Masticatory loading, function, and plasticity: A microanatomical analysis of mammalian circumorbital soft-tissue structures

Anatomical Record

Volumn 293, Issue 4, 2010, Pages 642-650

  Jašarević, Eldin ^a   Ning, Jie ^a   Daniel, Ashley N ^a   Menegaz, Rachel A ^a   Johnson, Jeffrey J ^a   Stack, M Sharon ^a   Ravosa, Matthew J ^a  

^a University of Missouri   (United States)

Author keywords

Adaptive plasticity; Circumorbital morphology; Dietary properties; Histology; Immunohistochemistry; Masticatory stresses loads; Ontogeny; Rabbit

Indexed keywords

COLLAGEN; COLLAGEN TYPE 2; PROTEOGLYCAN;

ANATOMY; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DIET; EUTHANASIA; FEEDING BEHAVIOR; FIBROCARTILAGE; FRONTAL BONE; MAMMAL; MASTICATION; NONHUMAN; ORBIT; PLASTICITY; PRIMATE; PRIORITY JOURNAL; PROTEIN EXPRESSION; RABBIT; SOFT TISSUE; ZYGOMA;

ADAPTATION, PHYSIOLOGICAL; ANIMALS; BIOMECHANICS; BITE FORCE; COLLAGEN; DIET; ELASTIC CARTILAGE; MODELS, ANIMAL; MUSCLE FIBERS, SKELETAL; MUSCULOSKELETAL DEVELOPMENT; ORBIT; PROTEOGLYCANS; RABBITS;

MAMMALIA; ORYCTOLAGUS CUNICULUS; PRIMATES;

EID: 77950879197     PISSN: 19328486     EISSN: 19328494     Source Type: Journal    
DOI: 10.1002/ar.21135     Document Type: Article

References (73)

