Integrative and Comparative Biology Advance Access originally published online on July 21, 2008
Integrative and Comparative Biology 2008 48(2):294-311; doi:10.1093/icb/icn071
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Patterns of variation across primates in jaw-muscle electromyography during mastication
*Department of Anatomy and Neurobiology, NEOUCOM, Rootstown, OH, USA; Department of Evolutionary Anthropology, Duke University, Durham, NC, USA; Department of Biomedical Sciences, Ohio University College of Osteopathic Medicine, Athens, OH, USA
Correspondence: 1E-mail: cvinyard{at}neoucom.edu
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Synopsis |
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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.
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Introduction |
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SynopsisIntroductionLevels of biological variation...Sources of biological variation...Materials and methodsResultsDiscussionConclusionsSupplementary dataAcknowledgmentsReferences |
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The primate masticatory apparatus is one of the best studied feeding systems in vertebrates. Over the past 30 years, most in vivo research into primate masticatory function during chewing has used: (1) strain gages to examine bone deformation (Hylander 1979a
, 1997b; Hylander et al. 1998; Ross 2001), (2) cineradiography, high speed video, or trackable implants to study jaw movements (Hiiemae and Kay 1973; Hylander et al. 1987; Wall 1999; Foster et al. 2006; Wall et al. 2006), or 3) electromyography (EMG) to quantify patterns of jaw-muscle activity (Luschei and Goodwin 1974; Hylander et al. 1987). More recently, EMG studies have come to dominate in vivo research into primate masticatory function (Hylander et al. 2000, 2004, 2005; Ross and Hylander 2000; Vinyard et al. 2005, 2006; Wall et al. 2006, in press). In large part, the recent emphasis on EMG follows from the ease of collecting useful in vivo data for testing functional hypotheses linking jaw loading and movements to variation in jaw form.
Outside of primatology, biologists studying feeding have maintained a discussion on the interspecific variability in jaw-muscle EMGs, whether these neuromuscular activation patterns are conserved, and how these motor activity patterns evolve (Hiiemae and Kay 1973; Hiiemae 1978, 2000; Schaffer and Lauder 1985; Lauder et al. 1989; Liem 1990; Lund 1991; Smith 1994; Langenbach and van Eijden 2001; Wainwright and Friel 2001; Wainwright 2002; Vinyard et al. 2007). These questions clearly apply to primates even though functional morphologists have only begun to explore the broader pattern of interspecific variation in primate jaw-muscle EMGs (Vinyard et al. 2005, 2007). In fact, primates are argued to exhibit neuromuscular conservation in motor activation patterns (Hiiemae and Kay 1972, 1973; Hiiemae 1978, 1984; Weijs 1994), although, this conclusion is based largely on EMGs from two species.
One of the difficulties in studying the evolution of patterns of jaw-muscle activity is the collection of data from enough closely related species to reliably document variation across a clade. In many cases, at least for mammals, activity patterns of jaw muscles for entire orders have been extrapolated from data taken on one, or at most a few, species. To date, we have compiled data on jaw-muscle EMGs during mastication from 14 primate species and one treeshrew species (as an out-group and early primate morphotype) using similar EMG data collection and analytical methods. This represents the largest jaw-muscle EMG dataset collected for mammals and allows us to begin a more detailed exploration of the variation in motor patterns during chewing.
Following German et al. (2008) and Schaffer and Lauder (1985), we examine how variation in EMG activity of jaw muscles is partitioned from the level of the chewing cycle through species. Even though these descriptions will not allow us to explicitly define evolutionary changes in primate EMGs, this hierarchical examination is an important step in understanding how jaw-muscle EMGs vary among primates and how muscle activation patterns might have evolved throughout primate history. Furthermore, because the biological factors influencing jaw-muscle EMGs dominate different hierarchical levels, comparing the relative magnitude of variation across these different levels allows us to refine hypotheses about the primary biological factors influencing the observed variation in jaw-muscle EMGs.
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Levels of biological variation in jaw-muscle EMGs |
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SynopsisIntroductionLevels of biological variation...Sources of biological variation...Materials and methodsResultsDiscussionConclusionsSupplementary dataAcknowledgmentsReferences |
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Activation patterns of jaw muscles can vary across biological levels of organization, ranging from the individual chewing cycle to species and to higher order clades. We initially consider five levels in which significant variation in jaw-muscle EMGs might exist: (1) among species, (2) among individuals of a species, (3) within an individual, (4) among chewing sequences, and (5) among chewing cycles in a chewing sequence. Each of these levels is hierarchically nested in the subsequent level and potentially influenced by a different combination of underlying factors.
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Sources of biological variation in jaw-muscle EMGs |
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SynopsisIntroductionLevels of biological variation...Sources of biological variation...Materials and methodsResultsDiscussionConclusionsSupplementary dataAcknowledgmentsReferences |
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The bioelectrical signals created by contracting muscles are known to have a number of experimental and biological sources of variation (Gans and Gorniak 1980
; Basmajian and De Luca 1985; Loeb and Gans 1986). Here, we only consider biological sources of variation specifically related to mastication in order to provide an interpretative baseline for the observed pattern of variation among the jaw-muscle EMGs of primates. We do not attempt an exhaustive list, but rather focus on the key factors that might help to interpret observed patterns of variation.
Food
Food is the external substrate of mastication. Given this role, the structural and mechanical properties of foods will significantly influence jaw-muscle activity patterns in multiple ways (Oron and Crompton 1985; Horio and Kawamura 1989; Ottenhoff et al. 1992, 1993, 1996; Huang et al. 1993; Hylander and Johnson 1994; Ahlgren 1966; Møller 1966; Agrawal et al. 1998; Mioche et al. 1999; Hylander et al. 2000; Agrawal and Lucas 2002; Peyron et al. 2002; Foster et al. 2006; Woda et al. 2006). For example, because size, texture, and mechanical properties of food are altered as foods are reduced during mastication, jaw-muscle EMGs will vary throughout a chewing sequence as the properties of the bolus change. Foods with distinct mechanical properties will elicit different recruitment patterns during chewing. Therefore, variation among chewing sequences may also be influenced by the range of foods consumed. Finally, the choice of food among individuals and the dietary variation among species will influence jaw-muscle EMGs, given the basic relationship between properties of food and feeding mechanics. Collectively, we predict that food will be a significant influence on the patterns of jaw-muscle EMGs in primates.
Location of bite point
The bite point can vary throughout a chewing sequence as well as among individuals and species. Changes in location of the bite point alter the mechanical leverage, amount of stretch of the jaw muscles and the degree of opening of the mouth required for a given size of particle. Given these underlying mechanical consequences, research on humans and nonhuman primates demonstrates that jaw-muscle activity changes systematically with the location of the bite point (Pruim et al. 1978; Manns et al. 1979; Hylander and Johnson 1985; Spencer 1998; Olmsted et al. 2005).
Morphology of the masticatory apparatus
Variation in several morphological components of the masticatory muscles can potentially influence patterns of jaw-muscle EMGs. Beginning with entire muscles, the relative position of a muscle affects its force-producing ability (all other factors held equal), indicating that variation in the leverage of jaw muscles may influence EMG patterns (Maynard Smith and Savage 1959; Herring 1992; Hylander 2006). Several variables broadly related to the architecture of muscle fibers also impact muscle mechanics and hence EMG patterns (Herring et al. 1979; Herring and Wineski 1986; Langenbach and Weijs 1990; van Eijden et al. 1997; Anapol and Herring 2000). The size of motor units and their distribution throughout a jaw muscle both potentially influence EMG patterns (Herring et al. 1989a, 1989b, 1991; van Eijden and Turkawski 2001). Finally, the composition and distribution of fiber types in a muscle can vary regionally within a muscle, between left and right sides as well as among individuals and species (Herring et al. 1979; Miller and Farias 1988; van Eijden et al. 1997; Hoh 2002). Given that recruitment thresholds typically vary with fiber types in a muscle (Yemm 1977; Clark et al. 1978; Lund et al. 1979; Korfage et al. 2005), we can expect variation in fiber types to influence patterns of jaw-muscle EMGs (Wall et al. in press).
