Content uploaded by Bryan L Riemann
Author content
All content in this area was uploaded by Bryan L Riemann
Content may be subject to copyright.
Effect of Peripheral Afferent Alteration
of the Lateral Ankle Ligaments on
Dynamic Stability*
Joseph B. Myers,†‡ PhD, ATC, Bryan L. Riemann,§ PhD, ATC, Ji-Hye Hwang,储MD, PhD,
Freddie H. Fu,† MD, and Scott M. Lephart,† PhD, ATC
From the †Neuromuscular Research Laboratory, Department of Orthopaedic Surgery,
University of Pittsburgh, Pittsburgh, Pennsylvania, the §Graduate Athletic Training Program,
Georgia Southern University, Statesboro, Georgia, and the 储Department of Physical Medicine
and Rehabilitation, Samsung Medical Center, College of Medicine, Sungkyunkwan University,
Seoul, Korea
Background: The sensorimotor influence of the lateral ankle ligaments in muscle activation is unclear.
Hypothesis: The lateral ankle ligaments have significant sensorimotor influence on muscle activation.
Study Design: Controlled laboratory study.
Methods: Muscle-firing characteristics in response to a high-speed inversion perturbation and during gait were assessed in 13
normal subjects. Solutions (1.5% lidocaine or a placebo of saline) were injected bilaterally into the anterior talofibular and
calcaneofibular ligaments (1.5 ml per ligament) to alter peripheral afferent influence. Subjects were again tested with the same
protocol.
Results: The protective response of the anterior tibialis and peroneal muscles during inversion perturbation and mean muscle
activation amplitude decreased during running after both injections. After injection, no significant differences were seen for
muscle reflex latencies, maximum amplitude, time to maximum amplitude during inversion perturbation, or mean amplitude
during walking.
Conclusion: The lateral ankle ligaments have a sensorimotor influence on muscle activation.
Clinical Relevance: Induced edema from the injected solutions may have altered the sensorimotor influence of the lateral ankle
ligaments, thereby inhibiting the dynamic ankle stabilizers. This finding suggests that dynamic stability may be compromised
because of swelling after joint injury.
© 2003 American Orthopaedic Society for Sports Medicine
Much has been written about the mechanical role of the
ligaments that surround the ankle joint in providing ankle
joint stability.
22,30, 34,35,56
The anterior talofibular liga-
ment limits talar tilt throughout sagittal plane motion,
especially with the joint in a position of plantar flex-
ion.
30,56
The calcaneofibular ligament appears to limit
talar tilting in dorsiflexion as well as in talocalcaneal
adduction.
22,34, 35
In addition, embedded within these ligaments are mech-
anoreceptors believed to be responsible for providing a
proprioceptive role in maintaining ankle joint stability.
15
Proprioception, which results from the afferent neural
input originating from mechanoreceptors about the joint,
contributes to dynamic joint stability mechanisms and
coordinated motor patterns.
42
Michelson and Hutchins
50
demonstrated histologically that Ruffini-type, Pacinian
corpuscle type, and Golgi tendon organ receptors are dis-
persed throughout the ankle ligaments, with Pacinian and
Golgi tendon-like organs making up a majority of the
mechanoreceptors present. Johansson and colleagues
27
described how ligamentous mechanoreceptors like these
play a role in providing joint stability that is equally as
important as the purely mechanical role of the ligaments.
By use of traction forces well below those associated with
* Presented at the interim meeting of the AOSSM, Dallas, Texas, February
2002.
‡ Address correspondence and reprint requests to Joseph B. Myers, PhD,
ATC, Neuromuscular Research Laboratory, UPMC Center for Sports Medi-
cine, 3200 South Water Street, Pittsburgh, PA 15213.
No author or related institution has received any financial benefit from
research in this study.
0363-5465/103/3131-0498$02.00/0
THE AMERICAN JOURNAL OF SPORTS MEDICINE, Vol. 31, No. 4
© 2003 American Orthopaedic Society for Sports Medicine
498
tissue damage and nociception, stimulation of the liga-
mentous mechanoreceptors has been demonstrated to
have potent effects on sensitivity and activation of the
gamma motor neurons associated with the muscle spin-
dle.
27,28, 51,57,63
These potent effects provide significant
contributions to muscle stiffness, motor control, and re-
flexive characteristics.
28,29
Except for temporal assess-
ment of reflex latencies,
8,13, 24,31,33, 37–39,44,47
no research
has specifically measured the contribution of ankle liga-
ment mechanoreceptors to muscle-firing characteristics
associated with joint stability. It is feasible that the influ-
ence of these mechanoreceptors on muscle-firing charac-
teristics may have nontemporal implications, such as am-
plitude of muscle activation, which may be overlooked in
temporal (latency) assessments.
The peripheral afferent contribution of ligamentous
mechanoreceptors on neuromuscular mechanisms, such
as muscle-firing characteristics, has been measured by
using anesthesia to block them. Feuerbach et al.
14
injected
lateral ankle ligaments with an anesthetic to block periph-
eral afferent influence, thereby determining the role that
ligaments play in supplying joint proprioception. Both
Hertel et al.
20
and DeCarlo and Talbot
9
injected an anes-
thetic into the lateral ankle ligaments to ascertain the role
of peripheral afferent information from these ligaments in
postural control tasks. Thus far, two groups have exam-
ined muscle reflex latencies of dynamic restraints after
injection into lateral ankle ligaments; both failed to reveal
significant latency changes in healthy subjects.
