1218

ORIGINAL ARTICLE

Comparison of Single Bout Effects of Bicycle Training Versus
Locomotor Training on Paired Reflex Depression of the Soleus
H-Reflex After Motor Incomplete Spinal Cord Injury
Chetan P. Phadke, PhD, Sheryl M. Flynn, PhD, Floyd J. Thompson, PhD, Andrea L. Behrman, PhD,Mark H. Trimble, PhD,† Carl G. Kukulka, PhD
ABSTRACT. Phadke CP, Flynn SM, Thompson FJ,
Behrman AL, Trimble MH, Kukulka CG. Comparison of single bout effects of bicycle training versus locomotor training on
paired reflex depression of the soleus H-reflex after motor
incomplete spinal cord injury. Arch Phys Med Rehabil 2009;
90:1218-28.
Objective: To examine paired reflex depression changes
post 20-minute bout each of 2 training environments: stationary bicycle ergometer training (bicycle training) andtreadmill with body weight support and manual assistance(locomotor training).
Design: Pretest-posttest repeated-measures.
Setting: Locomotor laboratory.
Participants: Motor incomplete SCI (n⫽12; mean, 44⫾16y);noninjured subjects (n⫽11; mean, 30.8⫾8.3y).
Intervention: All subjects received each type of training on
2 separate days.
Main Outcome Measure: Paired reflex depression at different interstimulus intervals (10s, 1s, 500ms, 200ms, and 100ms)
was measured before and after both types of training.
Results: (1) Depression was significantly less post-SCI
compared with noninjured subjects at all interstimulus intervals and (2) post-SCI at 100-millisecond interstimulusinterval: reflex depression significantly increased postbicycle training in all SCI subjects and in the chronic andspastic subgroups (P⬍.05).
Conclusions: Phase-dependent regulation of reflex excitability, essential to normal locomotion, coordinated by pre- andpostsynaptic inhibitory processes (convergent action of descending and segmental inputs onto spinal circuits) is impaired
post-SCI. Paired reflex depression provides a quantitative assay of
inhibitory processes contributing to phase-dependent changes inreflex excitability. Because bicycle training normalized reflex depression, we propose that bicycling may have a potential role inwalking rehabilitation, and future studies should examine theFrom the Departments of Physical Therapy (Phadke, Behrman, Trimble) and
Neuroscience (Thompson), University of Florida, Gainesville, FL; Division of Biokinesiology and Physical Therapy (Flynn), University of Southern California, Los
Angeles, CA; Veterans Affairs, Brain Rehabilitation Research Center, Malcolm
Randall Veterans Affairs Medical Center, Gainesville, FL (Phadke, Thompson, Behrman); and Department of Physical Therapy, University of Minnesota, Minneapolis,
MN (Kukulka).
Supported by the Christopher Reeve Paralysis Foundation (grant no. KA2-000202).
No commercial party having a direct financial interest in the results of the researchsupporting this article has or will confer a benefit on the authors or on any organization with which the authors are associated.
Reprint requests to Carl G. Kukulka, PhD, Program in Physical Therapy, University of Minnesota, 384 Children’s Rehab Center, Minneapolis, MN 55455, e-mail:kukul001@umn.edu.
†Deceased.
0003-9993/09/9007-00899$36.00/0
doi:10.1016/j.apmr.2009.01.022

Arch Phys Med Rehabil Vol 90, July 2009

long-term effects on subclinical measures of reflex activity and its
relationship to functional outcomes.
Key Words: Bicycling; H-reflex; Rehabilitation; Spinal
cord injuries.
© 2009 by the American Congress of Rehabilitation
Medicine
FTER SCI, SEGMENTAL REFLEX excitability is iniA
tially reduced during spinal shock and then becomes progressively enhanced. The loss of descending control and1-4