In addition to the muscles of mastication, morphological variation in other parts of the masticatory apparatus may also influence EMG patterns of the jaw muscles. These potential morphological sources of variation include size and number of teeth, occlusal morphology, mechanical leverage as dictated by the shape of the jaw, morphology of bones, and sensory inputs through mechanoreceptors and/or spindles of the jaw muscles. For many of these features, direct evidence linking specific morphological variation to changes in EMG patterns is lacking. Basic mechanical principles, however, suggest that these factors will influence the mechanics of mastication and hence the activity of the jaw muscles during chewing.
These morphological features vary intraspecifically, interspecifically, and throughout ontogeny. Intra- and inter-specific variation in the form of the masticatory apparatus is well documented in primates (Hylander 1979c; Bouvier 1986; Daegling 1989; Ravosa 1991; Taylor 2002). Jaw-muscle EMGs correlate with suites of features within and among primate species (Hylander and Johnson 1994; Hylander et al. 2000, 2004, 2005; Vinyard et al. 2005, 2006, 2007; Wall et al. 2006). Alternatively, we know less about how morphological changes during ontogeny influence jaw-muscle EMGs (Herring 1977, 1985; Huang et al. 1994). In particular, dental eruption and wear (Lanyon and Sanson 1986; Skogland 1988; Gaillard et al. 1993; German et al. 1996; Kojola et al. 1998; King et al. 2005; Kojola et al. 1998), changes in organization and orientation of muscles (Herring and Wineski 1986; Weijs et al. 1989; Langenbach and Weijs 1990; Anapol and Herring 2000), and allometric changes in facial shape (Williams and Sidote 2008) all potentially influence activity patterns of the jaw muscles. We only consider adults (and older subadults) here, thereby minimizing ontogeny as a source of variation.
We can readily envision morphological variation among individuals and species having significant influence on activity patterns of jaw muscles. While more subtle by comparison, food-by-morphology interactions, such as differential fatigue in oxidative versus glycolytic fiber types (Korfage et al. 2005), may also influence jaw-muscle EMGs across chewing cycles within a sequence (Buzinelli and Berzin 2001).
Structural and functional redundancy
Individual jaw muscles perform multiple functions during a chewing cycle and throughout a chewing sequence. Because the chewing muscles are architecturally complex, they can be recruited in many different ways that create a submaximal bite force. In addition to redundancy within a muscle, there are multiple ways to produce submaximal bite forces during mastication (Hylander 1979a). These structural and functional redundancies likely contribute to the variation in EMG patterns within individuals, among individuals, and among species. Unfortunately, we have little prospect for identifying their relative contribution to overall variation in jaw-muscle EMG patterns.
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Materials and methods |
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Subjects
We combine published and unpublished EMG recordings of jaw-muscle activity during chewing in 10 primate species groups and in Belanger's; treeshrew (Tupaia belangeri) (Table 1). [In some cases, recordings were made from two species of the same genus (e.g., Macaca) or subfamily (e.g., Callitrichinae) because of limited numbers of individuals available for some species. Rather than introduce marked discrepancies in phylogenetic distance at the interspecific level, we combined these closely-related species into "species groups" for analysis (Table 1)]. We included treeshrews as a primitive primate morphotype (Vinyard et al. 2005
) in an effort to capture the range of variation across primates, we observed the same pattern of results when treeshrews were excluded from the analysis (data not shown). All subjects were healthy subadults or adults. Nonhuman subjects were trained to accept food while in a restraining apparatus prior to recording EMGs. Whenever possible, we recorded EMGs from nonhuman subjects during at least 2–4 experiments. Human subjects were only recorded during a single session. All procedures were approved by the Duke University or NEOUCOM IACUCs as well as by the NEOUCOM IRB.
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Construction and placement of EMG electrodes
In all studies, we used fine wire, bipolar, indwelling electrodes (nickel–chromium alloy, 0.05 mm diameter; California Fine Wire) to record activity of jaw muscles during chewing. We sampled the superficial and deep masseters, as well as the deep anterior and posterior portions of the temporalis muscle in various combinations. Construction and placement of electrodes followed a standard protocol that insured similarity across experiments (see Hylander and Johnson 1985
, 1994; Hylander et al. 2000, 2004 for details). Prior to collection of EMG data, cadaveric specimens were dissected to determine the best position and approach for placement of electrodes. Placement and approach varied somewhat across species so that electrodes were inserted in anatomically homologous parts of the jaw muscles (Fig. 1). Tips of electrodes were placed in small-gage needles and inserted into a muscle until they contacted bone. We then removed the needle leaving the electrode embedded in the muscle a few millimeters from bone. Electrodes in the superficial masseter were placed midway between the muscle's anterior and posterior borders and embedded near the inferior edge of the mandibular ramus. Electrodes in the deep masseter were placed in the thickest and most transverse fibers of the muscle, meaning that anteroposterior positioning of the electrode varied among species. In all species, the needle was inserted inferior to the zygomatic arch at a downward angle of 
30°. We inserted electrodes in the deep portion of the anterior temporalis posterior to the posterolateral margin of the postorbital bar in the region of the postorbital constriction. Electrodes were placed in the posterior temporalis superior to the opening of the external auditory meatus. We did not verify electrode placement via dissection because subjects were not killed at the end of experiments.
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Recording and quantifying EMGs
Following implantation of electrodes, we allowed nonhuman subjects to recover from sedation or anesthesia. Human volunteers received no sedatives. Once a subject became fully alert, we offered food items (Table 1) one at a time. We recorded, amplified and band-pass filtered (100–3000 Hz) jaw-muscle EMG potentials during chewing to either a 14-channel FM tape recorder (Bell and Howell, Model 4020A), a 16-channel digital recorder (TEAC, RD-145T), or directly to a computer via a data-acquisition board (DAQ 6071E, National Inst., Austin, TX) and custom-written software routines (LabView, National Instruments) sampling at 10 KHz per channel. We continued feeding each subject until we had recorded sufficient data (usually 2–4 chewing sequences per food type) or the animal refused to continue eating. Following data collection, we removed the electrodes, freed nonhuman subjects from their restraints, and returned nonhuman animals to their cages. All recoveries from these procedures occurred without complications.
For analog data, we converted raw EMGs from selected chewing sequences to digital data sampling at 10 KHz, and recorded these digital data to a computer using a LabView routine. All digitized raw data were filtered with a digital Butterworth band-pass filter (100–3000 Hz). To provide a single waveform for analysis, we rectified and integrated EMGs by calculating the root-mean-square (rms) of each digitized raw EMG signal over a 42-ms time constant (Fig. 2) (Hylander and Johnson 1993; Hylander et al. 2000).
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rms-EMG data
Prior to extracting data, we visually inspected EMG waveforms for processing errors. Individual chewing cycles were assigned to left or right side, based on associated audio or video records as well as on empirically established tendencies determined using these independent audio/video data (Vinyard et al. 2005
). Subsequently, all muscles were designated as either a working side (W) or balancing side (B) muscle for each chewing cycle.
We examined two variables extracted from the rms-EMG waveform for each muscle during a chewing cycle. First, we calculated the Peak Timing of muscle activity during a chewing cycle. Peak Timing (in milliseconds) estimates when a muscle reaches peak activity during a cycle as measured by the highest value in the rms waveform (Fig. 2). To provide a uniform standard of comparison across cycles, all timing values were calculated as the number of milliseconds that peak activity in a muscle preceded or followed the peak activity of a predetermined reference muscle, the working-side superficial masseter (WSM) (Hylander et al. 2000). We calculated Peak Timing for the balancing-side superficial masseter (BSM), the working-side and balancing-side deep masseter (WDM, BDM), the working-side and balancing-side (deep) anterior temporalis (WAT, BAT), and the working-side and balancing-side posterior temporalis (WPT, BPT).
