1Medical Research Council Group in Sensory-Motor Neuroscience, 2Department of Physiology, and 3Department of Anatomy, Queen's University, Kingston, Ontario K7L 3N6, Canada; and 4School of Pharmacy, University of Southern California, Los Angeles, California 90033
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ABSTRACT |
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Richmond, Frances J. R., Kan Singh, and Brian D. Corneil. Neck Muscles in the Rhesus Monkey. I. Muscle Morphometry and Histochemistry. J. Neurophysiol. 86: 1717-1728, 2001. Morphometric methods were used to describe the musculotendinous lengths, fascicle lengths, pennation angles, and cross-sectional areas of neck muscles in adult Macaca mulatta monkeys. Additionally, muscles were frozen, sectioned, and stained for ATPase activity to determine fiber-type composition. Individual rhesus muscles were found to vary widely in their degree of similarity to feline and human muscles studied previously. Suboccipital muscles and muscles supplied by the spinal accessory nerve were most similar to human homologs, whereas most other muscles exhibited architectural specializations. Many neck muscles were architecturally complex, with multiple attachments and internal aponeuroses or tendinous inscriptions that affected the determination of their cross-sectional areas. All muscles were composed of a mixture of type I, IIa, and IIb fiber types the relative proportions of which varied. Typically, head-turning muscles had lower proportions of type II (fast) fibers than homologous feline muscles, whereas extensor muscles contained higher proportions of type II fibers. The physical and histochemical specializations described here are known to have a direct bearing on functional properties, such as force-developing capacity and fatigue-resistance. These specializations must be recognized if muscles are to be modeled accurately or studied electrophysiologically.
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INTRODUCTION |
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Our understanding of
human motor control often depends on extrapolating results from
experimental animals. In the past, most studies of head movement have
been conducted in cats. However, as more is learned about the skeletal
relationships and musculature of the feline neck, differences are
identified that may limit the usefulness of the cat as an appropriate
model for human head movement. In a standing or sitting cat, the normal
posture of the neck has a nearly right-angled flexure at the transition
between the cervical and thoracic parts of the vertebral column
(Vidal et al. 1986). The head and neck are cantilevered
rostrally to the body so that gravitational forces on the head must be
opposed by the actions of strong extensor muscles attaching to the
thoracic vertebral column and shoulder girdle (MacPherson and Ye
1998
; Runciman and Richmond 1997
). In contrast,
the human head is carried more directly over the trunk so that much of
its weight is borne passively on the pillar-like vertebral column
(Graf et al. 1994
, 1995a
,b
; Le Gros Clark
1962
; Tobias 1992
). The shoulder girdle in
humans is also configured differently to facilitate the use of the arms
and hands for object manipulation. For example, the clavicle is long
and fixed, and the scapula is oriented in the frontal rather than the
parasagittal plane. In parallel with skeletal changes, muscle
attachments are reorganized and the number of extensor muscles is
reduced (Kamibayashi and Richmond 1998
; Oxnard 1967
).
Monkeys may provide a better model than the cat for experimental
studies of head movement. Monkeys are already used as the species of
choice for many chronic studies of eye-movement control. Thus much is
known about the organization and properties of neural circuits that are
likely to participate in the control of at least one aspect of the
"gaze"-control system coordinating head and eye movement (e.g.,
Cullen and Guitton 1997; Freedman and Sparks 1997
; Moschovakis et al. 1996
). Further, monkeys
can be trained to carry out sophisticated movement sequences beyond the
capabilities of even the most cooperative and highly motivated cat.
However, studies on monkey head movements have been impeded by a
relatively poor foundation of information about musculoskeletal organization in the neck. A few anatomical surveys of neck muscles exist (e.g., Berringer et al. 1968; Hartman and
Straus 1961
; Szebenyi 1969
), but the reports are
qualitative and generally focus on superficial muscles. Further, almost
nothing is known about the relative force-generating capacities and
histochemical compositions of simian neck muscles even though such
information can provide significant insights into their functional
roles. These data must be acquired before neck muscles can be modeled
or studied physiologically in any detail. Further, they would help to
identify features that are dissimilar to those in humans. Some amount
of dissimilarity should be expected because rhesus monkeys are
terrestrial quadrupeds, although they can resort to facultative
bipedalism when required (Juschke 1972
; Napier
and Napier 1985
) with narrower shoulder girdles and scapulae
that are oriented more parasagittally than those of human primates
(Le Gros Clark 1962
; Oxnard 1967
).
