J Neurophysiol 98: 11021107, 2007.

First published July 18, 2007; doi:10.1152/jn.00371.2007.

Reflex Inhibition of Normal Cramp Following Electrical Stimulation of the

Muscle Tendon
Serajul I. Khan and John A. Burne
School of Medical Sciences, University of Sydney, Lidcombe, New South Wales, Australia
Submitted 1 April 2007; accepted in final form 10 July 2007

Khan SI, Burne JA. Reflex inhibition of normal cramp following

electrical stimulation of the muscle tendon. J Neurophysiol 98: 11021107,
2007. First published July 18, 2007; doi:10.1152/jn.00371.2007. Muscle
cramp was induced in one head of the gastrocnemius muscle (GA) in
eight of thirteen subjects using maximum voluntary contraction when
the muscle was in the shortened position. Cramp in GA was painful,
involuntary, and localized. Induction of cramp was indicated by the
presence of electromyographic (EMG) activity in one head of GA
while the other head remained silent. In all cramping subjects, reflex
inhibition of cramp electrical activity was observed following Achilles tendon electrical stimulation and they all reported subjective relief
of cramp. Thus muscle cramp can be inhibited by stimulation of
tendon afferents in the cramped muscle. When the inhibition of
cramp-generated EMG and voluntary EMG was compared at similar
mean EMG levels, the area and timing of the two phases of inhibition
(I1, I2) did not differ significantly. This strongly suggests that the same
reflex pathway was the source of the inhibition in both cases. Thus the
cramp-generated EMG is also likely to be driven by spinal synaptic
input to the motorneurons. We have found that the muscle conditions
that appear necessary to facilitate cramp, a near to maximal contraction of the shortened muscle, are also the conditions that render the
inhibition generated by tendon afferents ineffective. When the
strength of tendon inhibition in cramping subjects was compared with
that in subjects that failed to cramp, it was found to be significantly
weaker under the same experimental conditions. It is likely that
reduced inhibitory feedback from tendon afferents has an important
role in generating cramp.

Common muscle cramp is characterized by sudden, localized, involuntary, sustained, and painful contraction attended
by visible and palpable knotting of part or all of the affected
muscle (Baldissera et al. 1991; Denny-Brown et al. 1948; Ross
et al. 1995). Cramp is typically of short duration but may
warrant medical intervention if associated with long-lasting
pain (Mills et al. 1982). Its physiology is poorly understood,
largely due to its inaccessibility to experimental investigation.
It is difficult to induce in many normal subjects, it is typically
of short duration, and there is no animal model.
Cramp is accompanied by active muscle contraction, as
evidenced by high levels of muscle electrical activity. The
origin of the electrical activity remains unclear. The generator
may lie within the CNS or in peripheral neuromuscular membranes. Whatever the location of the generator, it appears to be
facilitated by a variety of factors that include strong voluntary
contraction, exercise (Layzer et al. 1986; Miles et al. 1994;
Schwellnus et al. 1997), sleep (Gootnick 1943; Nicholson et al.

1945), pregnancy (Oba 1967; Page et al. 1953), and several

pathologies such as myopathy, neuropathy, motoneuron disease (Brown 1951; McGee 1990), metabolic disorders (Layzer
et al. 1967; McArdle 1951; Tarui et al. 1965), electrolyte
imbalance (Edsall 1908; Oswald 1925; Talbott 1935), and
endocrine pathology (Satoh et al. 1983). However, the link
between these factors and the involuntary muscle electrical
activity that accompanies cramp remains unclear. In summary,
both intramuscular and neural mechanisms appear to contribute
to cramp but no integrating theory has been proposed.
Earlier studies suggested a cramp generator within peripheral nerve segments. It was reported that cramp could be
induced by electrical stimulation of motor fibers distal to an
anesthetic block (Lambert 1969). Fasciculations, which are
thought to be related to cramp (Denny-Brown 1953; Layzer
1971; Roth 1984), may also persist after peripheral nerve block
(Conradi 1982; Layzer et al. 1971; Tahmoush et al. 1991) or
complete section of the nerve (Forster et al. 1946).
A generator within the motorneuron is also suggested by
theories of motorneuron hyperexcitability or bistability (Baldissera et al. 1991). Bistability indicates an anomalous state in
which a self-sustained depolarization and repetitive firing of
alpha motor neurons is triggered by a depolarizing pulse or
intracellularly injected current (or possibly a short synaptic
excitation) and terminated by a hyperpolarizing current pulse
(or synaptic inhibition) (Hagbarth et al. 1966). Originally
bistability was described as a reflex phenomenon consisting of
a long-latency prolonged contraction of the soleus muscle that
was evoked by a burst of Ia afferent volleys and terminated by
a brief synaptic inhibition (Hultborn et al. 1975).
A limitation of the peripheral generator model is the difficulty of incorporating the known systemic and metabolic
effects that can be more easily integrated into a reflex model by
muscle afferents. A few observations suggest that central or
reflex factors are able to modulate cramp-related electrical
activity. Voluntary contraction of the antagonist muscle, without stretching the cramped muscle, causes an inconsistent
reduction of cramp discharge, suggesting spinal reflex inhibition (Norris et al. 1957). The Hoffmann (H) reflex is enhanced
after cramp (Ross et al. 1976) and transcutaneous nerve stimulation at sites remote from the cramped muscle are reported to
relieve severe, long-lasting, and widespread muscle cramp
(Mills et al. 1982).
Muscle stretching is reported to abruptly interrupt cramp
induced by voluntary contraction or high-frequency stimulation of peripheral nerve (Baldissera et al. 1991; Dennig 1926;

