A Review of Myotatic Reflexes and the Development
of Motor Control and Gait in Infants and Children:
A Special Communication
Although the mechanism of the phasic myotatic (or '?@etch'>reflex is well-known,
the role of this re@ in adult gait remains speculative. The acquisition and development of locomotor skills with respect to the development of the myotatic reflex
requirefurther study in both healthy and neurologically impaired children. In this
article, the well-documentedpropenies of the healthy adultk myotatic reflex are
compared with recentwings of the myotatic reflex in healtby infants and children and contrasted with reflex propertl'es in patients with cerebralpalsy. These
data allow us to begin to characterize the emergingfeatures of the stretch reflex
in normal andpathological early development. From these data, we can begin to
speculate about the relationship between changes in stretch reflexes and the acquisition of skillful movement and gait in early childhood [Mykkbust BM: A revlevleu
of myotatk reflexes and the development of motor control and gait in infants
and children:A special communication. Phys 7;6er 70:188-203, 1990]
Barbara M Myklebust
Key Words: Gait;Motor activity;Muscle pe@ormance, general; Pediam'cs,
development.
The age at which children start to
walk independently is quite variable,'
and there is considerable debate
about how children learn to walk.2
Studies of' children by Diet23 and Berger et a14 suggest developmental differences of the myotatic reflex in gait
between very young children (1-2
years of age) and older children (G
10 years of age). The acquisition and
development of locomotor skills with
respect to the development of the
myotatic reflex requires further study
in both healthy and neurologically
impaired children. Abnormal myotatic
or "stretch" reflexes (evoked by tendon tap) have been described in nonambulatory children and adults with
spastic cerebral palsy (CP).5 The
hypothesis that the hyperactive stretch
reflex is related to the inability to
walk in these patients remains to be
tested.~atafrom ambulatory adults
with spasticity suggest that hyperactive
stretch reflexes may interfere with
gaits and the performance of smooth
voluntary limb movements.7
B Myklebus~:,PhD, is Assistant Professor of Neurology and of Physical Medicine and Rehabilitation,
Medical College of Wisconsin, and Research Health Scientist, Laboratory of Sensory-Motor Performance, Clernent J Zablocki Veterans Administration Medical Center, Research Services 151, Milwaukee, W1 53295 (USA).
This work has been supported by research Funds from the VA Rehabilitation Research and Development, the Foundation for Physical Therapy Inc, the United Cerebral Palsy Foundation, and
National Institutes of Health Grant AM 33189 to Gerald L Gottlieb, PhD.
This solicited ariicle was submitted Februcuy 1, 1989; was with the authorfor ra~isionfor file
weeks; and was accepted October 25, 1989.
Physical TherapyNolume 70, Number YMarch 1990
'The phasic myotatic reflex, evaluated by tendon tap, is a standard
element of the clinical examination
used to characterize neurological
abnormalities. Although the mechanism of the myotatic reflex is wellknown, the utility of this reflex
response in identifying deficits of
posture and movement remains elusive. Although the role of the
stretch reflex in adult gait remains
speculative and has not been specifically addressed in classical texts
such as that of Inman et al,R recent
studies suggest that primary afferent
reflex pathways may play a role in
walking, running, and error correction in gait.Sl3
In this special communication, the
well-documented properties of the
healthy adult's myotatic reflex are
compared with recent findings of
the myotatic reflex in healthy infants
and children and contrasted with
188/51
reflex properties in patients with
CP! These data allow us to begin to
characterize the emerging features
of the stretch reflex in normal and
pathological early development.
From these data, we can begin to
speculate about the relationship
between changes in stretch reflexes
and the acquisition of skillful movement and gait in early childhood.
Motor control deficits in patients
with spasticity are presented to
illustrate the possible relationship
between abnormal myotatic reflexes
and impaired voluntary movement.
A
H-Reflex
1.5 m v
Y-B
Tendon Tap
0.75 mV
: -.J,,pSOL.
-
Y
Ct
Myotatic Reflexes and
Postmyotatic and Voluntary
Responses
20 mmc
C
During the last 15 years, the nomenclature has evolved for identifying
muscle electromyographic activity
that is evoked reflexively and voluntary contraction. Electromyographic
waveforms have been named
according to onset latency! For purposes of simplicity, the myotatic
refex (or spinal stretch reflex) is
defined as having onset latencies of
about 25 to 45 msec, depending on
the distance of the stretched muscle
from the spinal cord and the type of
perturbation (ie, tendon tap or
mechanical stretch of the muscle).
The amplitude of the myotatic reflex
has little dependence on prior
instruction to the subject and great
dependence on prior contraction.l5
Voluntary responses occur after
about 100 to 120 msec in adults.
The amplitude and latency of voluntary responses are dependent on
prior instruction to the subject and
less dependent on prior contraction
of the agonist muscle. Electromyographic activity evoked in the
intermediate interval is called postmyotatic responses. Postmyotatic
I
I
I
I
Mechanical
Ankle Rotation
2.01
-mvl
0
e
y
&
A
50 msec
Fig. 1. Soleus (SOL) and tibialis anterior (TA) muscle electromyogt-aphicresponses
in one health adult subject for (A) a single H-reflex responsefollowing electrical stimulation of the tibial nerve, (B) a single Achilles tendon tap, and (C) an average of 10
responses to a rapid mechanical dmiflmon of the ankle joint of 17 degrees. Electrom-yographicactivity is recordedfrom sutface electrodes. For rapid ankle dorszJIexion,
sutface EMG signals were full-wave rectijied In each diagram, onset of the reflex 13
identtfid with an arrow: m e II-reflex onset is at approximately 32 msec, the tendon
jerk reflex onset is at approximately 38 msec, and the stretch reflex onset in response to
mechanicalperturbation of the ankle joint is at approximate[v 48 msec.
responses are moderately affected
by prior instruction and may be
modified by prior agonist
contraction.
'Studies performed at the Motor Coordination Laboratory and the Laboratory of Motor Reflex
Development, Rush Medical Center, Chicago, IL, and the Laboratory of Sensory-Motor Performance,
Clement J Zablocki VA Medical Center, Milwaukee, W, have been approved by the human studies
research review committees. Informed written consent has been provided for all research studies.
+Tattonand Lee use the terms "MI,""M2,""M3,"and "voluntary response" to define these EMG
signals.14 The MI waveform is the myotatic reflex at 25 to 45 msec. The M2 response begins after
50 msec and peaks before 80 msec, and is followed by (and sometimes commingled with) the M3
response, or "long-latency"or "long-loop" response, which begins near 85 msec and peaks before
100 msec. Activity after 100 msec is considered "voluntary."
52 / 189
M
TA
Myotatlc Reflexes In
Healthy Adults
In the healthy adult, stretch of the
soleus (SOL) muscle evokes a synchronous burst of EMG activity in the
stretched (agonist) muscle at monosynaptic latencies (about 40 msec),
and relative electrical silence is
observed in the antagonist tibialis
anterior (TA) muscle (Figs. 1,2).5
Myotatic (or "stretch") reflexes in the
normal, relaxed TA muscle have an
extremely high threshold, resulting in
delayed or absent responses when the
TA tendon is tapped.5.16 The normal
Physical TherapyNolume 70, Number 3/March 1990
limb length (which increase the onset
laten~y).~3
&A
HEALTHY ADULT
subject, the latency of the stretch
reflex is shortest (approximately
35-40 msec) for the H-reflex and
longest for mechanical dorsiflexion
of the ankle (approximately 45-50
msec).
Rapid mechanical rotation of the
ankle joint causes a stretch of the SOL
muscle when a torque motor is used
to deliver torque pulses of 1 second's
duration to dorsiflex the ankle. The
ankle is rotated from the neutral position to approximately 10 degrees of
dorsiflexion over the period of 50 to
100 msec, and the dorsiflexed position is maintained for 1 second; then,
the ankle joint is returned to the neutral position before the next stimulus
is applied. The stretch-reflex onset
latency, measured from the onset of
the applied torque to the onset of the
EMG activity, is extremely stable at
about 45 msec, and it varies about
+ 10 msec among different subjects.16
This onset latency is approximately 5
to 10 msec longer than the reflex
evoked by tendon tap. Unlike the
tendon-tap stimulus (which lasts
about 5 msec), the mechanical dorsiflexion of the ankle is extended over
a 50- to 100-msec period, and the SOL
muscle's EMG response begins and
ends while the muscle is still lengthening. The short-latency reflex
response is more likely the result of
the large initial transient stimulus of
the ramp stretch (a change in muscle
length), rather than the change in
velocity, which is monitored by the
muscle spindles.
The SOL muscle's stretch reflex is
essentially unchanged by body orientation (sitting, supine, or prone
p ~ s i t i o n ) .However,
~ ~ ! ~ ~ suprasegmental control (including voluntary contraction of the SOL muscle) influences
and modifies the amplitude of the
H-reflex. The onset latency of the
monosynaptic reflex increases with
limb length in the adult subject.
Changes in the reflex latency in early
childhood development are attributable to central and peripheral myelinization (which increases conduction
time and consequently shortens the
onset latency) and to increases in
Differences in reflex onset latencies
between the H-reflex and Achilles
tendon tap are attributable to the different stimulation sites; that is, the
H-reflex directly stimulates the tibial
nerve at the posterior aspect of the
knee, and the tendon tap excites muscle spindles of the SOL muscle. The
electrical stimulation of the H-reflex
(1.5 msec duration) is a precisely controlled stimulus; this stimulus is
unlike the tendon tap (approximately
5 msec duration), which may excite
muscle spindles differently, depending on the angle, force, and exact
location on the tendon that is tapped.
