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Full Length Article
Occlusal Development and Masseter Activity in Alpacas (Lama pacos)
Article first published online: 6 NOV 2009
Copyright © 2009 Wiley-Liss, Inc.
The Anatomical Record
Volume 293, Issue 1, pages 126–134, January 2010
How to Cite
Williams, S. H., Sidote, J. and Stover, K. K. (2010), Occlusal Development and Masseter Activity in Alpacas (Lama pacos). Anat Rec, 293: 126–134. doi: 10.1002/ar.21016
- Issue published online: 28 DEC 2009
- Article first published online: 6 NOV 2009
- Manuscript Accepted: 10 JUL 2009
- Manuscript Received: 2 MAR 2009
- National Science Foundation. Grant Numbers: IOB-0520855, BCS-0241652
- tooth eruption;
Tooth eruption and the development of occlusion are significant ontogenetic changes in the masticatory apparatus of mammals. Here, we test the hypothesis that changes in masseter activity are correlated with increased occlusal contacts at major stages of dental development in the alpaca, Lama pacos. We compare electromyographic data from the superficial and deep masseter in infant and juvenile alpacas prior to and following m1 occlusion and from adults with full permanent dentitions. The pre-m1 and post-m1 occlusion groups exhibit similar masseter activity durations, chewing cycle durations, and with the exception of the balancing-side deep masseter, similar timing differences between the jaw muscles. On average, the balancing-side deep masseter fires significantly later in the post-m1 occlusion group. The m2–m3 group exhibits significantly longer chewing cycle length and an even later firing balancing-side deep masseter. Increased occlusion is also associated with an increase in the relative amount of working-side superficial and deep masseter muscle activity when compared with the balancing side muscles. Although the development of occlusal relations in infant and juvenile alpacas are associated with minor changes in masseter activation patterns, additional molar occlusal contacts increase chewing cycle duration resulting in concomitant changes in masseter recruitment patterns. Currently, we cannot rule out that musculoskeletal development influences masseter activity as demonstrated in other mammals. However, the data presented here indicate that alpacas have a relatively delayed onset of the adult motor pattern that may be correlated with changes in occlusal relations due to tooth eruption. Anat Rec, 2010. © 2009 Wiley-Liss, Inc.
The ontogeny of oral function has been of continued interest to researchers studying the development of muscle coordination and motor control. Mastication, in particular, is a behavior unique to mammals that requires the development of a complex dentition and the coordinated activity of multiple muscles. Most explanations for the appearance of the chewing motor pattern focus on its similarities to suckling and maturation of the central nervous system (Lakars and Herring,1980; Herring and Wineski,1986; Iriki et al.,1988; Iinuma et al.,1991; Langenbach et al.,1992; Westneat and Hall,1992; Kobayashi et al.,2002; Inoue et al.,2007). However, there appears to be later, species-specific changes in chewing electromyograms (EMG) associated with morphological maturation of the feeding apparatus as well (e.g., Møller,1966; Herring,1977,1985a,b; Lakars and Herring,1980; Herring and Wineski,1986; Huang et al.,1994; Green et al.,1997).
One of the most pronounced changes during the development of the masticatory apparatus is the eruption of the permanent dentition and replacement of deciduous teeth. However, the effects of occlusal development on the maturation of jaw-muscle activity have received little attention. Longitudinal studies have only been conducted in pigs and rabbits. In pigs, occlusion has only a minor effect on the ontogeny of jaw-muscle EMGs during chewing. Juvenile pigs at different stages of occlusal development exhibit more or less similar jaw-muscle activation patterns, although the youngest individuals with the fewest occlusal contacts do have longer and more variable bursts of jaw-muscle activity. Continued tooth eruption and occlusion, however, are not associated with additional changes in their jaw-muscle activity patterns, suggesting that the development of jaw-muscle activity is likely unrelated to the development of occlusion (Huang et al.,1994). On the other hand, a series of ontogenetic studies in rabbits links ontogenetic changes in feeding EMGs to the development of occlusion and, as in pigs, also to changes in the biomechanics of the masticatory apparatus because of musculoskeletal growth (Langenbach and Weijs,1990; Langenbach et al.,1991). With respect to the dentition, occlusion and wear of the first molar is correlated with shifts in the relative timing between muscles, an increase in the asynchronicity of the working- and balancing-side jaw muscles, and longer activity of muscles firing late in the power stroke (Weijs et al.,1987,1989; Langenbach et al.,2001).
