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J Dent Res 83(1): 55-59, 2004
© 2004 International and American Associations for Dental Research

RESEARCH REPORT
Biological

Variation in Daily Masticatory Muscle Activity in the Rabbit

G.E.J. Langenbach*, T. van Wessel, P. Brugman, and T.M.G.J. van Eijden

Department of Functional Anatomy, Academic Center for Dentistry Amsterdam (ACTA), Meibergdreef 15, 1105 AZ Amsterdam, The Netherlands;

* corresponding author, g.e.langenbach{at}amc.uva.nl


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS & METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
The daily use of masticatory muscles remains largely unclear, since continuous recordings were limited in space and time. This study’s purpose was to use radio-telemetry to examine daily muscle use and its inter- and intra-individual variations. A telemetric device was implanted into the rabbit masseter, and the transmitted signals were digitally stored for 7 days. Muscle use was analyzed by calculation of the total time each muscle was activated above 5, 20, and 50% of the day’s peak activity. Rabbits (n = 6) spent only 2% of the time chewing. Muscles were activated up to 20% of the total time at levels exceeding 5% of peak activity, and only about 0.5% of the time in forceful behaviors utilizing 50% of maximum contraction. It can be concluded that daily muscle use remained constant during succeeding days, but differed significantly among muscle regions and individuals.

KEY WORDS: masseter • EMG • duty time • telemetry


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS & METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Muscle activity, as determined by electromyography (EMG), has almost exclusively been studied for specific motor tasks, and this is no different for the masticatory muscles, in which feeding function has been examined in several species (Weijs, 1994; Langenbach and van Eijden, 2001). However, feeding occupies only a small proportion of the total time. To reflect the functional regime of a muscle, the contraction pattern of the muscle has to be recorded for at least one complete day, hence incorporating the complete range of functional demands. Only then can differences in muscle use be examined between animals, during the day, at various levels, or between muscles. Muscle use largely determines the loading within the masticatory system and plays a crucial role in the realization of fiber-type composition (Kernell, 1992; Pette and Vrbová, 1999).

Previously, subjects had to be cable-connected to a recording unit, which limits such studies in time and space. Although this is not much of a problem in lengthy sleep studies (e.g., Solberg et al., 1975; Kato et al., 2003), it restricts the study of natural daily behavior. Radio-telemetry has recently provided the possibility for true wireless EMG recording. Hensbergen and Kernell (1997, 1998) successfully used the technique to examine the daily activity of hindlimb muscles in the cat. However, the transmitter was worn on the back and imposed external forces which might affect the animal’s natural behavior. The evolution of electronics and battery technology has facilitated the development of smaller, fully implantable transmitters, which have become commercially available. Although the technique facilitates the lengthy (several months) recording of biopotentials, it has seldom been used to record striated muscle activities (Hinch et al., 2002; Langenbach et al., 2002).

The purpose of the present study was to examine the inter- and intra-individual variations in daily contraction patterns of the masseter muscle in the rabbit, to facilitate the study of the influence of muscle activity on the adaptive capacity of the masticatory system. We hypothesized that different animals would show similar total daily durations of muscle activity (duty time), and that the duty times would be constant for subsequent days. Knowing that the masseter muscle acts heterogeneously during different feeding behaviors, we presumed that the deep and superficial regions would differ in their total daily duration of activity.


   MATERIALS & METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS & METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
Telemetric System
To record muscle activities, we used a four-channel device for biopotential recording. The device (F50-EEEE, Data Sciences International [DSI], St. Paul, MN, USA) consists of an electronics module and a battery guaranteed to supply energy for at least 2 mos of continuous data transmission. The electrodes (length, 20 cm) contain a helix of stainless steel wire (diameter, 0.45 mm) enclosed by an insulating silicone tube (diameter, 0.8 mm). The implant is calibrated, sealed, biocompatible, and fully implantable.

In the device, the biopotentials are filtered (1st-order low-pass filter, 158 Hz) and sampled (250 Hz) on the input of each channel. A nearby receiver (RMC-1, 31 x 24.5 x 3.5 cm, DSI), placed above the animal inside the cage, ensures transmission of the digital data (3,600,000 samples/hr) to a PC hard disk, with the use of a data acquisition system (Fig. 1Go). Despite the limited frequency range and the low sampling frequency, the recorded EMGs are a reliable reflection of the actual biopotentials and can be used for estimation of muscle use (Langenbach et al., 2002).