The second variable we examined is scaled Peak Activity. Peak Activity is initially measured as the highest amplitude observed in the rms-EMG waveform during a chewing cycle (Fig. 2). To compare peak rms-EMG activity across different electrodes from multiple experiments, we identified the largest peak rms value observed across all cycles for an electrode in an experiment and assigned this peak a value of 1.0. The remaining, smaller peaks for that electrode were linearly rescaled to this value resulting in all scaled Peak Activity values ranging from 0 to 1 (Hylander et al. 2000). These scaled Peak Activity values represent relative estimates of muscle recruitment during the chewing cycle (Hylander and Johnson 1993; Hylander et al. 2000). Peak Activity was estimated for all locations of sampled muscles.
Patterns of variation in peak timing and peak activity across chewing cycle to species
We describe the pattern of variation in Peak Timing and Peak Activity across several hierarchical levels using a random effects (Model II) nested ANOVA model (Sokal and Rohlf 1995). We consider multiple factors including (1) species group, (2) animal, (3) experiment, (4) chewing sequence, and (5) chewing cycle in the following model:
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EMGijklm represents the Peak Timing or Peak Activity of a jaw muscle and µ is the parametric mean of the population. Factors below the species group are nested within higher level factors resulting in chewing cycle being nested in all other levels. Nesting is depicted in the above model by placing subscripts in parentheses such that "Animal(i)j" indicates nesting within "Species Groupi." We estimated the magnitude of variation (and percentage of total variation) attributable to each nested factor by calculating the respective variance components (Sokal and Rohlf 1995). Variance components were calculated by Statgraphics 5.0 software.
Because unavoidable problems arise during experiments (e.g., electrode failure or lack of animal compliance) and different numbers of animals were available, our dataset resulted in an unbalanced ANOVA design. Unbalanced designs do not have exact significance tests (Sokal and Rohlf 1995; Searle et al. 2006). Given this shortcoming, we focus on describing general trends observed in the hierarchical pattern of variances across factors (Khuri 2000).
The unbalanced nested ANOVA model poses additional limitations. Nested ANOVA models typically provide more precise estimates of variance components for lower level factors due to their increased degrees of freedom (Leone et al. 1968; Khuri 2000). This suggests that variance components from higher level factors should be viewed with greater caution. Estimation of variance components by ANOVA can yield negative estimates despite their logical impossibility. Negative estimates of variance components can result from an inappropriate ANOVA model and/or from statistical noise (Thompson and Moore, 1963; Searle et al., 2006). While a number of options are available for balanced designs, unbalanced data offer relatively few methods for addressing these negative estimates. Following Searle et al. (2006), we truncated all negative estimates at zero and infer that this value is the true estimate of a variance component. The disadvantage of this approach is that the remaining estimates of variance components are no longer unbiased for that particular measure of EMG (Searle et al. 2006).
EMG data were collected during mastication of several foods across these species (Table 1). These foods exhibit a variety of properties ranging from mechanically weak (e.g., apple, pear, or raisin) to stiff and/or tough (e.g., popcorn kernels, gummybears, or leaves) (Williams et al. 2005). Because food properties can have a significant influence on jaw-muscle EMGs, this variation in foods presents an important consideration for interpreting variance components. To facilitate these interpretations, we calculated variance components during mastication of (1) all foods, (2) stiff and/or tough foods, and (3) less mechanically resistant (hereafter "weak") foods. For stiff and/or tough foods, we identified a single food in each experiment with either the highest stress- or displacement-limited fragmentation index (typically subjects consumed one or the other) or toughest food (i.e., leaves for sifakas) based on the mechanical properties of foods reported by Williams et al. (2005) (Foods not included by Williams et al. (2005) were analyzed using similar methods and compared with published data in making these determinations). Finally, we examined variance components during mastication of weak foods, including apple, pear, or raisin. Not all species ate all of these foods meaning that this analysis considers fewer species-groups when estimating variance components.
An initial observation arising from the dataset is that humans show greater variation in Peak Timing of their jaw-closing muscles compared with other primates. The greater variation in humans may reflect biological and/or experimental factors. We were concerned that experimental issues in humans, such as the lack of sedation, range of consumed foods, and lack of repeated experiments, may confound the representativeness of the larger sample for primates. Therefore, we consider variance components both with and without humans.
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Results |
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SynopsisIntroductionLevels of biological variation...Sources of biological variation...Materials and methodsResultsDiscussionConclusionsSupplementary dataAcknowledgmentsReferences |
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We evaluated 13,454 chewing cycles across the 11 species-groups including primates and treeshrews. The basic distribution of data across levels is provided in Table 1.
Overall variances
The Peak Timing of the masseter muscles shows significantly greater variance for the combined sample compared with the Peak Timing of the temporalis muscle regardless of food type (Table 2). A clear pattern does not exist for timing variances among the masseters. Within the temporalis, the balancing-side muscles tend to exhibit equal or greater variances in Peak Timing than do the working-side muscles. Variance in Peak Activity is typically highest in the BDM and posterior temporalis (WPT and BPT) and lowest in the WDM and WAT (Table 2) across foods.
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Variance in Peak Timing typically decreases with stiff/tough foods and increases with weak foods (Table 2). For the most part, food has less of an influence on variances for scaled Peak Activity compared with Peak Timing. With the exception of a slight reduction of variance in the balancing temporalis (BAT and BPT), stiff/tough foods show similar variances as do all foods combined for Peak Activity (Table 2). Weak foods show reduced variance in masseter and increased variance in temporalis Peak Activity compared with all foods combined (Table 2).
The data from humans significantly increases the variation in Peak Timing (Supplementary Table 1a). For several muscles, variance in Peak Timing drops by half when humans are omitted. When humans are excluded, variances in Peak Timing are more similar across these food groups and consistent differences among foods are not apparent. Humans have little influence on overall variance for Peak Activity (Supplementary Table 1b). These disparate patterns primarily reflect the absolute versus the scaled nature of the variables of timing and activity, respectively.
Variance components
Peak timing
The largest variance component for Peak Timing is among chewing cycles (Table 3; Fig. 3). For the combined food sample, upwards of 80% of the variation in Peak Timing of the temporalis and 50–70% of that of the masseter is found among chewing cycles (Table 3; Fig. 3A). At the other end of the hierarchy, variance components among species are moderate at 20% for the deep masseter (WDM and BDM), but typically <5% for the remaining muscles (Table 3). Variance components tend to be lowest at the experiment level for all foods combined (Table 3; Fig. 3A).
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This basic set of observations persists when examining only stiff/tough foods (Table 4; Fig. 3C). Variance components among species groups increase slightly while most muscles show slightly reduced variation among chewing cycles (Table 4). When considering only weak foods, the percentage of variation at the level of the chewing cycle goes up slightly for most muscles compared with all foods combined (Table 4; Fig. 3E). Analysis of the timing of EMG activity in the jaw muscles during mastication of weak foods resulted in several negative estimates of variance components, raising concerns about the accuracy of interpretion of these results.
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Peak activity
Variance components for Peak Activity tend to be highest at the levels of the chewing sequence and the chewing cycle (Tables 3 and 4; Fig. 3). Across all foods combined, these two levels account for 60–90% of the total variance in EMG activity (Table 3; Fig. 3B). Relatively little to moderate variation exists among animals and among experiments. Among the masseters, the two balancing-side muscles (BSM and BDM) exhibit moderate variance components among species groups (Tables 3 and 4; Fig. 3). The working-side masseters tend to show little variation among species for Peak Activity. When considering stiff/tough foods, interspecific variation represents the largest variance component for peak activity of the BDM (Table 4; Fig. 3D).
