Measurement and Analysis of Human Infant Crawling for Rehabilitation: A Narrative Review.

When a child shows signs of potential motor developmental disorders, early diagnosis of central nervous system (CNS) impairment is beneficial. Known as the first CNS-controlled mobility for most of infants, mobility during crawling usually has been used in clinical assessments to identify motor development disorders. The current clinical scales of motor development during crawling stage are relatively subjective. Objective and quantitative measures of infant crawling afford the possibilities to identify those infants who might benefit from early intervention, as well as the evaluation of intervention progress. Thus, increasing researchers have explored objective measurements of infant crawling in typical and atypical developing infants. However, there is a lack of comprehensive review on infant-crawling measurement and analysis toward bridging the gap between research crawling analysis and potential clinical applications. In this narrative review, we provide a practical overview of the most relevant measurements in human infant crawling, including acquisition techniques, data processing methods, features extraction, and the potential value in objective assessment of motor function in infancy; meanwhile, the possibilities to develop crawling training as early intervention to promote the locomotor function for infants with locomotor delays are also discussed.

Analysis of the Inter-Joints Synergistic Patterns of Limbs in Infant Crawling.

Hands and knees crawling is an important motor developmental milestone, which is characterized by diagonal coordination between upper and lower limbs. However, the features of inter-joint synergy within each limb in infant crawling is still not clear. Therefore, the aim of this study was to extract the inter-joint synergistic patterns during infant crawling and to test the possibilities of using the extracted inter-joint synergy to distinguish developmental delayed (DD) infants from typical developing (TD) infants. In this paper, kinematic data were collected from the shoulder, elbow, wrist, hip, knee, and ankle joints when 9 TD infants and 9 DD infants were crawling on hands and knees at their self-selected velocity. Tangential velocity was firstly calculated from the three-dimensional (3D) trajectory of each joint. Then, the non-negative matrix factorization (NMF) method was used to extract the joints synergistic patterns of each limb from the tangential velocity data. Our preliminary results showed that the crawling movement could be represented by a joint synergistic pattern, which consisted of three joints' data. In addition, we observed that the distal joint had a greater impact than the proximal joints during infant crawling. Moreover, it was found that the DD infants could be preliminarily distinguished from the TD infants by the features of inter-joint synergy during their crawling stage.

Inter-Limb Muscle Synergies and Kinematic Analysis of Hands-and-Knees Crawling in Typically Developing Infants and Infants With Developmental Delay.

Hands-and-knees-crawling is an important motor developmental milestone and a unique window into the development of central nervous system (CNS). Mobility during crawling is regularly used in clinical assessments to identify delays in motor development. However, possible contribution from CNS impairments to motor development delay is still unknown. The aim of this study was to quantify and compare inter-limb muscle synergy and kinematics during crawling among infants at a similar developmental age, however, clinically determined to be typically developing (TD, N = 20) infants, infants at risk of developmental delay (ARDD, N = 33), or infants with confirmed developmental delay (CDD, N = 13). We hypothesized that even though all of the groups are at a similar developmental age, there would be differences in kinematic measures during crawling, and such differences would be associated with CNS impairment as measured by electromyography (EMG) features. Surface EMG of eight arm and leg muscles and the corresponding joint kinematic data were collected while participants crawled on hands and knees at their self-selected velocity. Temporal-spatial parameters and normalized Jerk-Cost (JC) function (i.e., smoothness of movement) were computed from the measured kinematics. The inter-limb muscle synergy and the number of co-activating muscles per synergy were measured using EMGs. We found that the infants with CDD demonstrated higher normalized JC values (less movement smoothness), fewer muscle synergies, and more co-activating muscles per synergy, compared to infants with TD (p < 0.05) and ARDD (p < 0.05). Furthermore, the normalized JC values were correlated (p < 0.05) with the number of co-activation muscles per synergy. Our results suggest a constrained neuromuscular control strategy due to neurological injury in infants with CDD, and such constrain may contribute to the reduced movement smoothness in infant crawling.

Inter-Limb Muscle Synergy of Hands-and-Knees Crawling in Typical Developing Infants and Infants with Developmental Delay.

The aim of this study was to quantify and compare the inter-limb muscle coordination during crawling between typically developing infants and infants with developmental delay. Typically developing (TD, $\text{N}=$20) infants and infants with at risk of developmental delay (ARDD, $\textbf{N}=$33) or confirmed developmental delayCDD, N=14) participated in this study. Surface electromyography of eight muscles from arms and legs and the corresponding joint kinematic data were collected while they were crawling on hands and knees at their self-selected velocity. The number of used inter-limb muscle synergies during crawling was identified by nonnegative matrix factorization algorithm. Our results showed that there was no significant difference in the number of used muscle synergies between ARDD and TD infants during crawling. However, a reduced number of synergies were identified in infants with CDD, as compared to that in TD and ARDD infants, indicating constrained neuromuscular control strategy during crawling in developmental delayed infants. The absence of inter-limb muscle synergies may be one of the mechanisms underlying the impairments of crawling in developmental delayed infants, who are at high risk of cerebral palsy. This result also suggests that the metrics of muscle synergy during infant crawling, such as the number of synergy, may be feasible as a biomarker for early diagnosis of infants with cerebral palsy.

