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. 2000 Oct 15;528(Pt 2):389–404. doi: 10.1111/j.1469-7793.2000.00389.x

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

Marco Y C Pang 1, Jaynie F Yang 1
PMCID: PMC2270131  PMID: 11034628

Abstract

  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.

The spinal cord in the cat contains circuitry (central pattern generator) capable of generating alternating flexion and extension activity for stereotypical limb movements such as walking (reviewed in Grillner, 1981). The circuitry can operate without any supraspinal input (Grillner, 1973) or peripheral sensory feedback (Grillner & Zangger, 1974, 1984). Evidence is mounting for a spinal central pattern generator in humans (e.g. Calancie et al. 1994; Dimitrijevic et al. 1998). Moreover, there is ample evidence that the timing and the amplitude of the motor output from the spinal generator is greatly affected by a variety of peripheral sensory information (Rossignol, 1996). The sophisticated sensory control mechanism of locomotion contributes to the activation of muscles (Severin, 1970; Yang et al. 1991; Hiebert & Pearson, 1999; Sinkjaer et al. 2000), and allows the animal to respond to changes in the external environment (Forssberg et al. 1980). One particularly well studied aspect of the sensory control of walking is the control of the transition from the stance to the swing phase.

Grillner & Rossignol (1978) found that preventing the hip from attaining an extended position in chronic spinal cats inhibits the generation of the flexor burst and hence the onset of swing phase. It was thus suggested that the hip position is important in initiating the stance to swing transition. Evidence consistent with this hypothesis was found in decerebrate cats, where the flexor burst was promoted and the extensor activity was shortened by stimulating Ia afferents in the iliopsoas muscle using stretch and vibration (Hiebert et al. 1996). Furthermore, the initiation of the fictive locomotor rhythm in decerebrate cats was reported to be easier when the legs were extended (Pearson & Rossignol, 1991). Entrainment of the locomotor rhythm was also obtained by using sinusoidal stretch of the iliopsoas muscle in non-immobilized decerebrate cats (Hiebert et al. 1996) or using rhythmic hip movements in immobilized spinal (Andersson et al. 1978; Andersson & Grillner, 1981, 1983) and decerebrate cats (Kriellaars et al. 1994).

Apart from hip position, unloading of the extensor muscles in the limb may also be an important sensory signal involved in initiating the stance to swing transition. Duysens & Pearson (1980) found that a contraction force of more than 40 N in ankle extensors led to tonic activation of the extensors in that limb. Previous animal work showed that stimulation of muscle nerves at a strength that recruits the Ib afferents in the extensors during the extensor burst causes prolongation of extensor activity. This result was found in different preparations of the cat, including immobilized decerebrate (Gossard et al. 1994; McCrea et al. 1995), non-immobilized decerebrate (Whelan et al. 1995), immobilized spinal (Conway et al. 1987; Pearson & Collins, 1993; Gossard et al. 1994; McCrea et al. 1995) and non-immobilized spinal (Pearson et al. 1992; Pearson & Collins, 1993). Furthermore, mechanical loading of the extensors in walking decerebrate cats also produced similar effects (Hiebert & Pearson, 1999). It has been proposed that the decrease in positive feedback signals carried by the group Ib afferents from the extensors at the end of stance phase allows for the subsequent generation of flexor activity.

In contrast to the robust effects of hip position and load on walking in the cat, the effects on humans are less certain. The effects of hip position in human walking have not been studied. Loading, whether by electrical (Stephens & Yang, 1996) or mechanical (Stephens & Yang, 1999; Misiaszek et al. 2000) methods, produced weak effects in adult human subjects. It is possible that there is a fundamental difference between humans and cats in the way stance and swing phase are regulated. Alternatively, it is also possible that the differences result from a difference between the state of the animal (i.e. healthy adult humans and decerebrate or spinal cats). There is some evidence to suggest that these effects are strongest in paralysed, spinal cats (Conway et al. 1987; Pearson & Collins, 1993; Gossard et al. 1994; McCrea et al. 1995) and weaker in the less reduced preparations (Whelan et al. 1995; Whelan & Pearson, 1997; Hiebert & Pearson, 1999). Perhaps these effects are a characteristic of the spinal circuitry, which is modified by the presence of supraspinal input (Whelan & Pearson, 1997; Hiebert & Pearson, 1999).

The stepping response in human infants is thought to be mainly controlled by the brainstem and spinal circuitry (Peiper, 1961; Forssberg, 1985). Full myelination of the corticospinal tract does not occur until the age of 2 (Yakovlev & Lecours, 1967). Moreover, the threshold for eliciting muscle activity in the upper and lower extremities using transcranial magnetic stimulation is very high in children under the age of 2 (Koh & Eyre 1988; Eyre et al. 1991; Muller et al. 1991). Hence, it is reasonable to suggest that the brainstem and spinal circuitry involved in the stepping response in infants is subject to less cortical influence than in adults. Therefore, infants provide a good human model for studying the underlying behaviour of brainstem and spinal circuitry in response to the changes in sensory input.