Address for reprint requests and other correspondence: J. A. Burne, School

of Biomedical Sciences, University of Sydney, PO Box 170, Lidcombe, NSW
1825, Australia (E-mail: J.Burne@usyd.edu.au).

The 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.

INTRODUCTION

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TENDON REFLEX INHIBITION OF CRAMP

1103

Lanari et al. 1973; Mills et al. 1982; Rowland 1985). Again the
mechanism is unclear, although it has been suggested (Layzer
et al. 1971) that passive stretch of the cramping muscle may
produce autogenic inhibition by the tendon organ reflex. The
possibility that cramp is inhibited by reflex afferents is worth
further exploration because such a mechanism would strongly
support a central or reflex origin of the cramp-related EMG and
might also guide more effective therapy.
Burne and Lippold (1996) showed that electrical stimulation
over muscle tendons produced a strong reflex inhibition of an
ongoing voluntary contraction. This has been suggested to
originate from group III tendon afferents (Priori et al. 1998).
More recently, Khan and Burne (unpublished observations)
found that the strength of reflex inhibition was related to
muscle length, being maximal in the stretched muscle and quite
weak in the fully shortened muscle. This finding is consistent
with the theory that tendon afferents mediate the stretchinduced reduction in cramp.
In the current study, we investigated the effect of tendon
electrical stimulation on the electrical activity associated with
muscle cramp in human subjects. The induced inhibition of
cramp activity was compared with the inhibition of a similar
level of normal voluntary contraction. If cramp activity shows
the same pattern of inhibition, it implies that it is driven by the
motoneurons synaptic connections rather than by an intrinsic
or peripheral generator. Conversely, if the cramp activity is
unresponsive to reflex input, an origin within the motorneuron
or the muscle itself is supported.

filtered (10- to 80-Hz pass), and full-wave rectified; average curves

were computed from a minimum of 30 successive trials. The area of
inhibitory and excitatory response components was then calculated by
software as previously described (Blanch and Burne 2001). The mean
value and the SD of 100 ms of prestimulus data were calculated and
points less than the SD were regarded as inhibitory points. The sum of
these points estimated the area of inhibition.

METHODS

Comparison of the inhibitory areas of cramp-related EMG and

voluntary EMG were made by one-way repeated-measures ANOVA.
Simple linear regression was used to relate inhibitory area to the mean
background contraction. Both analyses were performed using Statistica (StatSoft, Tulsa, OK). The level set for statistical significance was
P 0.05.

Subjects
Two women and eleven men aged 18 to 30 yr with no neurological
disorder but complaining of cramp in the gastrocnemius muscle (GA)
were recruited. All subjects gave informed consent and the university
ethics committee approved the study.

