JOURNAL OF NEUROTRAUMA
Volume 19, Number 10, 2002
© Mary Ann Liebert, Inc.

Recruitment of Spinal Motor Pools during Voluntary
Movements versus Stepping after Human Spinal Cord Injury
M. MAEGELE,1 S. MÜLLER,2 A. WERNIG,1 V.R. EDGERTON,3,4,5 and S.J. HARKEMA3,6

ABSTRACT
We investigated the activation of lower limb motor pools by supraspinal and spinal networks after
human spinal cord injury (SCI). We compared electromyographic (EMG) activity from six muscles
during voluntarily attempted non–weight-bearing single-joint movements, multijoint movements approximating stepping in a supine position, and weight-bearing stepping on a treadmill with bodyweight support (BWST) in seven clinically incomplete and three clinically complete SCI subjects.
Seven SCI subjects had previously completed Laufband therapy (a specific step training using variable levels of body weight support and manual assistance). Significant coactivation of agonists andantagonists and multijoint flexion or extension movements of the entire limb occurred during attempts at isolated knee or ankle single-joint movements in clinically incomplete SCI subjects. Further, some muscles that were not recruited during voluntary attempts at single-joint movements
were activated during voluntary step-like multijoint movements (5/16 comparisons). This suggeststhat the residual voluntary motor control in incomplete SCI subjects evokes more generalized motor patterns (limb flexion or extension) rather than selective activation of individual muscles. Clinically incomplete and clinically complete SCI subjects could achieve greater activation of motor
pools and more reciprocal patterns of activity between agonists and antagonists during weight bearing stepping than during non–weight-bearing voluntary movements. The EMG mean amplitudes
were higher during stepping than during voluntary movements in 50/60 muscles studied (p , 0.05).
These results suggest that stepping with knee and hip extension and flexion and alternating lower limb
loading and unloading provides proprioceptive inputs to the spinal cord that increases motor recruitment and improves reciprocity between agonists and antagonists compared to voluntary efforts.
Key words: coactivation; Laufband therapy; locomotion; locomotor training; motor recruitment; proprioception; spinal cord injury
INTRODUCTIONTHE SELECTION AND LEVEL OF ACTIVATIO N of the lower

limb motor neurons can be modulated effectively bydescending supraspinal input to the lumbosacral spinal

cord in humans. After spinal cord injury (SCI), the functionality of descending control of motor pools is estimated from movements that the individual can volitionally generate in selected muscle groups. This motor
output is also routinely used as a predictor of the level

1 Department of Physiology, University of Bonn, Bonn, Germany.
2 Klinikum Karlsbad–Langensteinbach, Karlsbad, Germany.

The 3Brain Research Institute, 4Department of Physiological Sciences, 5 Department of Neurobiology, and 6Department of Neurology, University of California Los Angeles, Los Angeles, California.

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MAEGELE ET AL.
of ambulation that will be regained after neurological injury (Crozier et al., 1992; Hussey and Stauffer, 1973; Waters et al., 1989, 1993, 1994). The assumption implied bythis assessment is that the limitation in the level of voluntary control of individual muscle groups of the lower
limbs is the only factor that predicts locomotor capacity.
Acceptance of this assumption then presumes that thesensory input associated with load-bearing stepping is oflimited functional relevance in the ability to executestanding and stepping.
However, sensory input plays an essential role in regulating both the level of activation and the coordinationof motor pools involved in stepping as demonstrated bya wide range of studies in laboratory animals (Andersson
and Grillner, 1981, 1983; Barbeau et al., 1993; Barbeau
and Rossignol, 1987; Conway et al., 1987; de Leon et al.,1998a; Duysens and Pearson, 1980; Gossard and Hultborn, 1991; Grillner and Rossignol, 1978; Grillner andZangger, 1979; Lovely et al., 1986; Pearson and Duysens, 1976). Although sensory input derived from themuscles, tendons, joints and skin of the lower limbs ofhumans can influence the mechanics of load-bearing
stepping, it is not known whether this influence is dependent on simultaneously occurring voluntary control
from supraspinal centers (Aniss et al., 1992; Burke et al.,
1991; Capaday and Stein, 1986; Crenna and Frigo, 1987;
Duysens et al., 1990; Yang and Stein, 1990). Evidence
from severely impaired SCI subjects suggests that thelevel of activation of motor pools involved in stepping
using body weight support on a treadmill (BWST) canbe influenced significantly by peripheral sensory input(Barbeau 1987; Barbeau and Blunt, 1991; Dietz et al.,
1994, 1995, 1998a,b; Dobkin et al., 1995; Harkema etal., 1997; Stewart et al., 1991; Wernig and Müller, 1991,
1992; Wernig et al., 1995, 1999, 2000).
We hypothesized that the level of activation of motor
pools during load-bearing stepping exceeds the level thata severely injured individual following SCI can develop
voluntarily without limb loading. We compared the EMG
from six lower limb muscles of SCI subjects during
voluntarily attempted non–weight-bearing single-joint
movements, multijoint movements approximating stepping in a supine position, and weight-bearing stepping
using BWST. Clinically incomplete and clinically complete SCI subjects demonstrated a greater level of motor
neuron activation and less coactivation among antagonistic muscles during load-bearing stepping than during
voluntary attempted movements. We also found that multiple muscle groups were activated (flexion and extension and even multiple joints) when single-joint flexion
or extension movements were intended in subjects with
reduced descending activity following SCI. These data
demonstrate that step-associated proprioception can co-ordinate spinal motor pools in an effective temporal sequence and at an adequate level of activation for generating stepping even when an individual is not able to voluntarily execute similar motor patterns in defined resting
positions.