While the earlier studies have focused on the effect of either hip position or load, the relationship between the two factors is largely unknown. Hip position and load usually vary together such that the observed effects are difficult to attribute to one or the other factor. Thus, it is critical that the experiment be designed in such a way that would allow for separating the effects of hip position from those of load. Moreover, it is important to determine how different sensory inputs are combined to reach decisions for motor output.

The present study examined how hip position and load affected the initiation of the swing phase in infant stepping. Our hypothesis is that the hip position and the amount of load both play a role in regulating the stance to swing transition in infant stepping. We used a variety of hip disturbances that also allowed us to study the interaction between the change in hip position and loading. The results suggest that both hip position and load have powerful effects on modifying the step cycle in human infants. The two factors are combined to determine the stance to swing transition. The behaviour of the brainstem and spinal circuitry involved in the stepping response is strikingly similar to that in reduced preparations of the cat.

METHODS

Subjects

The infants in this study were recruited through the maternity wards of the hospitals and the public health division of Capital Health in Edmonton, Alberta. All of the infants in this study were born at term. Ethical approval for this study was obtained through the Health Research Ethics Board, University of Alberta and the Capital Health Authority, Edmonton, Alberta. Twenty-two infants aged from 5 to 12 months (mean: 7.5 months) were studied. All of the infants studied could not walk independently. Approximately 2–3 weeks before the scheduled experimental session, the parent was asked whether the infant showed any stepping response. Only those infants who made six consecutive steps, as reported by the parent, were brought in for the experiment. The parent was instructed to practice stepping with the infants for 1–2 min daily until the date of the experiment (Yang et al. 1998a). Informed and written consent was obtained from the parent before the infant participated in the study. The study was performed according to the Declaration of Helsinki.

Recording procedures

The skin was cleaned with alcohol swabs before applying the Beckman-type, bipolar (1 cm diameter, electrode separation of 1 cm) surface electromyographic (EMG) electrodes. For 10 of the 22 subjects, the electrodes were placed over four muscle groups in the right leg: (1) tibialis anterior (TA), (2) gastrocnemius-soleus (GS), (3) quadriceps (Q), and (4) hamstrings (HAMS). For the other 12 subjects, the four pairs of EMG electrodes were placed on the TA and GS on both legs.

A twin-axis electrogoniometer (Penny and Giles, Biometrics, Blackwood, Gwent, UK) was placed over the right hip joint to assess the hip position during disturbed and undisturbed stepping. One arm of the goniometer was in line with the mid-axillary line of the trunk and the other with the longitudinal axis of the right femur pointing toward the lateral epicondyle. A video camera (Panasonic PV-950) recorded the movement of the left side of the infant. In order to identify the key landmarks on video, adhesive skin markers were placed over the superior border of the iliac spine, the greater trochanter, the knee joint line and the lateral malleolus of the left leg.

A Gaitway treadmill system (Kistler Instrument Corp., Amherst, NY, USA) was used for each experiment. Two force plates located beneath the treadmill belt one in front of the other were used to measure vertical ground reaction forces during walking. Each subject was weighed by sitting the infant on one of the force plates.

To elicit walking, a researcher held the infant under the arms, with one hand on each side of the infant’s upper trunk. The researcher attempted to hold the infant in a stationary position over the treadmill without imposing any movements on the infant. The infant was allowed to support as much as possible of its own weight and was centred on the treadmill at the junction of the two force plates. An accurate measurement of load on the limb at swing initiation during undisturbed stepping can be obtained by examining the rear force plate signals (for details regarding the interpretation of the force plate signals, see Fig. 1). The speed of the treadmill was adjusted so that optimal stepping responses could be obtained. Several trials of treadmill walking were conducted for each infant. The entire experiment was videotaped. Electromyography, force plate and electrogoniometer signals were amplified and recorded on VHS tape with a pulse code modulation encoder (A.R. Vetter, Rebersburg, PA, USA). The video and analog signals were synchronized by a digital counter at a rate of 1 Hz. The experiment was approximately 1 h long for each infant.

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

Figure 1

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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.

Hip disturbances

Four types of disturbances were employed to study the effects of hip position and load on the initiation of swing: (1) backward disturbance, which extends the hip and decreases the load, (2) mid-disturbance, which keeps the hip in a slightly flexed or neutral position and the load remains high, (3) forward disturbance, which flexes the hip and decreases the load and (4) loading, which increases the load as the hip extends in the late stance phase. The four disturbances generated different combinations of hip position and load, so that the relationship between the two factors could be examined by comparing the responses to different disturbances. All the disturbances were applied after good, sustained stepping was obtained.

The first three types of disturbances altered the foot position on the treadmill by placing a piece of cardboard under the right foot. Because the cardboard can slide against the treadmill belt, the position of the foot, and hence the whole leg, could be manipulated by pulling on the cardboard. The cardboard was always removed immediately after the disturbance, and undisturbed stepping continued.