Protocol
Subjects were positioned on their right side on a stretcher adjustable
for height. The right knee was fully extended and the right foot was
fitted to a footplate and stabilized to a supporting frame. The footplate
was designed to rotate in the horizontal plane, allowing the foot to be
fixed in its maximally plantarflexed position with GA in its shortened
position. The ankle joint was fixed to prevent muscle lengthening,
which could subsequently break the cramp. In this position, each
subject maximally contracted GA by pushing against the footplate
until cramp was induced. Subjects notified the onset, perceived
location, and relative intensity of the induced cramp, which was
attended by visible knotting. Subjects were instructed to attempt
maximal relaxation of voluntary drive once cramp was present so that
the activity present could be attributed to cramp. The typical occurrence of cramp in one head of GA permitted voluntary relaxation to be
assessed by confirming the absence of EMG in the noncramping head.
In the testing position, no subjects were able to voluntarily produce
EMG in one head of GA only. Induction of cramp was attempted
several times in each session, each attempt being followed by 1520
min of rest, unless a persisting cramp was obtained.

Statistics

RESULTS

Tendon stimulation

Inhibition of voluntary contraction

A stimulus intensity of 60 mA was used for all experiments because

it was found to produce maximal inhibition in previous experiments
(Khan and Burne, unpublished observations). Small metal plates
served as stimulating electrodes. The cathode was positioned centrally
on the GA tendon, about 1 cm below the musculotendonous junction
and the anode medially on the anterior calf adjacent to the cathode.
The technique for obtaining tendon inhibition from GA is described in
more detail in Khan and Burne (unpublished observations).

Figure 1, A and B illustrates the simultaneous inhibition of a

normal voluntary contraction [20% of maximum voluntary
contraction (MVC)] in the medial and lateral heads of GA
following tendon stimulation (60 mA, 1 ms). The features of
the reflex response and the timing of inhibitory and excitatory
phases were as described by Khan and Burne (unpublished
observations). The first and larger inhibitory component (I1)
commenced 55 0.57 ms (SD) after the stimulus onset and its
duration was 69.5 11.0 ms. This was followed by a smaller
inhibitory phase (I2) of latency 193 10.8 ms and duration
39 14.7 ms. I1 was followed by the excitatory peak (E1) of
latency 142.2 8.4 ms and I2 was followed by the excitatory
peak (E2) of latency 240 11.8 ms (mean SD).

Electrical recording
The surface electromyogram (EMG) was recorded with disposable
bipolar silversilver chloride electrodes, attached 3 cm above the
muscle tendon junction over the central belly of the lateral and medial
heads of GA. Careful attention to skin degreasing allowed low
interelectrode impedance. An earth electrode was also placed over the
tibia. Amlab (Amlab International, Sydney, Australia) hardware was
used to record and filter the EMG (band-pass 5 400 Hz), digitize it (1
kHz), and display the raw signals and mean root-mean-square (RMS)
values in real time on a computer screen. The RMS display was
available to subjects to match their isometric contractions to target
levels. The digitized raw data were saved to computer hard disk and
then further processed and analyzed off-line (Matlab v. 7, The MathWorks, Natick, MA). The raw EMG signals were digitally detrended,
J Neurophysiol VOL

Effect of mean background contraction

For all subjects, the strength of reflex inhibition, I1 and I2,
after tendon stimulation was negatively correlated with the
mean background contraction. The relationship was approximately linear as shown for one subject in Fig. 2, A and B. It can
be seen that the amount of reflex inhibition and the mean
background contraction were strongly correlated in this subject

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S. I. KHAN AND J. A. BURNE

FIG. 1. Simultaneous inhibition of a normal voluntary contraction at 20% of maximum voluntary contraction (MVC) in the
medial (A) and lateral (B) heads of gastrocnemius muscle (GA) after tendon stimulation
(60 mA, 1 ms). Effects of the same stimulus
on the cramping medial head (C) and relaxed
noncramping lateral head (D) of GA are also
shown. I1 and I2 denote the first and second
inhibitory periods. E1 and E2 denote the peaks
of the first and second excitation that followed the electromyographic (EMG) inhibition. Stimulus commenced at 300 ms, as indicated by the arrow on timescale.

(P 0.014, r2 0.97, linear regression). Figure 2, C and D

shows the pooled data for the reflex inhibition I1 (P 0.0001
and r2 0.7809) and I2 (P 0.7538 and r2 0.0001) after
tendon electrical stimulation. These data confirm an approximately linear inverse relation between strength of reflex inhibition
and the mean background contraction in the subject population.