MATERIALS AND METHODS
Subject Population
Ten SCI subjects (eight male, two female; 13–61 years;
29–87 kg) volunteered for this study. Clinical characteristics of all subjects are summarized in Table 1. A clinician classified the subjects with the use of the American
Spinal Injury Association (ASIA) impairment scale,
which categorizes individuals by their sensorimotor function below the level of lesion and designates a cumulative motor score (Ditunno et al., 1994; Maynard et al.,1997). In brief, the ASIA impairment scale classifies individuals as follows: A 5 Complete—no motor or sensory function is preserved below the lesion including
the sacral segments S4-S5; B 5 incomplete—sensory but
not motor function is preserved below the neurologicallevel and includes the sacral segments S4-S5; C 5
incomplete—motor function is preserved below the neurological level, and more than half of the key muscles
below the neurological level have a muscle grade lessthan 3; D 5 incomplete—motor function is preserved below the neurological level, and at least half of the key
muscles below the neurological level have a muscle gradeof 3 or more; or E 5 normal—motor and sensory function is normal. In one subject (A10), transcranial magnetic stimulation of the motor cortex and sensory evoked
potentials (recorded from the popliteal fossa, lumbar
spine, and scalp during tibial nerve stimulation) both reported absence of detectable supraspinal conductivity to
the lower limbs.
Motor function and ambulatory status before and after
Laufband therapy is summarized in Table 2. Some characteristics from these subjects presented here have previously been reported (Wernig et al., 1995, 1999). A recently established functional locomotor assessment (EUWalking) was performed (Wernig et al., 1995, 1999). In
brief, walking capability was tested by assessment ofwalking with and without assistive devices by three independent observers. EU Walking defines functionalclasses: 0 5 cannot walk even with moderate help of two
therapists, 1 5 can walk with moderate help of two therapists, 2 5 can walk at the railing with active help by one
therapist, 3 5 can walk without help by other persons using a rollator/walker, 4 5 can walk independently using
two canes, 5 5 can walk without devices. Classes 0–2 indicate dependence on help by others, and 3–5 indepen-

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RECRUITMENT OF MOTOR POOLS AFTER SCITABLE 1. CLINICAL C HARACTERISTICS OF SUBJECTS STUDIED

Subject(code)

Sex

Age(years)

Weight(kg)

Injurylevel(segment)

A8
A9
A10
C1
C5
C6
D1
D2
D3
D4

F
M
M
M
M
M
M
F
M
M

13
61
23
43
31
24
24
57
32
53

29
80
71
82
80
72
85
70
78
87

Th 7
C4
Th 5
Th 8
C4
C6
C4
Th 6
C4
C5

Lower limb
motor score

Time postinjury(years)

Etiology

ASIA
class

Left

Right

1
4
3
3
5
8
1
2
3
5

TraumaTraumaTraumaIschemia
TraumaTraumaTraumaVascular disorder
TraumaDisc protrusion

A
A
A
C
C
C
D
D
D
D

0
0
0
0
5
4
7
20
25
20

0
0
0
10
0
6
17
17
20
25

Th, thoracic; C, cervical.

dence for locomotion as defined. Reliability (reliability
index/interrater consistency/K 5 0.84) was determinedby comparing the independent assessments of 61 film sequences by two investigators (Cohen, 1960). The inability to use walking devices in quadriplegics due to severe
arm paralyses was assessed separately, since it may limit
the rating of such patients to classes 1 to 2 regardless oflower limb function. In this study, some subjects had
moderate (C5 and D3) or severe (D1 and D4) difficulties
in holding assistive devices such as canes or walkers due
to upper extremity paralysis (Table 2). Also, the Cumulative Muscle Index (CMI) scored voluntary activity indefined resting positions on a scale from 0 to 5 (with halfvalues in between; Kendall et al., 1993) for the gluteals(maximus and medius/minimus), iliopsoas, sartorius,
quadriceps, ischiocrurales, triceps surae and tibialis anterior. This index differs from the ASIA classification in
the specific muscles tested and is not limited to key muscles for a given segment. The CMI is restricted to thelower limb muscles so that in quadriplegics CMI values
may be high while EU Walking scores may not exceed
1 (individuals need moderate assistance from two people
to walk) because of arm weakness.
Experiments were performed at the Klinikum Karlsbad-Langensteinbach, Germany (subjects A8-A10; C5C6; D1-D4) and at the University of California Los
Angeles (subject C1). The Klinikum Karlsbad-Langensteinbach and the University of California at Los Angeles Human Subjects Protection Committees approved all
experiments and all procedures were within the guidelines of the code of ethics of the World Medical Association. Each subject signed an informed consent form prior
to the experiments.

Experimental Design
We measured EMG activity and joint kinematics during volitionally attempted single- and multijoint movements without limb loading and during stepping withTABLE 2. EU WALKING AND THE CUMULATED MUSCLE INDEX FOR SUBJECTS THAT COMPLETED LAUFBAND THERAPY
CMI, right

CMI, left

Subject(code)

EU(pretraining)EU(posttraining)

BeforeAfter

Before

After

A8
A10
C5
D1
D2
D3
D4

0
0
0
1
1
2
2

0
0
0*
2**
4
4*
3**

0
0
7.5
9
24
28
10

0
0
8.5
9.5
26
27
10.5

0
0
0
15.5
9.5
11
14

0
0
0
16
10.5
10.5
14

The *moderate or **severe difficulties in holding assistive devices are due to upper extremity paralysis and have a restrictive
effect on independent ambulation.

