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Shoulder region of the ratAnatomy and fiber composition of some suprascapular nerve branches.

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THE ANATOMICAL RECORD 239:332-342 (1994)
Sho ilder Region of the Rat: Anatomy and Fiber Composition of
-
Some Suprascapular Nerve Branches
R. NORLIN, C. HOE-HANSEN, G. OQUIST, AND C. HILDEBRAND
Departments of Orthopedic Surgery (R.N., C.H.-H.) and Cell Biology (G.O., C.H.), Faculty
of Health Sciences, University of Linkoping, Linkoping, Sweden
ABSTRACT
Background: The pathophysiology of chronic supraspinatus tendinitis is not fully understood. This may be due to the scarcity of
experimental studies on this issue.
Methods: In search for a system suitable for experimental analysis, the
present study describes the relevant gross anatomy of the rat shoulder
region (dissection), and examines the fiber composition of relevant suprascapular nerve branches (electron microscopy, selective denervations).
Results: The rat shoulder region is similar to the human shoulder in terms
of gross anatomy. The average suprascapular nerve (SSC) is derived
mainly from the spinal cord segment C5 and contains 3,435 axons, 74% of
which are unmyelinated. The supraspinatus branch (SSP)contains 627 fibers. Of the SSP fibers, 52% are myelinated, including 32% motor and 20%
sensory axons. Of the C-fibersin the SSP 16%are sympathetic efferents and
32% are sensory. Many of the latter disappear after neonatal capsaicin
treatment. The SSC emits a subacromial articular branch (ART),with some
260 axons, about 90% of which are unmyelinated. The myelinated ART fibers are sensory, and of the unmyelinated ones about 24% are sympathetic
efferents and 66% are afferents. The latter resist neonatal capsaicin treatment.
Conclusions: In view of the anatomy of the supraspinatus muscle, of the
subacromial space, and of relevant nerves, the rat shoulder should be appropriate for experimental studies on inflammatory conditions in the subaCrOmia1 space. 0 1994 Wiley-Liss, Inc.
Key words: Rat, Shoulder region, Gross anatomy, Subacromial space,
Supraspinatus muscle, Suprascapular nerve, Fiber composition, Electron microscopy
Many patients in primary health care, occupational
medicine, rheumatology, and orthopedic surgery suffer
from disorders of the shoulder region (Petersson, 1986;
Moren Hybinette, 1987; McCormack et al., 1990; Dimberg, 1991). Traumatic andlor degenerative changes in
the rotator cuff are common causes of pain and chronic
disability in this area. The supraspinatus muscle tendon and the associated subacromial bursa (Birnbaum
and Lierse, 1992) may be affected by chronic inflammatory conditions, which sometimes end up in tendon
rupture. It has been suggested that impingement of the
rotator cuff beneath the bony acromion and the coracoacromial ligament is a n important causative factor in
this respect (Neer, 1972; Watson, 1989; Dines e t al.,
1990; Birnbaum and Lierse, 1992). Accordingly, observations at dissection, during surgery, and by radiography show that the supraspinatus tendon can be impinged when the arm is abducted, and surgical
measures against impingement, i.e., anterior acromioplasty, relieve the pain (Neer, 1972). The development
of increasingly more sophisticated surgical techniques
has improved the results of active treatment of this
0 1994 WILEY-LISS, INC
type of disorder (Ellman, 1987; Gartsman et al., 1988;
Norlin, 1989), but our understanding of the basic
pathophysiological mechanisms remains very incomplete. This may be due to the fact that few experimental studies deal with this issue. Several studies suggest
that neural elements may be involved in the development and maintenance of inflammatory conditions in a
variety of tissues (see Discussion). It seems possible
that the emergence of chronic inflammatory conditions
in the shoulder might involve more complex mechanisms than the mechanical models discussed so far. In
the present paper we examine the rat shoulder region,
with emphasis on the supraspinatus muscle and the
subacromial space and on the course and fiber composition of some relevant suprascapular nerve branches.
The main purpose is to see if the rat shoulder may be
Received November 30, 1993; accepted February 17, 1994.
Address reprint requests to Claes Hildebrand, Department of Cell
Biology, Faculty of Health Sciences, University of Linkoping, 581 85
Linkoping, Sweden.
