Download Human automatic postural responses

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BrainResearch
Exp Brain Res (1988) 73:648-658
9 Springer-Verlag 1988
Human automatic postural responses:
responses to horizontal perturbations of stance in multiple directions
S.P. Moore, D.S. Rushmer, S.L. Windus, and L.M. Nashner
Neurological Sciences Institute, Good Samaritan Hospital and Medical Center, 1120 NW 20th Ave., Portland, OR 97209, USA
Summary. The effect of the direction of unexpected
horizontal perturbations of stance on the organization of automatic postural responses was studied in
human subjects. We recorded EMG activity from
eight proximal and distal muscles acting on joints of
the legs and hip known to be involved in postural
corrections, while subjects stood on an hydraulic
platform. Postural responses to horizontal motion of
the platform in 16 different directions were recorded.
The amplitude of the EMG responses of each muscle
studied varied continuously as perturbation direction
was changed. The directions for which an individual
muscle showed measurable EMG activity were
termed the muscle's "angular range of activation".
There were several differences in the response
characteristics of the proximo-axial muscles as opposed to the distal ones. Angular ranges of activity of
the distal muscles were unipolar and encompassed a
range of less than 180~. These muscles responded
with relatively constant onset latencies when they
were active. Proximo-axial muscles, acting on the
upper leg and hip showed larger angular ranges of
activation with bimodal amplitude distributions and/
or onset latency shifts as perturbation direction
changed. While there were indications of constant
temporal relationships between muscles involved in
responses to perturbations around the sagittal plane,
the onset latency relationships for other directions
and the response amplitude relationships for all
directions varied continuously as perturbation direction was changed. Responses were discrete in that for
any particular perturbation direction there appeared
to be a single unique response. Thus, while the
present results do not refute the hypothesis that
automatic postural responses may be composed of
mixtures of a few elemental synergies, they suggest
that composition of postural responses is a complex
Offprint requests to: S.P. Moore (address see above)
process that includes perturbation direction as a
continuous variable.
Key words: Unexpected postural perturbations Electromyographic activity - Muscle synergies Motor control - Human - Automatic postural
responses
Introduction
Postural responses to unexpected perturbations of
stance have been shown to be automatic and highly
stereotyped in humans (i.e. Diener et al. 1984;
Nashner 1977; Nashner et al. 1979) and cats (i.e.,
Rushmer et al. 1983, 1987). Responses to horizontal
translations of the support surface in the anteriorposterior (A-P) direction involve activation of particular muscle groups with distinctive amplitude and
latency relationships.
Based on observations of human postural responses to unexpected perturbations in the sagittal
plane, Nashner and McCollum (1985) and McCollum
et al. (1985) advanced the hypothesis that the nervous system reduces the degrees of freedom necessary
for coordinating complex postural movements by
synthesizing responses from combinations of a few
distinct patterns of motor outputs. The hypothesis
states that sensory inputs signalling an unexpected
disturbance of stance impinge upon the nervous
system, which analyzes them for context dependence
and selects an appropriate combination of output
patterns based upon prior experience with similar
sensory events. This higher level process for composition of complex postural responses has been termed
the "strategy", while the distinct patterns of motor
outputs used to compose complex strategies have
been termed synergies. Thus, for unexpected pertur-
649
bations in the A-P direction, the ankle strategy is
used to exert torque about the ankle and the hip
strategy is used when torque about the ankle is
insufficient to correct stance and the subject must
depend upon hip generated shear force to restore
balance. Postural responses composed of a single
synergy can be observed, such as their "ankle
synergy" or "hip synergy" however, Nashner and
McCollum hypothesize that in practice, more complex patterns of muscle activation are formed by
combining several synergies, for example when subjects adapt responses to changed support surface
conditions (Horak and Nashner 1986). These
responses are termed "mixtures". It is proposed that
such mixtures are the combinations of more than one
elemental synergy and that timing and latency variations of the responses are due to segmental reciprocal
delays, "a lower level segment' by segment interaction between individual muscle commands" (McCollum et al. p. 60, 1985). Such segmental mechanisms
would prevent antagonist muscles acting on the same
joint that participate in two different elemental
synergies from coactivating.
