[tsutomu and kayoko okamoto] development of gait b(bookza.org)
TRANSCRIPT
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evelopmento Gait
by Electromyography
pplication
t
Gait nalysis and Evaluation
sutomu Okamoto Ph.D.
Kayoko Okamoto Ph.D.
Walking evelopment Group
Osaka
apan
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Copyright © 2007 by Okamoto Okamoto
Published by
Walking
evelopment
Group
~ q T O O £ ; P J f ~ p J T
G-S04
Tenno
2-6
Ibaraki-shi,
Osaka
567-0S76, JAPAN
ll
LKING
All rights reserved.
o
part of this publication may be
reproduced or transmitted
in
any
form
or by any means
electronic
or
mechanical including photocopy recording
or any information storage and retrieval system without
permission
in
writing
from
the publisher.
ISBN978-4-902473-05-6
Printed in
apan
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reface
The gait of a human being continues to change over the course of a
lifetime. he first stage is that of neonatal reflex stepping which is
thought to be the origin of bipedal upright walking in human beings.
This then develops into young infant stepping at the age of one
to
two
months followed by inactive stepping and then by voluntary infant
supported walking at the age of six to twelve months. Infants then
acquire independent walking at around the age of one and begin to
acquire mature adult walking at around the age
of
three.
We have analyzed the detailed changes in the development of human
gait employing electromyography EMG) which has enabled us to carry
out motion analysis impossible with conventional methods.
At
present
very little longitudinally analyzed post natal gait development data is
available anywhere in the world because of the difficulty of carrying
out
the necessary experiments.
t
is even more difficult to
record
electromyographically the neonatal reflex stepping of newborn babies
or the moment when babies begin upright independent walking. Even
today the papers that I wrote on this subject in the 1970s and 1980s
continue to be cited.
We have continued up to the present to carry out additional cross-
sectional and longitudinal experiments concerning gait development
from the newborn baby stage to that
of
infant independent walking and
have in the process accumulated much electromyographical data. The
results of our analysis of normal gait development suggest that it can
not only contribute to the explanation and clarification of human bipedal
upright walking but also be applied to various areas
of
research such as
the diagnosis of and therapy for various walking disorders and the
evaluation of the level of gait function restoration and improvement.
We
have gathered together
in
this book the results of our study and
analysis of gait carried out over the last
40
years in the hope that this
rare elctromyographical data concerning
gait development
will
contribute to the further development of this field.
Part I contains our analysis based on movement and muscle activity
of the development and changes
in gait from birth until the age of eight
that is from the stage of neonatal reflex stepping thought to be the
origin
of
bipedal upright walking in human beings through that of the
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acquisition and mastering of infant independent walking to that of the
acquisition of mature adult walking.
Part
II
introduces our application of this to the analysis and evaluation
of gait.
We
have created
An
Index of Gait Instability based on the
results of our analysis of the gait development of infant independent
walking, which we apply to research into the nature of human stepping
and the evaluation of the level of restoration of walking functions
in the
elderly.
We
hope th t this book will prove useful to those engages in gait
studies, not only as a basic reference material analyzing the develop-
ment of gait, but also as a basis for research, analysis and application
in various fields that will help to generate new ideas about human gait.
Tsutomu Okamato
v
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Preface
Contents
ontents
iii
v
Part I Development of Gait -Birth to Age Eight-
1 . Newborn Stepping n Neonates and Young Infants 3
Early neonatal period 1 - 2 weeks) 8
Late neonatal period 3 - 4 weeks) 12
Onset
of
infant period 1- 2 months)
16
Initial infant period 3 - 4 months) 18
Discussion
20
2 . Independent Walking n Infants 5
1st day
of
learning
to
walk
28
2 weeks after learning to walk
30
At
around 1 month after learning
to
walk 32
From 2 to 3 months after learning to walk 34
Subsequent development 36
Standing posture on the 1st day
of
walking 38
Discussion 40
3 From Newborn Stepping to Mature Walking
- Developmental Changes n One Individual-
Neonatal stepping
Young infant stepping
Infant supported walking
Infant walking
Immature child walking: unsettled muscle activity
Mature walking: toward a mature pattern
Developmental period of gait
Discussion
45
48
50
5
54
56
58
59
61
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Part II
Application to Gait Analysis and Evaluation
An Index of Gait Instability
67
4
An
Index of Gait Instability
Based on the Development of Independent Walking
69
EMG findings during the development of gait
73
EMG activity in unstable walking
79
Criteria for Instability
84
n
Index of Gait Instability 86
5.
Application of an Index of Gait Instability 1)
Supported Walking in Normal Neonates and Infants
89
Until the 1st month of age
92
From 1 to 4 months of age
94
From 6 to
12
months of age
96
Developmental changes in EMG patterns
98
Application of an index of gait instability to supported walking
in babies
99
Discussion
101
6
Application of an Index of Gait Instability 2)
Recovery of Walking in an Elderly Man after Stroke
107
1 month after the stroke 110
7 months after
the stroke 112
1 year 7 months after the stroke
114
EMG evaluation of walking stability 116
Discussion 117
References
121
Appendix
125
Acknowledgements
131
About the Authors
133
v
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evelopment
of Gait
by lectromyography
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EMG
experiment of infant walking
The electromyographic EMG) recordings were done with a
pen writing
mUltipurpose
electroencephalograph, using surface electrodes 5
mm in
diameter. The skin at each electrode
locus was scratched lightly with a needle, reducing the resistance between pairs of electrodes
to less than 5000
n
Okamoto et
aI
, 1987).
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Neonatal stepping at weeks afte birth
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The purpose of this study was to examine the develop
mental
changes
in the
functional
mechanisms of leg
muscles in newborn stepping over the first 4 months in ten
normal neonates Neonatal stepping in the first month
showed excessive co-activation, that is, co-contraction pat
terns of
mutual
antagonists appeared especially during
stance phase. The discharge patterns of co-contraction in
neonatal stepping began to change to reciprocal patterns in
young infant stepping after the first month), but excessive
muscular activities associated
with a
slightly
squatted
posture
and forward lean still remained . Strong muscle
activities of leg extensors due to a parachute reaction of the
legs before floor contact, not seen in the neonatal period,
began to appear in the young infant period from 1 month
of age to 3 months.
e
suggest that these gradual changes
of leg muscular activity in newborn stepping are evoked
by development of balance, postural control, and strength,
thereby modulating the neonatal stepping reflex.
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When a newborn infant is held
under the rms
in an upright
position, well-coordinated walking movements stepping reflex) appear
to be elicited by tactile stimuli on the soles of the feet as they are
placed on the floor Fig.
1-1).
McGraw 1940) and Zelazo
et
al. 1972) have discussed
the
significance of early stepping movements for development
of
adult gait.
Newborn stepping has been an object of
study for a long time. Only a
few attempts so
far,
however, have been made to study characteristics
of newborn stepping by electromyography EMG).
Forssberg 1985) noted that the lateral gastrocnemius showed
strong activity just before the foot reached the floor Fig. 1-2). Because
this was like a digitigrade pattern,
he
concluded
th t
man is
born
with a quadrupedal locomotor program. Thelen
1982,
1987),
however,
did not find any strong activity in the gastrocnemius before floor
contact Fig.
1-2)
. To further study this problem of the EMG pattern
in
the gastrocnemius before foot contact in stepping, it would be
instructive to record
EMG
data during stepping not only in the neonatal
period up to 1 month of age),
but
also in the young infant period
after 1 month of age).
We
have thus closely examined the characteristics of newborn
stepping
in
ten babies during both neonate and young infant periods
in
terms of the functional mechanisms of leg muscles.
Four male and six female neonates were observed from 1 to 4 weeks
after birth. Criteria used for selecting the subjects were that they be
full-term with birth weight between 2500 g and 4200 g. They were
screened by pediatricians to rule out abnormalities and illnesses.
Motor development of each subject was within normal limits.
Fig 1 1. Newborn stepping at 2 days after birth
Development
o
Gait
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EMGs of
all
subjects were recorded from the neonatal period up to
the 1st month of age) to the young infant period from 1 to 4 months
after birth) at intervals of 1 to 4 weeks.
To induce newborn stepping, the examiner held the neonate under
the arms with the soles of the feet touching a horizontal flat surface.
