JOURNAL OF MORPHOLOGY 239:255–269 (1999)

Morphometry, Histochemistry, and Innervation of Cervical

Shoulder Muscles in the Cat
F.J.R. RICHMOND,* T.A. LIINAMAA, J. KEANE, AND D.B. THOMSON
MRC Group in Sensory-Motor Neuroscience, Department of Physiology,
Queen’s University, Kingston, Ontario, Canada K7L 3N6

ABSTRACT Morphometric and histochemical methods were used to esti-

mate the force-developing capabilities and fiber-type contents of four muscle
complexes (rhomboideus, levator scapulae, trapezius, and sternomastoideus)
that link the shoulder girdle to the skull and cervical vertebrae. Each complex
contained at least two member muscles that were distinctive architecturally
and often had specialized innervation patterns. Trapezius and sternocleido-
mastoideus were innervated by both cranial nerve XI and cervical spinal
nerves. Glycogen depletion of trapezius suggested that the nerves derived
from cervical roots might be entirely sensory. Muscles within each complex
varied in physiological cross-sectional area from less than 0.1 cm2 to greater
than 1 cm2. They showed differences in fiber-type composition that suggested
specialized roles for different behaviors. The morphometric features of the
cervical shoulder muscles suggest that they have considerable potential to
produce head movements and should be incorporated into feline head-
movement models. J. Morphol. 239:255–269, 1999. r 1999 Wiley-Liss, Inc.
KEY WORDS: cervical shoulder muscles; feline head-movement models; morphometry

The rostral half of a cat is often viewed as
if it is composed of two separate parts, an
appendicular forelimb and an axial body con-
sisting of the head, neck, and trunk. Experi-
ments to understand the control of these two
different parts have generally been con-
ducted as separate lines of research, with
little consideration of the dependencies be-
tween them. For example, biomechanical
models to date of the feline head-movement
system usually include the skull and cervi-
cal column but lack a scapula (Pellionisz and
Peterson, ’88; Statler et al., ’94); models of
the forelimb often represent the trunk as a
single unit without a head (Rushmer et al.,
’83; Lacquaniti et al., ’90).
A number of recent observations, however,
have drawn attention to the potential impor-
tance of understanding the physical intercon-
nections that link the head-neck and fore-
limb motor systems as a critical step in
appreciating the biomechanics and control
principles that govern their movements. In-
verse static analyses suggest that the shoul-
der is an important site at which ground-
reaction forces propagated through the
forelimb must be balanced by gravitational
and muscular forces acting on the cantile-
vered head and neck (Runciman and Rich-
mond, ’97). Shoulder muscles appear to
have a central role in this balancing act. The
EMG patterns of at least three large mus-
cles with scapular attachments— rhomboi-
deus, levator scapulae, and trapezius—are
known to be modulated during movements
of the head (Richmond et al., ’94; Thomson et
al., ’96). Further, contractions in these
muscles change not only the forces acting on
the shoulder girdle, but also the position of
the scapula; this affects the moment arms
and lengths of all other muscles with scapu-
lar attachments (Runciman and Richmond,
’97).
We are interested in understanding the
motor contributions of shoulder muscles dur-
ing head and forelimb movements. However,
our ability to study and model shoulder
muscles is limited by our incomplete under-
standing of even the most basic aspects of
their size, histochemistry, and innervation.
To address this need, we have carried out a
Contract grant sponsor: MRC of Canada.
*Correspondence to: Dr. Frances J.R. Richmond, Department
of Physiology, Queen’s University, Kingston, Ontario, Canada
K7L 3N6. E-mail: fjr@biomed.queensu.ca

r 1999 WILEY-LISS, INC.

