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Muscle Spindle Composition and Distribution in Human Young Masseter and Biceps Brachii Muscles Reveal Early Growth and Maturation.

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THE ANATOMICAL RECORD 294:683–693 (2011)
Muscle Spindle Composition and
Distribution in Human Young Masseter
and Biceps Brachii Muscles Reveal Early
Growth and Maturation
CATHARINA ÖSTERLUND,1 JING-XIA LIU,2 LARS-ERIC THORNELL,2
1
AND PER-OLOF ERIKSSON *
1
Department of Odontology, Clinical Oral Physiology, Umeå University, Umeå, Sweden
2
Department of Integrative Medical Biology, Section of Anatomy, Umeå University,
Umeå, Sweden
ABSTRACT
Significant changes in extrafusal fiber type composition take place in
the human masseter muscle from young age, 3–7 years, to adulthood, in
parallel with jaw-face skeleton growth, changes of dentitions and
improvement of jaw functions. As motor and sensory control systems of
muscles are interlinked, also the intrafusal fiber population, that is, muscle spindles, should undergo age-related changes in fiber type appearance.
To test this hypothesis, we examined muscle spindles in the young masseter muscle and compared the result with previous data on adult masseter spindles. Also muscle spindles in the young biceps brachii muscle
were examined. The result showed that muscle spindle composition and
distribution were alike in young and adult masseter. As for the adult
masseter, young masseter contained exceptionally large muscle spindles,
and with the highest spindle density and most complex spindles found in
the deep masseter portion. Hence, contrary to our hypothesis, masseter
spindles do not undergo major morphological changes between young age
and adulthood. Also in the biceps, young spindles were alike adult spindles. Taken together, the results showed that human masseter and biceps
muscle spindles are morphologically mature already at young age. We
conclude that muscle spindles in the human young masseter and biceps
precede the extrafusal fiber population in growth and maturation. This in
turn suggests early reflex control and proprioceptive demands in learning
and maturation of jaw motor skills. Similarly, well-developed muscle spindles in young biceps reflect early need of reflex control in learning and
C 2011
performing arm motor behavior. Anat Rec, 294:683–693, 2011. V
Wiley-Liss, Inc.
Key words: fiber types; intrafusal fibers; jaw muscle; skeletal
muscle
Grant sponsors: Department of Odontology (Medical Faculty
of Umeå University), Västerbotten County Council, Swedish
Dental Society.
*Correspondence to: Per-Olof Eriksson, Department of Odontology, Clinical Oral Physiology, Faculty of Medicine, Umeå University, Umeå S-901 87, Sweden. Fax: (þ46) – 90 13 25 78.
E-mail: per-olof.eriksson@odont.umu.se
C 2011 WILEY-LISS, INC.
V
Received 29 June 2010; Accepted 10 December 2010
DOI 10.1002/ar.21347
Published online 2 March 2011 in Wiley Online Library
(wileyonlinelibrary.com).
684
ÖSTERLUND ET AL.
INTRODUCTION
Control of jaw muscle function relies on selective
recruitment of motor units [cf. (Stålberg et al., 1986;
Hannam and McMillan, 1994)] and sensory information
from muscle, joint, periodontal, skin and mucosal mechanoreceptors (Bradley, 1995). Of muscle receptors, muscle
spindles have a unique influence on muscle activity
allowing the brain to simultaneously receive sensory
message and control muscle spindle length and change
in length (Ruffini, 1898; Boyd, 1962; Banks, 1994;
Zelená, 1994). Although far outnumbered by extrafusal
fibers, muscle receptors are equal to extrafusal fibers in
amount of nervous traffic (Matthews, 1981b). Muscle
spindles play multifunctional roles contributing in proprioception, postural and movement control, motor
learning and in plasticity of motor behaviors (Windhorst,
2007, 2008), in predicting future kinematic states by acting as forward sensory model (Dimitriou and Edin,
2010), and as suggested, in the genesis and spread of
chronic muscle pain (Johansson et al., 1999; Blair et al.,
2003; Johansson et al., 2003). They consist of a bundle of
intrafusal fibers enclosed in a fusiform connective tissue
capsule attached in parallel with the extrafusal fibers.
The intrafusal fibers have been classified based on their
enzyme-histochemical staining pattern (Ovalle and
Smith, 1972), their location of nuclei and their physiological properties (Boyd, 1962; Matthews, 1981a; Boyd
and Smith, 1984; Barker and Banks, 1994) into dynamic
nuclear bag (bag1), static nuclear bag (bag2) and static
nuclear chain (chain) fibers. Furthermore, a fourth type
acid stable bag1 (AS-bag1) is described in the adult masseter (Eriksson and Thornell, 1985, 1990; Eriksson et al.,
1994).
