EMG Responses to Maintain Stance During Multidirectional Surface Translations

Sharon M. Henry, Joyce Fung, and Fay B. Horak

R. S. Dow Neurological Sciences Institute, Portland, Oregon 97209

    ABSTRACT
Abstract
Introduction
Methods
Results
Discussion
References

Henry, Sharon M., Joyce Fung, and Fay B. Horak. EMG responses to maintain stance during multidirectional surface translations. J. Neurophysiol. 80: 1939-1950, 1998. To characterize muscle synergy organization underlying multidirectional control of stance posture, electromyographic activity was recorded from 11 lower limb and trunk muscles of 7 healthy subjects while they were subjected to horizontal surface translations in 12 different, randomly presented directions. The latency and amplitude of muscle responses were quantified for each perturbation direction. Tuning curves for each muscle were examined to relate the amplitude of the muscle response to the direction of surface translation. The latencies of responses for the shank and thigh muscles were constant, regardless of perturbation direction. In contrast, the latencies for another thigh [tensor fascia latae (TFL)] and two trunk muscles [rectus abdominis (RAB) and erector spinae (ESP)] were either early or late, depending on the perturbation direction. These three muscles with direction-specific latencies may play different roles in postural control as prime movers or as stabilizers for different translation directions, depending on the timing of recruitment. Most muscle tuning curves were within one quadrant, having one direction of maximal activity, generally in response to diagonal surface translations. Two trunk muscles (RAB and ESP) and two lower limb muscles (semimembranosus and peroneus longus) had bipolar tuning curves, with two different directions of maximal activity, suggesting that these muscle can play different roles as part of different synergies, depending on translation direction. Muscle tuning curves tended to group into one of three regions in response to 12 different directions of perturbations. Two muscles [rectus femoris (RFM) and TFL] were maximally active in response to lateral surface translations. The remaining muscles clustered into one of two diagonal regions. The diagonal regions corresponded to the two primary directions of active horizontal force vector responses. Two muscles (RFM and adductor longus) were maximally active orthogonal to their predicted direction of maximal activity based on anatomic orientation. Some of the muscles in each of the synergic regions were not anatomic synergists, suggesting a complex central organization for recruitment of muscles. The results suggest that neither a simple reflex mechanism nor a fixed muscle synergy organization is adequate to explain the muscle activation patterns observed in this postural control task. Our results are consistent with a centrally mediated pattern of muscle latencies combined with peripheral influence on muscle magnitude. We suggest that a flexible continuum of muscle synergies that are modifiable in a task-dependent manner be used for equilibrium control in stance.

    INTRODUCTION
Abstract
Introduction
Methods
Results
Discussion
References

The purpose of this study was to characterize the muscle synergy organization used for stance equilibrium control in response to multidirectional surface translations. Muscle synergy is defined as a group of muscles that are constrained to act in a concerted manner (Macpherson 1991; Sherrington 1961). We were interested in determining how muscle synergies are organized, what aspects of the muscle synergies are fixed, and what aspects are mutable. We hypothesized that muscle synergies are utilized to maintain postural equilibrium in response to surface translations, but there is not a unique muscle synergy for each translation direction.

Most of what is known about synergy organization for postural control is based on surface translations in the anterior/posterior (A/P) direction. Automatic postural responses to surface translations are triggered by somatosensory information (Horak and Macpherson 1996; Inglis et al. 1994), and they are scaled to the velocity and amplitude of the platform translation (Diener et al. 1988). In response to slow anterior surface translations, the tibialis anterior (TIB), quadriceps, and abdominal muscles are recruited, and in response to posterior translations the gastrocnemius, the hamstrings, and then paraspinal muscles are recruited in order (Horak and Nashner 1986). This distal-to-proximal muscle activation pattern is accompanied by corrective torques primarily exerted about the ankle. With larger or faster perturbations, active hip torque and early recruitment of proximal trunk muscles are used to restore balance, suggesting a continuum of available strategies for equilibrium control in the A/P direction (Horak and Nashner 1986; Kuo and Zajac 1993; Runge et al. 1998). More recent studies examining postural responses to lateral surface translations (Henry et al. 1998) suggested a unified mechanism for equilibrium control whereby the trunk is used for lateral as well as for A/P control.

Automatic postural responses to surface translations are not reflexively driven by simple feedback control mechanisms (Horak and Nashner 1986; Macpherson et al. 1986); that is, the muscle that is stretched during the translation is not necessarily activated first, but rather the muscle that is functionally relevant to the appropriate corrective response is activated first (Nashner 1976). In fact, mechanical displacement of a distal segment such as the hand or thumb can result in rapid postural reactions throughout the body (Marsden et al. 1983). Postural muscle responses to surface translations are not hard-wired, fixed synergies, but can be altered by prior experience (Horak 1995), intent (Burleigh et al. 1994; Horak et al. 1989), initial alignment (Horak and Moore 1993), and surface configurations (Horak and Nashner 1986). Similarly, authors have shown that muscle synergies in response to multidirectional arm perturbations are not governed by negative feedback control mechanisms (Lacquaniti and Soechting 1986) or organized in a fixed manner. Subjects exerting isometric torque at the elbow and shoulder joint activated complex muscle patterns suggested that muscle synergies are task dependent and may have no independent existence (Buchanan et al. 1986). Additionally, in a multidirectional arm reaching task, the spatiotemporal pattern for the shoulder muscles were fundamentally different for different directions, indicating a nonuniform pattern of central motor commands to different muscles at the same joint (Flanders et al. 1994). The maximal direction of activation of an arm muscle was not always predicted by the anatomic orientation of the muscle (Buchanan et al. 1986), suggesting that muscle stretch or optimal pulling direction alone cannot predict the recruitment of these muscles.