Well-coordinated walking movements were observed from around 1
week after birth to around 3 months. We could not induce stepping
simply at will, but tended to be successful when the infants were
lively,
crying, hungry, or slightly excited Figs. 1-1 and 1-2). For analysis we
selected well-coordinated walking movements consisting of three or
more steps.
The EMGs were recorded from six muscles
in
the right leg
Fig.1-2):
tibialis anterior fA), lateral gastrocnemius LG) , vastus medialis VM),
rectus femoris RF), long head of biceps femoris BF) , and gluteus
maximus GM), and from two to six muscles
in
the left leg, usually the
TA,
LG,
RF,
and BE
GM
: gluteus maximus
Hip extensor)
SF
: biceps femoris
Knee flexor, Hip extensor)
Mutual antagonist:
RF
LG
: lateral gastrocnemius
Ankle plantar flexor)
Mutual antagonist: TA
Fig.
1 2.
Muscles chosen for recording EMG.
RF: rectus femoris
Knee extensor, Hip flexor)
Mutual antagonist:
SF
VM: vastus medialis
Knee extensor)
TA : tibialis anterior
Ankle dorsiflexor)
Mutual antagonist :
LG
Newborn
Stepping
in Neonates and Young
nfants
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Surface electrodes 5 mm
in
diameter were used. To attenuate
artifacts in
the surface electrode recordings, skin impedance was
lowered by scratching loci of the electrodes lightly with a needle before
the
electrodes
were applied Okamoto
et
al., 1987).
he
EMG
recordings
were done with an 18-channel pen-writing electro
encephalograph
60
mm/sec) with the gain set at
12
mm/0.5mV. n
analog pulse signal from the video recording camera
60
frames/sec)
was recorded simultaneously with the EMGs. The walking cycle was
divided into swing phase
SW)
and stance phase
ST)
by the video
recordings.
Movement and EMG recordings obtained during newborn stepping
showed some variations both within and among subjects. Variations
in
stepping form and EMG patterns appeared to depend to some extent
on how the infant was supported. We thus selected as representative
data those movements and
EMG
patterns of stepping that were seen
relatively frequently in the neonatal or young infant period being
observed. For purpose of analysis, longitudinal observations were
divided into early neonatal period from 1
to
2 weeks after birth), late
neonatal period from 3 to 4 weeks), onset of infant period from 1
to
2
months), and initial infant period from 3
to
4 months).
ature adult walking pattern
We need to examine normal stable adult walking to compare with
gait in terms
of
developmental processes. Figure
1-3
shows a typical
EMG of adult walking the subject is a female 29 years of age). From
the basogram, stance and swing phases can be demarcated.
he discharge patterns of the TA and LG, which participate in
movement of the ankle joint, showed an almost reciprocal relationship.
he TA an ankle dorsiflexor) discharged through most of swing
phase and at the beginning of stance phase, whereas the LG an ankle
plantarflexor), which participates
in
push off motion, discharged
in
a
strong burst in the latter part of stance phase. The hip and knee
muscles, VM, RF,
BF,
and GM, acted for shock absorption during the
transition from swing phase to stance.
Development
o
Gait
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Typical MG pattern of normal adult walking
0.5
mv
k ~ j ~ A A j ~ A
26 333 339 346 356 365 372 378 388
Tibialis anterior TA)
Lateral gastrocnemius LG) - + - - - M ~ ~ I
M ' H ~ - - - 1 < Y , \ , ~ - . . . . I ( N J I N ' t - - t -
Vastus medialis VM)
Rectus femoris RF)
Biceps femoris BF)
Gluteus maxim us GM)
Ankle
lantar flexion
orsiflexion
Knee
xtension
lexion
Hip
Extension
Flexion
Basogram
Foot contact FC)
VTR
signal
t
t
*
Swing
Pho e
SW )
Stance hase
ST)
HC FF
Swing
Stance
O
TO
1 sec
. J . _ ' - ' ' ' ' ' ' ' ' ' ' ' ' ' ' ' N t ' ' ' , , , , ' ' ' ' , _ . J , - - * - J I J t r - , , _ , , f . , . , , , J t U l t . , , - - , ~
300 350 400
l ~ (
~ ~
H
Heel Contact)
FF
HO
Foot Flat) Heel Off)
TO
Toe Off)
Fig.
1-3.
Typical adult
EMG
pattern in leg muscles during walking.
Swing phase SW: short phase), Stance phase ST: long phase), Basogram: Foot contact
He,
FF, HO, TO).
Newborn Stepping in Neonates
nd
Young Infants
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ST
sw
Early neonatal period
1
- 2 weeks)
ST
R) ~ · · I · \ · f J · t W ~ ~ t ; ~ i ~
T
L
VM
RF
F
GM
l)
TA
L
,
,
i
I
VM - - - - ~ ~ ~ - - - - - - - - ~ - - - - - - _ - - - - - - - - - - ~ ~ ~ ~ ~ - - - - - - _
F - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - ~ - - - - - - ~ .
STANCE ST)
SWING
SW
)
_e_
_ _
- I 0 5 v
1 week Y.T.)
NEONATAL STEPPING
Fig. 1-4. EMGs of stepping at 1 week after birth Y.T.).
SW: swing phase, ST: stance phase, R): right leg, L): left leg, TA: tibialis anterior, LG: lateral
gastrocnemius, VM: vastus medialis, RF: rectus femoris , SF: biceps femoris, GM: gluteus maximus.
evelopment
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Gait
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Stepping
in
this period was characterized by quick hip flexion
in
which the thigh became approximately horizontal in the first part of
swing phase. The foot was raised forward and dorsiflexed strongly, as
shown in Figures 1-4, 1-5, and 1-6. In the middle part of swing phase,
the leg was often held in the flexed position. Then the foot began to
reach the floor slowly, the knee extending passively along with the hip.
The foot usually contacted the floor with the heel or sole first Fig.
1-7), but in a few instances toe contact was seen. A fairly squatted
posture was often observed during stance phase.
w k after birth Fig.
1-4):
In the beginning of stance phase, no
notable activity was seen
in
the leg muscles examined.
In
single stance
phase, continuous discharges were frequently observed in the TA,
VM,
RF,
and GM, activities not usually seen in adult gait.
he
discharge patterns of the VM and GM were highly consistent, but
activities at the ankle the TA and
LG)
and of two-joint muscles
crossing the knee and hip the
RF
and
BF)
showed slight variations.
That is, at the ankle, a reversed reciprocal
TA+,
LG-) pattern was
observed
in
many cases, but co-contraction TA+, LG+) and reciprocal
TA-, LG+)
patterns were seen
in
some of the subjects. Across the
knee and hip, a reversed reciprocal RF+, BF-) pattern was observed
in
many cases, but co-contraction RF+, BF+) and reciprocal
RF-,
BF+)
patterns were observed in some of subjects. In the first part of swing
phase, continuous discharge in the TA was
seen
in most cases.
Sometimes slight activity of the
RF
was observed in the same phase.
In the latter part of swing phase, when the leg was extending, activities
were hardly seen in the
LG,
VM, RF,
BF,
and GM.
Fig. 1 5. Foot contact of newborn stepping at 2 days after birth.
Newborn
Stepping
in Neonates and Young
nfants
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ST SW ST
(R)
V
, , , /
1 .1/
I , ,
W , / , , , W
I I
W
I I ; , I
......r
TA ,
L ________
__
~ _ _
VM
RF
BF
GM
(L)
TA- \
LG
RF
BF
L
I
ST
SW
1 sec 0 5 mv
2 weeks (A.
I.)
NEONATAL STEPPING
Fig. 1-6.
EMGs
of stepping at 2 weeks after birth
A
. .).
1 evelopment
o
Gait
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w ks after birth
Fig. 1-6 : In the beginning of stance phase,
continuous discharges in many leg muscles were observed more
often than at 1 week after birth, especially in single stance phase.
Continuous discharge patterns of the VM and GM were again
consistent, but EMG patterns of the
TA
and LG and
of
the RF and BF
showed some variations. That is, reciprocal, reversed reciprocal, and
co-contraction patterns were seen in those muscles. In the first part of
swing phase, continuous discharge patterns
of
the
TA
were similar
to
those of 1 week after birth.
In
contrast to the first week, continuous
discharge in the RF was observed during swing phase in many cases.
In the latter part of swing phase, activity in the BF frequently began to
appear before foot contact.