In present studies, we have evaluated the morphometry and fiber-type
distribution of neck muscles in the rhesus monkey. Methods were chosen
to complement a similar recently published analysis of human neck
muscles (Kamibayashi and Richmond 1998). Data from the
present work identify a number of differences in muscle structure between these two primates and serve as a basis for biomechanical models of the rhesus head-neck system. They further provided an anatomical guide for functional studies of neck muscles reported in the
companion paper (Corneil et al. 2001
).
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METHODS |
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Systematic morphometric measurements of neck muscles were made in three adult female rhesus monkeys Macaca mulatta (7.4-7.9 kg) and supplemented by further measurements on selected muscles in an additional four animals (2 female, 5.3-6 kg; 2 male, 5.7-6.3 kg). Histochemical analyses were carried out on neck muscles removed from six rhesus monkeys (4 female, 4.7-5.7 kg, and 2 male, 6.2 and 7.5 kg). The monkeys were housed in a light- and temperature-controlled environment. All animal-care and experimental procedures were carried out according to the guidelines of the Canadian Council on Animal Care and were approved by the Queen's University Animal Use committee. Some monkeys had previously been subjects in electrophysiological studies of the superior colliculus or in studies of reproductive hormone cycling that did not appear to affect the musculature. The animals were anesthetized intravenously with a mixture of Saffan (alphaloxalone and alphadolone acetate, Cooper's Agrofarm, Ajax, 0.5 ml/kg) and ketamine hydrochloride (Rogar/STB, 6-9 mg/kg iv). In some monkeys, the carotid arteries were catheterized, and the brains of the monkeys were perfused, first with phosphate-buffered saline and then with 4% paraformaldehyde solution. The other monkeys were killed with an overdose of pentobarbital sodium.
Morphometry
The muscles under investigation were weighed and fixed in 10%
formalin. Fixed muscles were reweighed. Fascicle lengths were measured
at different sites across the muscle width on both the superficial and
deep surfaces of the muscles. In muscles in which fascicle length
changed progressively across the width or depth of the muscle, the
muscle was modeled as one or more parallelograms and mean fascicle
length was computed by averaging the lengths of fascicles composing the
long and short sides. Cross-sectional areas of simian muscles were also
scaled up or down to facilitate comparisons with homologous muscles in
humans and cats by relating an 8-kg monkey to a 64-kg human or a
3.35-kg cat. If the musculature of the three species was to be similar
geometrically, the linear dimensions from cat to monkey to man should
scale in a ratio of 1.5:2:4 and cross-sectional areas (CSAs) should
scale in a ratio of 2.25:4:16 (linear dimension2)
(Schmidt-Nielsen 1984). Pennation angles (
) were
measured with respect to the line-of-pull of the muscle using a
protractor. Physiological CSAs (PCSAs) were calculated using the
equation, PCSA = mass (g) × cos
/fascicle
length (cm) × density (g/cm3). A uniform
density of 1.06 g/cm3 was assumed (Mendez
and Keys 1960
). Sarcomere lengths were measured by examining
the fibers of small excised pieces of muscle from at least three
different sites using 100 × oil immersion objective as described
in detail elsewhere (Selbie et al. 1993
). Fascicle lengths from the sampled muscle were then normalized by adjusting the
value of length to that appropriate for a standard sarcomere length of
2.5 µm (Herzog et al. 1992
).
Histochemistry
Muscles were dissected for histochemical analysis within 3 h after the death of the animal. They were divided into blocks 1-2 cm
in height that were mounted using embedding medium in a recorded
orientation onto numbered cryostat chucks. The blocks were covered with
talcum powder and immersed in liquid nitrogen where they were stored.
