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Mechanoreceptors in the human anterior cruciate ligament.

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THE ANATOMICAL RECORD 214904-209 (1986)
Mechanoreceptors in the Human Anterior
Cruciate Ligament
MARTLYN L. ZIMNY, MICHAEL SCHUTTE, AND EUGENE DABEZIES
Departments of Anatomy (M.L.Z.) and Orthopaedics (M.S. and E.D.), Louisiana State
University Medical Center, New Orleans, LA 70112
ABSTRACT This study was undertaken to identify and quantitate mechanoreceptors in the human anterior cruciate ligament (ACL). Ligaments from six human
subjects were obtained a t autopsy, cut into cross-sectional segments 1.0-1.5 cm thick,
and kept oriented as to the femoral and tibial attachments. The segments were
stained in bulk by using a modified gold chloride method, frozen, and sectioned on a
sliding microtome a t 100 pm. The sections were floated in alcoholic gelatin, mounted
on slides, dehydrated, and coverslipped. Serial sections were studied with the light
microscope and receptors were photographed. Cross-sectional maps of every tenth
section were made outlining the periphery of the ACL and the receptors within that
section. With these maps, a computerized, morphometric analysis of the ACL was
done, thus obtaining the percentage of receptors in each section and in each ACL. In
addition to free nerve endings, two morphologically distinct mechanoreceptors were
identified: (1)Ruffini end organs and (2) Pacinian corpuscles. Preliminary morphometric analyses show that populations of mechanoreceptors are greater at the
femoral and tibial ends of the ligament and constitute approximately 2.5% of the
ligament. Based on these findings the human ACL has the anatomic basis for a
discriminating afferent outflow to the central nervous system.
In recent years, there has been renewed orthopaedic
interest in the ligamentous neurology of the human
anterior cruciate ligament (ACL) due to the fact that
treatment of the anterior cruciate-deficient knee is still
a debatable subject. Most studies of neural elements in
the capsules of knee joints have been done in cats (Gardner, 1944; Samuel, 1952; Boyd, 1954; Skoglund, 1956;
Freeman and Wyke, 1967; Halata, 1977). The most extensive anatomical study of the nerve supply of the
human knee to date was published by Gardner (1945).
The constancy of certain branches and definite patterns
of joint innervations were established. Nerve fibers, ones
not associated with blood vessels, have been observed in
the human anterior cruciate ligament (Kennedy et al.,
1974). A study of the nerve supply of the human knee
was undertaken by Kennedy et al. (19821, using dissections of fresh amputation specimens. Histologically it
was found that axons and receptors are rarely found in
the deep fibrous substance of ligaments or menisci and
although pain endings predominate in the adjacent connective tissue, a variety of specialized receptors are also
present. No specialized receptors were recognized in the
human anterior cruciate ligament. Rovere and Adair
(1983), in a review article related to anterior cruciatedeficient knees, also noted that specialized receptors in
the human anterior cruciate ligament have not been
recognized. Considering that receptor specificity is likely
a major factor in sensory discrimination, the identification of specialized receptors within the human anterior
cruciate ligament would be a basis for defining its sensory function. The present study was undertaken to
0 1986 ALAN R. LISS, INC.
identify specialized mechanoreceptors in the human anterior cruciate ligament.
MATERIALS AND METHODS
Anterior cruciate ligaments from six human subjects
were obtained a t autopsy and placed in normal saline
solution. The ligaments were cut into cross-sectional
segments about 1.0-1.5 cm thick and kept oriented as to
the femoral and tibial attachments. The segments were
stained in bulk by using a modification (Zimny et al.,
1985) of a gold chloride method used by Gairns (1930)
for the demonstration of nerve endings in skeletal muscle. Essentially the recent modification consists of differences in staining time for the formic acid and gold
chloride and the use of frozen sections instead of teased
tissue.