Foot contact Fe)
eel contact with slow
leg
extension
Foot flat with slow
leg
extension
EMGs
of
leg
extensors before floor
contact
Early neonatal period
1-2
weeks after birth)
Fig.
1-7.
Foot contact of stepping in neonatal period
1-2
weeks after birth).
-): no
activity.
Newborn Stepping in Neonates and Young
nfants
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Late neonatal period
3
- 4 weeks)
r t ~ l l t
w
ST
' - H ' 1 ' - 1 V . - - r - - r - - t - . ' - I ~ ' - I - - ' ' - h ' - l - - i - W . , ~ t - H - 1 ' ' ' ' ' ' ' ' ' ' ' i , . . . . J ' ' h ' ' ' ' ~ I ' ' ' ' ' ' ' ~ ~ h - h ' '
(R)
TA_
Wi
LG
.,
VM
RF ,
BF- \
, I I ~
... .
Jill/ILl
'n'
r-
GM
L i A ' M ~ ~ ~ ~ ~ I ' J '
. \
~ ~ ~ ...
L G W ~ ~ ~
,
.; :; 1.; .;, 1 r ' ' W t ' ~
R F . ~
••
. O i . ~ i ~ ~ ' j I ~ '
B F ~ ~
w ~ t ~
ST
SW
se
I
0.5
v
3 weeks
H
. YJ
NEONATAL STEPPING
Fig. 1 .8. EMGs of stepping at 3 weeks after birth
H
.Y.).
2 evelopment
o
Gait
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SW
hS-rT-r-r--rr-h
h----r-r-r--r-,,-...,-,
R ) ~
II
A
LG
VM
RF
SF
GM
(L)
1ft.
I
b ,
'I'
~ ~ i
1
II.
I\,
I.
,
I
~ . , ~ f In ' - \ i N o ' ~
rIP
W
r-
.J.
.'
.'\' ',..
\1 '
/-h-
,I
,1. 1 .1,,,1,,,11,
I
r'lf
TA / J f t O o M i I \ - - ~ - - a W J ' M - - . . - j > , ~ ~ .., ........ I - -
L G ~ ~ ~ - - - - r - - - - - ~ - - ~ ~ ~ ~ ~ -
V M ~ ~ ~ ~ I ~ \ \ \ - \ f i \ ' o J - - . ' t o l \ - - + I I I ~ ~ 1 ' ~ ~ ~ t r
q j . - ' ~ ~ ~ 4 ~ ~ ~ ~ f t J t \ , j r \ -
I I I W I l f I M ~ . r - - - - - - + - - - 1 ' - ~ , ~ f r \ \
G M M M ~ v N ( i ~ / ' - - - + - - ~ ~ ~ ~ ' 4 \ t ' + . ' / i ' U I f , ~ , * , - -
ST
SW
1
sec
0.5
mv
4 weeks (T.
YJ
NEONATAL STEPPING
Fig, 1-9, EMGs of stepping at 4 weeks after birth (T.Y,
,
Newborn Stepping in eonates and Young
Infants
3
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As in the early neonatal period, leg flexion was very active in the
first part of swing phase in this period Figs. 1-8 and
1-9 .
The thigh
was outwardly rotated as it was raised diagonally
in
a forward and
lateral direction and the foot dorsiflexed strongly. Then the foot began
to approach the floor slowly, the knee extending passively along with
the hip. The foot usually contacted the floor with the lateral border
first Figs. 1-10, 1-11, and 1-12), but sometimes the heel, sole, or
forefoot made initial contact. The fairly deep squatting posture of the
early neonatal period began
to
become less pronounced during stance
phase.
and
4
weeks after birth
Figs.
1-8
and 1-9 : Throughout stance
phase, continuous discharges of leg muscles were observed in many
cases. EMG patterns of the VM and
GM
were consistent as in the
early neonatal period. The reversed reciprocal ankle pattern during
stance, seen in neonatal former period, was hardly evident, whereas
the reciprocal and co-contraction patterns became more frequent.
Discharge patterns of the two-joint knee and hip muscles showed
reversed reciprocal, reciprocal, and co-contraction patterns as in the
early neonatal period. In the first
part
of swing phase, continuous
activity was seen in the TA as in the early neonatal period, but weak
bursts of the RF and BF were seen often at the beginning of swing
phase. In the latter part of swing phase, activities began to be seen
in
the LG, VM, RF, BF, and GM in some of the neonates.
L -),
partly +) f - - - - - - r ~
Lateral gastrocnemius
Ankle plantar flexor)
VM H , partly +)
Vastus medialis
Knee extensor)
Lateral border with slow leg extension
EMGs of
leg
extensors
before floor contact
Late neonatal period
3-4
weeks
after
birth)
Fig. 1-10. Foot contact of stepping in neonatal period 3-4 weeks after birth).
-):
no activity, +)
:
noticeable activity.
4
Development o Gait
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Fig. 1 11. Neonatal stepping at 6 days after birth.
Fig. 1 12. Foot contact of neonatal stepping at days after birth.
Newborn Stepping in Neonates
and
Young nfants 5
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Onset o infant period
(1
- 2 months)
SW
ST
- -.-v
· · · · , Wr .... .... r-r-. .- .- ,....W·
,
j , , , , , U , , , , • •
(R)
TA
F
M ~
...
(Ll
T A ' I I A ( / ~ , ~ - ' t ' ' ' ' r ' T M ~ ~ . ~ ~ i ' ' J , r I I I . . ~ ~
I J f I t 4 > ~ J i
ST
SW
sec
0.5
mv
1.5
months
(T. YJ
YOUNG INFANT STEPPING
Fig. 1-13. EMGs of stepping at 1.5 months after birth (T.Y., same subject as in Fig. 1-9).
6 evelopment
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After 1 month, as shown in Figure
1-13,
leg flexion was performed
strongly in the first part of swing phase as in the neonatal period, but
the degree
of
hip flexion tended to decrease slightly. We found mostly
plantarflexion of the foot before floor contact rather than dorsiflexion,
which had been more prevalent in the neonatal period. The foot
usually contacted the floor with the lateral border of the forefoot first
Fig. 1-14). Knee extension began to be performed more actively than
in the neonatal period. A half-squatting posture during stance phase
tended
to
increase.
1 5 months after birth Fig. 1-13): During stance phase, continuous
discharges
of
the
VM
and GM were seen as
in
the neonatal period.
The ankle muscles likewise exhibited reciprocal and co-contraction
patterns as in the late neonatal period. The two-joint knee and hip
muscles showed reversed reciprocal, reciprocal, and co-contraction
patterns, similar to the neonatal period. In the first part of swing
phase, continuous activity of the TA was observed in many instances,
as in the neonatal period. In the beginning of swing phase, weak
activities of the RF and BF were seen often, but not always. In the
latter part of swing phase, activities of the
LG,
VM,
RF,
BF,
and
GM
appeared often before foot contact.
LG
-),
+)
1---+--+-.1
Lateral gastrocnemius
Ankle plantar flexor)
•
oot contact Fe)
Lateral
border of
forefoot with
f st
leg extension
EMGs
of leg extensors before floor contact
Onset
of
young infant period
1-2
months
after
birth)
Fig. 1-14. Foot contact of stepping
n
young infant period 1-2 months after birth).
-),
+)
: instances of no activity and of noticeable activity intermingled.
Newborn Stepping in Neonates and Young
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Initial infant period
3 - 4 months)
SW ST
h J f ...... ;
..
Wrl r r
h'
h
iho
h' h
W I' i
;
.. Wit ,
t o
\-T
(
R)
T A 4 ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ ~
(0
T A ~ ; ~ ~
L ~
•
' ~ ' ; ~
ST SW
t
sec 0 5 mv
3
months
CA
I.)
YOUNG INFANT STEPPING
Fig. 1-15. EMGs of stepping at 3 months after birth (A .I.. same subject as in Fig. 1-6).
8 Development
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In this period Fig.
1-15),
the lower limb flexed strongly in the first
part of swing phase as in the neonatal period, but the total degree of
hip flexion tended to decrease slightly. The foot usually approached
the floor with a more rapid and vigorous extension of the lower limb,
with the toes initially contacting the floor Fig. 1-16). Knee extension
and ankle plantarflexion were visibly active in many case
s.
