Development of Gait By Electromyography

Development of Gait by Electromyography Application to Gait Analysis and Evaluation Tsutomu Okamoto, Ph.D. Kayoko Okamo...

Author: Tsutomu and Kayoko Okamoto

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Development of Gait by Electromyography Application to Gait Analysis and Evaluation Tsutomu Okamoto, Ph.D. Kayoko Okamoto, Ph.D.

Walking Development Group Osaka, Japan

Copyright © 2007 by Okamoto & Okamoto

Published by

Walking Development Group ~qTOO3£;PJf~pJT

llJ WALKING

G-S04 Tenno 2-6, Ibaraki-shi, Osaka 567-0S76, JAPAN All rights reserved. No 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 Japan

Preface The gait of a human being continues to change over the course of a lifetime. The 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. It 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 crosssectional 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 iii

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 that this book will prove useful to those engages in gait studies, not only as a basic reference material analyzing the development 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

iv

Contents Preface Contents Part I

iii v

Development of Gait -Birth to Age Eight-

1 . Newborn Stepping in Neonates and Young Infants Early neonatal period (1 - 2 weeks) Late neonatal period (3 - 4 weeks) Onset of infant period (1- 2 months) Initial infant period (3 - 4 months) Discussion

2 . Independent Walking in Infants 1st day of learning to walk 2 weeks after learning to walk At around 1 month after learning to walk From 2 to 3 months after learning to walk Subsequent development Standing posture on the 1st day of walking Discussion

1

3

8 12 16 18 20 25

28 30 32 34 36 38 40

3. From Newborn Stepping to Mature Walking - Developmental Changes in One Individual-

45

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

48 50

52 54

56 58

59 61

v

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 EMG activity in unstable walking Criteria for Instability An Index of Gait Instability

73 79 84 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 7 months after the stroke 1 year 7 months after the stroke EMG evaluation of walking stability Discussion

References Appendix Acknowledgements About the Authors

vi

110 112 114 116 117 121 125 131 133

Development of Gait by Electromyography

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).

Neonatal stepping at 3 weeks afte birth

The purpose of this study was to examine the developmental 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 patterns 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. We 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.

When a newborn infant is held under the arms 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 that 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.

4 Development of Gait

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

RF: rectus femoris GM : gluteus maximus

(Knee extensor, Hip flexor)

(Hip extensor)

Mutual antagonist: SF

SF : biceps femoris (Knee flexor, Hip extensor) Mutual antagonist: RF

LG : lateral gastrocnemius

VM: vastus medialis (Knee extensor)

TA : tibialis anterior

(Ankle plantar flexor)

(Ankle dorsiflexor)

Mutual antagonist: TA

Mutual antagonist : LG

Fig. 1-2. Muscles chosen for recording EMG.

Newborn Stepping in Neonates and Young Infants 5

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). The EMG recordings were done with an 18-channel pen-writing electroencephalograph (60 mm/sec) with the gain set at 12 mm/0.5mV. An 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).

Mature 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. The discharge patterns of the TA and LG, which participate in movement of the ankle joint, showed an almost reciprocal relationship. The 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.


Typical EMG pattern of normal adult walking

0.5

k~j~AA:j~A 326

mv]

333

339

346

356

365

372

378

388

Tibialis anterior (TA)

Lateral gastrocnemius (LG) -+---M~"""~I M'H~---1,~~

.., ........~,''I'--

LG~~~----r-----~--~~~~~-

VM~~#~~I~\\\-\fi\'oJ--.'tol\--+III~~1'~~~tr qj.-'~~~4~~~~ftJt!\,jr\""-

IIIWIlfIM~.r------+---1'-~,~fr""\"\- GMMM~vN(i~/""""'---+--~~~~'4\t'+.'/i'UIf,~,*,-ST

SW

1 sec

I 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 Neonates and Young Infants

13

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. 3 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.

VM LG (-), partly (+) f----+--r~

H , partly (+)

Vastus medialis (Knee extensor)

Lateral gastrocnemius (Ankle plantar flexor)

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.


Fig. 1-11. Neonatal stepping at 26 days after birth.

Fig. 1-12. Foot contact of neonatal stepping at 22 days after birth.


15

Onset of infant period (1 - 2 months)

SW

ST

"-"-.-v · · · " · , Wr,,....,,,....,,r-r-.,.-,,.-,.,. . "W·

,

j

,

,

,

,

,

U ' , ,, ,••

( R)

TA

BF GM~--...

(Ll

TA'IIA(/~""",~-""'t"''''r'TM~~.~~i''J,rIII..~~.....~IJ1fIt4>~Ji'.

ST

SW 1 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).


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)

•

Foot contact (Fe) Lateral border of forefoot with fast 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 in young infant period (1-2 months after birth). (-), (+): instances of no activity and of noticeable activity intermingled.


17

Initial infant period (3 - 4 months)

h,J

SW

ST

W t'

' ihoIh'th ' f ...... ; i .. Wrlr'Ir'Ih'.h

I' "

i' "

;

..

Wit' , .

t'

of

~

\-T

( R)

TA---4~~~------~~~~--~--------~~~~

~ TA~:;~~

(0

LG~ ST

"'~';~

•

SW

t sec

3 months

0.5 mv

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).


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 cases. A halfsquatting posture during stance phase became more frequent. 3 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 (TALG+ 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.

VM (+), partly (-) LG (+), partly (-) f-+-+-~ Lateral gastrocnemius (Ankle plantar flexor)

Vastus medialis (Knee extensor)

Forefoot with fast leg extension EMGs of leg extensors before floor 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.


