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

Abstract

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. 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. 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. 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. 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.

Figure 1. The force plate signals in relation to the step cycle

Top, schematic illustration of the infant at three instances in the step cycle. Note that the infant was placed on the treadmill, at the junction between the front and the rear force plate. Bottom, the corresponding force plate (FP) signals are shown with the three instances in time indicated by the vertical dashed lines. The letters L and R under the front plate signal indicate the time of left and right foot contact, respectively. The L and R under the rear force plate indicate the time each foot slides onto the rear force plate. A, the right foot has made contact with the front force plate (note the corresponding rise in front force plate signal). The left leg is in late stance and its force is registered by the rear force plate (note the fall in rear force plate signal). B, the right leg is in the mid-stance phase. The force of the right leg is registered by the front and rear force plates (see the fall in front force plate signal and the rise in rear force plate signal). Meanwhile, the left foot is in swing phase, and does not contribute to any of the force plate signals. C, the right leg is in late stance and its force is registered by the rear force plate (see the fall in rear force plate signal). The left foot has made contact with the front force plate, causing a rise in the front force plate signal.

Figure 2. Schematic illustration of the disturbances

A, backward disturbance. A piece of cardboard was placed on the treadmill during the right swing phase. Immediately after the right foot came into contact with the cardboard, the hip was pulled toward extension by drawing the cardboard backward. The load on the limb was reduced as a result. B, mid-disturbance. The limb was maintained in a mid-stance position by keeping the cardboard stationary under the body. The load remained high. C, forward disturbance. The hip was pulled toward flexion by drawing the cardboard forward. The load was decreased as a result. D, loading. Extra load was added to the limb by applying manual pressure downward and backward on the superior iliac crest of the pelvis when the limb was in late stance.

Figure 8. Responses to loading disturbances

A, response to a loading disturbance from a single subject. Electromyography, force plate signals and right hip angle before, during and after a loading disturbance from subject BJ. Additional load was applied to the right limb during late stance. Note the increase in force associated with the disturbance (see arrow in rear force plate signal). The limb responded by delaying its swing initiation, thereby increasing the stance and step cycle durations. Also note the delay in TA onset. B, mean stance, swing and step cycle durations for the step preceding, during and after the disturbance (13 subjects). The stance and step cycle durations were significantly prolonged due to the disturbance. C, load at swing initiation for the steps preceding and during the disturbance (12 subjects). The load was significantly higher for the disturbed step than that for the pre-disturbed step.

Figure 3. Responses to backward disturbances

A, response to a backward disturbance from a single subject. Electromyography, force plate signals and right hip angle changes before, during and after a backward disturbance from subject GW. The duration of the disturbance is indicated by the thick horizontal line between the 3rd and 4th trace. The force in newtons (N) and as a percentage of the infant’s body weight (%BW) are both shown. Note that the rear force plate signal did not reach zero between the peaks for the steps preceding the disturbance. This is because the right foot came into contact with the rear force plate before the left foot came off. The hip was accelerated toward extension by the disturbance (see increase in downward slope of the goniometer signal during the disturbance). The load was simultaneously decreased (see arrow in rear force plate signal). The limb responded to the disturbance by initiating the swing phase earlier, thereby decreasing the stance phase and step cycle durations. Note also the early onset of TA activity caused by the disturbance (see arrow). B, mean stance, swing and step cycle durations for the steps preceding (pre), during (disturbed) and after (post) the disturbance (10 subjects). The error bars represent 1 standard error of the mean. The same convention is used in all figures of the same type. *Statistically significant difference compared to the pre-disturbed step. The stance and step cycle durations were significantly shortened by the disturbance. C, load at swing initiation (9 subjects). The limb was significantly unloaded by the disturbance. Some trials were excluded from the load comparison because the subject was not quite centred on the treadmill. An accurate measure of load, therefore, could not be obtained in those cases.

Figure 4. Responses to mid-disturbances

A, responses to a mid-disturbance from a single subject. Electromyography, force plate signals and right hip angle before, during and after a mid-disturbance from subject JU. During the disturbance, the hip was kept in a slightly flexed position (10–20 deg). The load of the limb remained high (about 25 %BW, see front force plate signal). The right limb stopped stepping while the left limb continued to step. Note the termination of alternating TA and GS activity in the right limb during the disturbance whereas the left limb showed alternating TA and GS throughout. B, mean hip angle at swing initiation for the pre-disturbed step and the hip angle during the disturbance (9 subjects). The hip angle was more flexed during the disturbance than that at swing initiation for the pre-disturbed step. C, load at swing initiation for the pre-disturbed step and the load during the disturbance (9 subjects). The results show that the load remained high during the disturbance.