It is well established that adult human jaw muscles differ from limb muscles in composition and distribution of
muscle fiber types and MyHC isoforms (Eriksson, 1982;
Eriksson and Thornell, 1983; Sciote et al., 1994; Stål
et al., 1994; Monemi et al., 1999; Korfage et al., 2005a,b).
It has also been shown that human jaw muscles in adults
diverge from limb muscles in number and morphology of
muscle spindles. Thus, the adult human masseter muscle
contains especially large and complexly arranged muscle
spindles (Freimann, 1954; Voss, 1971; Eriksson and Thornell, 1985, 1987, 1990; Eriksson et al., 1994; Eriksson
et al., 1995). Typical features are a high muscle spindle
density, large capsule diameter, a high number of intrafusal fibers per spindle and numerous compound spindles, that is, clusters of spindles located closely together
within a common capsule. In line with regional differences in the extrafusal fiber type composition, the muscle
spindles are also heterogeneously distributed. The largest
and most complex spindles are located in the deep masseter, which is composed mainly of type I (Eriksson and
Thornell, 1983) fibers or slow twitch motor units (Stålberg and Eriksson, 1987).
A recent study showed that the human masseter is
regionally differentiated in fiber type composition already at 3 years of age (Österlund et al., in press). The
study also revealed significant changes in the extrafusal
fiber population from young age to adulthood. Since
motor and sensory control systems of muscle are interlinked, we hypothesize that also muscle spindles
undergo changes in composition and distribution from
young age to adulthood. To address this question, the
present study examined muscle spindles in the young
masseter muscle, and compared the results with previously reported data on the adult masseter (Eriksson and
Thornell, 1985, 1987, 1990; Eriksson et al., 1994; Eriksson et al., 1995). For comparison muscle spindles in the
young biceps brachii were included in the study, and
likewise compared with adult biceps muscle spindles
(Liu et al., 2002).
MATERIALS AND METHODS
Muscle Specimens
Muscle samples were collected at autopsy 1–3 days
post mortem, a delay that does not hamper reliable fiber
typing (Eriksson et al., 1980). Two specimens from each
of the anterior (sup ant) and posterior (sup post) superficial portions, and the deep (deep) portion of the human
masseter muscle, were obtained from seven previously
healthy young subjects with normal bite and jaw-face
morphology, four males aged 3, 4, 4, and 6 years, and
three females aged 3, 7, and 7 years. In addition, one
specimen was obtained from the biceps brachii muscle
(biceps) of the same subjects. There were missing samples for the sup ant (male 4y), and biceps (female 7y).
The samples were collected before 1990 according to prevailing directions issued by the National Board of Health
and Welfare Stockholm, Sweden. The findings were compared with previously reported data from muscle spindles in the adult masseter (Eriksson and Thornell, 1987,
1990; Eriksson et al., 1995) and adult biceps brachii
muscles (Liu et al., 2002).
Enzyme-Histochemistry
The muscle samples were rapidly frozen in propane
chilled with liquid nitrogen and stored at 80 C. Serial
10 lm cross-sections were cut at –20 C in a cryostat
microtome and treated with an antibody against slow
tonic myosin heavy chain (ALD 19) (Sawchak et al.,
1985) for detection of muscle spindles/intrafusal fibers,
and processed for myofibrillar adenosine triphosphate
(mATP) at pH 10.3, 4.6, and 4.3 for classification of
intrafusal fibers.
Intrafusal fibers were classified into four types of fiber
bag1, acid stable bag1 (AS-bag1), bag2 and chain fibers
on the basis of their mATPase staining intensity. Fibers
with no or weak staining at pH 10.3, 4.6, and 4.3 (alkaline- and acid-labile reaction) were termed bag1 fibers.
Fibers with no or weak staining at pH 10.3 (alkaline-labile reaction) to strong staining at pH 4.6 and 4.3 (acid
stable reaction) were termed acid stable bag1 (AS-bag1).
Fibers with moderate to strong staining intensity at pH
10.3, 4.6, and 4.3 (alkaline- and acid stable reaction)
were termed bag2 fibers, and fibers with strong staining
at pH 10.3 (alkaline stable reaction) and 4.6 (acid stable
reaction) and no or weak staining at pH 4.3 (acid-labile)
were termed chain fibers (Eriksson and Thornell, 1990).