A half
squatting posture during stance phase became more frequent.
months after birth
Fig. 1-15): During stance phase, continuous
discharges
in
the VM and GM were observed until onset of the infant
period, as mentioned above, but continuous discharges in
the
anteriorly situated TA and
RF
tended to decrease or disappear, leading
to reciprocal patterns
TA- LG+
and
RF-
BF+)
in
most cases. In the
first part of swing phase, strong bursts in the
TA,
RF, and BF were
frequently observed.
In
the latter part of swing phase, strong activities
of the
LG,
VM,
BF,
and GM appeared often. Although strong activity in
the
LG
and VM were observed shortly before foot contact, activities in
the BF and GM were not generally seen. In the course of this period,
co-contraction patterns of the ankle
TA+,
LG+) and the knee and hip
RF+,
BF+), seen fairly often in stance phase in the late neonatal period
and onset of the infant period, gave way to reciprocal patterns TA
LG+ and
RF-
BF+) . Strong activities of the
LG
and VM
in
the latter part
of swing phase, hardly observed during the neonatal period, became
remarkably more frequent.
LG +),
partly -)
f - - - ~
Lateral gastrocnemius
Ankle plantar flexor)
V
+),
partly
-)
Vastus
medialis
Knee extensor)
Forefoot with
fast
leg extension
EMGs of leg extensors before f loor
contact
Initial young
infant
period 3-4
months after
birth)
Fig. 1-16. Foot contact of stepping
in
young infant period 3-4 months after birth).
+) :
noticeable activity, -): no activity.
Newborn Stepping in Neonates and Young
nfants
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iscussion
Although Thelen
et
al.
1982)
reported that when held upright,
newborn infants show well-coordinated walking movement th t
normally cannot be elicited after about 2 months of age, we could
induce infant stepping until around 3 months of life
in
a number of
cases. Forssberg 1985) and Thelen et
al.
1987) pointed out from
movement patterns and EMGs, that the locomotor pattern of the
newborn differs markedly from that of an adult.
From our results, newborn stepping was characterized by active leg
flexion with the thigh becoming horizontal, a somewhat squatted
posture, and variable forms of foot contact with the surface Figs.
1-17
and 1-18). Leg muscle activities in newborn stepping are usually
irregul r
and involve more co-activation th n in adult walking,
especially in stance phase. For example, in single stance continuous
discharge patterns were seen in the knee and hip extensors
VM
and
GM) in neonatal and infant stepping, associated with a progressively
decreasing but ever present squatted posture. These activities in the
leg extensors appear to be attributable to the squatted posture itself
and would thus not be seen in adult gait.
On the other hand, we did observe some similarities
in
leg muscle
activity between newborn stepping and adult gait.
As
swing phase was
beginning, for example, bursts were usually observed
in
the TA during
newborn stepping. Muscle activation seen in flexors of the lower limb
at the onset of the stepping cycle becomes incorporated into supported
walking
seen prior
to
independent
walking,
thence
into
e rly
independent walking, and so on to adult gait. These results suggest
that mature walking may evolve from the newborn movement pattern.
We could see a developmental trend across the neonatal and young
infant periods
in
stance phase and at the end of swing phase. n
stance phase, contractile activity between mutual antagonists varied
among co-contraction TA+ LG+ and RF+ BF+), reciprocal TA
LG+ and RF-
BF+)
, and reversed reciprocal
TA+
LG- and
RF+
BF-)
patterns. The reciprocal pattern tended to appear more often if the
baby happened to be inclined forward and the reversed reciprocal
pattern when the baby was inclined backward. Co-contraction might
be viewed as an intermediate situation between these two tendencies .
2
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evelopmental changes
in
the pattern o newborn stepping
1week Y.
T.)
Neonatal period
~ ~ ~ ~ j
Early.
1- 2
weeks)
A
2 weeks A.I.)
Neonatal period
jjlttf
Early.
1 2
weeks)
B
3 weeks H.Y.)
Neonatal period
tt ttttt
Late. 3 4 weeks)
C
1.5 months H.Y.)
Infant period
r t l
Onset. 1 2 months)
D
3 months A.I.)
Infant period
w ~ ~
Initial.
3 4
months)
E
3.5 months H.Y.
Infant period
r l ~ ~ ~ f
Initial. 3 4 months)
F
Fig. 1-17. Developmental changes in the pattern of newborn stepping.
B: same subject as E.
C:
same subject as D and F.
Newborn Stepping in Neonates
and
Young nfants
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he
reversed
reciprocal
pattern
was
seen
relatively often in
the
early neonatal period first 2 weeks), but the other two patterns became
more frequent
in
the late neonatal period 3rd and 4th weeks) and
as the infant period began 2nd month). In the initial infant period
3rd and 4th months) the reciprocal pattern became more dominant
than the other patterns, although all
three
patterns could still be
observed. Interestingly, this trend anticipates the changes
in
pattern
between mutual antagonists seen as a baby first begins to walk
independently and becomes more stable
in
the ensuing months.
At the end of swing phase in the neonatal period, the
LG
and VM
exhibited no activity until the foot actually touched the floor Fig. 1-18).
The foot reached the floor
in
a relatively passive action of the lower
limb, contacting the floor variously with the heel, entire sole, or lateral
border. Thelen et
al. 1982,
1987) did not find any strong activity in the
gastrocnemius before floor contact
in
the neonatal period. In the
second month, at the onset of the infant period, the LG and VM began
to become active before actual contact of the foot with the floor, with
the lateral part of the forefoot generally touching the floor first. Thelen
et al. 1987) and Forssberg 1985) reported that the gastrocnemius
showed strong activity just before the foot reached the floor
in
the
young infant period. The activities of the LG and
VM
subsequently
became more pronounced shortly before and during floor contact
in
the 3rd and 4th months,
to
the point that one might associate such
activity with the parachute reaction. Milani-Comparetti et al. 1967)
observed from movement analysis that the parachute reaction of the
lower limbs begins to appear at about 4 months after birth. Our
observations, if they are of the same phenomenon, suggest that the
beginnings of the parachute reaction can be found by EMG much
earlier than by visual observation of behavior.
hese changes
in
muscle activity during the stance and swing
phases of newborn stepping represent what might be considered as
the first developmental changes in human bipedal locomotion. Further
research would be necessary to elucidate the extents to which these
changes can be attributed to maturation of balance, postural control,
and strength, as well as to emergence and disappearance of the
neonatal stepping reflex itself.
evelopment
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Neonatal and
young
infant
period
Early neonatal
1-2
weeks
after
birth
Late neonatal
3 4 weeks
after
birth
Young
infant
onset)
1-2 months
after birth
Young infant initial)
3 4 months
after birth
Foot contact
with
leg
extension
Heel
contact or
foot
flat
with slow leg extension
Lateral border
with slow leg extension
Lateral
border
of
forefoot
with
fast
leg extension
Forefoot
with
fast
leg extension
EMGs
of VM and LG
before
floor contact
VM -)
LG -)
VMH, partly
+)
LG -), partly +)
VMH,
+)
LGH. +)
VM +), partly
-)
LG +),
partly -)
Fig.
1-18.
Developmental changes of foot contact
in
newborn stepping.
VM
: vastus medialis,
LG
lateral gastrocnemius, -) : no activity, +): noticeable activity,
-), +): instances of no activity and of noticeable activity intermingled.
Newborn Stepping in eonates and Young
Infants
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onclusion
In ten neonates first seen at 1 to 4 weeks after birth EMGs of
stepping were recorded at 1 to 4 week intervals until around 4 months
of age.
During stance phase in neonatal stepping many leg muscles showed
excessive continuous discharges compared with the adult walking
pattern. Continuous activity was seen in the vastus medialis and
gluteus maximus to maintain a partially squatted posture. Mutual
antagonists in the lower limbs variously showed reciprocal and
co-
contraction patterns during the neonatal period but the EMG patterns
began to shift toward predominantly reciprocal patterns in the young
infant period associated with leaning forward.
In the first part of swing phase activity in the tibialis anterior was
observed in most cases. During neonatal stepping in the latter part
of
swing phase muscular activity was not seen in the lateral gas-
trocnemius or
v stus
medialis but during young infant
stepping
EMG activity in these two muscles became marked before the foot
reached the
floor
suggesting that muscular activities participating
in
active ankle plantarflexion and knee extension began to act as a
precursor to the parachute response of the lower limb.
In summary these muscular activities of the lower limb characterize
the EMG features of newborn stepping. Changes in EMG patterns
during newborn stepping detectable well before corresponding
changes can be visually observed in movement analysis may be the
first signs of development in human locomotion.