19

Discussion Although Thelen et al. (1982) reported that when held upright, newborn infants show well-coordinated walking movement that 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 irregular and involve more co-activation than 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 early 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. In stance phase, contractile activity between mutual antagonists varied among co-contraction (TA+ LG+ and RF+ BF+), reciprocal (TALG+ 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.


Developmental changes in the pattern of newborn stepping 1week (Y. T.)

Neonatal period (Early. 1- 2 weeks)

A

~~~~j 2 weeks (A.I.)

Neonatal period (Early. 1-2 weeks)

B

jjlttf1 3 weeks (H.Y.)

Neonatal period (Late. 3-4 weeks)

C

fttfttttt 1.5

Infant period (Onset. 1-2 months)

D

months (H.Y.)

frftfflf 3

Infant period (Initial. 3-4 months)

E

iiw~~ 3.5

Infant period (Initial. 3-4 months)

F

months (A.I.)

months (H.Y.)

rl~~~(f

Fig. 1-17. Developmental changes in the pattern of newborn stepping. B: same subject as E. C: same subject as D and F.


The 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. These 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.


Neonatal and young infant period

Foot contact with leg extension

EMGs of VM and LG before floor contact

Early neonatal VM(-) LG(-)

1-2 weeks after birth Heel contact or foot flat with slow leg extension

Late neonatal VMH, partly (+) LG(-), partly (+)

3-4 weeks after birth Lateral border with slow leg extension

Young infant (onset) VMH, (+) LGH. (+)

1-2 months after birth Lateral border of forefoot with fast leg extension

Young infant (initial) VM( +), partly (-) LG(+), partly (-)

3-4 months after birth Forefoot with fast leg extension

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.


Conclusion 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 cocontraction 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 gastrocnemius or vastus 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.


In order to elucidate electromyographic (EM G) characteristics 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. In 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. In the latter half of swing phase, the vastus medialis and gastrocnemius showed strong activities with the knee extending and ankle plantarllexing for active leg extension to prevent falling. These 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.

Normal human infants begin to walk independently when they are about 1 year of age. Thelen et al. (1989) noted that 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 great deal of investigation has been done on development of gait, there are few EMG studies in the area. Crosssectional kinesiological 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.


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. The 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.

Independent Waiking in infants 27

1st day of learning to walk

fffffr (R)

TA LG VM RF BF GM (U TA LG VM RF BF GM sw

ST

( R)

KNEE~ (L)

KNEE

v

~

EXT. ~ FLEX.

~

-----------

V t sec

0.5 mv


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.


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.


Fig. 2-3. Foot prints on the 1st day of independently walking (at 1 year 1 month).


2 weeks after learning to walk

sw

ST

10.5 months

( R)

TA LG VM RF SF GM (L)

TA LG VM RF SF GM ST

( R)

KNEE ( L)

KNEE

sw

*

EXT . FLEX.

1 sec


Fig. 2-4. EMGs at 2 weeks after learning to walk (at 10.5 months).


0.5 mv

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.


At around 1 month after learning to walk

11 months ( R)

TA~~~~~~~~~~~~mM~~~~~~-+~WM~

GM+-~~~~~~~~~~--~--~~~-r~~~~+-~~~ (L)

TA~~~~NH~~~~~~~~~~~~~~~~~

( R)

KNEE EXT. ..

( Ll FLEX.• KNEE ---~

/---1 sec

1 month after learning to walk

Fig. 2-6. EMGs at 1 month after learning to walk (at 11 months).


I

0.5 mv

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 cocontraction 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.

~

~

21st day after learning to walk

43rd day after 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).


From 2 to 3 months after learning to walk

( R)

!il"~

~11

1'1'

11\'

ld'llLtk

LG ,~.

VM RF

GM

.I.

l' \

LG 1.1

I.

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111

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,

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11"'\lf 11/ It

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r .".

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2 months after learning to walk

Fig, 2·8, EMGs at 2 months after learning to walk (at 12 months),


lJ,,,•

,I.

~~, '~f l'll i~u ~ Jl: 1 ,.

~~

'1'

j~lI..lI..1c

'It '''I

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

sw

Fe

1 year

ST

TO

SW 1 sec

FC

1 year 3 months

ST

0.5 mv

1 week after learning to walk

1 sec

I

0.5 mv

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.


Subsequent development

TO

He

TO

HC

. 11.,

TA

.1 "" •

!,...~

I I~'II'J\'

~/~

LG

'JliLJ~jd ~

..Il ,U~

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,

.I

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.l/k.

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rr

"1'"

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1 sec

SW

10.5mv

-------' 1 year 9 month s IMMATURE CHILD WALKING PATTERN

ST

__,_,e_c_->I mv 0.5

3 years 2 months MATURE ADULT WALKING PATTERN

Fig. 2·10. EMGs of the learning process of walking. 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).


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+) patterns previously found in the first half of stance phase decreased 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 INFANT WALKING PATTERN

..

IMMATURE CHILD WALKING PATTERN

up to 3 months after learning to walk

3 months - 2 years after learning to walk

1 year - 1.3 years

1.3 years - 3 years

..

MATURE ADULT WALKING PATTERN after 2 years of learning to walk 3 years -

Fig. 2-11. Development of gait pattern from infant walking to mature walking.


Standing posture on the 1st day of walking

GM~~~n~~~--~~~~~~~~MM~~~~~~~~~ ( L)

TA

::~~~ GM..

... 11,

~~.

••