33,39
How-
ever, because of the influence of ligamentous mechanore-
ceptors on gamma reflex loops,
27,28, 51,57,63
it is plausible
that they mediate other characteristics of the response; to
date, no research has considered this possibility. Further-
more, we are unaware of any research that has examined
the influence of the lateral ankle ligaments on muscle-
firing characteristics during dynamic tasks such as walk-
ing and running. The purpose of this study was to evalu-
ate the role of peripheral afferent information from the
lateral ankle ligaments in spatial and temporal muscle
activation characteristics during an inversion perturba-
tion and during dynamic gait tasks such as walking and
running.
METHODS
Thirteen subjects (seven men, 24.7 ⫾4.2 years of age with
a height of 180.1 ⫾6.1 cm and mass of 78.8 ⫾6.8 kg; and
six women, 22.3 ⫾0.95 years of age with a height of
162.6 ⫾6.8 cm and mass of 62.3 ⫾5.2 kg) participated in
this study. All subjects were right-leg dominant (opera-
tionally defined as the foot the subject would use to kick a
ball) and had no significant history of lower extremity
injury. Informed consent was obtained before participa-
tion, in accordance with the requirements of the Univer-
sity of Pittsburgh Institutional Review Board. Each sub-
ject attended two testing sessions at least 48 hours apart.
A pretest-posttest research design was used during each
session.
Instrumentation
The ankle inversion perturbation device is a specially
designed platform that allows the ankle joint to drop from
a neutral position into 30° of inversion while the subject is
standing (Fig. 1). Both right and left plates of the platform
are connected to two tension springs that pull each plate
down into 30° of inversion at an average angular velocity
of 440 deg/sec. The plates are held level by spring plungers
connected to two independent levels that release each
plate independently when triggered, inducing the inver-
sion perturbation. Each plate is fitted with a 2g acceler-
ometer (Newh Ghant Technologies, LaGrangeville, New
York) to signal onset of platform drop. The inversion
plates are positioned over a Bertec forceplate (Model
#K80801, Type 4060–10, Bertec Corporation, Columbus,
Ohio) to ensure equal weight distribution between limbs
at the time of perturbation. Pilot testing of the device to
establish reliability for measurement of muscle-firing
characteristics was performed on 15 subjects and yielded
intraclass correlation coefficients (2,1) ranging from 0.71
to 0.76, with standard error of measurement of 6.1 to 8.2
msec calculated according to Denegar and Bell
11
and
Shrout and Fleiss.
60
Electromyographic Instrumentation and Preparation
Electromyographic data were collected with the Noraxon
Telemyo (Noraxon, Scottsdale, Arizona) EMG system, a
Figure 1. A subject positioned on the ankle inversion per-
turbation device.
Vol. 31, No. 4, 2003 Sensorimotor Influence of the Lateral Ankle Ligaments 499
frequency modulated (FM) telemetry system. Electromyo-
graphic signals collected from the electrodes were passed
through a single-ended amplifier (gain 500) to an eight-
channel FM transmitter. A receiver unit obtained the
telemetry signals from the transmitter, where the receiver
amplified (gain 500) and filtered (15 Hz low-pass, 500 Hz
high-pass Butterworth filter, common mode rejection ratio
of 130 db) the signals. Signals from the EMG receiver,
force plate, and acceleration were converted from analog
to digital data via a PCM16S/12 (16-channel, 12-bit) ana-
log-to-digital board (ComputerBoards, Inc., Middleboro,
Massachusetts) at a rate of 1000 Hz. The digital data were
collected and stored with Myoresearch 2.02 (Noraxon) on a
personal computer for later data reduction.
Silver-silver chloride surface electrodes (Medicotest,
Inc., Rolling Meadows, Illinois) were used for meas-
urement of muscle activity. Skin preparation to lower
impedance included shaving any hair present, mild abra-
sion with a low-abrasive emery board, and wiping the area
with 70% isopropyl alcohol. A ground electrode was placed
just distal to the tibial tuberosity, and two surface elec-
trodes were placed side by side and perpendicular to the
orientation of the anterior tibialis, peroneus longus, and
peroneus brevis muscle fibers, with 2 cm separating their
centers.
6,10
The same investigator applied electrodes on
all subjects during all sessions to control for intertester
variability. The peroneal muscles were chosen because of
their everter function, reported activity during the stance
phase of gait when the ankle is at risk of injury, and for
the role they play in dynamic balance during gait tasks.
46
The anterior tibialis muscle was chosen because of its
function as an antagonist to the peroneal muscles.
46
Cor-
rect position of all electrodes was confirmed through iso-
lated manual muscle tests of each muscle.
6
Komi and
Buskirk
36
established the reliability of surface electrode
EMG as 0.88 to 0.91 intraclass correlation coefficient
within sessions and 0.64 to 0.73 intraclass correlation
coefficient between testing sessions.
Stance and swing phases of the walking and running
tasks were identified with the NorSwitch (Noraxon) foot
switch system, which uses pressure-sensitive resistors
that output consistent voltage to signal gait events. The
pressure-sensitive foot switches were secured to the cal-
caneus and to the first ray on the plantar surface of the
foot.
Testing Procedures
Once informed consent and EMG preparation was com-
pleted, each subject was oriented to the testing proce-
dures. For inversion perturbation testing, all subjects
were asked to stand barefoot on the platform with the
second ray of both feet aligned with the axis of rotation of
the plates and with their hands placed on their hips.
Subjects were asked to wear a blindfold and a headphone
set emitting white noise to negate visual and auditory
cues. Before the start of the inversion trials, the subjects
were asked to maintain a quiet stance on the platform for
a period of 12 seconds. During that time, center of pres-
sure and EMG activity were assessed. Immediately after
the quiet stance, 12 randomized pretest inversion trials (6
trials per limb) were performed. Subjects were unaware of
which platform would drop for each trial. These pretest
trials served as control trials for comparison of muscle
activity before and after injection of the solution.