The nature of the variability in the postural muscle synergy groupings has become more apparent with multidirectional perturbation studies (Lacquaniti and Soechting 1986; Macpherson 1988). In response to only A/P surface translations, the postural muscle synergies in cats and humans are often limited to anatomic synergists, but anatomic groupings are often not sufficient in response to multidirectional surface translations (Henry et al. 1995; Macpherson 1988). Postural responses in standing cats (Macpherson 1988) have shown that the amplitude of muscle activation varied systematically with perturbation direction and that some muscle activation patterns included muscles that were not anatomic synergists. Furthermore, some muscle were recruited in response to directions that were not predictable based on the line of action of the muscle, again suggesting a complex central organization. Moore et al. (1988) examined the electromyographic (EMG) responses to surface translations in healthy humans by having subjects change their foot placement by 15° each time in preparation for a new perturbation direction. They reported a systematic modulation of EMG amplitude with perturbation direction and no significant differences in latency in the distal muscles with perturbation direction. However, these authors reported a continuous modulation of latencies in the proximal muscles with perturbation direction. Because prediction (Burleigh et al. 1994; Timmann and Horak 1997) and prior experience (Horak 1995) are known to affect postural responses, the current study was designed with a platform that moved in any direction in the horizontal plane; thus subjects did not need to change their stance position, allowing random, unexpected presentation of each of 12 perturbation directions. In addition to collecting EMG responses, we were able to examine force responses under each foot as well as the kinematic patterns (Fung et al. 1995; Henry et al. 1998).

    METHODS
Abstract
Introduction
Methods
Results
Discussion
References

Seven healthy subjects (4 female; 3 males; ages 21-41 yr) stood on a movable platform surface that was under the control of a hydraulic servomotor. Subjects were instructed to stand in a comfortable position with arms crossed, head facing forward, and with equal weight on each foot placed on separate force plates. At the beginning of the experiment, subjects were asked to lean forward/backward and laterally as far as possible without stepping or losing their balance, and the total A/P and lateral center of pressure (CoP) was noted. Before each trial, subjects were instructed to assume the same initial A/P and lateral weight distribution, as monitored by the experimenter. A sigmoidal signal was used to translate the platform 9 cm in 200 ms at a peak velocity of 35 cm/s (peak acceleration of 13.5 cm/s2). Subjects received 5 trials, of 3-s duration, presented randomly in each of 12 different perturbation directions, specified in polar coordinates (Fig. 1). A surface translation at 0° was a rightward surface translation, and the angle increased in 30° increments such that 90° was an anterior translation, 180° was a leftward translation, and 270° was a posterior translation. The subjects' heels were placed 10 cm apart with 10° of toe out to achieve a comfortable natural stance posture with a relatively small base of support. The same experiment was repeated on five subjects who returned for a second day of testing. Because there were no differences in the muscle latencies (0.102 < P < 0.945) between testing days, data were combined for a total of 10 trials in each of the perturbation directions for each subject.


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FIG. 1. Subjects were translated in 1 of 12 directions randomly in the horizontal plane. The translation directions were separated by 30° such that a 0° translation was a rightward translation, 90° an anterior translation, 180° a leftward translation, and 270° a posterior translation. The integrated electromyographic (EMG) response of the left tensor fascia muscle is the average of 5 trials and reflects the modulation of muscle activation with translation direction. The 1st integrals (70-270 ms after translation onset at time 0), indicated in black, are used to normalize the muscle activity across translation direction and to create tuning curves or polar plots (see Fig. 2). The latencies of the muscle burst, indicated by the arrows, do change with translation direction for this proximal muscle.

For the EMG recordings of leg and trunk muscles, bipolar, silver-silver chloride electrodes were placed over the following 11 left-sided muscles: TIB, peroneus longus (PER), medial gastrocnemius (MGS), soleus (SOL), vastus medialis (VSM), rectus femoris (RFM), adductor longus (ADL), semimembranosus (SEM), tensor fascia latae (TFL), rectus abdominis (RAB), and erector spinae (ESP). The MGS was chosen rather than the lateral gastrocnemius muscle to avoid potential cross talk between the lateral gastrocnemius and the PER and SOL muscles, which were recorded on the lateral aspect of the lower leg. A ground electrode was placed over the left medial tibial plateau. The EMG signals were amplified (5,000-10,000×), band-pass filtered (75-2,000 Hz), full-wave rectified, integrated at a cutoff frequency of 200 Hz, and then sampled at 480 Hz.