Sets of serial 16-µm sections were cut using a cryostat and mounted
on gelatin-coated slides. Sequential sections were stained with
hematoxylin and eosin and for myosin adenosine triphosphatase (ATPase)
activity after alkaline preincubation at pH 10.4 (Guth and
Samaha 1970). Sections to be stained for ATPase activity were
kept in a sealed container containing a desiccating compound for
2 h
after being cut to minimize hydration of tissue and loss of enzyme
reactivity. Systematic variation of staining variables for ATPase
staining showed that consistent differences between fiber types were
obtained by fixing sections in 5% formalin for 2.5 min rather than 5 min and preincubating them in alkali solution for 4 min rather than 15 min. Sections were immersed in 1% ammonium sulfide for 1 min rather
than the 3 min recommended in original protocols.
Stained sections were magnified and drawn with the aid of a microfiche
reader. Some sections were scanned using a high-resolution color
scanner or slide scanner adapted for histological sections (SprintScan
35 Plus, Polaroid). Regions containing obviously different fiber-type
proportions were identified. At higher magnification, fibers were
classified as type I (equivalent to SO; light staining), type IIa (FOG;
intermediate staining), and type IIb (FG; dark staining) types by
criteria described previously (Bagnall et al. 1983;
McIntosh et al. 1985
) (Fig.
1). Relative contents of different fiber
types were estimated by identifying the staining profiles of ~200
fibers at three to five sites in each cross-section (Richmond and Abrahams 1975
).
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RESULTS |
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Muscles invest the monkey neck in several layers. The largest and most superficial layer is composed of muscles that link the skull and cervical vertebrae to the shoulder girdle. Intermediate layers consist chiefly of long muscles linking the skull to lower cervical and thoracic vertebrae. The deepest muscles connect the skull to upper cervical vertebrae, or interconnect vertebral bones.
Muscles that link the head and neck with the shoulder girdle
TRAPEZIUS. Trapezius (TRAP) is a broad, sheet-like muscle that originates from occipital crest of the skull and the vertebral midline between the skull and T10 (Fig. 2; see Table 1 for a list of muscle abbreviations). At both ends of its vertebral origin, fibers attach directly to the midline raphe, but in the upper thoracic region, the muscle attaches to the midline by way of a diamond-shaped aponeurotic sheet. Fascicles run caudolaterally to attach in a continuous line onto the distal margin of the clavicle, the acromion, and the scapular spine. At the caudal-most end of the scapular spine, fibers from thoracic vertebrae converge to form a semilunar array radiating from a short, thick tendon that focuses much of the force-generating capacity of the caudal muscle on a narrow site (Fig. 2).
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STERNOCLEIDOMASTOID.
Sternocleidomastoid (SCM) is a superficial muscle whose
three strap-like heads wrap around the lateral neck in a pattern like that in man (Kamibayashi and Richmond 1998) (Fig.
3). The most medial head,
sternomastoid (SM), originates on the manubrium and inserts
at a pinnation angle of 10-20° onto a thickened tendon attaching to
the mastoid process. Two muscle heads with clavicular insertions are
located lateral and deep, respectively, to SM. The
cleidooccipital (CO) head has a similar length and CSA to SM
(~0.5 cm2, Table 1), but is wider and thinner.
It originates from on the medial part of the clavicle. As it runs
rostrally, it fuses to the lateral edge of SM and extends its
attachment onto the occiput adjacent to the mastoid process. The third
head, cleidomastoid (CM), has a relatively small CSA (~0.3
cm2). It originates deep and medial to CO,
crosses obliquely on the undersurface of SM and inserts deep to it on
the mastoid process. CM is mostly, or entirely, hidden when the muscle
is viewed from the superficial surface (Fig. 3).
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RHOMBOIDEUS. Rhomboideus (RH), like trapezius, has a broad origin from the skull and nuchal midline raphe. In most specimens, its rostral part appeared as a thin (CSA = 0.1-0.2 cm2), separate, strap-like head called rhomboideus capitis (RH cap) that ran between the medial part of the occipital crest and the vertebral border of the scapula (Fig. 4). In a few animals, the muscle origin also lapped from the skull onto the nuchal midline raphe. In a single case, this origin was particularly wide and the lateral edge of the muscle was fused to the adjacent rhomboideus cervicis.
