of the superficial masseter. The larger PCSA is due entirely to increased muscle mass, as the two rabbit groups show no differences in either fiber length or angle of pinnation. Thus, increasing pinnation angle is not a necessary biomechanical solution to improving muscle and bite force during growth. The change in PCSA but not fiber length suggests that variation in dietary consistency has an impact on maximum force production but not necessarily on excursion or contraction velocity.

35 citations


"Pushing the limit: masticatory stre..." refers background in this paper

  • ...Once weaned, mammals ingest ‘adult’ food items (e.g. Watts, 1985; Tarnaud, 2004) and develop ‘adult’ jaw-adductor activity patterns (Herring and Wineski, 1986; Weijs et al., 1987; Herring et al., 1991; Iinuma et al., 1991; Langenbach et al., 1991; Langenbach et al., 1992; Langenbach et al., 2001; Westneat and Hall, 1992; Huang et al., 1994), with associated skeletal and soft-tissue responses to ‘adult’ jaw-loading regimes (Ravosa, 1991a; Ravosa, 1992; Ravosa, 1996; Ravosa, 1999; Cole, 1992; Biknevicius and Leigh, 1997; Vinyard and Ravosa, 1998; Taylor et al., 2006)....

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  • ...Based largely on short experimental periods in growing mammals (<2 months), these studies support the hypothesis that altered, excessive and/or repetitive forces induce secondary osteonal remodeling of mandibular cortical bone and chondroblastic activity of articular cartilage, a suite of physiological responses or functional adaptations that maintain a sufficient safety factor for the tissues of a cranial element or joint complex to routine peak masticatory loads (cf. Lanyon and Rubin, 1985; Biewener, 1993; Bouvier and Hylander, 1996a; Bouvier and Hylander, 1996b; Vinyard and Ravosa, 1998; Hamrick, 1999; Ravosa et al., 2000)....

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  • ...Results suggest that evolutionary variation in symphysis and TMJ morphology, and thus by inference joint performance, among sister taxa is in part an epiphenomenon of interspecific differences in (dietinduced) jaw-loading patterns characterizing the individual ontogenies of the members of a species (Vinyard and Ravosa, 1998; Ravosa and Hogue, 2004)....

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  • ...…Langenbach et al., 2001; Westneat and Hall, 1992; Huang et al., 1994), with associated skeletal and soft-tissue responses to ‘adult’ jaw-loading regimes (Ravosa, 1991a; Ravosa, 1992; Ravosa, 1996; Ravosa, 1999; Cole, 1992; Biknevicius and Leigh, 1997; Vinyard and Ravosa, 1998; Taylor et al., 2006)....

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  • ...Thus, it is intimately related to the concept of functional adaptation, which typically refers to the dynamic coordinated series of cellular, tissue and biochemical processes of modeling and remodeling that occur to maintain a sufficient safety factor of a given element or system to routine peak stresses (Lanyon and Rubin, 1985; Biewener, 1993; Bouvier and Hylander, 1996a; Bouvier and Hylander, 1996b; Vinyard and Ravosa, 1998; Hamrick, 1999)....

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