1. Beecher RM, Corruccini RS. 1981. Effects of dietary consistency on craniofacial and occlusal development in the rat. Angle Orthod 51:61-69.
2. Beecher RM, Corruccini RS, Freeman M. 1983. Craniofacial correlates of dietary consistency in a nonhuman primate. J Craniofac Genet Dev Biol 3:193-202.
3. Benjamin M, Ralphs JR. 1998. Fibrocartilage in tendons and ligaments - an adaptation to compressive load. J Anat 193:481-494. (Pubitemid 29026948)
4. Benjamin M, Ralphs JR. 2004. Biology of fibrocartilage cells. In: Jeon KW, editor. International review cytology: a review of cell biology. San Diego: Elsevier. p 1-45.
5. Bloch JI, Boyer DM. 2002. Grasping primate origins. Science 298: 1606-1610.
6. Bookstein F, Schafer K, Prossinger H, Seidler H, Fieder M, Stringer C, Weber GW, Arsuaga JL, Slice DE, Rohlf FJ, Recheis W, Mariam AJ, Marcus LF. 1999. Comparing frontal cranial profiles in archaic and modern Homo by morphometric analysis. Anat Rec 257:217-224. (Pubitemid 30032807)
7. Bouvier M. 1987. Variation in alkaline-phosphatase activity with changing load on the mandibular condylar cartilage in the rat. Arch Oral Biol 32:671-675.
8. Bouvier M. 1988. Effects of age on the ability of the rat temporo-mandibular joint to respond to changing functional demands. J Dent Res 67:1206-1212.
9. Bouvier M, Hylander WL. 1981. Effect of bone strain on cortical bone structure in macaques Macaca mulatta. J Morphol 167:1-12. (Pubitemid 11021544)
10. Bouvier M, Hylander WL. 1982. The effect of dietary consistency on morphology of the mandibular condylar cartilage in young macaques (Macaca mulatta). In: Dixon AD, Sarnat BG, editors. Factors and mechanisms influencing bone growth. New York: AR Liss. p 569-579.
11. Bouvier M, Hylander WL. 1984. The effect of dietary consistency on gross and histologic morphology in the craniofacial region of young rats. Am J Anat 170:117-126. (Pubitemid 14101477)
12. Bouvier M, Hylander WL. 1996a. The mechanical or metabolic function of secondary osteonal bone in the monkey Macaca fascicularis. Arch Oral Biol 41:941-950. (Pubitemid 27066625)
13. Bouvier M, Hylander WL. 1996b. Strain gradients, age, and levels of modeling and remodeling in the facial bones of Macaca fascicularis. In: Davidovitch Z, Norton LA, editors. The biological mechanisms of tooth movement and craniofacial adaptation. Boston: Harvard Society for the Advancement of Orthodontics. p 407-412.
14. Carter D. 1987. Mechanical loading history and skeletal biology. J Biomech 20:1095-1109. (Pubitemid 18560645)
15. Cartmill M. 1970. The orbits of arboreal mammals: a reassessment of the arboreal theory of primate evolution. Ph.D. Dissertation, University of Chicago, Chicago, IL.
16. Cartmill M. 1972. Arboreal adaptations and the origin of the order primates. In: Tuttle RH, editor. The functional and evolutionary biology of primates. New York: Aldine de Gruyter. p 97-122.
17. Cartmill M. 1974. Rethinking primate origins. Science 184:436-443.
18. Cartmill M. 1980. Morphology, function, and evolution of the anthropoid postorbital septum. In: Ciochon RL, Chiarelli AB, editors. Evolutionary biology of the new world monkeys and continental drift. New York: Plenum Press. p 243-274.
19. Cartmill M. 1992. New views on primate origins. Evol Anthropol 1: 105-111.
20. Cox PG. 2008. A quantitative analysis of the Eutherian orbit: correlations with masticatory apparatus. Biol Rev 83:35-69.
21. Crompton AW, Lieberman DE, Aboelela S. 2006. Tooth orientation during occlusion and the functional significance of condylar translation in primates and herbivores. In: Carrano MT, Gaudin TJ, Blob RW, Wible JR, editors. Amniote paleobiology: perspectives on the evolution of mammals, birds, and reptiles. Chicago, IL: University of Chicago Press. p 367-388.
22. Gotthard K, Nylin S. 1995. Adaptive plasticity and plasticity as an adaptation: a selective review of plasticity in animal morphology and life history. Oikos 74:3-17. (Pubitemid 3005220)
23. Greaves WS. 1985. The mammalian postorbital bar as a torsion-resisting helical strut. J Zool 207:125-136.
24. Greaves WS. 1991. A relationship between premolar loss and law elongation in selenodont artiodactyls. Zool J Linn Soc 101: 121-129.
