 |
Previous Article | Next Article 
The Journal of Neuroscience, January 1, 2000, 20(1):409-426
Rapid Correction of Aimed Movements by Summation of
Force-Field Primitives
William J.
Kargo and
Simon F.
Giszter
Neurobiology Department, Medical College of Pennsylvania/Hahnemann
University, Philadelphia, Pennsylvania 19129
 |
ABSTRACT |
Spinal circuits form building blocks for movement construction. In
the frog, such building blocks have been described as isometric force
fields. Microstimulation studies showed that individual force
fields can be combined by vector summation. Summation and scaling of a
few force-field types can, in theory, produce a large range of dynamic
force-field structures associated with limb behaviors. We tested for
the first time whether force-field summation underlies the construction
of real limb behavior in the frog. We examined the organization of
correction responses that circumvent path obstacles during hindlimb
wiping trajectories. Correction responses were triggered on-line during
wiping by cutaneous feedback signaling obstacle collision. The
correction response activated a force field that summed with an ongoing
sequence of force fields activated during wiping. Both impact force and
time of impact within the wiping motor pattern scaled the evoked
correction response amplitude. However, the duration of the correction
response was constant and similar to the duration of other muscles
activated in different phases of wiping. Thus, our results confirm that
both force-field summation and scaling occur during real limb behavior,
that force fields represent fixed-timing motor elements, and that these
motor elements are combined in chains and in combination contingent on
the interaction of feedback and central motor programs.
Key words:
force field; spinal cord; reflex; superposition; primitive; motor control
 |
INTRODUCTION |
The spinal cord of lower vertebrates
and mammals may be organized into movement control modules (Grillner
and Wallen, 1985 ; Loeb, 1985 ; Mortin and Stein, 1989 ; Rossignol, 1996 ;
Kiehn et al., 1997 ; Smith and Stein, 1997 ). Such modules might control specific force patterns in the limb (Bizzi et al., 1991 ; Giszter et
al., 1993 ; Nichols, 1994 ). How spinal modules are recruited, combined,
and interact in the construction of limb behaviors has implications for
motor learning, neural repair and rehabilitation, and the design of
prosthetics and robotics. In this paper we present the first direct
evidence that force-field primitives, spinal control modules identified
in the frog, are combined to produce limb behaviors and their on-line adjustments.
Spinal microstimulation provided the initial evidence that the frog
spinal cord may be organized into modules that produce force-field
primitives (Bizzi et al., 1991 ; Giszter et al., 1993 ; Mussa-Ivaldi et
al., 1994 ). Force fields were constructed by measuring isometric forces
at the ankle with the limb held in a range of positions and with the
same stimulus applied at each position. Primitives were defined as
force fields that exhibited invariant force directions and magnitude
balances over time. Only a few force-field types were found for any
individual frog, force-field types were similar among frogs, and each
force field typically converged to a specific workspace location
(Giszter et al., 1993 ). The effect of coactivating force fields by dual
microstimulation could be described as the linear sum of the
individually activated force fields (Mussa-Ivaldi et al., 1994 ).
Theoretical studies showed that summation and scaling of a few
force-field types could be used to generate a large range of
force-field structures and might underlie movement synthesis
(Mussa-Ivaldi, 1992 , 1997 ; Mussa-Ivaldi and Giszter, 1992 ).
Descending and segmental systems might recruit, scale, and sum
force-field primitives in a manner similar to microstimulation (Bizzi
et al., 1991 ; Bizzi et al., 1995 ; d'Avella and Bizzi, 1998). Indeed,
force fields produced during certain reflex behaviors in the frog were
similar to microstimulation-generated fields (Giszter et al., 1993 ).
However, recent data have indicated that reflex behaviors and phases of
behaviors may not correspond in a one-to-one fashion with a muscle
synergy or force-field primitive, but instead correspond to
combinations of such elements (Kargo et al., 1998 ; Tresch et al.,
1999 ). Tresch et al. (1999) showed that different withdrawal responses
could be described as constructed from different combinations of a
basic set of muscle synergies. These synergies were similar to the
muscle synergies evoked by spinal microstimulation (Tresch,
1997 ). How these data, which were measured at a single limb
position, relate to the description of limb behaviors as a combination
of force-field primitives was not tested directly.
We therefore examined in this paper how force-field mechanisms might be
used to generate and control limb behavior. Specifically, we examined
how the targeted wiping reflex of the spinal frog is organized and how
on-line trajectory corrections are achieved. We found that force-field
primitives were recruited in chains and in combination to produce
wiping trajectories and their on-line adjustments. Furthermore, each
primitive exhibited a common activation waveform of constant duration.
Taken together, our data suggest that constant-duration force-field
primitives form building blocks for the construction of certain limb behaviors.
 |
MATERIALS AND METHODS |
Surgery
Detailed surgical procedures have been outlined in previously
published material (Giszter et al., 1993 ; Kargo and Giszter, 2000 ). All
procedures were approved and in accordance with Institutional Animal
Care and Use Committee recommendations. Briefly, bullfrogs received a
spinal transection at high cervical levels below the base of the
medulla, thereby isolating the spinal cord. The tectum was
heat-cauterized. Ten muscles in the wiping limb were implanted with
paired intramuscular electrodes for differential recording of muscle
electrical activity. Muscles that were implanted included monoarticular
hip flexors [iliopsoas (IL) and gluteus (GL)], biarticular hip/knee
flexors [biceps (BI) and sartorius (SA)], monoarticular hip extensor
[adductor magnus (AD)], biarticular hip flexor/knee extensors
[rectus anterior (RA) and vastus externus (VE)], and biarticular hip
extensors/knee flexors [semitendinosus (ST), rectus internus (RI), and
semimembranosus (SM)]. All skin incisions were sealed with wound clips
and cyanoacrylate tissue adhesive (Vetbond, 3M). Frogs were
permitted 12-24 hr recovery after the surgery and stored in a damp
container in the refrigerator at ~10°C.
Experimental protocol and design
Fourteen frogs were used in these experiments. We tested the
hindlimb-to-hindimb form of wiping. In this form, the wiping limb and
target limb both move such that the stimulus and the ankle of the
wiping limb (i.e., the wiping tool in this form) meet near the midline
of the frog, just caudal to the cloaca [for detailed kinematic
descriptions, see Giszter et al. (1989) and Kargo and Giszter (2000) ].
In both free limb and isometric trials, the wiping reflex was initiated
by a 500-600 msec train of 2 msec, 4-8 V biphasic pulses delivered at
33 Hz. The stimulus was applied via bipolar leads attached to the
dorsolateral surface of the foot of the target hindlimb. The stimulus
placement, and the parameters used, reliably elicited the
hindlimb-to-hindimb form of wiping [for detailed kinematic
descriptions, see Giszter et al. (1989) and Kargo and Giszter (2000) ].
In this form of wiping, and in our hands, the wiping limb initiates
movement 200-300 msec after onset of the stimulus and contacts the
stimulus (on the target limb) another 200-300 msec later. Therefore,
the 500-600 msec stimulus ends before or near the time of target limb
contact and usually evokes single, nonrepetitive movements of the
wiping and target limbs. The stimulation parameters therefore
approximate the pattern of stimulus successfully removed by the wipe.
However, similar wipes can be obtained with shorter pulse trains. The
parameters chosen here minimized habituation, sensitization, and
decline of response.