256 F.J.R. RICHMOND ET AL.
systematic analysis of the morphometry, his-
tochemistry, and innervation of cervical
muscles with scapular attachments. In-
cluded in this group are muscles with bran-
chial origins, including trapezius, sternomas-
toideus, and cleidomastoideus, as well as
muscles with segmentally-derived motor in-
nervation, including rhomboideus, levator
scapulae, and levator scapulae ventralis.
MATERIALS AND METHODS
Cadaveric dissections were carried out to
define the attachments and innervation of
cervical shoulder muscles of six cats (Felis
domesticus) euthanized for other physiologi-
cal studies. Additional experiments were con-
ducted on fourteen cats weighing 2.2–4.5 kg
that were anaesthetized with sodium pento-
barbital (initial dose, 35 mg/kg, supple-
mented as needed i.v. to suppress with-
drawal reflexes). Cats were housed and
tended according to guidelines of the Cana-
dian Council of Animal Care under protocols
approved by the animal ethics review com-
mittee of Queen’s University.
Anatomy and morphometry
The head of the cat was supported in a
stereotaxic frame and the neck was posi-
tioned in a vertical posture typical of alert,
sitting cats (Vidal et al., ’86). In three cats, X
rays were taken of the skull, vertebral col-
umn, and scapula to confirm the positions of
bones to which muscles of interest were at-
tached. The muscles were exposed and the
lengths of muscle fascicles were measured at
several sites across the width of the muscle.
In muscles in which fascicle length changed
progressively across the width or depth of
the muscle, the muscle was modelled as one
or more parallelograms and mean fascicle
length was computed by averaging the
lengths of fascicles on the long and short
sides. The orientation of the fascicles with
respect to the line-of-pull of the muscle was
measured with a protractor. Muscles were
removed and weighed. In three cats, muscles
on the contralateral side were allowed to go
into rigor after death with the neck in a
vertically held posture. Small bundles of rig-
ored muscle fibers were removed from at
least three different parts of the muscle and
mounted in glycerol on glass slides in order
to measure sarcomere lengths (Selbie et al.,
’93). Measurements made at 10–20 locations
throughout each bundle were averaged to
obtain a value that could be used to normal-
ize fascicle lengths to an optimal sarcomere
length of 2.5 µm (Herzog et al., ’92).
The physiological cross-sectional area of
each muscle was calculated by dividing the
mass of the muscle by the product of its
normalized fascicle length and density (as-
sumed to be 1.06 g/cm3; Mendez and Keys,
’60). The physiological cross-sectional area
is normally determined by multiplying the
cross-sectional area by the cosine of the angle
made by fibers with the estimated line-of-
pull of the muscle. For the neck muscles
studied here, attachments to tendons never
introduced a pinnation angle of more than
10° (cos 10° ⫽ 0.98). Because the cosine of
such small angles changes values by less
than 2%, the cross-sectional area was consid-
ered to be equivalent to the physiological
cross-sectional area (Selbie et al., ’93). The
potential tetanic force-developing capability
of each muscle was estimated by multiply-
ing its physiological cross-sectional area by
a previously determined estimate of specific
tension in feline muscle (31 N/cm2; Scott et
al., ’96; Brown et al., ’98).
Glycogen-depletion of nerve territories
Motor territories supplied by different mo-
tor nerves and nerve branches were studied
by stimulating nerve bundles using fine bipo-
lar stimulating electrodes with 0.2 ms pulses.
The distribution of resulting contractions, if
present, was observed and recorded. In seven
cats, one or more branches of the spinal
accessory nerve supplying trapezius were
isolated and sectioned. The nerve distal to
the section was placed on bipolar stimulat-
ing electrodes and coated with low melting
point paraffin wax. Nerves were stimulated
intermittently for 1 hour using 40-Hz trains
of stimuli at 4 X threshold for just-detect-
able contraction, delivered for 330 ms every
second. Immediately following stimulation,
the muscle was removed, divided into blocks
whose orientation was recorded, and frozen
in liquid nitrogen. Sets of 10 or more serial
sections were cut at 15-µm thickness at 1–5
mm intervals throughout the muscle and
stained using the periodic-Schiff procedure
for glycogen (PAS) with or without dimedone
blockade (Bulmer, ’59) and for ATPase activ-
ity. The distribution of depleted territories
was reconstructed from line drawings of
spaced sections onto which were mapped the
extent of territories containing different pro-
portions of blanched fiber profiles.
Fiber-type composition
and end-plate distribution
Muscles were removed immediately after
death and divided into numbered blocks that
 CERVICAL SHOULDER MUSCLES 257

were mounted on cryostat chucks in a re-
corded orientation. Blocks were coated in
talcum powder and frozen in liquid nitrogen.
Ten or more transverse serial sections, 10–
15-µm thick, were cut from well-spaced re-
gions within each muscle. At least six sec-
tions were stained for ATPase activity
following alkaline preincubation (pH 10.4)
(Guth and Samaha, ’70). This method was
found previously to produce reliable differen-
tiation of fast glycolytic (FG), fast oxidative-
glycolytic (FOG), and slow oxidative (SO)
fiber subtypes. In muscles from three
cats, additional sections were stained with
myofibrillar ATPase without preincubation
(Padykula and Herman, ’55) and with an
ATPase method following preincubation at
pH 4.35 (modified from Guth and Samaha,
’70). In the other muscles, remaining sec-
tions were processed to demonstrate NADH-
tetrazolium reductase activity (Dubowitz and
Brooke, ’73). Type FG, FOG, and SO fibers
were identified by their characteristic stain-
ing profiles as documented elsewhere (Rich-
mond and Abrahams, ’75). Fiber-type distri-
bution was determined in each cross-section
by counting the relative numbers of fibers of
different types in three separate sites, each
containing 100–300 fibers. Where regional
variations were present, one sample was
made in the region with highest slow-fiber
content, a second in the region with the
lowest slow-fiber content, and a third in a
region with intermediate proportions.
In two cats, muscles under study were
removed and stained for acetylcholinester-
ase activity using a modification of the tech-
nique described by Karnovsky and Roots
(’64) in which substrate concentration was
increased by a factor of 5–10 X.
RESULTS
Morphometry and innervation
Trapezius
Trapezius is a superficial, dorsal muscle
sheet that is divided into three separate
heads (Fig. 1). The most rostral head,
clavotrapezius, is largest (Table 1). Rostrome-
dially, clavotrapezius attaches along the
lambdoidal crest of the skull. This attach-

Fig. 1. Felis domesticus. Line drawings to show the location and anatomy of different
trapezius heads. The penetration of levator scapulae ventralis (LSV) between clavotrapezius
(CT) and acromiotrapezius (AT) is apparent close to the clavicular attachment of clavotrapezius.
ST, spinotrapezius.
258 F.J.R. RICHMOND ET AL.