RAT SHOULDER REGION
a n appropriate system for experimental studies on the
pathophysiology of chronic supraspinatus tendinitis.
MATERIAL AND METHODS
Dissection
Rats to be used for dissection (Sprague-Dawley,
n = 5) were anesthetized with chloral hydrate (30 mgl
100 g b.w., ip), and exsanguinated. Dissection was performed under a n operation microscope. A binocular dissection microscope with a Nikon F-300 camera
containing Kodak Tri-X film was used for photography.
333
fixed during 2 hours in the perfusate, and rinsed in
buffer. Segments and ganglia were immersed overnight in Millonig’s buffer with 30% sucrose, and serially sectioned at 60 pm in a freezing microtome. The
sections were mounted on slides and processed according to the TMB method for HRP visualization (Mesulam, 1982).
Capsaicin treatment
Five rat pups were anesthetized by hypothermia and
injected under the dorsal skin with a solution of capsaicin (1g capsaicin [analytical grade, KEBO, Sweden]
Radiography
in a mixture of 10 ml Triton X-100,lO ml ethanol, and
One rat was killed a s described above, and subjected 80 ml saline) on postnatal days 2, 3 (50 mg/kg, b.w.),
to radiographic examination. Standard radiographs, and 4 (100 mg/kg, b.w.1. Three control rats received
including anteroposterior, lateral, and outlet views vehicle only (Jancso et al., 1985; Fried et al., 1988).
(special Y view) were taken, using a Siemens Orbix These rats were perfused after a survival time of 3
apparatus supplied with Kodak mammography OM 1 months. Nerve specimens were collected and processed
film.
for electron microscopy, as described above. Fiber
counts were made on sections from SSP and ART specElectron Microscopy
imens. In order to check that treatment had been effective, the dorsal roots L5 were collected from 3 capNormal material
saicin-treated and 3 vehicle-injected animals. The
Adult male and female Sprague-Dawley rats ( n = 5 , average occurrence of C-fibers in the surroundings of a t
300-500 g) were anesthetized with chloral hydrate and least 500 myelinated fibers was determined in each of
perfused with Tyrode’s solution, followed by 5% glutar- the six cases. The analysis showed the presence of
aldehyde in a 300 mOsm Millonig buffer with 0.1M 71.8% C-fibers in vehicle-injected cases and 26.1% in
sucrose. After perfusion, suprascapular nerve speci- capsaicin-treated cases. Hence, the treatment worked
mens were removed, postfixed in glutaraldehyde, well.
rinsed in buffer, osmicated (2% OsO, in phosphate
buffer), dehydrated in acetone, and embedded in Vesto- Deeff erentation
pal W. Thin transverse sections from the suprascapular
The proportion of myelinated sensory and motor finerve trunk (SSC), from the supraspinatus branch
(SSP), and from a small subacromiaUarticular branch bers in the SSP and ART was determined through se(ART) were collected on one hole formvar-coated copper lective ventral rhizotomies in 3 adult rats anesthetized
grids. After contrasting, the sections were examined in with chloral hydrate. After a cervical hemilamineca JEOL JEM 1200 EX electron microscope. Montages tomy, the ventral roots C4-C6 on the right side were
of electron micrographs ( x 1,500) completely covering divided. Ten days later the animals were perfused, and
each cross-cut nerve specimen, were prepared and used the deefferented right suprascapular nerve and the
for myelinated axon countings. In order to determine normal contralateral nerve were collected and prethe number of C-fibers the sections were reexamined in pared for electron microscopy. The segmental levels afthe electron microscope ( x 10,000), using the montages fected by the rhizotomy were verified through dissecfor orientation. I n each of five nerves of each type, the tion. Analyses of the number and size distribution of
cross-sectional areas of all myelinated fibers present intact myelinated fibers were made on sections from
were measured on the montages, using a Kontron Vid- SSP and ART specimens, as described above.
eoplan 2 equipment. Fiber diameters (D, including myelin sheaths) were calculated from the areas, assuming Sympathectomy
circularity (Karnes et al., 1977).