This classification of intrafusal fiber types was performed in samples of three masseter muscles (female 3
years, male 4 years and female 7 years) and all six
biceps muscles.
685
MASSETER MUSCLE SPINDLES AT YOUNG AGE
TABLE 1. Muscle spindle (MS) density, number of single and compound muscle
spindles, total number of intrafusal fibers (IF) and number of intrafusal fibers per
muscle spindle detected in seven masseter and six biceps brachii muscles
Muscle spindles (MS):
Total number
Density MS/cm2 (SD)
Number in A, AB and B regions
Number in C-region
Single MS:
Number
Proportion (%)
Compound MS:
Number
Proportion (%)
Intrafusal fibres (IF):
Total number
IF per single MS:
Mean (SD)
Median
Min-max
IF per compound MS:
Mean (SD)
Median
Min-max
Sup ant
Sup post
Deep
Masseter
Biceps
224
27 (11)
89
101
22
4 (6)
8
12
378
43 (16)
144
190
624
25 (8)
241
303
97
20 (13)
54
34
80
90
8
100
110
76
198
82
52
96
9
10
0
0
34
24
43
18
2
4
800
46
1609
2455
434
8.0 (3)
7
1–23
6.4 (2)
6
3–10
9.4 (2)
9
2–21
8.3 (4)
8
1–23
7.4 (2)
7
3–19
18.8 (9)
17
7–38
22 (1)
22
22–23
Morphometric Analyses
Serial cross sections from enzyme-histochemistry were
analyzed using a microscope (Leica DMR) connected
with a digital camera (Leica DC 220). The morphometric
analyses, including muscle spindle density, compound
muscle spindle structure and number of intrafusal fibers
per muscle spindle was performed in samples of all
masseter (n ¼ 7) and biceps (n ¼ 6) muscles. Muscle
spindle density was measured as number of muscle spindles per area (MS/cm2). Definition of compound muscle
spindle structure is when two or more spindles share
the same capsule. The muscle spindle can be divided
into three morphological regions. The capsular regions the A region including the equator and the juxta-equatorial parts, containing the paraxial fluid space; the B
region extending from the end of the paraxial fluid space
to the end of the capsule; and the extra capsular C
region (Banks, 1994; Soukup et al., 2003). We also define
a transitional AB region in between the A and B regions.
Number of intrafusal fibers per muscle spindle and capsule diameter were measured in muscle spindle regions
A, AB and B, from three masseter muscles and from all
biceps muscles (n ¼ 6). The muscle spindle capsule and
intrafusal fiber diameters were measured on the computer screen processed in image analyses system (Leica
QWin). Incomplete serial sections were excluded from
analysis.
Statistical Analysis
Group data were presented as means and standard
deviations (SD). Paired t test and unpaired Mann-Whitney U test were used to test the null hypothesis (H0) of
no differences in density, muscle spindle capsule diameter, intrafusal fibers per muscle spindle, proportion of
intrafusal fiber types, and intrafusal fiber diameter
between masseter portions, masseter and biceps brachii
muscles and between young and adult masseter muscles.
H0 was rejected at the level of significance P 0.05.
RESULTS
In total 624 muscle spindles were detected in the
masseter muscle. Of these, 34 in the sup ant, two in the
sup post and 44 in the deep masseter were excluded for
further analysis due to incomplete serial sections. Of the
remaining 544 spindles, 241 were sectioned in the capsular regions A, AB and B, and 303 in the C-region. Of the
241 spindles sectioned in the capsular regions, 198 were
defined as single and 43 as compound spindles, altogether containing 2455 intrafusal fibers (1649 in single
and 806 in compound spindles). In the biceps, a total of
97 muscle spindles were detected, of which nine were
excluded due to incomplete sections. Of the remaining
88 spindles, 54 were sectioned in the capsular regions
and 34 in the C-region. Of the 54 biceps spindles, 52
were defined as single and two as compound spindles, altogether containing 434 intrafusal fibers (389 in single
and 45 in compound spindles) (Table 1).
Muscle Spindle Density
The muscle spindle density, MS/cm2, was higher
(mean, SD) in the deep 43 (16) than in the sup ant 27
(11) and sup post 4 (6) masseter portions (P ¼ 0.045 and
0.001, respectively), and higher in the sup ant than in
the sup post (P ¼ 0.002). The muscle spindle density in
the biceps brachii 20 (13) was lower than that of the
deep (P ¼ 0.044) masseter (Table 1).
Compound Muscle Spindles
Compound muscle spindles (Fig. 1) were seen in the
deep, 24%, and sup ant, 10%, masseter portions, and the
biceps brachii, 4% (Table 1).