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MAEGELE ET AL.
manual assistance using BWST. During volitionally attempted single-joint movements at rest without limb
loading, the subjects were lying on their side to neutralize gravitational effects on extensor-flexor movements.
The trainer held the leg in a neutral abduction-adduction
position and slightly flexed the hip and knee to avoid
extensor spasms. In this position, we requested subjects
to flex or extend the ankle or the knee joint (dorsi-/
plantarflexion and knee flexion/extension). Three consecutive trials were performed and after each trial thetrainer returned the leg to the initial resting position. The
subjects also volitionally attempted multijoint movements at rest without limb loading in a supine position
with their hip and knee joints slightly flexed to avoid extensor spasms. We requested subjects to perform alternating flexion/extension movements of the legs that approximated stepping movements.
When stepping, a harness (Wernig, 2000) attached tosuspension cables supported the subjects over a treadmill.
Elastic cords at the subjects’ hips or a trainer stabilized
the pelvis. Trainers held each leg distal to the patella toassist with knee extension during the stance phase and at
the popliteal fossa to assist knee flexion during the swing
phase. Trainers also held each leg proximal to the ankle
to assist with foot lift-off and placement when necessary(Table 1; A8, A9, A10, C1, C5, C6, D1, D4). Two subjects (Table 1, D2, D3) stepped independently on thetreadmill. Four subjects (Tables 1 and 2; D1-D4) ambulated overground with different levels of assistance. We
also recorded vertical ground reaction forces during stepping. The amount of body weight support (BWS) provided ranged from 15% to 56% and treadmill speeds
ranged from 0.22 to 0.33 m/sec.
Four subjects (A8, A10, C5, D1) had previously received an average of 12 weeks of Laufband therapy(Wernig and Müller, 1991, 1992) using BWST and manual assistance (30 min/day; 5 days/week) at treadmill
speeds of 0.05–0.42 m/sec. Characteristics of the motor
performance are reported in Table 2 (also reported in partin Wernig et al., 1995, 1999, 2000). Three subjects (Table
2; D2, D3, D4) had just completed 12 weeks of Laufband therapy prior to the experiments. All training
occurred at the Klinikum Karlsbad-Langensteinbach,
Germany.

Data Acquisition
We collected EMG and joint angles at 1,000 Hz using
a 24-channel hard-wired analog to digital board and acustom written LabView software acquisition program(National Instruments, Austin, TX). EMG data were AC
coupled into a differential amplifier (Konigsberg Instruments, Pasedena, CA). The signals were pulse-interval
modulated to a fiberoptic transmitter and relayed to de-

FIG. 1. Coactivation of functional agonists occurred during
attempts at single-joint movements. Electromyographic (EMG)
activity (mV) from the soleus (SOL), medial gastrocnemius(MG), tibialis anterior (TA), medial hamstrings (MH), vastus
lateralis (VL), and rectus femoris (RF); and knee and ankle angles (°) when clinically incomplete SCI subjects (C5, panel A;
C1, panels B and C and D4, panel D; as referenced in Table 1)
attempted to move a single-joint. The movement action requested by the experimenter was dorsiflexion (A), plantarflexion (B), knee flexion (C), and knee extension (D). Muscles
showing EMG activity usually differed from the ones expected
for the movement action requested by the experimenter. Boththe knee and ankle joints moved in each case even though thesubjects were asked to move only a single joint.

coding electronics. We measured EMG activity bilaterally from the soleus (SOL), medial gastrocnemius (MG),tibialis anterior (TA), medial hamstrings (MH), vastus
lateralis (VL), and rectus femoris (RF) muscles using
bipolar surface electrodes (Harkema et al., 1997). We
measured knee and ankle angles bilaterally with electrogoniometers placed over the axis of the joint rotation. Ankle angles were measured with the fibular head and 5th
metatarsal as landmarks. We measured limb load by

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RECRUITMENT OF MOTOR POOLS AFTER SCI
recording pressure distributon of the foot’s plantar surface using pressure sensor shoe inserts (Tekscan, Boston,MA). We dynamically calibrated (Carollo et al., 1993)
the Tekscan shoe inserts with a force platform (Kistler,
Amherst, NY) using nondisabled subjects of comparable
weight and shoe size to the SCI subjects (for details, see
Harkema et al., 1997). Force signals from pressure sensors were interpolated from 50 to 1,000 Hz and synchronized with EMG and joint angle signals. In addition,
we detected the stance and swing phases of the stepcycle using footswitches.

Data Analyses
We processed data using customized LabView software programs (National Instruments) by filtering EMG
signals using a 4th order bandpass Butterworth filter(40–500 Hz) and rectification. As a measure of EMG amplitude, we calculated EMG mean amplitude as the sumof the amplitudes of the rectified EMG from burst onset
to burst offset divided by burst duration. The onset of
EMG bursts was defined as the time when the signal amplitude remained above the threshold (three standard deviations above baseline for 50 msec and the offset when
the signal amplitude remained below the threshold for
150 msec). We compared the EMG mean amplitude dur-ing volitionally attempted single-joint movements, multijoint movements, and stepping from one limb of eachsubject. In subjects with detectable motor function in both
limbs determined by lower limb motor score testing (C6,
D1-D4), the limb with the lowest motor score was selected for analyses because in some subjects the contralateral limb was essentially normal. In subjects with
detectable motor activity in only one limb, that limb wasselected (C1 and C5) rather than making comparisons to
no activity. In subjects with no detectable voluntary lower
limb muscle activity in either limb (A8-A10), the left
limb was arbitrarily selected for analysis.
A one-way analysis of variance was used to test forsignificant differences among the averages of the EMG
mean amplitudes during single-joint movements, multijoint movements, and stepping with BWST. Pair-wisecomparisons were done using t tests with a Bonferroni
correction for multiple comparisons.

RESULTS
EMG Activity during Single-Joint Movements
Clinically incomplete SCI subjects could rarely generate isolated activity in single extensor and/or flexor

FIG. 2. Single- and multijoint movements and stepping from a clinically incomplete SCI subject (D3, reference Table 1) are
shown. Electromyographic (EMG) activity (mV) from the soleus (SOL), medial gastrocnemius (MG), tibialis anterior (TA), medial hamstrings (MH), vastus lateralis (VL), and rectus femoris (RF); knee and ankle angles (°); and limb load in Newtons (N)during an attempted single-joint movement (A), multijoint movements (B), and during weight-bearing stepping at 0.28 m/sec
with 15% body weight support (BWS) (C). The SOL, MG, MH, RF, and TA were activated, but not the VL, when knee extension was attempted, resulting in ankle dorsiflexion and knee extension (A). VL EMG activity was evident during multijoint movements (B) and stepping (C). Coactivity of the VL and MH was greater in multijoint movements (B) than during stepping (C).
Alternating patterns of the SOL, and RF were observed during multijoint movements and stepping, however, only during stepping in the MG, TA, MH, and VL.