25. Greaves WS. 1995. Functional predictions from theoretical models of the skull and jaws in reptiles and mammals. In: Thomason JJ, editor. Functional morphology in vertebrate paleontology. Cambridge: Cambridge University Press. p 99-105.
26. Hinton RJ, McNamara JA. 1984. Effect of age on the adaptive response of the adult temporomandibular joint. A study of induced protrusion in Macaca mulatta. Angle Orthod 54:154-162.
27. Hirano T, Burr DB, Cain RL, Hock JM. 2000. Changes in geometry and cortical porosity in adult, ovary-intact rabbits after 5 months treatment with LY333334 (hPTH 1-34). Calcif Tissue Int 66:456-460. (Pubitemid 30368377)
28. Hylander WL, Johnson KR. 1997. In vivo bone strain patterns in the zygomatic arch of macaques and the significance of these patterns for functional interpretations of craniofacial form. Am J Phys Anthropol 102:203-232.
29. Hylander WL, Johnson KR, Crompton AW. 1987. Loading patterns and jaw movements during mastication in Macaca fascicularis: a bone-strain, electromyographic and cineradiographic analysis. Am J Phys Anthropol 72:287-314.
30. Hylander WL, Johnson KR, Crompton AW. 1992. Muscle force recruitment and biomechanical modeling: an analysis of masseter muscle function during mastication in Macaca fascicularis. Am J Phys Anthropol 88:365-387.
31. Hylander WL, Picq PG, Johnson KR. 1991a. Masticatory-stress hypotheses and the supraorbital region of primates. Am J Phys Anthropol 86:1-36.
32. Hylander WL, Picq PG, Johnson KR. 1991b. Function of the supraorbital region of primates. Arch Oral Biol 36:273-281.
33. Hylander WL, Ravosa MJ, Ross CF, Johnson KR. 1998. Mandibular corpus strain in primates: further evidence for a functional link between symphyseal fusion and jaw-adductor muscle force. Am J Phys Anthropol 107:257-271.
34. Hylander WL, Ravosa MJ, Ross CF, Wall CE, Johnson KR. 2000. Symphyseal fusion and jaw-adductor muscle force: an EMG study. Am J Phys Anthropol 113:469-492.
35. Junqueira LC, Bignolas G, Brentani RR. 1979. Picrosirius staining plus polarization microscopy, a specific method for collagen detection in tissue sections. Histochem J 11:447-455. (Pubitemid 9238595)
36. Kiernan JA. 1999. Histological and histochemical methods. 3rd ed. Boston, MA: Butterworh-Heinemann.
37. Kiliaridis S, Engström C, Thilander B. 1985. The relationship between masticatory function and craniofacial morphology. I. A cephalometric longitudinal analysis in the growing rat fed a soft diet. Eur J Orthod 7:273-283. (Pubitemid 16257756)
38. Langenbach GE, Brugman P, Weijs WA. 1992. Preweaning feeding mechanisms in the rabbit. J Dev Physiol 18:253-261.
39. Langenbach GEJ, van Eijden TMGJ. 2001. Mammalian feeding motor patterns. Am Zool 41:1338-1351.
40. Langenbach GEJ, Weijs WA, Brugman P, van Eijden TMGJ. 2001. A longitudinal electromyographic study of the postnatal maturation of mastication in the rabbit. Arch Oral Biol 46:811-820. (Pubitemid 32744418)
41. Langenbach GE, Weijs WA, Koolstra JH. 1991. Biomechanical changes in the rabbit masticatory system during postnatal development. Anat Rec 230:406-416.
42. Lemme M, Liu ZJ, Rafferty KL, Herring SW. 2005. In vivo postorbital ligament deformation: temporalis incursion or masseteric pull. Int Assoc Dent Res 83:2519.
43. MacLean J, Lee CR, Grad S, Ito K, Alini M, Iatridis JC. 2003. Effects of immobilization and dynamic compression on intervertebral disc cell gene expression in vivo. Spine 28:973-981. (Pubitemid 36583325)
44. Menegaz RA, Kirk EC. 2009. Septa and processes: convergent evolution of the orbit in haplorhine primates and strigiform birds. J Hum Evol 57:672-687.
45. Menegaz RA, Sublett SV, Figueroa SD, Hoffman TJ, Ravosa MJ. 2009. Phenotypic plasticity and function of the hard palate in growing rabbits. Anat Rec A 292:277-284.
46. Menegaz RA, Sublett SV, Figueroa SD, Hoffman TJ, Ravosa MJ, Aldridge K. 2010. Evidence for the influence of diet on cranial form and robusticity. Anat Rec 293:630-641.
47. Meyer A. 1987. Phenotypic plasticity and heterochrony in Cichlasoma managuense (Pisces, Cichlidae) and their implications for speciation in cichlid fishes. Evol 41:1357-1369.