Backward disturbance (Fig. 2A)

Figure 2. Schematic illustration of the disturbances.

Figure 2

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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.

Typically, the cardboard was placed on the treadmill during the swing phase on the right. At the end of the swing phase, the right foot came into contact with the cardboard. At this time or slightly later, one of the experimenters disturbed the limb by pulling on the cardboard in a backward direction faster than the speed of the treadmill belt. This accelerated the limb toward hip extension and also decreased the load.

Mid-disturbance (Fig. 2B)

As the right foot stepped onto the cardboard, the experimenter maintained the right limb in a mid-stance position. As a result, the hip joint was slightly flexed or neutral and the load was relatively high during the disturbance. The disturbance was longer, because we wished to determine whether stepping could be prevented on one side while the other side continued stepping.

Forward disturbance (Fig. 2C)

The experimenter drew the cardboard slightly forward in order to flex the hip. As the hip was being flexed, the load on the limb was decreased simultaneously because of the forward movement.

Loading (Fig. 2D)

As the right limb approached late stance, extra load was added to the limb by briefly applying manual pressure downward on the superior iliac crest of the pelvis. Effort was made so that no observable hip flexion occurred as a result of the disturbance.

Data analysis

The data were analysed off-line. The EMG data were high pass filtered at 10 Hz, full-wave rectified and low pass filtered at 30 Hz. The force plate and the electrogoniometer signals were also low pass filtered at 30 Hz. All the signals were then A/D converted at 250 Hz (Axoscope 7, Axon Instruments, Foster City, CA, USA).

The video record was reviewed in detail to identify good sequences of walking and successful disturbances. The corresponding analog data were then identified. Sustained, undisturbed stepping was defined as four consecutive and alternating steps. All the undisturbed steps for each subject were selected and averaged using a custom written software program. The front and rear force plate signals during the averaged step cycle were then summed at each point in time, and the mean value over the cycle determined. This gave an estimate of how much weight the infant was bearing during stepping.

The disturbance was included in the analysis only if (1) it was preceded and followed by a good step, and (2) it succeeded in disturbing the limb as described under ‘hip disturbances’. The step cycle and swing durations of the undisturbed and disturbed steps were estimated by the time of right foot contact and toe off, respectively, as indicated by the force plate signals or the video image, whichever gave the clearest definition of the step cycle. The hip angle at which swing was initiated was determined by the goniometer reading, where it showed a clear reversal in direction from extension to flexion.

All disturbances were induced by the experimenter manually, so variability between disturbances was inevitable. It was therefore important to quantify the characteristics of each disturbance as accurately as possible. The magnitude of the disturbance in which the foot was displaced was determined by the distance the foot travelled during the disturbance, measured from the video record. The duration of the disturbance was also estimated from the video record (inter-frame interval: 33 ms), so that the velocity of the disturbance could be determined.

In order to estimate how much load was added during the loading trials, the rear force plate signal for the right leg during the pre-disturbed and disturbed step was analysed. An example of such a disturbance is shown in Fig. 8A. We assumed that the right leg slid onto the rear force plate at approximately the same time in its step cycle during the pre- and disturbed step. This is a reasonable assumption because the infants were held stationary over the treadmill while they stepped. The rear force plate signal for the right leg during the pre-disturbed step (demarcated by the vertical continuous lines in Fig. 8A) was superimposed on that during the disturbed step (demarcated by the dashed lines), with alignment at the beginning. The difference between the two signals was obtained for each point in time, and its mean value computed. This provided an estimate of the load added by the experimenter during the disturbed step. Only those trials in which the infant was centred on the treadmill with good force plate signals were used for this analysis.

Figure 8. Responses to loading disturbances.

Figure 8

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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.

For mid-disturbances, the load of the disturbed limb was registered by the front force plate. However, its signal might be affected by the left foot because it continued to step and made contact with the front part of the treadmill as well. Therefore, the load during the disturbance was estimated by averaging the selected sections of front force plate signal when the left limb was not in contact with the front force plate. The mean hip angle during the mid-disturbance was estimated by averaging the goniometer signal for the entire duration of the disturbance. These means were calculated using custom written software programs (MATLAB SIMULINK, Natick, MA, USA).

Statistical analysis

For each subject, the mean values of the stance, swing and step cycle duration, the hip angle (for pre-disturbed, disturbed and post-disturbed steps) as well as the load at swing initiation (for pre-disturbed and disturbed steps) were obtained by averaging the values obtained in all successful trials. The means from each subject were then entered into the following statistical tests. Repeated measures of analysis of variances (ANOVA) were used to determine if there were significant differences in (1) stance phase, (2) swing phase and (3) step cycle duration as well as (4) hip angle at swing initiation for the pre-disturbed, disturbed and post-disturbed steps (significance level at 0.05). Student’s t test with Bonferroni’s correction was used to compare the data post hoc. A significance level of 0.017 was used to reduce the probability of making type I errors associated with multiple comparisons (Glass & Hopkins, 1996). Paired t tests were used for comparison of data pairs such as load and hip angle at swing initiation, magnitude and velocity of the disturbance. An α level was set at 0.05 for all paired t tests.