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ATLANTOSCAPULARIS.
The scapula is linked to the cervical vertebral column by two
atlantoscapularis muscles. Atlantoscapularis anterior (AS
ant) is homologous to levator scapulae ventralis in cats and
humans (e.g., Kamibayashi and Richmond 1998;
Richmond et al. 1999a
). It is a thick strap lying
immediately deep to trapezius that attaches to the lateral (coracoid)
half of the scapular spine (Fig. 4). It runs rostrally for ~5 cm and
inserts on the ventral border of the transverse process of
C1.
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SCALENUS.
Scalenus is a laterally placed set of muscle heads whose complex
relationships and attachments between vertebrae and the scapulae and
ribs have been described and illustrated in detail previously for
M. cyclopis (Hsiao 1976). Only the most
cervical of the heads, scalenus brevis posterior (SCA
post), was studied quantitatively. It originates on a narrow
site dorsolaterally on the first rib and attaches to the transverse
processes of vertebrae of
C1-C7 (although in 1 animal the attachment to C1 was absent). Scalenus has an unusually high content of type IIa fibers (35-50%, Table 2)
and more modest densities of type IIb (15-40%) and I (20-35%) fibers. Type I fibers tend to be most dense in the core of the muscle.
Muscles linking the skull and vertebral column
SPLENIUS.
Splenius capitis (SP cap) is a large muscle (CSA 1.5 cm2, Table 1) that originates from the nuchal
midline as far caudally as T3 or
T4 and runs rostrolaterally to insert along the
whole width of the occipital crest (Fig.
7A). A narrow lateral strip that inserts on the lateral wing of the atlas called splenius cervicis (SP cerv) can also be recognized in some animals (Fig. 6C). Like feline splenius (Richmond et al.
1985
), rhesus SP cap is crossed laterally by two inscriptions
that do not span the whole width of the muscle (Fig. 7A).
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LONGISSIMUS.
Three parts of longissimus can be identified in the cervical region.
Lateral to SP, longissimus capitis (LONG cap) originates from the transverse processes of upper thoracic and lower cervical vertebrae and inserts onto a tough narrow tendon close to the mastoid
process (Fig. 6C and 7B). At its caudal limit it
appears to merge with the attachments of biventer cervicis. LONG cap
has at least one inscription through its midsection. It contains a relatively even mix of type IIb, IIa, and I fibers. Longissimus cervicis (LONG cerv) lies on the lateral aspect of LONG cap
(Hartman and Straus 1961). It is composed of shorter
fascicles spanning between the tubercular processes of thoracic
vertebrae and the transverse processes of cervical vertebrae (Fig.
6C). The complex relationships and relatively small size of
this component made analysis difficult and morphometric measurements
are not included in Table 1.
SEMISPINALIS CAPITIS.
Semispinalis capitis (SS cap) lies deep to splenius. It has
two parts, called biventer cervicis (BC) and
complexus (COM) (Hartman and Straus 1961)
that are partially fused in most animals but separated in a few
specimens (Fig. 7B). The more medial BC is a
parallel-fibered muscle that originates from tendinous strands attaching to the ribs and tubercular processes of thoracic vertebrae T3-T7. It inserts medially
on the occipital crest. The architecture of the muscle is made complex
by the presence of two to three tendinous bands or strips that vary in
prominence from one animal to another (Fig. 7B). Immediately
lateral on the occipital crest is the attachment of COM. Its fibers
arise as a series of slips from the tubercular processes of the most
rostral two or three thoracic vertebrae and from transverse processes
of vertebrae C3-C7. These
slips insert onto an inscription that crosses the width of the muscle.
From the other side of the inscription arise fibers that run rostrally
to the occiput.