ment extends caudally for about 4 cm along
the nuchal midline raphe. The muscle nar-
rows and thickens as it wraps ventrolater-
ally around the neck toward the clavicle.
Here, its fibers attach not only to the clavicle
itself, but also to a tendinous raphe, called
the cleidohumeral ligament, that extends
from the lateral end of the clavicle. The
clavicle and connective tissue raphe sepa-
rate clavotrapezius from the forelimb muscle
clavobrachialis that attaches to its distal
side. Clavotrapezius has the largest and most
variable physiological cross-sectional area of
the three heads, ranging from 0.33–1.1 cm2
(Table 1).
Acromiotrapezius muscles are thinner
sheets that originate from either side of an
aponeurotic saddle over the spines of lower
cervical and upper thoracic vertebrae (Fig.
1). Fiber bundles run laterally for 4–9 cm
and insert along the length of the scapular
spine and metacromion. At the midline, the
rostralmost edge of acromiotrapezius is ap-
posed to clavotrapezius, but it is separated
more distally from clavotrapezius by the pen-
etration of levator scapulae ventralis (Fig. 1).
Spinotrapezius is located most caudally. It
has a wide origin from the spinous processes
of thoracic vertebrae T1 to T10–12, and con-
verges as it runs laterally to insert into the
fascial covering of two deeper scapular
muscles, supraspinatus and infraspinatus,
close to their sites of insertion onto the scapu-
lar spine. The most rostral fiber bundles are
relatively short (4–5 cm) and are oriented
most perpendicularly to the vertebral col-
umn compared to the longer (7–9 cm) caudal
fiber bundles of this triangular muscle. De-
spite their differences in shape, acromiotra-
pezius and spinotrapezius have a similar
physiological cross-sectional area (Table 1).
Each accounts for about 25–30% of the total
physiological cross-sectional area of trape-
zius.
The three heads of trapezius receive a
dual innervation from cranial nerve XI and
from segmental nerves (Fig. 2). The spinal
accessory nerve from cranial nerve IX can be
identified as a large nerve trunk running
caudally from the jugular foramen along the
ventral surface of trapezius. It divides into
several branches along its course as re-
ported briefly by Liinamaa and coworkers
(Liinamaa et al., ’97). Two to three nerve
branches enter the rostral portion of
clavotrapezius close to C2 segmental nerve
branches. An additional one or two nerve
branches enter the caudal portion of the
muscle. Acromiotrapezius receives two or
three small nerve branches and the remain-
ing nerve enters spinotrapezius at its rostral
end. Segmental innervation is supplied by
shorter nerve bundles originating from sev-
eral spinal segments that often merge with
motor branches close to the muscle entry
point. Clavotrapezius is innervated by four
separate nerves supplied by C2 to C5 spinal
roots, which enter the muscle as a rostrocau-
dally spaced array (Fig. 2B). Acromiotrape-
zius appears to be innervated by a single

TABLE 1. Morphometric parameters used to estimate muscle force developing capacity

Mean Fascicle length (cm) Mass (g) PCSA (cm2 )
sarcomere
Short length Mean Estimated
form n (µm) Mean corrected Range Mean Range Mean Range Fo (N)
Sternomastoi-
deus SM 5 3.0
Lateral 10.8 8.7 10–12 2.1 1.1–3.3 0.22 0.12–0.33 6.82
Medial 8.1 6.5 7.5–9 1.2 0.6–2.0 0.16 0.07–0.26 4.96
Cleidomastoi-
deus CM 6 3.0 10.8 9.6 10–11 1.9 1.3–2.8 0.24 0.13–0.32 7.44
Clavotrapezius CT 7 2.7 10.1 9.7 10–12 6.4 4.5–10 0.65 0.33–1.1 20.15
Acromiotrape-
zius AT 3 2.5 6.2 6.2 4–9.5 3.4 2.5–4.4 0.56 0.41–0.71 17.36
Spinotrapezius ST 3 2.3 6.5 7.1 4–9 4.0 2.6–4.8 0.52 0.34–0.65 16.12
Rhomboideus
capitis RHcap 6 2.4 10.1 10.5 9–11 0.9 0.7–1.0 0.08 0.07–0.09 2.48
Rhomboideus
minor RHmin 3 2.3 5.5 6.0 4.5–7 4.9 4.7–5.1 0.76 0.69–0.82 23.56
Rhomboideus
major RHmaj 3 2.6 5.7 5.5 5–6.5 1.8 1.3–2.2 0.32 0.19–0.38 9.92
Levator scapulae LS 4 2.5 6.9 6.9 5.5–8 8.9 8.2–10.3 1.20 1.1–1.3 37.2
Levator scapulae
ventralis LSV 5 2.6 9.9 9.5 9–10 2.0 1.3–3.0 0.20 0.13–0.27 6.2
 CERVICAL SHOULDER MUSCLES
Fig. 2. Felis domesticus. Photomicrographs and inter-
pretive line drawings to show the dual innervation of
trapezius. A: Course of the spinal accessory nerve (SAN)
is shown and illustrated on the ventral surface of
clavotrapezius (CT) and acromiotrapezius (AT). B: Boxed
segmental nerve from the C5 spinal root
that has its entry point rostrally in the
muscle. Spinotrapezius is innervated by at
least three segmental nerves from T2, T3,
and T4 spinal roots that enter the rostral
third of the muscle as a spaced array. Nerve
branches from T5 and T6 spinal roots also
penetrate the muscle more caudally but it is
difficult from visual inspection to determine
whether a component of these nerves sup-
plies spinotrapezius or whether the nerve
bundles pass through the muscle without
innervating it.
Repetitive electrical stimuli delivered to
the centrally sectioned spinal accessory
nerve always evoked powerful contractions
in trapezius. As might be expected from their
attachments, clavotrapezius was seen to
259
area in A at higher power. In this view, levator scapulae
ventralis (LSV) has been retracted to show the complex
nerve bundles from cervical segments (marked by aster-
isks and shown in black on accompanying line drawing).
draw the proximal limb and shoulder dorso-
cranially as it rotated the head laterally and
ventrally towards the shoulder. Acromiotra-
pezius drew the scapula toward the midline,
and spinotrapezius rotated the vertebral bor-
der of the scapula in a dorsocaudal direction.
In contrast, electrical stimulation of each
segmental nerve branch produced what ap-
peared to be reflexive contractions. These
contractions were localized and inconsis-
tent. They were only elicited if segmental
and spinal accessory nerve branches were
intact.
Further evidence that motor innervation
was provided chiefly, if not exclusively, by
the spinal accessory nerve was obtained by
using glycogen depletion methods. Intermit-
tent tetanic stimulation of the spinal acces-
260 F.J.R. RICHMOND ET AL.