During the dynamic gait activities, subjects were asked
to walk and run barefoot on a treadmill (Biodex Treadmill,
Biodex Medical, Shirley, New York) (Fig. 2). Treadmill
speeds were standardized at 3.2 km/hr and 7.6 km/hr for
walking and running, respectively. Subjects were in-
structed to walk and run using their normal gait mechan-
ics. The subjects were not allowed to touch the handrails
of the treadmill to eliminate the influence that external
support has on muscle-firing patterns during gait.
46
Sub-
jects were given ample time for familiarization with the
treadmill and speed of movement before trial recording.
Once the standardized speed was obtained and the subject
indicated that a fluid gait pattern was achieved, EMG and
foot switch recording was initiated. Recording of the EMG
and foot switch signals continued until at least 20 strides
were completed, allowing for analysis of 12 strides for all
trials. A review of the literature indicated that at least six
strides are needed to obtain a representative EMG profile
during gait activity.
4,59, 73
Immediately after pretesting, a physician injected ei-
ther 1% preservative-free lidocaine HCl (Astra USA, Inc.,
Westborough, Massachusetts) or a placebo solution (pre-
servative-free 0.9% sodium chloride, Abbott Laboratories,
North Chicago, Illinois) with a 25-gauge
5
⁄
8
-inch syringe
into both the anterior talofibular and calcaneofibular lig-
ament regions (1.5 ml for each site) of each ankle (Fig.
3).
14,20
Subjects, who were blinded as to which solution
was being injected, were asked to remain inactive for 20
minutes after injection to allow for induction of the anes-
thetic effects. Subjects were again tested with identical
inversion perturbation and treadmill protocols. Testing
protocols were alternated within testing sessions. Subjects
returned for a second session at least 48 hours after the
initial session and were tested with identical procedures
but were injected with the other solution.
Figure 2. Assessment of muscle activity during dynamic ac-
tivities on the treadmill.
500 Myers et al. American Journal of Sports Medicine
Data Reduction
Inversion Perturbation. Because limb dominance has
been demonstrated to cause differences between limbs,
only the dominant limb was analyzed.
13,24
This decision
was justified because the purpose of the investigation was
not to measure bilateral differences but to measure
changes after peripheral afferent alteration, which can be
accomplished by making comparisons within the same
limb. Subjects were unaware that only the data from the
dominant limb would be considered. Accelerometer, EMG,
and force plate data were exported and conditioned with
LabVIEW 5.1 customized software (National Instruments,
Austin, Texas). Force and moment data obtained by the
force plate and accelerometer were filtered with a 10-Hz
cutoff, fourth-order zero-phase lag Butterworth filter.
70
Trial EMG data were rectified, filtered (20 to 500 Hz
bandpass fourth-order zero-phase lag Butterworth filter),
and normalized to the mean amplitude of a rectified fil-
tered linear envelope for each respective muscle during
the quiet stance trial.
67
Perturbation onset and muscle-firing characteristics
were calculated with customized software written in Vi-
sual Basic for Applications (Microsoft, Redmond, Wash-
ington). Perturbation onset was determined by using the
acceleration data. Muscle activation onset was ascer-
tained by using a similar algorithm of five standard devi-
ations above baseline activity 150 msec before perturba-
tion.
24
This method of determining onset has been proven
reliable.
24
The customized software allowed user interac-
tion so that a reviewer could subjectively accept or reject
data that contained nonphysiologic activity, similar to the
method described by Di Fabio
12
and Lynch et al.
47
The customized software calculated the maximum ampli-
tude, defined as the maximum amplitude of EMG activity
within 100 msec after muscle onset. Time to maximum am-
plitude was defined as the time from perturbation onset to
maximum amplitude. The protective response, the mean am-
plitude of the window from muscle activity onset to 100 msec
after onset, was calculated.
44
Figure 4 illustrates the meas-
ured muscle-firing characteristics.
Center-of-pressure standard deviation in the mediolat-
eral direction was calculated from the force and moment
data and compared with the center of pressure for both the
quiet stance and the window from 150
sec before pertur-
bation to perturbation onset to avoid unequal limb loading
due to subject anticipation. Any deviation in the center of
pressure three times that during quiet stance indicated
that unequal weight distribution occurred, invalidating
that trial. Invalid trials were discarded.
Muscle Activity during Gait. Raw EMG signals for all
muscles were both rectified and second-order low-pass
Butterworth filtered (6 Hz cutoff).
71
Stance and swing
phases of the walking and running tasks were visually
identified by the foot switch signals within the Myore-
search software. Twelve complete gait cycles were estab-
Figure 3. Injection into the anterior talofibular (A) and calca-
neofibular (B) ligaments.
Figure 4. Muscle reflex characteristics. A, ankle perturba-
tion onset; B, muscle reflex onset; C, muscle reflex latency;
D, maximum amplitude; E, time to maximum amplitude; and
F, muscle protective response.
Vol. 31, No. 4, 2003 Sensorimotor Influence of the Lateral Ankle Ligaments 501
lished for analysis and were normalized to both time and
mean amplitude for the gait cycle for establishment of a
linear envelope.
73
The mean amplitude for both stance
and swing phases was used for statistical analysis.
Statistical Analysis
Statistical analysis for each dependent variable consisted
of separate (two within and one between) repeated-meas-
ures analysis of variance models. The within factors were
test (pretest versus posttest) and muscle (anterior tibialis,
peroneus longus, and peroneus brevis), and the between
factor was treatment (placebo versus anesthetic). Al-
though each subject received both anesthesia and placebo
treatments, the weak reliability of between-session com-
parisons for surface EMG results demonstrated in the
literature warranted analyzing the two treatments as a
between factor rather than a within factor in the analysis
of variance model.