Effect of tendon stimulation on cramp

Of the thirteen subjects, eight successfully produced cramp
in one head of GA. Relaxation of voluntary contraction was
confirmed by inspection of the EMG from the noncramping
head of GA. In all subjects, reflex inhibition of cramp EMG

FIG. 2. Effect of mean background contraction level on the strength of reflex inhibition (A is I1, B is I2) of the contraction (closed
circles) and inhibition of cramp (open circle)
in the same subject. Solid line is the linear
regression line and the broken lines are 95%
confidence intervals for the data shown.
Pooled data for the effect of mean background contraction level on the strength of
reflex inhibition (C is I1, D is I2) is also
shown.

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TENDON REFLEX INHIBITION OF CRAMP

1105

activity was observed after tendon stimulation and the subjects

reported relief of cramp during or after 30 shocks had been
delivered to the tendon. Figure 1, C and D shows the inhibition
of cramp (I1, I2) after tendon electrical stimulation in the same
subject. The onset latency of I1 was found to be 55 0.58 (SD)
ms, similar to that reported earlier for the voluntary contraction
and previously in upper limb muscles (Burne et al. 1996a). The
onset latency of I2 was found to be 193 10.8 (SD) ms, which
was again similar to that reported earlier for the voluntary
contraction. The timing of I2 has not previously been reported
in the literature.
FIG. 3. Data from 8 cramped subjects showing the correlation between the
areas of inhibition of voluntary and cramp EMG. Solid line is the linear
regression line and the broken lines are 95% confidence intervals for the data
shown.

Comparison of inhibition of voluntary contraction and

cramp
Because the magnitude of voluntary inhibition varied with
the mean background level, we fitted the cramp inhibitory data
(I1, I2) to the regression plot relating voluntary inhibition to
mean background contraction level in the same subject (Fig. 2,
A and B). It was thus shown that the area of cramp inhibition
lay within the 95% confidence intervals for voluntary inhibition in all subjects. Table 1 summarizes the group data comparing the magnitude of inhibition of voluntary EMG and
cramp-related EMG in the same subjects and at the same level
of background contraction. There was no statistically significant difference in latency or area of inhibition (P 0.05,
repeated-measures ANOVA). In fact, the areas of I1 (P 0.01,
r2 0.93) measured during cramp and voluntary contraction
were strongly correlated in the same subjects. This result is
illustrated in Fig. 3.
Comparison of tendon inhibition in cramping and
noncramping subjects
The magnitude of reflex inhibition of voluntary contraction
following tendon stimulation was compared in subjects that
subsequently produced cramp during the experiment and subjects that could not be induced to cramp during the experiment.
It was found that I1 (group mean 2,360 Vms for cramping
subjects, 2, 720 Vms for noncramping subjects, P 0.09)
TABLE

1. Inhibitory reflex responses during voluntary contraction

and cramp
Inhibition (I1)

Mean
SD

Inhibition (I2)

Voluntary

Cramp

Voluntary

Cramp

3,600
1,600
4,900
2,500
1,500
1,100
4,500
3,000
2,533.4
1,609.9

3,400
1,500
4,800
2,300
1,000
800
3,600
3,400
2,322.3
1,572.1

1,175
641
2,413
203
184
107
1,173
1,150
794.3
769.1

829
456
2,131
127
100
50
1,084
1,021
651.7
688.5

Average
EMG, V
30
58
23
84
75
110
34
25

Voluntary and cramp inhibitions following tendon electrical stimulation

with the same level of mean background contraction (last column) are compared. I1 and I2 represent the first and secondary inhibitory components of the
reflex response following tendon stimulation. The reflex response was clearly
distinguished in all experiments. Population mean and SD values are shown.
J Neurophysiol VOL

and I2 (group mean 640 Vms for cramping subjects, 1,120

Vms for noncramping subjects, P 0.017, repeated-measures ANOVA) were smaller in the cramping subjects (Fig.
4B). This difference was highly significant for I2 but failed to
be significant for I1.
DISCUSSION