",., ..

~'" I",."""~¥,,,~ .Jr¥~!..."l~,

"'-1111-'....._ _ __

( R)

KNEE-------." ( L)

EXT . • FLEX.•

K N E E - - - - -...... ( R)

FC ( L)

FC FF

HC

TC

1 sec

0 .5 mv

Standing posture on the 1st day of walking

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.


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 the knee, the 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.


Discussion 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


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 ofthe 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 Independent Waiking in infants 41

pattern of two or three alternating bursts of the TA and LG, as mentioned above, co-contraction of ankle muscles can be considered the expression of an immature balancing system. It 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). The 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. It 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.


Table2-1. Developmental changes of EMG pattern during single leg support Joint

Ankle

EMG pattern

1st day

2 wks

1 mon

2-3 mons

Reciprocal (TA-, LG+)

(+)

(+)

(++)

(++)

Reversed Reciprocal (TA+, LG-)

(++)

(+)

(-)

(-)

Co-contraction (TA+, LG+)

(+)

(+)

(+)

(±)

Continuous (VM+)

(++)

(++)

(±)

(±)

Reciprocal (RF-, BF+ )

(+)

(+)

(++)

(++)

Reversed Reciprocal (RF+, BF-)

(±)

(±)

(-)

(-)

Co-contraction (RF+, BF+)

(+)

(+)

(±)

(±)

Continuous (GM + )

(++)

(++)

(++)

(++)

Knee

Knee & Hip

Hip

Frequency of occurrence, (++): very much, (+ ): much, (±): a little, (- ): little.

sw

ST

sw

ST

sw

ST

1 sec

I

0.5 mv


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.


Conclusion To determine EMG characteristics of infant walking, we longitudinally recorded EMGs using surface electrodes from twelve muscles of both legs in an infant from 306 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 playas 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. Cocontraction 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. It is in this sense that these leg muscle activities are considered EMG characteristics of infant walking at the onset of independent walking.


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 TA 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. The 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.

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). In 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 development. 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.


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 et 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).

t1tft~f frffff

Itlrftfi

llUli ~ i I f~€e It~l~~ Jilit/fA j 1111l\~lk 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).

From Newborn Stepping to Mature Walking 47

Neonatal stepping (up to 4 weeks after birth)

TO

FC ••11 .

TA

..".

\." ..

LG VM

RF

BF

j,

..1

,J.

,.I..

~~

." ....,"

GM SWING (SW)

STANCE (ST) 1 sec

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,


and the BF was relatively silent until stance phase 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 very pronounced, that is, during the double-stance phases. In single-stance phase, activities of mutually antagonistic muscles (TA versus LG and RF versus BF) showed reciprocal (TA- and LG+, RF- and BF+) , cocontraction (fA+ and LG+, RF+ and BF+), and reversed reciprocal (fA+ and LG-, RF+ and BF-) patterns, but activities of certain mutually antagonistic muscles were variable and inconsistent (Fig. 3-12).

Fig. 3-3. Neonatal stepping at 3 weeks after birth.


Young infant stepping (from 1 to 5 months of age)

ffffrJf Ir~~I~ TO

TA

Fe

TO

Fe

lilii! TO

Fe

U'"'

.1,

LG

VM II'

,j;..

RF BF

.,1, F

II

GM

.."

sw

1 sec

I 0.5 mv

1.5 months

SW

ST

SW

ST

1 sec

3.5 months

I 0.5 mv

ST

t sec

I 0.5 mv

5 months

Fig. 3-4. EMGs of young infant stepping (Left: at 1.5 months after birth, Center: at 3.5 months after birth, Right: at 5 months after birth).

1 ) Onset of young infant stepping (from 1 to 2 months of age)

Fig. 3-4 (left) shows EMGs at 1.5 months after birth. Step frequency was more regular than during neonatal stepping. Hip flexion was pronounced in the first part of swing phase as in neonatal stepping, but leg extension began to be more vigorous in the latter part of swing phase. The lateral border of the forefoot initially contacted the floor for the most part. In swing phase, continuous activity of the TA tended to terminate sooner in the latter part of swing phase than during the neonatal period, but bursts of the RF and BF during the phase showed the same tendencies as before. The LG and VM, which had been quiet during swing in neonatal stepping, began to exhibit activity shortly before foot contact, and sometimes activity in the GM was also observed before foot contact. During stance phase, continuous bursts or discharges of the VM were seen often, as in


neonatal stepping. The posteriorly located LG, BF, and GM showed continuous discharges that were comparatively variable in intensity. In single stance, the reciprocal pattern was observed as in neonatal stepping. Incidence of the co-contraction pattern decreased from that at the time of neonatal stepping, and the reversed reciprocal pattern was hardly seen (Fig. 3-12). 2) Initial young infant stepping (from 3 to 5 months of age)

Fig. 3-4 (center) shows EMGs at 3.5 months after birth. Stepping in this period was performed actively as foot contact was audible. Hip flexion was again conspicuous in the first part of swing phase as it was in the neonatal period and in the onset of young infant stepping. Leg extension in the latter part of swing phase was performed in a more active manner than in the onset of young infant stepping, often quite visibly so. Initial contact of the floor was, for the most part, by the forefoot. The supporting leg, especially the knee, tended to be relatively extended in this period. In swing phase, the TA, RF, and BF became less active at toe off than they did in the onset period of young infant stepping. This was especially true for the TA, but that muscle would always exhibit at least a weak burst in the first part of swing phase. In the latter part of swing phase, discharge patterns of the LG and VM tended to increase frequently. During stance phase, continuous bursts or discharges of the VM were seen often, and the LG, BF, and GM showed continuous discharges of variable intensity, as they did in the onset of young infant stepping. Mutually antagonistic muscles in single stance exhibited the reciprocal pattern more readily than previously. The co-contraction pattern was hardly seen, and the reversed reciprocal pattern was not seen at all in this period. Fig. 3-4 (right) shows EMGs at 5 months after birth. Stepping was actually difficult to elicit at that age, but we did manage to induce it and the resulting EMG pattern was basically similar to the initial period of young infant stepping at around 3.5 months after birth.