RESULTS

The speed of the treadmill ranged from 0.23 to 0.41 m s−1 (mean: 0.29 m s−1). The mean amount of weight borne by the infants during stepping was 37 N (s.d.= 16 N) or 40 % (s.d.= 12 %) of their own body weight (BW) (range = 15–85 N or 20–71 %BW).

Reponses to backward disturbances

The number of successful disturbances was 28 from 10 subjects (number of trials per subject: median, 2; mean, 3). A representative example is shown in Fig. 3A. With the application of a backward disturbance, the load on the disturbed limb was decreased (see Fig. 3A, arrow on rear force plate signal) while the hip was being extended (right hip angle). The stance phase and step cycle durations of the disturbed step were shortened. The EMG recording also showed an early onset of TA burst indicating an early onset of swing.

Figure 3. Responses to backward disturbances.

Figure 3

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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.

In examining the group data, the mean hip angle at which the disturbance was initiated and ended was 21 deg (s.d.= 14 deg) and −14 deg (s.d.= 10 deg), respectively, with positive angles representing flexion. The mean displacement and velocity of the disturbance was 0.35 m (s.d.= 0.08 m) and −0.86 m s−1 (s.d.= 0.25 m s−1), respectively, with positive values representing forward motion. The stance and step cycle durations for the disturbed step were significantly decreased (37 and 14 %, respectively) when compared to those of the pre-disturbed step (Fig. 3B). The swing phase, however, showed no significant difference. The hip angle at swing initiation was similar for the pre-disturbed (−10 deg, s.e.m.= 4 deg), disturbed (−12 deg, s.e.m.= 3 deg) and post-disturbed step (−6 deg, s.e.m.= 4 deg) and the difference was not statistically significant (not shown). With the application of backward disturbances, the load on the disturbed limb was also significantly reduced at the time of swing initiation (Fig. 3C). The results showed that the extension of the hip and the reduction of load apparently created a condition favourable for swing initiation. Note that the number of subjects included in the load comparison was less than that in other analyses, because some infants were not quite centred on the treadmill in some trials. Therefore, an accurate measure of load could not be obtained in some trials. This situation occurred occasionally in all other types of disturbances.

Responses to mid-disturbances

The number of successful disturbances obtained was 25 from nine subjects (number of trials per subject: median, 2; mean, 3). The consistent response was that the disturbed step remained in stance phase while the contralateral limb continued to step. An individual example is shown in Fig. 4A. The limb was held in a slightly flexed position and the load was quite high (around 20 N or 25 %BW). The disturbed limb stopped stepping while the contralateral limb continued to step. Correspondingly, the EMG from the right limb showed tonic GS and TA activity during the disturbance. In contrast, the EMG of the contralateral limb showed several alternating TA and GS bursts throughout. During the disturbance, the infant’s right foot remained on the front force plate. Hence, the force signal remained high on the front force plate. Superimposed on the signal level from the force of the right foot were additional peaks associated with the stepping of the left foot (Fig. 4A).

Figure 4. Responses to mid-disturbances.

Figure 4

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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.

When pooled across subjects, paired t tests revealed that the amount of hip flexion (24 deg, s.e.m.= 6 deg) and load (23 N, s.e.m.= 3 N) during the disturbance were significantly higher than those for the pre-disturbed step at swing initiation (5 deg, s.e.m.= 5 deg; 12 N, s.e.m.= 2 N) (Fig. 4B and C). The combination of increased hip flexion and load apparently created a condition unfavourable for swing initiation. Since the stance and step cycle duration could be indefinitely prolonged, and thus were entirely dependent on the duration of the disturbance, no statistical tests were used to compare the durations.

Responses to forward disturbances

The number of successful disturbances was 72 obtained from 14 subjects. The mean start and end positions of the disturbance were 19 deg (s.d.= 18 deg) and 24 deg (s.d.= 17 deg) of hip flexion, respectively. The mean displacement and velocity of the disturbance were 0.13 m (s.d.= 0.08 m) and 0.24 m s−1 (s.d.= 0.13 m s−1), respectively. Note that forward and backward disturbances started at approximately the same hip angle. The amount of hip movement due to the forward disturbance was smaller than that for the backward disturbance. This was because both types of disturbances were initiated soon after right foot contact (i.e. when the hip was quite flexed). Therefore, forward disturbances did not produce as great a change in hip angle as backward disturbances. The net velocity of the forward disturbances would have been much higher had the speed of the treadmill (mean: 0.29 m s−1) been taken into account. In other words, the change in the velocity of the foot was 0.24 m s−1+ 0.29 m s−1= 0.53 m s−1.