Differences in the effects of occlusal development on jaw-muscle activity during chewing in pigs and rabbits could be due to several factors. The most obvious factor is their difference in occlusal morphology. Pigs have a bunodont dentition consisting of relatively low cusps, whereas rabbits have lophodont teeth, in which the cusps are elongated to form shearing crests. Lophodont teeth also require wear to maintain function. This wear creates enamel ridges that affect the trajectory of the jaw and the orientation of the power stroke. Additionally, the observed differences might simply be attributed to different experimental designs. Huang et al. (1994) primarily looked at the influence of increased occlusal contacts on EMG patterns and jaw movements over a prolonged period of time. In contrast, Langenbach et al. (2001) focus on the postweaning period during which time significant occlusal wear develops to create functional occlusal relations. Thus, wear-induced changes in occlusal topography are argued to play a role in some of the early changes in jaw-muscle activity in rabbits.
In this study, we evaluate the extent to which occlusal development is associated with changes in masseter activation patterns in the alpaca (Lama pacos), a South American camelid artiodactyl. Alpacas are typical selenodont artiodactyls in having cheek teeth in which the enamel invaginates between the cusps and the cusps are elongated anteroposteriorly to create multiple enamel cutting ridges. Tooth eruption and replacement in alpacas is a relatively slow process, and therefore animals have prolonged periods of transitional dentitions. For example, neonatal alpacas typically have two deciduous premolars that come into occlusion shortly after birth. The first (permanent) molars (m1) come into occlusion around 9 months. The second molars (m2) come into occlusion significantly later, between 1.5 and 2 years, followed by the third molars (m3), between 2.5 and 3.5 years. Finally, the deciduous premolars are replaced between 3.5 and 5 years with one to two permanent premolars (Fowler,1998; Anderson,2006).
We focus specifically on the ontogeny of masseter recruitment patterns because this muscle has a primary role in generating occlusal force and transverse jaw movement during chewing in selenodont artiodactyls (De Vree and Gans,1976; Williams et al.,2007). Therefore, if ontogenetic changes in chewing EMGs occur, they are expected to be readily apparent in this muscle. Moreover, previous research on masseter activity in alpacas has shown significant differences in the timing of activity of the superficial and deep parts of the masseter in adult alpacas to coordinate these transverse movements. Thus, investigations into the ontogeny of masseter activity will provide insight into the development of functional compartmentalization observed in adults and complement studies on other species showing that intramuscular functional maturation may be delayed.
The first major change in occlusal relations that may influence jaw-muscle function occurs with occlusion of m1 in the juvenile alpacas. We also expect the jaw-muscle EMGs in adult alpacas with a full dentition to differ from the infant (pre-m1) and juvenile (post-m1) individuals. Occlusal development in alpacas is expected to be associated with changes in masseter EMG patterns reflecting changes in fast-closing and power stroke duration, overall chewing cycle duration, and muscle recruitment levels. Increased molar occlusion is expected to increase power stroke length. Because the working-side (i.e., chewing-side) superficial masseter and balancing-side (i.e., nonchewing-side) deep masseter facilitate jaw movements during the power stroke toward the balancing-side, these muscles may exhibit longer average durations of activity than the working-side deep masseter and balancing-side superficial masseter in animals at more advanced occlusal stages. This in turn may increase the total chewing cycle duration during ontogeny unless there are concomitant changes in opening and/or fast-closing duration.
