J Appl Physiol
89: 2191–2195, 2000.
Muscular reflexes elicited by electrical stimulation
of the anterior cruciate ligament in humans
POUL DYHRE-POULSEN1 AND MICHAEL R. KROGSGAARD2
1
Institute of Medical Physiology, Panum Institute, University of Copenhagen, and 2Department of
Orthopedic Surgery, National University Hospital, Rigshospitalet, DK-2200 Copenhagen, Denmark
Received 2 September 1998; accepted in final form 20 July 2000
knee joint; physiology; proprioception
of the anterior cruciate ligament
(ACL) is to restrain forward translation of the tibia in
relation to the femur. However, the ACL can only
sustain loads of ⬃1,735–2,000 N (19, 28), and it is,
therefore, often torn, especially during dynamic loading. Given the limited protection possible through the
mechanical properties of the ligament, it has been
suggested that muscular contractions, possibly of reflex origin, are necessary to protect the ACL and to
improve the dynamic stability of the knee (10, 23).
Furthermore, proprioception is impaired in the knee of
patients with ACL lesion (2), and histological studies
have proved the existence of abundant nervous tissue
and mechanoreceptors in the ACL (15, 29). Because
most thick myelinated afferents arising from the ACL
are activated by application of local pressure to discrete sites of the ligament (14), the ACL may serve both
as a sensory receptor element that signals load and a
movement-restraining mechanical device. It is therefore conceivable that articular mechanoreceptor reflexes are “significantly involved in the normal reflex
THE FUNCTIONAL ROLE
Address for reprint requests and other correspondence: P. DyhrePoulsen, Inst. of Medical Physiology 16-5, Panum Inst., Blegdamsvej
3, DK-2200 Copenhagen N, Denmark (E-mail: [email protected]).
http://www.jap.org
coordination of muscle tone in posture and movement”
(4).
In 1958, Palmer et al. (20) suggested that afferent
signals from the medial collateral ligament (MCL) of
the knee were able to modify the activity in the muscles
around the knee. Pulling the MCL with a suture sewn
into it or tapping the ligament elicited activity in the
hamstrings muscles in decerebrated cats. Ekholm et al.
(3) also reported such effects and suggested that the
effects were mediated via the ␥-muscle spindle system
rather than directly onto the skeletomotoneurons. The
same suggestion was further stressed by Freeman and
Wyke (4). The idea gained experimental support from
Sjölander et al. (24), who showed that low and moderate changes in the tension of the MCL and the lateral
collateral ligament (LCL) evoked fusimotor effects,
without concomitant activation of skeletomotoneurons.
The fusimotor activations were potent enough to significantly alter the sensitivity of muscle spindle afferents from both the extensor and flexor muscles around
the knee. Stener (26) described a method to selectively
pull the MCL, but he was unable to elicit any muscular
reflex from the MCL in neither cats (1) nor humans
(22). However, stimulation of nerve fibers next to the
MCL did, in fact, induce strong muscular activity in
the extensor and flexor muscles around the knee.
Solomonow et al. (25) were the first to show that
information from sensory receptors in the ACL influences electromyographic (EMG) activity in the hamstring muscles. By pulling the ligament with forces just
below the rupture threshold, EMG activity in the hamstrings could be elicited in anesthetized cats. Miyatsu
et al. (17) found that even low traction forces can
induce changes in both knee flexor and extensor muscle activity in spinalized cats, and they suggested that
the effects were primarily directed onto ␥-motoneurons. In humans, a hamstring muscle response to traction of the ACL during open surgery has also been
observed (8). Thus, from animal studies, there are
enough experimental data to confirm the existence of
“ligamento-muscular reflexes,” probably through lowthreshold mechanoreceptors that influence muscle activity via the ␥-muscle spindle system, whereas highThe costs of publication of this article were defrayed in part by the
payment of page charges. The article must therefore be hereby
marked ‘‘advertisement’’ in accordance with 18 U.S.C. Section 1734
solely to indicate this fact.