enhanced synaptic effectiveness of peripheral afferents results
in a reduced ability to modulate the stretch reflex5 and H-reflex6-8 during gait. This loss of modulation can result in unwanted interference contractions of lower-limb muscles duringlocomotor phases that require rapid lengthening of muscles.9,10
One of the ways in which the impaired spinal modulation
manifests post-SCI is a change in the transmission of successive volleys from Ia afferents to motoneurons.4,11-16 In noninjured subjects, 2 successive stimuli result in the second Hreflex being smaller in amplitude compared with the first,
which is termed paired reflex depression.17 This depression isan indirect measure of the probability of neurotransmitter release at the Ia afferent synapse.18 The degree of depression of
the second reflex amplitude is dependent on the interstimulusinterval: the shorter the interval, the greater the depression.19-22
This depression is also termed homosynaptic depression,
postactivation depression,18,23-25 or paired reflex depression.26
Post-SCI, however, paired reflex depression in both the
H-reflex and stretch reflex pathways is significantly impaired(lower).25,27 Accordingly, when a series of volleys of electricalstimulation are carried via Ia afferents, the depression of Hreflex that is normally seen is impaired or lost after SCI.2 The
firing of muscle spindles in response to stretch of soleus muscle(eg, swing phase of walking) post-SCI has a much higher
probability of producing reflex muscle activity in the soleus
muscle when it is normally inactive.5,28 Results from others7,29
and from our own previous work8,30 have shown that H-reflex
modulation during serial lengthening of the soleus muscle (asoccurs in stance and swing phases of walking) post-SCI is
impaired and reflex amplitudes are significantly greater com-

List of Abbreviations
AIS
BWS
EMG
GABA
MAS
SCI
5-HT

American Spinal Injury Association Impairment
Scalebody weight support
electromyography
gamma-aminobutyric acid
Modified Ashworth Scalespinal cord injury
5-hydroxytryptamine

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H-REFLEX AFTER BICYCLE AND LOCOMOTOR TRAINING, Phadke
Table 1: Demographic Information for Subjects With Incomplete SCI
Ashworth Scale (Ankle)

Subject

Age(y)Duration of
Injury (mo)Levelof Injury

1
2
3
4
5
6
7
8
9
10
11
12

50
48
76
48
42
55
23
44
51
50
22
22

4
26
35
5
88
3
84
33
21
6
12
19

C7
C5
C3–4
C6–7
C5–6
C5–6
C5–6–7
C6
C5–6
C8, T1
C5
C5–6

Sitting

Supine

Sex

ASIA
Grade

R

L

R

L

Motor
Score

Medication

Dose

Assistive
Device

M
M
M
M
M
M
M
M
F
F
M
F

D
D
D
D
D
D
D
D
D
D
D
C

1
NA
0
1
1
NA
NA
2
2
0
3
3

1
NA
0
0
1
3
NA
2
2
1
3
2

1
NA
0
0
1
NA
NA
3
0
1
3
3

1
NA
0
0
1
3
NA
3
2
2
3
2

83
87
NA
87
88
73
NA
64
70
87
87
47

Clonipen
None
Zanaflex
Gabapentin
None
Baclofen
NA
NA
None
None
N/A
None

4⫻/wk
NA
2⫻/d
1000mg; 4⫻/dNA5mg; 2⫻/d
NA
NA
NA
NA
NA
NA

Cane
W
None
PW
None
W⫹R-AFO
B/L LC
PW
None
None
None
PW⫹B/L AFO

NOTE. MAS scores of 2 indicates a slight increase in muscle tone in less than half the range of ankle dorsiflexion. Scores of 2 or higher indicate
greater increase in muscle tone and through the complete range of motion and scores less than 2 indicate lower tone.
Abbreviations: AFO, ankle foot orthosis; ASIA, American Spinal Injury Association; B/L, bilateral; C, cervical; L, left; LC, loftstrand crutches; NA,
not available; PW, platform walker; R, right; SCI, spinal cord injury; T, thoracic; W, walker.

pared with noninjured subjects. Thus, one of the problems
during walking post-SCI appears to be an impaired modulationof reflex activity during task-specific lengthening of lower
extremity muscles. Hence, a task-specific therapeutic strategy
consisting of alternating stretch-shortening cycles may improve
H-reflex modulation during muscle lengthening. Walking on atreadmill with body weight support and manual trainers (locomotor training) and training on a stationary assisted bicycle
ergometer (bicycle training) both feature rhythmic shortening
and lengthening of lower-extremity muscles.
Locomotor training that induces task-specific patterns of
sensory and motor activity may enhance the recovery of
walking by optimizing the activity-dependent neuroplasticity of the nervous system.31,32 Neuronal circuits may reorganize by strengthening existing and previously inactive
connections.32-34 It is hypothesized that such reorganization
could improve the sequencing of spinal inhibitory mechanisms
such as reciprocal inhibition9,35 and presynaptic inhibition6,7,36
and increase the modulation of reflex excitability during walking(eg, lengthening of the soleus muscle).
Although research indicates that recovery of walking can beobtained with task-specific training such as locomotor training
on a treadmill, thus providing load-bearing and sensorimotor
practice of walking,33,37 others have suggested that the coordinated coupling of the legs, the alternative phasing of theflexors and extensors of the limbs, and cyclical feedback fromperipheral afferents are important task-relevant components oflocomotion.38,39 Therefore, a task such as pedaling a bicycle
ergometer may induce neuroplastic changes that are beneficial
to improving modulatory neural processes (reciprocal inhibition, presynaptic inhibition).
The nature of the relationship between paired reflex depression and neurologic injury is not clearly understood.40 The
purpose of this experiment was to compare, in noninjured andsubjects with motor incomplete SCI, paired reflex depression
before and after a single bout of training on a bicycle ergometerand locomotor training on a treadmill (with partial BWS andtrainer assistance). On the basis of previous research,25,27 wehypothesized that reflex depression post-SCI will be significantly lower than recorded in noninjured subjects. In noninjured subjects, we hypothesized that reflex depression would
not change after both forms of training. Stationary bicycling

