[Tsutomu and Kayoko Okamoto] Development of Gait B(BookZa.org)

8/17/2019 [Tsutomu and Kayoko Okamoto] Development of Gait B(BookZa.org)

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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

o

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


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


24/145

Fig. 1 11. Neonatal stepping at 6 days after birth.

Fig. 1 12. Foot contact of neonatal stepping at days after birth.


and

Young nfants 5


25/145

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

o

Gait


26/145

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



•

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.


nfants

7


27/145

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

o

Gait


28/145

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 - - - ~



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.


nfants

9


29/145

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

evelopment

o

Gait


30/145

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.


and

Young nfants

2


31/145

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

o

Gait


32/145

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

3


33/145

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

o

Gait


34/145

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.


35/145

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.

6 Development

o

Gait


36/145

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


37/145

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

o

Gait


38/145

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


39/145

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

evelopment

o

Gait


40/145

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


41/145

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


42/145

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


43/145

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


44/145

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.

Independent aiking

in

infants 5


45/145

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

Development

o

Gait


46/145

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

evelopment

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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

inf nts

9


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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

4 evelopment

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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

ndependent aiking

in

infants 4


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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.

ndependent Waiking in

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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.

evelopment

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Gait


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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.


55/145

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


57/145

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

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[Tsutomu and Kayoko Okamoto] Development of Gait B(BookZa.org)