Burst characteristics of daily jaw muscle activity in juvenile rabbits
1 Department of Functional Anatomy, Academic Centre for Dentistry Amsterdam
(ACTA), Universiteit van Amsterdam and Vrije Universiteit, Meibergdreef 15,
1105 AZ, Amsterdam, The Netherlands
2 Department of Orthodontics and Craniofacial Developmental Biology,
Hiroshima University Graduate School of Biomedical Sciences, 1-2-3 Kasumi,
Minami-ku, Hiroshima 734-8553, Japan
* Author for correspondence (e-mail: t.vanwessel{at}amc.uva.nl)
Accepted 4 May 2005
![]() |
Summary |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Key words: EMG, duty time, motor control, burst number, burst length, rabbit, Oryctolagus cuniculus
![]() |
Introduction |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
A few studies have determined the duty time over longer time periods,
including a wide range of daily behaviors (hindlimb muscles in cat,
Hensbergen and Kernell, 1997;
monkey, Hodgson et al., 2001
;
jaw muscles in human, Miyamoto et al.,
1996
,
1999
; rabbit,
Langenbach et al., 2004
;
van Wessel et al., 2005
).
Although duty time is a valuable parameter, it is only a general indicator of
muscle use and cannot distinguish between different types of activation, such
as phasic or tonic. Further differentiation of the duty time into the number
and duration of the EMG bursts at various activity levels could provide
additional information on normal daily muscle use and motor control
mechanisms.
Jaw muscles participate in a wide range of oral behaviors, during which
timing and coordination between the muscles differ
(Langenbach et al., 1992;
Blanksma et al., 1995, 1997
).
These variations in muscle use can be related to differences in duty time
between the muscles (Langenbach et al.,
2004
; van Wessel et al.,
2005
). The latter study found that duty times of the jaw muscles
do not change during juvenile maturation. This is remarkable since maturation
is characterized by large anatomical and functional changes in these muscles
(Weijs et al., 1987
; Bredman
et al., 1990
,
1992
;
Langenbach et al., 1992
;
English et al., 1998
, 2002),
and a general increase in efficiency in timing and coordination of all
musculoskeletal systems (Westerga and
Gramsbergen, 1993
; Muir,
2000
). Although these changes are not reflected by a modification
of the duty time during the juvenile period, the activity profile of the
different muscles might differ in the number and/or duration of the EMG
bursts.
We therefore examined the daily burst number, burst length and duty time of
the jaw muscles in juvenile rabbits. Radio-telemetry-enabled wireless EMG
recording was as natural a measure for muscle behavior as possible. The duty
time has been shown to differ between jaw muscles
(van Wessel et al., 2005). As
the jaw muscles are diverse in their function and activated in different
combinations with varying duration, this duty time obtained by van Wessel et
al. (2005
) was used in the
present study and extended by differentiation into number and length of the
activity bursts. It was hypothesized that the muscles differ from each other
in daily burst number and burst length. Furthermore, the large maturational
changes in anatomy and function were expected to be related to a modification
in the number and/or length of the bursts over time.
![]() |
Materials and methods |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Surgical implantation and recording procedure
The surgical procedure was essentially the same as described previously
(van Wessel et al., 2005).
Under general anesthesia, nine juvenile male New Zealand White rabbits
Oryctolagus cuniculus L.; age, 8 weeks; mass range, 1200-1800 g) were
provided with a telemetric implant. The animals showed no visible muscular or
skeletal abnormalities and had adult dentition from the start of the
experiment (age 8 weeks). The implant was subcutaneously fixed in the shoulder
area of the animal. The bipolar electrodes (diameter 0.45 mm) were inserted,
parallel to the fiber direction, into the right jaw muscles. The electrodes
were fixed at the muscle surface. The distance between the electrodes was 1-3
mm and the effective electrode length was 7 mm. In different combinations
three or four jaw muscles were simultaneously recorded from each animal
(Fig. 1A).
