Jaynie F. Yang

The initiation of the swing phase in human infant stepping: importance of hip position and leg loading

1 Hip extension and low load in the extensor muscles are important sensory signals that allow a decerebrate or spinal cat to advance from the stance phase to the swing phase during walking. We tested whether the same sensory information controlled the phases of stepping in human infants. 2 Twenty‐two infants between the ages of 5 and 12 months were studied during supported stepping on a treadmill. Forces exerted by the lower limbs, surface electromyography (EMG) from muscles, and the right hip angle were recorded. The whole experimental session was videotaped. 3 The hip position and the amount of load experienced by the right limb were manipulated during stepping by changing the position of the foot during the stance phase or by applying manual pressure on the pelvic crest. Disturbances with different combinations of hip position and load were used. 4 The stance phase was prolonged and the swing phase delayed when the hip was flexed and the load on the limb was high. In contrast, stance phase was shortened and swing advanced when the hip was extended and the load was low. The results were remarkably similar to those in reduced preparations of the cat. They thus suggest that the behaviour of the brainstem and spinal circuitry for walking may be similar between human infants and cats. 5 There was an inverse relationship between hip position and load at the time of swing initiation, indicating the two factors combine to regulate the transition.

Spinal and Brain Control of Human Walking: Implications for Retraining of Walking

In this update, the authors will discuss evidence for both spinal and brain regulation of walking in humans. They will consider the sensory control of walking in young babies and spinal cord–injured adults, two models with weak descending input from the brain, to suggest that subcortical structures are important in shaping walking behavior. Based on evidence from development, the authors suggest that the primitive pattern of walking seen in babies forms the base upon which additional features are added by supraspinal input as independent walking develops. Increasing evidence suggests the motor cortex is important in the control of level-ground walking in adults, in contrast to quadrupeds. This brain input seems particularly important for distal flexors in the leg. Finally, the authors will consider evidence that the recovery of walking after incomplete spinal cord injuries is dependent on the presence of descending input from the motor cortex and our ability to strengthen that input. These findings imply that training methods for improving walking after injury to the nervous system must promote the involvement of both spinal and brain circuits.

Infant stepping: a method to study the sensory control of human walking

1 Stepping responses were studied in infants between the ages of 10 days and 10 months while they were supported to step on a slowly moving treadmill belt. Surface electromyography (EMG) from muscles in the lower limb, force exerted by the feet on the treadmill belt, and the motion of the lower limbs were recorded. 2 Two groups of infants were studied, those who had a small amount of daily practice in stepping and those who did not. Practice resulted in a dramatic increase in the incidence of stepping recorded in the laboratory, particularly for the periods between 1 and 6 months of age. 3 The majority of infants showed clear alternation between the flexor and extensor muscles during walking, regardless of age. Co‐contraction between flexors and extensors, estimated by the overlap in area between rectified and smoothed EMG from a muscle pair, was greater for some muscle groups in the infant compared with the adult. 4 Practice resulted in a significantly lower co‐contraction index for the tibialis anterior‐ quadriceps muscle pair. Practice did not affect the mean step cycle duration. 5 Infants of all ages could step at a range of treadmill speeds by adjusting their step cycle duration. The relationship between the treadmill speed and cycle duration was well fitted by a power function, similar to those reported for intact cats and adult humans. The change in step cycle duration resulted almost entirely from a change in the extensor burst duration, whereas the flexor burst duration remained constant. 6 Airstepping could be elicited in some infants. The cycle durations for airstepping were close to the shortest cycles recorded on the treadmill. 7 In conclusion, the system for generating rhythmic, alternating activity of the lower limbs for stepping is clearly developed by birth. The stepping is sustained and regular, particularly if stepping practice is incorporated briefly each day. The infant population provides a good subject pool for studying the afferent control of walking in the human, before cerebral influences are fully developed. The characteristics and maturity of the system remain to be determined.