Following the application of forward disturbances, two very different responses were obtained. One type of response was that the swing phase was much delayed. Once the disturbance was over, the limb continued through a stance phase and swing was initiated only after the hip was well extended, just as in undisturbed steps. In the other type of response, hip flexion was initiated at a very flexed hip angle immediately following the disturbance. Therefore, the data for forward disturbances were divided into two groups (A and B) according to the response obtained and they were analysed separately.

Responses from group A

The first type of response observed was that the disturbed limb did not initiate the swing until it reached an extended position. As a result, the stance phase and step cycle durations of the disturbed step were substantially prolonged. This response was observed in 39 out of a total of 72 successful forward disturbances (12 out of 14 subjects; number of trials per subject: median, 2; mean, 3). One representative example is shown in Fig. 5A. During the disturbance, the hip was kept in a flexed position (around 30 deg) and load was decreased to about 7 N (8 %BW). Swing did not occur until much later when the hip was extended to −4 deg. The EMG recording also showed a delay in onset of the TA burst.

Figure 5. The first type of response to forward disturbances.

Figure 5

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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.

In our group data, the mean stance and step cycle durations of the disturbed step showed a significant increase (137 and 82 %, respectively) in comparison to the pre-disturbed step (Fig. 5B). In this analysis, we compared the load at swing initiation for the pre-disturbed step with the load at the end of the disturbance. We were interested in whether the load was higher than normal at the end of the disturbance to prevent the initiation of swing. The results showed that the load on the right leg at swing initiation for the pre-disturbed step (11 N, s.e.m.= 3 N) and that at the end of the forward disturbance during the disturbed step (7 N, s.e.m.= 1 N) were not significantly different (Fig. 5C). Even though the load was similar between the pre-disturbed and disturbed steps, swing was initiated only after the limb continued through the stance phase and again reached an extended position. The mean hip angle at swing initiation for the disturbed step was 4 deg (s.e.m.= 4 deg), which was not significantly different from that for the pre-disturbed step (−1 deg, s.e.m.= 3 deg) and the post-disturbed step (5 deg, s.e.m.= 5 deg).

Responses from group B

Another type of response observed following the forward hip disturbance was that the swing phase of the disturbed limb could be initiated even when the hip was in a flexed position, provided that the load was extremely low (<5 N). This particular response was observed in 33 out of a total of 72 forward disturbances (11 out of 14 subjects; number of trials per subject: median and mean were both 3). A typical example is given in Fig. 6A. During the disturbance, the hip was flexed. Note that the load on the right limb was not well measured in the last one-third of the disturbance because the left limb stepped on the front plate. The vertical thick dashed lines in Fig. 6A represent the time period when both feet were on the front force plate. Our best estimate of load on the right leg during this same period is represented by the thin dotted line, which is a linear interpolation between the two points in time when only the right foot was on the front force plate. After this period, the force of the left foot was registered only by the rear force plate whereas that of the right foot was registered by the front force plate. Therefore, the load on the right limb at the end of the disturbance could be accurately measured by the front force plate after the left foot left the front force plate (see arrow), and was found to be very low (5 N, 5 %BW). The disturbed limb responded by initiating flexion at a flexed hip angle. The EMG signal also showed the TA burst immediately following the disturbance.

Figure 6. The second type of response to forward disturbances.

Figure 6

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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.

The pooled data indicated that the stance and step cycle durations for the pre-disturbed step were not significantly different from those for the disturbed step. The swing phase also showed no significant change (Fig. 6B). The mean hip angle at swing initiation for the disturbed step (18 deg, s.e.m.= 3 deg) was much more flexed than that for the pre-disturbed (−9 deg, s.e.m.= 2 deg) and the post-disturbed step (8 deg, s.e.m.= 5 deg) (Fig. 6C). The difference was statistically significant. The mean load at swing initiation on the right limb for the disturbed step was extremely low (2 N, s.e.m.= 1 N) compared with that for the pre-disturbed step (13 N, s.e.m.= 1 N) (Fig. 6D) and the difference was statistically significant.

In these particular trials, load was low (which favours swing initiation), and the hip was flexed (which does not favour swing initiation). We wanted to determine whether the state of the contralateral limb might also affect when the ipsilateral limb initiates flexion in this situation. Interestingly, in most trials, the swing initiation occurred just before the contralateral limb made foot contact or when it was in early to mid stance phase (Fig. 7).

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

Figure 7

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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).