Cramp in GA was painful, involuntary, and localized. In half

of the subjects it was absent or incomplete and did not persist
long enough to do the experiment. Induction of cramp was
indicated electrically by the presence of EMG activity in one
head of GA while the other head remained silent. In contrast,
no subject was able to voluntarily contract one head of GA and
relax the other in the testing position. These findings confirm
that cramp was localized and involuntary in nature.
Our observations clearly show that muscle cramp can be
inhibited by stimulation of tendon afferents in the cramped
muscle. When the inhibition of cramp-generated EMG and
voluntary EMG was compared at similar mean background
EMG levels, the area and timing of the inhibition did not differ
significantly. This strongly suggests that the same reflex pathway was the source of the inhibition in both cases. Thus the
cramp-generated EMG is also likely to be driven by spinal
synaptic input to the motorneurons.
It is well documented that tendon electrical stimulation
produces strong inhibition of the ongoing voluntary EMG
activity and this inhibition arises from tendon afferents by
reflex inhibitory pathway (Burne et al. 1996). Muscle stretching causes a sudden interruption of cramp induced by either
voluntary contraction or electrical stimulation of the peripheral
nerve (Bertolasi et al. 1992; Denny-Brown et al. 1948; Fowler
1973; Layzer et al. 1982; Schwellnus et al. 1996). Passive
stretch of a contracting muscle effectively activates autogenic
inhibitory Ib afferents in the tendon (Granit 1950). However, it
has been proposed that the inhibition following electrical
stimulation arises from group III tendon afferents that presynaptically inhibit the terminals of 1a stretch reflex afferents
(Priori et al. 1998). It is thus possible that these afferents are
responsible for inhibition of cramp, although little is known
about their response to passive stretch.
Regardless of the species of afferent involved, we have
shown in parallel experiments that tendon electrical inhibition
is approximately linearly related to the length of the contracting muscle and maximal when the muscle is fully stretched

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S. I. KHAN AND J. A. BURNE

FIG. 4. Pooled normalized data comparing the strength of inhibition I1 (A) and I2 (B)
of a normal voluntary contraction in cramping and noncramping subjects.

(Khan and Burne, unpublished observations). This implies that

these afferents are protective against cramp in the lengthened
muscle and less effective in preventing cramp when the muscle
is fully shortened. This role is further supported by the observation from the current experiments that electrical tendon
stimulation less effectively inhibits large than small voluntary
contractions. In summary, the muscle conditions that appear
necessary to facilitate cramp, a near maximal contraction of the
shortened muscle, are also the conditions that render the
inhibition generated by tendon afferents ineffective. It is thus
likely that reduced inhibitory feedback from the tendon may
have an important role in generating cramp (see also discussion
by Schwellnus et al. 1997). This conclusion is further supported by our observation that noncrampers produced significantly stronger inhibition than those that were subsequently
induced to cramp on the same day.
It was previously shown that stimulation of the nerve supplying the cramped muscle was effective in blocking cramp
activity (Lanari et al. 1973). Our findings support the proposal
of these authors that the inhibition they observed was due to
stimulation of tendon afferents.
It is well documented that the muscles most prone to
cramping are those that span two joints (Manjra 1991; Nicol
1996). Contraction in the shortened position would result in
decreased tension in the tendons of the muscle during contraction. Tendon activity would therefore be decreased in plantarflexion compared with dorsiflexion.
The common observation that the intensity of cramp tends to
increase progressively over time can be interpreted as evidence
of a positive feedback mechanism. There is also much evidence that intramuscular mechanisms facilitate cramp (Joekes
1982; Layzer et al. 1971; Mills et al. 1982). It is possible that
intramuscular changes, such as those associated with fatigue,
stimulate chemically sensitive intramuscular afferents, such as
group III afferents that are also stretch sensitive. These may
play a role in facilitating motorneuron activity in the absence of
negative feedback from tendon afferents. This imbalance in
positive and negative feedback signals can result in abnormal,
sustained motorneuron activity. Also Nelson and Hutton
(1985) found an increase in resting discharge frequency of type
Ia and type II afferents as well as a dramatic decrease in Golgi
tendon organ (type 1b) firing rates to slow stretches during
fatigue.
Our observation that voluntary inhibition was inversely
related to the mean background contraction level is consistent
with the proposal (Priori et al. 1998) that the stimulated group
III afferents produce presynaptic inhibition of 1a terminals.
J Neurophysiol VOL