4 evelopment
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n order to elucidate electromyographic (EM G charac
teristics of infant walking at the onset of independent gait, we
longitudinally recorded EMGs from muscles of both legs
during the learning process of walking in an infant, from
10
months after birth until about 3 years of age. We found EMG
characteristics of infant gait up to around 1 month after
learning to walk that are not usually seen in adult gait. n
stance phase from foot contact until push off, the role of the
vastus medialis for maintaining stability became clear as a
slightly squatted position was used to lower the
center
of
gravity. Orderly reciprocal or co-contraction patterns of activity
in the
rectus
femoris and biceps femoris or in the tibialis
anterior and gastrocnemius were found to be
related
to
returning the body s center of mass toward its initial position.
n the
latter
half of swing phase, the vastus medialis and
gastrocnemius showed strong activities with the knee extend
ing and ankle plantarllexing for active leg extension to prevent
falling.
hese
characteristically excessive muscle activities
in infant walking are considered to express weak muscle
strength
and an
immature
balancing system. As
months
and years pass, the muscles become stronger and balance
matures, obviating the need for so much myoelectric activity.
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Normal human infants begin to walk independently when they are
about 1 year of age. Thelen et al.
1989) noted
th t
independent
walking emerges when a threshold has been reached for muscle
strength and ability
to
balance, but the baby who has just become able
to walk independently exhibits a pattern notably different from adult
gait. Although a
gre t
deal of investigation
h s been
done on
development of
gait, there are
few
EMG studies in the area. Cross
section l
kinesiologic l EMG studies on the
development
of
independent gait in babies have been performed by Sutherland et
al.
1980), Forssberg 1985), and Thelen et al. (1987), but we have not
seen much longitudinal EMG study on the acquisition of gait outside
of that by Okamoto et
al.
1972, 1983,
1985, 2001,
2003). By means of
both longitudinal and cross-sectional EMG and cinematographic
findings,
we
have reported that specific changes can be observed at
certain times
in
the course of that development. That is, during the
early stage of independent walking, a baby squats slightly while
leaning forward and takes steps with strong active extension of the
legs, exhibiting considerable instability. After this early stage of
independent walking, the baby exhibits increased stability with the
body tilted only slightly forward
childhood walking pattern),
and by 3
years of age the body is upright as in adult walking
adult walking
pattern).
What seem to be most lacking, however, are EMG studies
during the very early stage of independent walking
in
the infant. The
purpose here is to explore a little further the onset of independent
walking in the infant and to determine
EMG
characteristics of infant
walking by longitudinal observations.
The subject was one baby who first began
to
walk independently at
306
days after birth.
We
made longitudinal observations on this child
from the time she first began to walk independently at 10 months after
birth until a stable adult-like walking pattern was achieved at around 3
years of age.
Figure 2-1 shows a representative form of infant walking at the onset
of independent walking, when the infant succeeded to walk 5 to 10
steps without support. Slight knee flexion was often observed in the
supporting leg, the foot base in the double support period was very
wide, and the body s center of gravity was lowered during stance. The
arms were spread apart and elevated.
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The gait in this baby first learning to walk was characterized by
quick hip and knee flexion in which
the
thigh became almost
horizontal
in
the first part of swing phase. The foot was raised forward
and slightly outward, then the foot began to reach the floor quickly,
the knee extending actively along with the hip. he foot usually
contacted the floor with the foot flat and forefoot first, but in a few
instances the heel made initial contact. A squatting posture with the
body inclined forward was often observed during stance phase. We
noticed several other characteristics that differ from adult gait, such as
a wide base at the feet and a high guard position of abducted arms
(Figs.
2-3,
2-5,
2-7,
and 2-9 .
Figures 2-2, 2-4, 2-6, 2-8, and
2-10
show longitudinal developmental
changes of EMG activity
in
the learning process of walking. Compared
with corresponding muscular activities of the adult walking pattern,
excessive muscular activities and variations appeared during the
learning process of infant walking from the 1st day of learning to walk
until 2 or 3 months after learning to walk. In the description that
follows, we focus attention on EMG activity patterns seen
in
the infant
that deviate from normal adult walking and examine developmental
changes in muscle activity related to infant independent walking.
Fig 2 1. Gait pattern at the onset of independent walking
ndependent aiking
in
infants 7
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1st day of learning to walk
fffffr
R)
TA
LG
VM
RF
BF
GM
U
TA
LG
VM
RF
BF
GM
ST
sw
R)
N ~
EXT.
L)
FLE X.
v
KNEE
V
t s
e
0.5
mv
1
st
day of learning
to
walk
Fig. 2-2. EMGs
on
the 1st day of independent walking at 10 months of age).
ST: stance phase,
SW
: swing phase,
R)
: right leg,
L)
: left leg, TA: tibialis anterior,
LG
:
lateral gastrocnemius, VM: vastus medialis, RF: rectus femoris,
BF
: biceps femoris , GM:
gluteus maximus, KNEE EXT: extension, KNEE FLEX: flexion.
8 evelopment
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Figure
2-2
shows a representative excerpt
of
the EMG patterns of
the infant s independent walking on the day when she succeeded in
walking 5
to
10
steps for the first time, at
10
months after birth.
In
stance phase, at the ankle, a pattern of
two
or three alternating
bursts between the
TA
and LG was most prevalent, but co-contraction
of both muscles was also seen frequently.
At
the knee, the VM was
continuously active from foot contact until push
off.
At
the hip and
knee, three types of discharge pattern were seen in the biarticular RF
and BF muscles. One was a reciprocal
RF-, BF+)
pattern
in
which
discharge of the RF tended to decrease or disappear while that
of
the
BF increased. A second was a reversed reciprocal
RF+,
BF-) pattern
in which discharge of the BF tended to decrease or disappear while
that
of
the RF increased. The third was a co-contraction RF+,
BF+)
pattern of the two muscles. When the infant became able to walk
continuously,
we
generally found a reciprocal or co-contraction pattern,
although
we
occasionally observed a reversed reciprocal pattern.
At
the hip, the GM was continuously active.
In
swing phase, the
LG
and VM often showed strong activity
in
the
latter half
of
the phase.
1st day o learning to walk
Fig. 2 3. Foot prints on the 1st day of independently walking at 1 year 1 month).
ndependent aiking
in
infants 9
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weeks after learning
to
walk
ST
sw 10 5
months
R)
TA
LG
VM
RF
SF
GM
L)
TA
LG
VM
RF
SF
GM
ST sw
R)
KN
L)
EXT.
*
LEX
KN
1
se
c
5
v
2 weeks fter learning
to
walk
Fig. 2-4. EMGs at 2 weeks after learning to walk at
10
.5 months).
3
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Figure
2-4
shows representative
EMG
patterns of infant walking at
about 2 weeks after learning to walk at 10
.5 months after birth), when
the infant was able
to
take more than
20
steps.
In stance phase, at the ankle, the earlier pattern of two
or three
alternating bursts between the TA and LG changed to one or
two
alternating bursts, but co-contraction of the
two
muscles was also seen
frequently. At the knee and hip the
VM,
RF,
BF, and GM), EMG
patterns in this period did not differ from those on the 1st day of
learning
to
walk
Fig. 2-2).
In swing phase, the LG and VM frequently showed strong activities
in the latter half of that phase, as on the 1st day of learning to walk.
Fig 2 5. Unstable infant independent walking
ndependent aiking
in
infants
3
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At around 1 month after learning to walk
months
R)
T A ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ m M ~ ~ ~ ~ ~ ~ - ~ W M ~
G M - ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ - - ~ - - ~ ~ ~ - r ~ ~ ~ ~ - ~ ~ ~
L)
T A ~ ~ ~ ~ N H ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ ~
R
KNEE
EXT
l FLEX •
KNEE
~
1 month fter learning
to
walk
Fig. 2-6. EMGs at 1 month after learning to walk at 11 months).
3 evelopment
o
Gait
1
sec
I 5 mv
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Figure 2-6 shows representative EMG patterns of infant walking at
around 1 month after learning to walk at 11 months after birth). At
this point, the infant began to walk by herself for long periods.
In stance phase, at the ankle, the previous pattern of one or two
alternating
bursts
between the TA and LG disappeared,
but
co
contraction of both muscles was also seen frequently. The reciprocal
fA-, LG+) pattern tended to increase, and co-contraction
TA+,
LG+)
of both muscles tended
to
be seen at about the same frequency as at 2
weeks after learning to walk Fig.