4-
+40msec
[ 50
0.5 mV
0.5 mV
k&&
&,A-
BIRTH-ONSET
C N S INJURY
0.5 mV
[ 30
ADULT-ONSET
CNS INJURY
[ 40
2.0 mv
2.0mv
Joint Angle SOL EMG TA EMG
Fig. 2. Repex responses in soleus (SOL) and tibialis anterior (TA) muscles to sudden
ankle d m @ m ' o n .Electromyographic raponses werefull-wave rectij7ed and filtered.
Top diagrams show respoms of a healthy, r e k e d adult subject. Middle di6gram.s show
resjmmes cda loyear-old child with spastic cerebral palsy. Bottom diagrams show data
from a spznul cord injured adult patient three months after injury. Each horizontal
record is the average of 10 respomes. Three dwerent torque levek were used, with
Stronger stimuli plotted toward the background. Time markers are at 50-msec intervals.
The dtferences in SOL muscle response latencies between the top and middle diagrams
are due to dtferences in age and size of the subjects. (CNS = central nervous system.)
(Adaptedfiom Myklebust et al.5)
SOL muscle's stretch reflex is produced by activation of the SOL muscle's motoneurons through monosynaptic (and oligosynaptic) spinal cord
path~ays.17~1"his agonist muscle activation is accompanied by an inhibition of the antagonist muscle through
a disynaptic pathway. This is the classically described pathway of reciprocal inhibition (Fig. 3). The myotatic
reflex loc~pconsists of the muscle
spindles, fast-conducting Ia aEerent
fibers, and agonist alpha motor fibers.
Activation of the myotatic reflex of
the SOL muscle may be achieved by
rapid dorsiflexion of the ankle16 or
by a tap to the Achilles tendon.19
The monosynaptic (or oligosynaptic) spinal reflex path may also be
activated by electrical stimulation of
the tibial nerve (Hoffmann reflex or
"H-reflex.")*(Fig. l).zOIn a single
*Unfortunately, the H-reflex has been referred to as a "late response" in electroneuromyopathy.
With respecr to onset latencies of nerve conduction studies of the tibial nerve and other peripheral
nerves, the H-reflex is "late."
Physical TherapyNolume 70, Number 3/March 1990
Differences in amplitude of stretch
reflex responses may be attributable
to the fact that muscle spindles are
'more sensitive to the velocity of
stretch than to changes in muscle
length. That is, the monosynaptic
reflex may be most effectively evoked
by the brief stimulus of the tendon
tap (stimulus duration of 55 msec)
than by mechanical rotation of the
ankle (stimulus duration of 50-100
msec). Furthermore, to an extent,
larger-amplitude tendon taps and
larger angular rotations of the ankle
tend to produce larger-amplitude
reflex EMG responses than smaller
stimuli.
In the "H-reflex recruitment curve,"
the changes in the amplitude of the
SOL muscle's EMG response are plotted with respect to the stimulus
amplitude. At low levels of electrical
stimulation, Ia afferent fibers from
SOL muscle spindles are excited.
About 30 msec after the stimulus, a
synchronized EMG burst, the "Hwave," is recorded from the SOL muscle. As the amplitude of stimulation is
increased, the H-wave increases until
the threshold of the SOL muscle's
motor fibers in the tibia1 nerve is
reached. About 8 msec after the stimulus, an EMG burst called the "Mwave" occurs as a direct motor
response to the stimulation. Further
increase in the stimulus amplitude
results in a monotonic increase in the
M-wave until the full recruitment of
all motor units is achieved. At this
stimulus level, the H-wave increases
only slightly and then decreases.
When the M-wave is maximal, the Hwave has vanished. Typical responses
to progressively stronger stimuli
(from threshold H-reflex to maximal
M-response) are shown in Figure 4.
This behavior results because largeamplitude electrical current stimulates
both efferent fibers and Ia afferent
fibers; the Ia afferent nerve fibers conduct the reflex wave faster than the
antidromic signal is conducted in the
alpha motoneuron fibers. Therefore,
at strong stimulus amplitudes, the Hwave is blocked by a collision of the
antidromic impulses and the reflexelicited orthodromic impulses in the
alpha motoneuron fiber.2"
The H-reflex recruitment curve is
characterized by the threshold of electrical stimulation amplitude to elicit
-
Inhibitory Synapses
Fig. 3. Spinal cord circuity depicting normal stretch reflexpathwa-y (paths 3 and 4)
and bypothetical "wiring"underlying pathological sh-etch reflexes d i b i t e d in p a t h t s
with cerebral paLy (CP) and in healthy neonates (paths 1 and 2). The healthy adultk
reqonse to sh-etch is the result of$ring fa affmentfifibers,which are excitatory on the
agonist alpha motor fiber (path 4) and simultaneously inhibitoty on the antagonist
alpha motorfiber through an interneuron (path -3). It is qeculated that in patients with
CP and in newborn infants, sh-etch is simultaneous!yfacilitoty on the stretched muscle
and its antagonist (ty m o n q m p t i c or polysynaptic pathways) (path I). This 'keciprocally excitatory connection" may be normally present at birth and then i s gradually
masked or dies during normal development. In patients with CP, the pathway of recqrocal excitation may persM (ie,fail to be masked or to die) or it may develop gradua l [ ~This
. pathway may be present, but tonically inhibited, in the healthy adult. Path 2
supposes the absence of the normal tonic inhibition as a developmental defect in
patients with CP and as a pathway that is not yet complete in the neonate. (Adapted
from Myklebust et a15 and from Myklebust.23)
the reflex contraction of the muscle,
by the maximum H-reflex amplitude
(H,,),
and by the extinction of the
H-reflex when stimuli of increased
intensity produce occlusion between
antidromic and orthodromic impulses
in the same alpha motoneurons. Mresponse recruitment curves are used
with H-reflex recruitment curves to
ensure that technical conditions for
stimulation and recording remain
constant.21
The H-reflex has a lower threshold
than the M-response and an H,,
that is half that of the maximum Mresponse (M,,,).
In adults, the
Hma.JMmaxratio, or WM ratio, is
0.54 + 0.10.25 The H/M ratio is
0.65 + 1.00 at birth; it decreases to
0.40 + 0.13 at age 1 year and then
slightly increases to age 3 years,
when values similar to those of the
healthy adult are reached. Use of
the WM ratio, rather than the absolute amplitude of the H-reflex, tends
to minimize errors attributable to
individual differences in test
conditions.
If the H-reflex is elicited by paired
stimuli, the amplitude of the reflex
varies according to the interval
between the stimuli.2Whe "H-reflex
recovery curve" is used to identlfy the
period during which a test (second)
reflex is influenced by a conditioning
(first) reflex. Using identical nearthreshold stimuli, a low-amplitude
H-reflex can be evoked with stimulation intervals between 5 and 9 msec
(early facilitation), which gradually
decays as the interval is increased to
20 msec. Between 20 and 80 msec,
Physical TherapyNolume 70, Number YMarch 1990
the reflex is completely inhibited
(early depression). As the interval is
increased further, the H-wave
increases (:second facilitation) but is
followed by a transient decline in
amplitude between 300 and 800 msec
(late depression). A slow return to
normal excitability is attained only
with intervals longer than 2 seconds.
HEALTHY ADULT'S H-REFLEX AND M-RESPONSE
RECRUITMENT CURVES
Myotatlc Reflexes in
Healthy Neonates
Studies of the H-reflex and the tendon jerk reflex in healthy newborn
infants have demonstrated dserences
between healthy neonates and healthy
adults. The excitability of the monosynaptic pathway has been studied in
newborn infants.27-32 Tests of the Hreflex (H-reflex recruitment curves,
WM ratio, and paired stimuli excitability curves) have demonstrated that
this reflex pathway of the lower limbs
of infants is hyperexcitable compared
with that of healthy adults.
Prechtl recorded muscle electrical
activity from the ipsilateral and contralateral quadriceps femoris (QUAD)
and hamstring (HAM) muscle groups
following patellar tendon taps.29 The
elevated excitability of the myotatic
reflex in the neonate has been attributed to a reduced level of supraspinal
inhibition33 and to facilitory
influences that outweigh inhibition
resulting from dfierences in myelination of descending pathwa~s.27!~8
In tendon jerk reflex studies of the
full-term neonate,* distinct myotatic
reflexes were evoked in 58 healthy
newborn infants when serial taps
were applied to the tendons of the
lower limb (Fig. 5).2334 The neonates
were 1 to 4 days old and were determined to be healthy by neurological
examination and by history of the
pregnancy and delivery. During testing, the irlfant was positioned supine
Stimulus Amplitude (V)
I
Fig. 4. H-reJlexand M-response recruitment curves of healthy adult subject in Figure I . (SOL = soleus muscle; EMG = electromyographic response.)
with the hips flexed and externally
rotated, the knees flexed, and the
ankles in'a neutral position. The
infant's head was in the neutral position when asleep and turned to the
right when awake. The "state" of consciousness (eg, awake or asleep35)
was documented for each tendon tap.