Infant supported walking (from 6 to 12 months of age)

TO

TO

Fe

ft~jtrtt ~~liil Fe

TO

Fe

"", 'I

TA+-~--------~~

.lIi,/"Il.

LG+-~~~~~~~

, d,~

'1"'1"'1"

'II'

,',!",'

VM +-~--------~~ RF+-~--------~~ .•1...., "11 "1

BF+-~~~~--~~

I~

I

GM+-~--------~~

sw

sw

ST

1 sec

\

0.5 mv

6 months

sw

ST

1 sec

9 months

.J

'\1'

11 I 0.5 mv

ST 1 sec

I

O.S my

11.5 months

Fig. 3-5. EMGs of infant supported walking (Left: at 6 months after birth, Center: at 9 months after birth, Right: at 11,5 months after birth),

Fig. 3-5 shows EMGs at 6, 9, and 11.5 months after birth. After around 6 months after birth, the infant began to crawl after toys and tended to show comparatively stable stepping when supported upright. At around 11 months, 1 month before walking independently, the infant became able to stand by herself and to walk with one-handed support. The relatively pronounced flexion of the hip seen in the first part of swing phase of the previous period was slightly reduced. Active leg extension tended to disappear in the latter part of swing phase. The heel usually contacted the floor first. The supporting leg was extended. In the first part of swing phase, activity of the RF was sporadic and bursts of the BF disappeared. In the latter part of swing phase, the LG and VM showed minimal activity at 6 and 9 months, but shortly before independent walking (at 11.5 months after birth), strong myoelectric discharges of the LG and VM were sometimes seen. During stance


phase, the continuous activity of the VM seen in earlier stages of development no longer appeared. The LG and BF, antigravity muscles, were markedly active in stance phase throughout this period of supported walking (Fig. 3-6). Mutually antagonistic muscles during this period seldom exhibited co-contraction patterns, but rather worked in reciprocal patterns as a rule.

621

385 days

0.5 mv

TA

LG

VM RF 8F

GM KNEE

Ext. Flex.

FC~ 600

700

1st day of independent walking

Fig. 3-6. EMGs on the 1st day of independent walking (at 1 year of age). SUPPORT: supported walking, INDEPENDENT: independent walking.


Infant walking (from 1 week to 2 months after learning to walk)

j~R'~~ i~A~~' TO

Fe

jl9Ajil TO

Fe

I

"I.

TA

,II. '·",1, IIIh~LL. [1'1'.1,

LG

1'1

VM RF

"" ~Ii••.

BF~~\~~~~~-+~' GM~~~~~~~--~~

sw

ill.

"~:~',r sw

ST 1 sec

0.5 mv

1 year

HI

111I~I'r

n

~

UI.._ TI~"

.11,

'I,'

sw

ST

1 sec

I

0.5 mv

1.1 years

ST

_-,-,1s"", ee'----.J

0.5 mv

1.3 years

Fig. 3-7. EMGs of learning process of infant independent walking (Left: 1 week after learning to walk at 1 year, Center: at 1 year 1 month, Right: at 1 year 3 months).

1) Onset of infant walking (up to 4 weeks after learning to walk)

Fig. 3-7 (left) shows EMGs of 1 week after learning to walk at around 1 year of age. The infant was able to walk more than 10 steps without external support. The walking in this period was characterized by quick hip flexion in which the thigh was raised forward diagonally in the first part of swing phase. Then the foot reached the floor quickly, the knee extending actively along with the hip. The foot usually contacted the floor with the forefoot or mid-sole first, but occasionally the heel made initial contact. 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 (Fig. 3-6).


At the beginning of swing phase, the TA and RF were strongly active, often accompanied by moderate activity of the BF that had continued from the previous stance phase. Later on in swing phase, the LG, VM, BF and GM all generally became active and, just before foot contact the TA might exhibit a burst of activity. Stance phase was characterized by large amounts of activity in the muscles investigated, variously intermittent or continuous for a given muscle, so that mutual antagonists displayed not only reciprocal patterns in single stance, but also co-contraction and reversed reciprocal patterns (Fig. 3-12). 2) Initial infant walking (from 1 to 2 months after learning to walk)

Fig. 3-7 (center) shows EMGs of 1 month after learning to walk, at 1 year 1 month of age. The infant was becoming accustomed to walking and began to walk by herself for extended periods of time. The femur was not lifted so high in the middle part of swing phase as at the onset of independent walking. Leg extension in the latter part of swing phase was active. The forefoot initially contacted the floor for the most part, but occasionally the entire sole made initial contact. There was a diminution in base width and a gradual decrease in the slight flexion at the knee of the supporting leg, and the body's center of gravity was slightly higher during stance. The upper extremities, which had been extended and abducted earlier, now began to approach the body. At toe off, just as swing phase was beginning, most muscles exhibited the same patterns of activity as at the onset of independent walking 1 month before. During stance phase, activities of the muscles become less sporadic. Continuous discharge of the VM began to appear less and less (Fig. 3-9). Strong maintained activities of the TA and RF seen at onset of infant walking became markedly moderated, whereas in the LG and BF such activities remained unabated though more consistent in nature during stance phase (Fig. 3-9). In singlestance, the discharge patterns of mutual antagonists described in Figure 3-12 showed the reciprocal pattern more often than in the initial period of infant independent walking. The co-contraction pattern decreased comparatively, but was sometimes still seen, while the reversed reciprocal pattern was hardly seen at all in this period.