Among temporalis muscles, the WAT shows very little variation among species, regardless of food, although estimates of variance components are negative for the two highest level factors during mastication of weak foods (Table 4). The posterior temporalis (WPT and BPT) show moderate variation among species across all foods (Table 3; Fig. 3B). For stiff/tough foods, all temporalis muscles except WAT show moderate variation at the species level (Table 4). This moderate variation among species increases to marked variation for these muscles when considering only weak foods, particularly the BPT where more than half of the variation exists at this level (Table 4; Fig. 3F).
The human influence
Excluding humans does not change the basic pattern of variance components for Peak Timing (Supplementary Tables 2 and 3). Most of the variation still exists among chewing cycles. Removing humans typically results in a slight elevation of variance components for levels above the chewing cycle, while variance among chewing cycles is concomitantly reduced. When humans are omitted, the BDM, and to a lesser extent the BPT, show modestly higher variance components at the species level (Supplementary Tables 2a and 3a). Humans do not exhibit a significant influence on the variance components for Peak Activity (Supplementary Tables 2b and 3b).
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Discussion |
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SynopsisIntroductionLevels of biological variation...Sources of biological variation...Materials and methodsResultsDiscussionConclusionsSupplementary dataAcknowledgmentsReferences |
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The examination of variance components across levels from chewing cycles through species provides several insights into the function of jaw muscles of primates during mastication. Variation in timing and recruitment of jaw muscles is not distributed equally across these hierarchical levels. Based on the large percentage of variation distributed among chewing cycles and among chewing sequences, there does appear to be certain pervasive influences on primate jaw-muscle EMGs focused on these lower hierarchical levels. Beyond these factors that affect all muscles, there are differences in the distribution of variance components among jaw muscles. These differences highlight the probability that the jaw muscles have undergone independent evolutionary changes and suggest that primate jaw muscles have not evolved as a single functional unit. We propose that these independent evolutionary changes were produced by different biological influences affecting individual jaw muscles or subsets of jaw muscles.
Factors influencing variation in jaw-muscle EMGs
Timing of jaw-muscle activity
The most striking outcome of the analysis of Peak Timing is the significant percentage of variation among chewing cycles. We attribute this variation to (1) changes in food properties throughout the chewing sequence, (2) variation in bite location, and (3) the multiple ways jaw muscles can be activated to produce submaximal bite forces. Variation in material properties between different foods is unlikely to be the major factor as differences among foods would primarily appear at the level of the chewing sequence or higher. While there is modest variation in Peak Timing among chewing sequences (10–20%), it does not approach the magnitude of variance components observed among chewing cycles. This interpretation is supported by the similar distribution of variance components when examining only stiff/tough or weak foods, given that variation due to different foods should be reduced in these two cases (but not eliminated as foods still varied within and among species). In summary, the large percentage of variation among chewing cycles is consistent with the ability of jaw muscles to dynamically alter their activity in ways that vary occlusal forces and mandibular movements, based on the changing mechanical demands of mastication (Ottenhoff et al. 1992, 1993).
Peak Timing of the WDM shows the smallest variance components at the level of the chewing cycle (Tables 3 and 4) as well as the least change in overall variances across the three different groupings of food (Table 2). Both observations suggest that the WDM is less affected by changes in the texture and consistency of food than were some of the other jaw muscles. This supports the hypothesis that the WDM plays a primary role in positioning the jaw in preparation for the upcoming power stroke in many primate species (Hylander et al. 2000, 2005; Vinyard et al. 2006; Wall et al. 2006). The modest variation at the species level for the WDM suggests that this positioning function varies among primates.
Peak EMG activity
Peak Activity shows the largest variance components among chewing sequences for most muscles, followed closely by the variance components among chewing cycles (Tables 3 and 4). We attribute variation among chewing cycles to the same set of biological factors discussed above for Peak Timing. We suggest that the variance components among chewing sequences is related to variation in properties among foods. Based on comparisons with variance components for Peak Timing, we hypothesize that differences in properties of foods have a larger effect on jaw-muscle recruitment than on the timing of activation of jaw muscles (see also Ross et al. 2007). One immediate concern is that variance components among chewing sequences are not reduced in comparisons to only stiff/tough or weak food as might be predicted by this hypothesis (Tables 3 and 4). As noted earlier, these restricted comparisons of foods do not eliminate variation in the mechanical properties of food. Additional experiments designed specifically to control variation in properties of food are needed to more appropriately test this hypothesis.
The working-side superficial and deep masseters (WSM and WDM) as well as the anterior temporalis muscles (WAT and BAT) exhibit small variance components among species (Tables 3 and 4) and the lowest overall variances for peak activity (with the exception of BAT in this latter case) (Table 2). This suggests that primates recruit relatively similar levels of scaled activity from these muscles during mastication (Fig. 4D). [It is worth noting that small variance components do not rule out the possibility of a significant difference among groups at a particular level. For example, the peak activity of the WAT differs significantly among several primate species (data not shown), despite the small variance component among species. This significant difference is problematic given the pseudoreplication in chewing cycles (see e.g., Hulbert 1984 or German et al. in press). More importantly, the analysis of the variance components suggests that any interspecific difference in this case represents a relatively small component of the total variation for peak activity in this muscle.] Alternatively, the balancing-side masseters (BSM and BDM) and posterior temporalis (WPT and BPT) exhibit modest variance components among species (Tables 3 and 4) and overall more variation (Table 2). Consequently, we hypothesize that primates differ in how they use these muscles to modulate relative force during mastication. Previously, researchers studying mastication by primates have focused on the ratio of recruitment from the working side relative to that from the balancing side (i.e., W/B ratios) in comparing activity patterns for these muscles (Hylander et al. 2000, 2004, 2005; Vinyard et al. 2005, 2006, 2007). This analysis suggests that interspecific variation in the balancing-side masseters and posterior temporalis are underlying differences in W/B ratios observed among primates.
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Food properties
Variance components show broadly similar patterns for all foods combined, stiff/tough foods, or weak foods (Tables 3 and 4; Fig. 3). In fact, removing humans from the dataset appears to have a greater influence on variance components than does restricting comparisons to specific food groups (and removing humans even left general patterns intact). Numerous studies demonstrate that the EMGs of primate jaw muscles are affected by the properties of food (see above citations). We also hypothesize that food properties play a significant role in the observed distribution of variance components among hierarchical levels. This apparent contradiction raises the question of whether we have controlled for variation in food properties by examining variance components among these different food groups. Two issues should be considered here. First, we could not control all variation in foods because of the range of dietary preference among primates (Table 1). Second, even if we could control foods more closely, different species will have dissimilar perceptions of the same food and the mechanical abilities required for reducing it. A more appropriate control would focus on explicit ecological links where the properties of natural diets dictate the most challenging foods given to each species in the laboratory. This ecological link would facilitate the interpretation of the activity patterns of jaw muscles in an evolutionary framework (Vinyard et al. 2006
; Williams et al. in press).
Even with this limited control for food, variance components for Peak Activity in the BDM and BPT show noticeable changes with food properties (Tables 3 and 4). Interspecific variance components increase for the BDM with stiff/tough foods and decrease with weaker foods. Interspecific variation represents the largest component of variance for stiff/tough foods, suggesting that primate species differ in how they use the BDM during mastication of challenging foods (Hylander and Johnson 1994; Hylander et al. 2000, 2004; Wall et al. 2006; Vinyard et al. 2007). The BPT shows the opposite pattern in which components of interspecific variance decrease slightly for stiff/tough foods and increase markedly for weak ones. Old World monkeys often markedly reduce the activitiy of their posterior temporalis during mastication of soft foods (Hylander et al. 2005; Wall et al. 2006, in press) and are likely driving this pattern.