Taps were applied to the tendons of
the SOL, TA, and QUAD muscles; sole
of the foot; and medial malleolus. A
twitch was observed with each tendon
tap recorded. Four to 43 taps were
applied to each tap site for each
infant. Tendon jerks were elicited
with a modified reflex hammer instrumented.with a strain gauge to measure haqmer force and activate the
data-collection system. Surface dfierential myoelectrodes were placed on
the skin overlaying the muscle bellies
of the antagonist SOL and TA muscles
and the QUAD and HAM muscles.
§~nthropornetricdata on neonates gives the distance from the pelvis to the sole of the foot as 23.1
a 1.9 to 28.8 2 2.6 cm in 40-week gestational age infants.23.36 Nerve conduction velocities for the
tibia1 nerves of full-term infants are 25.8 2 2.0 to 28.8 + 2.0 dsec.37 The resulting approximate
conduction time from the ankle to the lumbar spine and back ([2 x 23.1 cmy28.8 d s e c to [2 X
28.8 cmy258 d s e c ) is 16 to 22 msec. These figures are consistent with a rnonosynaptic pathway,
but do not preclude the existence of polysynaptic pathways.
Physical TherapyNolume 70, Number 31March 1990
Taps to the Achilles tendon frequently
evoked almost simultaneous EMG
bursts in SOL and TA muscles, of
comparable amplitudes and at monosynaptic latencies of approximately 20
msec23§For 537 Achilles tendon taps
to 18 neonates, the mean SOL muscle
stretch-reflex latency was 19.4 + 1.4
msec and the mean TA muscle
response was at 19.6 + 1.3 msec.
Sequential Achilles taps in these
healthy neonates evoked reflexes that
were more variable in amplitude,
onset latency, waveform, and ratio of
the peak-to-peakstretch-evokedEMG
voltages (or "TASOL muscle reflex
ratio") than those of the healthy adult.
Tendon taps consistently produced
near-synchronous (but variable)
responses at electrodes over the
tapped muscle, the antagonist muscle,
and distant muscles of the leg.
The onset latency of the Achilles tendon jerk reflex is quite variable
among neonates and between successive taps to one neonate. This variability persists even when limb position,
head position, and state of consciousness (eg, awake or non-REM [rapid
eye movement] sleep) are unchanged.
192155
8 2mv
AchBk,
Tondm Tap
TA
Tadon Tap
As in all studies using surface EMG
-a
7
82mv
k#lu
Tadon Tap
7
*
7
Fig. 5. (A) Ensemble electromyographicactivityfrom sequential tendon taps to one
heal@ I-day-old neonate during non-REM (rapid eye movement) sleep (size appropriate for gestational age, 40 week gestational age by examination and dates, Apgar
scores of 9 at 1 minute and at 5 minutes, normal spontaneous vaginal delivety). Surface EMG recordingsfrom gastrocnemius-soleus(SOL) muscle and tibialis anterior (TA)
musclefor taps to Acf~illestendon, TA tendon, and patellar tendon. During data collection, record numbers were serially incrernentedfrom 1 to 99 for SOL and TA muscle
EMG electrodes. (Adaptedfrom Myklebust et al.34) (B) Simultaneous EMG recordings
from SOL, TA, qqudricepsfernoris (QLrAD),and hamstring (HAM) muscles for a single
Achilles tendon tap to a dt@erent healthy neonate. During data collection, record numbers were serially incrementedfrom 1 to 99 for SOL and TA muscle EMG electrodes
and simultaneous record numbers for QUAD and HAM muscle EMG electrodes were
incremmztedfrom 101 to 199. (Adaptedfrom Myklebust.23)
As an example, for 80 serial Achilles
tendon taps of two different neonates,
the SOL muscle reflex latencies were
21.1 +- 2.93 msec and 23.4 + 0.99
msec, respectively. This variability in
the latency of the myotatic reflex may
be explained by incomplete myelination of the spinal cord and peripheral
nerves. Fluctuations in physiological
excitability levels would contribute to
variability in latencies. Variability in
thresholds for synaptic transmission
may be attributable to lability of
postsynaptic membranes. Furthermore, several monosynaptic and oligosynaptic pathways for stretch
56 / 193
manually applied hammer taps varied
from trial to trial. The measured force
of tap did not correlate with the
amplitude of the evoked agonist EMG
activity. That is, "light" taps sometimes
evoked reflex EMG responses with
amplitudes that were comparable in
size to responses to taps of twice the
applied force.
reflexes may coexist at the time of
birth; different circuits with dlferent
conduction times may be activated by
successive tendon taps. Current
research methods do not permit us to
determine which (if any) of these anatomic or physiologic conditions may
be responsible for the variability in
the reflex latency in the newborn
infant.
Measurements of peak EMG amplitudes were made 18 to 35 msec after
the tendon tap (the period that
includes the onset and duration of the
myotatic reflex). The force of these
recordings, the measured amplitude
of the reflex EMG response is difficult
to compare between taps of a single
neonate or among neonates. However, the relative amplitudes of the
agonist and the antagonist EMG
responses were significantly different
in the healthy neonates when compared with those of healthy adults. To
quantify the degree of simultaneous
activation of SOL and TA muscles, the
TASOL muscle reflex ratio was computed. This ratio is a measure of the
relative excitabilities of the antagonist
muscles for a single tap. The TA:SOL
muscle reflex ratios for Achilles tendon taps for all neonates tested were
higher than for healthy adults. The
mean TA:SOL muscle reflex ratio for
51 neonates was 0.69 + 0.78 (range
= 0.12455). This ratio compares
with a mean TA:SOL muscle reflex
ratio of 0.08 ? 0.04 for healthy adult
subjects.23
In an individual infant, the TASOL
muscle reflex ratio varied from tap to
tap. (For example, the TA:SOL muscle
reflex ratios for two neonates were
0.27 + 0.10 and 1.96 + 2.72, respectively.) The relative amounts of muscle activity in the two antagonist muscles varied even in infants who were
asleep. From a series of taps during a
30-minute test, there was no trend in
the relative amplitudes of muscle
activity, even when head and limb
position (as well as state of consciousness) were controlled.
Electromyographic responses were
consistently produced by tapping sites
not normally thought to excite shortlatency afferents in the corresponding
motoneuron pools. Simultaneous
short-latency EMG responses were
also recorded from HAM and QUAD
muscles when the SOL and TA ten-
Physical TherapyNolume 70, Number 3lMarch 1990
dons were tapped (Fig. 5), and the
HAM and QUAD muscle responses
were nearly coincident with the SOL
and TA muscle responses. This phenomenon of reflex-evoked EMG activity from distant limb muscles is called
reflex irradiation.
Several explanations, which are not
mutually exclusive, may account for
the large 'TA:SOL muscle reflex ratios
of neonates, the short-latency EMG
responses from distant muscles, and
the EMG 1:esponses recorded from
tapping sites such as the TA tendon,
the patellar tendon, and the medial
malleolus:
1. In these small limbs, the SOL mus-
cle EMG signals are electrically
volume-conducted from the
stretched agonist muscle to electrodes over the antagonist muscle
(ie, to the electrode overlying the
TA muscle) or over a distant portion of the limb (ie, to the electrode overlying the QUAD or HAM
musck:). 11
2. Vibration is mechanically transmit-
ted throughout the limb from the
tap site to provide an effective stimulus to other muscles of the limb.
3. At birth, muscle spindles are very
sensitive to stimulation and sense
taps at distant sites.
4. At birth, the spinal cord is physiologically hyperexcitable; therefore,
motoneurons respond to afferent
signals that would normally be
insignificant.
5. Each muscle fiber is innervated by
several efferent fibers (as in neonatal rats and kittens and chicken
ernbryos)38.39#;each muscle would
then be more sensitive to afferent
input.
6. Spinal pathways exist for "reciprocal excitation" of antagonist
motoneurons by primary afferent
fibers. That is, in reciprocal excitation, short-latency spinal cord pathways exist that simultaneously
excite the agonist and antagonist
muscles (Fig. 3).5,23,*0,44
Reciprocal excitation in neonates is
believed to be reflex generated and
segmental in 0rigin.~3The EMG
response from the stretched SOL
muscles, with an onset latency of
about 20 msec, is accompanied by
time-locked activity in the shortened
TA muscle. A parsimonious explanation of the observations of tendon
jerk reflexes in healthy neonates may
IIVolume conduction of electrical signals is a passive and stable phenomenon. If electrical conduction of SOL muscle activity to electrodes over the TA muscle is responsible for the observed TA
muscle response to Achilles tendon tap, then the data should have two features. First, the relative
waveforms of the two EMG responses should exhibit a constant relationship from tap to tap with
respect to relative amplitudes and latencies as long as the electrodes are not moved. Second, both
electrodes 'would be measuring a common signal through different, but invariant, passive tissue
filters. As a consequence, the TA:SOL muscle reflex ratio in a single testing session of an individual
neonate should be independent of the tap site. However, the data show independent variabiliry of
the two EMG responses from tap to tap. Furthermore, the relative changes in the reflex ratio are
not consistent between antagonist tap sites in one neonate. By these tests, volume conduction of
muscle sigrials is neither a sufficient nor a likely explanation of the data. Finally, with volume conduction, a signal attenuates rapidly with distance so that the more remote electrode pair always
yields the smaller EMG signal. This phenomenon is incompatible with the Achilles tendon taps, in
which the TA muscle response is sometimes larger than the SOL muscle response. The exclusive
role of volume conduction in these data cannot be assessed, and it cannot be excluded as a contributing factor. However, volume conduction is an insufficient explanation of these data because
the antagonist EMG signals are often larger than agonist EMG signals, regardless of the tap site.