After staining, the segments were frozen and sectioned on a sliding microtome at 100 pm. The sections
were floated in alcoholic gelatin, mounted on slides,
dehydrated, and coverslipped. The serial sections were
studied with a light microscope and receptors within the
ligaments were identified and photographed.
RESULTS
The anterior cruciate ligament was found to have a n
extensive intraligamentous neural network. Nerve fibers appear to enter the ligament via a neurovascular
bundle in the subsynovial connective tissue Figs. 1, 2).
Received April 30, 1985; accepted September 10, 1985.
MECHANORECEPTORS IN CRUCIATE LIGAMENTS
205
Fig. 1 . A line drawing of a section 8 mm from the femoral attachment of the anterior cruciate
ligament. The rectangular area designated by the lines is shown in the montage, Figure 2.
x 10.
Receptors are seen in the surrounding connective tissue
and in the ligament itself. Nerve fibers enter the ligament from the connective tissue and are seen terminating in various receptors (Fig. 3). The receptors
morphologically resemble those described in the cat
(Gardner, 1944; Boyd, 1954; Skoglund, 1956; Freeman
and Wyke, 1967). The identification of the mechanoreceptors in this study was based on these reports and
those of Halata (1977), Halata and Munger (19831, Munger and Halata (1983), and a personal communication
Wunger, 1984).
In addition to free nerve endings two morphologically
distinct mechanoreceptors were identified and categorized as follows: (1) Ruffini end organs (Figs. 4,5) and (2)
Pacinian corpuscles (Fig. 6). Although structure varied
to some degree, it is felt the morphology of these endings
in contiguous sections indicates that o w categorization
is valid. Preliminary observations seem to indicate that
the receptors are mainly localized a t each end of the
ligament and constitute approximately 2.5%of its area.
function as transducers, converting physical energy expressed as tension into a nervous signal. In respect to
the human anterior cruciate ligament, the intraligamentous mechanoreceptors would be stimulated by tension developed within the collagenous fibers in response
to knee motion. This investigation shows that the human anterior cruciate ligament has three morphologically different types of mechanoreceptors, each capable
of responding to tension within its substance. As the
knee moves through a range of motion about its instant
centers, variables to be deciphered by this population of
intraligamentous receptors include speed, acceleration,
direction of motion, and exact joint position. Another
physiologic characteristic of receptors is adaptability,
and all mechanoreceptors have some form of adaptation.
In the human anterior cruciate ligament these fall along
a spectrum ranging from slowly adapting to rapidly
adapting. In general, rapidly adapting mechanoreceptors are suited to signal change in the environment such
as motion, whereas the slowly adapting types are better
for determining stimulus characteristics, such as speed
DISCUSSION
and acceleration.
Mechanoreceptors play a role in the fundamental orTo our knowledge this is the first histological demonganization of the central nervous system. Basically they stration of two morphologically distinct rnechanorecep-
M.L. ZIMNY, M. SCHUTTE, AND E. DABEZIES
Fig. 2. A montage composed of light micrographs showing the nerves
(N) and blood vessels (BV) in the subsynovial connective tissue (CT) of
the anterior cruciate ligament (L) and free nerve endings within the
ligament (NE). ~ 3 0 .
tors in the human anterior cruciate ligament. The first
histological demonstration of mechanoreceptors in the
human cruciate ligaments was reported in the literature
by Schultz et al. (1984). Their paper illustrates a fusiform mechanoreceptor, axons within the substance of
the ligament, and a mechanoreceptor resembling a Golgi
tendon organ. Our work indicates the presence of Ruffini end organs and Pacinian corpuscles, in addition to
free nerve endings.
Ruffini end organs have been described in the joint
capsule of feline knee joints (Gardner, 1944; Boyd, 1954;
Skoglund, 1956; Polacek, 1966; Freeman and Wyke,
1967). Functionally, Ruffini corpuscles are slowly adapting mechanoreceptors (Freeman and Wyke, 1967; Wyke,
1973; Skoglund, 1973). In the articular capsule of the
feline knee joint, according to Wyke (1973) they have a
very low threshold, react to pressure changes within the
joint, and signal static and dynamic tensile stresses.