Immature child walking Unsettled muscle activity (from 3 months to 2 years after beginning to walk)

AJAlA II ~ll l ~~U~ TO

TA

He

TO

He

TO

He

,.1

IH.

Ill'

IJI~

LG

1,/

' '''"

AL.

'lr'

'WI

W-

VM RF

BF

, '\ I"""

,,\,/,,, I'll

.....1

GM SW

sw

ST

1 sec

0.5 mv

2 years

ST 1 sec

3 years

SW

!

0.5 mv

ST

1 sec

I

0.5 mv

7 years

Fig. 3-8. EMGs of learning process of child walking (Left: at 2 years, Center: at 3 years, Right: at 7 years).

Fig. 3-7 (right) shows EMGs of the child 3 months after learning to walk, at 1 year 3 months of age. The infant had begun to shift to a comparatively stable walking pattern of her own. The thigh was no longer strongly lifted up in the first part of swing phase. Subsequent knee extension, previously prominent in the latter part of swing phase, now began to become more passive. The heel and toe began to touch almost simultaneously. The heights of the hip joints were higher than in infant walking, and the child began to exhibit more force to propel her body forward. The foot base was narrowed to the width of the shoulders. The upper extremities were still held away from the body, although they were only slightly elevated now. At the beginning of swing phase, the TA and RF worked in the same way at 3 months of independent walking as at 1 month. The VM no longer exhibited activity in the middle of swing phase after 3 months


of walking, and activity in the LG was essentially absent throughout swing phase until the very end. During stance phase, activities in the leg muscles changed little between 1 and 3 months after beginning to walk, except for the GM, which exhibited less activity especially in the latter part of this phase. Figure 3-8 (left) shows EMGs at 2 years of age. The child had acquired a comparatively stable walking pattern at that time and was gaining control of movements related to running and fast walking. The thigh was no longer lifted up prominently in the first part of swing phase, nor did the lower leg extend rapidly in the latter part of swing phase. The heel and toe contacted the floor almost simultaneously. Slight knee flexion in the supporting leg was prolonged and the child propelled herself forward with a pumping action of the thighs, the trunk leaning forward slightly and the foot base narrowed. The forearms were slightly elevated during gait at ordinary speed. The TA was notably active as swing phase was about to begin, but neither the RF nor the BF exhibited activity as the foot left the ground. Just before the foot returned to the ground, the TA showed very little activity. During stance phase, continuous discharge patterns of the antigravity LG, BF, and GM were similar to those seen at 1 to 3 months after learning to walk. VM+

LG+

Terminal SW

Terminal SW

VM+

Ak ~rt 0-

Developmental period of gait lyear

H M+

Knee extension Plantarflexion

Onset of infant walking

-

(

~~:~ ~ :~~s_.~~r~~~n~n~ ~o_~.~)_____ Initial infant walking

Immature child walking

LG+, BF+

~F+

TA+

BFl

LO+

Squat

Backward

Forward

++)

(++ )

(++)

(++ )

(+ )

(_)

(+)

(_)

(_)

(++)

(-)

(-)

(-)

(-)

(++)

U -------n-------D.-------.[}-------. ----

(1-2 months after learning to walk)

(3 months - 2 years after learning to walk)

TA+, RF+

Throughout ST Throughout ST Throughout ST

~

Fig. 3-9. Developmental changes of EMG patterns in leg muscles from onset of infant walking to immature child walking. Frequency of occurrence, (++): very much, (+): much, (-): little.


Mature walking Toward a mature pattern (after 2 years of learning to walk)

Fig. 3-8 (center and right) shows EMGs at 3 and 7 years. The child had begun to acquire stable walking resembling that of an adult in this period. The thigh showed minimal flexion in the first part of swing phase. The foot usually contacted the floor with the heel first and the toes lifted like an adult. Walking with the body inclined forward was seen until around the end of 2 years of age, when the body began to become more erect. The child exhibited strong pushing-off motions of the foot, and the upper extremities were no longer held in any degree of elevation. In swing phase, the TA was consistently active as the foot was leaving the ground, sometimes accompanied by slight activity of the RF. The TA also began to show marked activity just before the foot touched the floor in many instances (Fig. 3-10) . During stance phase, continuous activity of the LG previously found in the first half of stance phase decreased or disappeared and strong bursts were observed instead in the latter part of stance phase. Strong continuous discharges of the BF and GM previously seen in stance phase began to decrease or disappear, thus assuming activity patterns similar to those of adults. TA+ Just before ST

Developmental period of gait

X~TA+ Dorsiflexion

1.3 years Immature child walking (3 months - 2 years after lea rning to walk)

3 years Mature walking (after 2 years of learning t o walk)

(-)

•

(++)

LG+, BF+ Throughout ST

al

LG+Forward (++)

D-(-)

Fig, 3-10, Developmental changes of EMG patterns in leg muscles from immature child walking to mature walking. Frequency of occurrence, (++): very much, (-): little.



After birth

Development of gait


Birth Neonatal reflex stepping (up to 4 weeks after birth) Neonatal stepping

1 month Onset of young infant stepping (1-2 months after birth)

2 months Young infant stepping (Inactive stepping)

6 months

~

,

Initial young infant stepping (3-5 months after birth)

Infant supported walking (6-12 months after birth)

Infant supported walking

1 year

1.1 years

Infant walking

Onset of infant walking (up to 4 weeks after learning to walk) Initial infant walking (1-2 months after learning to walk)

1.3 years

It

Immature child walking (3 months - 2 years after learning to walk)


3 years

A

Mature walking (after 2 years of learning to walk)

Mature walking

Fig. 3-11 . Developmental period of gait during newborn stepping, infant supported walking, and independent walking.


Neonatal st epping

Young infant stepping

Infant supported walking

Infant walking