and walking on a treadmill involve repetitive stretching andshortening of the soleus muscle; hence, we hypothesized that
paired reflex depression would increase after both forms of
training in subjects with incomplete SCI.
METHODS
Subjects
Data were obtained from 12 subjects with incomplete SCI(mean age, 44⫾16y) (table 1) and 11 noninjured subjects(mean age, 30.8⫾8.3y). Inclusion criteria for the subjects withincomplete SCI were: (1) adults more than 18 years old, (2) adiagnosis of first-time SCI including etiology from trauma,
vascular, or orthopedic pathology at cervical or thoracic levels,(3) a range of 3 months to 3 years post-SCI, AIS class C or D,(5) a medically stable condition, (6) no other degenerative
spinal disorders, (7) the ability to walk independently a minimum of ⬃18 meters continuously with or without an assistive
device, (8) the ability to walk at least ⬃90 meters total per day,and (9) the ability to give informed consent. The above criteria,
specifically AIS class C or D and ability to walk a minimum of
60 feet continuously, were set to ensure that SCI subjects
would be able to participate in the complete protocol andminimize subject dropout. In addition, we wanted to recruit
subjects who could actively participate in both the training
protocols rather than training passively. Able-bodied subjects
served as noninjured controls and had no history of neurologic
or orthopedic problems that could impair walking function. All
subjects signed written consent as approved by the institutional
review board at the University of Florida.
Initial Testing
The initial subject evaluation (1wk before testing) beganwith a clinical evaluation of the subjects with incomplete SCI
to identify levels of impairment and initial levels of function by
the AIS and bilateral upper- and lower-extremity motor andsensory scores.41 Bilateral ankle plantar flexor spasticity wasevaluated by the modified Ashworth scale.42
Experimental Protocol
Each subject returned 1 week later to undergo their initial
experiment. All persons with incomplete SCI first walked with
Arch Phys Med Rehabil Vol 90, July 2009

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H-REFLEX AFTER BICYCLE AND LOCOMOTOR TRAINING, Phadke