8750-7587/00 $5.00 Copyright © 2000 the American Physiological Society
2191
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Dyhre-Poulsen, Poul, and Michael R. Krogsgaard.
Muscular reflexes elicited by electrical stimulation of the
anterior cruciate ligament in humans. J Appl Physiol 89:
2191–2195, 2000.—Anterior cruciate ligament (ACL)-deficient knees have impaired proprioception, and, although
mechanoreceptors have been found in the ACL, the existence
of a reflex elicited from these receptors has not been directly
demonstrated in humans. In eight patients that underwent
knee arthroscopy and had no sign of ACL disease, thin wire
electrodes were inserted into the proximal and mid parts of
the ACL. Postoperatively, the sensory nerve fibers inside the
ACL were stimulated electrically while motor activity in the
knee muscles was recorded using electromyography. In seven
of the eight patients, a muscular contraction of the semitendinosus muscle could be elicited with stimulus trains consisting of at least two stimuli. The latency was 95 ⫾ 35 ms.
Stimulation during isometric contraction of either extensor
or flexor muscles elicited a short, complete inhibition of the
muscle activity in the contracting muscles. The latency of the
inhibitory responses was 65 ⫾ 20 ms in the semitendinosus
muscle and 70 ⫾ 15 ms in the rectus femoris muscle.
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CRUCIATE LIGAMENT REFLEXES
METHODS
Eight patients, suspect of a meniscus lesion and admitted
to the Department of Orthopedic Surgery for knee arthroscopy, participated in the study. All subjects had stable knees
on clinical evaluation. None had acute injury. The age and
gender distribution of the participants in the study are
shown in Table 1. In all cases, the cruciate ligaments appeared normal when viewed and probed arthroscopically.
Two 200-␮m, multistranded, Teflon-insulated stainless steel
wires with 3-mm exposed tips were inserted during arthroscopy in the proximal and mid parts of the ACL. Visual control
ensured that the uninsulated tips of the electrodes were
embedded completely inside the ACL. The measurements
were performed 6–8 h after the operation, when the effects of
anesthesia had subsided. Self-adhesive, surface EMG electrodes (Medicotest QA10) were mounted, with an interelectrode distance of 3 cm, over the medial head of the quadriceps
femoris, the rectus femoris, the long head of the biceps
femoris, the semitendinosus, and the medial head of the
gastrocnemius muscles. The recording electrodes were placed
over the midparts of the muscle bellies, and the ground
electrode was placed over the bony part of the tibia. EMG was
preamplified by small amplifiers taped to the skin and then
lead to custom-built amplifiers (amplification 2,000, frequency 20 Hz to 1 kHz, input impedance ⬎100 m⍀, and
CCMR ⬎120 dB). A constant voltage stimulator (DISA Ministim) was used to stimulate the ACL through the implanted
wires. EMG was sampled at 4 kHz by using a standard
personal computer. The sweep started 100 ms before the
stimulus, lasted 600 ms, and was displayed after every stimulus. Each stimulus consisted of a train of 1–8 monopolar
stimuli, with an interstimulus interval of 5 ms. The sensory
threshold, defined as the lowest amplitude at which the
patient could feel the stimulus, was found for a stimulus
train of 4 stimuli. The stimulus amplitude was held constant
at two times the sensory threshold during the experiments.
In all cases, the stimulus amplitude was ⬍10 V. The stimuli
produced a clearly perceived sensation inside the knee, and
subjects reported the feeling as a tap that felt very different
from pain. When the stimulus amplitude was increased to
four times the sensory threshold, the subjects reported a
sensation of pain inside the knee. The number of stimuli in
each stimulus train was constant during the experiments.
Finally, in one subject, we placed stimulus electrodes that
floated freely in the joint fluid anterior to the femoral notch
as a control for the specificity of the responses.
An experimental session consisted, in random order, of 10
sweeps while the knee was fully extended (patient supine
with extended hip), 10 sweeps while the knee was flexed 30°
(patient supine with the knee resting on a splint and with 30°
flexion of hips and knees), and 10 sweeps while it was flexed
90° (patient sitting with hip flexed 90° and the leg hanging
freely). The sessions were then repeated while the patient
maximally activated the knee extensors and then while the
patient maximally activated the knee flexors. The experimenter manually inhibited movements in the knee joint, so
the contractions were isometric. The force was not measured.