Synergistic recruitment of multi-scale myoelectric oscillations of upper limb during infant crawling.

It has been widely accepted that the central nervous system (CNS) modulates muscle synergies to simplify motion control. However, it is still unclear that if there is a synergistic recruitment strategy to organize oscillation components of surface electromyography (sEMG) signals for limb movement. The sEMG signals were recorded from bilateral biceps brachii (BB) and triceps brachii (TB) muscles during infant crawling. The multivariate empirical mode decomposition (MEMD) was applied to decompose multi-channel sEMG signals into multi-scale oscillations. Then, non-negative matrix factorization (NMF) method was employed to extract oscillation synergy patterns. The results indicated that there were three stable oscillation synergies in sEMG signals for crawling movement, and the recruitment coefficient curves reflected the role of muscle during crawling movement. Our preliminary work suggested that synergistic recruitment of multi-scale oscillation components maybe a new way to understand the organization of MU recruitment strategy by the CNS.

Motor Skill Development Alters Kinematics and Co-Activation Between Flexors and Extensors of Limbs in Human Infant Crawling.

Hands and knees crawling is an important motor developmental milestone but the current clinical measures of motor function during crawling stage are relatively subjective. Objective metrics using kinematics and electromyography (EMG) in infant crawling may provide more stable and accurate measures of such developmental milestone, demonstrating changes in locomotion during age span. The purpose of this paper was to determine whether joint kinematics and the underlying co-activation between flexor and extensor in infant crawling are different for arms and legs across the infant age span. Surface EMG of two pairs of flexors and extensors from arms and legs and the corresponding joint kinematic data were collected in twenty health infants (11 males and 9 females, range 8-15 months), while they were crawling on hands and knees. Co-activation index of averaged EMG was used to quantify the simultaneous contractions between flexor and extensor muscles. Coefficient of variation of joint's maximum vertical acceleration from multiple cycles was used to quantify the repeatability of kinematics during crawling. Our results indicated that the arm exhibited significantly higher co-activation and higher repeatability of joint movement than the leg, suggesting earlier development of arm compared to leg. Moreover, elder age groups, who had stronger walking ability developed, showed increased co-activation of the leg and significant increase in repeatability of the knee movement. These results were consistent with the rapid reinforcement of the leg during motor development from quadrupeds to bipedal walking. Furthermore, the EMG and kinematic parameters were significantly correlated with clinical variables. These results suggest that the EMG and kinematic analysis of infant crawling are useful in building effective assessment of infant's motor function before independent walking.

The variability of co-activation pattern of antagonist muscles in human infant crawling.

Infant crawling is part of normal human gross motor development, and a 4-beat gait that involves rhythmical flexion and extension of limbs and the underlying muscle co-activation of antagonist muscle around the joint. However, detection the co-activation pattern of antagonist muscle are sparse due to the general difficulty of measuring locomotion in human infants. In this paper, sEMG of antagonist muscles and the corresponding kinematics data of limbs were collected when infants were crawling on hands and knees at their self-selected speed. The infant's gross motor developmental status was assessed by the global Gross Motor Function Measure Scale (GMFM-88) as well. The method based on EMG-EMG plots was used to quantify the variability of co-activation pattern of antagonist muscle. After that, we observed that antagonist muscles of upper limb (triceps brachii and biceps brachii) showed less variability of co-activation pattern of muscles than lower limb(quadriceps femoris and hamstrings) during crawling, and this variability was also varied in different crawling phases (stance and swing). Furthermore, we found some varied behaviors in the co-activation patterns of antagonist muscles when gross motor developmental level increased. The preliminary work suggests that such adaptive changes may be related to the adjustment of neuromuscular in the early stage of gross motor development.

Antagonist muscle co-activation of limbs in human infant crawling: A pilot study.

Muscle Co-activation (MCo) is the simultaneous muscular activation of agonist and antagonist muscle groups, which provides adequate joint stability, movement accuracy during movement. Infant crawling is an important stage of motor function development that manifests non-synchronization growth and development of upper and lower limbs due to the well-known gross motor development principle of head to toe. However, the effect of MCo level for agonist and antagonist muscle groups on motor function development of limbs has not been previously reported. In this paper, sEMG signals were collected from triceps brachii (TB) and biceps brachii (BB), quadriceps femoris (QF) and hamstrings (HS) of limbs when fourteen infants were crawling at their self-selected speed. Antagonist muscle co-activation was evaluated by measuring two common indexes (co-activation index and Pearson's correlation coefficient).A significant difference was observed between upper limbs and lower limbs, but the relationship between MCo and speed of crawling was poor. This study is an opening for further investigation including a longitudinal study and compare against infant with CNS disorders.