Immature child Mature walking walking

:: ~ ~:-

Reciprocal pattern

:: ~~:

Co-contraction pattern

:::~:::

Reversed reciprocal pattern

Fig. 3-12. Developmental changes of EMG patterns in mutual antagonists (TA versus LG and RF versus BF) during ipsilateral single stance. TA: tibialis anterior, LG: lateral gastrocnemius, RF: rectus femoris, BF: biceps femoris,

+: noticeable activity, - : no activity.

Reciprocal pattern: posterior muscle is active while anterior muscle is inactive, associated with forward inclination of the trunk. At the hip, BF is active and RF is inactive. At the ankle, LG is active and TA is inactive.

Reversed reciprocal pattern: anterior muscle is active while posterior muscle is inactive, associated with backward inclination of the trunk. At the hip, RF is active and BF is inactive. At the ankle, TA is active and LG is inactive.

Co-contraction pattern: muscles on both sides of a joint are simultaneously active.


Discussion During the first 3 years of life (Fig. 3-11), movements related to walking appear to begin with gross patterns of muscle activation, frequently including co-activation of mutual antagonists. Not only in supported walking and then in subsequent independent walking, but even in neonatal primitive walking one can see over time progression from excessive gross activation to more efficient and economical production of muscle activities in the lower limbs (Figs. 3-12 and 3-13). Such findings are evident in both stance and swing phases of the walking patterns. Interestingly, even some specific changes noted in newborn stepping over the first couple of months recur as the baby later masters voluntary supported walking and then independent gait. As the foot leaves the floor, activities of the TA, and to some extent the RF, remain relatively consistent across primitive, supported, and independent modes of walking. The latter two modes might thus be characterized as containing a "primitive" component at toe-off. Activity of the BF, on the other hand, at this same point in the gait cycle, varies from mode to mode as well as within a given mode. In both neonatal primitive walking and independent walking the BF is active along with the TA and RF when the child first performs these modes of locomotion, but the BF subsequently works in a reciprocal pattern with the other two muscles as the child gains experience. Just before the foot returns to the floor, the LG and VM are active at around 3 or 4 months after birth and again during the first few months of independent walking. The appearance of this activity coincides with gradual emergence of the parachute reaction, which Milani-Comparetti (1967) describes as appearing at about 4 months after birth, so we need to consider the possibility that activity of the LG and VM as the foot approaches the floor may be closely related to the parachute reaction at 3 or 4 months. As supported walking becomes more voluntary in subsequent months, this activity of the LG and VM is no longer manifest, nor is it seen 1 to 3 months after first learning to walk independently. The absence of such muscle activity appears to reflect development of balance and postural control. These changes in activity of the LG and VM around floor contact might be interpreted as development from simple reflexes and subcortical motor responses through cortical inhibition of these reflexes to a growing influence of voluntary or cortical motor control. From Newborn Stepping to Mature Walking 61

The manner in which the foot contacts the floor undergoes a similar progression in both supported walking and independent gait. At first the forefoot initially contacts the floor, but as development progresses, the sole of the foot makes initial contact with the floor and subsequent to that the heel makes initial contact. A burst of activity from the TA just before touchdown becomes more distinct as this sequence proceeds, so it might be interpreted as an indicator of stability in gait. In this connection, other behaviors change during this progression that likewise reflect incremental achievement of stability in gait. For example, width of foot placement gradually decreases as the walking pattern becomes more stable, and a "high guard" position of abducted arms becomes "medium guard" and eventually an adult-like "low guard" in the process. After the foot contacts the floor, the muscles in that lower limb can be subjected to greater loads than is possible in swing phase. This is particularly apparent in the VM. In the primitive mode of gait, the VM exhibits considerable activity as the infant pushes the foot against the floor in the extension phase of the primitive pattern. From 6 months, however, the baby is in a supported mode of gait wherein the VM no longer impulsively pushes against the floor and the baby simply relies on the supporting person to bear weight during gait. The VM is not very active even at 11 months, when the baby is close to graduating from the supported mode to independent walking, apparently because she has learned to passively bear weight through the knee on the stance side when the center of gravity of the superincumbent body segments has been brought anterior to the knee joint. At the beginning of the independent mode of gait, however, the situation dramatically changes as the baby suddenly finds herself solely responsible for both maintaining balance and bearing weight. When the foot contacts the floor and the lower limb on that side accepts body weight, the knee remains slightly flexed, presumably to keep the center of gravity of the superincumbent segments low, and thus make the task of balancing easier. Only after gait in the independent mode has progressed to the point when the baby can skillfully bring her weight over and just anterior to the knee on the stance side, can the VM display a brief focused burst during weight acceptance and otherwise be silent or minimally active in stance phase. As the baby moves forward from double support to single support in stance phase, she encounters a more sophisticated task of dynamically maintaining balance. The interplay between the LG and