Evolution of activity patterns in primate's jaw muscles
Descriptions of variance components cannot explicitly tell how EMGs of jaw muscles have evolved in primates. For example, variance components found among species may reflect heritable variation in patterns of motor activation and/or in modulation of muscle activity related to interspecific differences in jaw form or diet. While we cannot use these data to argue strongly for, or against, prevailing views about the conservation of motor patterns during mastication (Langenbach and van Eijden 2001), we can address several basic evolutionary hypotheses. One of the most important evolutionary implications of this analysis is that the different patterns of variance components across muscles suggests that the primate jaw-closing muscles have not evolved as a single functional unit but have distinct evolutionary histories (Hylander et al. 2000, 2005; Vinyard et al. 2005, 2007). Furthermore, the analysis of variance components yields similar interpretations to those of previous analyses linking interspecific differences in timing and recruitment of jaw muscles to the evolution of the morphology of the jaws and muscles of primates.
Peak timing
The Peak Timing of the deep masseter (WDM and BDM) shows the largest variance components among species (Tables 3 and 4). Though the WDM and BDM represent only a small percentage of the total cross-section of the masseter muscle (Antón 1999; Wall et al. 2007; Perry and Wall, in press), they are thought to play an important role in producing transverse jaw movements and occlusal forces during the power stroke in anthropoids (with fused symphyses) and in certain strepsirrhines (with robust symphyses) (Hylander and Johnson 1994; Hylander et al. 2000, 2003, 2004; Ravosa et al. 2000; Wall et al. 2006; Vinyard et al. 2007). The higher variance components among species for these two muscles is consistent with previously observed differences in Peak Timing in which treeshrews and strepsirrhines with unfused symphyses showed less differentiation of the superficial and deep masseters while anthropoids and strepsirrhines, with robust symphyses, exhibited an early-peaking WDM and late-peaking BDM associated with significant strains in the mandibular symphysis (Fig. 4A) (Hylander and Johnson 1994; Hylander et al. 2000, 2004; Vinyard et al. 2006, 2007; Wall et al. 2006).
In contrast to the deep masseters, the temporalis muscles show the least overall variance in Peak Timing (Table 2) and the largest variance components among chewing cycles. This is particularly true for the WAT. The temporalis muscle is the largest jaw-closing muscle in primates (Turnbull 1970; Cachel 1979) and the force vector of the anterior portion is primarily vertical during mastication. Hylander et al. (2005) observed that the temporalis muscles fire in a consistent sequence during the chewing cycle across primates. The small variance components among species are consistent with this interpretation (Fig. 4B). We hypothesize that the timing of these deep parts of the temporalis is patterned across primates reflecting this muscle's functional role in producing the vertical bite forces and the jaw movements requisite for mastication in all primates.
The variance in Peak Timing for humans is noticeably different from other primates and from treeshrews (Fig 4A and C). While humans are the most sampled primate in studies of masticatory EMGs (Ahlgren 1966; Møller 1966; van Eijden et al. 1993; Mioche et al. 1999; Woda et al. 2006), the present analysis is the first direct comparison of humans to other primates using the same recording procedures. Despite similar EMG recording methods, key differences exist in experimental protocols. In particular, humans were not sedated directly prior to collecting EMGs. Previously, Thompson et al. (2007) found that capuchins chew more slowly soon after sedation. It is also possible that animals exhibit reduced variance in chewing rates and EMG activity following sedation. An alternative, and more interesting, interpretation is that humans are more variable in the activity patterns of their jaw muscles compared with other primates. Future work involving novel techniques for nonhuman primates are needed to address these competing, but not mutually exclusive, explanations.
Peak activity
Variance components among species for Peak Activity suggest that the balancing-side masseters (BSM and BDM) have evolved distinct patterns of force modulation across primates (Hylander et al. 2000, 2004; Vinyard et al. 2007). In particular, the BDM shows marked variation among species during mastication (Fig. 4C). This pattern supports previous findings that primates with unfused symphyses and treeshrews tend to recruit lower levels of activity from their balancing-side masseters (Hylander et al. 2000, 2004; Vinyard et al. 2005, 2007; Wall et al. 2006). These authors have functionally linked variation in both the timing and recruitment of the BDM to differences of symphyseal fusion among primates. Furthermore, the deep masseters appear to play a primary role in the significant evolutionary changes among primates in transverse movements of the jaw and in transversely directed occlusal forces (Hiiemae and Kay 1972, 1973; Hylander et al. 2000; Ravosa et al. 2000; Ross 2000; Vinyard et al. 2007).
The posterior temporalis (WPT and BPT) also shows a relatively large variance component among species for Peak Activity (Tables 3 and 4). Macaques and baboons exhibit relatively low levels of activity in both the WPT and BPT during mastication, particularly when chewing weak foods (Hylander et al. 2005). Alternatively, strepsirrhines with mobile symphyses and treeshrews show reduced activity in the BPT (Hylander et al. 2005). Reduced activity in both the WPT and BPT of macaques and baboons yields a lower, anthropoid like, W/B ratio for Old World monkeys as compared with species with unfused symphyses that maintain higher W/B ratios (Hylander et al. 2005). This higher W/B ratio in species with mobile symphyses supports the hypothesis that the evolution of a fused symphysis is related to load resistance during mastication (Hylander et al. 2000, 2005; Ravosa et al. 2000; Vinyard et al. 2005, 2007). Alternatively, the reduced levels of relative recruitment in the posterior temporalis of macaques and baboons requires further analysis to understand the functional and evolutionary significance of this derived neuromuscular pattern.
In contrast to the interspecific variation in these muscles, the working-side anterior temporalis (WAT) shows the lowest variance components among species. With the potential exception of galagos, the WAT shows consistent levels of relative activity among primates (Fig. 4D). Collectively, both the timing and recruitment levels of the WAT suggest that it maintains a conserved activity pattern across primates (Hylander et al. 2005; Vinyard et al. 2007).
Practical implications
We see two important practical implications of this work. First, the foods given to primates during EMG studies will significantly impact the results. Careful consideration is needed to avoid skewing interspecific patterns by giving species foods that present vastly different levels of challenge to oral processing relative to their natural diets. We argue that providing experimental subjects a range of foods that mimic those seen in the natural diets of conspecifics is a reasonable protocol for controlling dietary variation from an evolutionary perspective (Vinyard et al. 2005, in press; Williams et al. in press). Previous comparisons of food provided in the laboratory with natural foods suggest that laboratory experiments tend to capture averages, rather than the extremes, of foods eaten by primates in the wild (Vinyard et al. 2005).
The second observation is that variance components among experiments appear to be relatively low compared with those of other hierarchical levels. A similar pattern is found for patterns of activation of hyoid muscles in pigs during swallowing (German et al. in press). The low experimental variances suggest that careful electrode placement provides repeatable results and experiment-to-experiment variation in animal behavior adds little to the overall variance in EMG activity.
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SynopsisIntroductionLevels of biological variation...Sources of biological variation...Materials and methodsResultsDiscussionConclusionsSupplementary dataAcknowledgmentsReferences |
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The analysis of EMGs of jaw muscles across 14 primate species was facilitated by the relative ease of EMG as an in vivo technique and the application of a consistent EMG methodology across species. While we examined variance components, we also observed significant interspecific associations between EMG parameters of jaw muscles and the morphology of the masticatory apparatus in this same dataset. The trade-off in focusing on EMG to the exclusion of other in vivo approaches is that we cannot discern the details of muscle function at the level of the chewing cycle. While EMG describes basic muscle activity, a detailed explanation of the mechanics of jaw muscles requires the simultaneous implementation of additional techniques, such as strain gage, kinematic, and/or sonomicrometry approaches. We still see two important outcomes of this broad interspecific analysis of the EMGs of jaw muscles. First, the description of variation in EMGs both among species and across hierarchical levels can help generate novel evolutionary and functional hypotheses. Second, these descriptions highlight specific muscles and species for future studies incorporating additional in vivo techniques and/or more complicated experimental designs. Through these applications, EMG data can illuminate future studies aimed at furthering our understanding of the function and evolution of jaw muscles in primates.
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Supplementary data |
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SynopsisIntroductionLevels of biological variation...Sources of biological variation...Materials and methodsResultsDiscussionConclusionsSupplementary dataAcknowledgmentsReferences |
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Supplementary data are available at ICB online.