686
ÖSTERLUND ET AL.
Fig. 1. Cross-sections of two masseter compound muscle spindles (subjects aged 3 and 4 years)
stained for mATPase at pH 10.3. Spindle from the superficial (a) and deep (b) portions with 30 and 37
intrafusal fibers, respectively. Bar ¼ 100 lm.
Number of Intrafusal Fibers per
Muscle Spindle
Table 1 summarizes the number of intrafusal fibers
(mean, median and min-max) of single and compound
muscle spindles in the masseter and biceps. The mean
number of intrafusal fibers of single muscle spindles was
significantly larger in the deep masseter, 9.4, than in
the biceps, 7.4 (P ¼ 0.03). Figure 2 shows the different
distributions of the relative frequency of muscle spindles
(%) versus number of intrafusal fibers for single and
compound spindles, respectively.
Muscle Spindle Capsule Diameter
Measurement of capsule diameter in the masseter was
based on three muscles containing 126 muscle spindles
(104 single and 22 compound spindles) sectioned in the
A, AB and B capsular regions. Out of these 86 single
and 22 compound spindles were measured. Out of 52
single and two compound spindles in the biceps, 36 single and two compound were measured. In the masseter,
the mean capsule diameter of single muscle spindles
(lm, mean SD) in regions A, AB and B were, 162 (55),
112 (29), and 72 (16), respectively. The corresponding
values for the biceps were, 118 (25), 93 (14), and 56 (15),
respectively. For both the masseter and biceps, the diameters of muscle spindle regions A and AB were significantly larger than that of region B (masseter P ¼ 0.010
and P ¼ 0.024, biceps P ¼ 0.041 and P ¼ 0.013, respectively). The diameter of region A was significantly larger
than that of region AB (masseter P ¼ 0.035, biceps P ¼
0.035). In the masseter, the mean capsule diameter (lm,
mean SD) of pooled data for single muscle spindles (n ¼
86) was 96 (37) and in the biceps (n ¼ 36), 76 (28). There
were no significant differences in capsule diameter
between masseter portions or between masseter and
biceps. The mean capsule diameter of compound muscle
spindles (lm, mean SD) was 168 (60) in the masseter (n
¼ 22) and 134 (10) in the biceps (n ¼ 2).
Intrafusal Fiber Types
In the masseter, classification of intrafusal fiber types
was based on 126 muscle spindles sectioned in the A,
AB, B and C regions (32 in sup ant, six in sup post and
88 in deep masseter), containing 1251 intrafusal fibers
(246 in sup ant, 29 in sup post and 976 in the deep
masseter). Of these, 1091 (240 in sup ant, 29 in sup post
and 822 in deep masseter) were analysed in all serial
sections. In the biceps, 422 out of 434 intrafusal fibers
were classified.
Bag1, AS-bag1, bag2 and chain fibers were identified in
both muscles (Fig. 3). A variable pattern of ATPase
staining was seen at all pH levels and in all muscle spindle regions (Fig. 4). In both muscles, for all pH levels,
the bag1 fibers were unstained or weakly to moderately
stained in the A and B regions and moderately stained
or unstained in the C region. AS-bag1 fibers were weakly
to moderately stained or unstained at pH 10.3 and moderately to strongly stained at pH 4.6 and 4.3. Bag2 fibers
were in all regions strongly to moderately stained at pH
10.3 and 4.6 and moderately to weakly stained at pH
4.3. Chain fibers were strongly or moderately stained at
pH 10.3 and 4.6 and unstained at pH 4.3. In both
muscles, the bag1 fiber staining was stronger in the Cregion versus other regions. No regional differences
were detected in bag2 and chain fibers.
Intrafusal Fiber Type Population
Of all masseter spindles (n ¼ 126), 90% contained
bag1, 15% AS-bag1, 76% bag2, and 96% chain fibers. The
corresponding values for the biceps brachii were 96%,
45%, 28%, and 100%. In the masseter, 65% of the spindles contained the three-fiber types bag1, bag2 and chain
fibers and 10% contained all four fiber types. The corresponding values for the biceps were 28% and 4%. Compared with the biceps, the masseter contained
significantly more bag2 fibers, 16% versus 4% (P ¼
0.008) and less chain fibers, 52% versus 64% (P ¼ 0.024)
(Fig. 5). The average composition of intrafusal fiber
MASSETER MUSCLE SPINDLES AT YOUNG AGE
687
Fig. 2. Distribution of relative frequency of muscle spindles (%) versus number of intrafusal fibers (IF)
in single and compound masseter spindles and single biceps spindles. Note for the masseter, difference
in distribution between single and compound spindles indicating separate populations of muscle
spindles.
types in masseter single muscle spindles was 2 bag1, 1
bag2 and 4 chain, and in the biceps, 2 bag1 and 4 chain
fibers (Table 2).