*Pathways other than those responsible for reciprocal inhibition have not been reported in the
healthy human. Inappropriate spinal cord connections have been found in the normal development of chicken embryos.40Anomalous pathways in the neuromuscular j~nction3~.3%ndcerebral
cortex41 are present in neonatal mammals. In neonatal mammals, reorganization occurs during the
postnatal period by the elimination of processes or neuronal death. None of the results of animal
studies can be directly applied to human reflex studies. However, variabiliry and plasticiry are features of subprimate neonates that are not apparent in the adult. In many parts of the nervous system, "wirir;g" is rearranged during early postnatal life." Competitive interactions may be "the basis
of the human nervous system to adapt to an everchanging external environment."43(~5~~)
Physical TherapyNolume 70, Number 3/March 1990
be the presence of functional excitatory connections from primary
afferent neurons to both agonist and
antagonist motoneuron pools (Fig. 3).
We cannot assess the exclusive roles
of any of the possible mechanisms of
volume conduction, vibration of the
limb, hypersensitive muscle spindles,
motoneuron hyperexcitability, hyperexcitable motor units, or reciprocal
excitation. However, reciprocal excitation provides the most comprehensive (and the most speculative) single
explanation of the data. It does not
require that a new set of physiological
criteria be invoked to explain data of
different tap sites, the variability from
one tap to the next, or the variability
from one infant to the next. This
hypothesis does not preclude the contribution of other mechanisms.
The mechanisms of reflex irradiation
can be proposed to explain the shortlatency responses of muscles that are
distant to the tap site (ie, QUAD and
HAM muscle responses to SOL and TA
tendon taps, SOL and TA muscle
responses to patellar taps). All four
limb muscle groups are innervated by
nerves at the L4 level of the spinal
cord. It is possible that at the time of
birth, some shared communication
exists at this level of the spinal cord
among alpha motoneuron fibers to
the muscles of the thigh and the calf;
stimulation of the muscle spindles in
any one of these muscles may result
in the spread of the reflex responses,
which may be recorded from all the
muscles of the leg. We may speculate
that during normal maturation the
appropriate L4 connections develop
between afferent and efferent fibers
for a particular muscle and that the
inappropriate connections die or are
masked. Tests on a small population
of healthy children aged 1 year and
older have not demonstrated reflex
irradiation. On the other hand, reciprocal excitation has been reported in
healthy children as old as 3 years of
age. The significance of the apparent
differences in the time course for the
alteration of the functional pathways
of reciprocal excitation and reflex
irradiation remains to be identified.
It is hypothesized that reciprocal
excitation and reflex irradiation are
properties of tendon jerk reflexes in
infancy and that these properties
gradually disappear in normal
development. That is, "functional"
spinal cord pathways are proposed
to exist in the neonate, consisting of
excitatory connections from primary
afferent neurons to agonist and
antagonist motoneuron pools
(reciprocal excitation) and motoneuron pools of distant muscles
(reflex irradiation). These pathways
are gradually masked or eliminated
during normal development.
A
ACHILLES TENDON TAPS FROM
HEALTHY CHILDREN
30
-
K
Myotatic Reflexes in
Healthy Children
H-reflex studies have demonstrated
that the excitability of the shortlatency reflex pathway of the neonate
decreases in the early years of normal
de~eloprnent.*7~2~~3()~31
However, the
relationship of changes in stretch
reflex excitability to the normal development of motor skills from infancy
through early childhood is poorly
understood.
Preliminary studies of tendon jerk
reflexes of the lower limbs have been
performed in 15 healthy children
aged 1 month to 6 years.* Some children have been tested longitudinally,
but most of the data are from a population sampling.23The onset latency of
the tendon jerk reflex changes during
early childhood development with
myelinization of peripheral nerves
and central pathways (which tends to
increase conduction velocity and
thereby shorten the onset latency)
and increases in limb length (which
tends to increase the onset latency).23
In the 33 tests of 15 children, Achilles
tendon jerk reflex latencies ranged
from 16.5 + 1.0 msec (representing
20 tendon taps for an 11-month-old
child) to 25.3 + 4.5 msec (representing 14 tendon taps for an 8-month-old
child) (Fig. 6A).
The TA:SOL muscle reflex ratio is
used as a quantitative measure of the
EMG responses to tendon taps. During the first year of life, there was
considerable variability in the TA:SOL
mean neonate latency
= 19Af 1.4 mscc
ACHILLES TENDON TAPS FROM
HEALTHY CHILDREN
~umncoMIc
TkSOL .4.55
~aconatcTkSOL 1
healthy sdult TA:SOL
= 0.08 f 0.04
minimum nrmate
TkSOL 0 0.12
0
12
24
38
48
80
72
Fig. 6. Aterage soleus (SOL) muscle stretch reflex latencies (A) and average r@ex
ratiosfor tibialis anterior (TA) and SOL muscles (TA:SOLmuscle reflex ratios) (B)for
Achilles tendon taps of 15 children aged 1 to 67 months. Changes in SOL muscle refix
latencies over time are compared with the mean refix latency for healthy neonutes.
Changes in TA:SOL muscle reJd ratios are compared with minimum, maximum, and
mean valuesfrom healthy neonafes and with the healthy adultk mean TA:SOL muscle
refix ratio. (Adaptedfrom Myklebust.2.3)
muscle reflex ratio for Achilles tendon taps, and the ratio was higher
than in the healthy adult in all tests
(Fig, 6B). For children aged 1 to 11
months, the largest TA:SOL muscle
reflex ratio was 3.34 + 5.32 (repre-
senting 14 tendon taps for an 8monthald child) and the smallest
reflex ratio was 0.15 ? 0.07 (representing 15 tendon taps for a 10monthald child).23
Physical TherapyNolume 70, Number 3/March 1990
The period from 11 to 24 months of
age is the time when the children
learned to walk independently. During this time period, the mean TA:SOL
muscle reflex ratios were larger than
the mean values for adults. By age 4
to 6 years, the mean TA:SOL muscle
reflex ratio for each child, which
ranged from 0.17 to 0.05, was
approaching or comparable to the
mean adult values.23 These measures
need to be validated in a larger population of healthy children. Furthermore, the significance of these data
remains to be identified with respect
to changes in locomotor slull acquisition and the ability to hop, jump, and
perform tandem ("heel-toe") walking.
Postmyotatic Responses and
Voluntary Reaction Times in
Healthy Children
Bawa evaluated changes in the shortlatency (cnyotatic reflex) and longlatency (postmyotatic reflex)
responses and simple reaction times
of wrist flexor muscles in children
from 2 to 10 years of age.45Onset of
reflex responses was only slightly different in the 2- to 6-year-old subjects.
In children aged 2 to 6 years, the
duration of postmyotatic responses
was longer than in the adult; by age 8
years, this measure was in the range
of the healthy adult. By 10 years of
age, "simple" voluntary reaction
times**resembled those for adults.
Neural processing for simple voluntary reactions is more complex than
for reflex responses, and it appears to
develop later in childhood. This
finding may be due to the gradual
developnlent of supraspinal structures
or inhibitory spinal mechanisms,
increased central conduction velocities, or more effective synaptic transmission. Bawa asserts that the "hardwired" circuitry of reflexes appears to
develop earlier than the "open" circuits used in voluntary tasks.45
Myotatic Reflexes in Patients with
Cerebral Palsy
The myotatic reflex has been compared in patients with spasticity secondary to central nervous system
insults acquired in the perinatal
period and adulthood.5.44 Electromyographic activity evoked during
rapid mechanical dorsiflexion of the
ankle joint in patients with CP (eg,
birth onset injury to the CNS) differs markedly from that of the
healthy adult and patients with
stroke, incomplete spinal cord
injury, or traumatic head injury (eg,
insults to the mature CNS). In
severely handicapped adults and
children with CP, a strong SOL muscle myotatic reflex is accompanied
by simultaneous activation of the
antagonist TA muscle (Fig. 2). This
pattern of reciprocal excitation
evoked by forced ankle rotation is
in marked contrast to the reciprocal
inhibition normally seen. Reciprocal
excitation in patients with perinatal
CNS injuries has been confirmed by
studies of tendon jerk reflexes46 and
H-reflexes using concentric needle
EMG electrodes.5
Cerebralpalsy is classically defined as
brain injury that occurs during the
perinatal period. However, the
stretch-reflex behavior in severely
handicapped patients with CP with
reciprocal excitation suggests that the
definition of the disease may need to
be revised. A fundamental developmental error in neuronal interconnections of the spinal cord may exist in
patients with CP.5 This hypothesis
implies that reciprocal excitation in
patients with CP reflects functionally
disordered spinal cord circuitry.
These data suggest that damage to the
immature suprasegmental structure
may impose a secondary developmental disorder on the spinal cord. This
abnormality could represent an emer-
**"Simplen is contrasted to "choice" reaction studies. In a simple reaction paradigm, the subject is
instructed to make a voluntary movement in o n e direction only. In a choice reaction test, the subject is instructed that his o r her movements will be made in o n e of two (or more) directions, such
as wrist flexion o r extension. A visual cue or' target is generally used to specify the direction (and
distance) of movement; an auditory cue may be given to prepare the subject for the visual cue.