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Acknowledgments |
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SynopsisIntroductionLevels of biological variation...Sources of biological variation...Materials and methodsResultsDiscussionConclusionsSupplementary dataAcknowledgmentsReferences |
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Thanks to Nicolai Konow and Shannon Gerry for the invitation to participate in the symposium, "Electromyography Interpretation and Limitations in Functional Analyses of Musculoskeletal Systems." Thanks to Kirk Johnson for his assistance with much of the primary data collection and manipulation. Thanks also to B. Armfield, A. Doherty, N. Friedman, A. Mork, C. Ross, M. Ravosa, C. Thompson, and H. Wasserman for assisting in data collection from several of these species. We thank Ryan Seltzer and Victor Heh for assistance with the statistical design. Thanks to Kirk Johnson, Matt Ravosa, Tim Griffin, Andrea Taylor, Daniel Schmitt, and Patricia Vinyard for numerous helpful discussions. This article benefitted from the comments of three anonymous reviewers and H. Heatwole provided numerous stylistic changes. The veterinary staffs at the Duke University Lemur Center, Duke University Medical Center, and NEOUCOM provided animal care and surgical assistance. These data were collected with support from NSF (BCS-01-38565, SBR-9701425, BCS-0094666, SBR-9420764, BNS-91-00523, BCS-0094522, BCS-0552285), NIH (DE04531, DE05595, DE05663), and the Ohio Board of Regents. EMG data were collected with products from Grass Technologies.
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Footnotes |
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From the symposium "Electromyography: Interpretation and Limitations in Functional Analyses of Musculoskeletal Systems" presented at the annual meeting of the Society for Integrative and Comparative Biology, January 2–6, 2008, at San Antonio, Texas.
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Agrawal KR, Lucas PW. A review: neural control of mastication in humans as influenced by food texture. Indian J Dent Res (2002) 13::125–34.[Medline]
Agrawal KR, Lucas PW, Bruce IC, Prinz JF. Food properties that influence neuromuscular activity during human mastication. J Dent Res (1998) 77::1931–8.
Ahlgren J. Mechanism of Mastication. Acta Odontol Scand (1966) 24::1–109.
Anapol FC, Herring SW. Ontogeny of histochemical fiber types and muscle function in the masseter muscle of miniature swine. Am J Phys Anthropol (2000) 112::595–613.[CrossRef][Web of Science][Medline]
Antón SC. Macaque masseter muscle: internal architecture, fiber length, and cross-sectional area. Int J Primatol (1999) 20::441–62.[CrossRef]
Basmajian JV, De Luca CJ. Muscles alive: their functions revealed by electromyography (1985) Baltimore: Williams & Wilkins.
Bouvier M. A biomechanical analysis of mandibular scaling in Old World monkeys. Am J Phys Anthropol (1986) 69::473–82.[CrossRef][Web of Science]
Buzinelli RV, Berzin F. Electromyographic analysis of fatigue in temporalis and masseter muscles during continuous chewing. J Oral Rehabil (2001) 28::1165–7.[CrossRef][Web of Science][Medline]
Cachel SM. A functional analysis of the primate masticatory system and the origin of the anthropoid post-orbital septum. Am J Phys Anthropol (1979) 50::1–18.[CrossRef][Web of Science]
Clark RW, Luschei ES, Hoffman DS. Recruitment order, contractile characteristics, and firing patterns of motor units in the temporalis muscle of monkeys. Exp Neurol (1978) 61::31–52.[CrossRef][Web of Science][Medline]
Daegling DJ. Biomechanics of cross-sectional size and shape in the hominoid mandibular corpus. Am J Phys Anthropol (1989) 80::91–106.[CrossRef][Web of Science][Medline]
Dennis JC, Ungar PS, Teaford MF, Glander KE. Dental topography and molar wear in Alouatta palliata from Costa Rica. Am J Phys Anthropol (2004) 125::152–61.[CrossRef][Web of Science][Medline]
Fleagle JC. Primate adaptation and evolution (1999) New York: Academic.
Foster KD, Woda A, Peyron MA. Effect of texture of plastic and elastic model foods on the parameters of mastication. J Neurophysiol (2006) 95::3469–79.
Gaillard JM, Delorme D, Boutin JM, Van Laere G, Boisaubert B, Pradel R. Roe deer survival patterns – a comparative-analysis of contrasting populations. J Anim Ecol (1993) 62::778–91.[CrossRef]
Gans C, Gorniak GC. Electromyograms are repeatable: precautions and limitations. Science (1980) 210::795–7.
German RZ, Crompton AW, McCluskey C, Thexton AJ. Coordination between respiration and deglutition in a preterm infant mammal, Sus scrofa. Arch Oral Biol (1996) 41::619–22.[CrossRef][Web of Science][Medline]
German RZ, Crompton AW, Thexton AJ. Variation in EMG activity: a hierarchical approach. In: Int Comp Biol (2008) doi:10.1093/icb/icn022.
Herring SW. Mastication and maturity: a longitudinal study in pigs. J Dent Res (1977) 56::1377–82.
Herring SW. The ontogeny of mammalian mastication. Am Zool (1985) 25::339–49.[Web of Science]
Herring SW. Muscles of mastication: architecture and functional organization. In: The biological mechanisms of tooth movement and craniofacial adaptation—Davidovitch Z, ed. (1992) Columbus, OH: Ohio State University. 541–8.
Herring SW, Anapol FC, Wineski LE. Motor-unit territories in the masseter muscle of infant pigs. Arch Oral Biol (1991) 36::867–73.[CrossRef][Web of Science][Medline]
Herring SW, Grimm AF, Grimm BR. Functional heterogeneity in a multipinnate muscle. Am J Anat (1979) 154::563–76.[CrossRef][Web of Science][Medline]
Herring SW, Wineski LE. Development of the masseter muscle and oral behavior in the pig. J Exp Zool (1986) 237::191–207.[CrossRef][Web of Science][Medline]
Herring SW, Wineski LE, Anapol FC. Neural organization of the masseter muscle in the pig. J Comp Neurol (1989a) 280::563–76.[CrossRef][Web of Science][Medline]
Herring SW, Wineski LE, Anapol FC. Organization of the masseter muscle and nerve. In: Trends in vertebrate morphology—Splechtna H, Hilgers H, eds. (1989b) New York: Gustav Fischer. 318–20.
Hiiemae KM. Mammalian mastication: a review of the activity of the jaw muscles and the movements they produce in chewing. In: Development, function and evolution of teeth—Butler PM, Joysey KA, eds. (1978) London: Academic Press. 361–98.
Hiiemae K. Functional aspects of primate jaw morphology. In: Food acquisition and processing in primates—Chivers DJ, Wood BA, Bilsborough A, eds. (1984) New York: Plenum. 257–81.
Hiiemae KM. Feeding in mammals. In: Feeding—Schwenk K, ed. (2000) New York: Academic. 411–48.
Hiiemae KM, Kay RF. Trends in the evolution of primates mastication. Nature (1972) 240::486–7.[CrossRef][Web of Science][Medline]
Hiiemae KM, Kay RF. Evolutionary trends in the dynamics of primate mastication. Symposia of the fourth international congress of primatology. In: In: Craniofacial Biology of Primates (1973) Vol. 3:. Basel: S. Karger. 28–64.
Hoh JFY. ‘Superfast’ or masticatory myosin and the evolution of jaw-closing muscles of vertebrates. J Exp Biol (2002) 205::2203–10.
Horio T, Kawamura Y. Effects of texture of food on chewing patterns in the human subject. J Oral Rehabil (1989) 16::177–83.[Web of Science][Medline]
Huang X, Zhang G, Herring SW. Effects of oral sensory afferents on mastication in the miniature pig. J Dent Res (1993) 72::980–6.