36
A Tukey post hoc analysis was used
for pairwise comparisons of significant results (P⬍0.05)
RESULTS
Inversion Perturbation Reflex Characteristics
The descriptive statistics for muscle latency, maximum
amplitude, time to maximum amplitude, and protective
muscle response appear in Tables 1 to 4, respectively.
Statistical analysis revealed no significant difference
within or between factors for muscle latency, maximum
amplitude, and time to maximum amplitude. A test main
effect (F[1,24] ⫽11.10, P⫽0.03) did manifest for the
protective muscle response. These results indicated sup-
pressed muscle activity after injection of either solution
into the lateral ankle ligaments (Fig. 5).
Dynamic Activity Muscle-Firing Characteristics
The descriptive statistics for mean amplitudes of each mus-
cle during both the stance and swing phase while walking
and running appear in Tables 5 and 6. For analysis of the
gait data, separate repeated-measures analysis of variance
models demonstrated decreased mean amplitude of the per-
TABLE 1
Muscle Reflex Latency in Milliseconds (Mean ⫾SD)
Muscle
Anesthesia Placebo
Pretest Posttest Pretest Posttest
Anterior tibialis 87.92 ⫾15.21 94.26 ⫾15.71 98.20 ⫾19.66 91.59 ⫾15.05
Peroneus longus 88.92 ⫾9.95 89.94 ⫾7.38 89.61 ⫾15.40 90.04 ⫾15.43
Peroneus brevis 81.38 ⫾8.79 83.39 ⫾10.06 84.78 ⫾14.20 85.36 ⫾12.09
TABLE 2
Maximum Muscle Ampitude
a
(Mean ⫾SD)
Muscle
Anesthesia Placebo
Pretest Posttest Pretest Posttest
Anterior tibialis 49.29 ⫾43.59 34.54 ⫾31.55 48.04 ⫾46.17 45.54 ⫾34.26
Peroneus longus 36.00 ⫾23.47 41.53 ⫾19.22 49.66 ⫾37.04 47.18 ⫾34.28
Peroneus brevis 43.19 ⫾21.70 43.77 ⫾17.37 41.62 ⫾15.29 41.73 ⫾18.09
a
Muscle amplitudes are normalized to quiet stance and listed as a percentage of quiet stance EMG amplitude.
TABLE 3
Time to Maximum Muscle Amplitude in Milliseconds (Mean ⫾SD)
Muscle
Anesthesia Placebo
Pretest Posttest Pretest Posttest
Anterior tibialis 118.94 ⫾22.7 117.05 ⫾23.3 126.39 ⫾24.2 118.71 ⫾19.7
Peroneus longus 105.21 ⫾14.5 107.02 ⫾14.0 109.34 ⫾20.1 107.41 ⫾15.3
Peroneus brevis 111.37 ⫾14.9 113.97 ⫾19.5 115.10 ⫾22.7 113.08 ⫾16.2
TABLE 4
Normalized Muscle Protective Response
a
(Mean ⫾SD)
Muscle
Anesthesia Placebo
Pretest Posttest Pretest Posttest
Anterior tibialis 31.99 ⫾18.31 25.64 ⫾20.36 31.16 ⫾22.53 28.83 ⫾21.72
Peroneus longus 29.56 ⫾17.60 25.24 ⫾13.85 24.87 ⫾13.15 21.49 ⫾11.67
Peroneus brevis 28.80 ⫾17.13 26.14 ⫾17.62 24.14 ⫾13.39 23.18 ⫾13.96
a
Muscle amplitudes are normalized to quiet stance and listed as a percentage of quiet stance EMG amplitude.
502 Myers et al. American Journal of Sports Medicine
oneus longus muscle during the swing phase of walking
(F[1,24] ⫽6.10, P⫽0.021), the anterior tibialis muscle
during the swing phase of running (F[1,24] ⫽5.33, P⫽0.03),
and the peroneus longus (F[1,24] ⫽8.07, P⫽0.009) and
peroneus brevis muscles (F[1,24] ⫽10.62, P⫽0.003) during
the stance phase of running between pretest and posttest
(Fig. 6). No significant differences existed between the lido-
caine and placebo solution conditions.
DISCUSSION
The mechanical role of the anterior talofibular and calca-
neofibular ligaments on ankle joint stability has been
established.
22,30, 34, 35,56
It is believed that lateral ankle
ligament injury results in not only mechanical instabili-
ty
40,58
but also ligamentous deafferentation, contributing
to instability.
15,38, 66
Unfortunately, the sensorimotor in-
fluence of the lateral ankle ligaments is not completely
understood. The purpose of this study was to gain a better
understanding of their sensorimotor role through alter-
ation of the peripheral afferent influence that these liga-
ments may have on muscle-firing characteristics by using
a previously described lidocaine model.
9,14, 20, 33,39
Activi-
ties that resemble the mechanism of lateral ankle liga-
ment injuries (inversion perturbation) and the type of
activities that are performed when these injuries are sus-
tained (dynamic activities like running) were chosen to
assess these sensorimotor influences.
Inversion Perturbation Muscle Reflex Characteristics
It was predicted that peripheral afferent alteration of the
lateral ankle ligaments with lidocaine would influence the
muscle reflex characteristics of the dynamic stabilizers of
the ankle joint. Results from this study indicated that this
was not the case. Similar to previous reports,
33,39
periph-
Figure 6. Mean EMG amplitude during running. *, signifi-
cantly different from pretest amplitudes.
