| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
|
|
|
|||||||
|
|||||||||
Department of Physiology, University of Alberta, Edmonton, Canada
Submitted 16 May 2005; accepted in final form 28 July 2005
 |
ABSTRACT |
|---|
 TOP ABSTRACT INTRODUCTIONMETHODSRESULTSDISCUSSIONGRANTSACKNOWLEDGMENTSREFERENCES |
|---|
|
INTRODUCTION |
|---|
|
TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONGRANTSACKNOWLEDGMENTSREFERENCES |
|---|
; Duysens et al. 2000; Lam and Pearson 2002b; Pearson 2003). Sensory feedback is crucial for adapting motor output to injury or growth (Pearson 2000) and ensures that locomotor output is appropriate for the task at hand (Prochazka 1996; Rossignol et al. 1988). One of the most important roles for feedback during walking is to control the timing of the transition from stance to swing. This has been demonstrated in the walking systems of insects (Bässler and Büschges 1998; Pearson and Duysens 1976), cats (Grillner and Rossignol 1978; Pearson 1995; Whelan et al. 1995), and human infants (Pang and Yang 2000). In the hind leg of the cat, the sensory receptors involved in mediating the stance-to-swing transition have not been fully identified, but they include Golgi tendon organs in ankle extensor muscles (Pearson et al. 1998; Whelan et al. 1995) and muscles spindles fom hip flexor muscles (Hiebert et al. 1996). Behavioral observations in spinal cats and human infants also indicate the importance of afferent signals from the hip in controlling the initiation of the swing phase (Grillner and Rossignol 1978; Pang and Yang 2000).
Given the importance of afferent feedback in controlling the transition from stance to swing, it is reasonable to ask whether the transition from swing to stance is similarly controlled. Afferent regulation of this transition would be an effective way to ensure correct placement of the foot during stance despite the different movements required by different locomotor tasks. A crucial aspect of a stable transition to stance is a sufficiently protracted leg, thus making the position of the hip a good candidate for an afferent signal regulating the swing-to-stance transition. Evidence for this role has come from recent observations of the effects of perturbing hip movements in decerebrate walking cats (Lam and Pearson 2001). Assisting hip flexion during the swing phase results in a shortening of flexor burst duration and an increase in duration of the subsequent bursts in extensors. Resisting hip flexion during swing has the opposite effect. In some situations, resisting hip flexion leads to the maintenance of flexor activity for the duration of the resisting perturbation (Lam and Pearson 2001). Another indication for a role of hip afferents in promoting the transition from flexion to extension is that imposed flexion movements of the hip during fictive locomotion in DOPA/nialamide-treated spinal cats shorten flexor burst duration when applied near the end of the flexor bursts (Andersson and Grillner 1981). Recently a similar observation has been made in the foreleg during fictive locomotion in decerebrate cats (Saltiel and Rossignol 2004). Protraction of the shoulder near the end of the burst activity in flexor motoneurons shortens the duration of flexor bursts and promotes an earlier onset of extensor activity. Thus in both hind legs and forelegs, there are good indications that sensory receptors in proximal regions of the legs are involved in controlling the timing from swing to stance.
An important aspect of this transition in the hind legs is the initiation of activity in knee and ankle extensor muscles commencing 
80 ms before ground contact. This prestance extensor activity occurs during the first extension (E1) phase of the locomotor cycle, i.e., during the period when the knee and ankle joints are extending (Engberg and Lundberg 1969). Thus gaining an understanding of the mechanisms regulating the timing of swing-to-stance transition requires knowledge of the neuronal mechanisms responsible for initiating burst activity in the knee and ankle extensor muscles near the end of the swing phase. As mentioned earlier, there is now some evidence from reduced preparations to suggest that afferent signals linked to flexion movement of the hip joint can influence the timing of the onset of extensor activity. If this is also true for normal walking animals, then we predicted that some feature(s) of the kinematics of movement at the hip joint should be correlated with the timing of the onset of the E1-associated extensor activity. A similar logic was used in an earlier study reporting a role for hip afferents in regulating the extension to flexion (stance to swing) transition (Grillner and Rossignol 1978). Thus one objective of this investigation was to determine the relationship between joint kinematics and the time of onset of ankle extensor activity in normal walking cats. To dissociate movements at the hip from movements at the knee and ankle joints, we examined animals stepping in a variety of situations: a horizontal treadmill, up and down steps, and stepping over objects.