Huang X, Zhang G, Herring SW. Age changes in mastication in the pig. Comp Biochem Physiol (1994) 107A::647–54.[Medline]
Hulbert SH. Pseudoreplication and the design of ecological field experiments. Ecol Monogr (1984) 54::187–211.[CrossRef][Web of Science]
Hylander WL. Mandibular function in Galago crassicaudatus and Macaca fascicularis: An in vivo approach to stress analysis of the mandible. J Morphol (1979a) 159::253–96.[CrossRef][Web of Science][Medline]
Hylander WL. The functional significance of primate mandibular form. J Morphol (1979b) 160::223–40.[CrossRef][Web of Science][Medline]
Hylander WL. An experimental analysis of temporomandibular joint reaction force in macaques. Am J Phys Anthropol (1979c) 51::433–56.[CrossRef][Web of Science][Medline]
Hylander WL. Functional anatomy and biomechanics of the masticatory apparatus. In: TMDs: an evidence-based approach to diagnosis and treatment—Laskins DM, Greene CS, Hylander WL, eds. (2006) Chicago: Quintessence. 3–34.
Hylander WL, Johnson KR. Temporalis and masseter muscle function during incision in macaques and humans. Int J Primatol (1985) 6::289–322.
Hylander WL, Johnson KR. Modelling relative masseter force from surface electromygrams during mastication in non-human primates. Arch Oral Biol (1993) 38::233–40.[CrossRef][Web of Science][Medline]
Hylander WL, Johnson KR. Jaw muscle function and wishboning of the mandible during mastication in macaques and baboons. Am J Phys Anthropol (1994) 94::523–47.[CrossRef][Web of Science][Medline]
Hylander WL, Johnson KR, Crompton AW. Loading patterns and jaw movements during mastication in Macaca fascicularis: a bone-strain, electromyographic, and cineradiographic analysis. Am J Phys Anthropol (1987) 72::287–314.[CrossRef][Web of Science][Medline]
Hylander WL, Ravosa MJ, Ross CF, Johnson KR. Mandibular corpus strain in primates: further evidence for a functional link between symphyseal fusion and jaw-adductor muscle force. Am J Phys Anthropol (1998) 107::257–71.[CrossRef][Web of Science][Medline]
Hylander WL, Ravosa MJ, Ross CF, Wall CE, Johnson KR. Symphyseal fusion and jaw-adductor muscle force: an EMG study. Am J Phys Anthropol (2000) 112::469–92.[CrossRef][Web of Science][Medline]
Hylander WL, Vinyard CJ, Ravosa MJ, Ross CF, Wall CE, Johnson KR. Jaw adductor force and symphyseal fusion. In: Shaping primate evolution: papers in honor of Charles Oxnard—Anapol F, German R, Jablonski N, eds. (2004) Cambridge: Cambridge University Press. 229–57.
Hylander WL, Vinyard CJ, Wall CE, Williams SH, Johnson KR. Convergence of the "wishboning" jaw-muscle activity pattern in anthropoids and strepsirrhines: the recruitment and firing of jaw muscles in Propithecus verreauxi. Am J Phys Anthropol (2003) (36 Suppl):120.
Hylander WL, Wall CE, Vinyard CJ, Ross C, Ravosa MR, Williams SH, Johnson KR. Temporalis function in anthropoids and strepsirrhines: an EMG study. Am J Phys Anthropol (2005) 128::35–56.[CrossRef][Web of Science][Medline]
Khuri AI. Designs for variance components estimation: past and present. Int Stat Rev (2000) 68::311–22.[CrossRef]
King SJ, Arrigo-Nelson SJ, Pochron ST, Semprebon GM, Godfrey LR, Wright PC, Jernvall J. Dental senescence in a long-lived primate links infant survival to rainfall. Proc Natl Acad Sci USA (2005) 102::16579–83.
Kojola I, Helle T, Huhta E, Nivo A. Foraging conditions, tooth wear and herbivore body reserves: a study of female reindeer. Oecologia (1998) 117::26–30.[CrossRef][Web of Science]
Korfage JAM, Koolstra JH, Langenbach GEJ, van Eijden TMGJ. Fiber-type composition of the human jaw muscles-(Part 1). Origin and functional significance of fiber-type diversity. J Dent Res (2005) 84::774–83.
Langenbach GEJ, van Eijden TMGJ. Mammalian feeding motor patterns. Am Zool (2001) 41::1338–51.[CrossRef][Web of Science]
Langenbach GEJ, Weijs WA. Growth patterns of the rabbit masticatory muscles. J Dent Res (1990) 69::20–5.
Lanyon JM, Sanson GD. Koala (Phascolarctos cinerus) dentition and nutrition. II. Implications of tooth wear in nutrition. J Zool Lond (1986) 209::169–81.
Lauder GV, et al. How are feeding systems integrated and how have evolutionary innovations been introduced? Group Report. In: Complex organismal functions: integration and evolution in vertebrates—Wake DB, Roth G, eds. (1989) New York: John Wiley & Sons. 97–115.
Leone FC, Nelson LS, Johnson NL, Eisenstat S. Sampling distributions of variance components I. Empirical studies of unbalanced nested designs. Technometrics (1968) 10::719–37.[CrossRef][Web of Science]
Liem KF. Aquatic versus terrestrial feeding modes: possible impacts on the trophic ecology of vertebrates. Am Zool (1990) 30::209–21.[Web of Science]
Loeb GE, Gans C. Electromyography for experimentalists (1986) Chicago: University of Chicago Press.
Lund JP. Mastication and its control by the brain stem. Crit Rev Oral Biol Med (1991) 2::33–64.
Lund JP, Smith AM, Sessle BJ, Murakami T. Activity of trigeminal 
- and 
-motoneurons and muscle afferents during performance of a biting task. J Neurophysiol (1979) 42::710–25.
Luschei ES, Goodwin GM. Patterns of mandibular movement and jaw muscle activity during mastication in the monkey. J Neurophysiol (1974) 37::954–66.
Manns A, Miralles R, Palazzi C. EMG, bite force and elongation of the masseter muscle under isometric voluntary contractions and variations of vertical dimension. J Prosthet Dent (1979) 42::674–82.[CrossRef][Web of Science][Medline]
Maynard Smith J, Savage JG. The mechanics of mammalian jaws. Sch Sci Rev (1959) 40::289–301.[Medline]
Miller AJ, Farias M. Histochemical and electromyographic analysis of craniomandibular muscles in the rhesus monkey, Macaca mulatta. J Oral Maxillofac Surg (1988) 46::767–76.[Web of Science][Medline]
Mioche L, Bourdiol P, Martin JF, Noel Y. Variations in human masseter and temporalis muscle activity related to food texture during free and side-imposed mastication. Arch Oral Biol (1999) 44::1005–12.[CrossRef][Web of Science][Medline]
Møller E. The chewing apparatus. Acta Physiol Scand (1966) 280:(69 Suppl):1–229.
Olmsted MJ, Wall CE, Vinyard CJ, Hylander WL. Human bite force: the relation between EMG activity and bite force at a standardized gape. Am J Phys Anthropol Suppl (2005) 40::160–1.
Olson LE, Sargis EJ, Martin RD. Intraordinal phylogenetics of treeshrews (Mammalia: Scandentia) based on evidence from the mitochondrial 12S rRNA gene. Mol Phyl Evol (2005) 35::656–73.[CrossRef][Web of Science][Medline]
Oron U, Crompton AW. A cineradiographic and electromyographic study of mastication in Tenrec ecaudatus. J Morph (1985) 185::155–82.[CrossRef][Medline]
Ottenhoff FAM, van der Bilt A, van der Glas HW, Bosman F. Control of elevator muscle activity during simulated chewing with varying food resistance in humans. J Neurophysiol (1992) 68::933–44.