TABLE 5
Muscle Amplitude
a
during Treadmill Walking (Mean ⫾SD)
Muscle
Anesthesia Placebo
Pretest Posttest Pretest Posttest
Stance phase
Anterior tibialis 79.66 ⫾10.42 76.67 ⫾21.19 70.81 ⫾11.15 72.70 ⫾18.90
Peroneus longus 115.77 ⫾10.42 103.65 ⫾23.00 115.29 ⫾15.20 115.02 ⫾42.04
Peroneus brevis 109.57 ⫾10.95 100.11 ⫾17.99 114.52 ⫾12.60 107.40 ⫾35.16
Swing phase
Anterior tibialis 148.15 ⫾20.94 135.46 ⫾31.43 154.69 ⫾18.51 154.94 ⫾34.01
Peroneus longus 59.78 ⫾26.31 53.95 ⫾33.23 72.54 ⫾26.40 62.80 ⫾31.39
Peroneus brevis 61.01 ⫾18.00 82.02 ⫾49.48 72.58 ⫾22.85 68.93 ⫾24.86
a
Values expressed as percentage of the mean activity over the entire gait cycle.
TABLE 6
Muscle Amplitude
a
during Treadmill Running (Mean ⫾SD)
Muscle
Anesthesia Placebo
Pretest Posttest Pretest Posttest
Stance phase
Anterior tibialis 78.79 ⫾10.64 67.97 ⫾19.48 67.41 ⫾15.66 71.85 ⫾23.44
Peroneus longus 150.81 ⫾20.47 129.01 ⫾27.83 139.65 ⫾24.30 132.93 ⫾40.73
Peroneus brevis 142.33 ⫾22.92 127.45 ⫾42.80 153.89 ⫾31.65 131.34 ⫾24.59
Swing phase
Anterior tibialis 120.30 ⫾10.61 108.29 ⫾32.71 128.84 ⫾13.54 121.06 ⫾24.10
Peroneus longus 51.92 ⫾16.41 48.70 ⫾23.57 63.69 ⫾22.06 53.20 ⫾18.72
Peroneus brevis 61.01 ⫾18.00 57.84 ⫾28.86 55.96 ⫾17.28 53.44 ⫾16.80
a
Values expressed as percentage of the mean activity over the entire gait cycle.
Figure 5. Muscle reflex protective response. *, significantly
different from pretest mean amplitude.
Vol. 31, No. 4, 2003 Sensorimotor Influence of the Lateral Ankle Ligaments 503
eral afferent alteration with a lidocaine model had no
significant effect on muscle reflex latencies. Unlike these
previous investigations, however, this study also included
measurement of reflex amplitude characteristics (maxi-
mum amplitude and protective mechanism) after periph-
eral afferent alteration. Again, however, lidocaine injec-
tion had no significantly different effect compared with
that of the placebo solution.
A test main effect was present for the protective mech-
anism measured. This result demonstrated that injection
of a solution (independent of which solution was injected)
caused decreased muscle-firing amplitude over a 100-
msec period after muscle onset (Fig. 5). Because the re-
sults were independent of which solution was injected, a
mechanism other than anesthesia was most likely respon-
sible. Injection of solution into the ligament region possi-
bly induced artificial swelling similar to that seen with
injury. Unfortunately, we are unaware of any published
data assessing the effects of edema and joint effusion on
muscle-firing characteristics at the ankle joint. The effects
of joint effusion, whether through joint injury or injection
of saline solution, on muscle-firing characteristics have
been reported at the knee, however. Knee joint effusion
has been shown to have potent inhibitory effects on mo-
toneuron pool recruitment, strength, and muscle activity
of the quadriceps muscle.
23,25, 32, 64,65
As with reported
results in the knee, injection of fluid into the ankle joint
may inhibit the musculature that surrounds the ankle.
The question exists as to why both the lidocaine and the
placebo saline solution would have an inhibitory effect on
muscle-firing characteristics. Spencer et al.
64
demon-
strated that injection of saline solution into the knee joint
had inhibitory effects on the quadriceps muscle, but the
addition of lidocaine to the knee joint curbed the quadri-
ceps muscle inhibitory effects. In contrast, Agostinucci
1
reported no difference in soleus muscle motoneuron excit-
ability between anesthetic and placebo conditions. Any
suspected differences between the lidocaine and placebo
conditions, like those in the knee, may be less pronounced
in the ankle because type I Ruffini receptors are most
likely responsible for the inhibitory response associated
with joint pressure,
64
and there is a lack of Ruffini recep-
tors compared with type II and type III receptors in the
ankle ligaments and joint capsule.
50,72
Another causative
factor for suppressed muscle activity for both conditions
might have been the insertion of the needle, but data
presented by Jensen and Graf
26
demonstrated that the
insertion of a catheter had no effect on quadriceps muscle
inhibition, as measured by isokinetic strength. More re-
search is needed to examine the influence of edema on
reflex muscle-firing characteristics about the ankle joint
as well as the role that anesthesia plays in affecting these
characteristics.
Dynamic Gait Muscle-Firing Characteristics
Similar results were seen from the analysis of muscle
activity during the walking and running tasks. No differ-
ences between solutions existed within muscles before and
after injection of solution during the stance or swing
phases of both walking and running activities. Test main
effects were also present, indicating decreased muscle am-
plitude after injection of solution (independent of which
solution was injected). During running trials, the mean
amplitude of peroneal muscles decreased during the
stance phase of running and the anterior tibialis muscle
mean amplitude was depressed during the swing phase
(Fig. 6). Peroneus longus muscle activity also decreased
during the swing phase of walking.
Comparison of the dynamic activity data was difficult,
given the lack of published data examining the influential
role that lateral ankle ligaments play on muscle-firing
characteristics during dynamic gait activities. Again,
some references can be made to the research about the
knee. The results indicate decreased muscle activity dur-
ing gait after injection of solution. The existence of some
induced edema may have influenced the muscle activity.
Torry et al.