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  		Figure 1. Method of data collection and analysis. Bottom left: lateral view of the rabbit masticatory system. Indicated are the 2 electrode locations in the masseter. Implantation site (F50-EEEE, 45 x 17 x 10 mm, 14 g) in the neck area, the cordless transmission of data to the receiver, and storage of data on a personal computer with the DataQuest ART acquisition software. Right column: reduction of the daily amount of samples by distribution in 1500 EMG categories (0–1.5 mV).

 
Muscle Activity Registration
The device was subcutaneously placed in the shoulder area of 6 adult male New Zealand White rabbits (Oryctolagus cuniculus; age, 5–12 mos; weight, 2800–5000 g) under general anesthesia (Hypnorm and Dormicum, followed by inhalation of isoflurane in combination with oxygen). The 4 electrodes were subcutaneously guided to an incision in the submandibular region. From here, they were inserted into the muscles by means of a longitudinally ground hypodermic needle (Nuijens et al., 1997), and secured by the leads being sutured at the muscle surface. Two electrodes were inserted into the anterior superficial and posterior deep masseter, while the remaining were placed into the digastric and one of the other jaw elevators to ensure a correct interpretation of jaw behavior. Antibiotics (Baytril, Bayer BV, Mijdrecht, The Netherlands) were administered for two days preceding and following surgery. Analgesic (Temgesic, Schering-Plough, Maarssen, The Netherlands) was provided immediately after surgery and, as required, one or two days following surgery. The experiment was approved by the Animals Ethics Committee of the Medical School of the University of Amsterdam.

Each animal was held in a standard cage (45 x 50 x 55 cm) and provided with ad libitum pellets, hay, and water, and, except for the daily care and physical examination, was left undisturbed to minimize any external influence. Day-night rhythm was ensured by automatic dimmed lighting (7 am-7 pm). Muscle activities were continuously recorded for 7 days, starting several days after surgery when the animal had regained its usual feeding behavior. After the recording period, the animals were sedated (Hypnorm, Janssen Pharmaceutica, Tilburg, The Netherlands) and killed by an overdose of pentobarbital (Nembutal, Sanofi Sante, Maassluis, The Netherlands) for electrode location verification. The animals were weighed before and after the experiment.

Analysis
LabVIEW software (National Instruments, Austin, TX, USA) was used to filter the recordings of all animals to remove motion artifacts (5-Hz high-pass); recordings were then rectified and integrated (20-msec window, 5 samples). The samples of one total day (4,320,000 = [sampling frequency * seconds]/integration window = [250 * 86,400]/5) were indexed for their EMG amplitude and counted (steps of 1 µV, 0–1.5 mV; Fig. 1Go). The cumulative distribution of the EMG levels determined the peak EMG at 99.95% of the total number of samples, excluding possible artifacts. This enabled us to calculate the total duration of muscle activity (duty time) exceeding specified levels (5, 20, and 50%) of the peak EMG. The 50% duty time (percentage of time the muscle is active at more than 50% of the day’s peak activity) incorporates only the most forceful muscle usage, while the 5% duty time is a measure for the overall muscle use, including activities at lower levels. To visualize possible variation in muscle use during the day, we also calculated the duty times for each hour. Comparison of daily duty times between individuals (ANOVA) and muscle regions (paired t test) disclosed, respectively, the inter- and intra-individual differences.

To estimate the amount of time spent chewing, we used video surveillance (infra-red CCD camera, VCB-3372P; resolution, 560 x 400 TV lines; Sanyo Electric Co. Ltd., Osaka, Japan) of the daily behavior of 3 animals to see the approximate time that chewing occurred. Video registration time was time-linked to the EMG recording by a clock showing the time of the data acquisition system. The infra-red camera ensured reliable recording and chewing recognition during the entire diurnal cycle. After the identification of chewing periods, the EMG registrations permitted the determination of the exact period durations, which, summed, gave the total time spent feeding.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS & METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
The weight of the animals remained constant. During the first two post-surgical days only, all animals showed some modified behavior (less locomotion, decreased food uptake, less defecation), but water intake remained normal.