Three adult rats were anesthetized with chloral hydrate and used for surgical sympathectomy. The cerviHRP- labelling
cal portion of the sympathetic trunk was exposed, moIn order to determine the segmental level of origin of bilized, and cut out, from the superior cervical ganglion
the SSC, we performed retrograde labelling of “supras- to the level of the first rib. The animals were allowed to
capular” ventral horn and dorsal root ganglion neurons survive for 10 days. The operated animals showed a n
with horseradish peroxidase (WGA-HRP; Sigma). The obvious left-sided ptosis. For chemical sympathectomy
animals (n = 5) were anesthetized with chloral hydrate. rat pups were given daily injections of guanethidine
The SSC was exposed a t the neck of the scapula and cut (1.5%, 50 mgikg b.w.1 under the dorsal skin, during 3
with a pair of microscissors. The proximal stump was weeks, beginning day 3 after birth (Chad et al., 1983;
immersed in 2% WGA-HRP in saline. After one hour Johnson and Manning, 1984). These animals were left
the nerve stump was carefully cleaned and enclosed to survive until they were 3 months old. The injected
within a sealed Parafilm pocket, and the wound was animals were sparsely furred and they had slightly
closed. These animals were perfused 24 hours later, a s subnormal weights and loose stools, but no obvious ptodescribed above (perfusate: Ringer’s solution followed sis. The sympathectomized animals were perfused and
by 1%paraformaldehyde and 1.5% glutaraldehyde in the suprascapular nerves were collected and processed
Millonig’s phosphate buffer). The cervical spinal cord for electron microscopy, as described above. Counts of
segments and dorsal root ganglia were collected, post- myelinated and unmyelinated fibers were made on SSP
334
R. NORLIN ET AL.
Fig. 1. This dissected preparation shows the scapula, the clavicula,
and the humerus held together by the humeroscapular and acromioclavicular joints. The preparation is viewed from the head end of the
animal in a and from the lateral side in b. Note the distinct acromial
process from the long spina scapulae (a,b). Thin arrow in b points a t
tendon of long head of biceps muscle in intertubercular sulcus. Note
the absence of an incisura scapulae along the cranial edge of the
scapula (b). Arrowhead in b indicates the hook-like insertion site of
the deltoid muscle.
and ART specimens from 3 cases. In order to check that
the guanethidine treatment had been effective, the thoracic sympathetic trunk was cut out and examined under a dissection microscope. The paravertebral ganglia
were clearly seen in sympathetic trunks from normal
rats, but not in trunks from treated cases. This impression was confirmed by light microscopic examination of
sections from the superior cervical ganglion (not
shown). Hence, treatment had been effective.
All the experimental procedures described above
were approved by the local ethical committee.
RESULTS
Gross Anatomy
The thickened medial and lateral ends of the weakly
curved rat clavicula were anchored by ligaments in the
sternoclavicular and acromioclavicular joints. Two ligaments attached the lateral end of the clavicle to the
RAT SHOULDER REGION
335
Fig. 2. Radiographs showing antero-posterior (a) and lateral (b) views of the shoulder region.
SS = subacromial space, C =clavicle, CP = coracoid process, DM = insertion site of deltoid muscle.
Course of the SSC and its Branches
medially directed hook-like coracoid process. The rostral margin of the rat scapula lacked the incisure
Emerging as a distinct trunk from the brachial
present in man. Since the r a t scapula is longer in the plexus, the SSC traversed the supraclavicular fossa,
dorso-ventral t h a n in the rostro-caudal direction, the accompanied by a branch of the subscapular nerve (Fig.
spina scapulae is relatively longer than in man (Fig. 1). 3b). The SSC rounded the levator scapulae muscle and
A distinct acromion covered the humeroscapular joint approached the scapula without branching. While
(Figs. 1, 2). The oval articular surface of the glenoid passing collum scapulae, the SSC emitted the ART,
formation, which was enlarged by a cartilagineous la- which was composed of 1-3 fascicles (Fig. 3c). This thin
brum, was connected to the body of the scapula through branch could be followed into the subacromial space,
a comparatively long and narrow neck (Figs. 1,2). The where it ended in relation to the humeroscapular joint.