65
demonstrated quadriceps muscle activity
from artificially induced knee joint effusion during gait
activities that contributed to a quadriceps muscle avoid-
ance gait pattern. Similar to the suppressed muscle activ-
ity at the knee resulting from induced joint effusion, ankle
muscle-firing characteristics may have been altered with
the induction of solution into the lateral ankle ligament,
inducing edema accumulation similar to that with injury.
Clinical Significance
Interpretation of these results suggests that the injection
of solution (independent of which solution was injected)
resulted in suppressed muscle activity both during inver-
sion perturbation and dynamic activities. The accumula-
tion of fluid within the lateral ankle, similar to the edema
formation that exists with ankle injury, would suggest
that not only is mechanical stability compromised because
of the ligamentous trauma, but dynamic stability mecha-
nisms may also be affected. The suppressed activity may
compromise dynamic stability during the weightbearing
position during dynamic activities when the ankle is vul-
nerable to injury.
16
The consequence of this suppressed activity by the per-
oneal muscles is the decreased intrinsic stiffness that
exists at the ankle joint. Intrinsic stiffness is obtained
from mechanical properties of both muscle and passive
components about the joint.
17,53
Intrinsic stiffness is
strongly influenced by the level of muscle contraction
present.
69
As muscle contraction increases, stiffness also
increases.
7,45, 48, 52,54, 68,74
Muscle contraction creates sta-
ble crossbridges that resist stretch
18
while assisting with
the storage of muscle energy.
5
Intrinsic stiffness provides
the first line of defense for joint stability when force is
applied to the joint.
2,3, 7, 49,61, 62
Intrinsic stiffness pro-
vides an immediate and substantial response to perturba-
tion.
43
Therefore, when some type of injury inversion
mechanism occurs, the dynamic restraints system will be
less likely to prevent the perturbing force from injuring
the ankle joint when muscle activity is suppressed.
The suppressed activity of the ankle dynamic stabilizers
during inversion perturbation is also problematic. When a
destabilizing event like an inversion mechanism does oc-
504 Myers et al. American Journal of Sports Medicine
cur, the magnitude of the muscular response, as measured
by the 100-msec protective response,
44
to protect the ankle
may also compromise joint stability. Some authors sug-
gest that joint injury, such as that associated with an
inversion mechanism, happens too fast for the reflex ac-
tivity and accompanying force production to stiffen the
joint to prevent the injurious mechanisms.
19,41, 49, 55,61, 62
This hypothesis suggests that reflexive activity plays less
of a role than does the intrinsic stiffness associated with
joint stability. More research is needed on the role that
reflexive activity plays in providing joint stability.
Because the injection of either solution elicited a change
in muscle activity, rather than lidocaine as compared with
placebo, as hypothesized, more research is needed to de-
termine whether the resulting edema had an effect on
muscle-firing characteristics during both the dynamic gait
and inversion perturbation activities. In addition, in vivo
models are needed in which the proprioceptive role of
ankle ligaments in joint stability can be examined, given
that joint deafferentation is often described as a contrib-
utor to functional instability and “giving way”epi-
sodes.
15,21, 38, 66
It may be that the proprioceptive influ-
ence of the ankle ligaments contributes more to joint
position awareness and postural control capabilities
rather than to muscle-firing patterns.
CONCLUSIONS
The results of this study failed to demonstrate differences
in muscle-firing characteristic between lidocaine and pla-
cebo treatment for both dynamic gait activities and during
inversion perturbation. The results do indicate that the
lateral ankle ligaments play a sensorimotor role as evi-
denced by the muscle suppression that manifested after
the solution injection. Suppressed muscle activity was
demonstrated by decreased muscle-firing amplitude dur-
ing the stance and swing phases of gait activities and the
reflexive response of the ankle dynamic stabilizers. Clin-
ically, this result suggests that dynamic stability may be
compromised due to swelling after joint injury or injection
of fluid.
REFERENCES
1. Agostinucci J: The effects of topical anesthetics on skin sensation and
soleus motoneuron reflex excitability. Arch Phys Med Rehabil 75: 1233–
1240, 1994
2. Akazawa K, Aldridge JW, Steeves JD, et al: Modulation of stretch reflexes
during locomotion in the mesencephalic cat. J Physiol 329: 553–567, 1982
3. Akazawa K, Milner TE, Stein RB: Modulation of reflex EMG and stiffness
in response to stretch of human finger muscle. J Neurophysiol 49: 16–27,
1983
4. Arsenault AB, Winter DA, Marteniuk RG: Is there a “normal”profile of
EMG activity in gait? Med Biol Eng Comput 24: 337–343, 1986
5. Asmussen S, Bonde-Petersen F: Storage of elastic energy in skeletal
muscles in man. Acta Physiol Scand 91: 385–392, 1974
6. Basmajian JV, Blumenstein R: Electrode placement in electromyographic
biofeedback, in Basmajian JV (ed): Biofeedback: Principles and Practice
for Clinicians. Third edition. Baltimore, Williams & Wilkins, 1989, pp
369–382
7. Blanpied P, Smidt GL: Human plantarflexor stiffness to multiple single-
stretch trials. J Biomech 25: 29–39, 1992
8. Brunt D, Andersen JC, Huntsman B, et al: Postural responses to lateral
perturbation in healthy subjects and ankle sprain patients. Med Sci Sports
Exerc 24: 171–176, 1992
9. DeCarlo MS, Talbot RW: Evaluation of ankle proprioception following
injection of the anterior talofibular ligament. J Orthop Sports Phys Ther 8:
70–76, 1986
10. DeLuca CJ: The use of surface electromyography in biomechanics. J Appl
Biomech 13: 135–163, 1997
11. Denegar CR, Bell DW: Assessing reliability and precision of meas-
urement: An introduction to intraclass correlation and standard error of
measurement. J Sport Rehabil 2: 35–42, 1993
12. Di Fabio RP: Reliability of computerized surface electromyography for
determining the onset of muscle activity. Phys Ther 67: 43–48, 1987
13. Fernandes N, Allison GT, Hopper D: Peroneal latency in normal and
injured ankles at varying angles of perturbation. Clin Orthop 375: 193–
201, 2000
14. Feuerbach JW, Grabiner MD, Koh TJ, et al: Effect of an ankle orthosis and
ankle ligament anesthesia on ankle joint proprioception. Am J Sports Med
22: 223–229, 1994
15. Freeman MA: Instability of the foot after injuries to the lateral ligament of
the ankle. J Bone Joint Surg 47B: 669–677, 1965
16. Garrick JG: The frequency of injury, mechanism of injury, and the epide-
miology of ankle sprains. Am J Sports Med 5: 241–242, 1977
17. Gottlieb GL, Agarwal GC: Dependence of human ankle compliance on
joint angle. J Biomech 11: 177–181, 1978
18. Gregory JE, Morgan DL, Proske U: Changes in size of the stretch reflex of
cat and man attributed to aftereffects in muscle spindles. J Neurophysiol
58: 628–640, 1987
19. Grillner S: The role of muscle stiffness in meeting the changing postural
and locomotor requirements for force development by the ankle exten-
sors. Acta Physiol Scand 86: 92–108, 1972
20. Hertel J, Guskiewicz KM, Kahler DM, et al: Effect of lateral ankle joint
anesthesia on center of balance, postural sway, and joint position sense.