Two different responses are related to different amount of load reduction

In order to determine if the two very different responses to forward disturbances (A, swing phase delayed; and B, swing initiated) were a result of the difference in the amount of load reduction and not other characteristics of the disturbances, paired t tests were used to compare the disturbances. Only subjects who showed both types of responses were included in the analysis (9 subjects). The load at the end of the disturbance was statistically different between the two conditions (A: load = 7 N, s.e.m.= 1 N vs. B: load = 2 N, s.e.m.= 1 N). The hip angle at which the disturbances were initiated (A: 20 deg, s.e.m.= 5 deg vs. B: 20 deg, s.e.m.= 5 deg), the extent of the disturbances (A: 0.12 m, s.e.m.= 0.01 m vs. B: 0.18 m, s.e.m.= 0.04 m) and the velocity of the disturbances (A: 0.25 m s−1, s.d.= 0.10 m s−1vs. B: 0.28 m s−1, s.d.= 0.10 m s−1) were not significantly different between the two conditions (paired t tests, α= 0.05). Therefore, it is likely that the two types of responses resulted from differences in the load on the limb at the end of the disturbance, not from the other characteristics of the disturbance.

Responses to loading

The number of successful disturbances was 47 obtained from 13 subjects (median: 3; mean: 4). The mean load increase due to the disturbance for each subject was 10 N or 11 %BW (s.e.m.= 2 N, 2 %BW). Generally, the stance phase duration was prolonged and the swing was delayed due to the disturbance. A representative example is illustrated in Fig. 8A. The EMG recording demonstrated a delay in TA activation during the disturbed step. The group data showed that the stance and step cycle durations were increased significantly (30 % and 22 %, respectively) when compared to the pre-disturbed step (Fig. 8B). As the stance phase was prolonged, it was predicted that the hip would be brought to a more extended position by the motion of the treadmill belt before swing was initiated. Our results showed that there was a significant difference in the hip angle at swing initiation between the disturbed (−12 deg, s.e.m.= 3 deg) and post-disturbed step (−6 deg, s.e.m.= 2 deg). However, the difference between the pre-disturbed (−7 deg, s.e.m.= 4 deg) and the disturbed steps was not statistically significant. This could be related to the difficulty in recording hip angles accurately (see Discussion, Technical and methodological considerations). The results also indicated that the load at swing initiation was significantly higher for the disturbed step (19 N, s.e.m.= 3 N) than that for the pre-disturbed step (10 N, s.e.m.= 1 N) (Fig. 8C).

Interaction between hip position and load

The above data suggest that the decision to initiate the swing phase may depend on the interaction of the two variables: load and hip position. For example, load at swing initiation for the disturbed step was the highest in loading trials (19 N) and the lowest in forward disturbances with extremely low load (2 N). In contrast, the trend for the hip angle at swing initiation for these same conditions was exactly the opposite, with the largest degrees of flexion occurring in forward disturbances with extremely low load (18 deg) and the largest degrees of extension occurring in the loading trials (−12 deg) with higher loads. Using these two sets of data, the relationship between hip position and load was plotted in Fig. 9A. The data were quite scattered, however, probably because the placement of the goniometer varied between infants and the weight of the infants was different. To remove some of the variability that resulted from the goniometer signal, the mean hip angle at swing initiation for each subject was expressed as the difference from that in undisturbed stepping. A positive difference value indicates that the hip angle at swing initiation for the disturbed step was more flexed than that in undisturbed stepping. A negative value indicates the opposite. This value was referred to as the right hip angle difference in Fig. 9B. The load was also normalized and expressed as the percentage body weight of each infant. The scatter was much less and the data were fitted with a linear regression equation (r= 0.74).

Figure 9. The interaction of hip position and load.

Figure 9

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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 9A and B shows data points obtained at the time swing phase was initiated under the two specific disturbance conditions: forward disturbance with very low load and loading. In order to determine whether the other situations also agreed with the same regression line, the data from these other conditions were superimposed on the regression line from Fig. 9B. The disturbances that greatly delayed swing initiation (mid-disturbance and forward disturbance with higher load) are shown by filled symbols (Fig. 9C) and the conditions that facilitated an earlier transition into swing are shown by open symbols. The majority of the data points unfavourable for swing initiation lie above the regression line whereas those favourable for swing initiation were located below it. Thus, we feel that the regression line is a good representation of the critical combination of the two factors required to initiate swing phase.

DISCUSSION

The data demonstrate that the sensory control of the stance to swing transition in infant stepping is strikingly similar to decerebrate (Duysens & Pearson, 1980; Hiebert et al. 1996) and spinal cats (Grillner & Rossignol, 1978). It is apparent that the attainment of hip extension and the reduction of load at the end of the stance phase are both important for the initiation of the subsequent swing phase. Moreover, there is an inverse relationship between the two factors at the time of swing initiation, indicating that they are interdependent in determining the beginning of the swing phase.

Technical and methodological considerations

We will first address some technical issues that may have affected our results. First, there was considerable variability in the load and hip angle data (Fig. 9A). Variation in the load could be related to differences in body weight. Variation in the hip angle could be related to the difficulty in measuring joint angles accurately. While we attempted to position the goniometer in the same way for each infant, differences in the relative movement of skin and bone will clearly add to the variability. While the normalization removed some of the variability, the scatter was still large (Fig. 9B). Thus, while we are certain that both factors contribute to the initiation of swing phase and that there is a general inverse relationship between the two factors, we cannot be certain about the exact relationship (i.e. linear or non-linear).