Another objective of the present investigation was to examine in more detail the influence of imposing flexion movements of the hip on extensor activity in decerebrate walking cats. This influence was examined only qualitatively in the earlier study (Lam and Pearson 2001). Here we determined the relationship between the time of termination of flexor bursts and the time of onset of the subsequent extensor bursts with the aim of establishing the extent to which these two events are linked when hip flexion is assisted. In addition we measured the value of hip joint angle at the time of the transition from flexor to extensor activity with and without assisting hip flexion during the swing phase to assess whether a sensory signal related to hip position could be a factor in the initiation of the swing-to-stance transition. A preliminary description of some of our findings has been published (Pearson et al. 2003).
|
METHODS |
|---|
|
TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONGRANTSACKNOWLEDGMENTSREFERENCES |
|---|
Assisting hip flexion in decerebrate walking cats
The procedure for examining the effects of assisting hip flexion was similar to that used in an earlier investigation from our laboratory (Lam and Pearson 2001). Briefly, each animal (n = 2) was anesthetized with isoflurane, and a tracheal cannula inserted for continued administration of the anesthetic. Blood pressure was monitored via a cannula inserted into one carotid artery, and the other carotid was ligated. One jugular vein was cannulated for the administration of fluids and drugs. The left hind leg was then partially dennervated by cutting the saphenous, sural, superficial peroneal, and distal tibial nerves. This removed cutaneous input from most of the hind leg. Bipolar recording electrodes (Cooner Wire AS632) were then sewn into the iliopsoas (IP) and medial gastrocnemius (MG) muscles of both hind legs. The wires of these electrodes were led under to skin to a multi-terminal connector positioned above the animal's back. Next, the iliac crests were exposed, and a stout wire was threaded through holes drilled in both crests. The two ends of the wire were clamped to each crest. This wire was later clamped to an external frame to support the hindquarters while the animal was walking on a treadmill. Reflective markers (diameter: 0.5 cm) were placed above the iliac crest, the hip joint, and knee and ankle joints and on the paw and toe of the left leg. These markers were used to determine the kinematics of leg movements using the Peak Motus 8.2 motion-analysis system (Peak Performance Technologies). Triangulation was used to determine the position of the knee joint.
After this preparatory procedure, the animal was transferred to a frame mounted above a treadmill. The head was placed in a sterotaxic holder and wire through the iliac crest fixed to a supporting frame. Approximately 2.5-cm-wide surgical tape was wrapped around the thigh of the left hind leg, and a loop of 1.5 mm string was attached to the anterior edge of the tape. This loop was used to manually assist hip flexion during walking sequences. The animal was then decerebrated by transecting the brain stem rostral to the superior colliculus and mammillary bodies and removed from the anesthetic immediately following decerebration. Both animals began to walk spontaneously 30 min later, although electrical stimulation of the mesencephalic locomotor region (Grillner and Shik 1973; Shik et al. 1966) was used to facilitate walking in one animal.
EMG and kinematic analysis of hind leg movements in intact animals
The second objective of this investigation was to determine which kinematic parameters of hind leg movement correlate with the onset of ankle extensor activity immediately preceding the swing-to-stance transition. This was examined in four intact adult cats walking in a variety of situations: a horizontal treadmill at different speeds (described as "treadmill" in figures), along a series of steps at –25, 0, and 25° angles (described as "down pegs," "level pegs," and "up pegs" in figures), and stepping over an object placed on a horizontal walkway (described as "leading" or "trailing" in figures). Figure 4 shows three of these tasks. Each animal was first trained daily for 1–2 wk to walk consistently in the three situations. Training consisted of inducing animals to participate in the various tasks with food and affection rewards, and lasted for 1 h/day. Next, bipolar EMG electrodes (Cooner Wire AS632) were implanted into muscles of the right hind leg under general anesthetic (isoflurane) and aseptic conditions. In all animals, EMG electrodes were placed in the knee extensor vastus lateralis (VL), the hip flexor iliopsoas (IP), and the ankle extensors soleus (Sol), lateral gastrocnemius (LG), medial gastrocnemius (MG). In three animals, electrodes were also placed in knee flexor/hip extensor semitendinosus (ST) muscle. The leads from the EMG electrodes were led under the skin to a multi-pin socket fixed with screws and dental acrylic to the animal's skull. While anesthetized, adhesive reflective markers (diameter: 0.5 cm) were placed over the iliac crest, the hip, knee, and ankle joints, and on the end of the paw and the fifth digit of the right hind leg.
|
In decerebrate cats, data were collected for the duration of time that an animal walked regularly (between 1 and 2 h). In intact cats, data were collected for 10–20 trials/day for one to two tasks, rotating through the various tasks over the course of 1–2 wk. Because we were seeking kinematic parameters that were related to the onset of stance in different types of movements, we did not screen trials based on speed or range of movement. We did screen trials qualitatively for smoothness of movement.