|
Recording of muscle activities started 2-3 days after surgery when the animal had regained common feeding behavior. The daily behavior of four animals was monitored by video surveillance (infra-red CCD camera, VCB-3372P; resolution: 560 x400 TV lines; video frame rate: 15 frames s-1; Sanyo Electric Co. Ltd, Osaka, Japan). Following the 6-week recording period (maturation weeks 9-14), the animals were sedated (Hypnorm, Janssen Pharmaceutica, Tilburg, The Netherlands) and killed by an overdose of pentobarbital (Nembutal, Sanofi Sante, Maassluis, The Netherlands), after which signals were recorded for another 5 min to determine the level of recorded noise. The electrode locations were verified by dissection.
Analysis
Muscle activity was quantified per 24 h period. Two days were analyzed for
each maturational week, except for week 14, when only 1 day was analyzed. The
recordings were filtered to remove motion-artifacts (5 Hz high-pass),
rectified and averaged [20 ms window, 5 samples; Spike2 v5.0, Cambridge
Electronic Design (CED), Cambridge, UK]. Total signal loss due to transmission
problems was generally less than 5% of the total time and usually occurred
during exploring behavior when the animal with transmitter moved near to the
limits of the volume of reception. With one animal there were exceptionally
large dropout periods, up to 165 min per day.
Per day and for each muscle, the amplitude of all processed samples was determined (resolution 1 µV). Based on the distribution of amplitudes of each muscle over the different days, 0.001% (i.e. 43) of the samples with the largest amplitude were excluded from the analysis to eliminate possible artifacts. The largest amplitude of the remaining 99.999% of the samples indicated the maximum muscle activity for that day and was defined as the peak-EMG. Muscle activity level was expressed as a percentage of this peak-EMG.
Duty time was defined per 24 h period as the fraction of this period that a muscle was active. The duty time was determined for muscle activities exceeding 5%, 10%, 20%, 30%, 40%, 50%, 60%, 70%, 80% and 90% of the peak-EMG. For example, the duty time for activities exceeding 5% peak-EMG is the total relative duration of all EMG samples having amplitudes larger than 5% of the peak-EMG of that day.
To quantify burst number and length in relation to activity level, a custom-made code for the Spike2 software was used. The rectified and averaged recordings (Fig. 1B) were scanned to locate all the bursts exceeding the above-mentioned activity levels. A burst was defined as a series of consecutive samples exceeding a predefined level of activity (Fig. 1C, left). For the various levels all bursts were indexed for their length (20 ms resolution). The total burst number, mean burst length (± S.D.), median burst length and distribution of burst number as a function of burst length (Fig. 1C, right) were determined for each muscle and the various activity levels.
Data exclusion
On three occasions the electrode pair dislodged before the end of the
experiment, therefore these muscles were excluded from the analysis.
Eventually, 27 muscles were processed in the analysis, i.e. digastric
(N=5), superficial masseter (N=5), posterior deep masseter
(N=6), medial pterygoid (N=6), and temporalis
(N=5). For each muscle the level of noise
[(y2N-1)0.5, where
y = sample amplitude and N = number of samples] and the
maximum noise amplitude (2-9 µV) were estimated. In general, the estimated
noise levels were below the 1% peak-EMG. However, in some of the recorded
muscles the maximum noise amplitude approached the 5% peak-EMG. Therefore, the
5% activity level was taken as the lowest level in which, for all recorded
muscles, noise was not included in the analyzed signals.