The continuous EMG recordings showed an enormous variation in muscle activities, even in a five-minute period (Fig. 2AGo). Periods of feeding behavior (mastication and drinking) could easily be distinguished by their prolonged rhythmic character combined with, for mastication (Fig. 2BGo), the highest activity levels. The Fig. is not representative of the relative time different behaviors were performed. Most of the time, muscle activity was absent or barely detectable and very irregular (Fig. 2CGo). Sessions of higher, but still irregular, muscle activities involved behaviors like grooming, exploring, etc. (Fig. 2DGo). Calculation of the time animals spent chewing showed that the animals masticated, on average, 27'46''/day (range, 25'05'' to 30'43''), i.e., during 1.9% of the time.



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  		Figure 2. Rectified EMG recording of the superficial masseter. (a) Five min of recording, showing different behaviors. Indicated are the positions of the 20-second amplifications shown in b, c, and d. (b) Chewing behavior. (c) Silence period, with some small activity bursts. (d) Some grooming behavior. Scale of the vertical axes (0–100%) is identical in all plots. Broken lines indicate 5 and 50% of the peak activity (100%). Note that the distribution as shown in this Fig. is not typical for the total activity scheme during the entire day.

 
Hourly duty times showed an apparent circadian variation (Fig. 3AGo), indicating that the animals used their jaw muscles less during the first daylight hours. The Fig. is representative of the consistent circadian pattern that was observed for all animals and days. Also, the daily duty times of the two masseter regions were consistent during the entire experimental period (Fig. 3BGo, 3CGo, 3DGo). Averaged over all experimental days, the intra-individual variation in duty times for each muscle region was small (Fig. 4Go; note the small standard deviations), relative to the considerable inter-individual variation. Except for the overall inter-individual difference in muscle activity, 5 of the 6 animals displayed significant but not similar differences between the two masseter regions. For the 5% duty times, in 3 of the 6 animals (#3, 4, and 5), the deep masseter showed a longer duty time than the superficial masseter, while the opposite was found in one of the animals. Two animals did not show any significant difference between the two muscle portions. For the 20 and 50% duty times, 3 animals (#1, 3, and 4) did not show any differences, one used the deep masseter more, and two showed the opposite behavior. Note that the difference in duty time between the two muscle regions depended on the activity level.



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  		Figure 3. The duty times of the masseter of animal #5. (A) The hourly 5% duty time of the superficial masseter during the third (thick line) and fourth (thin line) experimental days. The bar above the curves indicates the day (open) and night (solid) periods. The 5% (B), 20% (C), and 50% duty times (D) for the superficial (open) and deep (solid) masseter regions as recorded during all experimental days. Note that, at all activity levels and for the entire experimental period (7 days), the deep masseter region was more active than the superficial muscle.

 


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  		Figure 4. The duty times of the masseters of all experimental animals. The (over all experimental days; n = 7) averaged 5% (A), 20% (B), and 50% duty times (C) for the superficial (open) and deep (solid) masseter regions as recorded for all 6 animals. Standard deviations are shown above the bars. Significant differences between muscle regions are indicated by single (p < 0.05) or double asterisks (p < 0.01).

 

   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS & METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
The telemetry technique, as used in this study, enables muscle activities in freely moving animals to be continuously recorded without interference of the observer or a connection to the recording unit. The utilization of an extremely lightweight, fully implantable transmitter ensured that the animal’s behavior could be as natural as possible, without disturbance of any recording component. In that sense, the current paper is a first. For the human masseter, Miyamoto et al.(1996, 1999) examined the activity during one day, using a portable recording unit in combination with surface electrodes.

At all examined activity levels, a broad range of duty times was found for both muscle regions. For the deep masseter, 2 of the 6 examined animals can be clearly typified as very active, with muscle activity (at more than 5% of the peak activity) during one-fifth of the total time, while in another animal (#6), this muscle was active just one-twelfth of the time (Fig. 4AGo). The results for the superficial masseter were comparable but less extreme. Also, the 20% and 50% duty times (Figs. 4BGo, 4CGo) showed a significant range in both muscle portions. In all animals, the majority of muscle contractions during chewing reached the 20% activity level (Fig. 2Go). In humans, Miyamoto et al.(1999) detected masseter contractions exceeding the 25% activity level only 0.5% of the time. This differs considerably from the duty times (1.5–4.5%) estimated for the 20% activity level in the current paper (Fig. 4BGo). The examined levels of activity in the current study are arbitrary. A change in or expansion of activity levels can readily be obtained.