During regular sequences of walking in the decerebrate animals, and in intact animals walking under different conditions, the EMG signals were recorded on an eight-channel Vetter 4000A PCM recorder. One channel of the recorder was reserved for a signal from the Peak Motus motion-analysis system for later use in synchronizing the EMGs with video data. During all trials video data were recorded, and a time code and a signal for synchronizing EMG with video were added to the video data. The Peak Motus system was later used to track joint movements and calculate the kinematics of movements at the hip, knee, and ankle joints. The length and velocity of MG was calculated from the knee and ankle angles. The length when both knee and ankle joints were at 90° was taken as 0, and changes from this were calculated using trigonometry assuming that the proximal attachment of MG is located on the femur 0.5 cm from the knee joint and the length of the attachment of MG on the calcanium is 1.5 cm from the ankle joint (Goslow et al. 1973). The velocity of the length changes was calculated by numerically differentiating the calculated length.
After the storage of EMG and video data, the EMGs recorded from decerebrate walking animals were digitized off-line at 1 kHz using the Axotape data-acquisition system (Axon Instruments). The Peak Motus system was used to track the movements of the joints and calculate the kinematics of the hip, knee, and ankle. Custom-written software (Matlab) was used to measure cycle periods, burst durations, the relative timing of the onset of burst activity in different muscles, and the relationship between muscle activity onset and kinematics. Figure 5 shows kinematic data and ankle extensor activity (MG muscle) from a down pegs and a leading trial. The angles measured at the time of onset of MG activity are indicated by the dotted lines.
|
Statistical analysis
A two-tailed F-test, which tests for equality of variance, was used to compare the amount of variance among angles at the time of ankle extensor activation (Woolson and Clarke 2002). Linear regression was used to calculate the correlation coefficients between variables. Student's t-test was used to test for changes in cycle periods and burst durations. ANOVA test was used to compare hip angles in assisted and unassisted conditions.
|
RESULTS |
|---|
|
TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONGRANTSACKNOWLEDGMENTSREFERENCES |
|---|
), and this activity is an early neuro-muscular event underlying the transition from swing to stance. The concept we wished to examine in this investigation was whether sensory feedback via afferents arising in the hip region contributes to the initiation of burst activity in the ankle and knee extensor muscles. Influence of imposed hip flexion during walking in decerebrate cats
A previous study from this laboratory (Lam and Pearson 2001) reported that assisting the flexion movement of the hip during treadmill walking in decerebrate cats shortened the duration of bursts in the hip flexor muscle IP. In that study, the shortening of the duration of hip flexor activity in response to hip flexion was associated with an advanced onset of burst activity in the ankle extensor muscle MG. In the present investigation, our initial goal was to examine the relationship between the time by which MG burst activity was advanced and the time by which IP burst activity was shortened.
Figure 1A shows EMG data for a short period of walking during which flexion of the hip was assisted during one step cycle. These data clearly show that assisting hip flexion reduced the duration of the burst in the IP muscle (a2 compared with a1) and advanced the following burst of activity in the MG muscle, which is consistent with previous observations. To quantify these and similar data, we plotted the reduction in the IP burst duration relative to the duration of the immediately preceding IP burst (a1 – a2 in Fig. 1A) versus the reduction in the interval between the onset of IP bursts and the onset of the following MG burst (b1 –b2 in Fig. 1A). Plots for two animals are shown in Fig. 1, B and C. The reduction in IP duration and the advance in MG burst onset parameters were strongly correlated (r2 = 0.80 and 0.83), and the best fitting lines were close to the line of identity (dotted in Fig. 1, B and C). It is important to note that the time of the onset of the IP bursts of the assisted cycles relative to the time of onset of the preceding IP bursts was not influenced by the imposed hip flexion (Figs. 3A and 4, B and C), thus eliminating the possibility that the hip flexion simply shortened the IP bursts, but did not influence the time of onset of MG activity. The shortening of the IP bursts and advance of the MG bursts did not significantly influence the timing of stepping in the contralateral leg. This can be seen in the example in Fig. 1 and was quantified by comparing the change in cycle period of the contralateral leg with the change in IP burst duration (not shown). Changes in the contralateral cycle period were insignificant (P < 0.05, paired t-test) and not correlated to changes in the IP burst duration (r2 = 0.015 and 0.070 for the 2 animals.) There were also no significant changes in the duration of the contralateral IP burst, indicating the absence of any influence on the timing of the contralateral swing-to-stance transition.
|
|
in the top traces in Fig. 2, B and C, indicate the average effect of assisting hip flexion in two animals. Note also in these figures that the timing of onset of the IP bursts relative to the preceding IP burst was similar during unassisted (top) and assisted (bottom) flexion of the hip.