When animals or humans are exposed to unexpected perturbations in either the anterior or posterior directions, motor responses that are appropriate
for the perturbation direction are always selected
(Rushmer et al. 1983; Moore et al. 1986). Thus, the
organization of the postural response, as exemplified
by the activated muscle groups, depends on the
direction of the unexpected perturbation. However,
past studies have only examined postural responses
to horizontal perturbations in the sagittal plane. The
question of how small changes in perturbation direction affect the organization of postural movements
has not been addressed using human subjects. In a
previous paper, we have demonstrated that in the
cat, which has only one strategy for response to
perturbations in the A-P direction, organization of
postural responses varies systematically as perturbation direction is changed (Rushmer et al. 1988). Does
the organization of postural responses follow the
same rules in humans, which have more complex
strategies for postural responses? As perturbation
direction is changed, will we see continuous variations in response patterns or can the changes in
responses be explained as different combinations of a
few distinct synergies? To examine this problem,
subjects were exposed to unexpected horizontal
translations of the support surface while oriented at
several different angles with respect to the platform
motion. The results of the study demonstrate that
amplitude and, in some cases, onset latency of each
individual muscle's EMG activity vary as a continuous function of perturbation direction. A second
finding is that the responses of proximo-axial muscles
are influenced by perturbation direction differently
than those of the distal leg muscles. Lastly, the
results also suggest that postural response organization, i.e., the relationship between amplitudes and
latencies of muscles active during the response,
varies as a continuous function of perturbation direction. Thus, if the idea of synergy as an elemental
building block of activity is to be retained, the
relations between muscles must be thought of as
functions of several variables rather than fixed
entities. Preliminary results of this study have been
presented elsewhere (Rushmer et al. 1986; Moore
and Rushmer 1987).
Methods
EMG and horizontal shear force were recorded from six normal,
healthy subjects, between the ages of 21 and 33, as they stood on a
moving hydraulically driven platform.
The platform was controlled by an hydraulic servomotor and
could be translated horizontally forward and backward. It consisted of two adjacent base plates, 20 cm by 42 cm. Strain guages
mounted within each plate provided horizontal shear force measures. For this study the platform moved 6 cm in 240 ms at an
average velocity of 25 cm/s.
To examine the effects of direction on human postural
responses in the horizontal plane, it was necessary to perturb the
subjects while they stood on the force platform at several different
angles from the direction of the platform motion. This was
achieved by having the subjects pivot on the platform at increments of 15~ keeping their feet a constant distance apart (approximately 6 in). Thus it was possible to present horizontal perturbations from 0~ to 360 o about the sagittal plane as shown in Fig. 1.
Bipolar surface electrodes were used to detect muscle activity.
The activity of up to 4 pairs of representative leg, thigh and hip
muscles on the subjects' right side were analyzed. Three pairs of
muscles were involved in responses to forward/backward horizontal translations and have been previously documented. They were:
medial gastrocnemius (MG) and tibialis anterior (TA); biceps
femoris of the hamstrings (HAM) and rectus femoris of the
quadrieeps (QUAD); paraspinal at the iliac crest level (PARA)
and rectus abdominus at the umbilicus level (ABDM). Because
most of the perturbations used in this study contained a lateral
component, it was necessary to also examine muscles that were
active during hip abduction (tensor fascia latae, ABDC) and
adduction (upper part of the hip adductors, ADDC), The
myoelectric signals were amplified with cutoff frequencies of 70
and 2000 Hz, rectified and then low pass filtered (time constant
10 ms). When the electrodes were applied, the skin over the
muscles was cleaned and electrodes were placed over the middle of
each muscle belly, approximately 3 cm apart, center to center. A
ground electrode was attached above the right lateral malleolus.
During the experiment, subjects stood on the platform and
were given several practice trials, in the backward and forward
directions (0~ and 180~ to get accustomed to the platform motion.
Subjects then performed 80 to 120 trials, which were presented in
blocks of 10 trials, while oriented in 8 to 12 different directions in
relation to the sagittal plane. Within each block of trials, there
were 5 forward and 5 backward platform translations, randomly
presented. The directions that the subject faced were also randomized.