SUBOCCIPITAL MUSCLES. The upper cervical vertebrae are invested with short muscles that cover all surfaces of the axis and atlas. Dorsally are two muscle groups, the rectus capitis posterior group and the obliquus capitis group (Fig. 7C). Rectus capitis posterior (RCP) has two fan-shaped layers that have similar CSAs. The most superficial layer is formed by rectus capitis posterior major (RCP maj), which arises below the lateral part of the occipital crest (Fig. 7C). It runs at an angle of ~25° with respect to the longitudinal midline and converges to a narrowed attachment on the spinous process of C2. Deep and medial to it is rectus capitis posterior minor (RCP min), which runs from the medial occiput to the dorsal arch of the axis. It is shorter and lighter than RCP maj, and can be difficult to remove without damage. Obliquus capitis inferior (OCI) is a fleshy short strap that runs obliquely from the spinous process of C2 to the transverse process of the atlas (Fig. 7C) Obliquus capitis superior (OCS) runs from the rostral aspect of the C1 transverse process to the lateral part of the occiput, deep and lateral to RCP maj. It has a pinnate organization around a buried aponeurosis so that its fascicle lengths are shorter and CSA is larger than might be predicted by modeling the muscle as a simple strap.
Both rectus and obliquus muscles were found to have a markedly nonuniform distribution of fiber types despite their small size, so that it is risky to assign a single value for fiber-type proportions (Table 3). RCP maj and min had a steep gradient in the distribution of fiber types in which type II fibers predominated on the dorsal surface whereas type I fibers predominated deeper. OCI had a particularly nonuniform organization. The deep surface of the muscle was composed exclusively or almost exclusively of type I fibers whereas the dorsal surface was composed almost entirely of type II fibers, as described in more detail elsewhere (Richmond et al. 1999b
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Intervertebral muscles
Several small muscles invest cervical vertebrae caudal to C2. Only limited sampling and observations of these deeply placed muscles were possible because they were difficult to remove without damage. Spinalis dorsi (SD) and semispinalis cervicis (SSC) lie dorsally and dorsolaterally, deep to semispinalis capitis (Fig. 7C). SD is relatively small and joins successive spinous processes of cervical vertebrae. It appears to fuse with SSC that joins the spinous processes of the same vertebrae with transverse processes of vertebrae located more caudally. Fascicles in the lateral part of the muscle are shorter and attach to more caudal cervical vertebrae than those in the medial part of the muscle. Medial fascicles also have a less angled orientation with respect to the vertebral midline. In two muscles, fascicles in most regions contained a relatively even overall mix of fiber types (Table 2), although some central fascicles contained 40-50% type I fibers.
Multifidus muscles are intertransverse muscle slips that invest the lateral aspects of the vertebrae, lateral to semispinalis cervicis. Fiber bundles link transverse processes, one, two, or three vertebrae away from their origins. These muscles were not sampled.
The ventral aspects of the vertebrae are invested by the muscle longus colli. This muscle is also complex. It is composed of fiber bundles that form pinnate slips joining the ventral surfaces of the cervical vertebrae to the transverse processes of more caudal counterparts. This complex architecture made morphometric analysis very difficult so that values of CSA could not be estimated reliably without more sophisticated microdissections beyond the scope of this analysis. In the one muscle that was examined histochemically, type I fiber proportions were low (~25%) and type IIb and IIa fibers accounted for 40 and 35% of fibers, respectively.
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DISCUSSION |
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Studies of rhesus neck muscles afford an opportunity to examine
the comparative anatomy of a species that appears to be transitional in
its neck-muscle organization between human bipeds and nonprimate quadrupeds such as cats (see also Graf et al. 1994). At
least two differences from previously studied quadrupeds may be
particularly significant functionally. First is the relative reduction
in the size and numbers of the available extensor muscles. Second is the differing arrangement of shoulder-girdle muscles around the fixed
clavicle and scapula. The differences in shoulder-girdle attachments
change the lines of pull of some muscles. These muscles also exhibit
differences in CSAs and fiber-type distributions when compared with
those of quadrupeds, presumably reflecting specializations in
functional roles.
Differences in dorsal extensors
In both cats and monkeys, dorsal neck muscles are larger and more
numerous than ventral muscles. A strong set of dorsal muscles is needed
presumably to hold up a heavy head whose center of mass is located in
front of the vertebral column (Tobias 1992). In cats,
the forward movement of the head is known to be opposed by tonic
contractions in at least two dorsal muscles, occipitoscapularis (equivalent to RH cap) and BC (Richmond et al. 1992
)
that are rich on type 1, or slow, fibers (Richmond and Abrahams
1975
). In rhesus monkeys, homologous muscles were found to have
somewhat lower type I fiber proportions than feline muscles (Fig.