J Sport Rehabil 5: 111–119, 1996
21. Hintermann B: Biomechanics of the unstable ankle and clinical implica-
tions. Med Sci Sports Exer 31(Suppl 7): S459–S469, 1999
22. Hollis JM, Blasier RD, Flahiff CM: Simulated lateral ankle ligamentous
injury: Changes in ankle stability. Am J Sports Med 23: 672–677, 1995
23. Hopkins JT, Ingersoll CD, Krause BA, et al: Effect of knee joint effusion on
quadriceps and soleus motoneuron pool excitability. Med Sci Sports Exerc
33: 123–126, 2001
24. Hopper D, Allison G, Fernandes N, et al: Reliability of the peroneal latency
in normal ankles. Clin Orthop 350: 159–165, 1998
25. Iles JF, Stokes M, Young A: Reflex actions of knee joint afferents during
contraction of the human quadriceps. Clin Physiol 10: 489–500, 1990
26. Jensen K, Graf BK: The effects of knee effusion on quadriceps strength
and knee intraarticular pressure. Arthroscopy 9: 52–56, 1993
27. Johansson H, Sjolander P, Sojka P: A sensory role for the cruciate
ligaments. Clin Orthop 268: 161–178, 1991
28. Johansson H, Sjolander P, Sojka P: Reflex actions on the gamma muscle
spindle systems of muscle activity at the knee joint elicited by stretch of
the posterior cruciate ligament. Neuro-Orthop 8: 9–21, 1989
29. Johansson H, Sojka P: Action on gamma-motoneurones elicited by elec-
trical stimulation of cutaneous afferent fibres in the hind limb of the cat.
J Physiol 366: 343–363, 1985
30. Johnson EE, Markolf KL: The contribution of the anterior talofibular liga-
ment to ankle laxity. J Bone Joint Surg 65A: 81–88, 1983
31. Johnson MB, Johnson CL: Electromyographic response of peroneal mus-
cles in surgical and nonsurgical injured ankles during sudden inversion.
J Orthop Sports Phys Ther 18: 497–501, 1993
32. Kennedy JC, Alexander IJ, Hayes KC: Nerve supply of the human knee
and its functional importance. Am J Sports Med 10: 329–335, 1982
33. Khin-Myo-Hla, Ishii T, Sakane M, et al: Effect of anesthesia of the sinus
tarsi on peroneal reaction time in patients with functional instability of the
ankle. Foot Ankle Int 20: 554–559, 1999
34. Kjaersgaard-Andersen P, Wetheland JO, Helmig P, et al: Effect of the
calcaneofibular ligament on hindfoot rotation in amputation specimens.
Acta Orthop Scand 58: 135–138, 1987
35. Kjaersgaard-Andersen PL, Wetheland JO, Nielsen S: Lateral talocalca-
neal instability following section of the calcaneofibular ligament: A kinesi-
ologic study. Foot Ankle 7: 355–361, 1987
36. Komi PV, Buskirk ER: Reproducibility of electromyographic meas-
urements with inserted wire electrodes and surface electrodes. Electro-
myography 10: 357–367, 1970
37. Konradsen L, Ravn JB: Prolonged peroneal reaction time in ankle insta-
bility. Int J Sports Med 12: 290–292, 1991
38. Konradsen L, Ravn JB: Ankle instability caused by prolonged peroneal
reaction time. Acta Orthop Scand 61: 388–390, 1990
39. Konradsen L, Ravn JB, Sorensen AI: Proprioception at the ankle: The
effect of anaesthetic blockade of ligament receptors. J Bone Joint Surg
75B: 433–436, 1993
40. Larsen E: Experimental instability of the ankle. A radiographic investiga-
tion. Clin Orthop 204: 193–200, 1986
Vol. 31, No. 4, 2003 Sensorimotor Influence of the Lateral Ankle Ligaments 505
41. Latimer HA, Tibone JE, Pink MM, et al: Shoulder reaction time and
muscle-firing patterns in response to an anterior translation force. J Shoul-
der Elbow Surg 7: 610–615, 1998
42. Lephart SM, Riemann BL, Fu FH: Introduction to the sensorimotor system,
in Lephart SM, Fu FH (eds): Proprioception and Neuromuscular Control in
Joint Stability. Champaign, IL, Human Kinetics, 2000, pp xvii-xxiv
43. Loeb GE, Brown IE, Cheng EJ: A hierarchical foundation for models of
sensorimotor control. Exp Brain Res 126(1): 1–18, 1999
44. Lohrer H, Alt W, Gollhofer A: Neuromuscular properties and functional
aspects of taped ankles. Am J Sports Med 27: 69–75, 1999
45. Louie J, Mote CD Jr: Contribution of the musculature to rotatory laxity and
torsional stiffness at the knee. J Biomech 20: 281–300, 1987
46. Louwerens JWK, van Linge B, de Klerk LW, et al: Peroneus longus and
tibialis anterior muscle activity in the stance phase. A quantified electro-
myographic study of 10 controls and 25 patients with chronic ankle insta-
bility. Acta Orthop Scand 66: 517–523, 1995
47. Lynch SA, Eklund U, Gottlieb D, et al: Electromyographic latency changes
in the ankle musculature during inversion moments. Am J Sports Med 24:
362–369, 1996
48. Ma SP, Zahalak GI: The mechanical response of the active human triceps
brachii to very rapid stretch and shortening. J Biomech 18: 585–598, 1985
49. McNair PJ, Wood GA, Marshall RN: Stiffness of the hamstring muscles
and its relationship to function in anterior cruciate deficient individuals.