650
anterior sway
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posterior sway
Fig. 1. Schematic drawing showing the different angles the subjects
faced in order to present horizontal perturbations from 0~ to 360~
about the sagittal plane. 0~ (anterior sway) and 180~ (posterior
sway) perturbations resulted when subjects stood facing forward
(F) and the support surface was translated backward (B) and F,
respectively. Similarly, 90~ and 270 ~ perturbations resulted when
subjects turned facing 90~ to the right and the support surface was
translated B and F, respectively
Data collected for all trials included the EMG signals, force
measures and platform position. A total of 1 s of data was
collected starting 150 ms prior to the onset of the perturbation.
Signals were converted from analog to digital form, on-line, by a
LSI-11/23 minicomputer, at a sampling rate of 500 Hz and stored
for subsequent processing.
The horizontal shear force was used to determine the onset of
the perturbation. For each trial, onset latencies of muscle activity
were determined by visual inspection and expressed with respect
to the perturbation onset. Amplitude of the EMG response was
determined by integrating the first 75 ms of muscle activity starting
from onset of muscle activity (IEMG). Onset latency and IEMG
measures were averaged for each direction, IEMG measures for
each muscle were normalized by assigning the largest IEMG
activity a value of 1 and expressing the IEMG values for all other
directions as fractions of that maximum value.
Results
The amplitude of each muscle's response varied
systematically as the direction of the perturbation
was changed. Figure 2 shows, for a single subject,
averaged EMG responses of tibialis anterior for each
of 16 different directions of platform motion. IEMG
of the postural response was calculated for the 75 ms
window defined by the vertical dashed lines. To
demonstrate amplitude variation with perturbation
direction, IEMG values were normalized and plotted
on a polar plot (center, Fig. 2). This variation of
IEMG with perturbation direction was defined as the
muscle's "angular range of activation", a term which
was first used by Buchanan et al. (1986) to describe
the variation of elbow muscle EMG activity as a
function of torque direction.
Each muscle studied showed a unique angular
range of activation for this set of horizontal translations. Figure 3 shows polar plots of the angular range
of activation for each muscle. The plots shown are
averaged responses across 5 or 6 subjects, as indicated on the figure. The lines in the radial directions
represent one standard deviation above the mean.
Muscles could be divided into two groups based
on their response characteristics. The first group
showed small angular ranges of activation and their
onset latencies remained relatively constant as perturbation direction was altered. This group included
medial gastrocnemius and tibialis anterior as well as
quadriceps and will be referred to as "distal" muscles. The second group, the "proximo-axial" muscles,
was comprised of the adductors, abductor, abdomirials and paraspinals. These muscles tended to show a
larger angular range of activation and demonstrated
bimodal IEMG distributions and/or variations in
onset latency as perturbation direction changed.
Unlike the other muscles, hamstrings showed considerable between subject variability. For some subjects
hamstrings behaved like a distal muscle while for
other subjects it behaved more like a proximo-axial
muscle.
Distal muscle responses. As shown in Fig. 3, both
gastrocnemius and tibialis anterior had relatively
narrow angular ranges of activation with very low
between subject variability. Gastrocnemius was most
active when the right leg participated in the correction for anterior sway and when it was loaded as a
result of lateral platform motion (270~176 As was
observed in the cat (Rushmer et al. 1988), the
angular range of activation was not oriented about
the sagittal plane, as might be predicted if this muscle
were primarily involved with responses to the A-P
components of sway. The angular range of tibialis
was more oriented about the sagittal plane
(120~
~ than that of gastrocnemius, although
maximal activity was observed when the platform
motion evoked posterior sway and loading of the
right leg. The onset latencies for both muscles
remained constant throughout the angular range of
activity: the mean latency throughout the range for
gastrocnemius was 101 + 8 ms and for tibialis was
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110 + 4 ms. Outside these directions, tibialis and
gastrocnemius were relatively silent.
The angular range of activation of quadriceps was
unimodal, about the sagittal plane (120 ~ to 240 ~ and
tended to overlap that of tibialis. The between
subject variability of quadriceps activity level was
relatively low. Quadriceps latencies varied little
throughout the angular range of activity (mean
latency 133 + 4 ms) and tended to lag those of
tibialis by about 23 ms.