Experiments were designed to test (1) the organization of correction
responses by the wiping limb to obstacles in its movement path, (2)
whether correction responses were produced in the isometric limb, and
(3) whether correction responses could be expressed as a summation of
force-field primitives.
Free limb testing. To test the organization of free limb
corrections, a rod was used as a path obstacle and was attached to a
six-axis force transducer (Assurance Technologies, Garner, NC). The rod
was placed in the movement path of the wiping limb, and wiping
movements were evoked. The initial postures of the wiping and target
limbs before the reflex was evoked were similar for all trials and for
each tested frog. The distance along the movement path of the wiping
limb at which the rod was placed was systematically varied in each of
the six frogs. The distance from the initial position of the heel to
the rod was measured for all trials. For each distance that was tested
in a frog, the rod was placed so that collision with the limb occurred
2-3 mm above the heel.
Isometric testing. To test whether correction responses
could be evoked in the isometric limb, we placed the ankle of the wiping limb in a custom-made restraint. The restraint was secured around the perimeter of the ankle, 2-3 mm above the heel, where obstacle collisions occurred during free limb trials. The restraint was
attached to the force/torque transducer by a custom-made shaft. We
recorded isometric force vectors produced at the ankle after evoking
the wiping reflex. The wiping limb was positioned in a number of
initial limb postures (10-12) that spanned the reachable workspace of
the wiping limb, and wiping was evoked at each posture. In these
experiments, although the wiping limb was restrained, the target limb
was not restrained. It was free to move and began from a similar
initial posture for each trial. We found that wiping reflexes could be
evoked in the isometric condition [also see Giszter et al. (1993) and
Kargo et al. (1998) ]. In addition, we found that the restraint acted
like a path obstacle and evoked a correction response that was similar
to the response evoked by obstacle collision during free limb trials
(see Data analysis and Fig. 4).
Cutaneous deafferentation. To test whether correction
responses were produced by on-line summation of force fields, we
performed a manipulation that selectively eliminated correction
responses without disrupting wiping reflexes. Cutaneous feedback was
removed from skin areas of the wiping limb in contact with the ankle
restraint. Small incisions were made at several sites around the calf
and foot, and lower-limb cutaneous nerves were dissected free, frozen with a cold copper rod to reduce injury discharge, and transected. We
attempted to evoke flexion withdrawal responses from deafferented skin
regions to test the completeness of the deafferentation. Both light
(dragging sharp forceps) and deep pressure (pinching skin with blunt
forceps) were applied to these skin regions. The skin incisions were
sealed with wound clips and Vetbond. Isometric wiping trials were then
performed 1-2 hr after this procedure, and isometric force vectors
produced during the trials were measured. The wiping limb was held in
the same series of initial positions as when cutaneous feedback was
intact. Despite the fact that muscle afferent feedback was fully
intact, no correction responses could be observed, even after
collisions of substantial velocity.
Bone pin implantation. To control for nonspecific effects of
the cutaneous deafferentation, we performed a number of experiments (n = 5) in which bone pins (Fine Science Tools, Foster
City, CA) were implanted into the distal tibia to immobilize the wiping limb. We used the smallest skin incision compatible with the
implantation procedure so that cutaneous feedback would be minimally
disrupted. In these experiments, we built up a base around the bone
pins with carboxylate cement (Durelon, Norristown, PA) into which we secured a metal standoff. The metal standoff could be attached directly
to the force/torque transducer without any direct skin contact. Such
frogs exhibited typical correction responses in free limb conditions
after obstacle collision. However, if held immobile, no correction was
evoked in the absence of skin contact.
In three of the frogs in which bone pins were used to immobilize the
limb, we examined whether the amplitude and duration of correction
responses depended systematically on the magnitude of obstacle
collision. We used a stepper motor to drive a mass into the heel of the
isometrically held wiping limb with a predetermined velocity (i.e.,
into skin areas where obstacle collisions occurred during free limb
trials). A custom-designed program implemented in DOS controlled the
stepper motor. This program was triggered at the onset of target limb
stimulation via a signal on the parallel port of the computer
controlling the stepper motor. Both the stepper motor velocity and the
latency of impact relative to the onset of target limb stimulation were varied.
To summarize, a typical experiment consisted of (1) ~20 unrestrained
wiping trials with and without path obstacles and with sensory feedback
intact, (2) ~10 trials with the wiping limb immobilized in an ankle
restraint to record endpoint isometric forces and with feedback intact,
(3) ~10 isometric trials after local cutaneous deafferentation of the
wiping limb (so that cutaneous feedback stemming from skin contact with
the restraint was absent), and (4) ~20 unrestrained wiping trials
with and without path obstacles and after the deafferentation. In five
frogs, the limb was restrained via bone pins, thus eliminating any skin
feedback from the restraint without having to deafferent skin regions.
Obstacle contact was produced in three of these frogs by driving a mass
into the isometric limb by a stepper motor.
Data collection
Limb kinematics, EMGs, and contact forces with the rod were
recorded during free limb trials. Movements of the wiping and target
limbs were videotaped at 60 fields per second perpendicular to the
horizontal plane of the wiping movement. A light-emitting diode was
triggered at the initiation of the wiping stimulus and allowed
movements and EMGs to be synchronized within 1-16.67 msec. EMGs were
amplified 1000× and bandpass-filtered (cutoffs 100 Hz and 10 kHz)
using A-M Systems amplifiers (A-M Systems, Everett, WA). EMGs were
analog-to-digital converted using a DAS16 A/D converter and stored on
computer using custom-made software. Forces were sampled at 250 Hz, and
EMGs were sampled at 1000 Hz. During isometric trials, forces generated
at the ankle were recorded by using the same force/torque transducer to
immobilize the ankle. Figure 1 shows the
experimental conditions (with and without local cutaneous deafferentation) and the data types collected (free limb kinematics and
isometric forces; EMGs were collected in both restrained and unrestrained trials).

View larger version (29K):
[in this window]
[in a new window]
|
Figure 1.
The hindlimb to hindlimb wiping trials described
here were evoked in spinalized frogs in two conditions: with sensory
feedback intact and with a local cutaneous deafferentation of the
calf/foot of the wiping limb (shaded area). Wiping was
evoked in all trials by electrical stimulation of the target limb (see
Materials and Methods). Two data types were collected: isometric forces
and free limb kinematics. Joint angles were measured as shown and
converted to engineering format as needed (e.g., for torque
calculations). In trials in which the wiping limb was free to move,
kinematic data were recorded after the wiping was evoked. In trials in
which the wiping limb was restrained, isometric forces were recorded at
the ankle. Hindlimb muscle EMGs were recorded during both trial types
(free limb and isometric) and during both conditions (feedback intact
vs cutaneous deafferentation).
|
|
Data analysis
Kinematic analysis. We examined changes in the free
limb kinematics that occurred during obstacle collision trials. The hip and knee joint locations of the wiping and target limbs (in the horizontal plane of the limb) were digitized from video recordings using a custom-designed program. The joint coordinates from the digitization procedure were imported into the S-Plus Statistics and
Display package (Statistical Science, Seattle, WA). These were used to
reconstruct movement of the thigh and calf and to derive the hip and
knee joint angles over time. Hip angle was measured as the angle
between the longitudinal axis of the frog and the thigh (Fig. 1). Knee
angle was measured as the internal angle between the thigh and calf
(Fig. 1). Because there was little variation in trial-to-trial duration
of the wiping movement for an individual frog, time normalization was
not necessary. Thus, averages and SDs of the hip and knee joint
angles over time were constructed after simply aligning individual
trials at the onset of movement for each condition.