The latency of each muscle burst was identified manually as the first burst that was >2 SDs above baseline with an interactive software program (Axograph, Axon Instruments, Foster City, CA). The mean baseline was calculated between 50 and 150 ms before platform onset. The first point above the mean + 2 SDs was noted. From this point, the EMG burst was followed back to the mean baseline, and the latency of this point was recorded as the onset of the muscle burst. A muscle had to be active in >= 6 out 10 trials (or 3/5 trials for the 2 subjects who had only 1 day of testing) to be considered physiologically significant in contributing to the postural response. To examine EMG latency differences across translation direction for each muscle, latencies for translation directions in which the muscle was activated >= 60% were used in a two-way analysis of variance (muscle latency × 12 translation directions) with the P value set at 0.05. If there were significant interactions, post hoc tests (Turkey's) were done to determine in which translation directions the muscle latencies were significantly different.


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FIG. 2. There is continuous modulation of EMG amplitude across translation directions, resulting in 2 main types of EMG spatial patterns. A: the top polar plot typifies a monopolar pattern, which has 1 direction of maximal activity and generally fills approximately 1 quadrant. B: the middle polar plot is an example of a muscle that is maximally active in a direction orthogonal to its anatomic orientation. C: the bottom polar plot reflects the 2nd main group of spatial patterns, the bipolar pattern, which has 2 directions of maximal activity, filling 2 quadrants. The EMG recordings are taken from left-sided muscles, and each polar plot is derived from the accompanying EMG traces, all 3 of which were recorded from the same subject. Time 0 indicates translation onset, and the integral between 70- to 270-ms posttranslation onset is shaded. A vertical line at 200 ms was added to aid in the comparison of burst onset across translation directions. TIB, tibialis anterior; ADL, adductor longus; ESP, erector spinae.

The mean amplitude of each muscle response was determined by integrating the area under the EMG response during a fixed 200-ms epoch from 70-270 ms after platform onset. The mean background level of EMG activity for the 100 ms before platform movement was subtracted. For each subject, the integrals from each muscle were averaged for each set of five trials in each of the 12 directions. For each muscle, the means were normalized to the maximum response of the 12 directions. The normalized data were then plotted against the direction of translation as muscle tuning curves in polar coordinates to compare EMG modulation across directions and across muscles. For each muscle, the number of subjects responding in each of the 12 translation directions was then used in a Kolmogorov-Smirnov procedure to test for uniform distribution in the 12 translation directions. This was done separately for each muscle to account for interindividual variabilities. The exact P value was obtained with StatXact (StatXact 3 for Windows by Cytel Software Corporation, Cambridge MA 02139).

The CoP in the horizontal plane was derived from the square root of the summed squares of the A/P and lateral CoP displacements from averaged trials for each subject in each translation direction. The CoP latency was chosen manually at the point where there was a significant change in the slope of the trace. The grand average latency of CoP across all subjects for all twelve translations directions was then calculated.

The above experimental protocol was approved by the Legacy Good Samaritan Hospital & Medical Center Institutional Review Board and all subjects signed a consent form.

    RESULTS
Abstract
Introduction
Methods
Results
Discussion
References

Amplitude of muscle activation

The amplitude of the EMG response was continuously modulated with perturbation direction resulting in either monopolar or bipolar EMG spatial patterns with their angular range of activation in either one or two quadrants, respectively (Fig. 2). Seven of the 11 muscles had monopolar spatial patterns with one maximum direction of activation. Five monopolar muscles (TIB, SOL, MGS, VSM, and TFL), exemplified by TIB in Fig. 2, had maximal activity consistent with anatomic pulling directions. The direction of maximal activity for all muscles was generally in response to diagonal translations, except for the TFL, which was maximally active in response to lateral translations. Two monopolar thigh muscles (ADL and RFM), exemplified by ADL in Fig. 2, were maximally active orthogonal to their direction of greatest lengthening (Smith et al. 1983). Although the ADL muscle functions as a hip adductor spanning the inner thigh, the ADL muscle was maximally active with anterior, and not lateral, translations. Similarly, the RFM muscle functions as a hip flexor and knee extensor with its orientation in the sagittal plane, but this muscle was maximally active with lateral translations. The bipolar group, consisting of four trunk and lower extremity muscles (ESP, RAB, SEM, and PER), responded maximally in two different translation directions separated by 150-180°, exemplified by ESP in Fig. 2.

The spatial patterns for each muscle were remarkably consistent across subjects except for the trunk muscles, which were more variable in shape. The polar plots shown in Fig. 3 are each from a representative subject (a different subject than that shown in Fig. 2), and each asterisk represents the direction of maximal activity for each subject. For example, the SOL muscle had a maximal response to the 300° diagonal translation in four subjects and a maximal response to the 330° diagonal translation in three subjects.


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FIG. 3. The 11 muscles recorded fall into 2 EMG spatial patterns. A representative polar plot for each muscle is shown, with each asterisk representing one subject's direction of maximal activity. Each polar plot, derived from the left-sided EMG recordings, is taken from a different subject. The muscles with monopolar spatial patterns include vastus medialis (VSM), tensor fascia latae (TFL), TIB, soleus (SOL), and medial gastrocnemius (MGS). Two other muscles, ADL and rectus femoris (RFM), with monopolar spatial patterns are maximally active orthogonal to their anatomic orientation. The muscles with bipolar spatial patterns include the rectus abdominis (RAB), ESP, semimembranosus (SEM), and peroneus longus (PER) muscles. For simplicity, 1 direction of maximal activity is shown for the bipolar muscle group.