8). The lower content of slow fibers did
not appear to be due to an "across-the-board" decrease in type I
fiber contents in rhesus muscles; other muscles in the rhesus neck had
higher type I fiber contents than homologous feline muscles (Fig. 8).
The relative CSAs of rhesus extensors also differed from values that
might be expected if the CSAs of homologous feline muscles were simply
scaled up (Fig. 9). The CSA of RH cap in
the monkey was found to be ~2.5 times that of feline
occipitoscapularis (rather bigger than might be expected from scaling
increases alone), whereas those of BC and COM were smaller than might
be expected. The overall diminution in CSA may reflect the fact that
the center of mass for the monkey skull is closer to the vertebral
column (Tobias 1992
), so that relatively smaller forces
should be needed to counteract gravitational torques at the
skull-C1 joint. Nevertheless, biomechanical
analyses will be needed to identify whether these differences, which
will affect force-developing capacity, are offset by moment-arm changes
due to differences in the skeletal geometry and muscular sites of attachment.
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The dorsal extensor muscles studied here contained a mix of anatomical
elements that could be related in some instances to forms described in
cats but in others to the quite distinct morphology of human muscles.
For example, "semispinalis capitis" was found to have two heads
homologous to BC and COM in cats. However, the two heads in different
rhesus specimens were often fused, and the number and prominence of
tendinous inscriptions were found to be reduced. This trend is
exaggerated in man by the more complete fusion into a single
semispinalis muscle. RH cap, absent in man (Kamibayashi and
Richmond 1998) was found to be present in rhesus as in the cat
(Reighard and Jennings 1963
).
Compared with the dorsal extensors, the suboccipital muscles were less
"cat-like" and more humanoid. The close anatomical resemblance
between simian and human suboccipital muscles might be viewed as
evidence that suboccipital muscles in the two species are used
functionally for similar purposes. One such purpose is likely to be the
execution of small head movements during which they are more likely to
be active than larger extensors (Corneil et al. 2001).
Rhesus and human eyes are organized similarly in the skull and are
thought to move in similar ways, so that functional correlates might be
expected in the muscles subserving these tasks. However, human
suboccipital muscles have significantly smaller CSAs than might be
expected from scaled-up rhesus values. For example, CSAs for human RCP
maj and min together are only ~1.5 times those in monkeys, despite
the fact that the human head is nearly 10 times larger than that of the
monkey (Fig. 9). The observations may suggest that less extensor force
is needed to control sagittal-plane head movements in man; this change
in requirements might affect the timing and patterns of suboccipital
muscle recruitment. The larger size of rhesus suboccipital muscles may
also suggest that the muscles have additional roles, such as assisting
head extension when the animal adopts a quadrupedal posture. Such
behaviors may not be used so commonly in humans who bear the weight of
the skull in compression on a vertically oriented vertebral column
during most of their waking hours.
Rearrangement of shoulder muscles
Rhesus TRAP and SCM, like rhesus suboccipital muscles, had
anatomical features similar to those described in man
(Kamibayashi and Richmond 1998) and other nonhuman
primates (Kang 1975
; Larson et al.
1991
) even though the different species varied in their habitual patterns of locomotion, brachiation and prehension
(Oxnard 1967
). For example, rhesus TRAP, like that in
man, chimpanzee, and gorilla, was a single fused muscle sheet confined
almost exclusively to the dorsal surface of the body. In comparison,
feline TRAP is divided into three highly differentiated heads
(Reighard and Jennings 1963
; Richmond et al.