Force analysis (single limb position). We examined
differences in the endpoint isometric forces generated during wiping
trials and between conditions, i.e., when sensory feedback was intact and when skin regions contacting the ankle restraint were deafferented. We first examined differences in the direction and magnitude of force
vectors generated at a single limb configuration. The direction and
magnitude of the wiping force vectors were calculated for a 3 sec
period after the reflex was evoked (wiping motor pattern typically
lasted 600-1000 msec). Endpoint polar force direction was calculated
in the plane of the limb (positive x-axis at 0°, longitudinal axis of frog at 90°) from the measured endpoint force at
time (t) by:
|
(1)
|
where Fy and
Fx are the recorded horizontal force
components over time. The magnitude of the force vectors was calculated by:
|
(2)
|
Averages and SDs of the force direction and magnitude at
each time point after initiation of wiping were constructed by aligning individual trials at the onset of force. The onset of force for each
trial was determined after the averaged baseline force (200 msec before
wiping was initiated) was subtracted from the force record. Both force
direction and magnitude were determined for active forces, i.e., when
resting, baseline forces were subtracted.
On the basis of analysis of EMG patterns (see EMG analysis), we
believed that feedback caused by skin contact with the ankle restraint
initiated a corrective response during isometric wiping trials. We
tested whether correction responses recruited an isometric force-field
primitive and whether this primitive was simply superimposed on the
underlying wiping forces. According to the definition used in this
paper, a force-field primitive is observed as a structurally invariant
force field over time. In its most general form, a force-field primitive would be a function of both position and velocity. In this
paper, we confine ourselves to isometric force measurements at which
velocity is always zero. Other experiments [for preliminary description, see Giszter et al. (2000) ] show, as expected, that velocity plays a role in force-field magnitude. However, because the
limb is brought to rest by an obstacle, the isometric measurement corresponds very well to the forces generated for the initiation of the
correction movement. Under these isometric conditions, at a single limb
position, the force vectors generated by a primitive will increase and
decrease in magnitude with activation-deactivation dynamics of the
primitive but, importantly, will have a fixed direction (Giszter et
al., 1993 ). At the same time, force magnitude ratios among the sampled
limb positions will remain constant, i.e., a primitive's time
evolution can be expressed in the form a(t) (r) (Eq. 3).
That is to say, a constant structure force field is scaled in amplitude
through time in a similar way at all locations. To derive the endpoint
forces generated by the evoked correction response under the hypothesis
that force-field primitives comprised the wiping and corrective
patterns, we therefore proceeded as follows. We subtracted the averaged
force vectors generated during wiping trials alone, i.e., after
cutaneous deafferentation, from the averaged force vectors generated
during wiping trials with an evoked correction response, i.e., with
cutaneous feedback intact:
|
(3)
|
|
(4)
|
|
(5)
|
where FC(r,t) represents
the total forces generated in a corrected wipe over time (t)
at configuration (r) with cutaneous feedback intact. This
field is minimally composed of a sum of primitives (r)
and (r) modulated by time varying scaling parameters b(t) and a(t), where (r) represents
the corrective primitive. FN(r,t) represents the forces
generated after local cutaneous deafferentation (without a correction
response). The subtraction produces a time series of resultant force
vectors FR(r,t) that represent
the endpoint forces specifically associated with the corrective
response. This procedure assumes that the endpoint forces sum linearly
(Mussa-Ivaldi et al., 1994 ). The critical test of our hypothesis is the
behavior and time evolution of the extracted corrective forces. We
expect that the forces FR(r,t) can be expressed in the form b(t) (r) if the correction
represents a force-field primitive as defined above, i.e., forces at
each location have fixed directions, constant magnitude ratios, and similar time evolution.
We first examined the direction of the resultant force vectors
FR(r,t) produced at a single
limb position (direction calculated by Eq. 1) and in some frogs
expanded this to full field descriptions (see below). We measured the
variance of the resultant force directions for each frog tested. For
each frog, there were 6-12 trials, trials were ~800 msec long, and
forces were sampled at 250 Hz. Thus the population of force vector
samples for an individual frog comprised from 1200 to 2400 samples
(0.8 × 250 × 12). Previous data showed that the forces
generated at the ankle during microstimulation recruitment of a
synchronously activated group of muscles exhibited 12° or less
variance in direction (Giszter et al., 1993 , their Table 1). Therefore,
we chose this degree of variance (12°) as our criterion for data to
support the hypothesis that the resultant forces (i.e., correction
response forces) have a fixed direction over time. Force vectors were
examined in these tests in both two and three dimensions. The results
in three dimensions are qualitatively similar to those in two. We have
therefore confined our presentation to the simpler two-dimensional data
with the exception of force-field inner product measures (Eq. 7-10) in
which measures that are presented apply to the three-dimensional force.
We also examined whether the x and y components
of the resultant forces were caused by multi-joint or single-joint
torque components in the plane of the limb. The static joint torques of
the hip and knee were determined from the endpoint forces, limb
position, and link lengths as below:
|
(6)
|
where lt and
lc are lengths of the thigh and calf
and h and k are the
hip and knee angles using the measurement convention in Asada and
Slotine (1986) , Fx and
Fy are the derived resultant force
components in the plane of the limb, and
TH and
TK are the hip and knee torques acting
in the horizontal plane of the limb, i.e., omitting elevator and
rotator hip torques acting out of this plane.
Force-field analysis. Isometric force fields generated with
and without cutaneous feedback intact were examined to test whether a
structurally invariant force field, i.e., a corrective response, was
superimposed on the underlying wiping force field. Force fields were
constructed for each condition as thoroughly described in Giszter et
al. (1993) . Data were time-aligned using the applied stimulus train. No
time dilation was necessary because durations of responses did not vary
across the workspace. Briefly, after a Delauney tesselation, a
piecewise, linear interpolation procedure was applied to the sparsely
sampled field of forces (10-12 wiping trials, each trial at a
different limb position) at each time point after initiation of wiping
(Giszter et al., 1993 ). This procedure allows estimation of force
vectors across the convex region of the sampled workspace over time.
We subtracted the force fields generated after local cutaneous
deafferentation from the force fields generated with all feedback intact at each time point after initiation of wiping (Eq. 3 and 4 applied at each position in the workspace). The force-field subtraction
produces a time series of corrective, or resultant, force fields. We
quantified the similarity of corrective force fields over time. A
detailed description of the comparison procedure is presented in
Mussa-Ivaldi et al. (1994) (Eq. 3-5). Briefly, an inner product
measure is calculated between two force fields:
|
(7)
|
where " " represents the inner product of two vectors.
Ft and
Ft+m denote the two resultant force
vectors that are compared at times t and t + m at N locations
x1, x2,
... xN.
The cosine of the angle between the two sampled fields is calculated:
|
(8)
|
where:
|
(9)
|
represents the norm of a sampled force field. If the correction
is generated by a field, which can be expressed in the form of Equation 5 above, then at two chosen time points (t) and
(t + m):
|
(10)
|
because the scalars b(t) and
b(t + m) determining force magnitude
do not affect the result of the cosine operator in Equation 8. The
value of 1 indicates that the two fields tested are simply scaled
versions of one another. If the value of the cosine measure from
Equation 8 was 0.9 for two test fields, these were considered to have
a similar force-field structure, as described in Mussa-Ivaldi et al.