Most of the patients felt a slight postoperative pain in the
knee, and, consequently, their maximal effort was limited. In
every position of the knee, at least 5 sweeps were recorded so
that the average of the responses could be calculated after
the experiment. Latency was defined as the time interval
from the second stimulus to the beginning of the muscular
response.
The study was approved by the local ethics committee. The
patients received written and oral information according to
the Helsinki Declaration.
RESULTS
Table 1. Arthroscopic diagnoses and analgesia type
for each patient
Age, yr
Gender
Analgesia Type
24
43
22
29
37
29
M
M
F
M
M
M
spinal
spinal
general anesthesia
general anesthesia
spinal
spinal
28
35
F
M
spinal
general anesthesia
M, male; F, female.
Arthroscopic Findings
medial meniscus lesion
osteochondritis
medial synovial plica
medial meniscus lesion
medial meniscus lesion
lateral/medial meniscus
lesions
subluxation of patella
medial meniscus lesion
Trains of electrical stimuli given to the ACL produced a clearly visible contraction in the hamstrings in
seven of the eight patients who were relaxed and resting supine with the knee flexed 30°. The EMG recordings showed a reflex response latency of 95 ⫾ 35 ms
(mean ⫾ SD) in the semitendinosus muscle (Fig. 1). At
least two stimuli were required to evoke either a visible
muscle contraction or a response in the EMG recordings. The latency did not change when the number of
stimuli was increased. One stimulus never elicited any
response.
When the knee flexors were isometrically activated
voluntarily, the response changed to a total inhibition
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threshold mechanoreceptors may exert effects directly
onto the skeletomotoneurons. However, the existence
of an “ACL reflex” in humans remains uncertain (9). A
major problem in establishing its existence is that it is
not possible to selectively stimulate the sensory receptors in the ACL by mechanical methods because sensory receptors in other ligaments, the capsule, and the
muscles will also be stimulated (23).
ACL injuries occur in young and active patients, and
reconstruction of the torn ligament is often necessary
to gain mechanical stability of the knee. Thus, if nervous activity elicited from the receptors in the ACL
modulates motor activity in knee muscles under normal activities, reconstructions should be approached in
a way that makes reinnervation of the ACL possible,
and rehabilitation programs that reestablish dynamic
knee function should be applied. It is, therefore, of
interest to determine whether an ACL reflex exists in
healthy young people during muscular activity.
The aim of this study was to establish a method to
selectively stimulate the sensory nerves in the ACL in
humans and to record any subsequent changes in the
EMG activity of the muscles around the knee. In the
present study, we implanted stimulus electrodes directly into the ACL under visual control. We selectively
activated the sensory nerve fibers in the ACL with
electrical stimuli and recorded subsequent changes in
EMG activity during rest and during isometric muscle
contractions in knee flexors and extensors.
CRUCIATE LIGAMENT REFLEXES
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elicited with stimulus amplitudes five times higher
than those normally used to elicit the ACL reflex.
DISCUSSION
of the active hamstring muscles in all eight patients
(Fig. 2). The inhibition had a latency of 65 ⫾ 20 ms and
lasted ⬃35 ms. Latency was often followed by a short
burst of activity lasting ⬃30 ms and then another
⬃35-ms silent period before the EMG returned to prestimulus activity. The silent period in the flexor EMG
activity was equivalent to a marked drop in force that
was felt by the investigator providing resistance
against the flexion and was also clearly visible on the
EMG. Similarly, when the subjects were voluntarily
contracting the knee extensor muscles, stimulation of
the ligament produced silent periods in the EMG of
those muscles in all eight subjects (Fig. 3). The latency
was 70 ⫾ 15 ms, and the drop in activity lasted ⬃60
ms. In most cases, the silent period was followed by a
short burst of activity and then another short silent
period. There was a complete inhibition of the gastrocnemius muscle after stimulation under both active
extension and flexion (Figs. 2 and 3). Changing the
position in the knee joint to 0° or 90° influenced neither
the amplitude nor the latency of the EMG responses.