Statistics
Over all animals, means and S.D. values of the daily duty times,
number of bursts, individual mean burst length, and median burst length were
calculated for each muscle, and for all examined activity levels. For each
muscle and for each activity level separately, a general linear model
(repeated measures) was used to test whether maturation had an effect on
normally distributed averages of burst number, mean and median burst length or
duty time. Parametric testing was used to reveal interaction effects between
activity level and maturation. In cases that did not meet the criteria for
homogeneity of variance the Greenhouse-Geisser correction was applied to
calculate the adequate P-value. Differences between muscles in burst
number, mean and median burst length or duty time were tested using
independent t-tests on normally distributed averages, for each
activity level and each analyzed day. In each animal a different combination
of muscles was continuously recorded. Therefore, independent testing was used
to reveal differences between muscles. Changes in peak-EMG during maturation
were also tested for each muscle separately using a general linear model
(repeated measures). For each muscle and for all analyzed days the
interindividual variation in burst number and burst length was expressed by
the coefficient of variation [COV=(S.D./mean) x100%]. Changes
during maturation in the interindividual variation for daily burst number and
burst length were tested using one-way analysis of variance (ANOVA) on the
COVs of these parameters for activations exceeding the 5%, 20%, 50% and 90%
levels. In all tests a P-value of less than 0.05 was considered
statistically significant. Statistical tests were performed using SPSS
statistical software package (SPSS Inc., Chicago, IL, USA), version
11.5.1.
![]() |
Results |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
The continuous EMG recordings showed a wide range of muscle activities (Fig. 1B). The peak-EMG varied among muscles and individuals (range for the different muscles: digastric, 0.07-0.62 mV; superficial masseter, 0.21-0.63 mV; deep masseter, 0.06-0.87 mV; medial pterygoid, 0.14-1.22 mV; temporalis 0.05-0.75 mV). During maturation the averaged peak-EMG values showed no significant differences for the individual muscles except for the superficial masseter, which showed a significant (d.f.=10, P=0.03) increase in peak-EMG from week 9-11. During maturation no statistically significant changes were detected in any of the muscles for burst number (d.f.=10, P>0.1), mean burst length (d.f.=10, P>0.2) or duty time (d.f.=10, P>0.2) for any of the tested activity levels. No interaction effects were found between maturation and activity level. Including almost all muscle activities (i.e. exceeding 5% peak activity), around 205 000 bursts per day were registered (temporalis, week 14), occupying one fifth of the total time (Fig. 2A). For the most powerful activities only (i.e. exceeding 90% peak activity), the number of bursts for any of the muscles was limited to a maximum of 120 each day, occupying only a few seconds (0.003% of the total time).
|
As the activity level increased a clear decrease was seen in burst number, mean burst length and duty time. For muscle activities exceeding the 20% level the number of contractions was limited to about 50 000 per day in week 14, occupying only 3% of the total time (i.e. about 43 min). At this level no significant differences in burst numbers and duty times were detected between the muscles. However, for activities exceeding the 50%, 60%, 70%, 80% and 90% levels the superficial masseter and medial pterygoid showed significantly (d.f.=6, P<0.05) larger burst numbers and duty times than the other three muscles (Fig. 2).
The distribution of burst lengths (Fig. 3) showed that for activities exceeding the 5% level the temporalis and deep masseter produced many short bursts. This was reflected in a median burst length of 0.03 s for both muscles, which differed significantly (d.f.=6, P<0.05) from the median burst length (0.05 s) of the digastric, superficial masseter and medial pterygoid. For the temporalis and deep masseter, large numbers of bursts (19% of the total) were found at a burst length of 0.05 s (Fig. 3). In contrast, the digastric showed a large number of bursts (16% of the total) at a longer burst length of 0.09 s, whereas the superficial masseter and medial pterygoid showed a bimodal distribution with a large numbers at burst lengths of 0.05 s (13% of the total) and 0.11 s (16% of the total). For contractions longer than 1.0 s the temporalis showed a large amount of bursts compared to the other muscles. For example, the 18% duty time of the temporalis in week 14 contained 1.5% duty time of these bursts longer than 1.0 s.
|
![]() |
Discussion |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Although this paper discusses differences between muscles and individuals
during development it should be noted that the activity of only a small muscle
region was recorded. In this paper we have focused on cumulative data, showing
the amount of muscle activity exceeding predefined levels, as this serves as a
measure for the complete daily loading under which a muscle functions. Further
analysis of video recordings could clarify the relationship between specific
behavior and muscle activation exceeding different levels. The duty time has
previously been determined as a general indicator for daily muscle use
(Monster et al., 1978;
Hensbergen and Kernell, 1997
;
Langenbach et al., 2004
;
van Wessel et al., 2005
). The
present study also determined the daily burst number and length, providing a
tool to examine the daily muscle use in more detail. Apart from understanding
muscle use, these parameters might also be relevant to increase insight in
muscle adaptation as the frequency and level of stimulation are both
considered as important factors in determining the fiber type composition
(e.g. Ausoni et al., 1990
;
Pette, 2002
).