(1994) . A consistent value of 0.9 over time thus supports a stable
force-field structure over time, as in Equation 5.
EMG analysis. To identify motor pattern changes during
trajectory corrections, EMG signals for individual trials were
rectified and filtered in S-Plus using a moving average filter [30
point, tapered boxcar filter, (Basmajian and DeLuca, 1985 )]. The
rectified, filtered signals were averaged for unobstructed and
obstructed wiping trials. Trials were aligned at the time of onset of
the first muscle (ST) in each frog's respective motor pattern.
Although laborious, onset and offset were determined visually from
rectified and filtered data in S-Plus. We found this more reliable than fixed algorithms using a baseline and noise-based threshold. Within a
frog, EMG bursts determined in this way had low variance (see Table 2).
The magnitude of the EMG envelope (the integrated area under the
rectified, filtered signal) from the time of EMG onset to offset was
determined for each of the 10 muscles. When EMGs were subtracted
between conditions, the variance of the EMG differences was estimated
as the summed variance of the individual conditions. Statistical
differences in the magnitude and onset and offset times of EMG
envelopes between conditions were tested by using standard, paired
t tests implemented in the S-Plus environment.
As stated earlier, we hypothesized that correction responses recruited
a force-field primitive. Force-field primitives are characterized by
structurally invariant force fields over time. Either a single muscle
or a group of coactive and linearly covarying muscles may generate
invariant force-field structures over time (Giszter et al., 1993 ;
Pellegrini and Flanders, 1996 ; Loeb et al., 2000). We examined whether
multiple muscles were recruited during correction responses and whether
these muscles' activations exhibited significant covariation. To test
this, we correlated muscles' rectified and filtered EMG waveforms over
time for correction trials using a standard linear regression algorithm
in S-Plus Statistical Software.
To examine the waveform shape of EMGs and their temporal evolution, we
proceeded as follows. We aligned individual rectified and filtered EMGs
at their peak or initial peak if they exhibited multiphasic activity.
We normalized each EMG to its own peak value and then averaged the
normalized waveforms for each muscle. SDs of the normalized waveforms
were calculated at each time point. As a result of normalization, SD at
peak was always zero.
 |
RESULTS |
Kinematic observations of the trajectory correction response
We first analyzed the kinematic features of corrective responses
during the hindlimb-to-hindlimb form of wiping. These corrections have
never been described in any detail. This kinematic analysis will form
the basis of subsequent analyses. In this form of wiping, when an
irritant is applied to the foot of the target limb, the wiping limb
attempts to reach and remove this stimulus. Figure 2A shows the normal,
free limb kinematics of the wiping and target limbs (i.e., the thigh
and calf of each limb) after we evoked this reflex behavior using our
standard electrical stimulation (500 msec duration, 2 msec biphasic
pulses, 33 Hz, 5 V). The ankle of the wiping limb followed a fairly
direct trajectory to a region caudal to the cloaca where target limb
contact occurred. In the trial shown, target limb contact occurred 233 msec after the onset of wiping limb movement. After contact with the
stimulus on the target limb, the ankle of the wiping limb followed a
trajectory that was directed away from the body of the frog. This final
portion of the trajectory ["whisk"; see Berkinblit et al. (1986) ]
normally acts to remove the stimulus.

View larger version (32K):
[in this window]
[in a new window]
|
Figure 2.
Path obstacles evoked trajectory correction
responses during hindlimb wiping movements.
A-D, Digitized stick figures of the
wiping and target limbs (thigh and calf) and the ankle path of both
limbs (traced by a bold line; arrows mark
direction of movement along path) are shown after initiation of the
wiping reflex in four experimental manipulations. Each stick figure is
separated in time from the next by 16.67 msec ( sec).
Bold stick figures mark the initial limb configurations
and their configuration at target limb contact. The frog's body would
be above each stick figure. A, The unobstructed
kinematics of the wiping limb with feedback intact consisted of a knee
flexion and hip extension that resulted in the ankle moving along a
trajectory directed to a midline region of stimulus contact. A final
knee extension ("whisk") occurred on stimulus contact.
B, When the wiping limb collided with a path obstacle en
route to stimulus contact, a hip flexion was evoked that enabled the
limb to clear the obstacle. Once clear there was an enhanced knee
flexion. Target limb contact occurred at a similar midline site and at
a time similar to unobstructed trials (see Results). C,
After local removal of cutaneous feedback from the wiping limb,
unobstructed free limb kinematics showed no apparent differences from
the kinematics seen with feedback intact (compare A,
C). D, When obstacles were placed in the
path of the locally deafferented limb, corrective responses were no
longer evoked, and the limb was driven further into the obstacle
(compare B, D).
|
|
Spinal frogs exhibited trajectory correction responses when obstacles
were placed in the movement path of the wiping limb. In Figure
2B such a trial is shown. The trajectory of the
ankle, after contact with the obstacle, was redirected toward the head of the frog. This rostral redirection of the ankle trajectory was
caused by a hip flexion, which was not seen in the unimpeded movement.
Once clear of the obstacle, there was an enhanced knee flexion, and the
ankle trajectory exhibited an increased velocity toward the target
region (compare distance between digitized ankle positions).
Interestingly, the time of target limb contact as determined from the
video record was similar to the unimpeded trial. In the frog shown in
Figure 2, the averaged difference in the time of target limb contact
between unimpeded and impeded wiping trials (in successful obstacle
avoidance) was only 30 msec.
In this portion of the study we examined nine frogs that all exhibited
successful correction responses when path obstacles were placed close
to the ankle of the wiping limb, i.e., with obstacles placed ~2-3 cm
or less from the initial position of the ankle. The straight-line
distance from the initial position of the ankle to the site of target
limb contact ranged from 10 to 13 cm for the nine frogs. In each frog,
two common kinematic features characterized successful correction
responses (Figs. 2,
3A,B,
bottom panels): (1) an evoked hip flexion that allowed the
ankle to clear the obstacle and (2) an enhanced knee flexion once the
obstacle was cleared. The enhanced knee flexion allowed the limb to
extend at the hip without further collision and also resulted in an
increased ankle velocity toward the target region. Taken together,
these effects acted to maintain target limb contact times that were
close to contact times in unimpeded wiping trials. In five of nine
frogs there was only a small increase of ~30 msec (significant at
p < 0.05) in the mean latency to target limb contact (mean of 283 ± 20 msec SD with path obstacles compared
with 250 ± 13 msec SD without obstacles) (Table
1). Thus, although there was a small and
significant difference, these frogs were able to maintain contact times
within the extremes of the range of variations seen during unobstructed
trials. However, in the other four frogs there were larger increases
(p < 0.01) in the mean latency to target limb
contact after movement initiation (mean 316 ± 25 msec SD with
path obstacles compared with 245 ± 12 msec SD without). The
increased latency to target limb contact in these four frogs was mainly
attributable to an increase in the time to clear the obstacle (mean
duration of 125 msec in contact with the obstacle in this group
compared with a mean duration of 66 msec in the five frogs with almost
normal movement durations).