|
5° (109° with unassisted cycles and 104° with assisted cycles; P = 0.0025, 1-way ANOVA). A noteworthy difference in the stepping behavior of the two animals was that the magnitude and rate of hip flexion was much larger in the first (Fig. 3, D and E). Furthermore, the assisted movements in the second animal noticeably increased the magnitude of hip flexion, and the change in angular velocity produced by the perturbation was larger in the this animal (compare slopes of flexion movements in Fig. 3, D and E). Relationships between leg kinematics and the onset of the ankle extensor activity in normal walking cats
Based on our observations in decerebrate walking cats, as well as results from previous studies (Lam and Pearson 2001, 2002a), we formed the hypothesis that signals related to hip position during swing contribute to initiating the transition from swing to stance. The issue we next explored was whether this is also true in normal walking cats. Initially we attempted to assist hip flexion in cats walking normally on a treadmill to establish whether this perturbation advanced the onset of extensor activity. However, this strategy failed because walking was consistently disrupted in an unpredictable manner thus preventing a clear assessment of the responses to the imposed flexion movements. As an alternative we examined a variety of kinematic parameters of hind leg movement when animals walked in different situations (Figs. 4 and 5 ) and looked for parameters that were most closely correlated with the onset of extensor activity during the swing phase. We predicted that one of these parameters would be the hip angle.
Consistent with this prediction was our finding that the angle at the hip at the time of MG burst onset remained relatively constant in all the tasks in three of the four animals (Fig. 6). In the fourth animal, the hip angle at the onset of MG activity was similar in five of the six tasks. In contrast to the relative constancy of hip angle at the onset of MG activity, the knee and ankle angles at the same instant varied considerably depending on the task. The highest variation was seen for the ankle, which had a range of 50–60°, twice that of the hip. This is apparent in Fig. 5, which shows two example trials for one cat. The hip angle at the time of MG onset is similar for all four steps, whereas the knee and ankle angles vary by 40°. This suggested that the position of the hip was an important signal for the initiation of MG activity. However, it should be emphasized that this does not indicate that the position of the hip was the sole afferent signal related to this initiation. The differences between the angles of the hip at the time of MG onset during different tasks suggests that other signals, in addition to signals from the hip, are probably involved in terminating swing. The pattern of variation in the knee and ankle angles at the time of onset of MG activity for the different tasks was consistent in the four animals. For example, this ankle angle was always smallest when the leg was leading over an object and largest when walking on the treadmill (Fig. 6).
|
300 ms before the onset of extensor activity.
Although our observations on joint angles indirectly support the hypothesis that afferent signals related to hip position play a role in initiating extensor activity, another possibility is that a signal derived from a combination of information from sensory receptors distributed throughout the leg is a critical factor regulating the onset of extensor activity. For example, this signal could provide information about global variables such as the position of the paw relative to the body or to the ground. The former has been termed "limb axis" by Bosco and Poppele (2001). To examine whether these variables could provide a reliable signal for initiating the swing-to-stance transition, we calculated the length and angle of the limb axis at the time of extensor activation (we define limb axis as the angle between the toe, the hip, and a vector from the hip, forward and parallel to the walking surface) as well as the distance and direction of the toe from where it eventually contacted the ground for the different tasks.
Figure 7 compares the variability of the limb axis angle to the variability of the hip, knee, and ankle angles at the time of the onset of MG activity for all tasks. In all four animals, the angle of the limb axis was more variable that the hip angle but less variable than the knee or ankle angles. We also examined the variability of these angles at the time of onset of MG activity within tasks (data not shown). The variability of all angles was lower for any individual task than that for all tasks pooled. Importantly, the difference between variability of the hip angle for individual tasks and for all tasks pooled was generally much less than the difference between the variability of individual and pooled tasks for other angles. This is consistent with our hypothesis that signals related to the hip angle contribute more to regulating the swing-to-stance transition the signals related to the other three angles. Examination of the length of the limb at the time of onset of MG activity revealed a large variability between tasks and major differences in the profiles of the limb axis length for the different tasks (Fig. 8). The limb axis length ranged from 15 to 20 cm at the time of the onset of MG activity, and during steps down pegs, for example, the limb axis length generally started quite short and became longer, but during leading steps over obstacles, the limb axis started long and shortened dramatically through the swing phase. We also examined the position of the toe relative to where it eventually touched the ground at the time of onset of MG activity. Again, there was no consistent pattern in the distance or the angle between the toe and the point where the toe eventually touched ground and the time MG became active. This can be seen in Fig. 6 in which the distance from the toe at the time of MG burst onset to the position of ground contact varied depending on the task.
