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Nerve endings in human fasciae tendons ligaments periosteum and joint synovial membrane.

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Nerve Endings in Human Fasciae, Tendons,
Ligaments, Periosteum, and Joint
Synovial Membrane’
HENRY J. RALSTON 111, MALCOLM R. MILLER AND
MICHIKO KASAHARA
Biomechanics Laboratory and Department o f Anutomy,
University of California School o f Medicine, San Francisco
In recent years there has been a revival
of interest in the morphology and physiology of bones and joints and structures
related to them. Both Gardner (’44) and
Stilwell (’57a, b, c, d j have emphasized
the need for investigation of the innervation of deep fibrous structures.
The first essential task to be accomplished is the description, classification,
and illustration of the types of nerve endings found in such structures as deep fasciae, ligaments, tendons, periosteum, and
synovial membrane. The pattern of distribution of these endings must then be determined. These descriptive studies should
ultimately aid in the correlation of structure and pattern of arrangement with
function.
study was facilitated by careful splitting
or division of the thicker tissues.
OBSERVATIONS
In most of the deep tissues that we
studied (deep fasciae, tendons, ligaments,
periosteum, and synovial membrane) we
found three major varieties of nerve endings.
The first and most simple type is the
free-fiber ending. These endings occur
either as single unbranched terminals or
in the form of several simple arborizing
branches. They have few or no varicosities
along the course of the terminal branch
or branches, and end with tapered tips.
They are derived from small myelinated
fibers less than 3 EL in diameter.
In addition to the free-fiber endings of
small myelinated fibers, we were also able
MATERIALS AND METHODS
The specimens of fasciae, tendons, liga- to demonstrate the presence of fine beaded
ments, periosteum, and synovial mem- amyelinated fibers. These were always
brane used in this study were from 20 found in association with blood vessels,
patients between 12 and 68 years of age. and we assumed them to be autonomic in
Most specjmens were obtained from upper form and function. We have never enor lower extremities amputated because countered any structure that we could
of tumors or vascular disease. A few interpret as a “sympathetic ground plexus.”
The second type of nerve ending found
specimens were of locally excised tissues
in
deeper tissues is unencapsulated and
from the regions around the joints. Within 10 minutes to three hours after surgical varies widely in complexity of structure,
removal, the amputated limbs were per- from relatively simple few-branched to
fused with 0.05% methylene blue, while multibranched and intricately intertwined.
the locally excised pieces of tissues were Regardless of the degree of complexity,
these endings have several features in
immersed in 0.01% methylene blue, accommon : ( 1 ) They are derived from fibers
cording to the technic of Schabadasch as
of
moderate size ( 5 w to 12 w in diameter);
described by Meyling ( ’ 5 3 ) . The speci( 2 ) they all consist of terminal branches,
mens were prepared for study in the manthough the number of these branches varner described by Miller et al. (’58). In
most cases it was possible to examine these
1 This investigation was supported by United
tissues as whole mounts but occasionally States Public Health Service grant RG-4856.
137
138
H. J. RALSTON 111, Sf. R. MILLER A N D M. KASAHARA
ies; (3) the end branches have varicose
swellings; ( 4 ) in many cases there are
anastomotic connections between the end
branches; and (5) many of the branches
end in small expanded tips. In classic
descriptions these complex unencapsulated structures have been termed Golgitype endings when they occur as groups
of expanded-tip structures closely applied
to the surface of bundles of dense connective-tissue fibers. When they appear to
be surrounded by a delicate membrane
(but not a capsule) and contain frequent
granular inclusions, they have been designated Ruffini or Ruffini-likeendings. When
these complexly arranged, branched, varicose endings surround a larger group of
connective-tissue fibers in a cylindrical
fashion, they have been referred to as
Golgi tendon organs.
Although most of the above specific
varieties may be found in deep tissues in
more or less classic form. endings that
are transitional in form are found perhaps
more frequently. Since all these transitional endings possess most of the features
mentioned above, and their modifications
seem to be in adaptation to their particular
anatomical site of location, it seems justified to include both transitional forms and
specific varieties in a single category and
term them complex unencapsulated endings.
A third category of nerve endings found
in deep tissues is the encapsulated type.
Varieties include Golgi-Mazzoni, paciniform and small and large pacinian corpuscles. There is little difficulty in the identification of these various subtypes, and for
the present it may be useful to classify
them all as encapsulated nerve endings.