View larger version (43K):
[in this window]
[in a new window]
|
Figure 3.
Wiping motor patterns and evoked correction
responses were similar for free limb and isometric trials. Rectified
EMGs are shown for six wiping limb muscles after the wiping reflex was
evoked in four separate conditions: (A)
unobstructed free limb trial, (B) free limb trial
with obstacle collision, (C) isometric trial, and
(D) isometric trial after local cutaneous
deafferentation of the wiping limb. Below the EMG panels in
A and B are shown obstacle contact forces
and hip and knee joint kinematics (in A, there was no
obstacle collision). First and second vertical
lines mark movement onset and target limb contact,
respectively. Below the EMG panels in C and
D are shown the recorded ankle force components
(Fx, Fy, and Fz) and the
derived hip and knee torques. A, The wiping motor
pattern consisted of three phases: initial knee flexor
(ST), subsequent hip extensor
(RI), and final knee extensor (VE)
activation. Hip flexors (IL) exhibited phasic activity
near the time of stimulus contact. B, The timing of
wiping motor phases was unaltered by obstacle collision. Hip flexor
muscles (IL, GL, and SA)
showed a strong synchronous activation after obstacle contact (see
contact force) that ended near the onset of RI. Their activation was
associated with a reversal of hip joint motion to flexion. After
obstacle clearance there was an enhanced knee flexion and resumed hip
extension. C, The time of onset of knee flexor
(ST) and hip extensor phases
(RI) was unaltered during isometric trials. The
knee extensor phase (VE) was absent. Hip flexor muscles
showed a strong activation after the onset of force, which represented
the correction response that ended near the onset of RI. The time of
hip flexor activation was associated with production of a hip flexor
torque (bolded line below), whereas RI activation was
associated with the onset of hip extensor torques. D,
The time of onset of knee flexor and hip extensor phases was unaltered
after local cutaneous deafferentation. Hip flexor activity and hip
flexor torque associated with the correction response were eliminated
by the deafferentation.
|
|
The movement path of the contralateral (i.e., target) limb did not
exhibit any major differences during wiping trials with and without the
path obstacle (Fig. 2), and in this study, we focus only on corrective
changes within the wiping limb.
Trajectory correction responses are evoked by
cutaneous feedback
The sensory basis of the evoked correction response in frogs has
not been described. Muscle, joint, or skin feedback could all
contribute to initiating and controlling the response. We determined
that the correction response in the wiping limb was initiated primarily
by feedback from cutaneous receptors. We could demonstrate this by
local removal of cutaneous feedback from the calf and foot of the
wiping limb alone (see Materials and Methods). The successful
correction responses depended on cutaneous feedback stemming from the
obstacle collision. In the frog shown in Figure 2, after cutaneous
deafferentation, the wiping limb did not exhibit a successful
corrective response and was in fact driven further into the path
obstacle by the extending hip.
Cutaneous feedback, although necessary for evoking successful
correction responses, was not necessary for controlling the unimpeded
free limb trajectory. In Figure 2C, the unimpeded kinematics of the wiping limb are shown after the local cutaneous deafferentation. The kinematics of the wiping limb did not exhibit any major
differences, e.g., in the latency to target limb contact (233 msec), in
its position at target limb contact (knee angle 50°, hip angle
42°), and in the shape of the endpoint path, from the trials in which cutaneous feedback was intact [see also Kargo and Giszter (2000) ]. In
summary then, spinal frogs exhibited smoothly integrated trajectory corrections during hindlimb wiping that were initiated by skin contact
with an obstacle. The removal of skin feedback eliminated successful
correction responses but did not interfere with control of the
unobstructed wiping trajectory.
To show that loss of corrections was not attributable to
nonspecific effects of the loss of cutaneous feedback, we performed a second series of experiments. Rather than using cutaneous
deafferentation, we used bone pins placed in the tibia to immobilize
the limb during the wiping reflex just as an obstacle would, but
without skin contact. At the same time, skin sensory fields were
largely undisturbed. We were unable to initiate corrective EMGs during
isometric holds (see below) in this arrangement in the absence of
cutaneous contact. However, true collisions evoked corrections. These
approaches allowed us to manipulate wiping and corrective responses in
isometric experiments.
Basis for isometric examination of wiping and
correction responses
In the following sections, we tested whether the observed
correction response forces
FC(r,t) were generated by the
on-line superposition of a structurally invariant, corrective force
field with an underlying wiping force field. Specifically:
|
(11)
|
where FN represents the normal
pattern of forces over time (t) at position (r)
activated by the skin stimulus on the contralateral limb and
FR represents the force-field
primitive activated by ipsilateral obstacle contact. To test this
hypothesis we recorded the endpoint isometric forces generated during
wiping and trajectory correction responses. Previous studies have shown
that forces and EMGs appropriate for wiping can be evoked in the
isometric limb (Giszter et al., 1993 ; Giszter and Kargo, 2000 ). We
wished to test the organization of correction responses using isometric methods. To do this we needed to establish the similarity of motor patterns for wiping and correction responses in free limb and isometric
conditions. We therefore analyzed the motor patterns evoked under each
condition in the same frog using EMG recordings.
Free limb EMG patterns generated during wiping and
trajectory corrections
We first examined the basic motor pattern that occurs during free
limb wiping trials. The normal wiping motor pattern consisted of three
periods of muscle activity (for detailed analysis, also see Kargo and
Giszter (2000) ]: an initial phase dominated by knee flexor activity
(ST and BI), a second phase during which the hip extensors (RI, SM, and
AD) become activated, and a final phase during which the knee extensors
(for example, VE) become activated. The first two phases contribute to
the hindlimb trajectory up to target limb contact (i.e., the aimed
portion of the wipe), and the final phase is initiated around the time
of target limb contact. Figure 3A shows the rectified EMGs
of six muscles in the wiping limb during individual trials without a
path obstacle. The corresponding hip and knee joint angles of the
wiping limb are shown below the EMGs. Figure 3B shows the
effect of an obstacle on this motor pattern and joint coordination.
A specific group of hindlimb muscles was commonly activated in response
to obstacle collision during free limb wiping trials. With obstacles
placed 2-3 cm from the initial position of the ankle, collisions
occurred during the initial knee flexor phase (see contact force below
EMGs in Fig. 3B). In the frog shown in Figure
3A,B, a group of hip flexor-related
muscles (IL and GL, monoarticular hip flexors, and SA, a hip/knee
flexor) were reflexively activated ~15 msec after obstacle contact.
The duration of their activation was ~150 msec. The reflex activation
of these muscles did not appear to interfere with or cause variation of
the onset times of subsequent wiping motor phases (see section entitled Correction responses are generated by addition of a muscle synergy to
the basic pattern and Table 2). None of
the comparisons of motor pattern latency differed significantly between
correction and free limb, unobstructed trials.