Proximo-axial muscle responses. The angular ranges
of activation of abdominals and paraspinals were
bimodal, showing E M G activity in both the backward and forward directions (centered about both 0 ~
and 180~ The between subject variability observed
for these two muscles was mainly due to peak activity
occurring at slightly different directions for each
individual subject. Peak activity for the paraspinals
ranged between 0 ~ and 30 ~ in the anterior direction
and between 180 ~ and 240 ~ in the posterior direction;
the abdominal's peak activity occurred between 315 ~
and 0~ in the anterior direction and between 150~ and
180~ in the posterior direction. Despite these differences between individuals, the shape of the angular
ranges of activity were similar for all subjects.
Onset latencies for responses of these two muscles varied considerably as a function of perturbation direction. Figure 4 shows amplitude and onset
latency changes for paraspinals (Fig. 4A) and abdominals (Fig. 4B) plotted as a function of perturbation direction. For perturbation directions containing
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Fig. 2. Polar plot representing the
amplitude of the automatic postural
E M G responses from tibialis anterior
to horizontal perturbations of stance in
16 different directions, for one subject.
EMG traces are the averages of 5 trials
for each direction perturbation. Vertical arrows denotes onset of platform
movement. The vertical dashed lines
show the 75 ms window of integration.
The polar plot is taken from the normalized amplitude values
100 msec
an anterior sway component (0 ~ abdominals activity
began early (89 _+ 17 ms) and paraspinals became
active later (160 + 29 ms). In contrast, for perturbations with a posterior sway component (180~ onset
latency of abdominals was 184 _+ 32 ms and that of
paraspinals was 100 + 20 ms. In both the paraspinals
and abdominals, transitions of onset latency generally occurred when platform motion was in the lateral
direction (90 ~ and 270~ and activity in these muscles
was relatively low. The increased between subject
variability over these transition periods was possibly
due to the difficulty in determining the onset latency
when the activity level was low.
The hip abductor showed a bimodal angular
range of activation with low between subject variability. This muscle was most active for those perturbation directions which Ioaded the right leg and active
to a lesser extent when the leg was unloaded (Fig. 3).
The angular range was oriented about platform
motion in the lateral directions. Hip adductors
showed a broad angular range which extended from
30 ~ to 240 ~, with maximal activity in perturbation
directions which evoked posterior sway and unloaded
the right leg. Onset latency variations with perturbation direction were also observed for these muscles
(Fig. 5). Transitions in latency relationships occurred
near the A-P directions; again there was an increase
in between subject variability during the transition
periods and when the activity level was low. Activity
in adductors occurred early (range of 9%100 ms) for
directions from 30 ~ to 90 ~ and late (range of
137-142 ms) from 210 ~ to 240 ~. The abductor was
active late (range of 139-151 ms) for directions from
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Fig. 4. Normalized IEMG (dotted line) and onset latency (solid
line) of paraspinals (A) and abdominals (B) plotted as a function of
perturbation direction. Vertical lines represent _+ one standard
deviation of the mean latency values
Fig, 3. Polar plots representing the average angular range of
activation of the eight muscles examined in this study. Normalized
IEMG (see text) is in the radial direction and perturbation
direction is in the angular direction9 The solid lines in the radial
direction indicate one standard deviation above the mean. The
number of data sets used to calculate the mean is shown under the
muscle name
45~ to 150~ and early (range of 91-96 ms) for directions from 240 ~ to 330 ~.
Hamstrings responses. As mentioned above, hamstrings showed large between subject variability
which appeared to be due to whether its response was
similar to that of the distal group of muscles or to that
of the proximo-axial ones. Averaged hamstrings
activity showed a bimodal distribution centered
about the sagittal plane. The greatest hamstrings
activity was generally centered about platform
motion in the anterior direction with lower activity
levels when motion was in the posterior direction.