TA, mutual antagonists at the ankle, as well as between the RF and BF, mutual antagonists at both the hip and the knee, becomes very important during single support. When a baby first begins to walk without external support, co-contraction between each pair of muscles provides gross stability to make this difficult task feasible for the uninitiated. Because this co-contraction pattern first arises from trial and error, the other possibilities of reciprocal and reversed reciprocal patterns also appear (Fig. 3-12). Interestingly, all three of these patterns appear in primitive walking as well, and we have observed that the reciprocal pattern at this very early stage tends to appear when the trunk is inclined forward and the reversed reciprocal pattern when the trunk is leaning back, suggesting that muscles naturally respond to mechanical loading. Since walking can be characterized as a succession of incomplete forward falls, the reciprocal pattern eventually becomes more dominant than the co-contraction pattern as the baby attains dynamic stability in walking forward. By 3 years of age, the refinements of activity between these mutual antagonists are fully in place and the child propels herself forward with precisely measured doses of muscular activity and full dynamic control of balance. One finding to emerge from longitudinal observations was that developmental changes and refinements of excessive muscular activity during newborn stepping and supported walking appear again during the learning process of independent walking. As strength and balance improve in a normal infant, unnecessary muscle activation disappears leading to a series of developmental stages of bipedal locomotion in both supported and unsupported walking (Fig. 3-13). We suggest that the refinement of excessive co-activation, which can serve as a barometer to indicate increasing level of skill in human locomotion, comes from changing posture by improvement of strength and balance control reflecting neuromaturation.


After birth

Birth

RF+ Initial SW

Dorsiflexion

I".

Hip flexion

Neonatal reflex stepping (up to 4 weeks after birth)

(++)

(++)

Onset of young infant stepping (1-2 months after birth)

(++)

(++)

(++)

(++)

(++)

(+),(-)

Onset of infant walking (up to 4 weeks after learning to walk)

(++)

(++)

Initial infant walking (1-2 months after learning to walk)

(++)

(++)

Immature child walking (3 months - 2 years after learning to walk)

(++)

(+),(-)

(++)

(+),(-)

Development of gait


1

,

TA+ Initial SW

~~.

Neonatal stepping 1 month

2 months

................................ _.....

Initial young infant stepping (3-5 months after birth)

Young infant stepping (Inactive stepping) 6 months

i

Infant supported walking (6-12 months after birth)

Infant supported walking 1 year

1.1 years

I

Infant walking 1.3 years

I

......................... _.......


3 years

A

Mature walking

(after 2 years of learning to walk)

Mature walking

Fig. 3-13. Developmental changes of EMG patterns in leg muscles during newborn stepping, infant supported walking, and independent walking.


BF+

VM+

LG+

Initial SW

Terminal SW

Terminal SW

"'~

If L.,

Knee flexion Knee extension Plantarflexion

TA+

VM+

TA+, RF+

LG+, BF+

Just before ST Throughout ST Throughout ST Throughout ST

~,~ Dorsiflexion

-};"

~F+

TA+

BFl LG+

Squat

Backward

Forward

(++)

(-)

(-)

(+),(-)

(++)

(+)

(+)

(++)

(+)

(+)

(-)

(++)

(-)

(+)

(+)

(++)

(++)

(-)

(++)

(-)

(++)

(-)

(-)

(-)

(-)

(- )

(-)

(++)

(+),(-)

(++)

(++)

(+),(-)

(++)

(++)

(+)

(+),(-)

(-)

(+)

(+),(-)

(-)

(-)

(++)

(-)

(-)

(-)

(-)

(-)

(-)

(++)

(-)

(-)

(-)

(++)

(- )

(-)

(-)

TA: tibialis anterior, RF: rectus femoris, BF: biceps femoris, VM: vastus medialis, LG: lateral gastrocnemius,

SW: swing phase, ST: stance phase. Frequency of occurrence, (++): very

much, (+): much, (-): little, (+),(-): instances of noticeable activity and of no activity intermingle.


Application to EMG biofeedback training

Infant independent walking at 1 year of age

To develop an index of gait instability from electromyographic (EMG) information, we made observations on infants from the time they first began to walk independently at about 1 year of age until around 3 years of age. From our findings we obtained the following criteria. (1) Very unstable gait: As seen in a child within the first month of learning to walk, the vastus medialis is active in the latter half of swing phase, the tibialis anterior and rectus femoris are active during stance phase, and activity of the vastus medialis is continuous. These EMG characteristics are not usually seen in subsequent childhood gait or in adult gait, and they serve as markers of very unstable gait. (2) Unstable gait: Activity of the gastrocnemius in the latter half of swing phase is generally noted only within the first 3 months after the child learns to walk, and that activity is interpreted as a sign of unstable gait. (3) Slightly unstable gait: Activity of the gastrocnemius in the first half of stance phase and the continuous activities of the biceps femoris and gluteus maximus from initial contact with the floor until push off are found in children until 3 years of age. These activities are considered EMG markers of slightly unstable gait.

Generally a baby becomes able to perform bipedal upright walking at about 1 year of age. Compared to quadrupedal crawling, walking involves maintenance of a mechanically unstable upright position and keeping one's balance while transporting the body's center of gravity. This requires a highly developed antigravity mechanism and operative balance reactions. Thelen et al. (1989) noted that 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. McGraw (1940) and Okamoto et al. (1985, 2001, 2003), for example, have both noted that, although initial contact of the heel on the floor can be found in babies first learning to walk, as might be found in adult gait, they also often contact the floor first with the forefoot, which is not characteristic of adult gait at all. Novice walkers have been noted to have several characteristics that differ from adult gait, such as increased cadence, decreased step length, excessive rotation or flexion in stance phase, a pattern of circumduction in place of the hip and knee flexion that arises (in the adult) at