Chapter 18 Modification of reflexes in normal and abnormal movements

The trajectories observed for the limb during human locomotion are determined by a mixture of influences, some arising from neural circuits entirely within the central nervous system and others arising from a variety of sensory receptors. Muscle reflexes are highly modulated during locomotion in an adaptive manner within each phase of the step cycle. Furthermore, the modulation can be modified quickly for different tasks such as standing, walking and running, probably by changes in presynaptic inhibition. This modulation is often lost or severely reduced in patients with spasticity after spinal cord or head injury. In normal subjects cutaneous reflexes can be completely reversed from exciting to inhibiting a muscle during each step cycle, particularly in muscles that normally show two bursts of activity per cycle (e.g., tibialis anterior). In some patients stimulation of a mixed nerve (e.g., common peroneal) can directly produce muscle contraction, generate a reflex response (flexor reflex) and transiently reduce spasticity in antagonist (extensor) muscles. Thus, simple systems employing stimulation can enhance gait to a certain extent in patients with incomplete injuries.

Younger is not always better: development of locomotor adaptation from childhood to adulthood.

New walking patterns can be learned over short timescales (i.e., adapted in minutes) using a split-belt treadmill that controls the speed of each leg independently. This leads to storage of a modified spatial and temporal motor pattern that is expressed as an aftereffect in regular walking conditions. Because split-belt walking is a novel task for adults and children alike, we used it to investigate how motor adaptation matures during human development. We also asked whether the immature pattern resembles that of people with cerebellar dysfunction, because we know that this adaptation depends on cerebellar integrity. Healthy children (3–18 years old) and adults, and individuals with cerebellar damage were adapted while walking on split belts (1:2 speed ratio). Adaptation and de-adaptation rates were quantified separately for temporal and spatial parameters. All healthy children and adults tested could learn the new timing at the same rate and showed significant aftereffects. However, children younger than 6 years old were unable to learn the new spatial coordination. Furthermore, children as old as age 11 years old showed slower rates of adaptation and de-adaptation of spatial parameters of walking. Young children showed patterns similar to cerebellar patients, with greater deficits in spatial versus temporal adaptation. Thus, although walking is a well-practiced, refined motor skill by late childhood (i.e., 11 years of age), the processes underlying learning new spatial relationships between the legs are still developing. The maturation of locomotor adaptation follows at least two time courses, which we propose is determined by the developmental state of the cerebellum.

Interlimb co-ordination in human infant stepping

We held infants (aged 4–12 months) over a treadmill to study how they co‐ordinated the two limbs during stepping. We disturbed one limb during the stance or swing phase and recorded the responses (muscle activity and movement) from both lower limbs. Manual disturbances were applied during the stance phase by sliding the foot backward, forcing the limb into the swing phase. Disturbances were also applied in the swing phase by manually extending the hip, interfering with the forward motion of the limb. Additional disturbances were applied to see if both limbs could perform the stance and swing phase synchronously. When the limb was forced to initiate the swing phase on one side, the contralateral limb either prolonged its contact with the ground or quickly established ground contact. When the forward motion of the limb was interrupted in the swing phase, the swing phase was prolonged on the disturbed side and the stance phase prolonged on the contralateral side. In most cases, one leg maintained ground contact. Moreover, it was easy to elicit bilateral, simultaneous stance phase, whereas it was difficult to elicit simultaneous swing phase. In cases where swing phase in the two limbs was initiated close in time, rhythmic alternate stepping was immediately restored in the following step. We conclude that human infants can generate co‐ordinated motor responses bilaterally in response to unilateral perturbations, well before the onset of independent walking.

Changes in Locomotor Muscle Activity After Treadmill Training in Subjects With Incomplete Spinal Cord Injury

Intensive treadmill training after incomplete spinal cord injury can improve functional walking abilities. To determine the changes in muscle activation patterns that are associated with improvements in walking, we measured the electromyography (EMG) of leg muscles in 17 individuals with incomplete spinal cord injury during similar walking conditions both before and after training. Specific differences were observed between subjects that eventually gained functional improvements in overground walking (responders), compared with subjects where treadmill training was ineffective (nonresponders). Although both groups developed a more regular and less clonic EMG pattern on the treadmill, it was only the tibialis anterior and hamstring muscles in the responders that displayed increases in EMG activation. Likewise, only the responders demonstrated decreases in burst duration and cocontraction of proximal (hamstrings and quadriceps) muscle activity. Surprisingly, the proximal muscle activity in the responders, unlike nonresponders, was three- to fourfold greater than that in uninjured control subjects walking at similar speeds and level of body weight support, suggesting that the ability to modify muscle activation patterns after injury may predict the ability of subjects to further compensate in response to motor training. In summary, increases in the amount and decreases in the duration of EMG activity of specific muscles are associated with functional recovery of walking skills after treadmill training in subjects that are able to modify muscle activity patterns following incomplete spinal cord injury.