The 1a stretch afferents are reported to contribute a decreasing

proportion of the total synaptic drive to motorneurons as the
contraction level increases toward maximum (Harrison and
Taylor 1981). The effects of tendon inhibition on the total
synaptic drive should thus also decrease with contraction level.
The central origin of cramp is also supported by studies of
motor unit properties, which report no marked changes in their
profiles during voluntary contraction and cramp (Ross et al.
1995). This contrasts with studies of fasciculation (Baldissera
et al. 1991; Denny-Brown 1984).
In summary: first, the inhibition of the voluntary EMG
activity recorded after tendon stimulation decreased with increased mean background contraction in an approximately
linear fashion. Second, cramp-related EMG was inhibited after
tendon electrical stimulation and the strength of inhibition was
strongly correlated with the strength of voluntary EMG inhibition at a similar level of mean background contraction in the
same subject. This result suggests that the cramp-generated
EMG is driven by spinal synaptic mechanisms rather than by a
generator within the motorneurons or by intramuscular mechanisms.
The recordings from both heads of gastrocnemius were
particularly important to determine the true onset of cramp.
Once cramp was induced in one head of gastrocnemius after a
sustained maximal voluntary contraction, the EMG activity in
the other head remained silent. These data thus provided an
objective measure of the involuntary and localized nature of
cramp (Norris et al. 1957).
REFERENCES

Baldissera F, Cavallari P, Dworzak F. Cramps: a sign of motoneurone

bistability in the human patient. Neurosci Lett 133: 303306, 1991.
Baldissera F, Cavallari P, Dworzak F. Motor neuron bistability: a pathogenetic mechanism for cramps and myokymia. Brain 117: 929 939, 1994.
Bertolasi L, Bongiovanni LG, Zanette GP. The influence of muscular
lengthening on cramp. Ann Neurol 33: 176 180, 1993.
Brown MR. The inheritance of progressive muscular atrophy as a dominant
trait in two New England families. N Engl J Med 245: 645 647, 1951.
Burne JA, Blanche T, Morris J. Electrical stimulation of muscle tendons in
essential tremor. Muscle Nerve 25: 58 64, 2002.
Burne JA, Lippold OCJ. Reflex inhibition following electrical stimulation
over muscle tendons in man. Brain 119: 11071114, 1996.
Caress JB, Bastings EP, Greg LH. A novel method of inducing muscle
cramps using repetitive magnetic stimulation. Muscle Nerve 23: 126 128,
1999.
Conradi S, Grimby L, Lundemo G. Pathophysiology of fasiculations in ALS
as studied by electromyography of single motor units. Muscle Nerve 5:
202208, 1982.
Dennig H. Uber den Muskelcrampus. Dt Z NervHeilk 93: 96 104, 1926.
Denny-Brown D. Clinical problems in neuromuscular physiology. Am J Med
15: 368 390, 1953.

98 SEPTEMBER 2007

www.jn.org

TENDON REFLEX INHIBITION OF CRAMP

Denny-Brown D, Foley J. Myokeymia and the benign fasciculation of
muscular cramps. Trans Assoc Am Phys 61: 88 96, 1948.
Edsall DL. New disorder from heat: a disorder due to exposure to intense heat.
J Am Med Assoc 11: 1969 1971, 1908.
Forster FM, Borkowski WJ, Alpers BJ. Effects of denervation on fasciculation in human muscles. Relation of fibrillations to fasciculations. Arch
Neurol Psychiatry 56: 276 283, 1946.
Fowler AW. Relief of cramp. Lancet i: 99, 1973.
Gootnick A. Night cramp and quinine. Arch Intern Med 71: 555562, 1943.
Granit R. Autogenetic inhibition. Electroencephalogr Clin Neurophysiol 2:
417 424, 1950.
Harrison PJ, Taylor A. Individual excitatory post-synaptic potentials due to
muscle spindle Ia afferents in cats triceps surae motoneurones. J Physiol
312: 455 470, 1981.
Hultborn H, Wigstrom H, Wangberg B. Prolonged activation of soleus
motoneurones following a conditioning train in soleus Ia afferentsa case
for a reverberating loop? Neurosci Lett 1: 147152, 1975.
Joekes AM. Cramp: a review. J R Soc Med 75: 546 -549, 1982.
Lambert EH. Electromyography in amyotrophic lateral sclerosis. In: Motor
Neuron Disease: Research on Amyotrophic Lateral Sclerosis and Related
Disorders, edited by Norris FN Jr, Kurland LT. New York: Grune &
Stratton, 1969, p. 135153.
Lanari A, Muchnik S, Rey N. Muscular cramp mechanism. Medicina 33:
12351240, 1973.
Layzer RB. Muscle Pain, Cramps, and Fatigue. New York: McGraw-Hill,
1986, p. 19071922.
Layzer RB. The origin of muscle fasciculation and cramps. Muscle Nerve 17:
12431249, 1994.
Layzer RB, Rowland LP. Muscle phosphofructokinase deficiency. Arch
Neurol 17: 512523, 1967.
Layzer RB, Rowland LP. Cramps. Physiol Med 285: 31 40, 1971.
Manjra SI. Muscle Cramps in Athletes [BSc (Sports Med) thesis]. Cape
Town, South Africa: Univ. of Cape Town, 1991.
McArdle B. Myopathy due to a defect in muscle glycogen breakdown. Clin
Sci 10: 1333, 1951.
McGee SR. Muscle cramps. Arch Intern Med 150: 511518, 1990.
Miles MP, Clarkson PM. Exercise induced muscle pain, soreness, and
cramps. J Sports Med Phys Fitness 34: 203216, 1994.
Miller TM, Layzer RB. Muscle cramp. Muscle Nerve 32: 431 442, 2005.
Mills KR, Newham DJ, Edwards RHT. Severe muscle cramps relieved by
transcutaneous nerve stimulation: a case report. J Neurol Neurosurg Psychiatry 45: 539 542, 1982.
Nelson LD, Hutton RS. Dynamic and static stretch response in muscle spindle
receptors in fatigued muscle. Med Sci Sports Exerc 17: 445 450, 1985.
Nicholson J, Falk A. Night cramp in young men. N Engl J Med 233: 556 559,
1945.