Figure 5. The first type of response to forward disturbances

A, example of the first type of response (from group A) to a forward disturbance from a single subject. Electromyography, force plate signals and right hip angle before, during and after a forward disturbance from subject GW. The right hip was kept in 20–30 deg in flexion transiently (see goniometer signal). The load was also reduced to 8 %BW by the disturbance (see arrow in front force plate signal). Despite the reduction in load, the limb continued its stance phase after the disturbance was over (note the increase in front force plate signal immediately after the disturbance). The swing phase was initiated only when the hip was again well extended. The stance and step cycle durations were prolonged as a result. Note also the delay in TA onset (see arrow). The L/R on the rear and front force plate signals indicate that both legs moved back onto the rear force plate and then stepped onto the front force plate at approximately the same time. B, mean stance, swing and step cycle durations for the steps preceding, during and after the disturbance (12 subjects). The stance and step cycle durations were significantly prolonged by the disturbance. C, load at swing initiation for the pre-disturbed step and the load at the end of the disturbance (9 subjects) were not significantly different.

Figure 6. The second type of response to forward disturbances

A, example of the second type of response (from group B) to a forward disturbance from a single subject. Electromyography, force plate signals and right hip angle before, during and after a forward disturbance with extremely low load from subject NA. The right hip was transiently flexed to about 10 deg. The thick dashed lines demarcate the period when both feet were on the front force plate. The thin dotted line in the front FP signal represents our best estimate of load on the right leg during this same period (see text for more details). Note that the right limb was almost completely unloaded at the end of the disturbance (5 %BW, see arrow in front force plate signal immediately following the second thick dashed line). Note also the decrease in GS activity during the disturbance. The limb responded by initiating a swing phase while the hip was still in flexion (see arrow in R hip angle trace). Note the onset of TA burst associated with the initiation of swing phase (see arrow). B, mean stance, swing and step cycle durations for the steps preceding, during and after the disturbance (11 subjects). The stance and the swing phase durations did not show any significant change. C, right hip angle at swing initiation for the steps preceding, during and after the disturbance (11 subjects). The hip angle for the disturbed steps was much more flexed than the pre-disturbed step. D, load at swing initiation for the steps preceding and during the disturbance (9 subjects). The limb was significantly unloaded by the disturbance.

Figure 7. Swing initiation as a function of the state of the contralateral (left) leg

The left step cycle duration (horizontal axis) was divided into eight different bins, four for the stance phase and four for the swing phase. The first bin begins at the time of left foot-floor contact and the last bin ends at the same event. The vertical axis indicates the number of occurrences of swing initiation of the right leg following forward disturbances with extremely low load (total: 11 subjects, 33 trials). The data shows that in most trials, swing phase was initiated on the right when the contralateral limb was either in early to mid stance phase or in very late swing (i.e. just before left foot contact).

Figure 9. The interaction of hip position and load

A, each data point represents the mean hip angle and load at swing initiation for each subject obtained in all successful trials of loading (12 subjects) and forward disturbances with extremely low load (9 subjects). Although a general inverse relationship was noted, the data were quite scattered. B, the data from A were normalized before plotting in this graph. The hip angle at swing initiation was subtracted from the mean hip angle at swing initiation in undisturbed stepping for each subject and expressed as the right hip angle difference. The load was expressed as the percentage of each subject’s body weight. The variability was much reduced. The data points were fitted with a linear regression equation (r= 0.74). The results indicate that there is an inverse relationship between hip position and load in regulating the stance to swing transition. C, the data points for mid-disturbances (9 subjects, represented by filled circles) and forward disturbances (not including those with extremely low load) (11 subjects, represented by filled triangles) were superimposed on the regression line. These represent conditions where swing phase was not initiated. Almost all the data points are located above the line. The data points for the backward disturbances (10 subjects) are shown by open squares. These represent conditions where swing phase was initiated early. All of the data points fall below the line. Thus, the area above the line represents conditions unfavourable for swing initiation whereas that below the line represents conditions favourable for swing initiation.

Figure 10. A model of the organization of the sensory input to the central pattern generator

The locomotor rhythm for each limb is generated by mutually inhibiting extensor (E) and flexor (F) half-centres. The black dots represent inhibitory connections whereas the bars represent excitatory connections. The extensor and flexor half-centres on each side project to the extensor (EXT) and flexor (FLEX) motoneuronal pools respectively. The stretch-sensitive afferents from the flexors inhibit the ipsilateral extensor half-centre and excite the ipsilateral flexor half-centre. The force-sensitive afferents from the extensors excite the ipsilateral extensor half-centre and inhibit the ipsilateral flexor half-centre. Strong reciprocal inhibition exists between the two flexor half-centres.