In the subject that had the stimulus electrodes
placed in the joint fluid, no motor responses were
Fig. 2. Averaged, rectified EMGs (n ⫽ 20) recorded from flexor and
extensor muscles of the knee after electrical stimulation of afferent
nerve fibers in the proximal part of the ACL while the patient was
flexing the knee. There was a strong inhibition of the active hamstring muscles (bf and st) and in the gas. Stimulus artifacts are
removed.
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Fig. 1. Electromyogram (EMG) recorded from flexor and extensor
muscles of the knee after electrical stimulation of afferent nerve
fibers inside the proximal part of the anterior cruciate ligament
(ACL) while the patient was at rest. Two stimuli at time 0 elicited a
low-amplitude burst of EMG activity in the semitendinosus muscle
(st) with a latency of 120 ms. Stimulus artifacts are removed. gas,
Gastrocnemius muscle; bf, biceps femoris; rf, rectus femoris; qm,
medial head of quadriceps muscle.
It was observed that activation of afferent nerve
fibers in the proximal part of the ACL influenced the
motor activity in the muscles around the knee in humans. In this model, with electrical stimulation of
sensory nerve fibers of the ligament, it was possible to
demonstrate the existence of an ACL reflex in awake
humans. The low-stimulus amplitudes and the location
of the uninsulated part of the stimulus electrodes inside the ACL made it likely that the stimulation was of
selective nerve fibers within the ACL. The proximal
electrode in the ACL was placed at least 10 mm from
the posterior capsule, and the distal electrode was
placed in the center of the knee. When the stimulus
electrodes were placed in the joint fluid of one subject,
no motor responses were elicited by a stimulus with an
amplitude five times higher than the stimulus that
elicited a reflex from the ACL. It is therefore unlikely
that sensory receptors of the capsule, muscles, or collateral ligaments were activated.
Because the experiments were performed shortly
after surgery and the patients felt postoperative pain,
afferent input from sensitized, group III pain receptors
may have influenced the response (3). However, the
patients did not report pain after the low-amplitude
stimuli used in the present experiments, which indi-
2194
CRUCIATE LIGAMENT REFLEXES
cates that no A␦ or C pain fibers were activated. Therefore, the muscular responses were most likely elicited
by stimulation of group II or III fibers, presumably
mechanoreceptors.
Evidence for both facilitatory and inhibitory influences on the activity in the ␣-motoneurons was found,
depending on the character of the ongoing activity. The
latency of the responses varied between 65 and 95 ms,
indicating that responses were of reflex rather than
voluntary origin. The observation that at least two
stimuli were needed to produce an excitation or inhibition and the rather long latency suggests that the
reflexes were polysynaptic or long-loop reflexes, giving
the central nervous system abundant possibilities to
modulate muscle activity. At rest, impulses elicited in
the ACL produced activation of the hamstring muscles,
supporting the contention of an automatic ACL-hamstring synergy. However, with stimulus amplitudes
two times the sensory threshold, as used in this experiment, this synergy was only present during rest and
changed to an inhibition during motor activity.
Considering a reflex latency of 70 ms, at least 110 ms
(reflex time ⫹ electromechanical delay) would pass
before substantial forces could be produced by the
muscles after application of load to the ACL. Therefore,
the excitatory reflex demonstrated in this study cannot
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Fig. 3. EMG recorded from flexor and extensor muscles of the knee
after electrical stimulation of afferent nerve fibers in the proximal
part of the ACL while the patient held the knee extended. After 100
ms, there was a strong inhibition of the rf and the qm as well as the
gas. Stimulus artifacts are removed.
serve as an automatic protective mechanism for the
ACL. In most situations, this reaction would be too
slow to prevent rupture of the ligament. The long
latency further suggests that direct regulation of force
would be unlikely.
