Patterns of variation across primates in jaw-muscle electromyography during mastication.

Biologists that study mammals continue to discuss the evolution of and functional variation in jaw-muscle activity during chewing. A major barrier to addressing these issues is collecting sufficient in vivo data to adequately capture neuromuscular variation in a clade. We combine data on jaw-muscle electromyography (EMG) collected during mastication from 14 species of primates and one of treeshrews to assess patterns of neuromuscular variation in primates. All data were collected and analyzed using the same methods. We examine the variance components for EMG parameters using a nested ANOVA design across successive hierarchical factors from chewing cycle through species for eight locations in the masseter and temporalis muscles. Variation in jaw-muscle EMGs was not distributed equally across hierarchical levels. The timing of peak EMG activity showed the largest variance components among chewing cycles. Relative levels of recruitment of jaw muscles showed the largest variance components among chewing sequences and cycles. We attribute variation among chewing cycles to (1) changes in food properties throughout the chewing sequence, (2) variation in bite location, and (3) the multiple ways jaw muscles can produce submaximal bite forces. We hypothesize that variation among chewing sequences is primarily related to variation in properties of food. The significant proportion of variation in EMGs potentially linked to food properties suggests that experimental biologists must pay close attention to foods given to research subjects in laboratory-based studies of feeding. The jaw muscles exhibit markedly different variance components among species suggesting that primate jaw muscles have evolved as distinct functional units. The balancing-side deep masseter (BDM) exhibits the most variation among species. This observation supports previous hypotheses linking variation in the timing and activation of the BDM to symphyseal fusion in anthropoid primates and in strepsirrhines with robust symphyses. The working-side anterior temporalis shows a contrasting pattern with little variation in timing and relative activation across primates. The consistent recruitment of this muscle suggests that primates have maintained their ability to produce vertical jaw movements and force in contrast to the evolutionary changes in transverse occlusal forces driven by the varying patterns of activation in the BDM.

[1]  W. Weijs,et al.  Jaw movements and muscle activity during mastication in growing rabbits , 1989, The Anatomical record.

[2]  K. Hiiemae,et al.  Trends in the Evolution of Primate Mastication , 1972, Nature.

[3]  J. Ahlgren Mechanism of mastication , 1966 .

[4]  H. Birkedal‐Hansen Biological mechanisms of tooth movement and craniofacial adaptation , 1993 .

[5]  Kirk R. Johnson,et al.  Temporalis function in anthropoids and strepsirrhines: an EMG study. , 2005, American journal of physical anthropology.

[6]  S. Herring,et al.  Age changes in mastication in the pig. , 1994, Comparative biochemistry and physiology. Comparative physiology.

[7]  Bernard Wood,et al.  Food Acquisition and Processing in Primates , 1984 .

[8]  A. van der Bilt,et al.  Control of elevator muscle activity during simulated chewing with varying food resistance in humans. , 1992, Journal of neurophysiology.

[9]  W L Hylander,et al.  Experimental analysis of temporomandibular joint reaction force in macaques. , 1979, American journal of physical anthropology.

[10]  Callum F. Ross,et al.  Into the Light: The Origin of Anthropoidea , 2000 .

[11]  J. Lanyon,et al.  Koala (Phascolarctos cinereus) dentition and nutrition. II. Implications of tooth wear in nutrition , 1986 .

[12]  S W Herring,et al.  Functional heterogeneity in a multipinnate muscle. , 1979, The American journal of anatomy.

[13]  Peter S Ungar,et al.  Dental topography and molar wear in Alouatta palliata from Costa Rica. , 2004, American journal of physical anthropology.

[14]  R. Martin,et al.  Intraordinal phylogenetics of treeshrews (Mammalia: Scandentia) based on evidence from the mitochondrial 12S rRNA gene. , 2005, Molecular phylogenetics and evolution.

[15]  W L Hylander,et al.  Jaw muscle function and wishboning of the mandible during mastication in macaques and baboons. , 1994, American journal of physical anthropology.

[16]  S. Herring,et al.  Development of the masseter muscle and oral behavior in the pig. , 1986, The Journal of experimental zoology.

[17]  A. Woda,et al.  Effects of increased hardness on jaw movement and muscle activity during chewing of visco-elastic model foods , 2001, Experimental Brain Research.