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MAEGELE ET AL.
muscles during attempted single-joint movements. Only
2/28 attempts to perform single-joint movements whilelying on a side (isolated dorsiflexion, plantarflexion, knee
flexion, or knee extension; seven incomplete SCI subjects) resulted in the appropriate joint movement and
EMG activity. In 6/28 attempted single-joint movementsfunctional agonists of other joints of the same limb wereactivated generating flexion or extension patterns of theentire limb (Fig. 1). For example, during attempted dorsiflexion of the ankle, EMG activity was observed in the
TA and also in the MH resulting in both ankle dorsiflexion and some knee flexion (Fig. 1A). Coactivation at
the ankle and knee muscles was also observed in clinically incomplete SCI subjects during attempted plantarflexion resulting in both plantarflexion and knee extension (Fig. 1B). During attempted knee flexion, the MH
and the TA were activated synchronously, and both theknee and the ankle were flexed (Fig. 1C). Similarly, bothknee extension and plantarflexion occurred during attempts to only extend the knee (Fig. 1D).
In 12/28 conditions, coactivation occurred in agonists
and antagonists associated with either flexion or extension movements during attempts at single-joint movements. During both plantarflexion or knee extension efforts, EMG activity occurred in both knee extensors andplantarflexors as well as in the antagonistic TA and MH(Fig. 2A). Similarly, during attempted knee flexion or ankle dorsiflexion several muscles were activated. In one
subject (D4), the TA was not activated during attempted
dorsiflexion (Fig. 3A) but was evident when knee flexion was attempted (Fig. 3B). In 8/28 conditions minimal
to no EMG activity was detected during voluntary attempts to move a single-joint (Figs. 3A and 4A). Clinically complete SCI subjects never generated EMG activity or joint movements during attempted single-joint
movements.

EMG Activity during Multi-Joint Movements
and Load-Bearing Stepping
Among the motor tasks attempted the clearest alternating burst patterns were observed during weightbearing stepping with independent alternating flexion andextension movements observed (Figs. 2–5). Individual
muscles that were inactive during attempts to flex or extend a single-joint became active in 5/16 muscles during
non–weight-bearing multijoint movements and in 15/16
muscles during weight-bearing stepping of incomplete
SCI subjects. In a number of subjects, burst patterns were
present during stepping, but not during single-joint or
multijoint attempted movements (Figs. 3–5). Reciprocity
of flexor and extensor bursts was more routinely observed
during stepping than during multijoint movements, when
the subjects were asked to approximate the kinematics of

stepping. For example, the VL was coactivated with the
MH during multijoint movement attempts (Fig. 2B) but
was coactivated less during stepping (Fig. 2C). When

FIG. 3. Single- and multijoint movements and stepping froma clinically incomplete SCI subject (D4, reference Table 1).
Electromyographic (EMG) activity (mV) from the soleus (SOL)
medial gastrocnemius (MG), tibialis anterior (TA), medial hamstrings (MH), vastus lateralis (VL), and rectus femoris (RF);knee and ankle angles (°); and limb load in Newtons (N) during an attempted single-joint movement (A and B), multijoint
movements (C), and during weight-bearing stepping at 0.33
m/sec with 35% body weight support (BWS) (D). The nonspecificity in the activation of the muscles was present during
attempts to dorsiflex the ankle and flex the knee. Slight activation of the VL and RF occurred with attempted ankle dorsiflexion (A). When the same subject attempted to flex the knee
the MH was activated, but so was the TA and RF (B). Notethat the TA was not activated during attempts to dorsiflex theankle (A). Each muscle was activated during multijoint efforts(C), although at a lower amplitude than during stepping (D).
MH EMG bursts were reciprocal to the VL and RF and the TA
EMG was largely synchronized with the SOL and MG during
stepping with some activation during swing.

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RECRUITMENT OF MOTOR POOLS AFTER SCI
subject D4 attempted dorsiflexion, activity occurred inthe VL, RF, and SOL with no activity observable in the
TA (Fig. 3A). When this subject attempted knee flexion
inappropriate muscle activation was evident in the TA
and RF, with the activation of the MH (Fig. 3B). Duringmultijoint movements, clear alternating activity was only
observed in the VL (Fig. 3C). During stepping, alternating activity occurred in all muscles (Fig. 3D).
In subjects C5 and C6, minimal to no EMG activity
occurred during single- or multi-joint attempted movements (Fig. 4A,B). However, in both subjects (C5 andC6) during stepping alternating bursts occurred in all
muscles studied (Fig. 4C) except the RF in C6.
EMG activation patterns of the clinically complete SCI
subjects were similar to those observed in the incomplete
SCI subjects during stepping. As expected, no muscles
innervated by motoneurons below the lesion were recruited during voluntarily attempted movements in theclinically complete subjects as exemplified by subject A8(Fig. 5A–E). This subject underwent 4 months of training prior to testing (Wernig and Müller, 1992). This subject repeatedly executed phases of unaided stepping withpartial weight support. During some steps, assistance wasneeded only to place the foot at the transition from swing
to stance. Small flexor bursts occurred at the initiation of
the swing phase of the step cycle and extensors were ac-tive during the stance phase (Fig. 5F). As in many SCI
subjects the TA activity was coactivated with plantarflexors during stance while the MH activity was more
reciprocal with the plantarflexors, beginning in early or
mid-swing and ending by mid-stance.
The degree to which the EMG patterns are attributable
to a given level of training cannot be determined fromthe present data. However, it should be noted that whensome of the clinically incomplete SCI subjects (D1, D2,
D3, and D4) received Laufband therapy they improved
their ability to walk overground (EU Walking; Table 2)with minimal changes in voluntary activity (CMI; Table2). These data suggest that these minor changes in voluntary control of muscle activity cannot account for themarked improvements in the walking capacity these individuals achieved (also see Wernig et al., 1995, 1999).

Mean EMG Amplitudes were Higher during
Weight-Bearing Stepping than during
Non–Weight-Bearing Voluntary Motor Tasks
The amplitude of the EMG bursts from the six muscles of each of the 10 subjects studied was the highest
during weight bearing stepping compared to non–weightbearing single- and multijoint movements in 50/60 possible conditions (six muscles and 10 subjects; Fig. 6A).