1999a
). The morphological differences between rhesus and feline
muscles appeared to be only one aspect of a broader range of changes
between the shoulder girdles of these two species. The cat has a small
floating clavicle that is functionally adaptive for cursorial
locomotion by increasing the range of limb excursion and thus the
length of stride (Jenkins 1974
). However, it provides
little space for the attachment of TRAP and SCM. In primates, the
clavicle forms a relatively long fixed strut between the manubrium and
the scapula. The rearrangement must change the biomechanical actions
and possibly the functional roles of muscles with clavicular
attachments such as SCM and TRAP. In similarly structured human
muscles, muscles are active during elevation of the shoulders (e.g.,
Bull et al. 1985
). Further, the attachment of TRAP and
SCM to the ribcage permits the muscles to play a role in lifting the
ribcage during forcible respiratory maneuvers (Campbell et al.
1970
; Legrand et al. 1997
). These roles seem to
contrast with patterns observed in cats, where the homologous muscles
appear to be recruited only by strong ballistic movements such as head
shaking (Richmond et al. 1992
).
Unlike TRAP and SCM, other rhesus muscles with shoulder-girdle
attachments seemed more similar to feline homologs. For example, rhesus
RH was found to have a strap-like "capitis" head of similar design
and fiber composition to the occipitoscapularis muscle in cats
(Richmond and Abrahams 1975). Its other RH heads, RH
cerv and dorsi, had features intermediate between feline and human counterparts. For example, the CSAs of RH cerv and dorsi were found to
be similar in rhesus; however, in man, RH min (equivalent to RH cerv)
is much smaller than RH maj (equivalent to RH dorsi), and in cats it is
much larger. Until the muscles are studied biomechanically and
physiologically in more detail, it will not be clear how these differences in force-generating capabilities relate to the roles played
by the muscles. We might speculate that the rostral parts of
rhomboideus in monkeys are larger than in humans because they help to
hold the necessary flexure between the thoracic and cervical column
when animals adopt a quadrupedal stance. Humans usually adopt this
posture for only the first year of life. The progressive expansion in
the CSA of caudal RH in rhesus and human may reflect a gradual
evolution in the use of the muscle in forelimb movements such as reaching.
Confusingly, certain rhesus shoulder muscles with the closest
resemblance to those in cats are called by different names in the most
commonly referenced text of rhesus anatomy (Hartman and Straus
1961). Atlantoscapularis anterior matches feline levator scapulae ventralis, and AT post was comparable to one part of feline
levator scapulae. Nevertheless, Hartman and Straus
(1961)
have chosen to distinguish the slip attaching to the
atlas as a separate muscle (AT post) and to consider the more caudal
contiguous part of the muscle as rostral serratus anterior. This
nomenclature has not been employed by all anatomists. Kato and
colleagues (1984
, 1993
) have considered the atlantal and
cervical muscle slips of this complex together as levator scapulae in
correspondence with descriptions in cats. We would prefer this latter
choice of names because it facilitates quantitative comparisons across species.
The functional roles of AS post (levator scapulae) and AS ant (levator
scapulae ventralis) are not well understood because both attachments of
the muscle are mobile. AS post in rhesus as in cat (Richmond et
al. 1999a) was found to be composed primarily of fast fibers as
might be expected of a muscle that aids head turning. However, it may
also rotate the scapula cranially (Hartman and Straus
1961
). AS ant has higher proportions of slow fibers than AS
post. A potential postural role may be suggested by the geometry of the
muscle; its laterally directed course from the base of the skull give
it the appearance of a guy wire that could be used to stabilize the
head from falling to one side. Crisco and Panjabi (1990)
have recently discussed the possible advantages of using superficial
muscles as tethers with a long moment arms to maintain stability of a
body part that is configured like an inverted pendulum, such as the neck.
Fiber-type distributions
The skeletal muscles of rhesus monkeys do not appear to differ
from human or cat muscles in the types of extrafusal fibers that they
contain at least when the ATPase reactivity after alkaline pretreatment
is used as the criterion. Further, the general features of the fiber
types were typical of descriptions in other muscles and other species.
