The Ontogeny of Masticatory Muscle Architecture in Microcebus murinus.
development
growth
mastication
muscle atrophy
senescence
Journal
Anatomical record (Hoboken, N.J. : 2007)
ISSN: 1932-8494
Titre abrégé: Anat Rec (Hoboken)
Pays: United States
ID NLM: 101292775
Informations de publication
Date de publication:
05 2020
05 2020
Historique:
received:
02
05
2019
revised:
01
07
2019
accepted:
04
07
2019
pubmed:
12
9
2019
medline:
17
2
2021
entrez:
12
9
2019
Statut:
ppublish
Résumé
The masticatory apparatus has been the focus of many studies in comparative anatomy-especially analyses of skulls and teeth, but also of the mandibular adductor muscles which are responsible for the production of bite force and the movements of the mandible during food processing and transport. The fiber architecture of these muscles has been correlated to specific diets (e.g., prey size in felids) and modes of foraging (e.g., tree gouging in marmosets). Despite the well-elucidated functional implications of this architecture, little is known about its ontogeny. To characterize age-related myological changes, we studied the masticatory muscles in a large (n = 33) intraspecific sample of a small, Malagasy primate, Microcebus murinus including neonatal through geriatric individuals. We removed each of the mandibular adductors and recorded its mass as well as other linear measurements. We then chemically dissected each muscle to study its architecture-fascicle length and physiological cross-sectional area (PCSA) which relate to stretch (gape) and force capabilities, respectively. We observed PCSA and muscle mass to increase rapidly and plateau in adulthood through senescence. Fascicle lengths remained relatively constant once maximal length was reached, which occurred early in life, suggesting that subsequent changes in PCSA are driven by changes in muscle mass. Quadratic curvilinear models of each of the architectural variables of all adductors combined as well as individual muscles regressed against age were all significant. Anat Rec, 303:1364-1373, 2020. © 2019 American Association for Anatomy.
Types de publication
Journal Article
Research Support, U.S. Gov't, Non-P.H.S.
Langues
eng
Sous-ensembles de citation
IM
Pagination
1364-1373Informations de copyright
© 2019 American Association for Anatomy.
Références
Anapol F, Barry K. 1996. Fiber architecture of the extensors of the hindlimb in semiterrestrial and arboreal guenons. Am J Phys Anthropol 99:429-447.
Anapol F, Shahnoor N, Ross CF. 2008. Scaling of reduced physiologic cross-sectional area in primate muscles of mastication. In: Vinyard C, Ravosa MJ, Wall C, editors. Primate craniofacial function and biology. New York: Springer. p 201-216.
Antón SC. 1999. Macaque masseter muscle: internal architecture, fiber length and cross-sectional area. Int J Primatol 20:441-462.
Antón SC. 2000. Macaque pterygoid muscles: internal architecture, fiber length, and cross-sectional area. Int J Primatol 21:131-156.
Bons N, Rieger F, Prudhomme D, Fisher A, Krause KH. 2006. Microcebus murinus: a useful primate model for human cerebral aging and Alzheimer's disease? Genes Brain Behav 5:120-130.
Cachel S. 1984. Growth and allometry in primate masticatory muscles. Arch Oral Biol 29:287-293.
Carlson DS. 1983. Growth of the masseter muscle in rhesus monkeys (Macaca mulatta). Am J Phys Anthropol 60:401-410.
Castanet J, Croci S, Aujard F, Perret M, Cubo J, De Margerie E. 2004. Lines of arrested growth in bone and age estimation in a small primate: Microcebus murinus. J Zool 263:31-39.
Chazeau C, Marchal J, Hackert R, Perret M, Herrel A. 2012. Proximate determinants of bite force capacity in the mouse lemur. J Zool 290:42-48.
Close R. 1972. Dynamic properties of mammalian skeletal muscles. Physiol Rev 52:129-197.
Cruz-Jentoft AJ, Baeyens JP, Bauer JM, Boirie Y, Cederholm T, Landi F, Martin FC, Michel J-P, Rolland Y, Schneider SM, et al. 2010. Sarcopenia: European consensus on definition and diagnosis. Age Ageing 39:412-423.