their customary assistive device on a level walkway (.63m long
digitized mat with embedded microswitches) at their selfselected walking speed. Three consecutive trials of walking
were recorded and comfortable walking velocity determined by
GAIT MAT IIa software. This test was repeated immediately
posttraining.
The soleus H-reflex was evoked, for the purpose of consistency, on the more involved side of persons with incomplete
SCI (determined by AIS lower-limb motor score) and on thedominant side of noninjured control subjects. Similar testing
conditions were maintained for all tests. The skin was shaved
and cleaned for application of electrodes. A bipolar (2cminterelectrode distance) Ag-AgCl surface EMG electrodeb wasplaced longitudinally over the soleus muscle approximating thefiber orientation of the muscle (just medial to the Achilles’
tendon). The electrodes are embedded in an epoxy mount withpreamplifier circuitry. The preamplifier and second stage amplifier provided a total amplification of 1000⫻ with a frequency band pass of 20Hz to 4kHz. We fixed the electrode to
the skin with adhesive collars and foam tape wrapped aroundthe electrode and the subject’s leg to minimize movement
artifact. The tibial nerve was stimulated to evoke H-reflexes;
1-millisecond current pulses were delivered via a constantcurrent stimulatorc with a 2cm half-sphere silver cathodeplaced in the popliteal fossa and a circular 10cm-diameter
silver dispersive pad (anode) positioned just superior to thepatella. The half-sphere shape of the cathode helped in ensuring good contact with the skin; the cathode was held in placewith a custom-fabricated Velcro strap. Data were acquired at asampling rate of 10kHz per channel and stored digitally by
Data-Pac III softwared on a personal computer.
H-Reflex Testing in Semireclined Position
Subjects were positioned semireclined, and soleus H-reflex
recruitment curves were derived. Subsequently, paired H-reflexes were then evoked with stimulus intensities that produced
M-wave amplitude of 10⫾3% Mmax. Stimulation intensity
was adjusted throughout the experiment to maintain stimulation levels that evoked an M wave amplitude 10⫾3% Mmax.
Interstimulus intervals used were 10 seconds, 1 second, 500
milliseconds, 200 milliseconds, and 100 milliseconds.43 A period of approximately 30 seconds was allowed to lapse between
testing at 2 consecutive interstimulus intervals in order toprevent a carryover effect. This testing procedure was repeated
immediately after both types of training.
The paired-reflex methodology has been reported to havestrong test-retest reliability using a mean of 4 paired pulses.44
Accordingly, at each interstimulus interval, 4 paired reflexes
were evoked with a minimum 30-second interval between 2
consecutive paired reflexes. To counter an order effect, subjects
were randomly assigned to undergo locomotor training or
bicycle training first, and the 2 training days were separated byat least 1 day. We did not control for the order effect of thepresentation of the interstimulus intervals. Surface EMG data
were also collected from bilateral tibialis anterior, soleus, quadriceps, and hamstrings during both training conditions. Surface
EMG data were continuously recorded for 1 minute each in the
2nd, 10th, and 18th minute of both types of training.
Overground Walking H-Reflex Testing
Subjects walked at a self-selected pace, and H-reflexes were
evoked according to a standardized procedure.7,45 Electrodeplacement for the soleus muscle, the cathode, and the anode
was the same as described earlier. The step cycle was divided
into 2 components, midstance and midswing, and the stimuli
Arch Phys Med Rehabil Vol 90, July 2009were presented randomly during a continuous gait cycle (eg,every fourth step at midstance) to acquire 15 responses perphase component. The phase of walking when the ipsilateralleg completely bore the body weight (ipsilateral ankle and hipin neutral position) was considered the midstance phase. Similarly, the phase when the contralateral leg completely bore thebody weight (contralateral ankle and hip in neutral position)
was considered the midswing phase. Because most subjects
post-SCI in this study walked slowly, it was not difficult toaccurately stimulate in the midstance and the midswing phases.
Approximately 50 milliseconds on either side of the exact
midpoint was considered as midpoint of the stance or swing
phases. The same experimenter evoked H-reflexes in all thesubjects and in all the conditions. The electrical stimulation
was manually delivered by visually determining midstance andmidswing phases (confirmed by foot-switch recording). It ispreferable to trigger electrical stimulation through footswitches, but in order to use this method, consistent footcontact pattern is necessary. In our subjects, we found that thefootfall pattern was very inconsistent, and step-to-step variations were common. Thus, it was difficult to precisely trigger
stimulation at midstance phase. Hence, we chose the manual
method, which controlled for the interstep variability and allowed the experimenter to visually detect the midstance or
midswing phase of walking. The consistency of stimuli current
was determined by maintaining a minimum test M-wave of
10⫾3% of maximal M-wave. H-reflexes of the same effective
stimulus strength, reflected by consistent M-wave amplitude,
were included, normalized to Mmax, and compared before andafter training. Peak-to-peak reflex amplitudes of the H and M
responses for each walking phase were pooled and averaged.
Locomotor Training Over Treadmill
For locomotor training, subjects walked with 40% BWS
with a special harnesse with 1 thoracic band, 1 pelvic band, and2 thigh straps on a Biodex rehabilitation treadmill.f Manual
assistance while walking was provided by gait facilitators (2people trained to facilitate the subject’s gait by assisting footplacement and knee extension and 1 trainer to assist with pelvic
movement and trunk alignment). Gait velocity was increased
toward normal values (1.2m/s) to the velocity at which thesubject’s gait kinematics (knee, hip, and ankle motions) visually appeared to be most efficient. Subjects trained for 5 to 10
minutes at a time with the goal of a total training duration of 20
minutes.
Bicycle Training
A tandem bicycle ergometerg setup was used in which thesubject rode on the first bicycle while a laboratory assistantrode the second to provide assistance in maintaining a consistent cadence. All subjects had their feet strapped to the pedals.
The pedal was very small, and only the forefoot (metatarsal
heads and toes) was supported on the pedal; this design encouraged soleus activity during bicycling. A harness was used
to help the subject maintain a comfortable sitting position andto provide a safety mechanism to prevent falls; however, no
BWS was provided. Subjects’ feet were secured over thepedals with Velcro straps. The height of the bike seat was
adjusted such that the knee position (5–10° of flexion when thefoot was in the lowest position while pedaling) was similar for
all the subjects. Subjects pedaled at a frequency (⬇54 –
56rpm)46 that approximately matched phasic soleus EMG
bursts seen during overground walking at normal speed of
1.2m/s.47 Subjects trained for 5 to 10 minutes at a time, withthe goal of 20 minutes’ total training duration. After training,paired reflex depression was immediately retested.