There was more variability among subjects' direction of maximal trunk muscle response compared with the shank and thigh muscles (Fig. 3). This intersubject variability may be related to different strategies for involving the trunk; some people recruit the trunk muscles early as prime movers, and others may recruit them later as stabilizers or antagonists (Horak and Nashner 1986). For the RAB, three subjects responded maximally to anterior translations (90 or 120°), two subjects responded maximally to posterior translations (270-300°), and two subjects responded maximally to lateral translations (0°). For left ESP, six subjects responded maximally to anterior/rightward or posterior/leftward translations (0, 60, and 240°), and one subject responded maximally to a posterior/rightward translation (330°).

Generally, most muscles were maximally active in response to diagonal translations and not to A/P or lateral translations. In fact, for the shank and some thigh muscles, the response to A/P translations was only 50-70% of the response to diagonal translations. The left SOL and MGS muscles and one pole of the RAB, SEM, and PER muscles had similar response patterns for posterior/rightward translations resulting in forward/leftward sway, suggesting a synergistic action for these muscles (Fig. 4). Similarly, in response to anterior/rightward translations resulting in backward/leftward sway, the left TIB, VSM, and ADL muscles, in addition to one pole of the PER and ESP muscles, were activated with a similar spatial pattern (Fig. 4). The only nondiagonal muscles, the left RFM and TFL, were active synergistically in response to primarily rightward translation resulting in leftward sway. Assuming symmetry, the anterior pole of the left SEM and RAB muscles would be synergistic with their corresponding diagonal cluster of the right-sided muscles. The diagonal clusters correspond to the horizontal force vectors exerted under each foot by subjects in response to these surface translations (Fung et al. 1995).


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FIG. 4. Muscle-tuning curves cluster into 1 of 3 regions. The 1st cluster consists of SOL and MGS muscles as well as the "posterior lobe" of the bipolar tuning curves of the RAB, SEM, and PER muscles. The 2nd cluster consists of muscle-tuning curves from TIB, VSM, and ADL muscles as well as the "anterior lobe" of the bipolar tuning curves of the PER and ESP muscles. The 3rd cluster consists of the RFM and TFL muscles.

The two different directions of maximal activation of RAB and ESP were related to a change in their latency of muscle activation, that is, the muscle was activated early with one direction of translation but later with the opposite direction of translation. Although the TFL muscle had a monopolar spatial pattern, this muscle also had discrete changes in the latency of recruitment relative to the direction of translation.

Timing of muscle recruitment

The latencies of the ESP, RAB, and TFL muscles were recruited early or late, depending on translation direction (Fig. 5A). For each of these three muscles, there was a significant effect of direction (P < 0.01) on muscle latency, revealing that the directions in which the RAB and ESP muscles were recruited late were 60-180 degrees apart from the direction in which these muscles were recruited early. For the TFL muscle, the degree of translation direction between early and late latencies ranged from 30-120°. In contrast, the latencies of all shank and thigh muscles did not change significantly with translation direction (P > 0.05, Fig. 5B).


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FIG. 5. Latency of muscle activation changes with translation direction for 3 more proximal muscles (ESP, RAB, and TFL) but not for the thigh and shank muscles. A: scatter plots represent the individual mean muscle latencies for each subject, and the asterisk represents the group mean for directions in which the muscle was recruited >60% of the trials (indicated by heavy bar along the x-axis, perturbation direction). For some translation directions, 2 asterisks are shown, reflecting the mean of a subgroup of subjects. Below each scatter plot is 1 subject's EMG trace for the left ESP, RAB, and TFL muscles (average of 5 trials) for 2 different translation directions as well as the corresponding center of pressure traces (average of 5 trials). The arrows indicate the onset of the muscle burst, and time 0 is the translation onset. B: latency of the thigh and shank muscle activation, when they are recruited, does not change with translation direction. If the latency is not indicated, the muscle was not active in >60% of the trials for that translation direction.

The left ESP was recruited 75 ms earlier on average for rightward/anterior translations (0-60°) compared with leftward/posterior translations (180-270°, Figs. 5 and 2C). For anterior translations (90°), the ESP muscle was activated early in four subjects at 124 ± 34 ms or later in two subjects at 160 ± 41 ms, suggesting that this direction of translation was a transition direction. One subject did not recruit the ESP at all for anterior translations. Similarly, the 330° translation direction also appeared to be a transition direction in which four subjects recruited ESP early at 128 ± 42 ms and three subjects recruited it late at 184 ± 41 ms.

The latency of the RAB muscle activation was more variable among subjects such that the left RAB muscle was recruited early (107 ± 19 ms) in three subjects, late (170 ± 32 ms) in two subjects, and not at all in the remaining two subjects in response to leftward/posterior translations (300°, Fig. 5). Similarly, the muscle was recruited early (102 ± 16 ms for 4 subjects) or late (175 ± 28 ms for 3 subjects) in response to a posterior translations (270°). In contrast, the RAB was consistently recruited late (208 ± 55 ms) for anterior translations (60-150°) and in <60% of the trials for rightward translations (330, 0, and 30°).

Like ESP and RAB, the TFL muscle was recruited 60 ms earlier on average for lateral translations (300-60°) compared with 120 and 270° translation directions. In response to anterior translations (90°), two subjects responded early (118 ± 18 ms), and five people responded late (159 ± 26 ms, Fig. 5). The TFL muscle was recruited in <60% of the trials for translation directions 150-240, to which the muscle was recruited late, if it was recruited at all. So, these three muscles (ESP, RAB, and TFL) were recruited either early or late, and the latency of activation did not continuously vary with translation direction.