Ottenhoff FAM, van der Bilt A, van der Glas HW, Bosman F. Control of human jaw elevator muscle activity during simulated chewing with varying bolus size. Exp Brain Res (1993) 96::501–12.[Web of Science][Medline]
Ottenhoff FAM, van der Bilt A, van der Glas HW, Bosman F, Abbink JH. The relationship between jaw elevator muscle surface electromyogram and simulated food resistance during dynamic condition in humans. In: J Oral Rehab (1996) 23::270–9.[Web of Science][Medline]
Perry JMG, Wall CE. Scaling of the chewing muscles in prosimians. In: Primate craniofacial function and biology—Vinyard CJ, Ravosa MJ, Wall CE, eds. New York: Springer. in press.
Peyron MA, Lassauzay C, Woda A. Effects of increased hardness on jaw movement and muscle activity during chewing of visco-elastic model foods. Exp Brain Res (2002) 142::41–51.[CrossRef][Web of Science][Medline]
Pruim GJ, Ten Bosch JJ, de Jongh HJ. Jaw muscle emg-activity and static loading of the mandible. J Biomech (1978) 11::389–95.[CrossRef][Web of Science][Medline]
Ravosa MJ. Structural allometry of the prosimian mandibular corpus and symphysis. J Hum Evol (1991) 20::3–20.[CrossRef][Web of Science]
Ravosa MJ, Vinyard CJ, Gagnon M, Islam SA. Evolution of anthropoid jaw loading and kinematic patterns. Am J Phys Anthropol (2000) 112::493–516.[CrossRef][Web of Science][Medline]
Ross CF. Into the light: the origin of Anthropoidea. Ann Rev Anthropol (2000) 29::147–94.[CrossRef][Web of Science]
Ross CF. In vivo function of the craniofacial haft: the interorbital "pillar". Am J Phys Anthropol (2001) 116::108–39.[CrossRef][Web of Science][Medline]
Ross CF, Dharia R, Herring SW, Hylander WL, Liu ZJ, Rafferty KL, Ravosa MJ, Williams SW. Modulation of mandibular loading and bite force in mammals during mastication. J Exp Biol (2007) 210::1046–63.
Ross CF, Hylander WL. Electromyography of the anterior temporalis and masseter muscles of owl monkeys (Aotus trivirgatus) and the function of the postorbital septum. Am J Phys Anthropol (2000) 112::455–68.[CrossRef][Web of Science][Medline]
Searle SR, Casella G, McCulloch CE. Variance components (2006) New York: Wiley.
Shaffer HB, Lauder GV. Aquatic prey capture in ambystomatid salamanders: patterns of variation in muscle activity. J Morphol (1985) 183::273–84.[CrossRef][Web of Science][Medline]
Skogland T. Tooth wear by food limitation and its life-history consequences in wild reindeer. Oikos (1988) 51::238–42.[CrossRef][Web of Science]
Smith KK. Are neuromotor systems conserved in evolution? Brain Behav Evol (1994) 43::293–305.[Web of Science][Medline]
Sokal RR, Rohlf FJ. Biometry (1995) New York: W.H. Freeman.
Spencer MA. Force production in the primate masticatory system: electromyographic tests of biomechanical hypotheses. J Hum Evol (1998) 34::25–54.[CrossRef][Web of Science][Medline]
Taylor AB. Masticatory form and function in African apes. Am J Phys Anthropol (2002) 117::133–56.[CrossRef][Web of Science][Medline]
Thompson CL, Jackson EM, Stimpson CD, Vinyard CJ. Assessing how experimental and surgical manipulations during in vivo laboratory research influence chewing speed in tufted capuchins (Cebus apella). Am J Phys Anthropol (2007) (44 Suppl):231.
Thompson WA, Moore JR. Non-negative estimates of variance components. Technometrics (1963) 5::441–9.[CrossRef][Web of Science]
Turnbull WD. Mammalian Masticatory Apparatus. Fieldiana:. Geology (1970) 18::148–356.
van Eijden TMGJ, Blanksma NG, Brugman P. Amplitude and timing of EMG activity in the human masseter muscle during selected motor tasks. J Dent Res (1993) 72::599–606.
van Eijden TMGJ, Korfage JAM, Brugman P. Architecture of the human jaw-closing and jaw-opening muscles. Anat Rec (1997) 248::464–74.[CrossRef][Medline]
van Eijden TMGJ, Turkawski SJJ. Morphology and physiology of masticatory muscle units. Crit Rev Oral Biol Med (2001) 12::76–91.
Vinyard CJ, Williams SH, Wall CE, Johnson KR, Hylander WL. Jaw-muscle electromyography during chewing in Belanger's treeshrews (Tupaia belangeri). Am J Phys Anthropol (2005) 127::26–45.[CrossRef][Web of Science][Medline]
Vinyard CJ, Wall CE, Williams SH, Johnson KR, Hylander WL. Masseter electromyography during chewing in ring-tailed lemurs (Lemur catta). Am J Phys Anthropol (2006) 130::85–95.[CrossRef][Web of Science][Medline]
Vinyard CJ, Ravosa MJ, Wall CE, Williams SH, Johnson KR, Hylander WL. Jaw-muscle function and the origin of primates. In: Primate origins and adaptations—Ravosa MJ, Dagosto M, eds. (2007) New York: Kluwer Press. 179–231.
Vinyard CJ, Yamashita N, Tan C. Linking laboratory and field approaches in studying the evolutionary physiology of biting in bamboo lemurs. In: Int J Primatol. in press.
Wainwright PC. The evolution of feeding motor patterns in vertebrates. Curr Opin Neuro (2002) 12::691–5.[CrossRef]
Wainwright PC, Friel JP. Behavioral characters and historical properties of motor patterns. In: The character concept in evolutionary biology—Wagner G, ed. (2001) San Diego: Academic Press. 285–301.
Wall CE. A model of temporomandibular joint function in anthropoid primates based on condylar movements during mastication. Am J Phys Anthropol (1999) 109::67–88.[CrossRef][Web of Science][Medline]
Wall CE, Perry JMG, Briggs M, Schachat F. Mechanical correlates of sexual dimorphism in the jaw muscles and bones of baboons. In: Am J Phys Anthropol (2007) 132,S44:242.
Wall CE, Vinyard CJ, Johnson KR, Williams SH, Hylander WL. Phase II jaw movements and masseter muscle activity during chewing in Papio anubis. Am J Phys Anthropol (2006) 129::215–24.[CrossRef][Web of Science][Medline]
Vinyard CJ, Ravosa MJ, Wall CE. Specialization of the superficial anterior temporalis for mastication of hard foods in baboons. In: Primate craniofacial function and biology. New York: Springer. in press.
Weijs WA. Evolutionary approach of masticatory motor patterns in mammals. Adv Comp Environ Physiol (1994) 18::282–320.
Weijs WA, Brugman P, Grimbergen CA. Jaw movements and muscle activity during mastication in growing rabbits. Anat Rec (1989) 224::407–16.[CrossRef][Medline]
Williams SH, Sidote JV. Ontogeny of rhythmic chewing and masseter activity in a selenodont artiodactyl. In: Proceedings of the Society for Integrative and Comparative Biology (2008) January. 2-6 in San Antonio, TX (http://www.sicb.org/meetings/2008/schedule).
Williams SH, Wright BW, Truong VD, Daubert CR, Vinyard CJ. Mechanical properties of foods used in experimental studies of primate masticatory function. Am J Primatol (2005) 67::329–46.[CrossRef][Web of Science][Medline]
Williams SH, Vinyard CJ, Glander KE, Deffenbaugh M, Teaford M, Thompson CL. A preliminary report on a telemetry system for assessing jaw-muscle function in free-ranging primates. In: Int J Primatol. in press.
Woda A, Foster K, Mishellany A, Peyron MA. Adaptation of healthy mastication to factors pertaining to the individual or to the food. Physiol Behav (2006) 89::28–35.[CrossRef][Medline]
Yemm R. The orderly recruitment of motor units of the masseter and temporal muscles during voluntary isometric contraction in man. J Physiol (1977) 265::163–74.
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