Motor patterns are similar under isometric conditions
After evoking a series of free limb wiping trials in each frog, we
immobilized the wiping limb using our ankle restraint. This apparatus
allowed us to examine isometric forces and force-field patterns. We
again recorded EMGs and also isometric forces generated at the ankle
after evoking the wiping reflex. We found that the initial knee flexor
phase and the subsequent hip extensor phases of the wiping motor
pattern were initiated in all frogs and remained similar to free limb
patterns (see Fig. 3C, restrained trial, and
compare with Fig. 3B, free limb trial with correction). The hip extensor phase maintained a similar time of onset relative to knee
flexor onset in eight of nine frogs (Table 2). With the exception of
bf74, the ST to RI latency did not differ significantly between free
limb, correction, and isometric tests. However, in the majority of
frogs (eight of nine), the usual, final phase of knee extensor
activation was absent (Fig. 3C,D). In the
one exception, the knee extensor phase was much reduced, although present. Loss of knee extensor activation was often associated with a
more abrupt termination of knee flexor and hip extensor EMG activity
(compare ST and RI EMGs in Fig. 3C,D,
isometric, with Fig. 3A,B, free
limb). The lack of the knee extensor burst representing initiation of
the final motor phase suggests that either triggering or aborting of
this phase of the motor program may occur based on successful or
unsuccessful achievement of target limb contact and/or a specific
wiping limb configuration. These observations are compatible with the
kinematic observations reported in Giszter et al. (1989) . Despite the
similarity of timing between isometric and free limb conditions, there
were some amplitude variations in EMGs in isometric conditions. These
are analyzed elsewhere.
We also examined the EMGs recorded during isometric wiping trials to
assess whether the ankle restraint evoked a correction response during
wiping. The ankle restraint was placed in contact with the same skin
areas (~2-3 mm above the ankle) upon which obstacle collision
occurred during the free limb trials. We found that the same hip
flexor-related muscles that were activated after obstacle collision
during free limb wiping were activated during isometric wiping in our
tested frogs. In the frog shown in Figure 3C,D, these hip flexor muscles were
activated during the initial knee flexor phase, ~90 msec after ST
onset and 65 msec after force onset (average onset time of 55 ± 11 msec relative to first measured force onset for the nine frogs taken
together). The evoked EMG activity always ended close to the onset of
the hip extensor phase. In fact, in eight of nine frogs of this study,
the duration of activation of these muscles during isometric trials was
similar to their duration of activation during collisions in free limb trials, e.g., the averaged duration of the evoked IL EMG during free
limb trials was 154 ± 16 msec, whereas in isometric trials it was
165 ± 20 msec (Table 2) (p > 0.1).
In addition to the EMG similarities, correction responses initiated
during isometric wiping could be abolished by cutaneous deafferentation
(Fig. 3D), similar to free limb trials. The deafferentation eliminated pertinent skin feedback caused by contact with the ankle
restraint. In the frog shown in Figure 3D, the IL, SA, and GL EMGs no longer exhibited a strong, phasic activation after cutaneous
deafferentation. However, the knee flexor and hip extensor phases of
the wiping motor pattern were clearly unaffected and had similar onset
and offset times. An examination of the derived hip and knee torques
generated during isometric trials showed the torque patterns produced
when cutaneous feedback was intact and when this feedback was
eliminated by the deafferentation procedure (Fig.
3C,D, bottom panels). With
feedback intact, a hip flexor torque was initiated soon after the
initial knee flexor torque and was associated with the onset of IL, GL,
and SA. After removal of cutaneous feedback, this strong hip flexor
torque was absent, as were the enhanced activities of IL, GL, and SA.
The wiping motor pattern also involved a substantial
z-direction force (Fig. 3C,D).
Variations in the z-force associated with corrections were small (Fig. 3, compare C and D,
Fz).
In summary, our analysis showed that wiping motor patterns can be
initiated in the isometric limb, and these differ primarily only in
amplitude from free limb EMGs. The first two phases of the motor
pattern, the initial knee flexor (ST and BI) and subsequent hip
extensor (RI, SM and AD) phases, had similar onset times as in the free
limb. A different report (Giszter et al., 2000 ) documents in detail the
differences between free limb and isometric wiping trials and the role
of proprioceptive feedback in force-field structure within a phase of
the motor pattern. When cutaneous feedback was left intact during
isometric trials, the ankle restraint acted like a path obstacle and
evoked a correction response. The same set of muscles activated during
free limb trajectory corrections was activated during isometric
corrections and with a similar duration (Fig. 3, compare B
and C). Last, the correction response could be eliminated by
local cutaneous deafferentation of the ankle/calf region without
affecting the timing of the underlying wiping motor phases.
In the following sections we exploit our observation that wiping and
correction motor patterns appear conserved in the isometric limb. We
used this to test the hypothesis that on-line superposition of force
fields underlies the generation of trajectory corrections during
wiping. We test this first at a single limb position and then at
multiple limb positions.
Superposition of isometric endpoint forces underlies
trajectory corrections
We examined the endpoint forces generated during wiping trials
with cutaneous feedback intact, i.e., when correction responses were
evoked, and after cutaneous deafferentation at a single, standard limb
position (hip 90°, knee 105°) in nine frogs. In each frog, when
cutaneous feedback was intact we observed a temporal pattern of
endpoint forces similar to those shown in Figure
4B. We plotted both the
angular directions and amplitudes of force vectors over time. Figure
4C shows the directions, expressed as an angle, over time in
each condition. Figure 4D shows the magnitudes. We
also expressed the angular variations of force direction as distributions in circular histograms (Fig.
5). In the frog shown in Figure
4B, the force vectors generated by the wiping limb
after evoking the wiping reflex were initially directed toward the
midline (~160°), where target limb contact normally occurs, and
remained in this direction for ~75 msec (Fig. 4B,
WCF). The forces then began to rotate toward the head
of the frog over the next 150 msec. This continuous rostral rotation
immediately followed the activation of IL, a hip flexor, and SA, a
hip/knee flexor (averaged period of activations shown in Fig.
4E as bars). At the onset of the hip
extensor burst (RI), the endpoint forces rotated in an opposite
direction, away from the frog, and back toward and through the target
region. They stabilized at a final direction of ~260° (measured
counterclockwise and relative to horizontal, 0°) (Fig.
4C).

View larger version (25K):
[in this window]
[in a new window]
|
Figure 4.
Cutaneous reflex pathways recruited a
fixed-direction force component that summed with an underlying sequence
of forces generated during wiping. In this figure, time is referenced
to stimulus onset. A, Force vectors in B
are plotted with respect to the frog shown. Thus, vectors pointing to
the left of the page are pointing to the midline of the
frog. The force vector shown here represents the scale for
B. Vector directions in C and Figures 5
and 6 are referenced relative to the axes in this panel.
B, Isometric force vectors are shown at 20 msec
intervals after initiation of wiping for two conditions (top two
rows; WCF, with feedback intact;
NCF, no cutaneous feedback). Forces in
each condition represent an average of seven trials. In a correction
response (WCF), force vectors were initially
directed to the midline, rotated rostrally toward the hip, and then
rotated back to and through the midline to caudal directions. In the
absence of a correction (NCF), force vectors were
initially directed to the midline for 200 msec and then rotated
caudally. In the third row, vectors, C, produced by a
subtraction of NCF vectors from WCF vectors are shown. These vectors
represent the correction response. Note that these appear uniformly
directed. C, Angular directions (see A)
of the force vectors for the two conditions and for the correction
vectors are shown at 4 msec intervals. In all trials
(WCF and NCF), force vectors were
initially similarly directed to 180°. In corrections
(WCF), force vectors rotated to ~140°,
whereas NCF vectors remained fixed in direction. In both
cases (WCF and NCF), force vectors
then rotated caudally at around the same time to a direction of 260°.