In contrast, there may be no differences in the order of recruitment of the jaw muscles as there is no a priori reason to believe that patterns of coordination change. Adult alpacas exhibit significant differences in the timing of the working- and balancing-side superficial and deep masseter muscles, but the firing pattern is consistent across individuals (Williams et al.,2007). Thus, infant and juvenile alpacas are expected to exhibit the adult masseter contraction patterns characterized by an early firing working-side deep masseter, followed by the balancing-side superficial masseter, working-side superficial masseter, and balancing-side deep masseter. If increased occlusal contacts increase power stroke length, then we may see an increase in the asynchrony of the jaw muscles (but the same firing order), and most notably an increase in the delay of the balancing-side deep masseter as this muscle is thought to be integral in lengthening the power stroke. Finally, increased contribution of the balancing-side muscles may coincide with occlusal development as a result of more thorough processing of food and the need to concentrate more force over a larger occlusal surface area.
MATERIALS AND METHODS
Masseter EMGs were sampled from five alpacas (two males and three females) over the course of 13 months, starting at approximately 5 weeks of age. All animals weaned naturally around 6 months but consumed solid foods using rhythmic mastication starting at around 1 month of age. All individuals exhibited normal tooth eruption patterns, as verified by either CT scanning, radiography, or visual inspection. Because of the relatively slow tooth replacement and eruption in alpacas, we grouped the experiments according to major transitions in the dentition. Specifically, the pre-m1 group consisted of experiments conducted prior to occlusion of the first molars. The post-m1 group consisted of experiments conducted following occlusion of the first molars, with no additional occlusal development. Previously recorded masseter EMG data from adult alpacas (Williams,2004; Williams et al.,2007) was also included in the study. This group, the m2–m3 group, consisted of 4 animals with a full complement of evenly but not excessively worn teeth (Fig. 1). All procedures performed on animals were approved by the Ohio University and the Duke University Institutional Animal Care and Use Committees.
Electrode Insertion and EMG Recording
Electromyograms from the left and right superficial and deep masseters were recorded using indwelling fine-wire bipolar electrodes. The electrodes were constructed with approximately 30-cm segments of nylon-insulated nickel–chromium alloy wire (California Fine Wire). Approximately 1 mm of insulation was removed from the tips of the individual electrode wires. The noninsulated electrode tip was inserted into the tip of a sterile 25-gauge needle. The electrode wires were then bent back to lie parallel to the shaft of the needle, creating small hooks in the terminal portion of the wires. The jaw muscles of a 6-month-old alpaca were dissected to determine the angle and location of insertion for proper intramuscular electrode placement in the superficial masseter and deep portions of the masseter in the infants.
Prior to insertion of electrodes, alpacas were sedated with an intramuscular injection of ketamine (5 mg/kg), butorphanol (0.5 mg/kg), and xylazine (0.05 mg/kg) (Mama,2000). The animals were then shaved, and the surface of the skin was cleaned with alcohol swabs. Electrodes were inserted into the superficial masseter by positioning the tip of the needle approximately 2 cm anterior to the angle of the mandible at approximately the level of the alveolar margin. The needle holding the electrode was then inserted into the muscle by aiming toward the mandibular angle until the tip contacted the bone. For the deep masseter, the needle was positioned just anterior to the mandibular condyle and below the zygomatic arch and then inserted into the muscle by aiming downward toward the ramus at a 30-degree to 45-degree angle from the surface of the skin. Following electrode insertion into the target muscle, the needle was removed as the wires were held against the skin leaving the electrode in the bulk of the muscle. Electrode placement was not verified by dissection because the animals were not sacrificed.