|
|
300 ms).
|
|
|
|
DISCUSSION |
|---|
|
TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONGRANTSACKNOWLEDGMENTSREFERENCES |
|---|
, 2002a; Saltiel and Rossignol 2004). A priori, sensory feedback related to hip position might be particularly important in regulating swing-to-stance transitions in the hind legs under a variety of conditions for two reasons. First, during the swing phase of walking, the position of the hip is most reflective of the protraction of the leg, whereas the positions of the knee and ankle joints are more reflective of the height of the foot relative to the ground. Second, the movement of the hip during locomotion is biphasic, passing through any one position only once during the swing phase. In contrast, the joints of the knee and ankle both extend and flex during the swing phase and thus may pass through the same position twice during the swing phase. The findings of the present investigation provide additional evidence that afferent signals arising from receptors in the hip region are an important component of the mechanism that regulates the swing-to-stance transition.
Although the position of the hip is a good candidate for an afferent signal regulating swing-to-stance transitions, other signals are also involved. For example, our laboratory has reported inhibitory coupling between, first, the systems that generate flexor activity of the two hindlegs (Lam and Pearson 2001), and secondly, the systems that generate flexor activity of ipsilateral fore and hind legs (McVea et al. 2005). Furthermore, studies of fictive locomotion have shown that a range of afferents, such as group I afferents from ankle and knee extensors as well as group II afferents from hip and knee flexors, have an effect on the duration of flexor activity (McCrea 2001).
Hip flexion influences swing-stance transition in decerebrate walking cats
Our conclusion that hip afferents have a role in regulating the timing of the swing-to-stance transition is strongly supported from our observations in decerebrate walking cats. First, assisting flexion movements of the hip joint shortened the duration of bursts in the IP muscle (hip flexor) and promoted an earlier onset of activity in the MG muscle (ankle extensor) that closely matched the shortening of hip flexor activity (Fig. 1). Because the onset of burst activity in ankle and knee extensors shortly before ground contact is the first neuromuscular event in the swing-to-stance transition, this observation demonstrates directly that signals related to hip position could be involved in initiating this transition. Assuming that the basic network for the timing of activity in the central pattern generator (CPG) is mutual inhibition between flexor and extensor half-centers (Lundberg 1980), the simplest explanation for the changes in timing of the IP and MG bursts is that sensory signals generated during hip flexion act to terminate activity in the flexor half-center and release the extensor half-center from inhibition. Alternatively, changes in timing of the IP and MG bursts could be produced by reflex modification of interneuronal networks located between the CPG and motoneurons or even by direct reflex actions on motoneurons. However, we believe these alternative possibilities are less likely because of the strong correlation between the time of termination of the IP bursts and the time of onset of the MG bursts (Fig. 1, B and C). Moreover, no studies on nonwalking preparations have reported any reflex action from hip muscle afferents on ankle extensor motoneurons. On the other hand, the group Ia afferents from hip extensors are known to form inhibitory connections onto IP motoneurons (Eccles and Lundberg 1958), so it is quite conceivable that increased activity in these afferents partially explains the reduction in the magnitude of the IP bursts we observed when hip flexion was assisted (Fig. 2).
An analysis of the kinematics of the hip joint at the time of extensor activation and flexor burst termination showed the hip angle could be similar in both control and assisted step cycles (Fig. 3). In one animal, the hip angles at the time of the termination of the IP bursts were virtually identical in the two situations (Fig. 3B), whereas in the second animal it was decreased by 5° during assisted trials (Fig. 3C). We have no explanation for this difference, but it may be due to differences in the strength of hip flexion movements in the two animals (compare Fig. 3, D and E). In the first animal, these movements were larger in magnitude and closer to those in normal walking animals. If this animal reflects the situation during normal walking, then the fact that hip angle at the time of the termination of IP activity remained constant suggests that a sensory signal related to hip position is involved in initiating the transition from flexor to extensor activity.
Hip position is part of a multi-modal signal controlling stance
Following our results from decerebrate walking animals, we predicted that the position of the hip could be an important signal controlling the swing-to-stance transition in intact walking cats. By examining the kinematics of leg movements in a variety of situations (Figs. 4 and 5), we found the hip angle at the time of onset of activity in ankle extensor muscles was relatively constant compared with knee and ankle angles (Fig. 6). Although indirect, we interpret this observation as evidence to support the hypothesis. It is important to note that we have not concluded that the position of the hip is the sole signal that triggers a transition from swing to stance. In fact, our data show this to be unlikely for three reasons. First the hip angle at which MG activity begins varies somewhat from task to task. This suggests the strength of the feedback from hip-related afferents is either modulated by descending, task-dependent connections or that other afferent signals are involved. Second, the hip angles at which MG became active varied from cat to cat. Third, cat 4 had a more varied hip position at the time of MG onset than the other cats. These points suggest that, although the position of the hip is an important part of a multi-modal afferent signal that triggers the transition to stance, the relative contribution of hip position to this signal likely varies from cat to cat and from task to task.