More recent studies have shown the Ruffhi endings in
the feline joint capsule to be very sensitive to capsular
stretching (Grigg and Hoffman, 1982). This receptor may
play a role in signaling proximity of the joint to its limit
of rotation in extension. It is very likely that these
receptors within the human anterior cruciate ligament
have similar characteristics and capabilities.
The ultrastructure of mechanoreceptors in the skin
was reviewed by Munger (1971)and Halata (1975). Since
these reviews were written, a second specific sensory
receptor has been identified by light and electron microscopy as a Ruffini corpuscle. Biemesderfer et al. (1978)
described Ruffini corpuscles associated with hairs, a piloRuffini complex, and Halata (1977) described Ruffini
corpuscles in feline knee joint capsules. In both studies
the receptors ultrastructurally resembled a Golgi tendon organ as described by Schoultz and Swett (1972,
1974) or subsequently by Zelena and Soukup (1977).
Golgi tendon organs are known to be slow-adapting
mechanoreceptors. The pilo-Ruffini complex was identified on the basis of slow-adapting response characteristics in single-unit studies by Biemesderfer et al. (1978).
In our study we have identified both types of Ruffini end
organs.
Pacinian corpuscles were described in the joint capsule
of feline knee joints (Gardner, 1944; Boyd, 1954; Skoglund, 1956; Freeman and Wyke, 1967). Physiological
studies showed them to be rapidly adapting mechanoreceptors (Boyd, 1954; Freeman and Wyke, 1967; Wyke,
1973; Skoglund, 1973). They were termed acceleration
receptors by Skoglund (1956). Other studies indicated
that these receptors were activated by all movements of
the joint regardless of position with the frequency of
response being a function of the speed of movement
(Burgess and Clark, 1969; Ecklund and Skoglund, 1960).
In the articular capsule of the feline knee joint, according to Wyke (1973), they have a very low threshold and
work as dynamic mechanoreceptors at the beginning
and end of movement.
Free nerve endings have been described in tissues of
feline knee joints (Gardner, 1944; Boyd, 1954; Skoglund,
1956; Barnett et al., 1961; Freeman and Wyke, 1967). It
is believed this system of free nerve endings and plexuses constitutes the pain receptor system of the joint
tissues (Freeman and Wyke, 1967). Free nerve endings
in the anterior cruciate ligament and subsynovial connective tissue could possibly subserve the same function.
It is indeed possible and probable that injury to the
anterior cruciate ligament causes not only a biomechanical derangement but also a neurological derangement.
The afferent flow to the central nervous system from the
knee is directly effected by the injury to the ligament
with its mechanoreceptors. The aberrant rotatory patterns associated with anterior cruciate ligament disruption will affect the tension patterns of other intraarticular structures, such as the capsule and the posterior
cruciate ligament, and extraarticular structures, such
as the medial and lateral collateral ligaments.
v
MECHANORECEPTORS IN CRUCIATE LIGAMENTS
Fig. 3.A nerve fiber (N) is seen entering the anterior cruciate ligament from the subsynovial connective tissue and terminating in a receptor (R). ~ 5 0 .
Fig. 4. A Ruffini end organ (R) within the anterior cruciate ligament. x 165.
207
208
M.L. ZIMNY, M. SCHUTTE, AND E. DABEZIES
Fig. 5. A Ruffini end organ (R) resembling a Golgi tendon organ within the anterior
cruciate ligament. x 110.
Fig. 6. A Pacinian corpuscle (R) within the anterior cruciate ligament. x 110.
MECHANORECEF'TORSIN CRUCIATE LIGAMENTS
ACKNOWLEDGMENTS
The authors wish to thank Mrs. Michele St. Onge for
her technical expertise in the preparation of tissues for
light microscopy and Mrs. Madelyn S. Garrity for her
secretarial skills.
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