Corrective, C, vectors as noted in B
remained stable in time. D, Vector magnitudes are shown
over time. With no correction (NCF), force
vectors exhibited a biphasic pattern of growth. Each phase is
associated with a period of fixed-direction force production as shown
in B. In corrections (WCF),
initial phase of vector growth is increased because of the summation of
C vectors along a similar direction. The second phase is decreased
because correction and wiping vectors are oppositely directed. C
vectors show a monotonic increase and decline. E,
Bar plots representing the averaged period of activation
of ST, RI, IL, and SA EMGs are shown. The horizontal
bars at each end represent ±1 SD. With feedback intact, the onset of IL and SA activation
was associated with the onset of the rostral force rotation. After
cutaneous deafferentation, IL and SA activation were absent, as was the
rostral rotation of forces. RI onset was similar in both conditions and
associated with the onset of caudally rotated forces.
|
|

View larger version (37K):
[in this window]
[in a new window]
|
Figure 5.
Corrective force components are directionally
stable. A-C, Circular histograms of the directions of
force vectors generated over wiping in five trials (600 msec duration
trials, 250 Hz sampling rate; thus ~750 samples total) are shown for
each condition: with feedback and correction response
(A) and without cutaneous feedback or a
correction response (B). The derived corrective
vectors are shown in C. Each bin represents 12°. See
D for orientation of the circular histograms to the
frog's body and wiping limb. A, With feedback intact,
vector directions exhibited two clusters: an initial cluster directed
toward the midline and a second cluster directed away from the frog.
The first cluster was broadly spread and spanned four bins.
B, Without cutaneous feedback, the initial cluster of
vector directions was more focally distributed to the midline, i.e.,
mainly in one bin (78-90°), whereas the second cluster of forces was
similar to that with feedback intact (252-264°). C,
Corrective vectors were obtained by subtracting time-matched forces in
B from A. The directions of the
corrective vectors clustered tightly in a single bin from 108 to 120°
and were directed to the hip joint. Thus, the corrective vectors summed
with the initial set of wiping vectors directed to the midline and
resulted in the rostral spread of these midline-directed force clusters
when feedback was intact.
|
|
After local removal of cutaneous feedback, the pattern of forces
generated by the wiping limb consisted of only two sequentially activated and uniformly directed force components (Fig.
4B, NCF). These could correspond to
stable force fields in each phase. In the absence of a corrective
response, the initial forces after the wiping reflex was evoked grew in
magnitude along a uniform direction (~160°) for ~200 msec (Fig.
4B,C). As the hip extensor burst
was activated, the forces rotated away from the frog and reached a
second set of uniformly directed forces (~260°) for the remainder
of the period of RI activation. There was no period of IL/SA activation
and no corresponding rostral rotation of endpoint forces without
cutaneous feedback.
We analyzed the distribution of the force directions expressed as
angles (as in Fig. 4C) that were generated during wiping trials both with and without cutaneous feedback intact. After cutaneous
deafferentation, i.e., no correction response, the force directions
clustered into two discrete subgroups (Fig. 5B). The forces
in the initial (midline-directed) subgroup were contained mainly within
a single 12° bin directed to 168-180° (mean direction of 175 ± 5 SD). Forces in the second (caudally directed) subgroup were mainly
contained within two bins directed to 252-276° (mean direction of
261 ± 7 SD). When feedback was intact (Fig. 5A), the
initial subgroup of forces directed toward the midline was more broadly
distributed than the corresponding initial subgroup of forces produced
when cutaneous feedback was removed (average direction of 156 ± 13 SD) (Fig. 5A). The subsequent caudal subgroup of forces
with feedback intact was similarly directed to the corresponding caudal
subgroup produced with cutaneous feedback removed, although the
variance was greater (mean direction of 258 ± 13 SD).
We hypothesized (Eq. 10; also see Eq. 4 and 5) that differences in the
variance and direction of the initial subgroup of forces produced with
and without cutaneous feedback intact were caused by differences in the
contribution of two fixed-direction force components (i.e., of low
directional variance). When cutaneous feedback was intact, a corrective
force component was activated and summed through time with an initial
wiping component. This summation resulted in the rostral rotation and
increased variance of the midline-directed force vectors. To test this,
we subtracted the time series of force vectors that were generated when
cutaneous feedback was removed from the force vectors that were
generated at the corresponding times with feedback intact. We examined
the time-varying pattern of resultant (corrective) forces, i.e.,
direction and magnitude. These are shown in Figure
4B-D (series marked C). In the
frog shown in Figures 4 and 5, the corrective force vectors exhibited a
monophasic increase and decrease in amplitude and were uniformly
directed to ~115° during the period of IL/SA activation (Fig.
4C,D). The distribution of the corrective force
directions over time showed low variance (Fig. 5C).
Eighty-one percent of the corrective vectors (n = 675 vectors; 5 trials × 135 force samples; 540 msec long trials)
were contained in a single bin (118-130°). The mean direction was
120°, and the SD was only 3°.
To summarize, cutaneous feedback triggered the activation of a
fixed-direction force component associated with a correction response.
This corrective component summed with an ongoing force component
produced during the initial phase of wiping. The subsequent onset of
the hip extensor phase of wiping was associated with the production of
a final, fixed-direction force component. Thus these data indicate that
three fixed-direction force components are activated both synchronously
and sequentially to generate correction responses during wiping. This
applies to isometric conditions and when testing at a single configuration.
We examined how the force component recruited during correction
responses varied among frogs. Polar plots of the distributions of
corrective force directions are shown for four frogs in Figure 6A. The limb posture at
which the wiping trials were evoked is shown in the inset of
Figure 6A (90° hip and 105° knee angles) and was
the same for each frog. For six of nine frogs tested, a large
percentage (>80%) of the corrective forces over time (and for
multiple trials) were contained in a single bin. For each of these
frogs, the variance of the corrective force directions was <12°. In
addition to the uniformity of corrective force directions over time for
each frog, the corrective vectors were similarly directed among frogs
(the modal bin for all frogs lay within a 30° segment).

View larger version (25K):
[in this window]
[in a new window]
|
Figure 6.
Cutaneous reflex pathways that signal obstacle
contact recruited similar corrective force components among frogs.
A, Circular histograms of the directions of corrective
forces over time are shown for four frogs (obtained as described in
Figs. 4 and 5 and Materials and Methods). For each frog, the collection
of corrective force directions clustered mainly within one bin and the
modal bins for each frog in the group were localized within a 36°
segment (from 84 to 120°). B, The averaged corrective
hip and knee torques are shown for each of the four frogs shown in
A. Knee and hip torques are normalized to the maximal
hip torque produced for each frog. For each frog, the corrective forces
were produced by a multi-joint torque response. In addition, in each
frog the knee to hip torque ratios were constant over time (linear up
to the peak corrective force). The small variability among frogs in the
direction of corrective forces was related to the magnitude of the
ratio of knee flexor torque to hip flexor torque, and in some frogs
(bf65) also to the direction of the knee torque component, e.g.,
extensor versus flexor.
|
|
The other three frogs showed deletions of the extensor phase. Extensor
phase deletions will not be further pursued here but are reported in
more detail in Giszter and Kargo (2000) .