48. Noble VE, Kowalski EM, Ravosa MJ. 2000. Orbit orientation and the function of the mammalian postorbital bar. J Zool 250:405-418.
49. Provenzano PP, Vanderby R, Jr. 2006. Collagen fibril morphology and organization: implications for force transmission in ligament and tendon. Matrix Biol 25:71-84.
50. Ravosa MJ, Johnson KR, Hylander WL. 2000a. Strain in the galago facial skull. J Morphol 244:51-66.
51. Ravosa MJ, Kunwar R, Stock SR, Stack MS. 2007. Pushing the limit: masticatory stress and adaptive plasticity in mammalian craniomandibular joints. J Exp Biol 210:628-641. (Pubitemid 46450810)
52. Ravosa MJ, López EK, Menegaz RA, Stock SR, Stack MS, Hamrick MW. 2008a. Using "Mighty Mouse" to understand masticatory plasticity: myostatin-deficient mice and musculoskeletal function. Integr Comp Biol 48:345-359.
53. Ravosa MJ, López EK, Menegaz RA, Stock SR, Stack MS, Hamrick MW. 2008b. Adaptive plasticity in the mammalian masticatory complex: you are what, and how, you eat. In: Vinyard CJ, Ravosa MJ, Wall CE, editors. Primate craniofacial biology and function. New York: Springer Academic Publishers. p 293-328.
54. Ravosa MJ, Ning J, Costley DB, Daniel AN, Stack MS. 2010b. Masticatory biomechanics and masseter fiber-type plasticity. J Musculoskel Neuronal Interac 10:46-55.
55. Ravosa MJ, Noble VE, Hylander WL, Johnson KR, Kowalski EM. 2000b. Masticatory stress, orbital orientation and the evolution of the primate postorbital bar. J Hum Evol 38:667-693.
56. Ravosa MJ, Ross CF, Williams SH, Costley DB. Allometry of masticatory loading parameters in mammals. 2010a. Anat Rec 293:557-571.
57. Ravosa MJ, Savakova DG, Johnson KR, Hylander WL. 2006. Primate origins and the function of the circumorbital region: what's load got to do with it? In: Ravosa MJ, Dagosto M, editors. Primate origins: evolution and adaptation. New York: Springer Academic Publishers. p 285-328.
58. Ravosa MJ, Vinyard CJ, Hylander WL. 2000c. Stressed out: masticatory forces and primate circumorbital form. Anat Rec 261: 173-175.
59. Rosenberger AL. 1986. Platyrrhines, catarrhines and the anthropoid transition. In: Wood BA, Martin L, Andrews P, editors. Major topics in primate and human evolution. Cambridge: Cambridge University Press. p 66-88.
60. Ross CF. 1995. Muscular and osseous anatomy of the primate anterior temporal fossa and the functions of the postorbital septum. Am J Phys Anthropol 98:275-306.
61. Ross CF, Hylander WL. 1996. In vivo and in vitro bone strain in the owl monkey circumorbital region and the function of the postorbital septum. Am J Phys Anthropol 101:183-215.
62. Rubin CT, Bain SD, McLeod KJ. 1992. Suppression of the osteogenic response in the aging skeleton. Calcif Tissue Int 50:306-313.
63. Sorensen MF, Rogers JP, Baskett TS. 1968. Reproduction and development in confined swamp rabbits. J Wildl Manag 32: 520-531.
64. Tattersall L. 1995. The Last Neanderthal. New York: Macmillan.
65. Taylor AB, Jones KE, Kunwar R, Ravosa MJ. 2006. Dietary consistency and plasticity of masseter fiber architecture in postweaning rabbits. Anat Rec A 288:1105-1111. (Pubitemid 44521965)
66. Wainwright SA, Biggs WD, Currey JD, Gosline JM. 1976. Mechanical design in organisms. Princeton: Princeton University Press.
67. Wolpoff MH. 1996. Human evolution. New York: McGraw-Hill.
68. Weijs WA, Brugman P, Grimbergen CA. 1989. Jaw movements and muscle activity during mastication in growing rabbits. Anat Rec 224:407-416. (Pubitemid 19191690)
69. Weijs WA, Brugman P, Klok EM. 1987. The growth of the skull and jaw muscles and its functional consequences in the New Zealand rabbit (Oryctolagus cuniculus). J Morphol 194:143-161.
70. Weijs WA, Dantuma R. 1981. Functional anatomy of the masticatory apparatus in the rabbit (Oryctolagus cuniculus). Neth J Zool 31:99-147.
71. Weijs WA, de Jongh HJ. 1977. Strain in mandibular alveolar bone during mastication in the rabbit. Arch Oral Biol 22:667-675.
72. Yamada K, Kimmel DB. 1991. The effect of dietary consistency on bone mass and turnover in the growing rat mandible. Arch Oral Biol 36:129-138.
73. Yardin M. 1974. Sur l'ontogénèse de la mastication chez le lapin Oryctolagus cuniculus. Mammalia 38:737-747.