[18]  W. Turnbull Mammalian masticatory apparatus / [by] William D. Turnbull -- , 1970 .

[19]  Susan H. Williams,et al.  Telemetry System for Assessing Jaw-Muscle Function in Free-ranging Primates , 2008, International Journal of Primatology.

[20]  G. Loeb,et al.  Electromyography for Experimentalists , 1986 .

[21]  K. Liem Aquatic Versus Terrestrial Feeding Modes: Possible Impacts on the Trophic Ecology of Vertebrates , 1990 .

[22]  S. Herring Mastication and Maturity: A Longitudinal Study in Pigs , 1977, Journal of dental research.

[23]  Y. Kawamura,et al.  Effects of texture of food on chewing patterns in the human subject. , 1989, Journal of oral rehabilitation.

[24]  Roger Pradel,et al.  Roe deer survival patterns: a comparative analysis of contrasting populations , 1993 .

[25]  P. Wright,et al.  Dental senescence in a long-lived primate links infant survival to rainfall. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[26]  W. Hylander,et al.  Modelling relative masseter force from surface electromyograms during mastication in non-human primates. , 1993, Archives of oral biology.

[27]  M. Ravosa Structural allometry of the prosimian mandibular corpus and symphysis , 1991 .

[28]  G. Langenbach,et al.  Growth Patterns of the Rabbit Masticatory Muscles , 1990, Journal of dental research.

[29]  Kirk R. Johnson,et al.  Masseter electromyography during chewing in ring-tailed lemurs (Lemur catta). , 2006, American journal of physical anthropology.

[30]  Callum F Ross,et al.  Shaping Primate Evolution: Jaw adductor force and symphyseal fusion , 2004 .

[31]  M. Bouvier A biomechanical analysis of mandibular scaling in old world monkeys , 1986 .

[32]  A. Miller,et al.  Histochemical and electromyographic analysis of craniomandibular muscles in the rhesus monkey, Macaca mulatta. , 1988, Journal of oral and maxillofacial surgery : official journal of the American Association of Oral and Maxillofacial Surgeons.

[33]  H. Shaffer,et al.  Aquatic prey capture in ambystomatid salamanders: Patterns of variation in muscle activity , 1985, Journal of morphology.

[34]  C. Gans,et al.  Electromyograms are repeatable: precautions and limitations. , 1980, Science.

[35]  R Yemm,et al.  The orderly recruitment of motor units of the masseter and temporal muscles during voluntary isometric contraction in man. , 1977, The Journal of physiology.

[36]  W. Weijs Evolutionary Approach of Masticatory Motor Patterns in Mammals , 1994 .

[37]  T. Skogland Tooth wear by food limitation and its life history consequences in wild reindeer , 1988 .

[38]  D. J. Daegling Biomechanics of cross-sectional size and shape in the hominoid mandibular corpus. , 1989, American journal of physical anthropology.

[39]  Susan H. Williams,et al.  Mechanical properties of foods used in experimental studies of primate masticatory function , 2005, American journal of primatology.

[40]  Kirk R. Johnson,et al.  Specialization of the Superficial Anterior Temporalis in Baboons for Masticationof Hard Foods , 2008 .

[41]  S. Herring,et al.  Motor-unit territories in the masseter muscle of infant pigs. , 1991, Archives of oral biology.

[42]  Andrea B. Taylor Masticatory form and function in the African apes. , 2002, American journal of physical anthropology.

[43]  Mark F. Teaford,et al.  Development, Function and Evolution of Teeth: Tooth tissues: development and evolution , 2000 .

[44]  C. Palazzi,et al.  EMG, bite force, and elongation of the masseter muscle under isometric voluntary contractions and variations of vertical dimension. , 1979, The Journal of prosthetic dentistry.

[45]  G. Wagner The character concept in evolutionary biology , 2001 .

[46]  P. Wainwright The evolution of feeding motor patterns in vertebrates , 2002, Current Opinion in Neurobiology.

[47]  Kirk R. Johnson,et al.  Symphyseal fusion and jaw-adductor muscle force: an EMG study. , 2000, American journal of physical anthropology.