Once all electrodes were inserted, the free ends were connected via pins and a WPI connector to Grass HZP high impedance probes and Grass A-C high gain amplifiers (Model P511), in which the EMG signals were simultaneously amplified (×200–10,000) and filtered (bandpass, 100–3,000 Hz). Amplified and filtered EMG potentials were recorded directly to a Dell Precision 650 running Labview 8.0 outfitted with a National Instruments A/D Card (PCI-6071E) at 10,000 Hz per channel. Once the animals were fully alert and standing, they were fed hay. EMGs during rhythmic chewing on both left and right sides were recorded until the animal refused to eat or until sufficient data were collected. EMGs from the superficial and deep masseters were sampled bilaterally in each experiment. Chewing-side was noted for each sequence recorded. After sufficient data were recorded, the electrodes were gently removed and the animals were returned to their stall or pasture where they received food ad libitum in between experiments.
EMG Data Analysis
Chewing sequences exhibiting rhythmic mastication were selected from each experiment for analysis. When possible, attempts were made to select both left and right chewing sequences from each experiment. The raw EMGs of selected chewing sequences were transformed into a single, positive waveform by calculating the root-mean-square (rms) using a 42-msec time constant in 2-msec intervals (Hylander and Johnson,1994). Five variables were calculated from the rms waveforms. The chewing cycle duration was calculated as the time between 100% of peak EMG activity in the working-side superficial masseter of two consecutive rhythmic chews on the same side (Fig. 2A). Individual working- and balancing-side superficial and deep masseters activity durations were calculated for each chew as the time from 25% of peak EMG activity during the onset of the muscle to 25% of peak EMG during the offset of the muscle (see Fig. 2A). Finally, total masseter activity duration was calculated as the time between the first muscle to reach 25% of peak EMG during onset and the last muscle to reach 25% during offset for each chewing cycle (Fig. 2B). Timing differences between the jaw muscles were calculated at 100% of peak EMG. To determine the order the time at which each muscle reached 100% of peak EMG was calculated relative to a reference muscle, the working-side superficial masseter, which was set to reach 100% peak EMG at time 0 (see Fig. 2B). From these data, timing differences between any two muscles can be determined. When the peak activity of a muscle occurred prior to 100% of peak EMG of the working-side superficial masseter, the timing difference was assigned a positive value. When the peak activity of a muscle followed 100% of peak EMG of the working-side superficial masseter, the timing difference was assigned a negative value.
Finally, to compare the relative magnitude of recruitment of working- and balancing-side muscles, we created a W/B ratio following the methods of Hylander et al. (2000). These ratios are determined by first determining the chew exhibiting the single largest rms EMG value at 100% of peak activity for each electrode within each experiment. This value was assigned a value of 1.0, yielding one value of 1.0 for each electrode within each experiment. For all remaining chews in that experiment, the rms EMG value for each electrode at 100% of peak EMG was linearly scaled to its single largest rms value. Finally, the scaled peak value of the working-side muscle was divided by the scaled peak value of the balancing-side muscle for each chew. A W/B ratio of 1.0 indicates equal amounts of relative muscle activity, and therefore equal amounts of relative recruitment. A W/B ratio of 0.5 indicates that the scaled working-side magnitude is half that of the scaled balancing-side magnitude.
Within each experiment, the average of the individual and total masseter activity durations, chewing cycle durations, peak timing differences, and W/B ratios were calculated for chewing sequences on the left and right sides separately. The left and right means were then averaged to create an experimental mean and standard deviation (SD) for each variable. The differences in each muscle activity duration and chewing cycle duration between the pre-m1, post-m1, and m2–m3 groups were assessed using a one-way ANOVA to test for significant differences in group means for each variable. For all of the significant ANOVA results, posthoc t-tests comparing all pairs were conducted. Because multiple comparisons were conducted, we used Bonferroni-adjusted probability values in lieu of the more liberal α of P < 0.05 (Rice,1989). Using the peak timing data, we conducted a t-test to determine if the jaw muscles exhibited the same peak firing time in the pre-m1 and post-m1 groups. We also determined whether the working- and balancing-side muscles fired asynchronously as in the adults.