Nerve endings in deep fasciae
and joint capsules
In thick, dense connective tissues, as
in retinacula, and in fibrous joint capsules
and their associated collateral ligaments,
all three major categories of nerve endings
are found in combination. Free-fiber endings are illustrated in figure 1. The variety
of types of complex unencapsulated endings is large. These endings include simple few-branched types (figs. 2, 3 ) , more
spread-out transitional forms (fig. 4 ) , and
the classic Rusni-like endings (fig. 5).
Either the Golgi-type or the Ruffini-like
endings may be composed of groups of a
dozen or more “units” or subgroups of
endings, each a complex ending in itself.
Encapsulated endings of the Golgi-Mazzoni and paciniform types are frequently
encountered in these regions in association with the other two.
Nerve endings in tendons
In the tendons of both the upper and
lower extremities, the most frequently encountered nerve terminations are freefiber endings, relatively simple varieties
of complex unencapsnlated endings, and
small paciniform endings.
In tendons which are continually involved in muscular activity, such as that
of the quadriceps femoris, relatively large
Golgi tendon organs were found. In our
classification these are considered elongated cylindrical varieties of complex unencapsulated endings.
Nerve endings in ligaments
Like deep fasciae or tendons, many ligaments possess all three major types of
nerve endings. The complex unencapsulated endings are perhaps even more diverse and variable in iorm in these structures than they are in tendons or joint
capsules.
In figure 6 is shown a large spread-out
complex unencapsulated ending from the
patellar ligament. The constituent fibers
are less confined than those in the usual
Ruffini-like ending, while the terminal
expansions are less well developed than
in a typical Golgi-type ending. However,
since this ending is similar to both the
Ruffini and the Golgi type of ending, it
seems convenient to include all these types
of endings in the second category. Figure 7 depicts a more classic Ruffinj-like
ending, while figure 9 shows a structure
similar to the Golgi tendon organ. An
encapsulated ending of the Golgi-Mazzoni
type is illustrated in figure 8.
Nerve endings in. periosteum
The nerve endings in the periosteum of
the long bones of the extremities are par-
NERVE ENDINGS IN FIBROUS STRUCTURES
ticularly abundant near the sites of muscular, tendinous, or ligamentous attachments and the three categories are easily
demonstrated. Figure 10 shows a diffuse
variety of Golgi-type unencapsulated complex ending. Encapsulated Golgi-Mazzoni
endings similar to the one illustrated in
figure 8 are also abundant in periosteum.
Nerve endings in joint
synouial membrane
In joint synovial membrane we have
seen only free-fiber endings. In the connective tissue overlying the tissue of the
joint capsule, both complex unencapsulated and encapsulated endings are also
present.
DISCUSSION
Most students of deep-tissue innervation
agree that free, complex (Ruffini and
Golgi types), and encapsulated endings
are to be found in many of the deep connective tissues of the body (Hromada and
PolBEek, '58; Stilwell, '57a, b, c, d; Skoglund, '56; Andrew, '54; Samuel, '52; Gardner, '56, '44; Weddell and Harpman, '40).
It is probable, too, that most of these workers would accept a three-category classification of types of nerve endings; at least,
no one has argued the case for the rigid
separation of a large variety of types.
Most importantly, the physiological evidence is against such a rigid separation
(Andrew, '54). There is general concurrence that the morphological variations
observed in the complex unencapsulated
endings (Ruffini or Golgi types or their
variants) probably represent adaptations
to local anatomical configurations of receptors that may have similar functions.
We have postulated previously (Miller
et al., '58) that the varieties of nerve endings found in cutaneous areas are homologous to those found in the deeper tissues.
In both superficial and deep tissues one
encounters ( 1) free-fiber endings, ( 2 )
complex unencapsulated or expanded-tip
endings (the groups of Merkel's disks at
the dermal-epidermal junction, the Ruffini endings of the dermis, and the Ruffini-like or Golgi-type endings of the deeper
tissues), and ( 3 ) encapsulated endings
(the Meissner's corpuscles or the hair
139
follicles of the skin, the Krause end-bulbs
of the dermis, or the Golgi-Mazzoni and
pacinian endings of the deeper structures).
As far as correlation of structure with
function is concerned, one general hypothesis has been that free-fiber endings are
associated with the reception of painful
stimuli, the unencapsulated endings
largely with touch in the skin or proprioception in the deeper tissue, and the encapsulated endings with pressure reception. The basic problem still remains:
Do individual types of endings play fundamentally different roles in sensory perception, or do they produce different sensations by participating in different patterns
of activity?
LITERATURE CITED
Anclrew, B. L. 1954 The sensory innervation
of the inedial ligament of the knee joint. J.
Physiol., 123: 241-250.