Curtis AA, Santana SE. 2018. Jaw-dropping: functional variation in the digastric muscle in bats. Anat Rec 301:279-290.
Dammhahn M, Kappeler PM. 2008. Comparative feeding ecology of sympatric Microcebus berthae and M. murinus. Int J Primatol 29:1567.
Dickinson E, Fitton LC, Kupczik K. 2018. Ontogenetic changes to muscle architectural properties within the jaw-adductor musculature of Macaca fascicularis. Am J Phys Anthropol 167:291-310.
Dumont ER, Herrel A, Medellin RA, Vargas-Contreras JA, Santana SE. 2009. Built to bite: cranial design and function in the wrinkle-faced bat. J Zool 279:329-337.
Elliott D, Crawford G. 1965. The thickness and collagen content of tendon relative to the cross-sectional area of muscle during growth. Proc R Soc Lond B 162:198-202.
Eng CM, Ward SR, Vinyard CJ, Taylor AB. 2009. The morphology of the masticatory apparatus facilitates muscle force production at wide jaw gapes in tree-gouging common marmosets (Callithrix jacchus). J Exp Biol 212:4040-4055.
Ezran C, Karanewsky CJ, Pendleton JL, Sholtz A, Krasnow MR, Willick J, Razafindrakoto A, Zohdy S, Albertelli MA, Krasnow MA. 2017. The mouse lemur, a genetic model organism for primate biology, behavior, and health. Genetics 206:651-664.
Fabre PH, Herrel A, Fitriana Y, Meslin L, Hautier L. 2017. Masticatory muscle architecture in a water-rat from Australasia (Murinae, Hydromys) and its implication for the evolution of carnivory in rodents. J Anat 231:380-397.
Gans C. 1982. Fiber architecture and muscle function. Exercise Sport Sci Rev 10:160-207.
Gans C, Bock WJ. 1965. The functional significance of muscle architecture-a theoretical analysis. Ergeb Anat Entwicklungsgesch 38:115-142.
Gans C, Gaunt AS. 1991. Muscle architecture in relation to function. J Biomech 24:53-65.
Goldspink G. 1980. Growth of muscle. In: Goldspink DF, editor. Development and specialization of skeletal muscle. Cambridge: Cambridge University Press. p 19-35.
Hartstone-Rose A, Perry JMG, Morrow CJ. 2012. Bite force estimation and the fiber architecture of felid masticatory muscles. Anat Rec 295:1336-1351.
Hartstone-Rose A, Deutsch AR, Leischner CL, Pastor F. 2018. Dietary correlates of primate masticatory muscle fiber architecture. Anat Rec 301:311-324.
Herrel A, De Smet A, Aguirre LF, Aerts P. 2008. Morphological and mechanical determinants of bite force in bats: do muscles matter? J Exp Biol 211:86-91.
Huhov J, Henry-Ward W, Phillips L, German R. 1988. Growth allometry of craniomandibular muscles, tendons, and bones in the laboratory rat (Rattus norvegicus): relationships to oromotor maturation and biomechanics of feeding. Am J Anat 182:381-394.
Knuttgen HG. 1976. Development of muscular strength and endurance. In: Knuttgen HG, editor. Neuromuscular mechanisms for therapeutic and conditioning exercise. Baltimore: University Park Press. p 97-118.
Langenbach GEJ, Weijs WA. 1990. Growth patterns of the rabbit masticatory muscles. J Dent Res 69:20-25.
Lieber RL, Friden J. 2000. Functional and clinical significance of skeletal muscle architecture. Muscle Nerve 23:1647-1666.
Lutermann H, Schmelting B, Radespiel U, Ehresmann P, Zimmermann E. 2006. The role of survival for the evolution of female philopatry in a solitary forager, the grey mouse lemur (Microcebus murinus). Proc R Soc B 273:2527-2533.
Martin R. 1971. A laboratory breeding colony of the lesser mouse lemur. Breeding primates. Basel: Karger Publishers. p 161-171.