FIG. 4. Single- and multijoint movements and stepping from a clinically incomplete SCI subject (C5, reference Table 1). Electromyographic (EMG) activity (mV) from the soleus (SOL), medial gastrocnemius (MG), tibialis anterior (TA), medial hamstrings (MH), vastus lateralis (VL), and rectus femoris (RF); knee and ankle angles (°); and footswitches (black bars indicate
stance phase) during an attempted single-joint movement (A), multijoint movements (B), and during weight-bearing stepping at
0.28 m/sec with 56% body weight support (BWS) (C). Minimal EMG was observed only in the VL during attempted knee extension (A), and only the MH became more active (although no clear EMG burst) during multijoint effort (B). Minimal movement of the knee or ankle occurred. This EMG pattern contrasts with the alternating bursts in each muscle during stepping (C).
The TA was largely synchronized with the SOL and MG while the MH EMG was reciprocal to that in the VL and RF and withthe ankle muscles.

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MAEGELE ET AL.

FIG. 5. Single- and multijoint movements and stepping froma clinically complete SCI subject (A8, reference Table 1). Electromyographic (EMG) activity (mV) from the soleus (SOL) medial gastrocnemius (MG), tibialis anterior (TA), medial hamstrings (MH), vastus lateralis (VL), and rectus femoris (RF);knee and ankle angles (°); and limb load in Newtons (N) during an attempted single-joint movement (A–D), multijoint
movements (E), and during weight-bearing stepping at 0.22
m/sec with 56% body weight support (BWS) (F). None of themuscles studied were recruited during attempted single- andmultijoint movements with limbs unloaded (A–E). During stepping (F) discrete flexor bursts occurred at terminal stance/initial swing and extensors were active during stance. Similar toclinically incomplete SCI subjects, MH activity occurred during terminal swing and early stance. The TA was coactivatedwith plantarflexors during stance.

The EMG mean amplitudes of the SOL and the MG werehigher during stepping than during non–weight-bearing
voluntary motor tasks in all 10 subjects. The highest amplitudes in the TA and the VL occurred during steppingin 7/10 subjects, and in the MH and RF in 8/10 subjects.
In the three subjects with no detectable EMG activity or
motor score that were classified as being clinically complete, EMG activity was evident in all six muscles studied in two subjects (A8 and A10) and in three muscles(SOL, MG, and MH) in one subject (A9) during weightbearing stepping. In contrast, no detectable EMG bursts
were observed during voluntary movements when thelimbs were unloaded.
The amplitude of the EMG bursts in the MG and MH
in three of the subjects with less severe SCI injuries(D1–D3) and in the TA and VL in two of these subjects(D2 and D3) during attempted multi-joint efforts washigher than those observed during single-joint efforts(Fig. 6A). Slightly higher EMG mean amplitudes during
attempts to move the limbs in a step-like, multijoint action while supine were also noted in the SOL and RF of
D1, whereas amplitudes in both muscles were similar or
smaller in subjects D2 and D3. In subjects D4 and C1,
EMG amplitudes in most cases were smaller duringmultijoint efforts. In the remainder of the subjects withmore severe SCI injuries (A8–A10, C5 and C6), the EMG
mean amplitudes were similar during single-joint andmultijoint efforts (except the TA and MH of C5 and of
the RF of C6). Also, in each of these five subjects(A8–A10, C5, and C6), the mean EMG amplitudes during these efforts were considerably smaller than those observed during similar efforts by the less severely impaired
subjects (D1–D4).
In comparing the EMG mean amplitudes of all subjects for each muscle, a pattern similar to that observedin individual subjects was noted (Fig. 6B). The group averages of EMG mean amplitudes of the SOL, MG, MH,
and VL during weight-bearing stepping were higher thanduring voluntary tasks without weight bearing (p ,0.05). Although the mean TA and RF EMG mean amplitudes were significantly higher during stepping, they
did not differ statistically among the motor tasks. The
EMG mean amplitudes of all subjects were similar during the multijoint and single-joint tasks in all muscles
studied.

DISCUSSION
This study demonstrates that the level of activation of
motor pools of the lower limbs of SCI subjects during
stepping exceeded that which was generated voluntarily
in the absence of weight bearing. The motor pools of agonists and antagonists were more reliably and more appropriately activated during stepping compared to voluntary efforts to move single or multiple joints in similar
patterns in the absence of weight bearing.

Lack of Selectivity in Activation of Motor Pools
during Single-Joint Efforts
When clinically incomplete SCI subjects in the present
study were asked to either flex or extend the knee or the1224

RECRUITMENT OF MOTOR POOLS AFTER SCI
ankle, agonist EMG activity was observed in muscles
controlling both the ankle and knee. Multijoint flexion or
extension movements of the entire limb occurred rou-tinely when single-joint movements were attempted. Synchronous activation of agonists and antagonists were also
observed during these single joint efforts. These observations are consistent with previous findings that voluntary activation of severely paralyzed limbs using Jendrassic maneuvers induces complex flexor and extensor
movements involving multiple joints (Dimitrijevic et al.,
1984; Wernig and Müller, 1991, 1992). The failure ofclinically incomplete SCI subjects to perform single-joint
movements indicates that the remaining supraspinal motor input to the spinal cord can initiate entire flexion or
extension patterns, but has a limited capacity to selectively activate specific muscles of a single joint or to simultaneously inhibit the antagonist.