The differences in burst numbers between the muscles were reflected by the differences in duty time (Fig. 2). In contrast, mean burst length was similar for all muscles. This indicates that differences in duty time between the muscles are mainly determined by variation in burst number and not by changes in burst length. Despite the similar mean burst lengths the distribution curves of the burst lengths, and consequently the median burst lengths, differed considerably between the muscles (Fig. 3). These differences depended on activity level. With increasing activity level, the peaks of the distribution curves showed a shift towards shorter burst lengths, which can be explained by the fact that the high amplitude portion of a burst is generally shorter than its low amplitude portion. Consequently, long bursts present at the 5% level are identified as bursts with shorter duration at higher activity level and most likely represent powerful muscle activation. Short bursts present at low activity levels disappear with increasing activity level and are associated with low level, and thus non-powerful muscle activation.
Shape differences in the distribution curves between the muscles were apparent, especially for activities exceeding the 5% level. At this level the temporalis, deep masseter and digastric showed unimodal distributions, whereas the distributions of the superficial masseter and medial pterygoid were bimodal. The peaks in the curves of the temporalis and deep masseter were found at short burst lengths (0.05 s).As explained above, this suggests that both muscles are predominantly activated in non-powerful motor behaviors of short duration, such as mouth cleaning and grooming, although the temporalis showed many more bursts than the deep masseter. On the other hand, the temporalis also showed a relatively large amount of long bursts (>0.2 s), indicating that this muscle is also involved in behaviors requiring a prolonged low level activity. For activities exceeding the 5% level the distribution curve of the digastric was relatively wide in shape, with a peak number at 0.09 s and a relatively large number of bursts between 0.1 and 0.2 s. For activities exceeding the 20% level the digastric showed a relatively large amount of bursts compared to the temporalis and deep masseter, suggesting that the digastric is more involved in behaviors that require activation at higher levels.
For rhythmic motor behavior, such as mastication, it has been shown that
multiple centrally located pattern generators control the contraction patterns
of the different muscles (Lund,
1991). The described differences in burst numbers and lengths for
various activity levels suggest that the temporalis, deep masseter and
digastric are differently controlled during generation of motor behavior. In
contrast, the distribution curves of the superficial masseter and medial
pterygoid were similar for various activation levels. Although we could not
determine a time relation in EMG activity between the muscles, the similarity
between the distribution curves could imply that the activation of the
superficial masseter and medial pterygoid is commonly generated, both during
powerful and non-powerful motor tasks, and that this activation is different
from that of the other jaw muscles. The distribution curves for activities
exceeding the 5% level showed two peaks (0.05 s and 0.11 s), indicating that
the superficial masseter and medial pterygoid are activated using at least two
ranges of burst lengths. As explained above, non-powerful motor behavior is
presumably responsible for the peak at shorter burst lengths, whereas powerful
motor behavior is related to the longer burst lengths at the 5% level.
Furthermore, the superficial masseter and medial pterygoid showed a relatively
large amount of bursts for activities exceeding the 50% level compared to the
other muscles. This implies a larger contribution to powerful behaviors, such
as biting and clenching. For the rabbit masseter only it has been reported
that the firing pattern of single motoneurons covers a broad range of firing
rates and durations (English and Widmer,
2003
). Compared to this study we found a wider range in burst
durations, which is probably related to the recording of more than one motor
unit.