Accepting that multi-modal sensory signals are important in regulating the swing-to-stance transition, with signals from the hip being especially important, we need to consider which receptors give rise to these signals. Receptors in the hip joint capsule are unlikely to be involved because inactivation of these receptors has no effect on entrainment of the fictive locomotor rhythm in decerebrate cats (Kriellaars et al. 1994). More likely possibilities are stretch-sensitive receptors in hip extensor muscles and/or muscle spindles and Golgi tendon organs in hip flexor muscles (Lam and Pearson 2002a; Perrault et al. 1995). As for receptors in other regions of the leg, we know that electrical stimulation of group I afferents arising from spindles and Golgi tendon organs in ankle extensor muscles can reset the fictive rhythm to extension (Conway et al. 1987; Guertin et al. 1995) and thus have the potential for regulating the swing-to-stance transition. However, if we assume that gamma drive is similar during the different tasks examined, we can use the length and velocity of the MG muscle as an approximate indication of from group Ia afferent activity at the time of the swing-to-stance transition. The large variation in the length of MG at the time of activation (Fig. 9) and the weak relationship between the interval from the time of maximum MG velocity to MG activation and the maximum MG velocity (Fig. 10), indicate that signals from receptors in the ankle extensors are unlikely to have a significant role in controlling the swing-to-stance transition in intact walking cats.
Another possible signal regulating the timing of the swing-to-stance transition is one derived from a combination of information from sensory receptors distributed throughout the leg to indicate global variables such as the position and angle of the paw relative to the hip (Bosco and Poppele 2001). However, we found that the distance between the toe and the body at the time of ankle extensor activation varied widely depending on the task (Fig. 8) and that the orientation of the toe relative to the body was less consistent than the angle of the hip (Fig. 7). We cannot definitively say that the endpoint of the limb is not a factor in activating extensors in late swing, but if it is, then the computation of the endpoint would necessarily require information about the position of all the joints of the leg. Our data, particularly those from decerebrate animals, show that the position of the hip would be an important component in this computation.
Integration of hip position signals into the CPG
An important question raised by our results is how sensory signals related to the hip position might be integrated into the CPG to influence transitions from flexor to extensor half-centers. This requires an understanding of the functional organization of the CPG. At issue is whether or not the onset of activity in the knee and ankle extensors is linked to an overall switch from flexor to extensor activity in muscles throughout the leg. Lundberg (1980) has argued that it is not. This conclusion was based on the fact that the EMG recordings of Engberg and Lundberg (1969) showed that IP activity lasted well into the E1 phase and overlapped the early activity in ankle extensors. Lundberg concluded that "the E1 burst of activity in extensors has an origin extraneous to that of the half-centers," and proposed that the half-centers switch from flexor to extensor activity at the time of the termination of IP activity, i.e., at a time close to the time of ground contact. However, another interpretation of the same data, and one consistent with observations we have made in this investigation, is that the overall switch from flexor to extensor activity occurs at the time of onset of extensor activity and that the E1-associated activity in IP is generated by the extensor half-center. Evidence supporting this interpretation is that the termination of IP bursts was normally associated with the onset of MG activity at or near the F-E1 transition when animals walked on the treadmill (Fig. 11A) and, in situations in which activity in IP did occur during the E1 phase, that this activity was often distinctly segregated from the preceding flexion associated activity (Fig. 11, B and C). If the extensor-associated activity in IP is produced via an excitatory pathway linking the extensor half-center to the IP motoneurons, then we must assume that transmission in this pathway is task-dependent to allow for the variable occurrence of IP activity during E1 phase (Fig. 11). This scheme accounts for the strong linkage between the termination of IP bursts on the onset of MG bursts that occurs in decerebrate walking animals (Fig. 3) as a complete closing of the pathway from the extensor half-center to IP motoneurons due to loss of supraspinal facilitation of the pathway. If this scheme is accepted, then we propose that signals generated by flexion of the hip during swing inhibit the interneuronal networks generating the F phase of flexion (flexor half-center) and help promote the switching from the flexor to extensor half-center. This transition is associated with the onset of activity of knee and ankle extensors, and extensor related IP activity may or may not continue depending on the state of the putative connection from the extensor half-center to the IP motoneurons described in the preceding text.