Combinations of Intrafusal Fiber Types
For the masseter single muscle spindles, there were
67 different combinations of bag1, AS-bag1, bag2 and
chain fibers. Of these, 47 (70%) appeared once, nine
twice, nine three times, one four times and one eight
times. The corresponding values for the biceps were 39
combinations, of which 31 (79%) appeared once, five
twice, two three times and one four times (Table 3).
Data for compound masseter and biceps muscle spindles
are shown in Table 3. Of the 67 different combinations
in the masseter, two overlapped the sup ant and sup
post masseter portions, six overlapped the sup ant and
deep, three sup post and deep, and only one combination
(2 bag1 and 2 chain fibers) overlapped all three portions.
Of the 67 masseter and 39 biceps fiber type combinations, thirteen were found in both muscles. A comparison
between subjects showed that of the 67 masseter combi-
nations, 31 (46%) were seen in subject one, 17 (25%) in
subject two and 36 (53%) in subject three. Only 2 (3%)
overlapped all three subjects. Of the 39 combinations in
the biceps, 16 (41%) were seen in subject one, 6 (15%) in
subject two, 5 (13%) in subject three, 7 (19%) in subject
four, 5 (13%) in subject five and 5 (13%) in subject six,
without any overlap among the six subjects.
Diameter of Intrafusal Fibers
The diameter of intrafusal fiber types in the masseter
was measured in 884 out of 1223 fibers (255 bag1, 22
AS-bag1, 162 bag2 and 445 chain), and for the biceps in
349 out of 434 fibers (89 bag1, 25 AS-bag1, 13 bag2 and
222 chain). The diameters of the masseter intrafusal
fiber types (lm, mean SD) were bag2 18.4 (1.6) > bag1
15.2 (1.8) > AS-bag1 14.9 (2.2) > chain 10.2 (1.2). In the
biceps the diameters were bag2 17.8 (3.1) > AS-bag1 15.0
(2.4) > bag1 13.9 (2.1) > chain 8.2 (0.3). In the masseter,
bag2 fibers were significantly larger than both bag1 and
chain fibers (P ¼ 0.028 and P ¼ 0.013, respectively).
There were no differences between the masseter muscle
688
ÖSTERLUND ET AL.
Fig. 3. Serial cross-sections of single spindles of the deep masseter (left) and biceps (right), stained for mATPase pH 10.3, (a, d), pH
4.6 (b, e) and pH 4.3 and (c, f). The deep masseter spindle (subject 4
years) contains 20 intrafusal fibers (5 bag1, 6 bag2 and 9 chain fibers
þ 4 fibers within the capsule tissue), and the biceps spindle (subject 3
years) nine intrafusal fibers (1 bag1, 1 AS-bag1 and 7 chain fibers).
Fiber types bag1, AS-bag1 bag2 and chain have been labelled. Bar ¼
50 lm.
portions. Also in the biceps, bag1, AS-bag1 and bag2,
were significantly larger than chain fibers (P ¼ 0.001, P
¼ 0.002 and P ¼ 0.002, respectively). Masseter bag1
fibers were significantly larger than those of the biceps
(P ¼ 0.049). The mean intrafusal fiber diameter for
pooled data of bag1, AS-bag1, bag2 and chain fibers (lm,
mean SD) was significantly larger in the masseter (n ¼
884), 13.5 (2), than in the biceps (n ¼ 349), 10.0 (1) (P ¼
0.045).
Comparison Between Young and Adult
Masseter Muscle Spindles
The muscle spindle density was significantly higher (P
¼ 0.005) in young masseter, 25, than in adult (Eriksson
and Thornell, 1987) masseter, 7. In both young and
adult masseter, the deep portion contains the majority of
spindles (young 61% and adult 74%), and compound
muscle spindles occur in a significant amount. Young
689
MASSETER MUSCLE SPINDLES AT YOUNG AGE
Fig. 4. Myofibrillar ATPase-staining pattern at pH 10.3, 4.6 and 4.3 of bag1, AS-bag1, bag2 and chain
fibers in the A, AB, B and C regions of masseter and biceps muscle spindles. Proportion (%) of
unstained, and weakly, moderately or strongly stained fibers.