Until now, activity of the jaw muscles has mainly been studied during food
uptake (e.g. Schwartz et al.,
1989; Weijs et al.,
1989
; Langenbach et al.,
1992
; Widmer et al.,
2003
). Using principal component analysis of the changes in burst
amplitude during chewing, Weijs et al.
(1999
) concluded that the jaw
muscles can be divided into three independently controlled groups: (1) the jaw
closers, superficial masseter and medial pterygoid; (2) the jaw openers,
digastric and lateral pterygoid; and (3) the deep masseter. The present
results point to four groups; the same three groups as found in the Weijs
study and a fourth group, the temporalis, which was not included in the latter
study. Thus these results suggest that muscles are used differently during
various behaviors, which could be related to differences in central control of
motor behavior between muscles or muscle groups
(Weijs et al., 1999
;
Widmer et al., 2003
). Our
results also suggest that muscle use depends on the activation level, since
the temporalis was the most active muscle during non-powerful behavior while
the superficial masseter and medial pterygoid were the most active during
powerful behavior. The differences between activation levels could be related
to central regulated mechanisms or to peripheral feedback of the muscles
(Lund, 1991
;
Langenbach and van Eijden,
2001
).
Muscle activation exceeding the 90% level occurred less than 120 times a
day. According to the size principle
(Henneman, 1981), only during
these powerful bursts are the least easily recruited, fast-twitch and most
fatigable units recruited. Consequently, the entire range of activities
(>5% level) likely includes recruitment of all different types of motor
units, i.e. slow fatigue resistant motor units as well as fast and fatigable
motor units. If this principle is applied to the present results it can be
speculated that the large burst numbers of the temporalis and deep masseter at
low activity levels require many relatively fast units, which are not
necessarily fatigue-resistant because of the short duration of their
contractions. In contrast, the longer bursts of the digastric, including all
activities (>5%), would require more fatigue-resistant units, whereas the
superficial masseter and medial pterygoid would require a mixture of fast and
slow units, resulting from their bimodal distributions for activities
exceeding the 5% level. High duty times imply prolonged muscle activity and
this has been associated with large percentages of slow fatigue-resistant
fiber types (Monster et al.,
1978
; Kernell and Hensbergen,
1998
). Although this might be true, the detailed characterization
of muscle activity presented in the present study shows that high duty times
can also be generated by large numbers of short bursts (see temporalis) and
thus could be related to large percentages of fast fiber types. The
differences in burst length distribution between the deep and superficial
masseter are in line with reported differences in histochemical and
physiological properties between these muscle regions, indicating that the
deep masseter contains more fast type units than the superficial masseter
(English et al., 1999
;
van Eijden and Turkawski,
2001
).
In a previous study (van Wessel et al.,
2005) we found that the duty time of the jaw muscles in rabbits
did not change during maturation. The present study revealed that burst number
and burst length were also unchanged during maturation. This is remarkable,
since maturation of the jaw muscles is characterized by large anatomical
changes, such as an increase in fiber length and muscle cross-sectional area
(Weijs et al., 1987
), and
substantial changes in fiber type composition
(Bredman et al., 1992
;
Eason et al., 2000
;
English and Schwartz, 2002
).
Despite these anatomical changes, the mastication pattern of young animals
resembles that of adults (Weijs et al.,
1989
; Langenbach et al.,
1992
). Thus although timing and coordination between muscles are
improved during maturation, the pattern of contraction is established long
before the anatomical changes have completed.
Although duty time did not change during maturation, we reported, for
activities exceeding the 5% level, a significant decrease in the
interindividual variation in duty time for the digastric and the superficial
and deep masseter (van Wessel et al.,
2005). Since variation in duty time is associated with variation
in burst number it can be expected that the interindividual variation in burst
number is also reduced during maturation. This reduction in interindividual
variation was indeed found for burst number and also for burst length, for all
muscles except the medial pterygoid (data not shown). This decrease in
interindividual variation could be related to a reduction in neuromuscular
plasticity during maturation (Kernell,
1998
). Muscles are susceptible to an adaptive range in which
muscle properties can adapt through alterations in use. During maturation this
adaptive range decreases, not only by changes in central control, but also by
alterations in afferent feedback mechanisms
(Westerga and Gramsbergen,
1993
).