[48]  R. German,et al.  Coordination between respiration and deglutition in a preterm infant mammal, Sus scrofa. , 1996, Archives of oral biology.

[49]  F. Ottenhoff,et al.  Control of human jaw elevator muscle activity during simulated chewing with varying bolus size , 2004, Experimental Brain Research.

[50]  Karl J. Friston,et al.  Variance Components , 2003 .

[51]  John G. Fleagle,et al.  Primate Adaptation and Evolution , 1989 .

[52]  P. Lucas,et al.  Food Properties that Influence Neuromuscular Activity During Human Mastication , 1998, Journal of dental research.

[53]  P. Wainwright,et al.  Behavioral characters and historical properties of motor patterns , 2001 .

[54]  J. Hoh 'Superfast' or masticatory myosin and the evolution of jaw-closing muscles of vertebrates. , 2002, The Journal of experimental biology.

[55]  A. van der Bilt,et al.  The relationship between jaw elevator muscle surface electromyogram and simulated food resistance during dynamic condition in humans. , 1996, Journal of oral rehabilitation.

[56]  C. Vinyard,et al.  Primate Craniofacial Function and Biology , 2008 .

[57]  Kirk R. Johnson,et al.  Phase II jaw movements and masseter muscle activity during chewing in Papio anubis. , 2006, American journal of physical anthropology.

[58]  Kirk R. Johnson,et al.  Loading patterns and jaw movements during mastication in Macaca fascicularis: a bone-strain, electromyographic, and cineradiographic analysis. , 1987, American journal of physical anthropology.

[59]  R. Greenberg Biometry , 1969, The Yale Journal of Biology and Medicine.

[60]  M. Spencer Force production in the primate masticatory system: electromyographic tests of biomechanical hypotheses. , 1998, Journal of human evolution.

[61]  Kirk R. Johnson,et al.  Temporalis and masseter muscle function during incision in macaques and humans , 1985, International Journal of Primatology.

[62]  Kirk R. Johnson,et al.  Jaw-Muscle Function and the Origin of Primates , 2007 .

[63]  C. Vinyard,et al.  Evolution of anthropoid jaw loading and kinematic patterns. , 2000, American journal of physical anthropology.

[64]  Kirk R. Johnson,et al.  Mandibular corpus strain in primates: further evidence for a functional link between symphyseal fusion and jaw-adductor muscle force. , 1998, American journal of physical anthropology.

[65]  K. Hiiemae Mammalian mastication : a review of the activity of the jaw muscles and the movements they produce in chewing , 1978 .

[66]  P. Bourdiol,et al.  Variations in human masseter and temporalis muscle activity related to food texture during free and side-imposed mastication. , 1999, Archives of oral biology.

[67]  E. Luschei,et al.  Patterns of mandibular movement and jaw muscle activity during mastication in the monkey. , 1974, Journal of neurophysiology.

[68]  K. Hiiemae CHAPTER 13 – Feeding in Mammals , 2000 .

[69]  T. van Eijden,et al.  Architecture of the human jaw‐closing and jaw‐opening muscles , 1997, The Anatomical record.

[70]  R. German,et al.  Variation in EMG activity: a hierarchical approach. , 2008, Integrative and comparative biology.

[71]  Kathleen K. Smith Are neuromotor systems conserved in evolution? , 1994, Brain, behavior and evolution.

[72]  J. P. Lund Mastication and its control by the brain stem. , 1991, Critical reviews in oral biology and medicine : an official publication of the American Association of Oral Biologists.

[73]  K. Hiiemae,et al.  Functional Aspects of Primate Jaw Morphology , 1984 .

[74]  Kirk R. Johnson,et al.  Jaw-muscle electromyography during chewing in Belanger's treeshrews (Tupaia belangeri). , 2005, American journal of physical anthropology.

[75]  T. van Eijden,et al.  Morphology and physiology of masticatory muscle motor units. , 2001, Critical reviews in oral biology and medicine : an official publication of the American Association of Oral Biologists.

[76]  S. Antón Macaque Masseter Muscle: Internal Architecture, Fiber Length and Cross-Sectional Area , 1999, International Journal of Primatology.