Physical TherapyNolume 70, Number 3/March 1990
gent pathological condition that develops subsequent to perinatal injury
(Fig. 3).5 It may also indicate a failure
of normal maturation in which the
pathway of reciprocal excitation
would be suppressed. To distinguish
between these alternatives, the pattern
of myotatic reflex responses in
healthy infants and in infants at risk
for CP must be compared and evaluated longitudinally during
development.
Voluntary Lower Limb
Movement and Gait
Normal Development of Motor
Function in Infants and Chlldren
Little information is available on the
neural development of human motor
control or on the development of
neural regulation of locomotion in
children and their ability to adapt to
the environment.47 Bawa45 and Forssberg and Nashner48 have suggested
that changes in supraspinal structures
or in the spinal reflex mechanism
may correlate with the acquisition of
motor slulls. To begin to understand
neural control mechanisms in the
development of motor control, the
kinematics and muscle activity of the
lower extremities have been monitored during lucking and stepping
movements in infants, as well as in
gait in early childhood.
Development of lower limb movements. Electromyographic activity
has been recorded in response to
tactile stimuli in neonates.29 Electromyographic activity and joint kinematics associated with voluntary kicking
and stepping movements have been
monitored in small populations of
infants from birth to the time of first
independent steps.4951 In early
infancy, lower limb movements usually begin without inhibition by antagonist muscles. In contrast, antagonist
inhibition is well-expressed in children between 2.5 and 3 years of age.
Voluntary kicking movements of
infants in the supine position demonstrate close temporal and spatial synchrony of hip, knee, and ankle joint
movements. These rhythmic kicking
196 / 59
movements are associated with simultaneous activation of agonist and
antagonist muscles.29~50~~
The reciprocal organization of antagonist muscle
contractions during voluntary movements reportedly develops gradually
during the first year. The processes of
excitation and inhibition appear to
undergo continuous development and
maturation during early childhood.
Voluntary limb movements in healthy
neonates may differ from those of the
adult because descending pathways
may not be complete,49 spinal inhibition may be variable:' and facilitation
of the CNS may outweigh inhibiti0n.~7J~
In addition to neural mechanisms, the changes in "biodynamic"
properties of body segments during
normal growth and development may
contribute to the evolving character of
voluntary limb movements.50
Interactions between limb biomechanics and neural systems are not
well-understood, and they may be
even more complicated when neural
control is impaired, as in patients with
CP. As higher levels of organization
are achieved in normal development,
neural systems probably undergo d s appearance and remodeling of earlier
networks, development of inhibition,
and changes in connection of sensory
and motor channels in response to
the rivalry between developing neural
~atterns.5~
Motor development
appears to be uneven in character.
Major reorganizations in function
probably undergo regressions and
transformations, but the underlying
neural mechanisms are not known.50
Development of postural-control
strategies in stance. Our understanding of the neurophysiological
bases for the development of equilibrium in children is fragmentary. Forssberg and Nashner studied strategies
used to maintain upright standing
when the support surface and visual
conditions were changed in children
aged 1.5 to 10 years.48 Children
younger than 7.5 years of age were
unable to suppress responses because
of conflicting orienting information
and often lost their balance. When
evaluated by EMG recruitment patterns, all the children made postural
adjustments and used strategies similar to adults. However, the children's
EMG responses were more variable
and slower than those of adults. In
children, the stereotyped automatic
postural adjustments of lower limb
EMG recruitment patterns are interpreted as evidence for central networks within lower levels of the
motor hierarchy that control walking
and standing. The variability in
responses in children under 7 years
of age is evidence that adaptive mechanisms are undeveloped. If the automatic postural system is an elementary unit of motor action that can be
integrated into complex behaviors,
then the performance limitations of
the child result from his or her inability to systematically coordinate elementary units of action into a complex act.43
Berger et a1 report that the pattern of
coaaivation of antagonist SOL and TA
muscles is predominant when children first change to a bipedal gait
from quadrupedal locomotion (crawling); the EMG pattern later becomes
reciprocally organized when independent wallung and running develop.47
The authors suggest muscle coactivation at this early stage of development
seems to be less related to propelling
the body forward in locomotion, but
may be important in maintaining the
body's equilibrium in the upright
posture.
Development of gait patterns.
Children demonstrate the ability to
walk unsupported at about 1 year of
age.'.5=54 Children walk independently as early as age 9 months
and as late as 17 months.1.52.53 Children who do not walk by age 18
ttVolume conduction of EMG signals from small infant limbs cannot be excluded as a contributing
factor. However, the relative amplitudes and waveforms of antagonist EMG signals are not constant
in one infant. Therefore, as in studies of the tendon jerk reflex in neonates, it is unlikely that the
EMG responses recorded in normal-kicking infants are attributable to volume conduction alone.
601 197
months are usually evaluated for
developmental delays.'
Gait patterns of children have been
studied on level ground52.53.55.56 and
using a treadmill with surface EMG
recordings.4,47,57Forssberg and Wallberg tested children as young as 5
hours of age and as old as 12 months
of age." Limb movements were
recorded via light-emitting diodes
placed on joints of the lower limbs,
and surface EMG responses were
recorded from antagonist limb muscles. Reaction forces were recorded in
separate trials on a force plate. Burnett and Johnson tested healthy children from 9 months to 11 years of
age and compared joint kinematics
with cinematography and
electrogoniometry.52~53Using cinematography and surface EMG recordings,
Berger and colleagues studied gait in
healthy children aged 6 months to 10
years and in children with CP.4.47
Ankle joint angles were measured by
goniometry, and footswitch&swere
used to record foot contactitime.
Neonatal gait patterns and stepping
in the first 6 months. Newborn infants
demonstrate a primitive walking pattern, with extreme hip flexion followed by rapid placement of the
forefoot.57 In stance, the limb cannot
fully support the body or propel it
forward. This sequence of events has
been attributed to a "spinal locomotor
generator" (ie, "central-pattern generator"). In the proposed neural network, basic activity is generated in the
spinal cord; supraspinal centers provide only minor influences.57The
early foot contact pattern seen in
infancy resembles a digitigrade
pattern.
Berger et a1 reported that, in the 6month-old infant, forefoot contact
with the ground causes a short, quick
dorsiflexion of the ankle with a fast
stretch of the slightly preactivated calf
mu~cles.~7
~lectrom~o~ra~hic
responses were recorded 25 to 30
msec after the onset of stretch at
amplitudes two to three times the
amplitude of tonic EMG activity.
Physical TherapyNolume 70, Number 3March 1990
Electromyographic responses in
young infants are irregular and
exhibit a high degree of coactivation.
The TA muscle is active throughout
the step cycle.47.57The gastrocnemius
muscle is active prior to foot contact.
This fact has been taken as evidence
against a 1:eflexively induced response
and as evidence in favor of a "central
program" for the control of movement patterns.57
Berger et a1 have characterized the
"immaturity" of the irregular early
stepping pattern of 6-month-old
infants by three features: 1) Coactivation of an.tagonist muscles of the leg
is prominent and becomes less pronounced when independent steps are
first taken; 2) the amplitude of the TA
muscle's :EMG response during the
swing p h s e of gait is often larger
than the gastrocnemius muscle's EMG
response in the stance phase of gait;
and 3) large-amplitude solitary bursts
of EMG activity are evoked, primarily
7
in the gastrocnemius m ~ s c l e . ~These
EMG responses are associated with
rapid ankle joint movements and,
based on constant onset latencies,
appear to represent reflex-evoked
EMG responses. These data recorded
during early stepping suggest that
immature gait patterns are under spinal control and may be reflexive.
-
NORMAL CHILD (D.M.)
SUPPORTED WALKING
INDEPENDENT WALKING
I- l SEC-4
LEFT LWEI)
&*
SI
'-,
mwcrc:
Y
-
-
W
I
I-
&*
LIMB
I amI
-
I
H
--I
I
H
-4
I
HEEL
0
H - I
TOE
N m l gait patterns in thefirst 7
years. Sutherland et a1 described five
kinematic: gait characteristics that
change in normal childhood developyears): me duration
ment (age
of single--limbstance increases with
age (especially up to age 2.5 years);
2 ) walking velocity increases steadily
(especially up to age 3.5 years);
3) cadence (and its variability)
decreases with age; 4) step length
increases (especially until age 2.5
years); and 5) the ratio of body width
to stride widthss increases rapidly
until age 2.5 years, increases more
slowly until age 3.5 years, and then
plateaus. Furthermore, the "step factor" (step length divided by limb
o
, s & ~ m ~ s m ~
Ifc
IFC
Ifc
IFC
IFC
IFC
~
IFC
S
S IW
IFC
sIFC
Fig. 7. Displacementpatterns of the rght lower limb during supported walking and
independent walking of a healthy child. Patterns were measured at 0.07-second intervals through two successive walking cycles. Walking cycles began and ended at the
instant of initiulfloor contact (IFC) and consisted of one period of stance (St) and one
period of swing (Sw). For sagittal rotation patterns, upward deflections on the ordinate
representflemon (FI) and downward deflections represent extension (Ex). Flexion of the
ankle is dotstJltxion; extension of the ankle is plantarJlexon. For heel and toe patterns, ordinate values indicate distance of heel target or toe target from floor (0 on
ordinate scale). (Reprinted with permision from Statham and Muma-y and J B L@pincott C0.59)
length) increases during the first 4
years of life and is suggested as a
measure of neuromuscular
maturation.58
**The ratio of body width to stride width is computed from the "pelvic span," measured from the
level of the anterior superior iliac spines, and from the "ankle spread," the distance between left
and right ankle centers during double-limb support.
