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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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Citations
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Book ChapterDOI
06 Dec 2019

1 citations

01 Jan 2015
TL;DR: These analyses emphasise the importance of a multi‐site and hierarchical approach to understanding determinants of morphological variation, one which incorporates critical data on performance.
Abstract: Experimental analyses directly inform how an anatomical feature or complex functions during an organism's lifetime, which serves to increase the efficacy of comparative studies of living and fossil taxa. In the mammalian skull, food material properties and feeding behaviour have a pronounced influence on the development of the masticatory apparatus. Diet-related variation in loading magnitude and frequency induce a cascade of changes at the gross, tissue, cellular, protein and genetic levels, with such modelling and remodelling maintaining the integrity of oral structures vis-a-vis routine masticatory stresses. Ongoing integrative research using rabbit and rat models of long-term masticatory plasticity offers unique insight into the limitations of functional interpretations of fossilised remains. Given the general restriction of the palaeontological record to bony elements, we argue that failure to account for the disparity in the hierarchical network of responses of hard versus soft tissues may overestimate the magnitude of the adaptive divergence that is inferred from phenotypic differences. Second, we note that the developmental onset and duration of a loading stimulus associated with a given feeding behaviour can impart large effects on patterns of intraspecific variation that can mirror differences observed among taxa. Indeed, plasticity data are relevant to understanding evolutionary transformations because rabbits raised on different diets exhibit levels of morphological disparity comparable to those found between closely related primate species that vary in diet. Lastly, pronounced variation in joint form, and even joint function, can also characterise adult conspecifics that differ solely in age. In sum, our analyses emphasise the importance of a multi-site and hierarchical approach to understanding determinants of morphological variation, one which incorporates critical data on performance.

1 citations


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

  • ...The first study was carried out using rabbits raised for 3.4 months from weaning until subadulthood (4.5 months old) on either an under-use or over-use diet (Taylor et al., 2006; Ravosa et al., 2007a, 2008a,b; Menegaz et al., 2009, 2010)....

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  • ...…of rabbits subjected to elevated masticatory stress during biting and chewing of hay (Weijs & de Jongh, 1977), there is a stereotypical adaptive response with members of the ‘over-use’ dietary cohort developing larger and more biomineralised condylar heads (Ravosa et al., 2007a, 2010a) (Table 3)....

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  • ...…interpretation of past behaviours (e.g. White et al., 2009; Foth, Tischlinger & Rauhut, 2014), evidence on joint function and musculoskeletal biomechanics is inevitably lost because such functional systems are not wholly composed of mineralised tissues (Ravosa et al., 2007a; Holliday et al., 2010)....

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  • ...…latter is more mechanically challenging (i.e. tougher and with a higher elastic modulus) in terms of the forces and chewing cycles required for fragmentation along the postcanine dentition, thus inducing elevated osteogenesis of masticatory structures (Ravosa et al., 2007a; Menegaz et al., 2009)....

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  • ...…plasticity in rabbits is consistent with similar shorter-term experiments in other mammals (Beecher & Corruccini, 1981; Bouvier & Hylander, 1981, 1984, 1996; Beecher, Corruccini & Freeman, 1983; Yamada & Kimmel, 1991; He & Kiliaridis, 2003; Lieberman et al., 2004; Ravosa et al., 2007a, 2008a,b)....

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Dissertation
03 Oct 2013

1 citations

Journal ArticleDOI
TL;DR: In this article , the value of joint mobility as a lens through which to study articular form and function is discussed, and a deep understanding of the strength and causality of articular forms and function relationships is developed.
Abstract: Joints enable nearly all vertebrate animal motion, from feeding to locomotion. However, despite well over a century of arthrological research, we still understand very little about how the structure of joints relates to the kinematics they exhibit in life. This Commentary discusses the value of joint mobility as a lens through which to study articular form and function. By independently exploring form-mobility and mobility-function relationships and integrating the insights gained, we can develop a deep understanding of the strength and causality of articular form-function relationships. In turn, we will better illuminate the basics of 'how joints work' and be well positioned to tackle comparative investigations of the diverse repertoire of vertebrate animal motion.

1 citations

References
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Book
01 Jan 2003

4,928 citations

ReportDOI
01 Jan 1995

2,339 citations


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

  • ...Using the NIST tabulation of mass attenuation coefficients (Hubbell and Selzer, 2001), the effective energy for Northwestern University’s Scanco MicroCT 40 operated at 70·kV is about 30·keV....