The latency of the muscle burst for the ESP, RAB, and TFL muscles can be compared with the onset in change of CoP for directions in which these muscles were recruited early and late (Fig. 5A). The CoP latencies were similar for all directions in all subjects and ranged from 140 to 160 ms. For directions in which the muscles were recruited early, the CoP change was coincident with or after the muscle burst, suggesting that these muscles may contribute to the force generation at the feet needed to change the CoP.

In contrast to the ESP, RAB, and TFL muscles, each of the shank and thigh muscles was recruited at a similar latency, regardless of the translation direction (P > 0.05 for all muscles, Fig. 5B). Although the PER and SEM muscles showed a bipolar spatial pattern, these two muscles were recruited at the same latency for all directions, despite the large changes in magnitude.

Muscle sequencing

Generally, one of the three more proximal muscles (TFL, RAB, and ESP) was recruited before, or at least as early as, a distal-to-proximal muscle activation pattern of the shank and thigh muscles (Fig. 6). The TFL muscle was activated for lateral, the RAB for posterior, and the ESP for anterior translations. In response to diagonal translations, the TFL muscle was activated early with the RAB or ESP muscles for posterior- or anterior-lateral translations, respectively.


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FIG. 6. Sequencing of muscle activation in response to 2 different quadrants of translation (0-90 or 180-270°) is shown. The direction of translation is indicated by the arrow. On the basis of the muscle firing probability of >= 60%, the average latency and SE of muscle recruitment across 7 subjects is shown. Muscles that had a firing probability of <60% are indicated with an asterisk at their respective average latency. The 1st column of the figure shows the quadrant in which the platform moves rightward/anteriorly, resulting in leftward/backward body sway and loading of the left leg; the 2nd column shows the quadrant in which the platform moves leftward/posteriorly, resulting in rightward/forward body sway and unloading of the left leg. For directions 0 and 90°, there is early activation of either TFL or ESP, respectively, whereas for the intervening directions (30 and 60°), there is early activation of both the TFL and ESP muscles. In addition, there is a concomitant distal-to-proximal activation of other muscles. Similarly, for directions 180-270°, there is a concomitant distal-to-proximal muscle activation pattern, indicating an active unloading response. There is also early active of the RAB muscle in response to the posterior translation (270°) for some subjects, and the RAB is active early with the TFL muscle in the 300° translation (data not shown for that quadrant, but refer to Fig. 5).

In response to a lateral rightward translation (0°) resulting in loading of the left leg, the TFL muscle was activated first, followed by a co-contraction of the ipsilateral ankle muscles (Fig. 6). This was followed by activation of the other thigh and trunk muscles (RFM, ESP, VSM, and SEM). The ADL and RAB were not active in >= 60% of the trials for this translation direction, but the average latency of response trials is indicated by asterisks. Note that the TFL was recruited before the average latency of CoP change, suggesting its role as a prime mover, whereas the other muscles were recruited after the onset of CoP change.

A distinct unloading response to lateral translations was observed in the muscles of the unloaded leg such that the muscles were recruited in a distal-to-proximal sequence. In the unloaded leg (left leg in response to a leftward translation, 180°), the distal-to-proximal muscle activation sequence started with the TIB, followed by the SEM and ADL, and then the ipsilateral ESP muscle.

Generally, in response to A/P translations, there was a distal-to-proximal muscle activation pattern concomitant with relatively early activation of trunk muscles on the opposite side of the body. However, not all subjects recruited either the ESP or RAB muscle early in response to this velocity of A/P translations (the number of subjects with early vs. late latencies is indicated in Fig. 6). The muscle activation pattern for backward sway to anterior surface translations (90°) was TIB, followed by ESP, VSM, SEM, and then the RAB muscle. In addition, the TFL muscle was coactivated with the ADL muscle when the TFL was recruited early (2 subjects). The other muscles, including PER, were not active in >= 60% of the trials (asterisks in Fig. 6).

The muscle activation pattern for forward sway to posterior translations was the RAB muscle (4 subjects who recruited this muscle early), followed by ankle and thigh muscles (SOL, MGS, PER, TFL, and SEM), and then the ESP muscle. Even if the RAB muscle was recruited late (3 subjects), it was still recruited before the ESP muscle. The other muscles were not active in >= 60% of the trials (asterisks in Fig. 6).

The muscle responses to rightward and leftward diagonal translations were combinations of muscle responses to the orthogonal directions. For rightward/anterior translations (30 and 60°), the TFL muscle was activated early with the ESP muscle, concomitant with a distal-to-proximal muscle activation pattern (Fig. 6). For rightward/posterior translations (300°), the TFL and RAB (2 subjects) were recruited early for the 300° direction, concomitant with a distal-to-proximal muscle activation pattern. For 330° translation the TFL muscle was also activated early, but the RAB muscle was recruited in <60% of the trials (data not shown in Fig. 6, refer to Table 1). The muscle responses to leftward/posterior diagonal translations included a distal-to-proximal activation of TIB, SEM, ADL, and ESP muscles (Fig. 6). The muscle responses to leftward/anterior diagonal translations included a similar distal-to-proximal muscle activation pattern, with the addition of the VSM and TFL muscles for the 120° direction and the RAB muscle for both the 120 and 150° translations (data not shown in Fig. 6, refer to Table 1).