The opposite result was obtained for one subject,
where the greatest activity level was observed in the
posterior direction. This accounts for the large standard deviation of the averaged responses in the
anterior and posterior directions. Hamstrings activity
was lowest when platform motion was in the lateral
directions (see Fig. 3). Two types of onset latency
changes were observed. One type (N = 3) was
similar to the distal muscle response, that is, as
I E M G changed, there was little change in the onset
latency of E M G activity. For example, one subject
showed onset latencies of 111 _+ 13 ms at 0~ and
115 + 4 ms at 180 ~ For the other response (N = 2),
onset latency changes were similar to those observed
for proximo-axial muscle response. One of these
subjects showed hamstrings response onset latency of
121 + 8 ms at 0~ and 83 + 8 ms at 180 ~ Apparently
each subject grouped hamstrings either as a proximoaxial muscle or as a distal muscle and for the
perturbations used in this study, this strategy did not
change from one trial to the next.
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Fig. 5. Normalized IEMG (dotted line) and onset latency (solid
line) of hip adductors (A) and hip abductors (B) plotted as a
function of perturbation direction. Vertical line represent + one
standard deviation of the mean latency values
Postural response organization. To show the relationships between muscles during postural responses,
EMG responses were plotted as "musical scores", for
each the directions examined. These are illustrated in
Fig. 6. The magnitude of the muscle activity is
indicated by the height of the triangles. Averaged
onset latency is shown at the left edge of the
triangle's base. The width of each triangle is arbitrarily set at 75 ms to denote the time during which the
EMG was integrated. Activity of the muscles for
each direction is shown across the figure. When
presented in this manner, there appears to be a
unique response organization for each of the directions since the amplitude and timing relationships
between the muscles and/or the muscle groups
involved in each response are different for each of
the perturbation directions.
The EMG responses seen at 0~ were a distinct
initial abdominal burst followed by gastrocnemius,
hamstrings and paraspinals which were activated in a
distal to proximal temporal order. The temporal
relationships between muscles involved in the post-
ural responses for perturbation directions from 300~
to 0~ were similar. However, although the temporal
relationships between the muscles remained constant, their response amplitudes did not change
proportionally. For example, while gastrocnemius
was most active at 300~ and 315 ~, hamstrings was just
becoming active and was most active at 0~ Also,
gastrocnemius dropped out of the response at 30~
while both hamstrings and paraspinals were still quite
active.
As the perturbation direction changed from 30~
to 120~ there was a gradual decrease in the activity of
both hamstrings and paraspinals and there was little
activity in the distal muscles. Abdominals also
showed a decreased response amplitude with an
increasing onset latency. Adductors activity level
increased while the amplitude of the longer latency
abductor responses decreased.
For perturbation directions between 120~ and
225~ the ventral muscles were involved in the
postural response. Tibialis anterior, quadriceps and
abdominals responded in a distal to proximal temporal order which remained relatively constant for
these perturbation directions. The relative response
amplitudes varied considerably as direction was
changed and did not change proportionally. At 180~,
paraspinal became involved early in the response and
hamstrings and quadriceps were coactivated. Abductor and adductors were also relatively active and
appeared to cocontract in response to this perturbation, perhaps to stabilize the hip joint. These results
suggest that the 180~ perturbation was more destabilizing than the translation at 0~
From 225 ~ to 300~ the posterior sway postural
response component decreased, i.e. tibialis, quadriceps, abdominals and paraspinals activity levels
decreased, and a more lateral component to the
response became apparent. The abductor showed a
gradual increase in amplitude and an earlier onset
latency while the adductor response decreased and
displayed a later onset latency, although activity in
these muscles overlapped in time with a latency
difference of only 30 ms. At 270~ the first muscle
activated was the abductor. Interestingly, it was in
this direction that the gastrocnemius response reappeared and a temporal switch from an early to a later
onset latency occurred in the abdominals.
If a small number of discrete synergies are
utilized by the nervous system in response to postural
perturbations, the muscles involved should show
tightly coupled amplitude and onset latency relationships as direction of the perturbation is changed. To
test this hypothesis, linear regression analysis was
performed on the EMG responses for each pair of
muscles across the set of perturbation directions. The
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correlations were generally low, which would be
expected given Fig. 6. Several significant, positive
correlations (P < 0.05) were found for response
amplitudes: tibialis on quadriceps (r -- 0.958),
adductors on quadriceps (r = 0.805) and addSctors
on tibialis (r -- 0.672). However, the onset latency
correlations were insignificant for these muscle pairs
(r = 0.103; r = - 0 . 2 4 7 and r = - 0 . 0 5 5 , respectively). A significant correlation was found between
the amplitude response of hamstrings and paraspinals
(r = 0.631). As previously stated, two types of onset
latency changes were found for hamstrings. Thus
correlations were performed for each individual
subject. For the subjects who showed little change in
onset latency, no significant positive correlations
were found. For the subjects who showed a variable
hamstrings onset latency, significant correlations of
r = 0.853 and 0.699 were found.