sory nerve appeared to deplete extrafusal
fibers throughout the muscle heads when
their glycogen levels were compared to un-
stimulated contralateral muscle. Over 85%
of extrafusal fibers in all muscles appeared
blanched. The remaining fibers were light
pink in color (Fig. 3) and were found to have
the histochemical profile of type SO fibers in
adjacent ATPase stained sections.
Sternomastoideus and cleidomastoideus
The ventral muscle sternomastoideus can
be subdivided for descriptive purposes into a
medial part, taking origin from the ventral
midline, and a conjoined lateral part, origi-
nating from the sternum (Fig. 4). The medial
part is fan shaped, with progressively length-
ening fascicles from its medial to lateral
edge. The fascicles all converge onto an apo-
neurosis inserting on the mastoid process.
Fascicles composing the lateral head are
longer (Table 1), running from sternum to
lambdoidal crest. The medial part of sterno-
mastoideus usually has a smaller physiologi-
cal cross-sectional area than the lateral part
(0.16 vs. 0.22 cm2).
Cleidomastoideus originates from the
clavicle and the cleidohumeral ligament deep
to clavotrapezius, and runs alongside the
lateral aspect of sternomastoideus to attach
onto the mastoid process deep to sternomas-
toideus. Its physiological cross-sectional area
is about half of that of sternomastoideus
(Table 1). Both cleidomastoideus and sterno-
mastoideus receive their motor supply from
the spinal accessory nerve, and their sen-
sory supply from C1 and C2 spinal segments
(Liinamaa et al., ’97).
Rhomboideus
Rhomboideus in the cat has commonly
been considered as a single muscle but can
be subdivided for purposes of analysis into
two parts that are homologous to rhomboi-
deus minor or cervicis and rhomboideus ma-
jor or dorsi in other species (Craigie, ’60;
Reighard et al., ’61; Greene, ’68). In addi-
tion, rhomboideus has a third head, usually
called occipitoscapularis in feline descrip-
tions, that is homologous to rhomboideus
capitis in primates (Hartman and Straus,
’61). Occipitoscapularis is a delicate strap
with a physiological cross-sectional area of
less than 0.1 cm2 that runs for 10 cm or more
between the coracovertebral border of the
scapula and the lamboidal crest (Fig. 5).

Fig. 3. Felis domesticus. Differences in glycogen staining in trapezius following stimulation

of the spinal accessory nerve. The arrows mark the edge of the muscle, which apposes adjacent
unstimulated muscle whose fibers stain more intensely. Scale bar ⫽ 100 µm.
 CERVICAL SHOULDER MUSCLES
Fig. 4. Felis domesticus. Structure and relationships
of the two heads of sternocleidomastoideus. The sterno-
mastoid head (SM) has two regions, sternomastoid me-
dial (SM med), attaching to the ventral midline and
sternomastoid lateral (SM lat), attaching to the ster-
num. It lies medial to the cleidomastoid head (CM).
Rhomboideus minor is a much larger muscle
that attaches along the vertebral border of
the scapula between the glenovertebral angle
and a point about 1 cm rostral to the verte-
bral spine. It fans to insert along the nuchal
raphe from the level of C2 to T2 vertebrae.
Its rostral fiber bundles angle more rostro-
caudally and are relatively long (6–9 cm)
compared with the caudal bundles (4.5–5
cm) that run nearly perpendicular to the
vertebral column. Rhomboideus minor ap-
pears contiguous with rhomboideus major,
but a dividing line between the two muscles
can be usually discerned near the scapular
site of attachment. Rhomboideus major is
widest at its vertebral origins from upper
thoracic spinous processes. It narrows and
twists as it wraps over the vertebral border
261
of the scapula to insert on its superficial
surface near the glenovertebral angle. In
contradiction to its name, adopted from con-
ventions in man, rhomboideus major is much
smaller than rhomboideus minor (about 2
vs. 5 g) and has less than half the physiologi-
cal cross-sectional area (Table 1). As has
been noted previously (Liinamaa et al., ’97),
the muscle heads are innervated by several
nerve bundles from different segments.
Stimulation of these nerves resulted in re-
gional contractions of strip-like, in-parallel
subvolumes running from the muscle origin
to insertion.
Levator scapulae and levator
scapulae ventralis
Levator scapulae is a thick sheet that runs
deep to rhomboideus minor from the medial
aspect of the vertebral border of the scapula
to the transverse processes on cervical verte-
brae caudal to C2. Thus its fibers run
obliquely with respect to the long axis of the
vertebral column (Fig. 5). At its caudal bor-
der, levator scapulae can be difficult to distin-
guish from serratus anterior to which it is
joined. The line of division between these
two muscles was considered to be marked by
the presence of a blood vessel that pen-
etrated between the muscles at the level of
vertebra T1. Levator scapulae was the only
muscle of the present study whose values of
physiological cross-sectional area were con-
sistently larger than 1 cm2, even in the small-
est cats (Table 1). Its rostral fiber bundles
were 20–30% longer than the caudal bundles
and they were angled more acutely toward
the head.
Levator scapulae ventralis is a narrow
strap that runs rostrally for 9–10 cm from
the ventral border of the metacromion and
the adjacent scapular fossa to the skull and
atlas (Fig. 1). The primary attachment of the
muscle is onto the caudal border of the lat-
eral process of C1, but some fibers also in-
sert onto the tendon of longus capitis, which
ultimately attaches to the basiocciput of the
skull (Reighard et al., ’61).
Fiber histochemistry
All shoulder muscles contained three sub-
types of histochemically differentiable fibers
with FG, FOG, and SO profiles (Table 2).
Fibers of all three types had a wide range of
diameters from over 50 µm to less than 10
µm (Fig. 3).
262 F.J.R. RICHMOND ET AL.