It has been suggested by many authors (3, 4, 12, 24)
that mechanoreceptors in joint capsules and ligaments
contribute to normal coordination of muscle activity in
movements and posture. Johansson et al. (11) showed
that electrical stimulation of joint afferent fibers running in the posterior articular nerve of the cat exert
influence on the activity of the ␥-motoneurons that
project to both the flexors and extensors of the knee.
Thus articular mechanoreceptor reflexes operating via
the ␥-loop may contribute to the regulation of muscle
stiffness and joint stability.
Gómez-Barrena et al. (5) have shown that, in the cat,
afferent impulses from the ACL are directed to lumbar
segments 5–7. These segments correspond to the sciatic and femoral nerves. On the basis of this finding,
Gómez-Barrena and co-workers suggested that afferent impulses from the ACL are important for an optimal balance between the hamstrings (innervated by
the sciatic nerve) and the quadriceps (innervated by
the femoral nerve). We have demonstrated, in this
study, that stimulation of the afferent nerve fibers in
the human ACL induced changes in the hamstrings
and quadriceps muscles.
Experiments in cats present conflicting results regarding a link between afferent nerves from the MCL
and ACL and the muscles around the knee. In some
experiments, such a link could be demonstrated (3, 17,
25), and, in others, it could not be found (1, 6, 23). One
reason for the contrasting findings may be that the
experimental designs differ. In some experiments, the
cats were decerebrated, and, in others, they were also
spinalized (3, 17). In one experiment (23), the cats were
anesthetized with high doses of chloralose, which is
known to influence the excitability of ␣-motoneurons
(18). Notwithstanding the conflicting results from animal studies, it is always hazardous to apply animal
data to humans. However, it was recently shown that
nonnoxious stimulation of the glenohumoral joint capsule in the shoulder of human subjects produces inhibition of ongoing motor activity (27).
The latency of the reflex demonstrated in our experiment was much longer than the latency found by
Solomonow et al. in cats (25). In that study, a short
latency reflex was elicited when the ACL was pulled
with forces that were close to the rupture threshold of
the ligament. These high forces may elicit the sensation of pain and may be equivalent to much higher
stimulus amplitudes than we used in the present
study.
Input from muscle and joint afferents converge with
cutaneous input on the ␣-motoneurons, and reflex reversal that is dependent on motor activity is well
known and described during walking (7). Lundberg et
al. (16) showed that volleys in the posterior articular
nerve in feline knees may facilitate transmission in
both excitatory and inhibitory reflex pathways from Ib
CRUCIATE LIGAMENT REFLEXES
This study was supported by The Danish Research Council for
Sports and The Danish Elite Sport Association.
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afferents and that input from joint afferents may influence tension regulations from Golgi tendon organs.
Instead of a direct protective function, it is more likely
that sensory input plays an important role in the
updating and formation of motor programs (12) that
instruct humans to preactivate the muscles properly
and to protect the knee during the next step. The
maximal motor output in the knee extensors is substantially smaller during static and slow movements
than is expected from the force velocity curve. Therefore, it is suggested that neural mechanisms restrict
the maximal muscle tension (21). Protective reflexes
originating from the knee ligaments may be responsible for this drop in maximal static force. Training
rapidly increases the maximal motor output, and it is
possible that training also modulates the inhibitory
neural feedback (i.e., sensory inputs may help the
neuromuscular system create the patterns of muscular
activity that are the basis for normal movements). The
ACL reflex may, therefore, be an essential part of
normal knee function.
The hamstring muscles are normally regarded as
key to dynamic knee stability. The observed inhibition
of the gastrocnemius muscle after stimulation of the
nerves of the ACL during both active extension and
flexion suggests that this muscle also plays an important role in functional knee stability. Patients with
poor knee function after ACL rupture have an impaired function of the gastrocnemius compared with
patients with good knee function (13). Training of both
the hamstrings and the gastrocnemius muscles functions should be considered in rehabilitation programs.
In this experiment, we have demonstrated that activity in the muscles around the knee is influenced by
sensory input from afferent nerves in the ACL. Further
experiments are needed to characterize this ACL reflex
and to establish its functional significance.
2195