caput humeri had a half-spherical articular surface, a Having entered the fossa supraspinata, the SSC split
tuberculum majus, a tuberculum minus, and a n inter- into two branches while on the deep side of the sutubercular sulcus. A prominent deltoid tuberosity praspinatus muscle. The smaller SSP branch coursed
formed a broad-based hook-like process laterally on the dorsally on the deep side of its muscle, sending fiber
proximal half of the humerus (Figs. 1,2). The humero- bundles into it. The larger infraspinatus branch
scapular joint was enclosed by a distinct capsule, the rounded the ventral edge of the spina scapulae reachouter aspect of which was apposed by flattened ing the fossa infraspinata, where i t entered the inscapulo-humeral muscle tendons. The lateral end of the fraspinatus muscle from its deep side.
clavicle, the acromion, and a coracoacromial ligament
Fiber Composition of the SSC, SSP, and ART
formed on osteofibrous arch delimiting the subacromial
space. This space contained a synovial bursa, the ten- ssc
The labelling experiments demonstrated that SSC
don of the supraspinatus muscle, a portion of the joint
capsule, and part of the tendon of the long head of the motor axons originate mainly from neurons in the segbiceps muscle, which traversed the joint capsule (Figs. ment C5, with additional components in the caudal
half of the segment C4, or the cranial half of the seg2, 3a).
336
R. N O R I J N ET AL.
Fig. 3. These photographs show different views on a dissected rat
shoulder. a: View from cranial end. S M = supraspinatus muscle,
SP = spina scapulae, C =clavicle, A = acromion. Black triangle is located in subacromial space on top of the supraspinatus tendon. b
View from ventral side. This picture shows the cranial part of the
brachial plexus (BP). Arrow indicates suprascapular nerve. c: Dorso-
lateral view, showing the site where the suprascapular nerve (SSC)
rounds the levator scapulae muscle (LSM), approaches the upper border of the scapula (SCAP), and splits into three branches (ART=
articular nerve, SSP = supraspinatus nerve, INF = infraspinatus
nerve). SM = supraspinatus muscle.
ment C6. The sensory fibers come from corresponding
dorsal root ganglia (data not shown). The average normal SSC was monofascicular (Fig. 4a), and contained
3,435 axons, of which 26% were myelinated and 74%
unmyelinated (Table la). The myelinated fibers exhibited a distincly bimodal size distribution, ranging from
2 pm to about 17 pm. The two peak frequencies were
located at about 3 pm and 13-14 pm, and there was a
minimum a t 6-8 pm (Fig. 5a).
lb). The myelinated fibers exhibited a bimodal size distribution, ranging from 2 pm to about 16 pm. The two
peak frequencies were located at about 3 pm and 10-12
pm, with a minimum at 6-8 pm (Fig. 5b). After ventral rhizotomy the average SSP contained 116 myelinated axons, a reduction by 64% (Table lb). The deefferented SSP showed a reduced myelinated fiber size
range and a single peak at 3-4 pm. The upper peak
seen in the normal nerve was not obvious (Fig. 5c). In
capsaicin-treated animals, the proportion of unmyelinated axons was clearly subnormal (Table lb). No reductions occurred in vehicle-treated animals (data not
shown). Both after surgical and chemical sympathec-
SSP
The average normal SSP (Fig. 4b) contained 627 f i bers. Almost half of these were unmyelinated (Table
RAT SHOULDER REGION
Fig. 4. Electron micrographs showing general appearance of a)the suprascapular nerve ( x 450), b) the
supraspinatus nerve ( x 525), and c ) the articularisubacromial nerve ( x 4,000).
337
338
R. NORLIN ET AL.
TABLE lc. Fiber composition of the
subacromial/articularnerve in the normal state
and in various experimental conditions'
TABLE la. Numbers of myelinated (M) and
unmyelinated (U)fibers in the normal
SuDrascaDular nerve'
Normal
Mean
'%
=
913
888
948
940
840
905
2,546
2,579
2,580
2,480
2,472
2,530
73.6
74.3
73.1
72.5
74.6
73.6
proportion of unmyelinated axons, Tot
=
3,459
3,458
3,528
3,420
3,312
3,435
total number of axons.