 
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TABLE 1. Muscle latencies for seven subjects

    DISCUSSION
Abstract
Introduction
Methods
Results
Discussion
References

This study characterized the coordination of muscle recruitment in response to destabilizing surface translations and to examine the nature of the variability in the muscle groupings in response to these perturbations. It was suggested that muscles may be activated together as a unit by the CNS as a means of simplifying the control of multiple degrees of freedom (Bernstein 1967; Macpherson 1991). It would not be computationally cost-effective or efficient to have each muscle independently controlled by the CNS. Thus the term synergy was introduced to describe the concerted action of a group of muscles (Macpherson 1991; Sherrington 1961). The results of this study are consistent with our hypothesis that muscles are recruited synergistically in response to external perturbations, but the muscle synergies can be altered in a flexible, task-dependent manner to accommodate for changes in biomechanical constraints of the musculoskeletal system or the task.

Synergies used in postural control

Previous studies in arm and neck muscle recruitment have not supported fixed synergy organization to decrease the degrees of freedom (Buchanan et al. 1986; Keshner 1994; Lacquaniti and Soechting 1986). Perhaps the CNS is controlling more global variables than muscle recruitment pattern to achieve the goals of reaching or head movement so that the observed EMG patterns reflect the implementation of a higher order invariant (Horak et al. 1997). In the case of postural equilibrium, which may be controlled at a lower level than voluntary reaching or head movements, it appears that simple, fixed synergies are not employed either (Macpherson 1991). Rather, groups of muscles are activated in response to similar directions of perturbations in a modifiable manner based on perturbation velocity and amplitude (Horak and Nashner 1986; Macpherson et al. 1986; Runge et al. 1998).

The evidence for synergy organization underlying postural control comes in part from the fact that unique muscle activation patterns are not observed for each direction of translation (Moore et al. 1988). Instead, there are three robust groupings of muscles, two that were maximally active on a diagonal and one that was maximally active in response to lateral surface translations (Fig. 4). The muscle activation patterns were consistent as evidenced by the overlapping patterns in the polar plots. Muscles were active over a range of translation directions, although their magnitudes were maximally tuned to one translation direction.

The evidence for a modifiable synergy organization is supported by the observation of continuous modulation in EMG amplitude with respect to translation direction and by the observation of variability among subjects with regard to EMG amplitude. The modifiability of postural muscle synergies is also obvious because some subjects recruited trunk muscles early, whereas others recruited them late, in response to the same direction of translation. Previous studies described how the A/P synergy can be modified by support surface configuration (Horak and Nashner 1986), by initial alignment (Horak and Moore 1993), and by amplitude and velocity of translation (Runge et al. 1998). It now appears that the A/P synergy is part of a more global, modifiable, diagonal synergy.

The continuous modulation of muscle magnitude suggests that peripheral sensory input plays an important role in signaling changes in translation direction. For each direction of translation, there were subtle changes in amplitude of muscle activation, although latencies often remained similar. The continuous changes in muscle magnitude may be determined by biomechanical constraints and need for stability in all planes, although the perturbation is in only one direction at a given time. Thus, for the task of stance maintenance in response to surface translations, muscle synergies are utilized, but in a flexible, modifiable manner to accommodate for changes in the biomechanical constraints of the task.

Why a diagonal pattern

Most of the muscles were maximally active to diagonal translations 30-60 or 300-330°. Lawrence et al. (1993) also demonstrated a diagonal orientation of torque vectors for the SOL and gastrocnemius muscles of cats in response to electrical nerve stimulation. This diagonal preference in humans cannot be contributed solely to foot placement, which was only a 10° toe out position. However, the subtalar joint axis does have an oblique axis, inclined 52° from the horizontal and 57° from the frontal plane (Root et al. 1977). This orientation would allow muscles such as TIB to have its optimal line of pull for torque production on a 30-60° diagonal. Nonetheless, the SEM and VSM muscles, which act primarily as knee flexors or extensors (a sagittal plane movement), also had maximum activation patterns on the diagonal. These diagonal muscle activation patterns suggest that equilibrium control is not the result of simple, negative feedback loops nor activation based on mechanical advantage.

More global control variables, such as force control, may be used to govern muscle recruitment (Fung et al. 1995; Jacobs and Macpherson 1996; Macpherson 1988). Diagonal synergies may be present to produce horizontal force vectors at the ground in a diagonal orientation (Fung et al. 1995), which provide stability against rotary moments that accompany horizontal translations (Henry et al. 1998; Macpherson 1994).

Timing of muscle recruitment

Although the magnitude of the ESP, RAB, and TFL muscles was continuously modulated with translation direction, the latency of ESP, RAB, and TFL muscle recruitment was discrete, activated either early or late. This is in contrast to the shank and thigh muscles that were activated at consistent latencies across all translation directions.

The postural responses observed in this task cannot be explained only by stretch reflexes for several reasons. First, early activation of trunk muscles accompanied a distal-to-proximal muscle activation pattern for shank and thigh muscles on the opposite dorsal/ventral side of the body. Second, distal ankle muscles had the longest distance for the afferent and efferent information to travel, and yet the distal muscles were activated first in 8 of 12 directions, suggesting a central delay in the activation of the proximal muscles. Third, early activation of trunk muscles was often observed before the trunk moved in space (Henry et al. 1998; Runge et al. 1998).