To understand the coordination of muscles in each occlusal group, t-tests were used to compare the time of peak activity of each muscle within the pre-m1 and post-m1 groups. Working-side muscles were also compared with their balancing-side counterpart (e.g., working-side superficial masseter versus balancing-side superficial masseter), and muscles on each side were compared with each other (e.g., working-side superficial masseter versus working-side deep masseter). Finally, we also determined whether there was a change in the variability of masseter activity associated with occlusal development by comparing variances for each variable among the three groups using an F-test. Again, the more conservative Bonferroni-adjusted probability values were used.
Average individual and total masseter activity durations did not change markedly with the eruption of m1 (Table 1). The superficial masseter activity durations on the working- and balancing-sides are virtually identical in the pre-m1 and post-m1 groups. Following the occlusion of m2 and m3, the activity duration of the superficial masseter increases by approximately 20 msec on the working side and 14 msec on the balancing side. However, differences in superficial masseter activity between the occlusal groups are not significant. There is a slight but nonsignificant increase in working-side deep masseter activity duration following m1 occlusion, but virtually no change with additional occlusal contacts. On the balancing-side, deep masseter activity decreases and then increases in duration, but differences between the occlusal groups are not significant. Finally, total masseter activity duration shows the most pronounced differences with an approximately 30-msec increase in duration with the occlusion of m2 and m3. However, as with the other temporal variables, differences between groups are not significant. When working- versus balancing-side muscles are compared, only the adults have significantly longer working-side superficial masseter activity durations (P < 0.05, paired t-test). In contrast, working-side deep masseter activity durations are significantly longer than on the balancing-side in all three groups. A one-way ANOVA demonstrates significant differences in chewing cycle duration among the three groups (Table 2). This is largely due to the longer chewing cycle duration in the m2–m3 group, which is significantly longer than both the pre-m1 and m1 groups.
|Occlusal group||WS superficial masseter||WS deep masseter||BS superficial masseter||BS deep masseter||Total masseter|
|pre-m1 (N = 5)||125.89||14.31||142.34||16.95||129.71||13.80||118.57||27.97||196.96||20.26|
|post-m1 (N = 5)||127.50||14.39||150.32||15.75||127.70||16.43||108.14||8.90||191.40||19.20|
|m2–m3 (N = 4)||147.35||30.51||148.71||15.74||141.53||31.15||121.23||14.18||223.96||25.87|
|Chewing cycle duration|
|pre-m1 (N = 5)||460.98||16.96|
|post-m1 (N = 5)||476.16||32.49|
|m2–m3 (N = 4)||568.34||80.86|
|One-way ANOVA||F(2,11) = 6.39*|
|Paired comparisonsa||m2–m3 > pre-m1**|
|m2–m3 > m1*|
Peak firing order differed between the pre-m1 and post-m1 individuals (Table 3). These differences are illustrated in Fig. 3, which shows the rms EMGs from a pre-m1 and post-m1 experiment in Animal 3. In the pre-m1 group, the balancing-side superficial masseter peaks first, followed very closely by the balancing-side deep masseter and the working-side deep masseter, which fire almost simultaneously. The working-side superficial masseter is the last muscle to reach peak activity. In the post-m1 group, the balancing-side superficial masseter also peaks first, followed almost immediately by the working-side deep masseter. The working-side superficial masseter peaks next, which is then followed by the balancing-side deep masseter peaked shortly thereafter. Within each group, the working-side deep masseter and balancing-side deep masseter peak significantly earlier than the working-side superficial masseter (see Table 3). However, the timing difference between the reference muscle and the balancing-side deep masseter is not significant in either group. The timing differences between working- and balancing-side superficial masseters are significantly different in the pre-m1 (P < 0.001) and post-m1 (P < 0.002) groups, but only in the post-m1 group for the deep masseters (P < 0.019). The comparisons among occlusal groups reveal no differences in the timing of peak activity between the reference muscle and the working-side deep masseter or balancing-side superficial masseter. However, the groups differed in the relative timing of the balancing-side deep masseter (P < 0.05) (see Table 3). Finally, the comparisons among groups also reveal no differences in the offset between the balancing-side superficial and deep masseters or the working-side and balancing-side deep masseters.