Fig. 5. Felis domesticus. Line drawings to illustrate the anatomy and relationships of
rhomboideus [occipitoscapularis (OS), rhomboideus minor (RHMIN), rhomboideus major
(RHMAJ)] and levator scapulae (LS).

Trapezius Slow fiber proportions were higher in the

Fiber-type proportions were dissimilar in more caudal heads of trapezius. Acromiotra-
the three heads of trapezius. Clavotrapezius pezius contained about 25–40% SO fibers,
was composed predominantly of fast fiber and spinotrapezius usually had more than
subtypes (Table 2); typically only about 10– 40% SO fibers (Table 2).
15% of fibers had type SO profiles. The pre- Sternomastoideus and cleidomastoideus
dominance of type FG and FOG fibers was
particularly apparent on the superficial Sternomastoideus and cleidomastoideus
muscle surface where some fiber fascicles had the lowest proportions of slow fibers of
were devoid of SO fibers. The proportion of the muscles studied (Table 2). Typically ster-
SO fibers increased toward the core and nomastoideus contained less than 10% SO
ventral surface of the muscle. fibers and cleidomastoideus had about 15%
type SO fibers. However, sternomastoideus
also had a relatively high content of FOG
TABLE 2. Fiber-type distributions fibers, usually between 25–35%. Thus, its
in cervical shoulder muscles1 content of FG fibers was similar to or lower
Muscle n %FG %FOG %SO than that typically found in clavotrapezius.
In sternomastoideus, SO fibers were concen-
Rhomboideus trated in core regions of the muscle and in
minor
Rostral cleidomastoideus, they were richest in the
-core 4 31 (23–45) 15 (6–19) 55 (48–59) deep half. In both muscles, SO fibers were
-deep 4 53 (45–59) 16 (6–25) 32 (17–48) rare or absent on the superficial surface of
Middle 4 47 (39–58) 19 (3–31) 34 (30–41) the muscle.
Caudal 5 62 (52–71) 22 (15–30) 15 (14–18)
Rhomboideus Rhomboideus
major 3 72 (63–78) 17 (13–21) 11 (5–16)
Levator scapulae 5 62 (54–66) 19 (13–26) 18 (17–21) Rhomboideus had a markedly non-uni-
Levator scapulae form distribution of fiber types (Table 2, Fig.
ventralis 3 50 (46–59) 23 (16–28) 26 (24–28)
Clavotrapezius 4 62 (57–64) 22 (15–26) 16 (13–21) 6). The rostralmost part of rhomboideus mi-
Acromiotrapezius 3 39 (36–42) 26 (24–29) 35 (29–39) nor, like occipitoscapularis described previ-
Spinotrapezius 3 21 (18–23) 32 (23–40) 47 (42–54) ously (Richmond and Abrahams, ’75), was
Sternomastoideus 3 61 (56–65) 30 (27–34) 9 (8–10) composed primarily of type SO fibers. The
Cleidomastoideus 3 55 (53–56) 27 (21–31) 15 (14–16)
deep muscle layer in rhomboideus minor
1n, number of cats from which data are reported; FG, fast-
typically contained fewer SO fibers than the
glycolytic fibers; FOG, fast-oxidative-glycolytic fibers; SO, slow-
oxidative fibers. Mean percentages of type FG, FOG, and SO superficial surface. In most muscles, concen-
fibers are accompanied by ranges in parentheses. trations of 30–40% were typical in deeper
 CERVICAL SHOULDER MUSCLES
Fig. 6. Felis domesticus. Non-uniform distribution of
fiber types in rhomboideus. The line drawing (top) sche-
matizes the greater concentration of type SO fibers in
regions, but in one muscle the deep rim
contained less than 10% SO fibers. More
caudal parts of the muscle showed progres-
sively decreasing SO fiber proportions, so
that the most caudal part of rhomboideus
minor generally contained less than 30%
type SO fibers. Rhomboideus major had even
lower SO fiber proportions, from 3–15% in
different specimens (Fig. 6). Instead, type
FG fibers predominated.
Levator scapulae and levator
scapulae ventralis
Levator scapulae had a relatively uniform
distribution of fiber types. FG fibers predomi-
nated, accounting for 45–65% of fibers (Table
2). Proportions of SO fibers were usually
between 15–25%. Levator scapulae ventra-
lis was also relatively rich in fast fibers. SO
fibers were concentrated in the muscle core,
where they accounted for 30–40% of fibers,
and were lowest on the outer rim of the mus-
cle, where they accounted for 15–30% of fibers.
Distribution of end-plate bands
All of the shoulder muscles stained suc-
cessfully for acetylcholinesterase activity
263
rostral parts of rhomboideus minor. Photomicrographs
of typical cross-sections from different regions are shown
(bottom). Scale bar ⫽ 100 µm.
were crossed by multiple end-plate bands.
The bands were discontinuous across the
width of the muscle, so that each band was
relatively short and spaced at a variable
distance of about 0.3–1.2 cm with respect to
nearby bands (Fig. 7). The muscles, how-
ever, shrank to nearly half of their length as
a result of histological treatment. Thus, we
estimate that bands are spaced by an aver-
age distance of about 1 cm in untreated
muscles.
DISCUSSION
The shoulder girdle is linked to the head
and cervical vertebral column by two major
muscle systems. One system, comprised of
trapezius and sternomastoideus-cleidomas-
toideus muscles, is thought to be of bran-
chial origin (but see McKenzie, ’55, ’62),
whereas the other is somatic. Present work
suggests that each of these systems has a
substantial force-generating capability that
could have important effects on head and
shoulder movement. However, the heteroge-
neous distributions of fiber types among the