2-4),
but the reverse reciprocal TA+,
LG-) pattern began to decrease or disappear.
At
the knee,
VM
activity
tended to decrease or disappear.
At
the hip and knee, although the
reciprocal
RF-, BF+)
pattern increased, the reverse reciprocal
RF+,
BF-) and co-contraction RF+, BF+) patterns tended to occur much less
frequently than at the onset of independent walking.
At
the hip, activity
of the
GM in
this period did not change from the pattern at the onset
of independent walking Figs.
2-2
and 2-4).
In
swing phase, discharges of the VM began to decrease in intensity
or even disappear in the latter half of that phase, in contrast to the
situation at the onset of independent walking Figs.
2-2
and
2-4).
Discharges
of
the
LG,
on the other hand, still remained strong
in
the
latter half
of
swing phase.
2 st day fter learning
to
walk
43rd day
fter
learning
to
walk
Fig. 2 7. Foot prints of initial infant walking on the 21 st and 43rd days after learning to walk at
1 year 1 month).
Independent aiking
in
infants
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From 2 to 3 months after learning to walk
SW
ST
~ ' \ J
w
1 111
I ~ .
~ 1 1
Il.Iil.
l ~ h . J ,
IU.,
IJI
( R)
TA
LG
i l " ~
11\'
'llLtk
1 1
1 1 1 ' ' 1 I \ ~ J . i l a l '
l
1\1
11
Ill'
'r
TI'
I
jJo..
c., ..
Ji b
d j ~ J .
11'
·frr".r'"'
'1'''''
I'
"1'
'\ "r\'
l ' l r
VM
RF
SF
GM
(L)
TA
LG
VM
RF
SF
GM
-
'r
I.o .
' f '
II
••1..11,
l ...
1,dl
'II
" II'
'11'
r .
.Ii L
..J.'ll ..
"'11"
r'l
11/
.I.
~ , ~ I
.Il,lil ,
~ , U J
l'
\
I l r \ 1 ~ q l ~ T . ,
1.1
I. kL.L 1\
11'
r
'I'
'w
~ . .
,
,i
111 .oiJ
' I : ' ~ U
j
""..•
d.
3 I . l j ~ h .
1,\
"'1"
'Ir,
hUll,
111
1
1'1'
~ I I "
ST SW
(R)
KNEE
2 months after learning
to
walk
11"
,I.
,t ..
.
1
~ L l L l .
~
II I I ~ j J l l
11 '\lf
'r'l'II"I"
11/
It
UUi,
,I.
' r ~ 'If"
r
~ r J l
:r'll
III.
1.1 'ILl,
~ f
~ L ~
'I
I ~ "
11
1
.1 lhlLJ
.1. .L
I 'lI'm
1'''
I'
1
,.
JL . ~ .
.1
"
I "
'1'
r I
I
,1J.Jlil, I
J ~ u
Ilfll'
,JIJld.
'.Jj.
' . / . ~ j
..L
I""", ,'
'11r'
~ ~ h : '
II
'I'T''''
'I
'JI.J...iIIo,
.lJ,.
,1I
n"r'
llllll
~ r ' "
, s
ec
Fig, 2·8, EMGs at 2 months after learning to walk (at 12 months) ,
4 evelopment
o
Gait
12 mo
nths
iJI.l
11"1
.L
I d l L ~ .
I fU llr
T
I , ~ I .
I''''' ['or
j ~ l I . . l I . . 1 c
'IIITI'H
lJ,,,•
, r . I ~ I ~ · 1
ItJ,
l'll
Jl:
rm"
'1"
...
It
[,IIJljA,
~ ( l
, ~ ~ r
'It
,lIl.
,1"""
'''I
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Figure
2-8
shows representative EMG patterns
of
infant walking at
about 2 months after learning to walk at 12
months after birth). The
infant had acquired comparatively stable walking.
In
stance phase, at the ankle, the co-contraction
TA+, LG+)
pattern
began to decrease in frequency, whereas the reciprocal TA-, LG+) and
reversed reciprocal
TA+, LG-)
patterns were the same as at 1 month
after learning to
walk
Fig.
2-6).
At
the knee and hip, there were
no
obvious changes in EMG patterns of the VM, RF, BF, and GM.
In swing phase, although strong discharges
of
the
VM
decreased or
even disappeared in the latter half of that phase, discharges of the LG
still remained the same in the latter half of swing phase as at 1 month
after learning to walk Fig.
2-6).
TO Fe 1
year
TO
FC 1
year
3 months
sw
ST
SW ST
1
sec
0.5 mv
1
sec
I 0.5
mv
1 week after learning
to
walk
3 months
after
learning to walk
Fig.
2-9.
EMGs
in
mutual antagonists TA versus
LG
of infant independent walking.
TO: toe off,
Fe
foot contact,
SW:
swing phase,
ST:
stance phase, Left: at 1 week after
learning to walk at 1 year), Right: at 3 months after learning to walk at 1 year 3 months).
Muscle activity progressed
from
excessive co-contraction of mutual antagonists to reciprocal
patterns.
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in
infants 5
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Subsequent development
TA
LG
V
RF
BF
GM
TO He
SW ST
1 se
5 v
- - - - - - -
1 year 9 month s
IMMATURE CHILD
WALKING PATTERN
~ ~
I
l/k
'\1'
Fig. 2·10. EMGs of the learning process of walking.
TO HC
.
11.
,
1 •
, . . . ~
i L J ~ j
11' '11
,
. 1 ,
rr
'
SW ST
ec_->I 0 .5 mv
3 years 2 months
MATURE ADULT
WALKING PATTERN
TO: toe off,
He
: heel contact, SW: swing phase, ST: stance phase, Left: at 1 year 9 months
immature child walking pattern), Right: at 3 years 2 months mature adult walking pattern).
6
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Figure 2-10 left panel) shows representative EMG patterns of
immature childhood walking at 1 year 9 months of age. The infant
acquired comparatively stable walking with the body inclined forward
Fig.
2-11)
.
In stance phase, at the ankle, a reciprocal fA-, LG+) pattern was
observed most often. Reciprocal RF-, BF+) patterns were also seen at
the hip and knee, and continuous activities of antigravity muscles LG,
BF, and
GM)
were found. In swing phase, discharges of the LG seen at
around 2 or 3 months after learning to walk decreased or disappeared
in
the latter half of swing phase and more greatly resembled the usual
adult walking pattern.
Discharge patterns of the leg muscles did not appreciably change
from 3 months after learning to walk until approaching the third year
of age.
Figure
2-10
right panel) shows representative EMG patterns at 3
years 2 months of age, resembling mature adult walking. At this point,
the infant appeared to have acquired the adult walking pattern using a
strong push-off of the foot with the body erect Fig. 2-11).
In stance phase, at
the
ankle, reciprocal
TA-, LG+)
p tterns
previously found in the first half of stance ph se decre sed
or
disappeared and strong bursts were observed instead in the latter part
of stance phase, as in adult walking.
At
the knee and
hip,
reciprocal
RF-,
BF+) patterns decreased or disappeared. Strong continuous discharges
of the LG, BF, and GM, that had been seen until about the end of 2
years
of
age, began to decrease or disappear. EMG activity patterns
that decreased or disappeared at around 3 years of age were closely
approximating adult forms.
IMMATURE IMMATURE MATURE
INFANT WALKING
CHILD WALKING
ADULT WALKING
PATTERN PATTERN
PATTERN
up to
3 months 3 months 2 years after 2 years
after learning to walk after learning to walk of learning to walk
1
ye r
1.3 ye rs
1.3
ye rs
3
ye rs
3
ye rs
Fig. 2 11. Development of gait pattern
rom
infant walking to mature walking.
Independent aiking
in
infants 7
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Standing posture
on
the
st
day o walking
G M ~ ~ ~ n ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ M M ~ ~ ~ ~ ~ ~ ~ ~ ~
L)
T
~ ~ ~
GM ... 11 ~ ~
,., I , . ~ ¥ , , , ~ . J r ¥ ~ . . . " l ~ , 1111-
R)
KNEE-------.
EXT •
L) FLEX•
KNEE-----......