|WS deep masseter||BS superficial masseter||BS deep masseter|
|Mean (msec)||SD||Mean (msec)||SD||Mean (msec)||SD|
|pre-m1 (N = 5)||19.40*||11.52||35.03***||4.95||19.22||23.58|
|post-m1 (N = 5)||33.19**||15.24||35.77**||11.81||−7.76||10.11|
|Paired t-test (pre-m1 vs. post-m1)||NS||NS||*|
W/B ratios for the three groups are presented in Table 4. The pre-m1 group has the lowest W/B ratio for superficial masseter, and thus the working-side and balancing-side superficial masseters are recruited nearly equally. In the post-m1 group, there is a tendency for the working-side superficial masseter to exhibit slightly higher levels of recruitment than the balancing-side superficial masseter. However, there are no differences between the pre-m1 and post-m1 groups in superficial masseter W/B ratios. The m2–m3 group also exhibits approximately 60% higher relative recruitment levels from the working-side superficial masseter than the balancing-side superficial masseter. Only the differences in W/B ratios between the m2–m3 and pre-m1 groups are significant. For the deep masseter, the pre-m1 group again shows the most similar working-side and balancing-side recruitment levels although the working-side deep masseter exhibits close to 75% more relative recruitment than its balancing-side counterpart. The post-m1 and m2–m3 groups have nearly identical deep masseter W/B ratios indicating a large increase in recruitment from the working-side deep masseter relative to the balancing-side deep masseter. Individuals in these two groups show more than twice the amount of relative recruitment from the working-side deep masseter.
|Superficial masseter||Deep masseter|
|Mean (msec)||SD||Mean (msec)||SD|
|pre-m1 (N = 5)||1.03||0.13||1.73||0.21|
|post-m1 (N = 5)||1.16||0.19||2.27||0.59|
|m2−m3 (N = 4)||1.57||0.43||2.29||0.55|
|One-way ANOVA||F(2,11) = 4.89*||NS|
|Paired comparisonsa||m2–m3 > pre-m1*|
There are no significant differences in the variance of the individual and total muscle activity durations, chewing cycle duration, or peak timing of the masseter components between the pre-m1, post-m1, or m2–m3 groups (P > 0.05 in all comparisons).
One of the most significant ontogenetic changes in the anatomy and morphology of the mammalian masticatory apparatus involves the eruption of the permanent dentition. In ungulate herbivores, wear-induced changes in occlusal surface topography also occur throughout life, starting with early ontogeny when the teeth come into occlusion. Wear creates and maintains the functional shape of the tooth, with function typically decreasing with excessive wear (Lumsden and Osborn,1977; Fortelius,1985). To date, only two studies have addressed quantitatively the effects of structural and functional changes in the dentition on jaw-muscle EMGs during mastication (Weijs et al.,1987,1989; Huang et al.,1994; Langenbach et al.,2001). The studies on pigs indicate that jaw-muscle activation patterns are altered very little during sequential phases of tooth eruption and occlusion (Huang et al.,1994). In contrast, rabbits exhibit more pronounced changes in chewing EMGs associated with molar occlusion and wear (Weijs et al.,1987,1989; Langenbach et al.,2001). The results presented here for alpacas are also mixed. As in rabbits, we expected changes associated with the occlusion of the first permanent molar because it expands the surface area for chewing tough and fibrous food. However, there are few changes in jaw-muscle EMGs correlated with the transition to this stage of dental and occlusal development. There are no changes in muscle activity durations, chewing cycle duration, or in the relative magnitude of working- or balancing-side recruitment levels. There are also no differences in the separation of the working- and balancing-side muscles. Thus, in general, many aspects of masseter behavior appear to be maintained for a significant period of time until further occlusal development. In this regard, our results are similar to those found by Huang et al. (1994).