different muscles and individual muscle
heads suggest that the muscles play special-
264 F.J.R. RICHMOND ET AL.
Fig. 7. Felis domesticus. Multiple end-plate banding in rhomboideus. Note the staggered
appearance of bands crossing different blocks of fascicles (marked by arrows). Scale bar ⫽ 1 cm.
ized functional roles ranging from the main-
tenance of tonic posture to the production of
rapid ballistic movements. These character-
istics must be kept in mind when attempting
to model or understand the motor roles of
individual shoulder muscles. Such model-
ling will also require determination of the
moment arms of each muscle with respect to
each axis of motion and each joint crossed.
These values could change greatly with over-
all posture.
Muscles supplied by the spinal
accessory nerve
The muscles of the spinal accessory com-
plex are unusual because of their dual nerve
supply. Research has been undertaken for
nearly a century to understand whether the
motor innervation to the muscles is supplied
only by the spinal accessory nerve or whether
motor axons derive also from the ventral
roots of cervical spinal segments (see Straus
and Howell, ’36; Corbin and Harrison, ’39 for
historical review). Surprisingly, these stud-
ies have not yet produced a firm consensus.
Most researchers appear to favor the view
that the sensory and motor supply are sepa-
rated (Corbin and Harrison, ’39; Anderson
and Flowers, ’69; Green and Brien, ’85;
Krammer et al., ’87), but others have been
less convinced (e.g., Straus and Howell, ’36;
McKenzie, ’55; Short et al., ’84; Soo et al.,
’93; Clavenzani et al., ’94; Nori et al., ’97).
In the cat, Corbin and Harrison (’39) re-
ported that no muscle contractions could be
elicited by stimulating the distal stumps of
segmental nerves C3–5. These findings are
consistent with present observations that
essentially all muscle fibers in trapezius
showed evidence of glycogen depletion follow-
ing exhaustive stimulation of the spinal ac-
cessory nerve. The only fibers that appeared
to retain some level of glycogen were type
SO fibers. However, it is well known that
type SO fibers have a high oxidative capac-
ity that makes them relatively immune to
glycogen depletion (Burke and Tsairis, ’73;
Toop et al., ’82). Thus we might expect that
the SO fibers of stimulated motor units would
continue to show some level of coloration. It
seems likely that there is no extrafusal inner-
vation from segmental nerves, but an intra-
fusal role cannot be excluded.
In contrast, the small, localized contrac-
tions that were sometimes seen in trapezius
following stimulation of intact cervical nerve
 CERVICAL SHOULDER MUSCLES
branches were found to be abolished by nerve
section central to the stimulating electrodes
and were likely to be the result of reflex
activation. Similar localized contractions in
other neck muscles have been reported pre-
viously and have been called cervicocollic
reflexes (Bilotto et al., ’82; Ezure et al., ’83).
The pathways responsible for the reflexes
are still not well understood. In muscles of
the limb, such reflexes are often assumed to
arise from monosynaptic pathways between
spindle primary endings and motoneurons.
However, it has proven difficult to demon-
strate robust monosynaptic reflexes in neck
muscles (Abrahams et al., ’75; Anderson, ’77;
Rose and Keirstead, ’88; Richmond and Loeb,
’92). Thus cervico-collic reflexes may be pro-
duced, at least in part, by longer-loop path-
ways (Peterson et al., ’92). Whether neck
muscles with branchial origins will prove to
share similar reflex characteristics with so-
matic neck muscles remains to be explored.
The presence of muscle reflexes may ex-
plain some of the contradictory findings, par-
ticularly in the human literature, regarding
a potential motor role for segmental nerve
branches (e.g., Soo et al., ’93; Nori et al., ’97).
In human subjects, it is obviously not accept-
able ethically to section muscle nerves and
thus discriminate between a direct or reflex
origin of the contractions observed when cer-
vical nerve branches are stimulated intraop-
eratively (e.g., Nori et al., ’97). However, the
extensive paralysis of trapezius that follows
spinal accessory nerve palsy argues against
the presence of any substantial segmental
motor supply (e.g., Roy and Beahrs, ’69; Big-
liani et al., ’96). If segmental motor axons
were available, they would not only provide
some degree of motor function immediately
after damage to the cranial nerve supply,
but also might sprout to innervate adjacent
denervated muscle fibers and thus improve
muscle function within a few weeks after the
insult.
Histochemical analysis of muscles served
by the spinal accessory nerve showed that
all were relatively rich in fast fibers com-
pared to most previously studied neck
muscles (e.g., Richmond and Abrahams, ’75;
Richmond and Vidal, ’88). The predomi-
nance of FG fibers is an attribute shared
with homologous rodent muscles (Brichta et
al., ’87). It is significant functionally because
FG fibers are generally thought to be re-
cruited only for short-lived but powerful con-
tractions during motor tasks requiring a
265
strong burst of force (e.g., Burke, ’81). The