The masseter muscle is known for its extreme heterogeneous function, i.e., large timing differences between muscle regions during chewing (Weijs and Dantuma, 1981) and sucking (Langenbach et al., 1992), and a regionally dependent change in motor unit activity (Blanksma et al., 1992, 1997; McMillan and Hannam, 1992). This last type of behavioral heterogeneity, in particular, will generate the detected intra-individual variation in duty times of the superficial and deep masseter muscle regions. However, it must be emphasized that each of the current duty times is true for a limited volume of muscle, consisting of a small number of motor units out of a much larger motoneuron pool. The heterogeneous activity combined with these small recording volumes can easily produce the detected duty time differences between individuals. Whether these differences originate in different behavior patterns at the animal and/or muscle portion level remains unclear.

Behavioral differences in muscle use are related to variations in the fiber-type composition. According to the size principle (Henneman, 1981), the smallest motor units, which are commonly slow and fatigue-resistant, will be activated first. Only for powerful contractions will the larger motor units, which are fast but fatigable, be used. As a result, muscle regions with a high percentage of slow motor units can be expected to show a higher 5% duty time than regions with faster motor units. Such a linkage between anatomy and function was found for ankle muscles (e.g., Hensbergen and Kernell, 1998; Hodgson et al., 2001). Here, a muscle composed of mainly slow fibers was active at circa 15% (cat) or 9% (rhesus monkey) of the time, while a fast muscle showed activity in, respectively, 2% and 4% of the time. From studies examining the fiber-type composition in the rabbit’s masseter (Bredman et al., 1990, 1992; English et al., 1998, 1999; Eason et al., 2000), it becomes clear that an enormous variation in fiber composition can be found. A study combining the present functional results with individually computed fiber-type composition at the recording site could clarify the degree in which they are linked in the jaw musculature. Animals in the present study were adult males, excluding sexual (Eason et al., 2000) and age differences (Bredman et al., 1990, 1992) in fiber composition.

A few remarks regarding the method should be made. In every EMG study, variability in the recorded muscle activities is a topic in the data analysis. When results obtained from different recording sessions are being compared, the peak EMG value often serves as a reference, but the comparison depends entirely on the efforts of the subject of study and is hard to control in animal experiments. For this study, the peak activity was determined over an entire day, based on the assumption that, during such a period, the muscle will show a reproducible activity pattern. The regular duty times found for successive days support this assumption.

Another problem experienced during EMG analysis is electrical noise, since its level can vary during the experimental period. We bypassed this by determining solely peak activity, which can be reliably and easily defined. The disadvantage is that this method will not define the lowest detectable EMG levels. In this study, the lowest EMG level used for analysis was 5% of the peak activity, which probably surpasses the activity level needed for jaw posture. In contrast to other muscles that support the total body, the postural activity in jaw muscles is small (Yemm, 1976; Langenbach and Hannam, 1999), caused by the relatively small weight of the mandible and surrounding soft tissues.

In conclusion, masseter duty times are very constant over time, but large inter-individual differences in muscle use can be detected. Moreover, different muscle regions are not evenly activated. When lower activity levels were included, the muscles were active up to 20% of the total time. The method presented facilitates the study of adaptations related to muscle activity patterns.


   ACKNOWLEDGMENTS
 
We are grateful to Kor Brandsma and Anton van der Wardt for the anesthetic and surgical support, to Ties van den Berg for the animal care, to Leo van Ruijven for the technical support, and to Jan Harm Koolstra for his constructive criticism. This study was supported by the Interuniversity Research School of Dentistry (IOT), through the Academic Center for Dentistry Amsterdam (ACTA).

Received April 1, 2003; Last revision September 10, 2003; Accepted September 29, 2003


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 ABSTRACT
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 MATERIALS & METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
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Bredman JJ, Weijs WA, Moorman AF, Brugman P (1990). Histochemical and functional fibre typing of the rabbit masseter muscle. J Anat 168:31–47.[ISI][Medline]

Bredman JJ, Weijs WA, Korfage HA, Brugman P, Moorman AF (1992). Myosin heavy chain expression in rabbit masseter muscle during postnatal development. J Anat 180:263–274.

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