Physical TherapyNolume 70, Number 31March 1990
Statham and Murray also identified
differences in hip and ankle flexion
and extension patterns and vertical
trajectory of the heel and toe in early
walking patterns of children (Fig. 7).59
Mature patterns of heel-strike, kneeflexion wave (knee flexion after heelreci~strike!
rocal arm swing, and joint angle
198161
rotations throughout the gait cycle are
acquired by the age of 3 years, before
the development of mature cadence,
step length, and walking speed. A
longer step length, not greater step
frequency, is responsible for
increased walking velocity with
growth and maturation. Inadequate
step length in the immature child
appears to be due to lack of stability
in the supporting limb. Sutherland et
a1 suggests this inadequate step length
may be the result of lack of balance,
weak ankle plantar-flexor muscles
(which would prevent undue drop of
the center of mass of the body and
allow the body to be extended forward beyond the point of support), or
lack of control of these muscles.5~
Electromyographic studies of young
children demonstrate that muscle
activation changes with age.-'.47.58
Children younger than 2 years of
age demonstrate coactivation of TA
and gastrocnemius-SOL muscle
activity during gait. In children aged
1 to 2 years, the TA muscle's EMG
activity is insufficient to lift the foot
during the swing phase. In these
children, the foot contacts the floor
in the foot-flat position, rather than
with a heel-strike.
The adult-like pattern of reciprocal
recruitment of antagonist muscle activation begins to emerge at about 2
years of age with the appearance of a
true heel-strike." This EMG pattern,
in which the TA muscle's EMG
response is electrically silent during
most of the stance phase, is generally
established and consistent by the age
of 5 or 6 years.
To compare the movement performance of healthy children with that of
children with CP who walk on their
toes, Berger et a1 asked healthy 4- and
6-year-old children to perform a toewalking test.47 In the 4-year-old group,
biphasic EMG potentials were
recorded from the gastrocnemius
muscle at stretch reflex latencies following forefoot contact with the
ground. In contrast, in the 6-year-old
group, contact of the forefoot with the
ground did not evoke a stretch reflex.
Gait patterns in childrm with deuelopmental disorders. Habitual "toewalkers" (eg, patients with CP) contact
the floor with the forefoot. Children
with CP aged 8 years and older demonstrate a digitigrade gait pattern, similar to that seen in I-year-old
children.47 The EMG patterns associated with toe-walking in children with
CP are similar to recordings made
from healthy I-year-old chi1dren:'The
amplitude of the gastrocnemius EMG
response is lower than in healthy children aged 6 years and older, the TA
muscle fails to actively dorsiflex the
ankle during the swing phase of gait,
antagonist muscles of the leg are
coactivated during stance, and large
reflex EMG signals are recorded at
the beginning of the stance phase.
It is significant that Berger et a1 have
identified stretch-reflex-induced EMG
activity during foot contact in older
patients with CP.4' Although this EMG
pattern is similar to early gait patterns
in healthy I-year-old children and in
toe-wallung patterns of healthy 4-yearold children, these stretch-evoked
EMG responses are abnormal in children after about age 6 years. They
suggest that, in children with CP, spinal patterns that control locomotion
are impaired before the children
learn to walk. As a consequence, children with CP use a simpler and
immature locomotor pattern. These
patients appear to lack the ability to
modify EMG firing patterns to adapt
to different environmental conditions
and modulate their walking speed.
Berger et a1 conclude that during normal maturation, stretch-reflex activity
is integrated into preprogrammed
muscle activity.47Locomotor patterns
of older children with developmental
disorders (eg, CP) resemble early gait
"The relationship between the EMG patterns evoked in gait and in tendon jerk reflex trials has
not been specifically addressed in this context. Preliminary studies suggest that reciprocal excitation is still evocable hy tendon tap in 2- and 3-year-old children, but not in children older than 6
years of age."
62 1199
patterns of young healthy children;
the immature patterns fail to be suppressed during development.
Movement Deficits in Patients
with Spastlclty
The effect of impaired stretch reflexes
on the performance of voluntary tasks
requires further study. In our
laboratory,* patients with spasticity
secondary to adult-acquired injuries to
the CNS (eg, stroke), did not demonstrate stretch-evoked reciprocal excitation of SOL and TA muscles, yet they
had limitations in independent ambulation and demonstrated movement
deficits, as revealed by clinical examination. On the other hand, the
patients we tested with perinatal
insults to the CNS did have reciprocal
excitation of SOL and TA muscles,
were severely limited in voluntary
movements of the lower extremities,
and were functionally nonambulatory.
Reciprocal excitation is not a necessary condition for impaired performance of slulled motor tasks, but it
may be a sufficient condition. Tests to
evaluate the relationship between
impaired voluntary movement and
stretch-evoked reciprocal excitation
remain to be performed.
Corcos et a1 evaluated the ability of
patients with spasticity secondary to
adult-onset CNS iquries to make
accurate, rapid ankle dorsiflexion and
plantar-flexion movements over different distances to a target.7 In three
of the eight patients tested, dorsiflexion evoked velocity-dependent
activation of the antagonist (SOL)
muscle, which impeded the movement, and the limb reversed the
direction of movement (Fig. 8). The
authors propose that this EMG activity
is reflexive because it is highly synchronized with the limb movement,
has a large peak amplitude, occurs
about 50 msec after the initiation of
movement, and is velocity dependent.
These neurophysiologic criteria must
be met to consider these EMG
responses as reflexes.
It is hypothesized that in some
patients with spasticity, hyperactive
stretch reflexes in the SOL muscle are
Physical The:rapyNolume 70, Number 3lMarch 1990
ing the execution of voluntary movements; therefore, these reflexes may
modulate movement performance.
Figure 8 demonstrates that in one
patient, the voluntary dorsiflexion
movement is initiated by a typical
EMG burst in the agonist (TA) muscle.
The delay from the onset of the TA
muscle's EMG response to the onset
of dorsiflexion (determined from the
velocity trace) is about 45 msec. The
further delay to the antagonist (SOL)
muscle burst is another 50 msec. Dorsiflexion is arrested in another 80
msec. The latency and pattern of the
SOL muscle's EMG response is indistinguishable from what is observed if
the ankle were being passively dorsiflexed by a torque motor.5 The magnitude of the stretch-evoked reflex in
the SOL muscle is proportional to the
stretch velocity, and the latency
decreases with increasing stretch
velocity. It is proposed that increased
velocity in these voluntary movements
results in an antagonist TA muscle
EMG burst by stretch reflex mechanisms. This EMG activity is often sufficient to arrest the movement and, in
some cases, to reverse the direction
of movement.
Fig. 8. Recordingsfrom agont3t (tibialis anterior [TA]) and antagonist ( s o h
(SOL]) muscles, with position and velocity
projles for an I8degree ankle dorsiflexion movement to an 8-degree target
from an adult with qastic cerebral paly.
Electrom~lographicmeasurements are in
a r h i ~ r units;
y
joint angle is measured
in degrees, and velocity is measured in
degrees per second. (Reprinted with permhion fiom Corcos et a1 and Oxjord
UniversiQ Press Inc. 7 )
not incidental to voluntary
movements but instead play a causal
role in the execution of those movements. In other words, in some
patients with spasticity, hyperactive
stretch reflexes may be activated dur-
The presumed contributions of the
stretch reflex to antagonist muscle
activity in healthy individuals and in
patients with spasticity remain to be
determined. However, the patients
Corcos et a1 have tested have reflex
excitabilities that are greater than normal, which is to their distinct
disadvantage.' Some individuals with
impairments of voluntary movement
may have learned an adaptive mechanism to avoid the problems imposed
by hyperreflexia: By slowing their
movements, they can reduce their
rate of movement to the preferred
level.
The role of stretch-evoked reciprocal
excitation in modulating voluntary
movements remains to be evaluated.
The patients with CP in whom Myklebust et a1 identified reciprocal excitation were unable to actively dorsiflex
and plantar flex the ankle more than
a few degreess; therefore, the authors
cannot comment on the impact of
reciprocal excitation in modulating
Physical TherapyNolume 70, Number 3/March 1990
voluntary movements in these
patients. Berger et a1 have suggested
that patients with CP who walk on
their toes appear to lack the ability to
modify EMG firing patterns to modulate their walking speed.47Whether
these patients also have reciprocal
excitation of SOL and TA muscles has
not been determined by tendon jerk
reflex studies. It is possible that both
reciprocal excitation and hyperreflexia of spasticity interfere with the
execution of rapid voluntary movements because movements that are
"too fast" evoke a stretch reflex and
reverse the direction of movement. It
is also possible that patients with spasticity "intentionally" move slowly
because their impaired stretch
reflexes do affect the execution of
movements. The possibility of differential effects on voluntary movement
performance of reciprocal excitation
and hyperreflexia has not been
assessed. The relationships of
impaired stretch reflexes and abnormal voluntary limb movements,
including gait, will require further
study in patients with spasticity. The
development of stretch reflexes and
the impact that reflexes may have on
the acquisition of normal motor and
locomotor skills will also need to be
tested in healthy and developmentally
delayed children.