In conclusion, differences in duty time between muscles are mainly caused by variation in burst number and not burst length. Activation of the jaw muscles is differently controlled during powerful and non-powerful motor behaviors, for at least four different muscle groups. In addition, burst number, burst length and duty time of the jaw muscles do not change during maturation from 9-14 weeks, indicating that functional organization of motor control patterns does not change during this period.
![]() |
Acknowledgments |
---|
![]() |
References |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Ausoni, S., Gorza, L., Schiaffino, S., Gundersen, K. and Lomo, T. (1990). Expression of myosin heavy chain isoforms in stimulated fast and slow rat muscles. J. Neurosci. 10,153 -160.[Abstract]
Blanksma, N. G. and van Eijden, T. M. G. J.
(1995). Electromyographic heterogeneity in the human temporalis
and masseter muscles during static biting, open/close excursions, and chewing.
J. Dent. Res. 74,1318
-1327.
Blanksma, N. G., van Eijden, T. M. G. J., van Ruijven, L. J. and
Weijs, W. A. (1997). Electromyographic heterogeneity in the
human temporalis and masseter muscles during dynamic tasks guided by visual
feedback. J. Dent. Res.
76,542
-551.
Bredman, J. J., Weijs, W. A., Moorman, A. F. M. and Brugman, P. (1990). Histochemical and functional fibre typing of the rabbit masseter muscle. J. Anat. 168, 31-47.[Medline]
Bredman, J. J., Weijs, W. A., Korfage, H. A., Brugman, P. and Moorman, A. F. M. (1992). Myosin heavy chain expression in rabbit masseter muscle during postnatal development. J. Anat. 180,263 -274.[Medline]
Eason, J. M., Schwartz, G., Shirley, K. A. and English, A. W. (2000). Investigation of sexual dimorphism in the rabbit masseter muscle showing different effects of androgen deprivation in adult and young adult animals. Arch. Oral Biol. 45,683 -690.[CrossRef][Medline]
English, A. W. and Schwartz, G. (2002).
Development of sex differences in the rabbit masseter muscle is not restricted
to a critical period. J. Appl. Physiol.
92,1214
-1222.
English, A. W. and Widmer, C. G. (2003). Sex differences in rabbit masseter motoneuron firing behavior. J. Neurobiol. 55,331 -340.[CrossRef][Medline]
English, A. W., Eason, J., Pol, M., Schwartz, G. and Shirley, A. (1998). Different phenotypes among slow/beta myosin heavy chain-containing fibres of rabbit masseter muscle: a novel type of diversity in adult muscle. J. Muscle Res. Cell Motil. 19,525 -535.[CrossRef][Medline]
English, A. W., Eason, J., Schwartz, G., Shirley, A. and Carrasco, D. I. (1999). Sexual dimorphism in the rabbit masseter muscle: myosin heavy chain composition of neuromuscular compartments. Cell. Tissue Org. 164,179 -191.[CrossRef]
Henneman, E. (1981). The size principle of motoneuron recruitment. In Motor Unit Types, Recruitment and Plasticity in Health and Disease, pp.26 -60. Basel: Kager.
Hensbergen, E. and Kernell, D. (1997). Daily durations of spontaneous activity in cat's ankle muscles. Exp. Brain Res. 115,325 -332.[Medline]
Hodgson, J. A., Wichayanuparp, S., Recktenwald, M. R., Roy, R.
R., McCall, G., Day, M. K., Washburn, D., Fanton, J. W., Kozlovskaya, I. and
Edgerton, V. R. (2001). Circadian force and EMG activity in
hindlimb muscles of rhesus monkeys. J. Neurophysiol.
86,1430
-1444.