Summary
In this study, we have shown that the position of the hip is an important part of the signal that initiates the swing-to-stance transition in the hindlegs of the walking cat. This expands our understanding of the role of sensory feedback in regulating phase transitions during walking and complements our knowledge of the role of hip position in regulating the stance-to-swing transition (Grillner and Rossignol 1978; Hiebert et al. 1996). In this role, the position of the hip is one part of a multi-modal signal that initiates swing (Pearson 2003), and we suggest that the hip has a similar role as part of a distributed signal initiating stance.
|
GRANTS |
|---|
|
TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONGRANTSACKNOWLEDGMENTSREFERENCES |
|---|
|
ACKNOWLEDGMENTS |
|---|
|
TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONGRANTSACKNOWLEDGMENTSREFERENCES |
|---|
Present addresses: J. M. Donelan, School of Kinesiology, Simon Fraser University, Canada; A. Tachibana, Dept. of Physiology and Neuroscience, Kanagawa Dental College, Kanagawa, Japan.
|
FOOTNOTES |
|---|
Address for reprint requests and other correspondence: D. A. McVea, Dept. of Physiology, University of Alberta, Edmonton T6G 2H7, Canada (E-mail: dmcvea{at}ualberta.ca)
|
REFERENCES |
|---|
|
TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONGRANTSACKNOWLEDGMENTSREFERENCES |
|---|
Bässler U and Büschges A. Pattern generation for stick insect movements—multisensory control of a locomotor program. Brain Res Rev 27: 65–88, 1998.[CrossRef][Medline]
Bosco G and Poppele RE. Proprioception form a spinocerebellar perspective. Physiol Rev 81: 539–568, 2001.
Conway BA, Hultborn H, and Kiehn O. Proprioceptive input resets central locomotor rhythm in the spinal cat. Exp Brain Res 68: 643–656, 1987.
Dietz V and Duysens J. Significance of load receptor input during locomotion: a review. Gait Posture 11: 102–110, 2000.[CrossRef][ISI][Medline]
Duysens J, Clarac F, and Cruse H. Load-regulating mechanisms in gait and posture: comparative aspects. Physiol Rev 80: 83–133, 2000.
Eccles RM and Lundberg A. Integrative patterns of Ia synaptic action on motoneurones of hip and knee muscles. J Physiol 144: 271–298, 1958.
Engberg I and Lundberg A. An electromyographic analysis of muscular activity in the hindlimb of the cat during unrestrained locomotion. Acta Physiol Scand 75: 614–630, 1969.[ISI][Medline]
Goslow GE, Reinking RM, and Stuart DG. The cat step cycle: hind limb joint angles and muscle lengths during unrestrained locomotion. J Morphol 141: 1–42, 1973.[CrossRef][ISI][Medline]
Guertin P, Angel MJ, Perreault MC, and McCrea DA. Ankle extensor group I afferents excite extensors throughout the hindlimb during fictive locomotion in the cat. J Physiol 487: 197–209, 1995.[ISI][Medline]
Grillner S and Rossignol S. On the initiation of the swing phase of locomotion in chronic spinal cats. Brain Res 146: 269–277, 1978.[CrossRef][ISI][Medline]
Grillner S and Shik ML. On the descending control of the lumbosacral spinal cord from the "mesencephalic locomotor region." Acta Physiol Scand 87: 320–333, 1973.[ISI][Medline]
Hiebert GW, Whelan PJ, Prochazka A, and Pearson KG. Contributions of hindlimb flexor muscle afferents to the timing of phase transitions in the cat step cycle. J Neurophysiol 75: 1126–1137, 1996.
Kriellaars DJ, Brownstone RM, Noga BR, and Jordan LM. Mechanical entrainment of fictive locomotion in the decerebrate cat. J Neurophysiol 71: 2074–2086, 1994.
Lam T and Pearson KG. Proprioceptive modulation of hip flexor activity during the swing phase of locomotion in decerebrate cats. J Neurophysiol 86: 1321–1332, 2001.
Lam T and Pearson KG. Sartorius muscle afferents influence the amplitude and timing of flexor activity in walking decerebrate cats. Exp Brain Res 147: 175–185, 2002a.[CrossRef][ISI][Medline]
Lam T and Pearson KG. The role of proprioceptive feedback in the regulation and adaptation of locomotor activity. In: Sensorimotor Control of Movement and Posture, edited by Gandevia SC, Proske U, and Stuart DG. New York, Kluwer Academic, 2002b, p. 343–356.
Lundberg A. Half-centres revisited. In: Regulatory Functions of the CNS. Motion and Organization Principles, edited by Szentagothai J, Palkovits M, and Hamori J. London: Pergamon, 1980, p. 155–167.