Summary
As previously stated, Bawa suggested
that the "hard-wired" circuitry of
reflexes appears to develop earlier
than the "open" circuits used in voluntary tasks.45 Studies of the stretch
reflex in infancy and childhood also
suggest that even the stretch reflex
pathways may not be "hardwired,"22.23.34 as previously described
by classical studies of neurophysiology. That is, the spinal pathways of
reciprocal inhibition have characterized our understanding of spinal cord
circuitry for a hundred years. However, studies of ddferences in myotatic
reflex responses in infants and children suggests that spinal cord circuitry in normal early development
may be more complicated than the
simple spinal pathway of the healthy
adult. Plasticity of the "wiring" of the
spinal cord may help us explain the
existence of reciprocal excitation in
infancy and the apparent modulation
of reciprocal excitation in early childhood until the pattern of reciprocal
inhibition emerges later in childhood.
Studies of the healthy neonate suggest
that stretch-evoked reciprocal excitation and reflex irradiation may be
properties of the normal spinal cord
in early development, before the
acquisition of motor skills. In the
healthy infant, the pathway of reciprocal inhibition may develop later, o r it
may be present at birth but with a
higher threshold than the pathways of
reciprocal excitation and reflex irradiation. The normal spinal cord pathway of reciprocal inhibition may fail
to develop in children with CP, or
abnormal suprasegmental structures
may foster the persistence of the
reciprocally excitatory pathways.
The possibility of the causal role of
reciprocal excitation and reflex irradiation in impaired ambulation in children with CP requires further study.
Precise relationships between reciprocal excitation (and reflex irradiation)
and impaired voluntary movements
have not yet been determined in
patients with CP or spasticity secondary to adult-onset CNS injuries. However, reciprocal excitation and reflex
irradiation may be a sufficient,
although not a necessary, cause of
impairments in skilled movements.
Measures of the myotatic reflex and
gait in children may help us understand the physiologic mechanisms
of motor control in normal early
development, as well as the pathophysiology of delayed and abnormal
development in children with
perinatal-onset CNS injuries. The
changing pattern of reciprocal excitation in the healthy child may have
a direct impact on the time that
independent ambulation begins;
failure of the CNS to suppress o r
inhibit this functional pathway at an
appropriate time may make independent ambulation impossible.
Correlated studies of tendon jerk
reflexes and kinematic and EMG mea-
64 / 201
sures during gait in healthy children
and in children with CP could be
used to construct an objective index
of development. Berger et a1 have
demonstrated that the antagonist leg
muscles of children with CP who walk
on their toes are coactivated during
stance and that an abnormal burst of
SOL muscle EMG activity is evoked at
a short latency after the toe contacts
the floor.47Because this burst of SOL
muscle EMG activity occurs at a short
latency following the toe contact and
the response is obligatory and stereotypic, this abnormal EMG activity in
gait is presumed to result from an
abnormal spinal reflex. Whether these
same children have reciprocal excitation evoked by tendon jerk reflexes
has not been determined.
Coexistence of stretch-evoked reciprocal excitation and abnormal reflex
EMG activity in gait is not sufficient to
demonstrate that the same spinal
reflex pathways are responsible for
these two types of abnormal behavior
or that reciprocal excitation causes
toe-walking. Moreover, we may never
be able to prove the anatomic or
physiologic mechanism of either
reciprocal excitation or reflex EMG
responses in gait.
The same caveats apply to identification of patterns of tendon jerk
reflexes and kinematic and EMG
changes during normal childhood
development. That is, if reciprocal
excitation disappears (or decreases
to some low o r infrequently triggered level) at the same time children make their first independent
steps, this fact does not prove that
these events are related. The coexistence of two events in time does
not guarantee a causal role o r that
these events are correlated.
However, without records of both
tendon jerk reflex data and gait data
in children, we will not be able to
evaluate the hypothesis that reciprocal
inhibition must be a dominant feature
of spinal cord circuitry at a critical
time in human development for children to be able to learn to take steps
and walk independently and without
deviations. Preliminary studies to
address this issue are being
conducted.GO*
The identification of a "template" of
normal development of motor coordination, by tests of tendon jerk reflexes
and gait, could provide a method of
screening developmental delays or
disabilities in children as well as a
predictive index of development for
early assessment of neurodevelopmental delays of locomotor skills.
Such a template could also provide an
objective assessment tool to evaluate
the effectiveness of early therapeutic
intervention in children with motor
delays. If this template of motor
development can be designed, then
we may be able to make better recommendations about therapeutic
interventions to minimize motor
handicaps.
The clinical utility of such investigations of the myotatic reflex and gait in
children may be understood by the
following hypothetical scenario. Suppose we have identified that, in children aged 18 to 24 months, the persistence of reciprocal excitation or
reflex irradiation (monitored in tendon jerk reflex studies) is consistently
associated with persistent obligatory
toe-walking, with abnormal reflex
EMG responses evoked at foot contact, and with impaired velocity profiles at the knee and ankle. We might
then develop biofeedback exercise
programs61 or inhibitory casting
methodsG2.@or evaluate other pharmacologic or surgical methods that
may modulate the abnormal stretch
reflexes in these children. If methods
are developed to modulate abnormal
reflexes and minimize gait abnormalities in 2-year-old children, then we
may introduce these therapeutic measures as a preventive therapy in
younger children. We may be able to
use longitudinal tendon jerk reflex
evaluations as an early identification
measure to screen children of about 1
year of age who are "at risk" for toewalking and other gait abnormalities
and as a method of deciding which
children will benefit from this early
preventive therapy.
Physical TherapyNolume 70, Number 3/March 1990
How children construct coordinated
actions or what neurological, psychological, and environmental conditions
are essential for the development of
motor slulls is largely unknown. Maturation is necessary,"* but it is probably
not sufficient for human motor
development,"5 as witnessed in the
individual. variability in achieving
motor milestones. Similarly, experience is not a sufficient condition for
motor slull acquisition, such as learning to walk. Although we do not
understand all of the controlling circumstances of motor skill acquisition,
research on motor development of
children has identified the following:
1. The onset of voluntary motor skills
does not occur if primitive reflexes
(and a.ssociated motor automatism) of infancy persist." That
is, conlplex motor skills require
flexibility in their organization and
cannot develop in the presence of
obligarory reflex-induced motor
stereoiypes.
2. The ability to increase the speed
and accuracy of movement
requires practice.
3. At a certain age, children can learn
from past performance to improve
their motor output.
4. The ability to acquire a motor skill
depends on the inhibition of extraneous movements, a process that
requires effort.
5. The brain is required for the
adjustments necessary for motor
coordination.65
In addition to the neural development
required for acquisition of locomotor
skills, Thelen suggests that
biodynamic changes occur in early
childhood.' During the first year of
life, the center of mass moves closer
to the legs, which increases the eficiency of' locomotion. Strength of the
limb and trunk muscles increases for
support, and a balance between flexor
and exte~nsormuscle groups develops.
According to Thelen,
Learning to walk is a complex, gradual
process of maturation of motivation,
the integration of subcortical patterngenerating centers with neural substrate for control of posture and balance, and important changes in body
proportions and bone and muscle
strength.z(pl39)
Acknowledgment
I am indebted to Gerald L Gottlieb,
PhD, for his collaborative efforts in
the scientific endeavors described in
this manuscript.
References
1 Lundberg AE: Normal and delayed walking
age: A clinical and muscle morphological and
metabolic study. In Berg K, Eriksson BO (eds):
Children and Exercise. Baltimore, MD, University Park Press, 1979, vol 10, pp 23-31
2 Thelen E: Learning to walk is still an " o l d
problem: A reply to Zelazo (1983). Journal of
Motor Behavior 15:139161, 1983
3 Dietz V: Role of peripheral aEerents and
spinal reflexes in normal and impaired human
locomotion. Rev Neurol (Paris) 143:241-254,
1987
4 Berger W, Quintern J, Dietz V: Merent and
efferent control of stance and gait: Developmental changes in children. Electroencephalogr Clin Neurophysiol 66:244-252, 1987
5 Myklebust BM, Gotrlieb GL, Penn RD, et al:
Reciprocal excitation of antagonistic muscles
a a differentiating feature in spasticity. Ann
Neurol 12:367-374, 1982
6 Berger W, Horstmann G, Dietz V: Tension
development and muscle activation in the leg
during gait in spastic hemiparesis: Independence of muscle hypertonia and exaggerated
stretch reflexes. J Neurol Neurosurg Psychiatry
47:1023-1033, 1984
7 Corcos DM, Gottlieb GL, Penn RD, et al:
Movement deficits caused by hyperexcitable
stretch reflexes in spastic humans. Brain
109:1043-1058, 1986
8 Inman VT, Ralston HJ, Todd F: Human Walking. Baltimore, MD, Williams & Wilkins, 1981
9 Dietz V. Quintern J, Berger KT:Corrective
reactions to stumbling in man: Functional significance of spinal and transcortical reflexes.
Neurosci Lett 44131-135, 1984
10 Greenwood R, Hopkins A: Monosynaptic
reflexes in walking man. J Neurol Neurosurg
Psychiatry 40:448454, 1977
11 Llewellyn M, Prochazka A, Vincent S: Transmission of human tendon jerk reflexes during
stance and gait. J Physiol (Lond) 382:82P, 1987
12 Pierrot-Deseilligny E, Bergego C, Mazieres
L: Reflex control of bipedal gait in man. Adv
Neurol39:699-716, 1983
13 Stein RB, Capaday C: The modulation of
human reflexes during functional motor tasks.