The occlusion of additional teeth, in particular m2–m3, results in subtle changes in jaw-muscle recruitment patterns. The adults have longer superficial masseter activity durations, longer total activity durations (as a result of longer superficial masseter activity durations), and longer chewing cycle durations, although only the latter are significantly different from the pre-m1 and post-m1 groups. All of the adults in this study had a full permanent dentition and thus had undergone not only the eruption of two additional molars but also replaced their premolars. Because of the substantial change in the dentition, it is difficult to determine exactly when the longer muscle activity durations and chewing cycle durations were attained. Weijs et al. (1989) also observed an increase in chewing cycle duration in adult rabbits when compared with infants, but no additional increase in power stroke length. Thus, an increase in chewing cycle duration in the adult rabbits is attributed primarily to a longer period of jaw opening. In this regard, rabbits and alpacas may differ. In alpacas, the jaw muscles exhibit increased masseter activity durations following m2–m3 occlusion and a proportional increase in chewing cycle duration. This is best demonstrated by scaling the duration of masseter activity to chewing cycle duration. Relative muscle activity durations are virtually identical in the pre-m1, post-m1, and m2–m3 groups (Fig. 4). For example, in all three groups, the working-side superficial masseter is active for approximately 27% of the chewing cycle. Moreover, the working-side and balancing-side superficial masseters always have similar activity durations, whereas the working-side deep masseter is always active longer than its balancing-side counterpart.
Although there are no changes in muscle durations following m1 occlusion, there were some notable changes in both the timing and relative magnitude of activity of the balancing-side deep masseter. Specifically, young alpacas shift the timing of activity of their balancing-side deep masseter to later in the power stroke, converging on the approximately 40-msec delay relative to the working-side superficial masseter observed in the adult (see Fig. 4 in Williams et al.,2007). This shift in timing increases the asynchrony between the balancing-side deep masseter relative and its working-side counterpart in the post-m1 group and relative to the balancing-side superficial masseter. Thus, both intermuscular and intramuscular timing differences increase because of the shift in timing of this muscle. This is even more pronounced in the m2–m3 group because of an earlier firing working-side deep masseter and later firing balancing-side deep masseter (relative to the superficial masseter) (Williams et al.,2007). Weijs (1994) has suggested that asynchrony of these two muscles in herbivores guides the early and late transverse jaw movements during fast-closing and the power stroke, respectively, and correlated kinematic data in adult alpacas support this hypothesis (Williams et al.,2007). In contrast to the m2–m3 group, on average, a delay in the timing of the balancing-side deep masseter does not increase the duration of jaw-closing (fast-closing and power stroke) in the post-m1 group when compared with the pre-m1 group (see Table 3).
In contrast to studies in other mammals, most notably in primates, the delay in activity of the balancing-side deep masseter is not coupled with increased firing levels of this muscle. Anthropoid primates exhibit a late-firing balancing-side deep masseter muscle relative to the working-side superficial masseter, and W/B ratios for this muscle are close to 1.0. In contrast, strepsirrhine primates have an early firing balancing-side deep masseter and W/B ratios ranging from 2.0 to 4.0 (Hylander et al.,1987,2000; Hylander and Johnson,1994). It is thought that anthropoid primates require the recruitment of more transverse muscle force from the balancing-side deep masseter to process tougher foods. This may not be the case in alpacas as we do not see a comparable shift with increased occlusion and the acquisition of an adult diet. Although the older juveniles and adults exhibit the late-firing balancing-side deep masseter, they have W/B ratios that are much larger than 1.0. These differences may stem from the fact that the alpaca power stroke involves significant movement, and food breakdown may be more influenced by prolonged force to propagate cracks for complete fracture rather than by increasing force magnitude (Lucas,2004).
Closer examination of the data from individual experiments reveals that the grand mean indicating near-simultaneous recruitment of the balancing-side deep masseter and the working-side superficial masseter may be the result of significant variability in the timing of this muscle. In two of the five individuals, the balancing-side deep masseter exhibits the adult pattern of a late-firing balancing-side deep masseter in some of the experiments following m1 occlusion (Fig. 5). In these experiments, the balancing-side deep masseter was delayed on average between 20 and 30 msecs relative to the working-side superficial masseter. Thus, there may be significant individual variability in the coordination of the jaw muscles throughout ontogeny.