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Journal ArticleDOI
TL;DR: For thirty-two areas of cartilage from nine osteo-arthritic and four "normal" femoral heads a histologic-histochemical grade was assigned as an index of severity of the osteo -arthritic process.
Abstract: For thirty-two areas of cartilage from nine osteo-arthritic and four "normal" femoral heads a histologic-histochemical grade was assigned as an index of severity of the osteo-arthritic process. The DNA and hexosamine concentrations were determined as indicators of cell density and polysaccharide con

2,168 citations


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

  • ...progressively deeper zones of TMJ articular cartilage are as follows: articular, filamentous network of elongate cells densely packed and tangentially arranged (high H2O, low proteoglycan, collagen rich); proliferative, ovoid or circular cells random in distribution (proteoglycan/protein production area); chondroblastic, large cell bundles arranged in columns (tidemark separates this from subjacent layer); hypertrophic chondrocyte/calcified, cells heavily encrusted in apatitic salts (Mankin et al., 1971; Newton and Nunamaker, 1985; Ostergaard et al., 1999)....

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  • ...Lower proteoglycan content throughout the FC pad and in the lower two layers of the condylar cartilage of O-diet rabbits mirrors findings for the articular surface of mammal limb elements, where age-related onset of cartilage degradation is linked to decreases in proteoglycan content (Mankin et al., 1971; Newton and Nunamaker, 1985; Haskin et al., 1995; Ostergaard et al., 1999)....

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  • ...…condylar cartilage of O-diet rabbits mirrors findings for the articular surface of mammal limb elements, where age-related onset of cartilage degradation is linked to decreases in proteoglycan content (Mankin et al., 1971; Newton and Nunamaker, 1985; Haskin et al., 1995; Ostergaard et al., 1999)....

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  • ...…(proteoglycan/protein production area); chondroblastic, large cell bundles arranged in columns (tidemark separates this from subjacent layer); hypertrophic chondrocyte/calcified, cells heavily encrusted in apatitic salts (Mankin et al., 1971; Newton and Nunamaker, 1985; Ostergaard et al., 1999)....

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  • ...…in cartilage composition reflect the early onset and progression of degenerative effects that compromise the structural integrity of a joint (Mankin et al., 1971; Newton and Nunamaker, 1985; Haskin et al., 1995; Kamelchuk and Major, 1995; Ishibashi et al., 1996; Ostergaard et al., 1999;…...

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Journal ArticleDOI
TL;DR: It is shown that VEGF-mediated capillary invasion is an essential signal that regulates growth plate morphogenesis and triggers cartilage remodeling and VEGf is anessential coordinator of chondrocyte death, chondROclast function, extracellular matrix remodeling, angiogenesis and bone formation in the growth plate.
Abstract: Hypertrophic chondrocytes in the epiphyseal growth plate express the angiogenic protein vascular endothelial growth factor (VEGF). To determine the role of VEGF in endochondral bone formation, we inactivated this factor through the systemic administration of a soluble receptor chimeric protein (Flt-(1-3)-IgG) to 24-day-old mice. Blood vessel invasion was almost completely suppressed, concomitant with impaired trabecular bone formation and expansion of hypertrophic chondrocyte zone. Recruitment and/or differentiation of chondroclasts, which express gelatinase B/matrix metalloproteinase-9, and resorption of terminal chondrocytes decreased. Although proliferation, differentiation and maturation of chondrocytes were apparently normal, resorption was inhibited. Cessation of the anti-VEGF treatment was followed by capillary invasion, restoration of bone growth, resorption of the hypertrophic cartilage and normalization of the growth plate architecture. These findings indicate that VEGF-mediated capillary invasion is an essential signal that regulates growth plate morphogenesis and triggers cartilage remodeling. Thus, VEGF is an essential coordinator of chondrocyte death, chondroclast function, extracellular matrix remodeling, angiogenesis and bone formation in the growth plate.

2,003 citations


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

  • ...In the growth plate of a joint, apoptosis is a normal terminal event for hypertrophic chondrocytes, and such cells express angiogenic factors initiating vascular invasion, erosion of mineralized cartilage and bone formation (Gerber et al., 1999)....

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Journal ArticleDOI
12 Oct 2001-Science
TL;DR: Phenotypic responses in species interactions represent modifications that can lead to reciprocal change in ecological time, altered community patterns, and expanded evolutionary potential of species.
Abstract: When individuals of two species interact, they can adjust their phenotypes in response to their respective partner, be they antagonists or mutualists. The reciprocal phenotypic change between individuals of interacting species can reflect an evolutionary response to spatial and temporal variation in species interactions and ecologically result in the structuring of food chains. The evolution of adaptive phenotypic plasticity has led to the success of organisms in novel habitats, and potentially contributes to genetic differentiation and speciation. Taken together, phenotypic responses in species interactions represent modifications that can lead to reciprocal change in ecological time, altered community patterns, and expanded evolutionary potential of species.

1,485 citations


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

  • ...628 Introduction Of late, adaptive plasticity has attracted considerable attention in myriad fields of biology (Gotthard and Nylin, 1995; Agrawal, 2001; Holden and Vogel, 2002; West-Eberhard, 2003)....

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