The latency of trunk muscle activation in response to diagonal translations seems to be a combination of the lateral and A/P responses (Fig. 7). Figure 7 illustrates schematically the inferred coordination pattern of the ESP, RAB, and TFL muscles based on the recordings from the left sided trunk and limb muscles. Given that the force patterns for the two feet were symmetrical (Fung et al. 1995), it is assumed the left and right muscle activation patterns would be symmetrical also. Given this assumption, it appears that relatively early proximal muscle activation occurs with all translation directions, suggesting that trunk position and orientation is an important controlled variable. Perhaps the timing of the synergy is under central influence, given the discrete latency changes for trunk muscle recruitment, whereas the modulation of EMG magnitude is influenced by peripheral information given the continuous changes of EMG magnitude with translation direction.


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FIG. 7. Schematic showing the directions in which the left-sided proximal muscles are activated early and by inference the directions in which the right-sided proximal muscles would be activated early (based on responses from left-sided muscle recordings). The schematic demonstrates that through early activation of proximal muscles the trunk is controlled in response to all translation directions. LTFL or RTFL, left or right TFL; LRAB or RRAB, left or right RAB; LESP or RESP, left or right ESP.

Our results showed discrepancies from Moore et al. (1988), who reported that the latencies of proximal muscles were continuously modulated with translation direction. The discrepancy may be methodological in that Moore et al. (1988) averaged the latencies of all the subjects, and this would produce a grand average that appeared to be modulated continuously with perturbation direction. In addition, the latencies of the postural responses may have been altered in Moore's study because the subjects knew the perturbation direction in advance, and prediction has been shown to influence postural responses (Timman and Horak 1997).

Control of proximal muscles

The control of the ESP, RAB, and TFL muscles is different from the shank and thigh muscles in that there appears to be a complex interaction between central and peripheral contributions for control of the trunk and pelvis. Two discrete latencies were observed as translation direction changed for these three muscles (ESP, RAB, and TFL). Similarly, Flanders et al. (1994) reported the timing of latissimus dorsi muscle burst switched abruptly from the timing of an antagonist to the timing of an agonist with different directions of arm reaching movements within the same quadrant of a multidirection reaching paradigm. Because so much of the body mass is located in the trunk, perhaps the CNS is controlling trunk orientation in space and the position of body CoM by regulating the timing and magnitude of proximal muscle activation. Early activation of these proximal muscles can increase active hip torque to assist the corrective postural response (Runge et al. 1998).

Muscles that are activated early may be prime movers to exert torques that move the body CoM, whereas muscles activated later may stabilize joints to counteract interactive torques (Zernicke and Smith 1996). Early activation of the RAB and ESP muscles has been shown to exert hip torque to control body CoM in the sagittal plane (Kuo and Zajac 1993; Runge et al. 1998). By a logical extension in the frontal plane, early activation of TFL muscle may be important as a prime mover to exert hip torque to control the body CoM in lateral direction, and TFL plus either RAB or ESP may be activated early to exert hip torque for responses in the diagonal direction. Given that the average latency of TFL was before the average onset of CoP change (Fig. 5A), this muscle could be active as a prime mover to generate the corrective forces at the ground. Thus the trunk-pelvis complex appears to be actively controlled in all directions to restore equilibrium. The postural task of maintaining equilibrium given unexpected surface translations is different from maintaining quiet stance on a nonmoving surface. Winter et al. (1996) previously suggested that an ankle mechanism can be used to control body CoM in the A/P plane while a hip mechanism is used to control body CoM in the medial/lateral plane during quiet stance. Because our study involved surface translations of moderate velocity, perhaps more active trunk control is needed to restore equilibrium under these dynamic conditions.

Not all subjects demonstrated a switch to early activation of the ESP, RAB, and TFL muscles, suggesting that addition of active hip torques was not the primary mechanism used by all subjects to maintain equilibrium in response to similar translation directions (Fig. 6). When the velocity and amplitude of the platform translation is increased, there seems to be a subject specific threshold (35-45 cm/s) for adding early activation of the RAB muscle (Runge et al. 1998). The translation velocity and acceleration in the current study were within the moderate range of perturbations and thus may be within the threshold range of adding the RAB muscle. Thus a subject may add ESP or RAB muscles to the distal-to-proximal synergy when the perturbation is destabilizing enough to require the addition of hip torque to ankle torque to restore equilibrium (Gordon 1990; Kuo and Zajac 1993). Given that the addition of RAB muscle appears to be velocity dependent (Runge et al. 1998), the control of trunk muscles could be a combination of stretch-evoked local responses and centrally triggered responses.

Although it has a unipolar spatial pattern, the TFL muscle is similar to the RAB and ESP muscles in that the TFL muscle showed a discrete change in latency with translation direction. The muscle was recruited early with a large burst of activity in directions in which the left leg was loaded and with a later, smaller burst in other directions in which the left leg was unloaded. The TFL muscle was activated before the distal muscles in response to the loading of the left leg. Because the ankle muscles have very small moment arms in the frontal plane and the knee does not move in the frontal plane, early activation of the TFL muscle was presumably to move the body CoM back quickly, similar to the role of RAB and ESP muscles in the more A/P translations.