R)
FC
L)
FC
FF HC
TC
Standing postur on
th
1
st
day
of
walking
sec 0.5 mv
Fig. 2-12. EMGs of standing posture with a slight squat on the 1st day of independently
walking at 10 months).
R): right leg, L): left leg, FF: foot flat with the body erect, HC: heel contact with the body
inclined backward, TC: toe contact with the body inclined forward.
8
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Figure
2-12
shows EMGs of standing with a slight squat on the 1st
day
of
independent walking. These discharge patterns were similar to
those during stance phase on the same day Fig. 2-2).
During maintenance of standing posture at the ankle, alternative
bursts between the TA and LG generally showed a reciprocal TA-,
LG+)
pattern at toe contact fC) with the body inclined forward, and a
reversed reciprocal fA+,
LG-)
pattern at heel contact HC) with the
body inclined backward. Occasionally a co-contraction TA+,
LG+)
pattern was seen at toe contact TC) with the body inclined forward.
At th knee, th VM showed continuous strong activity during
maintenance of slight knee flexion. At the hip and knee, the three
discharge patterns reciprocal, reversed reciprocal, and co-contraction)
between biarticular muscles RF and BF) could be seen.
At
the hip,
the
GM
generally showed continuous activity during the maintenance
of standing.
Fig 2 13. Standing posture just before independent walking at 1 year of age.
ndependent Waiking in
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iscussion
When a baby is just beginning to walk, characteristic EMG patterns
can be seen that are excessive when compared to the corresponding
patterns in adults. We consider here certain EMG patterns that
gradually changed from the time of first learning to walk, principally
those in stance phase and
in
the latter part of swing phase.
In stance phase, we have found that excessive muscular activity and
patterns
peculiar to
gait
in an infant who has just begun to
independently walk, strongly resemble lower limb activity during
maintenance of an upright standing posture in the same period of
development (Figs. 2-2, 2-4, and 2-12), suggesting that a common
mechanism operates both
in
standing and in the initiation of gait. From
a mechanical point of view, at this very early stage, both activities
require a
low
center of gravity and a wide base of support to assure
maximum stability. Generally these tasks can be accomplished, even
though strength and balance are yet undeveloped, by spreading the
legs apart to widen the base of support and by maintaining the knees
in slight flexion to lower the center of gravity. During knee flexion in
stance phase, continuous discharges of the VM are generally seen
until around 1 month after learning to walk (Figs. 2-2 and 2-4). In
stationary standing, the VM is continuously active as the baby stands
fairly squatted on the 1st day of independently walking (Fig.
2-12).
The
VM activity seen at the onset of independent gait thus appears to
contribute to holding a posture with slight knee flexion, permitting the
body s center of gravity to be lowered so that balance is easier to
maintain.
Mer
the first month of walking, such continuous discharges
of the VM tend to decrease or disappear (Figs.
2-6, 2-8,
and 2-10). This
agrees with observations by Okamoto et al.
1985,
2001, 2003) that the
load at the knees decreases as strength and balance develop.
Another
important
factor to consider is keeping the vertical
projection of the body s center of gravity
well
within the bounds of the
base of support. In our study, the baby who had just begun to walk
independently exhibited control over inclination of the trunk during
walking or standing, thus keeping the center of gravity within the base
of support by
orderly
patterns of activity in
the
leg muscles
(Figs.
2-2, 2-4,
and 2-12). As mentioned above, three types of discharge
patterns were seen
in
the biarticular RF and BF muscles. First, the
reciprocal RF-, BF+ pattern
is
considered to be necessary for gait
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with an anteriorly inclined trunk. Before strength and balance have
matured to the point that push off can be effectively used with the
trunk upright, as in adult gait, this pattern tends to increase after 1
month of learning to walk. This pattern is similar to a child s walking
pattern Fig. 2-10, left panel). Second, the reversed reciprocal
RF+,
BF-) pattern is considered to help control displacement of the body s
center of mass by participating
in
maintenance of posterior inclination
ofth trunk. Third, a co-contraction
RF+,
BF+ ) pattern
is
considered
to keep balance control with the body erect. The reversed reciprocal
and co-contraction patterns are normally seen during the very unstable
period of the first month after beginning to walk (Figs.
2-2
and
2-4),
but not thereafter. These patterns are not seen in the child or adult
walking pattern. These EMG patterns thus suggest that excessive
muscular activity is a characteristic feature of balance control when the
baby takes steps for the very first time. While these two muscles RF
and
BF)
act at the hip and knee, Nashner et
al. 1985)
have pointed
out that ankle strategy is the most efficient for returning the body s
center of mass
to
its initial position. Indeed,
in
our study the TA and
LG
exhibited alternating reciprocal patterns of
activity,
thus affording
anteroposterior control over the center of gravity to help maintain
upright stability. That is, activity of the TA is considered to participate
in
maintenance of posterior inclination of the trunk, while activity of
the LG is considered to be necessary for gait with an anteriorly
inclined trunk. We also found variations
in
the alternating reciprocal
patterns of the ankle muscles at about 2 weeks after learning to walk
(Fig. 2-14). From the viewpoint of the developmental process, it clear
that two or three alternating bursts of these muscles TA and LG),
seen
in
the very unstable period at the onset of independent walking
and stationary standing, disappear at around 1 month after learning to
walk (Figs.
2-2
and 2-6). The fact that this alternating burst pattern
becomes attenuated with experience of walking further suggests that it
is
a characteristic EMG feature of balance control when the baby takes
steps for the very first time. The TA and
LG
have previously been
reported to co-contract
in
many instances at the onset of independent
walking, and McGraw 1940) pointed out that co-contraction of these
mutual antagonists is indicative of maintaining balance by strongly
stabilizing the ankle. However, basograms recording using foot contact
switches during stationary standing
Fig. 2-12),
when the trunk was
markedly inclined forward, suggest that the TA in synchrony with the
LG acts for inversion to actively prevent falling. In addition to the
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pattern of
two
or three alternating bursts of the
TA
and LG, as men
tioned above, co-contraction of ankle muscles can be considered the
expression
of
an immature balancing system.
t would be very difficult for an infant to maintain a prolonged single
stance phase at the onset of independent walking. In the adult walking
pattern, strong myoelectric discharges during single leg support are
hardly seen from foot contact until push off. In contrast, excessive
discharges at the onset of independent walking in infant are often
observed during single leg support. During single leg support, as
shown in Table 2-1, up to around 1 month of learning to walk, the
anteriorly located muscles of the lower limb TA, VM, and RF) are just
as active as the posteriorly located muscles
LG,
BF, and GM). But
after a full month of walking, activity of the anterior muscles tend to
disappear. On the other hand, reciprocal EMG TA-, LG+ and RF-,
BF
+)
patterns seen
in
childhood gait become more prevalent. Reversed
reciprocal EMG TA+, LG- and RF+, BF-) patterns disappear and are
not seen in child and adult gait patterns. This suggests that excessive
activity of the anterior muscles indicate marked instability, whereas
excessively activity of the posterior muscles should be associated with
a lesser degree of instability.
In swing phase, up to the first month of walking, the VM a knee
extensor) is generally active from the middle of swing phase until the
subsequent
foot
contact
(Figs. 2-2 and 2-4).
he
LG (an ankle
plantarflexor) is likewise active in this
part
of swing phase during
about the first three months of independent gait (Figs. 2-2, 2-4, 2-6, and
2-8).
Compared
to
the situation of standing on both feet, these patterns
occur when only the contralateral leg is providing a very small base of
support, and the airborne foot is being actively plantarflexed while the
knee is being actively extended, suggestive of operation of the
protective parachute reflex to prevent falling.
t thus becomes clear that when a baby first begins
to
walk, muscle
activity plays a relatively great role in providing stability to maintain
posture and to keep the body s center of gravity low and within the
base of support. From the early stages of walking, the muscles become
stronger and balance matures as months and years pass, obviating the
need for so much myoelectric activity. Thus some patterns of EMG
activity can be identified
that
are present in infant walking but
are subsequently no longer present
in
child or adult gait.
As
the baby
matures, these excesses gradually become refined until, at about three
years of age, they very much resemble muscle activities of adults.
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Table2-
1.