For example, slow (type I) fibers were found to be most common in the
centers of muscle fascicles and in the deep or core regions of some
muscles. However, one aspect of fiber-type distribution in rhesus
monkeys did appear to be unusual. Adjacent fiber fascicles often
contained surprisingly different fiber-type proportions and occasional
fascicles of fibers were found to be composed exclusively of type I
fibers in regions of muscle that were otherwise typified by fascicles
containing a mix of fiber types. The explanation for these fascicles is
not clear. The loss of a fiber mosaic in a mixed muscle is most
commonly considered to reflect a previous denervation-reinnervation
process where a single motor unit "takes over" a grouping of motor
units whose axons are lost (Swash and Schwartz 1998).
However, the loss of mosaic is typically seen over a relatively wide
field of fascicles not a single fascicle whose fibers show no other
sign of damage, such as centrally placed nuclei or connective-tissue fibrosis.
Considerations for biomechanical models
The quantitative analysis presented here was motivated in part by
a need for data appropriate to model neck muscles biomechanically. The
CSAs calculated for neck muscles provide some insight into muscle
capabilities. Nevertheless the actions of a muscle can only be
understood fully if we can evaluate its capacity to produce torque
across the joint or set of joints to be moved. Because the lengths and
orientations of the muscle attachments differ from one species to
another, the pulling directions and moment arms of different muscles
relative to different joint-sets may change as well. To gain insight
into these relationships, biomechanical models will be needed to
quantify muscle moments at different joints. Realistic graphical models
of the human neck are now available (Vasavada et al.
1998), and similar models for cats (Statler et al.
1994
) and monkeys (M. Choi and B. Peterson, unpublished data) are being developed using data such as that presented here. When the
biomechanical attributes and identified activity patterns of muscles
(e.g., Corneil et al. 2001
) are eventually combined with
the morphometric information reported here, it will be easier to
compare the muscles and motor control systems in species commonly used
as laboratory proxies for the human head-neck system.
Many of the muscles described here will pose significant modeling
challenges. For example, SCM is a complex muscle whose fiber lengths
and fascicular attachments vary. The complex organization of its
multiple heads ensures that most of its force is directed laterally
onto the mastoid process. Thus it would be inappropriate to model the
muscle as if its line of pull was directed onto the midpoint of the
occipital attachment as might be suspected from simply considering its
width. In TRAP, changing fiber-type proportions and multiple
attachments onto thoracic vertebrae strongly suggest a nonuniform
action in different muscle parts. The cervical part of human TRAP like
monkey TRAP is richer in fast fibers and is more suited to phasic
activities whereas caudal parts are richer in slow fibers and may be
more important for repetitive or postural roles. Thus muscles may have
to be divided into subvolumes for modeling purposes as suggested for
comparable human muscles (Johnson et al. 1996;
Van der Helm and Veebaas 1991
). A combination of morphometry and EMG analysis will be important to guide these decisions.
The results presented here were intended to provide an archival base of data that could be used as a foundation for biomechanical modeling and for electromyographic examinations of monkey neck muscles such as those that follow. In the past, studies of primate muscles have often focused on only a few easily accessible muscles, and this has led to an unrealistic assessment of the "divisions of labor" between different muscle groups. By combining the morphometric and histochemical data with a knowledge of biomechanical features and EMG activities, it may be possible to recognize evolving trends in the reorganization of the head-neck system. This may be important clinically because neck muscles often seem to be vulnerable to damage in ways that may be related to the rapid evolution of musculoskeletal relationships in the vertebral column and shoulder of bipeds.
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ACKNOWLEDGMENTS |
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We thank J. Creasy for excellent technical assistance and E. Cheng and E. Chung for help in collecting portions of the data. We thank E. Au-Yeung, M. Scythes, and S. Wong for excellent illustrations. We also gratefully acknowledge the aid of Dr. D. Van Vugt in obtaining some of the experimental animals.
This work was supported by a group grant from the Medical Research Council (MRC) of Canada. K. Singh was supported by a doctoral award from the MRC. B. D. Corneil was supported by an Ontario Graduate Scholarship and a doctoral award from the MRC.
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FOOTNOTES |
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Present address and address for reprint requests: B. D. Corneil, Div. of Biology, California Institute of Technology, MC 216-76, Pasadena, CA 91125 (E-mail: brian{at}vis.caltech.edu).
Received 14 August 2000; accepted in final form 5 July 2001.
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REFERENCES |
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