TABLE lb. Fiber composition of the supraspinatus
nerve in the normal state and in various
experimental conditions'
Normal
Mean
Rhitzotomy
Mean
Capsaicin
Mean
Guanethidine
Mean
Surg.
sympathectomy
Mean
M
344
285
371
312
309
324
U
285
286
313
310
319
303
%
45.3
50.0
45.8
49.8
50.8
48.3
Normal
Mean
Rhizotomy
Mean
Capsaicin
Tot
629
571
684
622
628
627
100
124
124
116
Mean
Guanethidine
Mean
Surg.
sympathectomy
233
256
24 1
243
102
97
90
96
30.4
27.5
27.2
28.4
335
353
33 1
340
258
369
281
303
105
188
144
146
28.9
33.8
33.8
32.2
363
557
425
444
299
274
230
268
108
200
152
153
26.5
42.2
39.8
36.4
407
474
382
42 1
'M = number of myelinated axons, U = unmyelinated axons, %
proportion of unmyelinated axons, Tot = total number of axons.
=
tomy, the proportion of C-fibers was subnormal (Table
lb).
ART
The average normal ART (Fig. 4c) contained 259 axons. About 90% of all axons in the normal ART were
unmyelinated (Table lc). Although some myelinated
fibers reached up to 7-9 pm in diameter, most of them
had diameters below 4-5 km, with a peak a t about 3
pm (Fig. 5d). In cases subjected to ventral rhizotomy,
the proportions of myelinated and unmyelinated axons
were normal. In capsaicin-treated animals, the proportion of unmyelinated ART axons was 84% (Table lc),
i.e., slightly subnormal. No abnormality was observed
in vehicle-injected cases (data not shown). In animals
subjected to surgical sympathectomy, the ART contained 90% C-fibers, like in control cases. Following
Mean
M
26
29
31
24
26
27
U
255
245
222
193
245
232
90.7
89.4
86.0
88.9
92.7
89.5
Tot
281
274
253
217
271
259
19
13
31
21
175
169
234
193
90.2
92.9
88.3
90.2
194
182
265
214
37
36
51
41
293
250
155
233
88.8
87.4
75.2
83.8
330
286
206
274
45
62
41
49
58
118
134
103
56.3
65.6
76.6
66.2
103
180
175
153
34
59
37
43
274
615
317
402
89.0
91.2
89.5
89.9
308
674
354
445
%
'M = number of myelinated axons, U = number of unmyelinated
axons, % = proportion of unmyelinated axons, Tot = total number of
axons.
chemical sympathectomy with guanethidine, the proportion of C-fibers was 66%, i.e., markedly subnormal
(Table lc).
DISCUSSION
The present study was prompted by the deficient understanding of the pathophysiology of chronic inflammatory disorders affecting the subacromial space and
the supraspinatus muscle tendon in man. The r a t appeared to be generally suitable for analysis since i t has
a clavicle, unlike many other quadrupeds. Our analysis
showed that the rat shoulder region has obvious anatomical similarities with the human shoulder. This
might, conceivably, be related to the fact that the rat
uses its forepaws for object manipulation. The scapula has a distinct spine with a well developed acromion
that articulates with the clavicle. As in man, the acromion, the coracoid process, and bridging ligaments
form the roof of a narrow subacromial space containing
a synovial bursa, the tendon of the supraspinatus muscle, and the long head of the biceps muscle. The other
parts of the human "rotator cuff" are also present in
the rat. As in man, the deltoid muscle covers the shoulder joint, but in the rat the bony insertion of this muscle on the humerus is much more prominent than the
human deltoid tuberosity (Fig. lb). We conclude that,
in terms of gross anatomy, the rat shoulder is surprisingly similar to the human shoulder.
In agreement with previous observations in man
(Gardner, 1948; Kato, 1989) and rat (Greene, 1963;
339
RAT SHOULDER REGION
:]
%
%
20
4
I
10
10
5
5
D
0
0
5
10
15
20
m)
D
0
0
5
10
15
20
m)
b
a
il&
46
15
10
- 0
5
5
10
d
20
D
6 4
Fig. 5. Representative histograms showing size distribution of myelinated fibres (D, myelin sheaths
included) in the suprascapular nerve (a), the normal supraspinatus nerve (b), the deefferented supraspinatus nerve (c), and the articular/subacromial nerve (d).