The observed ontogenetic changes in the activity of the balancing-side deep masseter have implications for testing hypotheses for the evolution of chewing motor patterns in mammals. In mammals, the timing of the balancing-side deep masseter relative to the other jaw muscles, particularly the working-side superficial masseter, is highly correlated with the morphology of the mandibular symphysis. Mammals with ossified mandibular symphyses, such as alpacas, pigs, horses, and anthropoid primates, exhibit a late-acting balancing-side deep masseter relative to the working-side superficial masseter. In contrast, mammals with patent and mobile symphyseal joints exhibit an early firing balancing-side deep masseter relative to the working-side superficial masseter (Herring and Scapino,1973; Hylander and Johnson,1994; Vinyard et al.,2001,2006; Hylander et al.,2004; Williams et al.,2007). Because of the correlation between symphyseal morphology and the activity of the balancing-side deep masseter, symphyseal fusion may be required to resist or transfer routine masticatory forces over the lifespan of the animal generated by this muscle during chewing (e.g., Hylander,1984,1985; Hylander et al.,1987,1998; Lieberman and Crompton,2000; Williams et al.,2008). Thus, it is not entirely unexpected that infant alpacas with unfused symphyses do not exhibit the late-acting balancing-side deep masseter observed in adults. However, the shift to the adult activity pattern does not appear to coincide with symphyseal fusion, which is completed by 6 months (Stover and Williams,2009). This is because the delayed balancing-side deep masseter recruitment pattern is not present in three of the five animals even after 1 year. Rather, as observed in this study, the appearance of adult balancing-side deep masseter activation pattern in alpacas is variable among individuals. This suggests that some quantitative tests of species-level hypotheses on the evolution of chewing motor patterns require EMGs recorded from individuals exhibiting the adult pattern as well as additional ontogenetic studies on the relationship between jaw-muscle activity patterns and symphyseal fusion in other mammals.
Finally, although the data presented here suggest that occlusal development may influence some aspects of masseter activation patterns in alpacas, we cannot rule out that some of these changes are the result of musculoskeletal growth that affects the biomechanics of the masticatory system. The studies on both pigs and rabbits point to altered masticatory biomechanics associated with growth (e.g., Herring,1985a,b; Herring and Wineski,1986; Weijs et al.,1987; Langenbach et al.,1991). We are currently evaluating changes in craniofacial morphology during ontogeny that may influence force generation and movement in the masticatory apparatus. Preliminary observations suggest that the most significant skeletal changes occur in the first few months, with one specific change being the progressive shift in orientation of the ascending ramus as it becomes more anteriorly inclined (see Fig. 1). The height of the ascending ramus relative to the skull also changes during ontogeny. Both of these may influence muscle action lines resulting in concomitant changes in jaw-muscle activity. However, in general, the differences observed in the masseter activity during the early period of rapid musculoskeletal growth in alpacas appear to be quite minor, with more notable differences in masseter activity occurring during the juvenile period. Thus, jaw-muscle EMG data during the critical stage between 1.5 and 3.5 years when the remaining molars come into occlusion would be particularly useful for determining the influence of dental development versus craniofacial growth on masseter activity.
The authors thank Dr. David Anderson, DVM at Kansas State University for the alpacas used in this study, and Dr. Valerie Samii and Andrew Niehaus, Ohio State University College of Veterinary Medicine, for facilitating the CT scans of the animals. The adult data used in this study were collected with the help of Drs. William Hylander, Chris Vinyard, and Christine Wall, whose collaboration is gratefully acknowledged. Two anonymous reviewers provided helpful comments on the manuscript. The authors also thank the staff in the Department of Lab Animal Resources at Ohio University for overseeing the care and maintenance of the alpacas used in this study.
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