Control of shank-thigh muscles

In contrast to the RAB and ESP muscles, the PER and SEM muscles exhibited no change in latency, although both muscles also exhibited a bipolar activation pattern, suggesting they play two different roles. The PER muscle is perhaps a prime mover in addition to the MGS and SOL muscles in restoring equilibrium in response to posterior translations. The PER muscle also functions as a stabilizer and as an antagonist to the TIB muscle to stabilize the ankle complex in response to anterior/rightward diagonal translations. The bipolar response pattern for the PER muscle suggests that the muscle is not being activated in response to stretch only because the muscle is activated maximally in response to two different translation directions.

Similarly, the SEM muscle may have two functions; the muscle may be synergistic with the ESP muscle in response to anterior translations as part of the hip synergy to extend the hips and move body CoM back over base of support quickly, or the SEM muscle may play a role in the distal-to-proximal ankle synergy in response to posterior translations. The SEM muscle may have two roles in postural responses, but the latency does not change because SEM is an intermediate muscle and can behave as a more distal or a more proximal muscle.

Two muscles, ADL and RFM, were maximally active in directions orthogonal to their anatomic orientation. In six of seven subjects, the ADL muscle, which adducts the hip, was maximally active with anterior translations resulting in backward sway. The ADL was coactivated with TFL, perhaps to stiffen hip joint and stabilize pelvis in frontal plane so that other pelvic and trunk muscles could function appropriately. Given the robust pattern of response, the control mechanism governing ADL muscle recruitment is not responding to stretch of this muscle because the muscle would most likely be stretched with hip abduction rather than hip flexion or extension, given its anatomic orientation.

Similarly, the RFM muscle was maximally activated in response to lateral translations, which is not the direction of anatomic orientation. The RFM may have a role in stabilizing the knee when the leg is loaded in response to lateral translations and/or play a role in providing pelvic stability so the other trunk/thigh muscles can be functional. Similar muscle activation patterns orthogonal to the line of pull have been shown in quadrapedal responses to multidirectional surface translations (Macpherson 1988). In standing cats, the gracilis muscle, a hip extensor and adductor, exhibited a tuning curve both different in extent and direction of maximal activation compared with other hip extensors. This observation suggests that the muscles were recruited differently, although they were anatomic synergists. Others (Lawrence et al. 1993; Nichols et al. 1993) also reported different spatial patterns and torque vectors for ankle muscles stimulated in cats, although the muscles were anatomic synergists.

The dual role of the muscles with bipolar spatial patterns (ESP, RAB, SEM, and PER) supports the notion that synergies are modifiable because, for each direction of maximal activation, the same muscle is recruited, but for a different function, and for ESP and RAB, also at a different latency. In addition, the complex spatial patterns exhibited by RFM and ADL add further evidence that the observed postural responses are the result of more complex control mechanisms that involve the interaction of peripheral and central processes. McCollum et al. (1984) and Horak and Nashner (1986) suggested that the timing of postural muscle synergies are discretely controlled, whereas the duration and amplitude of muscle activation can be changed continuously. The results of this study agree with these previous findings because muscle recruitment was discretely limited to one or two latencies for each muscle, most likely influenced by central mechanisms. Furthermore, the amplitude of muscle activation was continuously modulated with translation direction, suggesting peripheral information about perturbation direction influenced muscle magnitude.

The control of muscle activation for postural control can be achieved by constraining individual muscles to work together synergistically. In this study, the muscle activation patterns did tend to cluster primarily into two diagonal groups. The underlying distal-to-proximal activation pattern is consistent with a centrally influenced muscle synergy. Recruiting proximal muscles early provides a mechanism for adding active hip torque to ankle torque to restore equilibrium. Peripheral influences may also play an important role as evidenced by continuous modulation of muscle magnitude with translation direction. Because control of the trunk appears to be a significant factor in all directions, trunk orientation may be a highly controlled variable that the nervous system regulates. The observed EMG patterns with the discrete changes in latency and the continuous modulation of muscle amplitude of the more proximal muscles are a reflection of a higher order controlled variable (Horak et al. 1997). Future studies where the velocity and amplitude are varied for multidirectional surface translations will allow us to test for the presence of a higher order invariant. Thus postural coordination is a complex interaction of central and peripheral information. Centrally mediated mechanisms may influence the timing of muscle activation, and peripherally mediated mechanisms may influence the magnitude of muscle activation.

    ACKNOWLEDGEMENTS

  The authors thank A. Gross for technical assistance in analyzing the data and Dr. Jane Macpherson for thoughtful comments and discussions regarding this work.

    FOOTNOTES

   Present address of J. Fung: School of Physical and Occupational Therapy, 3654 Drummond St., McGill University, Montreal, Quebec H3G 1Y5, Canada.

  Present address and address for reprint requests: S. M. Henry, Physical Therapy Dept., 305 Rowell Bldg., University of Vermont, Burlington, VT 05405-0068.

  Received 25 September 1997; accepted in final form 6 July 1998.

    REFERENCES
Abstract
Introduction
Methods
Results
Discussion
References

0022-3077/98 $5.00 Copyright ©1998 The American Physiological Society