Training of Walking Skills Overground and on the Treadmill: Case Series on Individuals With Incomplete Spinal Cord Injury

Background and Purpose: Walking in the home and community is an important goal for individuals with incomplete spinal cord injury (iSCI). Walking in the community requires various skills, such as negotiating curbs, doors, and uneven terrain. This case report describes the use of a method to retrain walking overground that is intensive, variable, and relevant to daily walking (skill training). The aims of this case series were to determine the effectiveness of skill training in a small group of people with iSCI and to compare skill training with body-weight–supported treadmill training (BWSTT) in the same individuals. Case Description: Four individuals who were a median of 2.7 years (interquartile range [IQR]=12.8) after iSCI participated in alternating phases of intervention, each 3 months long. All patients started with BWSTT. Two patients subsequently engaged in skill training while the other 2 patients engaged in BWSTT, after which a third phase of intervention (opposite to the second) was repeated. Outcomes: The Modified Emory Functional Ambulation Profile, the 10-Meter Walk Test, the 6-Minute Walk Test, the Berg Balance Scale, and the Activities-specific Balance Confidence Scale were administered before training, monthly throughout training, and 3 months after training. Discussion: Overall improvements in walking speed met or exceeded the minimal clinically important difference for individuals with iSCI (≥0.05 m/s), particularly during the skill training phase (skill training: median=0.09 m/s, IQR=0.13; BWSTT: median=0.01 m/s, IQR=0.07). Walking endurance, obstacle clearance, and stair climbing also improved with both types of intervention. Three of the 4 patients had retained their gains at follow-up (retention of walking speed: median=92%, IQR=63%). Thus, the findings suggest that skill training was effective in this small group of individuals.

Interlimb Coordination in Human Crawling Reveals Similarities in Development and Neural Control With Quadrupeds

The study of quadrupeds has furnished most of our understanding of mammalian locomotion. To allow a more direct comparison of coordination between the four limbs in humans and quadrupeds, we studied crawling in the human, a behavior that is part of normal human development and mechanically more similar to quadrupedal locomotion than is bipedal walking. Interlimb coordination during hands-and-knees crawling is compared between humans and quadrupeds and between human infants and adults. Mechanical factors were manipulated during crawling to understand the relative contributions of mechanics and neural control. Twenty-six infants and seven adults were studied. Video, force plate, and electrogoniometer data were collected. Belt speed of the treadmill, width of base, and limb length were manipulated in adults. Influences of unweighting and limb length were explored in infants. Infants tended to move diagonal limbs together (trot-like). Adults additionally moved ipsilateral limbs together (pace-like). At lower speeds, movements of the four limbs were more equally spaced in time, with no clear pairing of limbs. At higher speeds, running symmetrical gaits were never observed, although one adult galloped. Widening stance prevented adults from using the pace-like gait, whereas lengthening the hind limbs (hands-and-feet crawling) largely prevented the trot-like gait. Limb length and unweighting had no effect on coordination in infants. We conclude that human crawling shares features both with other primates and with nonprimate quadrupeds, suggesting similar underlying mechanisms. The greater restriction in coordination patterns used by infants suggests their nervous system has less flexibility.

Mechanism for reflex reversal during walking in human tibialis anterior muscle revealed by single motor unit recording.

1. A reversal in the sign of a cutaneous reflex during walking was recently described in the human. Such reversals were most clearly seen in muscles that were active in two parts of the step cycle, such as the tibialis anterior (TA). The current study determined whether the reversal resulted from differential activation of a single group of motor units. 2. Single motor units were recorded from the TA muscle of healthy human subjects while they walked on a treadmill with a splint that limited motion of the ankle joint. The majority of motor units from which recordings were made (43 out of 46) were active in both the swing phase and the transition from swing to stance, indicating that the two bursts of activity from the TA muscle do not represent the activity of two separate populations of motor units. 3. The firing behavior of three motor units was observed during walking steps when stimuli were applied to the posterior tibial nerve during either the swing phase or the transition from swing to stance. The post‐stimulus time histograms indicated that the same motor unit was excited during the swing phase, and inhibited during the transition from swing to stance. 4. The results support the hypothesis that there are parallel excitatory and inhibitory pathways from cutaneous afferents to single motoneurones of the TA muscle. A shift in balance between the two pathways as a function of the step cycle most probably generates the reflex reversal observed.