Role of Proprioception in the Modulation of
EMG Activity
The proprioception associated with the kinematics ofthe moving limb and kinetics of weight bearing during
stepping modulated the levels and patterns of activationof lower limb motor pools. For example, individual muscles that could not be activated during attempts to flex or
extend a single-joint or during multijoint movements became active during weight-bearing stepping. In the threeclinically complete subjects, that is, without any detectable voluntary activity in lower limbs, bursts of EMG
activity were recorded from the majority of muscles studied during weight-bearing stepping. EMG mean amplitudes were higher during weight-bearing stepping thanduring non–weight-bearing voluntary motor tasks in
50/60 muscles from all 10 SCI subjects studied. These

FIG. 6. Mean electromyographic (EMG) amplitudes werehigher during weight-bearing stepping than during non–weightbearing voluntary motor tasks. The upper panel (A) shows average EMG mean amplitudes (mV) from the soleus (SOL),
medial gastrocnemius (MG), tibialis anterior (TA), medial hamstrings (MH), vastus lateralis (VL), and rectus femoris (RF) for
all 10 SCI subjects studied during voluntarily attempted
non–weight-bearing single-joint movements (white bars), multijoint movements approximating stepping in a supine position(black-white crossed bars), and weight-bearing stepping (blackbars). Mean EMG amplitudes were the highest during weightbearing stepping in 50/60 possible conditions. The EMG mean
amplitudes of all subjects combined for each muscle were highest during stepping (lower panel, B). The SOL, MG, MH, andVL had a higher group average EMG mean amplitude during
weight-bearing stepping compared to conditions when the subject performed voluntary tasks without weight bearing (p ,0.05). The mean TA and RF EMG amplitudes did not differ
statistically among the motor tasks. The group mean EMG amplitudes during the multijoint and single-joint tasks were similar in all muscles studied.

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MAEGELE ET AL.
results strongly support that the kinematics and loadingof the lower limbs provide an important source of continuous sensory signals needed for successful stepping.
Some specific sensory cues (termed “rules of spinal locomotion”; Wernig et al., 1995) important for the generation of locomotion that have been identified both in animal and human studies include limb loading during
stance and hip extension and shift of body weight (unloading) in terminal stance to initiate swing (Behrman
and Harkema, 2000; for reviews, see Grillner, 1981; Gossard and Hultborn, 1991; Harkema, 2001).

Sensory Processing by the Human Spinal Cord
Evidence that the human spinal cord can process proprioceptive information is supported by the observations
that weight supported by the lower limbs is positively
correlated to the amplitude of EMG signals of the flexorand extensor muscles (Harkema et al., 1997). This relationship between loading and EMG amplitude was observed in subjects regardless of the presence or absenceof injury or even the severity of the injury. These results
indicate that proprioceptive input to spinal neurons canbe processed so that the motor pools that generate stepping are activated in a temporally effective sequence.
In the present study, the EMG amplitudes of most of
the lower limb muscles of severely injured subjects weresignificantly higher during weight bearing stepping thanduring voluntary efforts to flex or extend the knee or ankle. Furthermore, the higher EMG amplitudes during
weight-bearing stepping were accompanied by the emergence of EMG bursts from other muscles that were silent
during voluntary efforts to activate single or multiple motor pools without weight bearing. Both of these observations suggest that the ability of the SCI subject to voluntarily activate a muscle group in the absence of loading
is not necessarily a predictable indicator of the potential
utility of that muscle group to contribute to load-bearing
stepping.
The comparisons of the EMG amplitude during voluntary efforts to activate a single muscle group and toactivate multiple muscle groups in a step-like motion
without weight support were similar. However, identifiable EMG bursts were generated from motor pools insome subjects during multijoint movements that were notpresent in efforts to activate a single muscle group. These
data are consistent with there being some synergistic orinteractive effects among multiple motor pools when attempting to generate a more complex cycling task evenin the absence of loading.
It has been shown previously that the sensory modalities associated with weight-bearing stepping can facilitate activation of muscles of the lower limbs in severely
incomplete SCI subjects. For example, one subject wasreported to have discrete activity only from the right TA(see patient Z in Wernig and Müller, 1991, 1992). However, even with this limited voluntary function this individual could walk overground for 40 m with a reciprocal gait using a walker without braces. This individual
used a starting position that included hyperextension of
one hip combined with contralateral loading, followed byipsilateral unloading. The unloaded limb would thenswing forward to begin the stance phase as the contralateral hip would extend. In this case, specific afferent
signaling associated with weight-bearing stepping seems
to have facilitated the recruitment of muscles during
walking. In this subject, muscles that became active during stepping were not activated during voluntary attempts
to generate multijoint movements without weight bearing. Similar observations in the clinically incomplete SCI
subjects were made in the present study. For example,
one subject (D2) after being wheelchair bound for 2 years
improved from a class of 1 to 4 (EU Walking) following
Laufband therapy. Her voluntary activity minimally improved (e.g., right limb 9.5 before and 10.5 after training; CMI Score; Table 2) with right hip flexors gradingzero both before and after training. However, a flexion
pattern including hip flexion was readily generated during an initial test of stepping using BWST and manual
assistance while providing the “rules of spinal locomotion.” This observation prompted the investigators to initiate the Laufband therapy on this subject. This suggeststhat even when individuals present low scores with voluntary manual testing the evaluation of flexion and extension patterns while stepping using BWST and manual
assistance is a very important assessment when considering therapeutic approaches for the rehabilitation ofwalking.

Interactions of Supraspinal Input andProprioception Facilitating Stepping
The EMG amplitudes of almost all muscles studied
were higher during stepping than in single- or multijoint
movements without weight bearing. It cannot be determined in these incomplete subjects whether the elevated
EMG amplitudes during weight-bearing stepping were
due to enhanced supraspinal control, a result of spinal facilitating events driven by proprioceptive input, or interactive spinal and supraspinal control. However, in clinically complete SCI subjects there is no dichotomy in thesource of the activating input being supraspinal or spinal. In clinically complete SCI subjects, clearly the EMG
mediation is initiated by the sensory input derived fromthe kinematics of the limb.
Previous reports have suggested that there are substantial differences between voluntary muscle activity
during unloaded postures and muscle activity evoked dur-

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RECRUITMENT OF MOTOR POOLS AFTER SCI
ing stepping on a treadmill and overground walking inincomplete SCI subjects (Wernig and Müller, 1991,
1992; Wernig et al., 1995, 1999). In the present study,
we demonstrated significant muscle activity during stepping from a clinically complete SCI subject without any
ability to voluntarily activate the lower limbs. This subject displayed most of the EMG activation patterns andelements of a typical step cycle, that is, stepping withflexion and extension movements with one limb independently completing a step cycle and the other needing
only assistance with foot placement. However, this subject could not execute consecutive and completely unassisted bilateral step cycles on the treadmill while fully
bearing weight. Comparable patterns of EMG activities
to those observed here have been reported from otherclinically complete SCI subjects during assisted steppingon the treadmill (Dietz et al., 1994, 1995, 1998b; Dobkin
et al., 1995; Harkema et al., 1997; Stewart et al., 1991);
however, complete unassisted stepping even after locomotor training has not been observed as it has in the adultcomplete spinal transected cat (Barbeau and Rossignol,
1987; de Leon et al., 1998a; Lovely et al., 1986).