Hebel and Stromberg, 1986), our dissections showed
that the SSC sends branches to the supra- and infraspinatus muscles. According to our labelling experiments, this nerve originates from neurons in the segment C5, with contributions from either of the adjacent
segments. The same levels have been indicated by
other workers as segments of origin for the SSC in the
rat (Kitamura et al., 1981), and kangaroo (Kato and
Hopwood, 1993), and in man (Kerr, 1918; Horiguchi,
1980; Kato, 1989). The rat shoulder joint is innervated
from the segments C3-C5 (Yoshida et al., 1992).
Our counts show that the SSC contains some 3,400
axons, about 314 of which are unmyelinated. This proportion of C-fibers is higher than in other muscle
nerves, which suggests that the SSC may contain nonmuscular components. The size spectrum of the SSC
showed a bimodal distribution, as in other muscle
nerves (Romero and Skoglund, 1965), but the proportion of small myelinated fibers was relatively high.
Since the cutaneous branch sometimes emerging from
the human SSC (Horiguchi, 1980) was absent in the
rat, the surplus of unmyelinated and small myelinated
fibers in the rat SSC should not represent cutaneous
axons. Instead, i t might reflect the presence of articular axons, some of which leave the SSC with the ART.
Joint nerves typically contain high proportions of C-fibers and small myelinated axons (Langford and
Schmidt, 1983a; Hildebrand et al., 1991).
The muscular supraspinatus branch (SSP)was found
to contain about 620 axons, half of which were unmyelinated. Nerves to various r a t hindlimb muscles contain 44-63% unmyelinated axons (Jenq and Cogges-
hall, 1984, 1985; Peyronnard et al., 1986). In the rat
sternomastoid nerve, 50% of all axons are unmyelinated and 40% of these are sympathetic efferents (Sandoz and Zenker, 1986). The rat phrenic nerve contains
43% unmyelinated axons (Langford and Schmidt,
1983b). About 113 of the myelinated SSP fibers should
be sensory, since they persisted after ventral rhizotomy. This figure is within the range presented for other
nerves (e.g., Sherrington, 1895; Gottschall et al., 1980).
The myelinated axons exhibited a distinctly bimodal
muscle-type size distribution. Our measurements on
rhizotomized cases showed that most of the muscle afferents are relatively thin, although some reach relatively large sizes (Sherrington 1895; Lloyd and Chang,
1948), and that a large proportion of the thick myelinated axons are motor efferents. Following neonatal
capsaicin treatment, the proportion of C-fibers had decreased from 48% to 28%. This suggests a substantial
loss of C-fibers. The number of myelinated axons was
also low, but we feel that this may be due to individual
variations. According to other workers, both myelinated and unmyelinated axons are lost from peripheral
nerves after neonatal capsaicin treatment, but the figures show a considerable variation (see Lawson, 1981;
Jancso et al., 1985). We conclude that the SSP contains
many unmyelinated capsaicin-sensitive axons. The
functional role of these fibers remains to be found out.
Following both surgical and chemical sympathectomy,
the proportion of C-fibers in the SSP was reduced from
the normal level of about 48% to some 32%. This indicates that 113 of the C-fibers in this nerve may by sympathetic. Chad et al. (1983) concluded that sympathetic
340
R. NORLIN ET AL
The supraspinatus n e n e (SSP)
’ I h e subacromial n e n e (.\RT)
100 %
25
10 sens
6
Fig. 6. Diagrams showing estimated relative proportions of different fiber types in the supraspinatus
nerve (SSP) and the subacromialiarticular nerve (ART).
postganglionic unmyelinated axons account for 20 25%of all unmyelinated axons in cutaneous, muscular,
and mixed nerves. According to Peyronnard et al.
(1986), sympathetic axons account for 23-34% of all
C-fibers in r a t hindlimb muscle nerves.
Our analysis showed that the average ART is composed of 10% myelinated axons, all of which are sensory, and 90% C-fibers. The myelinated axons showed a
unimodal size distribution and a limited size range.