Clin Biomech 7: 131–137, 1992
50. Michelson JD, Hutchins C: Mechanoreceptors in human ankle ligaments.
J Bone Joint Surg 77B: 219–224, 1995
51. Miyatsu M, Atsudta Y, Watakabe M: The physiology of mechanoreceptors
in the anterior cruciate ligament. An experimental study in decerebrate-
spinalised animals. J Bone Joint Surg 75B: 653–657, 1993
52. Morgan DL: Separation of active and passive components of short-range
stiffness of muscle. Am J Physiol 232: C45–C49, 1977
53. Mussa-Ivaldi FA, Hogan N, Bizzi E: Neural, mechanical, and geometric
factors subserving arm posture in humans. J Neurosci 5: 2732–2743,
1985
54. Olmstead TG, Wevers HW, Bryant JT, et al: Effect of muscle activity of
valgus/varus laxity and stiffness of the knee. J Biomech 19: 565–577,
1986
55. Pope MH, Johnson RJ, Brown DW, et al: The role of musculature in
injuries to the medial collateral ligament. J Bone Joint Surg 61A: 398–402,
1979
56. Rasmussen O, Tovborg-Jensen I: Mobility of the ankle joint: Recording of
rotatory movements in the talocrural joint in vitro with and without the
lateral collateral ligaments of the ankle. Acta Orthop Scand 53: 155–160,
1982
57. Raunest J, Sager M, Burgener E: Proprioceptive mechanisms in the
cruciate ligaments: An electromyographic study on reflex activity in the
thigh muscles. J Trauma 41: 488–493, 1996
58. Renstrom P, Wertz M, Incavo S, et al: Strain in the lateral ligaments of the
ankle. Foot Ankle 9: 59–63, 1988
59. Shiavi R, Frigo C, Pedotti A: Electromyographic signals during gait: Cri-
teria for envelope filtering and number of strides. Med Biol Eng Comput
36: 171–178, 1998
60. Shrout PE, Fleiss JL: Intraclass correlations: Uses in assessing rater
reliability. Psychol Bull 86: 420–428, 1979
61. Sinkjaer T, Hayashi R: Regulation of wrist stiffness by the stretch reflex.
J Biomech 22: 1133–1140, 1989
62. Sinkjaer T, Toft E, Andreassen S, et al: Muscle stiffness in human ankle
dorsiflexors: Intrinsic and reflex components. J Neurophysiol 60: 1110–
1121, 1988
63. Sojka P, Johansson H, Sjolander P, et al: Fusimotor neurones can be
reflexively influenced by activity in receptor afferents from the posterior
cruciate ligament. Brain Res 483: 177–183, 1989
64. Spencer JD, Hayes KC, Alexander IJ: Knee joint effusion and quadriceps
reflex inhibition in man. Arch Phys Med Rehabil 65: 171–177, 1984
65. Torry MR, Decker MJ, Viola RW, et al: Intra-articular knee joint effusion
induces quadriceps avoidance gait patterns. Clin Biomech 15: 147–159,
2000
66. Tropp H, Ekstrand J, Gillquist J: Stabilometry in functional instability of the
ankle and its value in predicting injury. Med Sci Sports Exerc 16: 64–66,
1984
67. Viitasalo JT, Salo A, Lahtinen J: Neuromuscular functioning of athletes
and non-athletes in the drop jump. Eur J Appl Physiol Occup Physiol 78:
432–440, 1998
68. Weiss PL, Hunter IW, Kearney RE: Human ankle joint stiffness over the
full range of muscle activation levels. J Biomech 21: 539–544, 1988
69. Wilkie DR: The relation between force and velocity in human muscle.
J Physiol (London) 110: 249–280, 1950
70. Winter DA: Biomechanics and Motor Control of Human Movement. Sec-
ond edition. New York, John Wiley & Sons, Inc, 1990
71. Winter DA: The locomotion laboratory as a clinical assessment system.
Med Prog Technol 4: 95–106, 1976
72. Wyke B: Articular neurology–a review. Physiotherapy 58: 94–99, 1972
73. Yang JF, Winter DA: Electromyographic amplitude normalization meth-
ods: Improving their sensitivity as diagnostic tools in gait analysis. Arch
Phys Med Rehabil 65: 517–521, 1984
74. Zhang LQ, Portland GH, Wang G, et al: Stiffness, viscosity, and upper
limb inertia about the glenohumeral abduction axis. J Orthop Res 18:
94–100, 2000
506 Myers et al. American Journal of Sports Medicine