TINS 11:32%332, 1988
14 Tatton and Lee, referred to in Brooks VB:
The Neural Basis of Motor Control. New York,
NY, Oxford University Press Inc, 1986
Physical TherapyNolume 70, Number 3/March 1990
15 Jaeger RJ: Stretch-evoked Myoelectric
Responses at the Human Wrist. Doctoral Dissertation. Urbana, IL, University of Illinois,
1981
16 Gottlieb GL, Agarwal GC: Response to sudden torques about ankle in man: Myotatic
reflex. J Neurophysiol 42:91-106, 1979
17 Burke D, Grandevia SC, McKeon B: Monosynaptic and oligosynaptic contributions to
human ankle jerk and H-reflex. J Neurophysiol
52435448, 1984
18 Lloyd DPC: Conduction and synaptic transmission of reflex response to stretch in spinal
cats. J Neurophysiol 6:317-326, 1943
19 Agarwal GC, Berman BM, Lohnberg P, et
al: Studies in postural and control systems: 11.
Tendon jerk input. lEEE Trans Syst Sci Cybernet 6:122-125, 1970
20 Gottlieb GL, Agarwal GC: Effects of initial
conditions on the Hoffmann reflex. J Neurol
Neurosurg Psychiatry 34:225230, 1971
21 Myklebust BM, Gottlieb GL, Agarwal GC:
Orientation-induced artifacts in the measurement of monosynaptic reflexes. Neurosci Lett
48:223-230, 1984
22 Myklebust BM, Gottlieb GL, Agarwal GC, et
al: Stretch retlexes in children. Soc Neurosci
Abstr 10:915, 1984
23 Myklebust BM: On the Tendon Jerk Reflex
in the Human iieonate. Doctoral Dissertation.
Chicago, IL, Rush University, 1986
24 Gottlieb GL: Interactions Between the Voluntary and Postural Mechanisms of the Human
Motor System. Doctoral Dissertation. Urbana,
IL, University of Illinois, 1970
25 Guiheneuc P: The use of monosynpatic
retlex responses in man for assessing the different types of peripheral neuropathies. In
Desmedt JE (ed): Motor Control Mechanisms
in Health and Disease. New York, IVY, Raven
Press, 1983, vol39, pp 927-949
26 Goodgold J, Eberstein A: Electrodiagnosis
of Neuromuscular Diseases. Baltimore, MD,
Williams & Wilkins, 1977
27 Mayer RF, Mosser RS: Excitability of motorneurons in infants. Neurology 19:932-945,
1969
28 Mayer RD, Mosser RS: Maturation of
human reflexes. In Desmedt JE (ed): New
Developments in Electromyography and Clinical Neurophysiology. Basil, Switzerland,
S Karger AG, Medical and Scientific Publishers, 1973, vol 3, pp 294-307
29 Prechtl HFR: Exteroceptive and tendon
reflexes in various behavioral states in the
newborn infant Biol Neonate 11:159175,
1967
30 Thomas JE, Lambert EH: Ulnar nerve conduction velocity and H-reflexes in infants and
children. J Appl Physiol 15:l-9, 1960
31 Vecchierini-Blineau MF, Guiheneuc P:
Excitability of the monosynaptic reflex pathway
in the child from birth to four years of age. J
Neurol Neurosurg Psychiatry 44:309-314, 1981
32 Hodes JR, Gribetz I: H-reflexes in normal
human infants: Depression of these electrically
induced reflexes (EIRs) in sleep. Proc Soc Exp
Biol Med 110:557-580, 1962
33 Vecchierini-Blineau MF, Guiheneuc P: Electrophysiological study of the peripheral nervous system in children. J Neurol Neurosurg
Psychiatry 42:753-759, 1979
34 Myklebust BM, Gottlieb GL, Agarwal GC:
Stretch reflexes in human infants. Dev Med
Child Neurol 28:440449, 1986
35 Prechtl HFR: The behavioral states of the
newborn infant: A review. Brain Res 76:185212, 1974
36 Snyder RG, Schneider LW, Owings Cl., et
al: Anthropometry of Infants, Children and
Youths to Age 18 for Produce Safety Design
SP-450. Warrendale, PA, Society of Automotive
Engineers, 1970
37 Goeschen K, Purta M, Rothe J, et al: Measurement of motor nerve conduction velocity:
Precise method of estimating maturity in newborns. Br J Obstet Gynaecol 9061-68, 1983
38 Bagust J , Lewis DM, Westerman RA: Polyneuronal innervation of kitten skeletal muscle.
J Physiol (Lond) 229241-255, 1973
39 O'Brien RAD, Ostberg AJC, Vrbova G:
Observations on the elimination of polyneuronal innervation in developing mammalian
skeletal muscle. J Physiol (Lond) 282:571-582,
1978
40 O'Donovan MJ, Lee MT: Excitatory sensorimotor connections between anlagonists in the
isolated chick embryo spinal cord. Soc Neurosci Abstr 14:579, 1988
41 Stanfield BB: Postnatal organization of cortical projections: The role of collateral elimination. Trends Neurosci 737-41, 1984
42 Thompson WJ: Changes in the innervation
of mammalian skeletal muscle fibers during
postnatal development. Trends Neurosci 9:2528, 1986
43 Easter SS, Purves D, b k i c P, et al: The
changing view of neural specificity. Science
230:507-511, 1985
44 Gottlieb GL, Myklebust DM: Some effects of
cerebellar stimulation of cerebral palsy
patients: Changes in spinal reflexes and ankle
joint complia~ice.In Myklebust JB, et al (eds):
Neural Stimulation. Boca Raton, FL,CRC Press
Inc, 1985, vol 2
45 Bawa P: Neural development in children: A
neurophysiological study. Electroencephalogr
Clin Neurophysiol 52:24'+256, 1981
46 Gottlieb GL, Myklebust BM, Penn RD, et al:
Reciprocal excitation of muscle antagonists by
the primary aferent pathway. Exp Brain Res
46:454456, 1982
47 Berger W, Altenmueller E, Dietz V: Normal
and impaired development of children's gait.
Human Neurobiol 3:16%170, 1984
48 Forssberg H, Nashner LM: Ontogenetic
development of postural control in man: Adaptation to altered support and visual conditions.
Neuroscience 2:545-552, 1982
49 Gatev V: Role of inhibition in the development of motor coordination in early childhood. Dev Med Child Neurol 14335-341, 1972
50 Thelen E: Developmental origins of motor
coordination: Leg movements in human
infants. Dev Psychobiol 18:l-22, 1985
51 Thelen E, Cooke DW: Relationship
between newborn stepping and later walking:
A new interpretation. Dev Med Child Neurol
29:38&393, 1987
52 Burnett CN, Johnson EW: Development of
gait in childhood: Part 1. Method. Dev Med
Child Neurol 13196-206, 1971
53 Burnett CN, Johnson EW: Development of
gait in childhood: Part 11. Dev Med Child Neurol 13207-215, 1971
54 Grillner S: Control of locomotion in
bipeds, tetrapods, and fish. In Brooks VB (ed):
Motor Control: The Nervous System. Philadelphia, PA, American Physiological Society, 1981,
vol 2, pp 1173-1236
55 Sutherland DH, Olshen RA, Biden EN, et
al: The Development of Mature Walking. Philadelphia, PA, J B Lippincott Co, 1988
56 Sutherland DH: Gait Disorders in Childhood and Adolescence. Baltimore, MD, Williams & Wilkins, 1984
57 Forssberg H, Wallberg H: Infant locomotion: A preliminary movement and electromyographic study. In Berg K, Eriksson BO (eds):
Children and Exercise. Baltimore, MD, University Park Press, 1979, vol 10, pp 3 2 4 0
58 Sutherland DH, Olshen R, Cooper L, et al:
The development of mature gait. J Bone Joint
Surg [Am]62:336-353, 1980
59 Statham L, Murray MP: Early walking patterns of normal children. Clin Orthop 79%-24,
1971
60 Myklebust DM, Gottlieb GL, Tomski MA, et
al: Myotatic reflexes and gait: Relative roles in
early development and successful aging. Soc
Neurosci Abstr 14:263, 1988
61 Harrison A: Spastic cerebral palsy: Possible
spinal interneuronal contributions. Dev Med
Child Neurol 30:76'+780, 1988
62 Hinderer KA, Harris SR, Purdy AH, et al:
Effects of "tone-reducing" vs standard plastercasts on gait improvement of children with
cerebral palsy. Dev Med Child Neurol 30:37&
377, 1988
63 Malouin F, Richards CL, Dumas F, et al:
Interactions in the modifications induced by
prolonged muscle stretch on reflex, voluntary
and semi-automatic muscle activations. Soc
Neurosci Abstr 14:62, 1988
64 Gesell AL, Amatruda CS: Developmental
Diagnoses: Normal and Abnormal Child Dttvelopment-Clinical Methods and Pediatric Applications. New York, NY, Hoeber, 1947
65 Wolff PH: Theoretical issues in the development of motor skills. In: Developmental
Disabilities in Preschool Children. Laurel, MD,
Intellectual Spectrum, 1981
66 Milani-Comparetti A, Gidoni EA: Pattern
analysis of motor development and its disorders. Dev Med Child Neurol 9625-630, 1967
Physical TherapyNolume 70, Number 3lMarch 1990