Electromyographic developmental changes in one individual from newborn stepping to mature walking

doi:10.1016/S0966-6362(02)00049-8

Gait & Posture

Volume 17, Issue 1, February 2003, Pages 18-27

https://doi.org/10.1016/S0966-6362(02)00049-8 Get rights and content

Abstract

Electromyographic (EMG) recordings of the lower limbs were made from a girl from 3 weeks after birth until 7 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 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.

Introduction

During the first 3 years of life, human bipedal locomotion develops gradually towards mature walking throughout a series of phases: newborn stepping, infant supported walking (Fig. 1), infant independent walking, and child walking [1], [2], [3], [4], [5], [6], [7], [8], [9], [10], [11], [12]. In the 20th century, some studies have provided detailed technical descriptions (kinematics, kinetics, temporal events, and electromyography (EMG)) of the developmental process of infant locomotion, although to study gait in babies using adult techniques [13], [14] is very difficult.

McGraw [1] 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 [15] 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 [2], [3], [5], [6], [7], [9], [11]. Forssberg [6], Thelen et al. [5], and Okamoto et al. [2], [7], [11] have studied the developmental process from newborn stepping until infant supported walking prior to independent walking, and Sutherland et al. [9] and Okamoto et al. [3], [7], [11] 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 7 years, from 3 weeks after birth to 7 years of age, so that the entire span of gait development could be examined in one individual.

Section snippets

Methods

We made longitudinal observations on a female infant from 3 weeks after birth until 7 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 select

Results

Based on the longitudinal EMG findings of the present investigation as well as from previous studies [2], [3], [7], [11], 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 Fig. 2, Fig. 3, Fig. 4

Discussion

During the first 3 years of life, movements related to walking appear to begin with gross patterns of muscle activation, frequently including co-activation of mutual antagonists. We observed a progression from excessive gross activation to more efficient and economical production of muscle activities in the lower limbs. This was seen, not only in supported walking and then in subsequent independent walking, but also in neonatal primitive walking (Fig. 7, Fig. 8) [2], [3], [5], [6], [7], [9],

Acknowledgements

The authors express deep gratitude to Dr H. Yamashita, H. Tsutsumi (Kansai Medical University), and Dr Y. Goto (Hyogo University of Teacher Education) for their cooperation.

References (17)

M.B. McGraw
Neuromuscular development of the human infant as exemplified in the achievement of erect locomotion
J. Pediat.
(1940)
T. Okamoto et al.
Electromyographic study of newborn stepping in neonates and young infants
Electromyogr. Clin. Neurophysiol.
(2001)
T. Okamoto et al.
Electromyographic characteristics at the onset of independent walking in infancy case
Electromyogr. Clin. Neurophysiol.
(2001)
E. Thelen et al.
The developmental origins of locomotion
E. Thelen et al.
Relationship between newborn stepping and later walking: a new interpretation
Dev. Med. Child. Neurol.
(1987)
H. Forssberg
Ontogeny of human locomotor control, Infant stepping, supported locomotion and transition to independent locomotion
Exp. Brain Res.
(1985)
T. Okamoto et al.
Human infant pre-independent and independent walking
E. Thelen et al.
Newborn stepping: an explanation for a ‘disappearing’ reflex
Dev. Psychol.
(1982)

There are more references available in the full text version of this article.

Cited by (65)