[77]  C. Ross,et al.  Electromyography of the anterior temporalis and masseter muscles of owl monkeys (Aotus trivirgatus) and the function of the postorbital septum. , 2000, American journal of physical anthropology.

[78]  J. J. Bosch,et al.  Jaw muscle EMG-activity and static loading of the mandible. , 1978 .

[79]  C. Wall A model of temporomandibular joint function in anthropoid primates based on condylar movements during mastication. , 1999, American journal of physical anthropology.

[80]  Kylie D. Foster,et al.  Adaptation of healthy mastication to factors pertaining to the individual or to the food , 2006, Physiology & Behavior.

[81]  C. Ross,et al.  In vivo function of the craniofacial haft: the interorbital "pillar". , 2001, American journal of physical anthropology.

[82]  K. Foster,et al.  Effect of texture of plastic and elastic model foods on the parameters of mastication. , 2006, Journal of neurophysiology.

[83]  E. Møller The chewing apparatus. An electromyographic study of the action of the muscles of mastication and its correlation to facial morphology. , 1966, Acta physiologica Scandinavica. Supplementum.

[84]  W. Hylander Mandibular function in Galago crassicaudatus and Macaca fascicularis: An in vivo approach to Stress Analysis of the mandible , 1979, Journal of morphology.

[85]  C. Wall,et al.  Scaling of the Chewing Muscles in Prosimians , 2008 .

[86]  S. Herring,et al.  Ontogeny of histochemical fiber types and muscle function in the masseter muscle of miniature swine. , 2000, American journal of physical anthropology.

[87]  André I. Khuri,et al.  Designs for Variance Components Estimation: Past and Present , 2000 .

[88]  F. Berzin,et al.  Electromyographic analysis of fatigue in temporalis and masseter muscles during continuous chewing. , 2001, Journal of oral rehabilitation.

[89]  T. van Eijden,et al.  Amplitude and Timing of EMG Activity in the Human Masseter Muscle during Selected Motor Tasks , 1993, Journal of dental research.

[90]  H. Devries MUSCLES ALIVE-THEIR FUNCTIONS REVEALED BY ELECTROMYOGRAPHY , 1976 .

[91]  Stuart O. Landry,et al.  Turnbull, William D. Mammalian Masticatory apparatus. Fieldiana: Geol., 18:149–356, 1970 , 1971 .

[92]  S. Hurlbert Pseudoreplication and the Design of Ecological Field Experiments , 1984 .

[93]  Norman L. Johnson,et al.  Sampling Distributions of Variance Components II. Empirical Studies of Unbalanced Nested Designs , 1966 .

[94]  C. Vinyard,et al.  Linking Laboratory and Field Approaches in Studying the Evolutionary Physiology of Biting in Bamboo Lemurs , 2008, International Journal of Primatology.

[95]  Susan H. Williams,et al.  Modulation of mandibular loading and bite force in mammals during mastication , 2007, Journal of Experimental Biology.

[96]  A. Crompton,et al.  A cineradiographic and electromyographic study of mastication in Tenrec ecaudatus , 1985, Journal of morphology.

[97]  S. Herring The Ontogeny of Mammalian Mastication , 1985 .

[98]  A. M. Smith,et al.  Activity of trigeminal alpha- and gamma-motoneurons and muscle afferents during performance of a biting task. , 1979, Journal of neurophysiology.

[99]  I. Kojola,et al.  Foraging conditions, tooth wear and herbivore body reserves: a study of female reindeer , 1998, Oecologia.

[100]  W. A. Thompson,et al.  Non-Negative Estimates of Variance Components , 1963 .

[101]  S. Cachel A functional analysis of the primate masticatory system and the origin of the anthropoid post-orbital septum. , 1978, American journal of physical anthropology.

[102]  S. Herring,et al.  Neural organization of the masseter muscle in the pig , 1989, The Journal of comparative neurology.

[103]  S. Herring,et al.  Effects of Oral Sensory Afferents on Mastication in the Miniature Pig , 1993, Journal of dental research.

[104]  E. Luschei,et al.  Recruitment order, contractile characteristics, and firing patterns of motor units in the temporalis muscle of monkeys , 1978, Experimental Neurology.

[105]  T. van Eijden,et al.  Mammalian Feeding Motor Patterns1 , 2001 .