McCrea DA. Spinal circuitry of sensorimotor control of locomotion. J Physiol 533: 41–50, 2001.
McVea DA, Akay T, Tachibana A, Pearson KG. Asymmetry in the neuronal mechanisms coordinating stepping in the fore and hind legs of walking cats. Soc Neurol Abstr In press.
Pang MYC and Yang JF. Sensory control of the initiation of the swing phase in infant stepping: importance of hip position and loading. Soc Neurosci Abstr 26: 461, 2000.
Pearson KG. Proprioceptive regulation of locomotion. Curr Opin Neurobiol 5: 786–791, 1995.[CrossRef][ISI][Medline]
Pearson KG. Neural adaptation in the generation of rhythmic behavior. Annu Rev Physiol 62: 723–753, 2000.[CrossRef][ISI][Medline]
Pearson KG. Generating the walking gait: role of sensory feedback. Prog Brain Res 143: 123–129, 2003.
Pearson KG, Donelan JM, and McVea D. Initiation of stance phase activity in walking cats: a possible role for hip afferents. Soc Neurosci Abstr 33: 276.14, 2003.
Pearson KG and Duysens JD. Function of segmental reflexes in control of stepping in cockroaches and cats. In: Neural Control of Locomotion, edited by Herman RM, Grillner S, Stein PSG, and Stuart DG. New York: Plenum, 1976, p. 519–538.
Pearson KG, Misiaszek JE, and Fouad K. Enhancement and resetting of locomotor activity by muscle afferents. Ann NY Acad Sci 860: 203–215, 1998.
Perreault M-C, Angel MJ, Guertin P, and McCrea DA. Effects of stimulation of hindlimb flexor group II afferents during fictive locomotion. J Physiol 487: 211–220, 1995.[ISI][Medline]
Prochazka A. Proprioceptive feedback and movement regulation. In: Handbook of Physiology. Regulation and Integration of Multiple Systems. New York: Am. Physiol. Soc., 1996, sect. 12, p. 89–127.
Rossignol S, Lund JP, and Drew T. The role of sensory inputs in regulating patters of rhythmical movements in higher vertebrates. In: Neural Control of Rhythmic Movements in Vertebrates, edited by Cohen A, Rossignol S, and Grillner S. New York: Wiley, 1988, p. 201–283.
Saltiel P and Rossignol S. Critical points in the forelimb fictive locomotor cycle and motor coordination: effects of phasic retractions and protractions of the shoulder in the cat. J Neurophysiol 92: 1342–1356, 2004.
Shik ML, Severin FV, and Orlovsky GN. Control of walking and running by means of electrical stimulation of the mid-brain. Biophysics 11: 756–765, 1966.
Whelan PJ, Hiebert GW, and Pearson KG. Stimulation of the group I extensor afferents prolongs the stance phase in walking cats. Exp Brain Res 103: 20–30, 1995.[ISI][Medline]
Woolson RF and Clarke WR. Statistical Methods for the Analysis of Biomedical Data (2nd ed.). New York: Wiley, 2002.
This article has been cited by other articles:
|
|
 |
|
  C. Heng and R. D. de Leon The Rodent Lumbar Spinal Cord Learns to Correct Errors in Hindlimb Coordination Caused by Viscous Force Perturbations during Stepping J. Neurosci., August 8, 2007; 27(32): 8558 - 8562. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 L. Guevremont, J. A. Norton, and V. K. Mushahwar Physiologically Based Controller for Generating Overground Locomotion Using Functional Electrical Stimulation J Neurophysiol, March 1, 2007; 97(3): 2499 - 2510. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
K. E. Musselman and J. F. Yang Loading the Limb During Rhythmic Leg Movements Lengthens the Duration of Both Flexion and Extension in Human Infants J Neurophysiol, February 1, 2007; 97(2): 1247 - 1257. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
D. A. McVea and K. G. Pearson Long-Lasting, Context-Dependent Modification of Stepping in the Cat After Repeated Stumbling-Corrective Responses J Neurophysiol, January 1, 2007; 97(1): 659 - 669. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 |
, maximum lengthening velocity in MG during the 1st half of the swing phase, and the 
shows intervals from maximum velocity to MG activation. B: relationships between maximum lengthening velocity in MG and interval from maximum velocity to MG activation for the 4 experimental animals. Data from all 6 tasks are combined in each plot. Results of linear regression are also shown. Note the maximum intervals are large, and the relationship between the 2 parameters is weak.
) overlapped MG activity when the animal stepped over the object and when it walked on the pegs. These bursts began close to the time of the onset of MG activity (- - -).