Developmental changes of EMG pattern during single leg support
Joint EMG pattern 1st day 2 wks 1 mon 2-3 mons
Reciprocal (TA-, LG+)
(+) (+)
++) ++)
Ankle Reversed Reciproca l (TA+, LG-)
++) (+) -) -)
Co-contraction (TA+, LG+)
(+) (+) (+)
±)
Knee Continuous (VM+)
++) ++)
(±) (±)
Reciprocal (RF-, BF +)
(+) (+)
++) ++)
Knee Hip Reversed Reciproca l (RF+, BF-)
±)
(±)
-) -)
Co-contraction (RF+, BF+) (+) (+)
(
±)
(±)
Hip Continuous (GM+)
++) ++) ++) ++)
Frequency of occurrence,
++):
very much, (+): much,
±):
a little, (- ): little.
sw
ST
sw ST
sw
ST
sec I 0 5 mv
2 weeks
after
learning to walk
Fig. 2
-1
4. Variations
in
EMG pattern of ankle joint muscles at 2 weeks after learning
to
walk (at
10.5 months of age).
ST: stance phase,
SW
: swing phase, TA: tibial is anterior,
LG:
lateral gastrocnemius, Left (ST-
l):
two or three alternating bursts between the TA and LG Center (ST-2): one or two alternating
bursts between the TA and
LG
, Right (ST-3): one continuous discharge pattern.
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onclusion
To determine EMG characteristics of infant walking we longi
tudinally recorded EMGs using surface electrodes from twelve
muscles of both legs in
an
infant from 3 6 days after birth.
Up to around 1 month after learning to walk in stance phase the
VM
showed activity associated with holding a slightly flexed knee
joint. Alternating reciprocal patterns between the
RF
and BF muscles
came into pl y s the body inclined backward and forward whereas a
co-contraction pattern of both muscles appeared when the body was
erect. Alternating reciprocal patterns between the
TA
and
LG
helped
to maintain balance and to prevent falling backward or forward. Co-
contraction patterns of these
two
muscles were seen to stabilize the
ankle joint to maintain body balance preventing strong forward falling.
In the latter half of swing phase the VM and
LG
showed strong
activities with the knee extending and the ankle plantarflexing to
prevent falling.
These characteristically excessive discharge patterns of infant gait
were not seen
in
subsequent childhood gait or
in
adult gait and they
began to decrease or disappear after about 1 month of learning to
walk. t is in this sense that these leg muscle activities are considered
EMG characteristics of infant walking at the onset of independent
walking.
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Electromyographic EMG) recordings of the lower limbs
were made from a girl from 3 weeks after birth until 8 years of
age
to
determine
EMG
changes in the development of human
bipedal locomotion. Recordings were taken from the tibialis
anterior TA), lateral gastrocnemius LG), vastus medialis
VM),
rectus femoris RF), biceps femoris BF), and gluteus
maximus GM) muscles. In
each
of three developmental
stages of gait, primitive walking, supported walking, and
independent walking, muscle activity progressed from
excessive co-contraction of mutual antagonists to reciprocal
patterns. For the stance limb, the predominant reciprocal
pattern to emerge was continuous activity of the posteriorly
located
LG
and BF as opposed to the anteriorly located T and
RF In
independent walking this preponderance
of
maintained
activity by the LG and BF in stance phase gradually waned
over the first 2 years of walking to focused bursts of activity.
he developmental changes observed in this girl appear to
have been attributable to
changes
in posture reflecting
increased strength and
to
improvements
in
control of balance
reflecting neuromaturation.
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During the first
three
years of life, human bipedal locomotion
develops gradually toward mature walking throughout a series of
phases: newborn
stepping
infant supported walking infant
independent walking, and child walking
Fig. 3-1). n
the 20th century,
some studies have provided detailed technical descriptions kinematics,
kinetics, temporal events, and electromyography)
of
the developmental
process of infant locomotion, although to study gait in
babies using
adult techniques
is
very difficult.
McGraw
1940)
analyzed seven selected phases in the development
of erect locomotion from newborn stepping to mature erect walking,
using film analysis, and pointed out the relations between several
reflexes and the development of motor behavior. Touwen 1976)
clarified the interactions between reflexes and the development of
motor behavior, emphasizing the longitudinal study of motor develop
ment. Using EMG can provide information about the maturation of
gait that
is
both significant and otherwise unavailable
in
conventional
motion analysis.
Although the study of human locomotion in infants using EMG
is
difficult, some cross-sectional and longitudinal EMG studies on the
development of gait have been done. Forssberg
1985),
Thelen et
al.
1987),
and Okamoto et
al. 1972,
1985,2001,2003), have studied the
developmental process from newborn stepping until infant supported
walking prior to independent walking, and Sutherland et
al. 1980)
and
Okamoto et
al. 1972, 1985, 2001, 2003)
have researched the learning
process from early infant independent walking to mature walking.
These studies have generally described developmental changes of
various leg muscular activities in both supported and unsupported
walking.
We
are unaware, however, of any studies that have described
EMG developmental changes from newborn stepping all the way to
mature walking longitudinally in the same individual.
The purpose of this study was to study longitudinal developmental
changes of human locomotion
in
terms
of
leg muscle activity. EMGs
of
the same subject were recorded over a period of 8 years, from 3 weeks
after birth to 8 years of age, so that the entire span of gait development
could be examined
in
one individual.
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We made longitudinal observations on a female infant from 3 weeks
after birth until 8 years of age. At the beginning, to induce newborn
stepping, the examiner held the infant under the arms with the soles
of the feet touching a horizontal flat surface. Well-coordinated walking
movements were observed fairly consistently from shortly after birth
to around 3 or 4 months. Although newborn stepping could not simply
be arbitrarily elicited at the will of the examiner, we were able to
induce selected well-coordinated walking movements of three or more
steps during this period.
From 3 weeks after birth to 3 years of age, EMGs were recorded 38
times, at intervals ranging from 2 weeks to 2 months. After that, from
3
to
8 years of age, EMGs were recorded 10 times, about every 6
months.
Based on the longitudinal EMG findings of the present investigation,
as well as those from previous studies Okamoto t al.,1972, 1985,
2001), we divided the early development of gait into the following four
phases: neonatal stepping, onset of young infant stepping, initial young
infant stepping, and infant supported walking. Subsequent maturation
of gait was also divided into four phases: onset of infant walking, initial
infant walking, immature child walking, and mature walking. The data
in Figures 3-2, 3-4, 3-5, 3-6, 3-7, and
3-8
show representative EMG
patterns and forms from our longitudinal observations of the same
subject Figs. 3-1 and 3-3 .
t t f t ~ f
r
tlrftfi
llUli ~ i ~ € e I t ~ l ~ ~
Jilit fA j l \ ~ l k
Fig. 3 1. Developmental changes of gait in one individual birth to age eight).
Top : neonatal and infant stepping, Middle: infant supported and independent walking,
Bottom: child walking same subject).
rom
Newborn
Stepping
to Mature alking 7
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T
LG
VM
RF
BF
GM
Neonatal stepping
(up to 4 weeks after birth)
TO
FC
•• .
.
j
.
1
J.
,.I..
. ....,
SW
ING (SW STANCE (ST)
\
..
se I
0.
5 mv
3
weeks
Fig.
3-2.
EMGs of neonatal stepping (at 3 weeks after birth).
TO: toe off,
Fe :
foot contact, SW : swing phase (short phase), ST: stance phase (long
phase), TA: tibialis anterior, LG : lateral gastrocnemius, VM: vastus medialis, RF : rectus
femoris,
BF:
biceps femoris,
GM:
gluteus maximus.
Fig.
3-2
shows EMG patterns of leg muscles at 3 weeks after birth.
The stepping in this period was characterized by quick hip and knee
flexion
in
which the thigh became horizontal
in
the middle part of
swing phase. The foot dorsiflexed strongly as it was brought forward.
The foot then approached the floor more
slowly
the knee extending
relatively passively as the hip extended. The foot usually contacted the
floor with the lateral border first but sometimes the heel sole or
forefoot made initial contact instead. The supporting leg was relatively
flexed during stance phase.
The TA RF and BF exhibited notable myoelectric activity as the
ipsilateral foot was leaving the floor to begin swing phase. The TA
continued to be active throughout much
of
swing phase whereas the
RF showed
no
more than sporadic weak activity during that period
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and the BF was relatively
silent
until st nce ph se was being
approached. The LG, VM, and GM did not show any remarkable
activity during swing phase. During stance phase, the LG, BF, and GM
showed relatively continuous activity as antigravity muscles. The VM
and RF tended to be active when knee flexion was not v