:
Fig. 6. "Musical scores" showing the
response relationships of the eight muscles
examined in the present study for each
direction of platform movement. Height of
the triangles is the normalized IEMG
response. Onset latency is shown at the left
edge of the triangle's base. The width of
each triangle is arbitrarily set at 75 ms to
denote the time during which the E M G was
integrated
Discussion
This study, which examined the effects of small
changes in perturbation direction on human postural
responses, revealed three significant findings. First,
EMG activity, and in some cases, onset latency of
individual muscle responses varied continuously as a
function of perturbation direction. A similar result
was obtained in an analogous experiment with cats
(Rushmer et al. 1988). Secondly, a dramatic difference in response characteristics between the distal
and proximo-axial muscles was observed. We believe
that this difference was due to the role that each
group of muscles played in the control of posture as
well as to biomechanical contraints. Lastly, as in the
cat experiments, the results suggest that for each
perturbation direction there was a unique postural
response. While there were indications of constant
655
temporal relationships between muscles involved in
responses around the sagittal plane, the amplitude
relationships varied continuously with perturbation
direction. Thus it appears that perturbation direction
is a key sensory variable in determining response
organization and that the response organization may
depend upon more factors than the summation of a
few discrete synergies.
Responses of individual muscles - distal~proximoaxial differences. EMG activity in each of the muscles
studied varied in a systematic and continuous manner
with perturbation direction. Such variation was
observed in both the amplitude of the EMG bursts
and, for some muscles, in the onset latencies for
EMG activity. In general, the angular ranges of
activation of the most distal muscles, medial gastrocnemius and tibialis anterior, as well as hip adductor
were not aligned about either the A-P or the lateral
axes, while the other muscles examined in the
present study were aligned about these two axes.
Alignment on the A-P or lateral axes is a difference
from similar studies in the cat, in which none of the
muscles studied were aligned about these axes (Rushmet et al. 1988). An explanation for this discrepancy
may be the methods of recording. In the cat individual muscles were identified anatomically and
studied with indwelling EMG electrodes sewn into
the muscles. The surface electrodes used in the
present studies most likely provided summed EMG
activity from more than one muscle within a muscle
group (i.e., hamstrings and quadriceps) except
perhaps for the records from tibialis anterior and
medial gastrocnemius, which could be isolated with
more certainty.
Our data suggests that the operational rules for
the action of proximo-axial muscles are different
from those of the distal muscles. First, the angular
ranges of the distal muscles were relatively narrow
(< 180~ while the angular ranges of the proximoaxial muscles were broader and in many cases, had
bimodal distributions. Second, both the agonist and
antagonist of a proximo-axial muscle pair tended to
be involved in the postural response. Lastly, when
activated, the onset latencies of the distal muscles
were relatively constant while the onset latencies of
proximo-axial muscles varied dramatically as perturbation direction was altered.
The differences in the response characteristics
between the proximo-axial and distal muscles appear
to be due to the different roles these muscles play in
the control of posture. According to Smith and
Zernicke (1987), a muscle can function to either
control the limb dynamics (i.e., to produce move-
ment about the joint) or to counterbalance interactive torques which are developed from mechanical
interactions between limb segments. Thus, during
the control of posture, the distal muscles may only
function to produce movement about the ankles, and
would not be subjected to interactive torques. The
work of Buchanan et al. (1986) supports this conclusion, since none of the muscles that they studied
showed any sign of playing the role of a stabilizer.
The angular ranges of activation for the distal muscles in our experiments were similar to those
reported by them for isometric elbow movement, a
task where the muscles also did not have to deal with
intersegmental torques.