Similar characteristics have been observed in the posterior articular nerve of the r a t knee joint (Hildebrand
et al., 1991). Following neonatal capsaicin treatment,
the proportion of C-fibers in the ART was close to normal. Hence, this nerve contains few capsaicin-sensitive
units. Usually, a large proportion of the sensory C-fibres, as well as some small myelinated axons, disappear from peripheral sensory nerves after treatment of
neonatal rat pups with capsaicin. The content of substance P in the dorsal horn is also markedly reduced
(Lawson, 1981; Nagy et al., 1983; Jancso et al., 1985;
Holzer, 1988). Since the examined dorsal roots exhibited a dramatically decreased proportion of C-fibers,
the very limited alteration in the proportion of C-fibers
in the ART should be real. A relative insensitivity to
neonatal treatment with capsaicin has also been noted
in the posterior articular nerve of the knee joint (Hildebrand et al., 1991), in pulpal nerves (Holje et al., 1985;
Fried et al., 1988), and in the spinal pia mater (Karlsson and Hildebrand, 1994) of the rat. Capsaicin primarily affects neurons with unmyelinated and small myelinated axons involved in polymodal or chemical
nociception (see Nagy et al., 1983). The insensitivity of
articular, pulpal, and pial nerves could reflect a basically mechanosensitive function (Dubner et al., 1978;
Schaible and Smith, 1983a,b). In animals subjected to
surgical sympathectomy, the proportion of C-fibers in
the ART remained unchanged at 90%. Therefore, the
surgery failed to remove ganglia responsible for sympathetic axons in the ART, although i t did affect the
SSP. After chemical sympathectomy, however, the proportion of C-fibers in the ART had decreased to 66%.
This suggests that 114 of all C-fibers in this nerve may
be sympathetic, Some 50% of the numerous C-fibers
present in cat articular nerves are sympathetic (Langford and Schmidt, 1983a), and in the posterior articular
nerve of the rat knee joint about 213 of the C-fibers are
sympathetic (Hildebrand et al., 1991).
In man, the SSC provides sensory fibers to a major
part of the shoulder joint. It emits articular branches
which follow a course similar to that of the ART in the
rat, and which ramify in the region where the supraspinatus tendon enters the capsule and around the
acromioclavicular joint (Gardner, 1948; Kato, 1989;
Gad0 and Emery, 1993). Whether the human ART
projects to the subacromial bursa, which exhibits a n
extensive neural network (Tomita et al., 19921, is unknown. On the basis of our anatomical observations,
the typical “articular” fiber composition of the ART,
and the discussion above, we suggest that this suprascapular nerve branch provides the rat shoulder joint
(and possibly the subacromial bursa) with sensory and
sympathetic axons. In humans, articular branches may
also reach the shoulder joint through, e.g., the infraspinatus branch of the suprascapular nerve and the
axillary nerve (Gardner, 1948).
There is increasing evidence t h a t sensory and sympathetic C-fibers may play active roles in inflammatory conditions in the locomotor system (Levine et al.,
1985; Fitzgerald, 1989; Kidd e t al., 1990; Weinstein,
1991) and in various other tissues (Saria et al., 1983;
Foreman and Jordan, 1984; Szolcsanyi, 1988; Bienenstock e t al., 1991; Donnerer and Amann, 1993; Dray
and Perkins, 1993). Afferents from arthritic joints have
a n abnormal spontaneous activity and the articular receptors are markedly responsive to normally innocuous
stimuli (Guilbaud et al., 1985; Grigg et al., 1986). Injection of substance P (SP)into arthritic r a t knee joints
aggravates inflammation and destruction (Levine et
al., 1984). The occurrence of SP is increased in joints
and sciatic nerves of arthritic rats (Lembeck et al.,
1981; Levine et al., 1984). It has also been suggested
that activity in sympathetic axons can amplify neurogenic inflammation (Coderre e t al., 1989). These and
other data indicate that nociceptive and autonomic
nerve fibers may be actively involved in inflammatory
conditions, pain, and tissue destruction forming a vicious circle (see Fitzgerald, 1989; Lam and Ferrell,
1991).To what extent the rat suprascapular nerve participates in experimental inflammatory conditions in
the subacromial space remains to be found out.
RAT SHOULD'ER REGION
34 1
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