paucity of SO fibers suggests that feline
clavotrapezius, sternomastoideus, and clei-
domastoideus are poorly equipped for tonic
postural activities. This conclusion is consis-
tent with the results of EMG studies show-
ing that clavotrapezius and sternomastoi-
deus are not active when cats sit quietly or
move their heads slowly, but were found to
be activated vigorously during rapid, force-
ful movements such as head shaking or aver-
sive maneuvers (Richmond et al., ’92). These
rapid forceful contractions are likely to be
essential for certain behaviors that are cen-
tral to the animal’s survival in the wild, such
as fighting and killing prey. In bipedal spe-
cies, such as monkeys and humans, these
whip-like head movements tend to be lost
from the behavioral repertoire. Perhaps to
support different roles, the attachments of
the brachiomeric muscles are reorganized in
primates. The clavicular component of trape-
zius is much smaller, and the muscles con-
tain higher proportions of slow fibers (Lind-
man et al., ’91; Kamibayashi and Richmond,
’98). This is reflected in a change in usage
patterns. Sternomastoideus is active during
a broader range of head turning movements
(Winters and Peles, ’90; Mazzini and Schiep-
pati, ’92) and rostral trapezius is used also
for relatively slow, undemanding shoulder
movements (Bull et al., ’84; Eliot, ’96).
The fact that the large neck muscles,
clavotrapezius, sternomastoideus, and clei-
domastoideus, appear to be composed pri-
marily of fast, seldom-used fibers poses an
interesting problem for those who wish to
model the neck using conventional optimiza-
tion techniques. In most animal or human
models so far developed, the potential of a
muscle to produce or influence a particular
movement has been inferred from a knowl-
edge of its force-generating capabilities (esti-
mated from physiological cross-sectional
area, moment arm, and pulling direction)
without consideration of fiber-type composi-
tion (e.g., Winters, ’88; Pellionisz and Peter-
son, ’88; Winters and Peles, ’90; Keshner et
al., ’97; Vasavada et al., ’98). Because cla-
votrapezius and sternomastoideus-cleido-
mastoideus have large physiological cross-
sectional areas and large moment arms with
respect to vertebral joints, large muscles
might be assigned roles in the maintenance
of posture or the production of small, slow
movements for which they are poorly suited.
266 F.J.R. RICHMOND ET AL.
The more caudal heads of trapezius, acro-
miotrapezius, and spinotrapezius, were
found to have higher proportions of SO fi-
bers, typical for muscles that are recruited
more frequently during activities of daily
living. Because the muscle heads attach more
caudally, they are unlikely to participate
directly in head movement but are probably
more important for controlling the position
of the scapula during locomotor activities.
This prediction is consistent with results of
EMG recordings made from shoulder
muscles of instrumented cats. Acromiotrape-
zius was found to be active nearly continu-
ously during locomotion, whereas spinotra-
pezius was active when the limb was at the
extremes of flexion and extension (English,
’78). Spinotrapezius is particularly rich in
type SO fibers and may also play a signifi-
cant postural role. For example, it may help
to stabilize the scapula by opposing the
ground reaction forces from the forelimb that
tend to rotate the vertebral border of the
scapula caudoventrally when cats hold sit-
ting or standing postures (Runciman and
Richmond, ’97). However, EMG studies will
be needed to test this prediction.
Rhomboideus and levator scapulae muscles
The rhomboideus and levator scapulae
muscles are among the largest muscles to
attach onto the cervical vertebral column in
the cat (see Richmond and Vidal, ’88, for
comparisons). Surprisingly, however, only the
smallest head, occipitoscapularis or rhomboi-
deus capitis, which has an attachment to the
skull, appears to have been studied in detail
using EMG methods (Richmond et al., ’92;
Keshner et al., ’97). Rhomboideus capitis
has been shown to be active during quiet
sitting and standing and is modulated dur-
ing flexion and extension of the head and
neck. Its postural role is reflected in its
wealth of type SO fibers (Richmond and
Abrahams, ’75) that presumably permit the
head to be held extended for long periods
without fatigue.
A similar postural role is probably played
by the rostral part of rhomboideus minor at
least, although specific actions may vary
along the muscle width. Rhomboideus minor
is supplied by several muscle nerves that
compartmentalize its motor units into sepa-
rate strip-like territories (Liinamaa et al.,
’97). In present studies, rostral parts of the
muscle were found to be richest in SO fibers.
This muscle part would seem particularly
well suited to hold the heavy neck tonically
in a vertical orientation, because it has a
better moment arm across the lower cervical
joints. In contrast, more caudal parts of
rhomboideus minor were found to be rela-
tively fast. The functional role of caudal
rhomboideus minor has not yet been studied
specifically by EMG analysis, but fiber-type
distributions and attachments are consis-
tent with a role in scapular movement dur-
ing locomotion.