masseter did not differ from the adult (Eriksson and
Thornell, 1990) in number of intrafusal fibers of single
spindles (young 8.3, adult 7.3), capsule diameter of single spindles (young 96 lm, adult 98 lm) or intrafusal
fiber diameter (young 13.5 lm, adult 16 lm). The ratio
between the mean bag fiber diameter (pooled data for
bag1, AS-bag1 and bag2 fibers, (n ¼ 439) and the mean
diameter of extrafusal type I fibers (Österlund et al., in
press) was 0.8 (16.5 lm/21.7 lm) for the young masseter
versus 0.4 (18.1 lm/43.9 lm) for the adult (Eriksson and
Thornell, 1990).
Comparison Between Young and Adult Biceps
Muscle Spindles
Young and adult (Liu et al., 2002) biceps muscle spindles were similar in enzyme-histochemical staining pattern of intrafusal fiber types, mean number of intrafusal
fibers per muscle spindle, heterogeneity in combinations
of intrafusal fiber types and lack of bag2 fibers.
DISCUSSION
Fig. 5. Relative proportion (%) of intrafusal fiber types bag1, ASbag1 bag2 and chain in the spindle populations of young masseter
and biceps. Data based on average values for three masseter and six
biceps muscles. Note, more bag2 and less chain fibers in the
masseter.
The main finding of this study was the general resemblance in muscle spindle morphology between young
masseter and adult masseter (Eriksson and Thornell,
1987, 1990; Eriksson et al., 1995). Hence, contrary to
690
ÖSTERLUND ET AL.
TABLE 2. Average composition (mean, median, and min-max) of intrafusal fiber types in single and
compound masseter and biceps muscle spindles (MS)
Single MS
Masseter
Mean (SD)
Median
Min-max
Biceps
Mean (SD)
Median
Min-max
Compound MS
Bag1
AS-Bag1
Bag2
Chain
Bag1
AS-Bag1
Bag2
Chain
2.0 (2)
2
0–8
0.2 (0)
0
0–3
1.0 (1)
1
0–5
4.0 (4)
4
0–12
5.5 (3)
6
0–11
0.2 (1)
0
0–4
3.4 (3)
2
3–12
7.7 (5)
7
5–20
1.8 (1)
2
0–5
0.5 (1)
0
0–4
0.3 (1)
0
0–2
4.8 (2)
4
1–14
7.0 (1)
7
6–8
1.5 (1)
2
1–2
0.5 (1)
1
0–1
13.5 (4)
14
12–15
our hypothesis, masseter muscle spindles do not undergo
major changes in morphology and composition and distribution of intrafusal fiber types from young age to
adulthood. The result was similar for the biceps muscle,
that is, young spindles were alike adult spindles (Liu
et al., 2002). These findings show that the human masseter and biceps muscle spindles are differentiated and
morphologically mature already at young age. The current result contrasts our recent findings of significant
differences between young and adult masseter extrafusal
fiber type compositions (Österlund et al., in press). We
therefore conclude that muscle spindles precede the
extrafusal fiber population in growth and maturation.
This in turn suggests early proprioceptive demands during growth and maturation of jaw motor skills. Correspondingly, well-developed muscle spindles in young
biceps brachii reflect significant need of reflex control in
learning and performing arm motor behavior. Nevertheless, the more complex morphology of young masseter
spindles versus young biceps spindles indicates a more
advanced proprioceptive control of the masseter muscle.
Notably, difference between masseter single and compound spindles in distribution of frequency of spindles
versus number of intrafusal fibers indicates two separate
populations of muscle spindles in young masseter.
Young and adult masseter muscle spindles were similar in containing exceptionally large capsule diameter
and high number of intrafusal fibers, high frequency of
compound spindles and heterogeneous distribution and
most complexly arranged spindles located in the deep
masseter. However, the muscle spindle density was three
times higher in the young than in the adult (Eriksson
and Thornell, 1987) masseter. Muscle spindle density
varies significantly between different muscles (Boyd and
Smith, 1984) and can be regarded as an indicator of
functional differences. Muscles active in gross movements have low spindle density whereas muscles initiating fine movements or maintaining postural stability
have a high spindle density, for example, the extra ocular (Bruenech and Ruskell, 2001; Boyd-Clark et al.,
2002), lumbrical (Soukup et al., 2003) and neck (BoydClark et al., 2002; Liu et al., 2003) muscles. Given that
the extrafusal fiber diameter is about two times larger
in the adult than in the young masseter (Österlund
et al., in press) the adult masseter volume is about twice
that of the young masseter. Therefore, since young and
adult spindles are of similar size, an age-related
decrease in spindle density is explainable. An additional
marker for comparing young and adult spindles is the
ratio between intrafusal and extrafusal fiber diameter.