The proximo-axial muscles may serve both to
produce movement and to counterbalance interactive
torques. When hip movement was part of the postural strategy, the burst of the first proximo-axial
muscle controlled the limb dynamics by producing
movement about the hip to bring the center of mass
over the base of support. For example, from experimenter observation it appeared that for some perturbations, particularly those involving lateral sway, the
postural response involved movement about the hip.
In this case, the right hip abductor responded first
when the lateral perturbation loaded the right leg
(270~
There were postural responses where no hip
movement was observed but a proximo-axial muscle
still responded first. Such a response was at 0~ when
the abdominalis were the first muscles activated.
Diener et al. (1988) also report a similar abdominal
burst for this stimulus direction and size. Their
kinematic data indicated that this postural response
does not involve hip movement. We conclude that
the initial burst of the abdominals is part of the
postural response and functions to counterbalance
the inertial loads that are generated as a result of the
response.
The present results suggest that response characteristics of hamstrings and possibly quadriceps may
depend upon how destabilizing the perturbation is to
the subject. When the perturbation is very destabilizing, it may be necessary to activate these muscles
early (i.e., hamstrings for perturbations about 180~
and quadriceps for perturbations about 0~ For
example, an early response of hamstrings was
observed for perturbations about 180~ A similar
response was not seen in quadriceps for perturbations about 0~ since a 25 cm/s translation is much
more destabilizing in the 180~ direction due to the
biomechanics of the human foot. It is possible that if
a more destabilizing perturbation was used, the
response of both these muscles would be similar to
the proximo-axial muscles while a less destabilizing
656
perturbation would result in responses similar to the
distal muscles.
Referring back to Fig. 6, the initial burst of the
proximo-axial muscle is always followed by a later
burst of its antagonist muscle. According to McCollum et al. (1985), this late proximal muscle burst
occurs after distal muscle activity and acts to brake
the hip torque which follows the ankle torque. This
braking function is similar to the role of the antagonist burst in arm movement (i.e., Marsden et al.
1983; Wierzbicka et al. 1986). During step-tracking
wrist movements in different directions (Hoffman
and Strick 1986) and in the proximo-axial muscles in
our own experiments, as the direction of movement
changed, the muscles changed their role from agonist
to antagonists through relative changes in onset
latencies.
Differences in action of distal and proximo-axial
muscles have been described in other movement
paradigms as well. Hoy and Zernicke (1985, 1986)
reported distal/proximal differences for locomotion
and the paw shake in the cat. During the paw shake
(Hoy and Zernicke 1986), muscle moments at the
ankle generated paw acceleration while muscle
moments at the hip acted to counterbalance movements due to acceleration of the more distal segments
as well as to maintain the hindlimb postural orientation. Although these results were for on oscillatory
movement, it is possible that similar mechanics are
involved in the control of posture.
Muscle response relationships. A goal of the present
study was to test the hypothesis of Nashner and
McCollum that automatic postural responses are
organized by mixing a small number of elemental
synergies. We theorized that support of their hypothesis might be indicated by relatively discrete
changes in the organization of postural responses as
the perturbation direction was systematically varied
and boundaries between synergic actions were
crossed. The continuous variation of response
organization with perturbation direction observed in
the present study does not support or refute the
hypothesis that the automatic postural responses are
simple mixtures of a few synergies. The data do show
that the postural response organization is determined
by sensory cues which include directionality. As long
as perturbation direction is held constant, response
organization is discrete. However, as perturbation
direction is varied, response organization is dominated by continuous aspects.
The results show that the response organization
in directions near the sagittal plane did show relatively constant onset latency relationships between
muscles that participated in the postural responses.
The temporal relationships between muscles
involved in Nashner and McCollum's ankle synergies
are relatively constant for perturbation directions on
or near the sagittal plane. From 300 ~ to 15~ abdomirials always responded first followed by medial gastrocnemius, hamstrings and paraspinals. Similarly,
latency relationships between tibialis anterior, quadriceps, paraspinals and abdominals were relatively
constant for perturbation directions from 165~ and
225 ~. However, onset latency relationships between
these muscles varied continuously for other perturbation directions. In addition, the response amplitude
relationships between the same muscles varied continuously over the entire range of perturbation directions. While the latency relationships provide some
evidence for discreteness in the postural responses,
sharp transitions in latency and/or amplitude were
not observed.