Gardner, E. 1944 The distribution and termination of nerves i n the knee joint of the cat.
J. Comp. Neurol., 80: 11-32.
1956 Nerves and nerve endings i n
joints and associated structures of monkey
(Macaca mulatta). Anat. Rec., 124: 293.
Hromadaf, J., and P. PolAEek 1958 A contribution to the morphology of encapsulated nerve
endings i n the joint capsule and in the periarticular tissue. Acta Anat., 33: 187-202.
Meyling, 13. A. 1953 Structure and significance
of the peripheral extension of the autonomic
nervous system. J. Comp. Neur., 99: 495-544.
Milker, M. R., H. J. Ralston I11 and M. Kasahara
1958 The pattern of cutaneous innervation
of the human hand. Am. J. Anat., 102: 183218.
Stilwsll, D. L.. Jr. 1957a Regional variations in
the innervation of deep fasciae and aponeuroses. Anat. Rec., 127: 635-654.
1957b The innervation of tendons and
aponeuroses. Am. J. Anat., 100: 289-318.
1957c The innervation of deep structures of the foot. Ibid., 101: 59-74.
1957d The innervation of deep structures of the hand. Ibid., 101: 75-100.
Samuel, E. P. 1952 The autonomic and somatic innervation of the articular capsule.
Anat. Rec., 113: 53-70.
Skoglund, S. 1956 Anatomical and physiological studies of knee joint innervation in the
cat. Acta Physiol. Scand. 36, suppl. 124: 1-101.
Weddell, G . , and J. A. Harpman 1940 The
neurohistological basis for the sensation of
pain provoked from deep fascia, tendon and
periosteum. J. Neurol. Psychiat., 3: 319-328.
-
~
PLATES
The tissues in figures 4, 6, 7, 8, 9, and 10 were
stained by methylene-blue immersion. The tissues in
all other figures were stained by methylene-blue perfusion.
PLATE I
EXPLANATION O F FIGURES
1 Extensor retinaculum of wrist. Fr.ee-fiber endings.
140
x
200.
2
Extensor retinaculum of wrist. Golgi-type ending. We consider this type of ending
a simple form of the complex unencapsulated ending. x 500.
3
Extensor retinaculum of wrist. A nerve ending which has some branches ending
freely while others end with expanded tips. Since there are anastomoses between
some end branches, this ending assumes some of the characteristics of a complex
unencapsulated ending but is transitional i n nature i n that it also is a typ.e of reduplicated free-fiber ending. X 250.
NERVE ENDINGS IN FIBROUS STRUCTURES
H. J. Ralston 111, M. R. Miller and M. Kasahara
PLATE 1
141
NERVE ENDINGS I N FIBROUS STRUCTURES
H. J. Ralston 111, M. R. Miller and M. Kasahara
4
142
PLATE 2
Joint capsule of knee. A complex unencapsulated .ending resembling a Golgi tendon
organ. x 400.
NERVE ENDINGS IN FIBROUS STRUCTURES
H. J. Ralston 111, M. R. Miller and M. Kasahara
5
PLATE 3
Extensor retinaculum of wrist. A group of more than a dozen Ruffini-like endings
(complex unencapsulated endings). x 120.
143
NERVE ENDINGS I N FIBROUS STRUCTURES
H. J. Ralston 111, M. R. Miller and M. Kasahara
6
144
PLATE 4
Patellar ligament. Complex unencapsulated endings: Some units are similar to Golgitype complexes in that they ar.e spread out; however, they do not have expanded
terminal tips. Other units are more confined and similar to Ruffini-like terminals. X 200.
NERVE ENDINGS IN FIBROUS STRUCTURES
H. J. Ralston 111, M. R. Miller and M. Kasahara
PLATE 5
7 Medial collateral ligament of knee. Two Ruffini-like endings (complex unencapsulated).
x
8
300.
Interosseous ligament of hand. Golgi-Mazzoni encapsulated corpuscle. X 200.
145
NERVE ENDINGS IN FIBROUS STRUCTURES
H. J. Ralston 111, M. R. Miller and M. Kasahara
9
146
PLATE 6
Medial collateral ligament of knee. A long cylindrical Golgi tendon organ (complex
unencapsulated). X 200.
NERVE ENDINGS I N FIBROUS STRUCTURES
H. J. Ralston 111, M. R. Miller and M. Kasahara
10
PLATE 7
Femoral periosteum. A Golgi-type variety of a complex unencapsulated ending.
x 250.
147
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periosteum, fasciae, ending, nerve, joint, tendon, ligament, membranes, synovial, human
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