This ratio was larger in the young than in adult masseter, 0.8 versus 0.4. Likewise, for the biceps, corresponding ratios were 0.6 and 0.3. Taken together, these data
suggest larger functional influence of muscle spindles at
young age, especially for the masseter muscle.
Both the masseter and biceps were strikingly heterogeneous in allotment of types and number of intrafusal
fibers, and the ‘‘average’’ composition of intrafusal fiber
types (Table 2) should not be taken as ‘‘the typical’’ muscle spindle appearance. Rather, most spindles were
unique in the combination of intrafusal fiber types, that
is, the majority of combinations occurring only once.
Furthermore, only one intrafusal fiber type combination
overlapped all three masseter portions, and few combinations overlapped the young masseter and biceps. Also
individuals were unique in fiber type composition of
muscle spindles, with hardly any overlapping combinations between subjects. Although noted in a limited
number of subjects, this variability in morphology
between spindles, muscle portions, muscles and subjects
suggest highly differentiated proprioceptive abilities allocated in governing mandibular and arm positions and
movements.
The present data showed that lack of bag2 fibers was
common in the young masseter and biceps muscle spindles. Spindles lacking bag2 fibers have previously been
reported for the human adult biceps brachii (Liu et al.,
2002) and deep neck (Liu et al., 2003) muscles. Bag1
fibers are known to play a major role in the production
of the velocity-sensitive (dynamic) response in the primary endings whereas bag2 fibers mediate the length
(static) sensitivity along with chain fibers (Boyd, 1980;
Matthews, 1981a; Barker and Banks, 1994). Furthermore, five of the young masseter spindles (4%) lacked
chain fibers, but of these, all contained bag1 and four
contained bag2 fibers, suggesting ability for both
dynamic and static sensitivity. Taken together, lack of
bag2 and chain fibers would again reflect diversity in
physiological qualities between spindles and muscles,
preferentially in static length sensitivity properties.
AS-bag1 fibers, described previously in the adult masseter (Eriksson and Thornell, 1985, 1987, 1990; Eriksson
et al., 1994) but not in the biceps, were more frequent in
the young biceps. Its physiological characteristics and
role in proprioceptive control remains to be examined.
Reflex mediated stiffness contributes to the maintenance of mandibular posture relative to the maxilla during locomotion (Miles et al., 2004; Miles, 2007). It has
been hypothesized that the jaw stretch reflex may play
an important role in contributing to the stiffness of the
691
MASSETER MUSCLE SPINDLES AT YOUNG AGE
TABLE 3. Combinations of intrafusal fiber types
in single and compound masseter and biceps brachii
muscle spindles. In the masseter single muscle
spindles, there were 67 combinations of intrafusal
fiber types, in the biceps 39. In the masseter
compound muscle spindles, there were 22
combinations of intrafusal fiber types, in the biceps
two
Masseter single MS
Combinations
1
1
1
1
2
1
1
1
1
2
1
1
1
5
5
3
1
1
1
1
6
3
1
3
2
3
5
5
1
1
4
P
Bag1
AS-Bag2
Bag2
Chain
8
7
6
5
5
4
4
4
4
4
4
3
3
3
3
3
2
2
2
2
2
2
1
1
1
1
1
1
0
0
0
0
l
0
1
0
3
1
0
0
0
0
2
0
0
0
0
2
1
1
1
0
0
1
1
1
0
0
0
2
1
0
2
3
0
1
1
1
0
3
2
1
0
1
3
2
1
0
1
5
3
1
1
0
3
1
0
2
1
0
1
1
1
12
7
9
11
3, 12
4
9
7
0, 7
3, 4
5
2
3
1, 2, 3, 5, 6
2, 4, 5, 6, 8
3, 5, 8
3
8
6
5
1, 3, 4, 5, 6, 11
2, 3, 4
4
1, 2, 3
3, 4
0, 4, 8
2, 4, 5, 7, 10
0, 1, 3, 4, 5
3
3
0, 2, 3, 4
67
Biceps single MS
Combinations
2
1
1
2
2
3
1
4
3
3
1
6
4
4
2
P
Bag1
AS-Bag1
Bag2
Chain
5
4
3
3
3
3
2
2
2
2
1
1
1
1
0
0
1
2
0
0
0
4
1
0
0
1
1
0
0
1
0
0
0
2
1
0
0
0
1
0
1
0
1
0
0
6, 7
5
7
2, 14
5, 8
5, 6, 7
5
3, 4, 5, 6
5, 7, 8
2, 4, 5
3
1, 3, 4, 5, 6, 7
3, 4, 8, 9
2, 3, 4, 6
2, 3
39
mandible in speech production (Smith, 1992). During fetal life survival reflexes are gradually succeeded by automatic postural reflexes in neonatal life. The trigeminal
sensori-motor system develops early in neonatal period
(Jääskälainen, 1993). Actually, the earliest reflex found
Table 3. (continued)