Clinical Implications
These data provide substantial evidence that the potential recovery of walking cannot be predicted solely by theindividual’s ability to voluntarily generate force in a single
or multiple lower limb muscle groups with the limbs unloaded. The specificity of training that improved steppingand standing in laboratory animals (de Leon et al., 1998a,b)
and the SCI subjects’ ability to activate motor pools at levels and patterns that approximate normal stepping may contribute to more successful recovery of overground walking.
The present findings provide some of the underlying logic
for why SCI subjects can improve their functional overground walking by specific locomotor training. Further, wesuggest that assessments of the motor patterns of individuals where appropriate kinematics and kinetics of walking
can be facilitated (on a BWST system using manual assistance) may be more reflective of locomotor potential than
individual voluntary motor tests alone.

REFERENCES
ANDERSSON, O., and GRILLNER, S. (1981). Peripheral control of the cat’s step cycle. I. Phase dependent effects of rampmovements of the hip during “fictive locomotion.” Acta
Physiol. Scand. 113, 89–101.
ANDERSSON, O., and GRILLNER, S. (1983). Peripheral control of the cat’s step cycle. II. Entrainment of the central pattern generators for locomotion by sinusoidal hip movements
during “fictive locomotion.” Acta Physiol. Scand. 118, 229–
239.
ANISS, A.M., GANDEVIA, S.C., and BURKE, D. (1992). Reflex responses in active muscles elicited by stimulation of
low-threshold afferents from the human foot. J. Neurophysiol. 67, 1375–1384.
BARBEAU, H., and BLUNT, R. (1991). A novel interactive
locomotor approach using body weight support to retrain gaitin spastic paretic subjects, in: Plasticity of Motoneural Connections. A. Wernig (ed), Elsevier Science Publishers BV:
Amsterdam, pps. 461–474.
BARBEAU, H., CHAU, C., and ROSSIGNOL, S. (1993). Noradrenergic agonists and locomotor training affect locomotor recovery after cord transection in adult cats. Brain Res.
Bull. 30, 387–393.
BARBEAU, H., and ROSSIGNOL, S. (1987). Recovery of locomotion after chronic spinalization in the adult cat. Brain
Res. 412, 84–95.
BARBEAU, H., WAINBERG, M., and FINCH, L. (1987). Description and application of a system for locomotor rehabilitation. Med. Biol. Eng. Comput. 25, 341–344.
BEHRMAN, A., and HARKEMA, S. (2000). Locomotor training after human spinal cord injury: a series of case studies.
Phys. Ther. 80, 688–700.
BURKE, D., DICKSON, H.G., and SKUSE, N.F. (1991). Taskdependent changes in the responses to low-threshold cutaneous afferent volleys in the human lower limb. J. Physiol.
432, 445–458.
CAPADAY, C., and STEIN, R.B. (1986). Amplitude modulation of the soleus H-reflex in the human during standing andwalking. J. Neurosci. 6, 1308–1313.
CAROLLO, J.J., PAREKH, R., and WINCHESTER, P. (1993).
Calibration and force correction of the F-Scan foot pressure
measurement system. RESNA 189–191.

ACKNOWLEDGMENTS
This study was supported by a fund from the Deutsche
Stiftung Querschnittlähmung to A. Wernig and by thefollowing National Institute of Health grants: NS 16333,
NS 38654, NRSA HD 07416 and M01 RR 00865. We
would like to thank the administration and staff of theKlinikum Karlsbad-Langensteinbach, Germany, for theirinterest and support of this work, and the subjects who
participated in the study.

COHEN, J. (1960). A coefficient of agreement from nominal
scales. Educ. Psychol. Measure. 20, 37–46.
CONWAY, B.A., HULTBORN, H., and KIEHN, O. (1987).
Proprioceptive input resets central locomotor rhythm in the
spinal cat. Exp. Brain Res. 68, 643–656.
CRENNA, P., and FRIGO, C. (1987). Excitability of the soleus
H-reflex arc during walking and stepping in man. Exp. Brain
Res. 66, 49–60.

1227

MAEGELE ET AL.
CROZIER, K.S., CHENG, L.L., GRAZIANI, V., et al. (1992).
Spinal cord injury: prognosis for ambulation based on quadriceps recovery. Paraplegia 30, 762–767.
DE LEON, R.D., HODGSON, J.A., ROY, R.R., et al. (1998a).
Locomotor capacity attributable to step training versus spontaneous recovery after spinalization in adult cats. J. Neurophysiol. 79, 1329–1340.

GRILLNER, S. (1981). Control of locomotion in bipeds,
tetrapods and fish, in: Handbook of Physiology: The Nervous
System II. American Physiological Society: Baltimore, MD,
pps. 1179–1236.
HARKEMA, S.J., HURLEY, S.L., PATEL, U.K., et al. (1997).
Human lumbosacral spinal cord interprets loading during
stepping. J. Neurophysiol. 77, 797–811.

DE LEON, R.D., HODGSON, J.A., ROY, R.R., et al. (1998b).
Full weight-bearing hindlimb standing following stand training in the adult spinal cat. J. Neurophysiol. 80, 83–91.

HARKEMA, S.J. (2001). Neural plasticity after human spinal
cord injury: application of locomotor training to the rehabilitation of walking. Neuroscientist 7, 455–468.