J Neurophysiol VOL

1107

Nicol J. Exercise-Associated Muscle Cramps in Distance Runners: The Role of

Serum Electrolytes Both During and Following an Ultra-Marathon and
IEMG Activity in the Recovery Post-Cramp [MPhil (Sports Med) thesis].
Cape Town, South Africa: Univ. of Cape Town, 1996.
Norris FH, Paul OC, Gasteiger EL. An electromyographic study of induced
and spontaneous muscle cramps. Electroencephalogr Clin Neurophysiol 9:
139 147, 1957.
Oba T. Study on leg cramp in pregnancy in Japanese. Acta Obstet Gynecol
Scand 19: 459 468, 1967.
Oswald RJW. Saline drink in industrial fatigue. Lancet 16: 1369 1370, 1925.
Page EW, Page EP. Leg cramps in pregnancy. Acta Obstet Gynecol Scand 1:
93100, 1953.
Priori A, Berardelli A, Inghilleri M, Pedace F, Giovannelli M, Manfredi
M. Electrical stimulation over muscle tendons in humans. Evidence favouring presynaptic inhibition of Ia fibers due to the activation of groups III
afferents. Brain 121: 373380, 1998.
Roeleveld K, Van Engelen BGM, Stegeman DF. Possible mechanisms of
muscle cramp from temporal and spatial surface EMG characteristics. J Appl
Physiol 88: 1698 1706, 2000.
Ross BH. Muscle cramp and the Hoffmann reflex. Proc 20th World Congress
Sports Medicine, Carlton, Australia 6770, 1976.
Ross BH, Thomas CK. Human motor unit activity during induced muscle
cramp. Brain 118: 983993, 1995.
Roth G. Fasciculations dorigine peripherique. Electromyogr Clin Neurophysiol 11: 523526, 1971.
Rowland LP. Cramps, spasms and muscle stiffness. Rev Neurol 141: 261273,
1985.
Satoh A, Tsusihata M, Yoshimura T, Mori M, Nagataki S. Myasthenia
gravis associated with Satoyoshi syndrome: muscle cramps, alopecia and
diarrhea. Neurology 33: 1209 1211, 1983.
Schwellnus MP, Derman EW, Noakes TD. Aetiology of skeletal muscle
cramps during exercise: a novel hypothesis. J Sports Sci 15: 277285,
1997.
Schwellnus MP, Nicol J, Laubscher R. Serum electrolyte concentration and
hydration status are not associated with exercise associated muscle cramping
in distance runners. J Sports Med 38: 488 492, 2004.
Stone MB, Edwards JE, Babington JP, Ingersoll CD, Palmieri RM.
Reliability of an electrical method to induce muscle cramp (Letter). Muscle
Nerve 27: 122123, 2003.
Tahmoush AJ, Alonso RJ, Tahmoush GP, Heiman-Patterson TD. Crampfasiculation syndrome: a treatable hyperexcitable peripheral nerve disorder.
Neurology 41: 10211024, 1991.
Talbot HT. Heat cramps. Medicine 14: 323376, 1935.
Tarui S, Okuno G. Phosphofructokinase deficiency in skeletal muscle: a new
type of glycogenosis. Biochem Biophys Res Commun 19: 517523, 1965.

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