Masseter compound MS
Combinations
1
1
1
1
1
1
1
1
2
1
1
2
1
1
1
1
1
1
1
P
Bag1
AS-Bag1
Bag2
Chain
11
11
9
9
7
7
7
7
6
5
5
4
4
3
3
2
1
1
0
0
0
1
0
0
0
0
0
0
0
0
0
4
0
0
0
0
0
0
7
2
10
5
0
1
5
2
2
2
1
2
3
6
3
1
4
1
12
20
14
8
12
10
5
8
3
1, 6
4
4
6, 13
7
1
10
5
2
10
14
22
Biceps compound MS
Combinations
1
1
P
Bag1
AS-Bag1
Bag2
Chain
8
6
1
2
1
0
12
15
2
in the human embryo is the trigemino-neck reflex. A
head withdrawal effect from stimulation of the upper lip
has been detected already at the seventh gestational
week (Humphrey, 1952). Studies in neonates, infants
and children have shown that reflex response properties
change dramatically with development. For both myotatic and cutaneous reflexes, ‘‘mature’’ patterns do not
emerge until late childhood (Finan and Smith, 2005).
These functional changes occur in parallel with substantial morphological transformations of the skeleton,
muscles and nervous system. The morphological and
functional changes may also include modification of the
functional role of reflexes coincident with developing
motor skills. Our present finding of a general resemblance between young and adult masseter muscle spindles suggests that the morphological basis for reflex jaw
motor control in learning and improving jaw motor tasks
is well differentiated and matured already at young age.
In both the adult (Eriksson and Thornell, 1987) and
young masseter, the deep portion contained the highest
spindle density and the most complex spindles. This portion is composed of vertically running fibers and a preponderance of type I fibers, which build up slow twitch,
low threshold motor units. Therefore, its extrafusal and
intrafusal fibers in combination make the deep portion
well adapted for postural mandibular control, possibly of
special importance in early learning and improving
speech function. In speech, precise jaw movements occur
within a three-dimensional space around the mandibular
postural position. Interestingly, the number of muscle
spindles in the jaw muscles seems to increase in the evolutionary series from lower primates towards man
(Kubota and Masegi, 1975, 1977). This observation
692
ÖSTERLUND ET AL.
suggests changes during evolution towards stronger proprioceptive impact on jaw motor control as for movements in mastication and learning and production of
speech, a function evolved only in man.
Previous findings of coordinated mandibular and
head-neck movements during natural jaw-opening closing tasks suggest a functional interlinkage between the
jaw and the neck sensori-motor systems. Studies also
indicate that this functional connection between the jaw
and neck sensori-motor systems is innate (c.f. Zafar
et al., 2000; Häggman-Henrikson and Eriksson, 2004;
Eriksson et al., 2007). Furthermore, there is experimental evidence of reflex connections between the masseter
and neck muscles (Hellström et al., 2000). To evaluate
the functional maturation of the jaw-neck motor coupling at young age we have examined concomitant mandibular and head-neck movements during jaw openingclosing motor activities in 5–6-year-old children. The
results contrast findings in adults. Adults show well
coordinated and regular spatiotemporal patterns of both
mandibular and head-neck movements, whereas movement patterns in children are irregular and variable
(Zafar et al., unpublished results). The findings suggest
an immature reflex motor programming of jaw actions in
children, although, as demonstrated in the present
study, the muscle spindle system may be morphologically
well differentiated and matured.
In conclusion, resemblance in muscle spindle morphology between young and adult human masseter and
biceps muscles, respectively, suggests early growth and
maturation of muscle spindles, in favour of learning and
improving jaw and arm motor skills. We also conclude
that masseter and biceps muscle spindles precede extrafusal fibers in growth and maturation.
ACKNOWLEDGMENTS
The authors thank Mrs. Inga Johansson for excellent
technical assistance and associate professor Albert Crenshaw for English revision and valuable comments.
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