the very beginning of stance phase, a lack of accompanying arm movement, or strong co-contraction or other form of muscle hyperactivity. McGraw (1940), Burnett et al. (1971), and Okamoto et al. (1985, 2001, 2003) have analyzed the development of independent walking and noted a regular progression from an initially wide base at the feet and a "high guard" position of abducted arms as evidence of instability in walking, giving way to a slightly narrower base and "medium guard" posture as the walking becomes more stable, finally to an adult-like "low guard" posture associated with stable gait. The mechanism of the motor development of babies has usually been studied in relation to postural development, often with, for example, the motor development evaluation form of Milani-Comparetti et al. (1967), which relates primitive reflexes to postural and motor development. To study gait in babies using electromyography (EMG) , goniometers, and force plates as is done with adults is very difficult, although some investigators have used film analysis to study the development of gait. Longitudinal study of motor development, emphasized by Touwen (1976) as very important, has been rare. McGraw (1940) studied the relations between several reflexes and the development of motor behavior, and Touwen (1971, 1976) has clarified the interactions between reflexes and the development of motor

70 Application to Gait Analysis and Evaluation

behavior. Cross-sectional kinesiological EMG studies on the development of infant walking have been performed by Sutherland et al. (1980), Forssberg (1985), and Thelen et al. (1987), but we have not seen much in the way of longitudinal EMG study on the acquisition of gait outside of that by Okamoto et al. (1972, 1983, 1985, 2001, 2003).

TA

LG

RF

SF

.EMG patterns began to decrease or disappear at about 1-3 months after learning to walk •

EMG patterns began to decrease or disappear at about 3 years of age

D

EMG patterns began to appear at about 3 years of age

IMMATIURE CHILD WALKING PATTERN

.+11]+0 11]+0

MATURE ADULT WALKING PATTERN

0

IMMATURE INFANT WALKING PATTERN

Fig. 4-1. Schematic diagram of EMG activity as indication of unstable walking. TA: tibialis anterior, LG: lateral gastrocnemius, VM: vastus medialis, RF: rectus femoris, BF: biceps femoris, GM: gluteus maximus.

An Index of Gait Instability 71

Knowing the developmental changes in the EMG features of the process of acquiring gait in normal babies should be helpful in better understanding the diagnosis and treatment of abnormal gait in developmentally delayed children. EMG enables one to view the ability to walk and to maintain balance and control during gait in ways that would not be noticed otherwise. Even for the elderly individual, the stages of motor development can be considered in relation to therapeutic exercise for maintaining gait function. To examine the role of muscle activity in the developmental process of normal gait in babies, we used EMG with surface electrodes to longitudinally study babies from the very unstable stage of first learning to walk at 1 year of age to the attainment of adult-like stability in gait at about 3 years of age. In addition to reconfirming the forward lean with shuffling in the early stages of gait and the more erect gait with decisive push off in stable adult-like gait, we were able to derive from these longitudinal EMG observations an index for the instability of gait based on developmental processes (Figs. 4-1 and 4-2) .

••

••+

·· ..

···· ···

......

+•

INFANT PATTERN

++.

.

••

·:......_-..A IMMATURE INFANT WALKING

IMMATURE CHILD WALKING

MATURE ADULT WALKING

Fig. 4-2. Refinement of excessive muscular activity during the development of gait. 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.

72 Application to Gait Analysis and Evaluation

EMG findings during the development of gait The subjects were three babies who first began to walk independently at about 1 year of age (at 306 days, 375 days, and 385 days after birth). We made longitudinal observations on these three children from the time they first began to walk independently at about 1 year of age until a stable adult-like walking pattern was achieved at around 3 years of age. EMGs were recorded every 1 or 2 weeks in the initial period of independent walking and after that every 1 or 2 months. For purposes of comparison, these observations were supplemented with cross-sectional observations taken from fifteen babies in the first year of age (five infants at the onset of independent walking, five at 1 month after learning to walk, and five at 3 months after learning to walk), five babies in the second year, five more in the third year of age, and five adults. To more precisely search for EMG characteristics of gait stability, we also observed maintenance of standing posture in infants in the initial period of learning to walk.

1. Learning process of walking Fig. 4-3 shows longitudinal changes in EMG activity patterns in the learning process of walking for subject A, who began to walk on the 385th day after birth for the first time. Fig. 4-4 shows EMGs in the learning process of walking for subject B, who began to walk on the 306th day. In all subjects tested, excessive muscular activities appeared from the initial period of learning to walk until around 3 years of age, as compared with the corresponding muscular activities of adult walking. In the description that follows, we focus attention on the peculiar EMG activity patterns seen in the infant that deviate from normal adult walking. We looked for EMG patterns that gradually changed and were refined in the transition between first learning to walk and achieving an adult-like pattern, finding such refinements principally in stance phase and in the latter part of swing phase. (See chapters 2 and 3, Figs. 4-1 and 4-2) (Okamoto et al. 1972, 1983, 1985,2001,2003).

An Index of Gait Instability 73

TO

TO

12.5 months

Fe

Fe

1 year 1 month

TA (Tibialis anterior) LG (Gastrocnemius) VM (Vastus medialis) RF (Rectus femoris) BF (Biceps femoris) GM (Gluteus maximus) +--4I+:iI

f'it>l

~r\{"

LG '!ri,"

VM~'Mt~..

~,~,""

1 1 -

,.'#' .,!"",~

"""

,

01

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