What lies beneath the brain: Neural circuits involved in human locomotion
2020, The Neural Control of Movement: Model Systems and Tools to Study Locomotor Function
Understanding neural circuitry involved in human locomotor behavior depends on inferences due to the difficulty in making direct measures. In this chapter, we provide a brief history of the inferences that have been drawn from observations in other animals, highlight the mechanistic conservation between species, and suggest how advances in technology have progressed our understanding of the neural control of locomotion in humans.
Biomechanics of the infant foot during the transition to independent walking: A narrative review
2018, Gait and Posture
Citation Excerpt :
This was matched in a larger research study (N = 8) at the onset of independent walking and 3 months later; co-contraction of the lower limb musculature was evident, alongside high variability between steps in individuals with low walking experience [26]. Similarly, longitudinal changes in muscle recruitment strategies have been quantified in infants of 6 to 12 months of age, with reductions in agonist-antagonist coactivation [59,60]. The pattern of lateral gastrocnemius activation (in terms of probability of onset over the gait cycle) from early infancy appears to relatively closely replicate that of the more experienced independent walking and young adults [27,61].
Recognising structural and functional development of the paediatric foot is fundamental to ensuring a strong theoretical framework for health professionals and scientists. The transition of an infant from sitting to walking takes approximately 9 months and is when the structures and function of the foot must respond to the challenges of bearing load; becoming increasingly more essential for locomotion. Literature pertaining to the phase of development was searched. A narrative approach synthesised the information from papers written in English, with non-symptomatic infant participants up to the development stage of independent walking or two years of age. A range of literature was identified documenting morphological, physiological, neuromuscular and biomechanical aspects of the infant within this phase of development. The progression of variable gait to a regular pattern is documented within a range of studies focusing on neuromuscular control and ambulation development. However, methodological approaches may have compromised the external validity of such data. Additionally, limited consideration for the specific function and development of the foot is evident, despite its role as the primary site of weight bearing and interface with the floor. A lack of consideration of infants prior to ambulation (i.e. before cruising or walking) is also apparent which prevents a reference baseline being used effectively. This review also identifies future research priorities such that a comprehensive understanding of foot development from a non-weight bearing to a weight bearing structure during locomotor advancement can be gained.
Tibial impact accelerations in gait of primary school children: The effect of age and speed
2017, Gait and Posture
Tibial stress fractures are associated with increased lower extremity loading at initial foot-ground contact, reflected in high peak positive acceleration (>8 g) of the tibia in adults. There is no reported data on peak positive acceleration of the tibia in children during walking and running. The aim of this study was to establish tibial peak positive acceleration responses in children across a range of age and gait speeds. Twenty-four children aged 8.5 ± 1.4 years with no known gait pathology comprised two age groups; Young (7–9 year, n = 12) and Older (10–12 years, n = 12). Wireless Inertial Measurement Unit comprising a tri-axial accelerometer was securely taped to the anteromedial aspect of the distal tibia to measure peak positive acceleration responses while walking and running on the treadmill at 3 different speeds (20% below baseline, baseline, and 20% above baseline). Results showed significant increase in peak positive acceleration with increased gait speed and greater variability in young children compared to older children. The study suggests that ground impact in walking, but not running, is mature by age 7 years. Future studies should explore strategies using peak positive acceleration responses to monitor ground impact during sport activities and its application in gait retraining.
Dual-belt treadmill familiarization: Implications for knee function in moderate knee osteoarthritis compared to asymptomatic controls
2017, Clinical Biomechanics
Effect of treadmill familiarization on knee function in osteoarthritis is not clear. Purpose was to determine whether spatiotemporal characteristics, knee joint biomechanics and muscle activation patterns change as individuals with and without medial compartment knee osteoarthritis familiarize to dual-belt treadmill walking over 6 min.
20 individuals with knee osteoarthritis and 20 asymptomatic controls walked at a self-selected speed. Spatiotemporal characteristics, sagittal plane joint motions, sagittal and frontal plane moments and knee joint muscle activation patterns, amplitude normalized to maximum isometric contractions were analyzed. Discrete measures were extracted from each biomechanical waveform and principal component analysis was used to determine knee joint muscle activation patterns. Statistical significance was determined using Analysis of Variance models (alpha = 0.05).
Spatiotemporal gait characteristics, knee motion and moment differences were found between groups however no group by time interactions existed and no changes in these variables were found over 6 min of walking. Group differences in muscle activation patterns were found in all muscle activations. Muscle activation amplitude and patterns at minute 5 and 6 were generally lower, less prolonged and more dynamic when compared to minute 1 and 3.
Individuals with and without medial compartment knee osteoarthritis familiarized to treadmill walking in a similar manner. Minimal changes to knee biomechanics were found during treadmill familiarization. Five to six minutes of familiarization should be considered for surface electromyography in these populations.
The developmental dynamics of gait maturation with a focus on spatiotemporal measures
2017, Gait and Posture
Gait analysis is recognised as a powerful clinical tool for studying relationships between motor control and brain function. By drawing on the literature investigating gait in individuals with neurological disorders, this review provides insight into the neural processes that contribute to and regulate specific spatiotemporal sub-components of gait and how they may mature across early to late childhood. This review also discusses the roles of changing anthropomorphic characteristics, and maturing sensory and higher-order cognitive processes in differentiating the developmental trajectories of the sub-components of gait. Importantly, although studies have shown that cognitive-gait interference is larger in children compared to adults, the contributing neurocognitive mechanisms may vary across age groups who have different types of attentional or cognitive vulnerabilities. These findings have implications for current models of gait maturation by highlighting the need for a dynamic model that focuses on the integration of various factors that contribute to gait though experience and practice. This is essential to elucidating why gait and other motor deficits are often contiguous with cognitive neurodevelopmental disorders.
Time since onset of walking predicts tibial bone strength in early childhood
2014, Bone
Citation Excerpt :
During crawling and standing bodyweight is supported on two or more limbs, whereas a single limb supports the body during walking. During early walking the forefoot is predominately in contact with the ground [50], creating a long lever for the calf muscle to act against. Hence, the effect of walking may have ‘over-ridden’ any previous associations with the other activities.
Bone strength in adulthood is known to be affected by health at birth and early childhood. Habitual bone loading is a primary determinant of bone strength in later childhood and adulthood. However, the effects of physical activity in early childhood (e.g. crawling, standing and walking) on bone strength are unknown. Fifty-three children (twenty-seven males) were included in a longitudinal study in their early infancy. Shortly after birth (0.3 ± 0.3 months), details of mass and height were obtained along with a pQCT scan at 20% distal–proximal tibia length. At 14.8 ± 0.5 months of age the same data were collected, along with details of age at onset of standing, crawling, supported and unsupported walking. Time since onset of walking unsupported was associated with greater bone mass, cortical bone area, pericortical circumference and polar moment of inertia of both total and cortical bone (all P < 0.05). There were no significant associations between other physical activity timepoints and bone measures. Age at onset of walking was not significantly related to mass, length or bone measures at birth. The results suggest that time since attainment of independent walking — representing exposure of the tibia to the large reaction and muscular forces associated with locomotion — is a primary determinant of bone strength in early childhood. This finding raises the possible opportunity of physical activity interventions at young age in paediatric populations associated with low childhood bone strength and late walking (e.g. low birth weight, cerebral palsy and Down's Syndrome, etc.).

View all citing articles on Scopus

View full text

Electromyographic developmental changes in one individual from newborn stepping to mature walking

Abstract

Introduction

Section snippets

Methods

Results

Discussion

Acknowledgements

J. Pediat.

Electromyographic study of newborn stepping in neonates and young infants

Electromyogr. Clin. Neurophysiol.

Electromyographic characteristics at the onset of independent walking in infancy case

Electromyogr. Clin. Neurophysiol.

The developmental origins of locomotion

Relationship between newborn stepping and later walking: a new interpretation

Dev. Med. Child. Neurol.

Ontogeny of human locomotor control, Infant stepping, supported locomotion and transition to independent locomotion

Exp. Brain Res.

Human infant pre-independent and independent walking

Newborn stepping: an explanation for a ‘disappearing’ reflex

Dev. Psychol.