Maughan RJ, Watson JS, Weir J. 1983. Strength and cross-sectional area of human skeletal muscle. J Physiol 338:37-49.
Mittermeier RA, Louis EE, Richardson M, Schwitzer C, Langrand O, Rylands AB, Hawkins F, Rajaobelina S, Rasimbazafy J, Rasoloarison RM, et al. 2010. Lemurs of Madagascar. 3rd ed. Arlington, Virginia: Conservation International.
Murphy RA, Beardsley AC. 1974. Mechanical properties of the cat soleus muscle in situ. Am J Physiol 227:1008-1013.
Narici MV, Maganaris CN, Reeves ND, Capodaglio P. 2003. Effect of aging on human muscle architecture. J Appl Physiol 95:2229-2234.
Otten E. 1988. Concepts and models of functional architecture in skeletal muscle. Exercise Sport Sci Rev 16:89-138.
Perret M. 1997. Change in photoperiodic cycle affects life span in a prosimian primate (Microcebus murinus). J Biol Rhythms 12:136-145.
Perry JMG, Hartstone-Rose A. 2010. Maximum ingested food size in captive strepsirrhine primates: scaling and the effects of diet. Am J Phys Anthropol 142:625-635.
Perry JMG, Wall CE. 2008. Scaling of the chewing muscles in prosimians. In: Vinyard C, Ravosa MJ, Wall CE, editors. Primate craniofacial function and biology. New York: Springer. p 217-240.
Perry JMG, Hartstone-Rose A, Wall CE. 2011. The jaw adductors of strepsirrhines in relation to body size, diet, and ingested food size. Anat Rec 294:712-728.
Perry JMG, Macneill KE, Heckler AL, Rakotoarisoa G, Hartstone-Rose A. 2014. Anatomy and adaptations of the chewing muscles in Daubentonia (Lemuriformes). Anat Rec 297:308-316.
Pfaller JB, Herrera ND, Gignac PM, Erickson GM. 2009. Ontogenetic scaling of cranial morphology and bite-force generation in the loggerhead musk turtle. J Zool 280:280-289.
Pfaller JB, Gignac PM, Erickson GM. 2011. Ontogenetic changes in jaw-muscle architecture facilitate durophagy in the turtle Sternotherus minor. J Exp Biol 214:1655-1667.
Prufrock KA, Perry JMG. 2018. Strepsirrhine diets and the pattern of masticatory muscle development. FASEB J 32:780-785.
Rassoul RA, Alves S, Pantesco V, De Vos J, Michel B, Perret M, Mestre-Frances N, Verdier J-M, Devau G. 2010. Distinct transcriptome expression of the temporal cortex of the primate Microcebus murinus during brain aging versus Alzheimer's disease-like pathology. PLoS One 5:e12770.
Rayne J, Crawford GNC. 1972. The relationship between fibre length, muscle excursion and jaw movements in the rat. Arch Oral Biol 17:859-872.
Röhrle O, Pullan AJ. 2007. Three-dimensional finite element modelling of muscle forces during mastication. J Biomech 40:3363-3372.
Rosenberg IH. 1997. Sarcopenia: origins and clinical relevance. J Nutr 127:990S-991S.
Santana SE. 2018. Comparative anatomy of bat jaw musculature via diffusible iodine-based contrast-enhanced computed tomography. Anat Rec 301:267-278.
Santana SE, Cheung E. 2016. Go big or go fish: morphological specializations in carnivorous bats. Proc R Soc B 283:20160615.
Schumacher G-H. 1961. Funktionelle morphologie der kaumuskulatur. Jena, Germany: G. Fischer.
Taylor AB, Vinyard CJ. 2009. Jaw-muscle fiber architecture in tufted capuchins favors generating relatively large muscle forces without compromising jaw gape. J Hum Evol 57:710-720.
Taylor AB, Jones KE, Kunwar R, Ravosa MJ. 2006. Dietary consistency and plasticity of masseter fiber architecture in postweaning rabbits. Anat Rec 288:1105-1111.