Rhomboideus capitis, rhomboideus minor,
and rhomboideus major in cats differ from
their homologues in bipeds, and these differ-
ences must be borne in mind before using
cats as models for the study of head move-
ments with the expectation of generalizing
results to human subjects. In monkeys, the
rostral heads of the rhomboideus are rela-
tively small and rhomboideus major is, in-
deed, the major head of the rhomboideus
family (Berringer et al., ’74). In human sub-
jects, these trends are even more apparent.
Rhomboideus major is much larger than
rhomboideus minor, and, rhomboideus capi-
tis is usually absent (Johnson et al., ’96;
Kamibayashi and Richmond, ’98). The
changes in size may be part of the adapta-
tion of shoulder muscles to an upright pos-
ture of the trunk, which frees the forelimbs
for object manipulation rather than locomo-
tion (Tobias, ’92). Accordingly, muscle forces
to hold the neck in an erect posture appear
to be less important, because the weight of
the skull is borne largely as a compressive
force on the vertebral column. Further, the
scapula has rotated to a frontal rather than
parasagittal orientation (Hogfors et al., ’95).
Levator scapulae and levator scapulae ven-
tralis have a more lateral placement and
orientation than rhomboideus, and are char-
acterized by a higher fast-fiber content.
These findings are consistent with EMG evi-
dence that the muscles have more phasic
patterns of activation associated with head
turning but not with the maintenance of an
upright, midsagittal posture (Thomson et
al., ’96). The feline levator scapulae has con-
siderable force-developing capability, com-
pared to other neck muscles implicated in
head turning. For example, the physiologi-
cal cross-sectional area of levator scapulae
(1.1–1.3 cm2) reported here is nearly twice
that of splenius (0.78 cm2; Richmond and
Vidal, ’88), a muscle that is often considered
as a particularly important muscle for head
turning. The role of levator scapulae in cats
is different from that in man. In man, leva-
 CERVICAL SHOULDER MUSCLES
tor scapulae appears to be relatively inac-
tive during head movement, but is recruited
readily during arm movements (e.g., Eliot,
’96; Ludewig et al., ’96; Mayoux-Benhamou
et al., ’97).
Fiber architecture in neck muscles
The neck muscles studied here all spanned
a relatively long distance between origin
and insertion. Histochemical demonstra-
tions of multiple end-plate bands and pres-
ence of small fiber diameters in many histo-
logical sections (e.g., Fig. 6) were viewed as
evidence that the long muscles were com-
posed of relatively short fibers arranged in
overlapping ‘‘in-series’’ arrays. Such arrange-
ments have been described quite commonly
in other mammalian and avian species (for
review see Gaunt and Gans, ’92; Trotter et
al., ’95). In muscles like clavotrapezius, a
specialized pattern of innervation also ap-
pears to be present in which different nerve
branches supply fibers at different rostrocau-
dal levels (Liinamaa et al., ’97) and produce
contractions in the fascicles localized to the
site of muscle entry (as described previously
in other feline neck and hindlimb muscles;
Richmond et al., ’85; Loeb et al., ’87; Rich-
mond and Armstrong, ’88). Whether this non-
uniform innervation poses problems for bal-
ancing force development along the length of
the muscle has been discussed elsewhere
(e.g., Heron and Richmond, ’93; Trotter et
al., ’95). It may predispose some muscles to
internal tearing during strong, eccentric con-
tractions if forces are distributed non-uni-
formly. In humans, long neck muscles such
as sternomastoideus are known to be vulner-
able to damage during eccentric muscle con-
tractions, such as may occur during whip-
lash injuries (MacNab, ’64). However, much
work remains to determine whether this
type of damage is more likely to occur be-
cause of the series-fibered architecture.
Implications for neck-muscle models
In the past, musculoskeletal models of the
head and neck have usually failed to incorpo-
rate the cervical shoulder muscles. This deci-
sion to exclude some muscles might have
been taken in part because the quantitative
data-set describing the shoulder muscles has
been so incomplete. However, the simplifica-
tion of such models may have also resulted
from the belief that muscles with attach-
ments to the shoulder girdle are not impor-
tant for head movements. Such views are
267
likely to oversimplify the motor problem and
restrict the strategies for motor control. Re-
cent biomechanical studies of force transmis-
sion between the forelimb, shoulder girdle,
and trunk suggest that stabilization of the
scapula is likely to depend on a dynamic
balance between the gravitational loading
on the head-neck complex, and ground-
reaction torques from the forelimb (Runci-
man and Richmond, ’97). A role for cervical
shoulder muscles as dynamic tethers or force-
transmitting elements in this system must
be explored if the biomechanics of the fore-
quarters, neck, and head are to be described
realistically.
ACKNOWLEDGMENTS
We thank O. Morris, D. Reesor, Su Lin
Lim, and Janet Creasy for excellent techni-
cal assistance.
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