Second, there was no direct measurement of the force produced by the extensor muscles. Only the vertical ground reaction forces were used as an indication of the load on the limb. Therefore, one cannot claim with certainty that the load measured reflects the load in the extensor muscles. In the loading trials, the load was applied along the long axis of the stance limb. Thus, the extensor muscles of that limb must have borne some of the extra load, because otherwise, the limb would have collapsed. In the forward disturbances, when the load measured by the force plate was low, presumably the ankle and knee extensors were unloaded, because both extensors were in a shortened position. The hip extensors, however, were in a stretched position, so they may have been experiencing some additional load due to the forward disturbances. Thus, while the ground reaction force cannot provide an accurate estimate of forces in the extensor muscles, it provides a reasonable estimate of the total load experienced. Load-sensitive receptors of all types, including those in muscle, bone and skin, could have contributed to the responses.

Third, we had a global measure of hip angle only. Changes in hip angle will be associated with stretch of the muscles, joint capsule and skin around the hip. This study cannot address the role of these different afferent systems.

Similarities between human infants and reduced preparations of the cat

Infant stepping showed many striking similarities to reduced preparations of the cat. For example, in spinal cats, the generation of the alternating extensor and flexor bursts was inhibited and replaced by tonic extensor activity when the limb was held in a flexed position while the contralateral limb continued stepping throughout (Grillner & Rossignol, 1978). The human infants showed exactly the same response to mid-disturbances (Fig. 4). In spinal cats, the flexor burst was generated only when the limb reached an extended position (Grillner & Rossignol, 1978). The human infants showed a similar response to the backward disturbances (Fig. 3). Accelerating the limb toward extension causes an early onset of TA. The responses to leg loading in human infants are also consistent with the findings in previous experiments in decerebrate and spinal cats (Conway et al. 1987; Pearson et al. 1992; Pearson & Collins, 1993; Gossard et al. 1994; McCrea et al. 1995; Whelan et al. 1995; Hiebert & Pearson, 1999). Increased load on the limb caused a prolongation of the stance phase and a delay of the onset of the swing phase.

Relationship between hip position and load

Our data indicate not only that both hip position and load contribute to the regulation of the stance to swing transition, but also that there is an interaction between the two factors. There is not a specific value of hip extension or load that must be reached before swing can be initiated, rather, it is a combination of the two factors (Fig. 9B). For example, as the load increases, the hip position required for swing initiation becomes increasingly more extended. On the other hand, as the load decreases, the critical hip angle for swing initiation becomes more flexed, i.e. the range of hip angle in which swing can be initiated is quite large. Observations consistent with this idea of interaction between the two systems were reported by Hiebert et al. (1996) based on their observations in decerebrate cats. They found that stretching the iliopsoas muscle by the same amount caused less reduction in the duration of extensor activity during quadrupedal walking than when the disturbed leg was immobilized. Perhaps when the limb was immobilized, the feedback from competing afferents was less and hence the same stretch in the iliopsoas muscle produced a greater effect (Hiebert et al. 1996). Moreover, their unpublished data showed that electrically stimulating the nerves to the ankle extensors or stretching these muscles in an immobilized leg preparation also decreased the influence of the stretch-sensitive afferents from the flexors to the central pattern generator (K. G. Pearson, personal communication).

Hiebert et al. (1996) have proposed a model of the organization of the sensory input to the central pattern generator based on their work on decerebrate cats. The model is based on the ‘half-centre’ organization, which is an over-simplification of the real system, but a useful conceptual model for this purpose. According to their model, inputs from stretch-sensitive afferents from flexor muscles have an excitatory effect on the ipsilateral flexor half-centre and an inhibitory effect on the ipsilateral extensor half-centre, whereas the force-sensitive afferents from extensor muscles have an excitatory effect on the ipsilateral extensor half-centre only (Hiebert et al. 1996). According to their model, when forces are high in the extensor muscles, the flexor half-centre is inhibited as an indirect effect from the extensor half-centre (e.g. consistent with data from Gossard et al. 1994). However, the possibility of an inhibitory input from the force-sensitive afferents directly onto the ipsilateral flexor half-centre cannot be excluded. For example, if the generation of the flexor burst was dependent solely on the removal of the inhibition from the extensor half-centre, one would have expected a significant decrease in the level of extensor activity just before the swing phase is initiated. There were numerous examples in our data, such as that shown in Fig. 4, which showed that the eventual initiation of the TA burst was not preceded by a sudden decrease in GS activity. Therefore, we favour a model that includes the inhibitory input from the extensor force-sensitive afferents to the ipsilateral flexor half-centre (Fig. 10). Our data cannot address the specific afferents involved, but qualitative comparison with the model can still be made. For example, in the situation when load is high and hip flexors are stretched (i.e. loading trials), the model would predict that there are competing inputs to the flexor half-centre on the ipsilateral side. Since the load is higher than normal in late stance, the flexor half-centre would receive more inhibition than usual. Consequently, a greater degree of hip extension would be necessary to generate sufficient excitation to allow swing to start. Conversely, the initiation of swing is also possible when the hip is quite flexed as long as the load is extremely low.