DIETZ, V., COLOMBO, G., and JENSEN, L. (1994). Locomotor activity in spinal man. Lancet 344, 1260–1263.

HUSSEY, R.W., and STAUFFER, E.S. (1973). Spinal cord injury: requirements for ambulation. Arch. Phys. Med. Rehabil. 54, 544–547.

DIETZ, V., COLOMBO, G., JENSEN, L., et al. (1995). Locomotor capacity of spinal cord in paraplegic patients. Ann.
Neurol. 37, 574–582.
DIETZ, V., CURT, A., and COLOMBO, G. (1998a). Locomotor pattern in paraplegic patients: training effects and recovery of spinal cord function. Spinal Cord 36, 380–390.
DIETZ, V., WIRZ, M., COLOMBO, G., et al. (1998b). Locomotor capacity and recovery of spinal cord function in paraplegic patients: a clinical and electrophysiological evaluation.
Electroencephalogr. Clin. Neurophysiol. 109, 140–153.
DIMITRIJEVIC, M.R., FAGANEL, J., and SHERWOOD,
A.M. (1984). Suprasegmentally induced motor unit in paralyzed muscles of patients with established spinal cord injury.
Ann. Neurol. 16, 216–221.
DITUNNO, J.F., YOUNG, W., DONOVAN, W.H., et al.
(1994). The international standards booklet for neurologicaland functional classification of spinal cord injury. Paraplegia 32, 70–80.
DOBKIN, B.H., HARKEMA, S.J., REQUEJO, P.S., et al.
(1995). Modulation of locomotor-like EMG activity in subjects with complete and incomplete spinal cord injury. J. Neurol. Rehabil. 9, 183–190.
DUYSENS, J., and PEARSON, K.G. (1980). Inhibition of
flexor burst generation by loading ankle extensor muscle inwalking cats. Brain Res. 187, 321–332.
DUYSENS, J., TRIPPEL, M., HORSTMANN, G.A., et al.
(1990). Gating and reversal of reflexes in ankle muscles during human walking. Exp. Brain Res. 82, 351–358.
GOSSARD, J.P. and HULTBORN, H. (1991). The organization of the spinal rhythm generation in locomotion, in: Plasticity and Motorneuronal Connections. A. Wernig (ed), Elsevier Science Publishers BV: Amsterdam, pps. 385–404.
GRILLNER, S., and ROSSIGNOL, S. (1978). On the initiationof the swing phase of locomotion in chronic spinal cats. Brain
Res. 146, 269–277.
GRILLNER, S., and ZANGGER, P. (1979). On the central generation of locomotion in the low spinal cat. Exp. Brain Res.
34, 241–261.

KENDALL, H.O., KENDALL, F.P., and WADSWORTH, G.E.
(1971). Muscle Testing and Function, 2nd ed. William andWilkins: Baltimore.
LOVELY, R.G., GREGOR, R., ROY, R.R., et al. (1986). Effects of training on the recovery of full-weight-bearing stepping in the adult spinal cat. Exp. Neurol. 92, 421–435.
MAYNARD, F.M., BRACKEN, M.B., CREASEY, G., et al.
(1997). International standards for neurological and functional classification of spinal cord injury. Spinal Cord 35,
266–274.
PEARSON, K.G., and DUYSENS, J. (1976). Function of segmental reflexes in the control of stepping in cockroaches andcats, in: Neuronal Control of Locomotion. R.M. Herman, S.
Grillner, P. Stein, and D. Stuart (eds), Plenum Press: NY,
pps. 519–537.
STEWART, J.E., BARBEAU, H., and GAUTHTER, L. (1991).
Modulation of locomotor patterns and spasticity with clonidine in spinal cord injured patients. Can. J. Neurol. Sci. 18,
321–332.
WATERS, R.L., ADKINS, R.H., YAKURA, J.S., et al. (1994).
Prediction of ambulatory performance based on motor scoresdeprived from standards of the American Spinal Injury Association. Arch. Phys. Med. Rehabil. 75, 756–760.
WATERS, R.L., YAKURA, J.S., and ADKINS, R.H. (1993). Gait
performance after spinal cord injury. Clin. Orthop. 288, 87–96.
WATERS, R.L., YAKURA, J., ADKINS, R.H., et al. (1989).
Determinants of gait performance following spinal cord injury. Arch. Phys. Med. Rehabil. 70, 811–818.
WERNIG, A., and MÜLLER, S. (1991). Improvement of walking in spinal cord injured persons after treadmill training, in:
Plasticity of Motorneuronal Connections. Elsevier Science
Publishers BV: Amsterdam, pps. 475–485.
WERNIG, A., and MÜLLER, S. (1992). Laufband locomotion
with body weight support improved walking in persons withsevere spinal cord injuries. Paraplegia 30, 229–238.
WERNIG, A., MÜLLER, S., NANASSY, A., et al. (1995).
Laufband therapy based on “rules of spinal locomotion” is1228

RECRUITMENT OF MOTOR POOLS AFTER SCI
effective in spinal cord injured persons. Eur. J. Neurosci. 7,
823–829.
WERNIG, A., NANASSY, A., and MÜLLER, S. (1999). Laufband (treadmill) therapy in incomplete paraplegia andtetraplegia. J. Neurotrauma 16, 719–726.
WERNIG, A., NANASSY, A., and, MÜLLER, S. (2000). Laufband (LB) therapy in spinal cord lesioned persons. Prog.
Brain Res. 128, 89–97.
WERNIG, A. 2000. On-line. Available. www.meb.uni-bonn.de/wernig.
YANG, J.F., and STEIN, R.B. (1990). Phase-dependent reflex
reversal in human leg muscles during walking. J. Neurophysiol. 63, 1109–1117.

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Address reprint requests to:
Susan J. Harkema, Ph.D.
Department of Neurology
A386 1000 Veteran Ave.
University of California Los Angeles,
Los Angeles, CA 90095-7147
E-mail: sharkema@mednet.ucla.edu
orAnton Wernig
University of Bonn
Wilhelmstr. 31, D-53111
Bonn, Germany
E-mail: Wernig@physio.uni-bonn.de