Kernell, D. (1998). The final common pathway in postural control-developmental perspective. Neurosci. Biobehav. Rev. 22,479 -484.[CrossRef][Medline]
Kernell, D. and Hensbergen, E. (1998). Use and fibre type composition in limb muscles of cats. Eur. J. Morphol. 36,288 -292.[CrossRef][Medline]
Langenbach, G. E. J. and van Eijden, T. M. G. J. (2001). Mammalian feeding motor patterns. Am. Zool. 41,1338 -1351.
Langenbach, G. E. J., Brugman, P. and Weijs, W. A. (1992). Preweaning feeding mechanisms in the rabbit. J. Dev. Physiol. 18,253 -261.[Medline]
Langenbach, G. E. J., van Ruijven, L. J. and van Eijden, T. M. G. J. (2002). A telemetry system to chronically record muscle activity in middlesized animals. J. Neurosci. Methods 114,197 -203.[CrossRef][Medline]
Langenbach, G. E. J., van Wessel, T., Brugman, P. and van
Eijden, T. M. G. J. (2004). Variation in daily masticatory
muscle activity in the rabbit. J. Dent. Res.
83, 55-59.
Lund, J. P. (1991). Mastication and its control
by the brain stem. Crit. Rev. Oral Biol. Med.
2, 33-64.
Miyamoto, K., Yamada, K., Ishizuka, Y., Morimoto, N. and Tanne, K. (1996). Masseter muscle activity during the whole day in young adults. Am. J. Orthod. Dentofacial Orthop. 110,394 -398.[Medline]
Miyamoto, K., Ishizuka, Y., Ueda, H. M., Saifuddin, M., Shikata, N. and Tanne, K. (1999). Masseter muscle activity during the whole day in children and young adults. J. Oral Rehabil. 26,858 -864.[CrossRef][Medline]
Monster, A. W., Chan, H. and O'Connor, D. (1978). Activity patterns of human skeletal muscles: relation to muscle fiber type composition. Science 200,314 -317.[Medline]
Muir, G. D. (2000). Early ontogeny of locomotor behaviour: a comparison between altricial and precocial animals. Brain Res. Bull. 53,719 -726.[CrossRef][Medline]
Pette, D. (2002). The adaptive potential of skeletal muscle fibers. Can. J. Appl. Physiol. 27,423 -448.[Medline]
Schwartz, G., Enomoto, S., Valiquette, C. and Lund, J. P.
(1989). Mastication in the rabbit: a description of movement and
muscle activity. J. Neurophysiol.
62,273
-287.
van Eijden, T. M. G. J. and Turkawski, S. J.
(2001). Morphology and physiology of masticatory muscle motor
units. Crit. Rev. Oral Biol. Med.
12, 76-91.
van Wessel, T., Langenbach, G. E. J., Brugman, P. and van Eijden, T. M. G. J. (2005). Long-term registration of daily jaw muscle activity in juvenile rabbits. Exp. Brain Res. 162,315 -323.[CrossRef][Medline]
Weijs, W. A., Brugman, P. and Klok, E. M. (1987). The growth of the skull and jaw muscles and its functional consequences in the New Zealand rabbit (Oryctolagus cuniculus). J. Morphol. 194,143 -146.[CrossRef][Medline]
Weijs, W. A., Brugman, P. and Grimbergen, C. A. (1989). Jaw movements and muscle activity during mastication in growing rabbits. Anat. Rec. 224,407 -416.[CrossRef][Medline]
Weijs, W. A., Sugimura, T. and van Ruijven, L. J. (1999). Motor coordination in a multi-muscle system as revealed by principal components analysis of electromyographic variation. Exp. Brain Res. 127,233 -243.[CrossRef][Medline]
Westerga, J. and Gramsbergen, A. (1993). Changes in the electromyogram of two major hindlimb muscles during locomotor development in the rat. Exp. Brain Res. 92,479 -488.[Medline]
Widmer, C. G., Carrasco, D. I. and English, A. W. (2003). Differential activation of neuromuscular compartments in the rabbit masseter muscle during different oral behaviors. Exp. Brain Res. 150,297 -307.[CrossRef][Medline]