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

Figure 10

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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.

In the situation where sensory input from both the extensors and flexors to the central pattern generator are reduced (i.e. forward disturbance with extremely low load), what additional factors may have been important in determining when the swing phase was initiated? The data indicated that the activity of the contralateral limb may have an effect. In the majority of cases when the load was very low during forward disturbances, swing phase was initiated when the contralateral limb was either in very late swing or in early to mid stance (Fig. 7), that is, when the contralateral extensor half-centre was active. Presumably, there might have been less inhibition from the contralateral flexor half-centre on the ipsilateral flexor half-centre at those times. Rarely did the initiation of the swing phase occur when the contralateral limb was in the middle of the swing phase. This is different from the spinal cat, in which the swing initiation occurred most frequently when the contralateral limb was either in mid-stance or in mid-swing (Grillner & Rossignol, 1978). It was suggested that the swing initiation during contralateral mid-swing corresponds to a gallop step. If this is so, our results suggest that the human infants, unlike the cat, rarely show in-phase stepping. It also indicates that the inhibition between the two flexor half-centres is quite strong. The relationship between the two extensor half-centres, in contrast, seems to be much less potent. One limb could remain in the stance for a prolonged period while the contralateral limb continues to step (Fig. 4). Exactly how the contralateral limb affects the initiation of swing in the ipsilateral limb will require further study.

How do the various factors combine to reach a decision whether or not to initiate the swing phase? A variety of models have been proposed to explain how sensory signals might be used in combination for motor decisions (Bassler, 1993; Prochazka, 1996a, b). Our results do not support the model of finite state (conditional) control (Prochazka, 1996a). For example, one of the rules that has been proposed for this situation is that IF extensor force is low AND hip is extended, THEN initiate swing (Prochazka, 1996a). This rule is inconsistent with our results during forward disturbances (i.e. when the hip was flexed). Our interaction model (Figs 9 and 10) suggests that the swing initiation in infant walking is governed by a combinatory approach similar to one used in engineering control systems, called ‘fuzzy logic’ (Prochazka, 1996a,b). According to this model, motor behaviour is determined by the relative contribution of various sensory inputs at a particular point in time. The concept of fuzzy logic is analogous to the ‘parliamentary principle’ proposed by Bassler (1993) based on the work in stick insects. The final motor output is dependent upon the relative strength of opposing inputs. Intracellular recordings provided evidence for this parliamentary principle at the interneuronal and motoneuronal level in stick insects (Bassler, 1993). Our results suggest a similar control mechanism in regulating the initiation of swing phase in infant walking.

Difference between human infants and adults

There are some clear differences in the sensory control of walking between human adults and infants. The effect of changes in hip position is technically very difficult to test in adult humans. The effects of load have been tested and shown to be much more modest in adult subjects compared to infants (Stephens & Yang, 1996, 1999; Yang et al. 1998b). One of the reasons for these differences between adults and infants might be that there is increased supraspinal control of walking with maturation of the nervous system (Stephens & Yang, 1999). Presumably, cortical control can override the spinal and brainstem circuitry, and initiate the swing phase when it deems this to be appropriate. Alternatively, the spinal and brainstem circuitry might change with maturation such that these earlier patterns of control are modified. Whatever the reason, it remains interesting that the behaviour of the immature human system is so similar to that in reduced preparations of the cat. Whether this spinal and brainstem circuitry plays a more important part in controlling walking after damage to the cortex or descending input remains to be determined. A decrease in hip extension during late stance is seen commonly in patients with cortical or spinal cord damage (Visintin & Barbeau, 1989; Moseley et al. 1993). Moreover, spasticity in extensor muscles may make it difficult to relax and prepare the limb for swing. There are some reports that the hip has to be moved into extension in order for spontaneous hip flexion to occur during assisted treadmill locomotion in spinal cord-injured subjects (Dobkin et al. 1995). The extensor EMG amplitude also varies with the degree of body weight support after spinal cord injury (Visintin & Barbeau, 1989; Dobkin et al. 1995). These factors could contribute to the difficulties encountered by patients in initiating the swing phase of walking and will require further study.

Acknowledgments

This work was supported in part by a Medical Research Council of Canada grant and a Natural Sciences and Engineering Research Council grant to J.F.Y.; M.Y.C.P. was supported by scholarships from the Alberta Heritage Foundation for Medical Research, the Province of Alberta and the Faculty of Graduate Studies and Research at the University of Alberta. We thank Ms Serah O and Dr Adrienne Wright for technical assistance, Dr S. Patrick for the line drawings, and Drs K. G. Pearson and A. Prochazka for helpful comments on earlier versions of this manuscript.

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