The present data are not totally consistent with
previous work. First, the postural response we
observed at 0~ was similar to the ankle response
observed by Horak and Nashner (1986). However,
unlike the response described by these workers, a
distinct abdominal burst was seen prior to the onset
of activity in gastrocnemius, hamstrings and paraspinals. Others have also reported this initial abdominal
burst (Diener et al. 1988). Second, assuming an
average burst duration of 75 ms (Diener et al. 1988),
we observed coactivation of agonist-antagonist pairs,
both in the individual and in the averaged data, when
both the agonist and antagonist were involved in the
postural response. This coactivation is evident in
Fig. 6 between hamstrings and quadriceps, and
between abductors and adductors. Abdominals and
paraspinals showed little coactivity, due to their large
variation in onset latency. Thus, while segmental
modulation of postural responses most certainly does
occur, mechanisms such as the reciprocal delay
mechanisms postulated by McCollum et al. (1985) do
not seem to act to prevent cocontraction of agonistantagonist pairs during postural responses. There are
several reasons which may account for these discrepancies. The perturbation used by Horak and
Nashner (1986) was 13 cm/s, which is slower than the
25 cm/s translation used in the present experiment.
As well, past work has concentrated on anterior
sway, with little emphasis on posterior sway. When
cocontraction was observed in the present study,
there was usually a posterior sway component to the
perturbation.
The muscle response organization appears to be
dependent on similarities of biomechanical function
of the muscles and highly dependent on the task. For
example, during postural corrections, the amplitude
of tibialis anterior and quadriceps covaried as direc-
657
tion changed while those of medial gastrocnemius
and hamstrings did not. Response coupling between
these muscles does occur under different mechanical
conditions. When subjects were required to produce
an isometric force at the foot in directions about the
horizontal plane, the activity of gastrocnemius and
biceps femoris appeared to be similar (Wells and
Evans Stuber 1986). Similarly, in the different
biomechanical conditions of quadrupedal stance, the
amplitudes of the cat's lateral gastrocnemius and
vastus lateralis responses covary as a tightly coupled
unit during horizontal perturbations of stance (Rushmer et al. 1988).
The present study does have limitations. First, six
of the eight muscles examined were involved in
flexion or extension and participated primarily in
postural corrections in the sagittal plane. Largely
because of difficulties in accessing involved muscles
with surface electrodes, we only sampled from one
abductor and one adductor of the hip and did not
sample enough muscles that were primarily responsive to perturbations in the lateral direction to
describe a lateral synergy. However, given the present findings, we would predict that the response
amplitude and latencies of the additional muscles
involved in a possible lateral synergy would also vary
continuously with respect to changes in perturbation
direction.
Secondly, it is also possible that we did not
examine enough muscles to be able to detect the
contribution of synergies to the responses. For instance, if the subjects were mixing eight synergies,
four for the A-P direction (hip and ankle, forward
and backward) and four for the lateral direction,
records from eight muscles would not allow delineation of responses related to any single program.
However, we believe that we can discount this
explanation for the present results. Continuous variation of muscle response organization with perturbation direction was also observed in cats (Rushmer et
al. 1988) which, because of their biomechanics, have
only two synergies in the A-P direction and probably
a similar number in the lateral direction. Eight
muscles were also studied in these experiments,
enough to identify contributions from individual
synergies, yet the results were similar to those
reported here.
While our data do not support a specific theoretical mechanism for the production of automatic
postural responses, they do indicate that, hke initial
perturbation velocity (Diener et al. 1988), perturbation direction is a key variable for the determination
of response characteristics. The response organization is always appropriate for a specific perturbation
direction and is largely unaffected by any previously
presented disturbances. Thus, perturbation direction
may be processed differently than support surface
size since the latter variable's affect on postural
responses is strongly influenced by set and previous
experience and is subject to adaptation over several
trials.
Acknowledgements. Supported by NIH grants R01-NS 12661 and
R01-NS 19484. S.P. Moore was funded in part by a post-doctoral
fellowship from the Natural Sciences and Engineering Research
Council of Canada.
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Received August 10, 1987 / Accepted June 29, 1988