A hip flexion torque was primarily responsible for generating the
corrective endpoint forces. Figure 6B shows the
balance of corrective knee torque versus hip torque, displayed from the onset of corrective force up to the peak corrective force. In each
frog, there was an almost constant ratio of hip flexion torque to knee
torque over time. This constant joint torque ratio resulted in the
uniformly directed corrective forces. However, the direction (flexor vs
extensor) and relative magnitude of the corrective knee torque
exhibited some variability among frogs (knee torques are normalized to
peak hip torque in Fig. 6B). In four of six frogs, a
corrective knee flexion torque accompanied the hip flexion torque. In
the other two frogs, there was a small knee extensor torque component.
This variability may be related to differences among frogs in the
coactivation of other muscles in addition to monoarticular hip flexors
(IL and GL) during correction responses. For instance, SA, a hip
flexor/knee flexor, and RA, a hip flexor/knee extensor, were both
commonly activated during corrective responses. The balance of these
muscles' activations would then determine the resulting knee torque.
We examine in more detail the EMGs underlying corrective responses (in
the sections entitled Correction responses are generated by addition of
a muscle synergy to the basic pattern and Muscles recruited during
correction responses exhibit covariation).
Superposition of isometric force fields underlies
trajectory corrections
Although the correction responses at a single location showed
clear superposition of forces, this guarantees nothing about the forces
generated at other configurations or the stability over time of a
force-field primitive. We therefore examined the force fields generated
during wiping trials with and without cutaneous feedback intact, i.e.,
with and without evoked correction responses. Force fields were
constructed by measuring the isometric forces generated at a range of
initial limb positions. Thus, force-field measurements describe the
configuration-dependent effects of both muscle actions and changes in
muscle activation (caused by changes in proprioceptive feedback).
Conceivably, responses might differ radically across the workspace, and
field structure might be complex or divergent.
In Figure 7, a time series of force
fields generated by the wiping limb with cutaneous feedback intact
(Fig. 7A) and after cutaneous deafferentation (Fig.
7B) are shown for one frog. The force fields were initially
similar between conditions. Approximately 90 msec after the onset of
force, the force fields began to exhibit apparent differences. With
feedback, intact force fields rotated rostrally toward the hip joint,
whereas force fields produced with no cutaneous feedback continued to
grow in magnitude and remained directed toward the midline region of
stimulus contact. The time points at which the force fields are shown,
i.e., 130-330 msec at 40 msec intervals, are marked as successive
vertical lines on an EMG record collected at a single, central location
in the workspace (Fig. 7; EMG record to the right of each
force-field series). The EMG record includes four muscles that
represent the knee flexor phase (BI), the hip extensor phase (RI), and
the corrective response (IL and RA). The alteration in force-field
structure between conditions was associated with the reflex activation
of IL and RA when feedback was intact, i.e., a correction response.

View larger version (56K):
[in this window]
[in a new window]
|
Figure 7.
Cutaneous reflex pathways signaling obstacle
contact recruited a corrective force field that summed with an
underlying force-field sequence produced during wiping. Time series of
force fields are shown after initiation of wiping both with feedback
intact and after cutaneous deafferentation. A typical EMG pattern of
representative muscles associated with field generation is shown to the
right of each time series. For the fields, a single
vector represents the force generated at that position at the specified
latency after wiping initiation. The black dot marks the
location of the hip joint. The lightly shaded ellipse
indicates the region of contact with the target limb in free limb
trials. A, With feedback intact, force fields were
initially directed to the midline where target limb contact normally
occurred (bold line overlaid on the 130 msec field shows
the unrestrained ankle path up to limb contact. At 210 msec up to 330 msec, force fields rotated rostrally toward the hip and away from the
target region. At 330 msec, force fields began to rotate back to the
target region. The hip extensor burst began around this time (see EMG
record to the right; rectified EMGs from
BI knee flexor, RI hip extensor, and
IL/RA-hip flexors are shown for a single
trial taken from the middle of the workspace). B, After
removal of cutaneous feedback, initial force fields were directed to
the midline. Subsequent fields (210-330 msec) converged to the target
region and did not rotate to the hip joint. The strong IL/RA activation
was absent without cutaneous feedback (see EMGs to the right). At 330 msec, the field began to rotate caudally because of hip extensor
activation. C, Procedure used to produce corrective
force fields. Time-matched fields in B were subtracted
from corresponding fields in A. The procedure was
performed at each time point after wiping initiation. D,
Corrective fields are shown at three times, at 40 msec intervals.
Corrective fields were structurally similar (similarity measures > 0.95) over a 100 msec period starting shortly after IL EMG onset.
These rostrally directed fields summed with the underlying wiping force
fields.
|
|
We hypothesized that the alteration in force-field structure was caused
by the reflex activation and superposition of a structurally invariant
corrective field on a wiping field. To examine the time-varying structure of the corrective force fields, we subtracted vector fields
between conditions (feedback intact fields feedback removed fields; procedure graphically represented in Fig. 7C). In
Figure 7D, corrective fields are shown at three successive
time points (130, 170, and 210 msec after force onset). We used a
correlation method to examine the similarity of corrective force fields
over a 200 msec interval (IL and RA were activated for ~200 msec)
starting at 90 msec after force onset [see Materials and Methods,
Mussa-Ivaldi et al. (1994) ]. Over this time period, the correlations
between corrective field structures at any two time points were 0.95 or larger. This high correlation measure between field structures suggests
that the corrective force fields over time represent scaled versions of
a structurally similar force field. This is in keeping with the low
variance of corrective force directions at a single limb position
described in Superimposition of isometric endpoint forces underlies
trajectory corrections. In addition, it shows that the force magnitude
ratios across the limb's workspace are relatively constant during the
period of the corrective response. The constant structure of the
extracted, corrective force field over time implies uniform temporal
dynamics at all positions. This and the smooth unimodal rise and fall
of its force magnitude at each location (Fig. 4) are both consistent
with the hypothesis of force-field summation. All tested frogs showed
the high correlations (>0.9) for corrective force-field structure over
time (i.e., structure was conserved in the field resulting from the
vector subtraction procedure). Finally, we found that the
corrective and wiping force fields were similar among tested frogs
(n = 4).
In summary, we addressed configuration-based variations in forces and
corrective responses by measuring entire force fields. Examination of
these force fields showed that trajectory corrections were generated by
a dynamically evolving force-field structure. Our subtraction procedure
showed that this dynamic force-field evolution was generated by
combining the force-field primitive evoked in the correction response
with the force-field primitives associated with the wiping reflex.
Correction responses are generated by addition of a muscle synergy
to the basic pattern
The data above suggest that cutaneous feedback triggered the
activation of a force-field primitive. This corrective force field sums
with and does not disrupt the underlying wiping force-field sequence.
In this section, we examine directly whether muscle activation
triggered by obstacle collision sums with and does not disrupt the
ongoing wiping motor pattern.
We found that two to three hip flexor-related muscles were activated in
response to obstacle collision in each of the nine frogs tested in free
limb conditions. The activation of these muscles was added to and did
not interfere with the underlying motor pattern (Table 2; see list of
reflexly activated muscles). In Figure
8A,B,
rectified, filtered, and averaged EMGs (n = 11 trials
per condition) are shown for one frog during unobstructed, free limb
wiping trials (bold lines, thin lines, 1 SD above
and below average, respectively) and for obstacle collision trials, respectively (similar convention). The obstacle was placed next to but
not touching the wip |