H-REFLEX AFTER BICYCLE AND LOCOMOTOR TRAINING, Phadke

Data Analysis
In all the pairs of H-reflexes, the second H-reflex was normalized to the amplitude of the first H-reflex (tested at therespective interstimulus intervals). Thus, the reflex depression
data are presented as a percentage of the control (first) H-reflex.
So a lower value of paired reflex depression indicates greater
depression and a higher value indicates lesser depression. Typically, in noninjured subjects, paired reflex depression values
are low because noninjured subjects produce greater depressionof the second H-reflex compared with the first. To facilitate
interpretation of the data, from this point on, paired reflex
depression will be referred to as “depression.” H-reflex amplitude (mean of 4 trials) at each interstimulus interval wascompared within the same condition pre- and posttraining by
nonparametric tests (Wilcoxon signed-rank and Mann-Whitney
U test) and between controls and incomplete SCI by parametricstatistics (independent samples t test). Statistical significancewas set at P less than .05. We were specifically interested in
exploring the differences between pre- and posttraining at
100-millisecond interstimulus interval. The human muscle
spindle afferents usually fire at the rate of approximately 8 to
15Hz.48 Thus, the 100-millisecond interval approximated normal firing rates of muscle spindles. Subsequently, we performed post hoc tests (pre- vs posttraining) in subgroups on thebasis of spasticity and chronicity at 100-millisecond interstimulus interval (Wilcoxon signed-rank test). To adjust for increased type I error, we divided the P value by the number ofpost hoc tests (P/2). After the Bonferroni adjustment, the new
P value was P equal to .025. For the ease of data interpretation,
actual P values are shown for all tests.
RESULTS
H-reflex depression was compared between noninjured subjects and subjects with incomplete SCI at each interval by1221

independent-samples Mann-Whitney U tests. Within the training conditions, paired Wilcoxon signed-rank tests were performed comparing H-reflex paired reflex depression pre- versus
posttraining at each interstimulus interval in subjects withincomplete SCI and noninjured controls.
Paired Reflex Depression in Noninjured Subjects
Noninjured control subjects revealed a decrease in the amplitude of the second response relative to the first (paired reflex
depression) (fig 1). The greatest depression was observed at aninterval of 100 milliseconds (after both types of training),
where the second H-reflex amplitude was approximately 46%of the amplitude of the first H-reflex (fig 2).
At an interstimulus interval of 100 milliseconds, depression
postlocomotor training (.49⫾.33) was significantly greater thandepression pretraining (.60⫾.27; P⫽.011). Although paired
reflex depression pre- and postbicycle training at a 100-millisecond interval was not significantly different, there was atrend toward greater depression postbicycle training (pretraining .46⫾.25 and posttraining .37⫾.24; P⫽.11). There were no
significant differences in pre- versus posttraining in the amountof reflex depression for the rest of the interstimulus intervals(10s, 1s, 500ms, and 200ms) in both types of training (fig 3).
Paired Reflex Depression: Incomplete SCI vs Noninjured
Significantly less depression was seen in subjects with incomplete SCI (when compared with noninjured subjects) at allinterstimulus intervals (P⫽.000, P⫽.000, and P⫽.001, respectively for comparisons at 1s, 500ms, 200ms intervals) except
intervals of 100 milliseconds, where although the difference
was not statistically significant, there appeared to be a trend forlesser depression post-SCI (58% in the subjects with incomplete SCI compared with 46% in noninjured subjects; P⫽.21)(see fig 2).

Fig 1. Raw H and M waves ina single noninjured and SCI
subject. Abbreviations: 1st,
first H-reflex; H, H wave; i-SCI,
incomplete SCI; M, M wave;
2nd, second H-reflex.

Arch Phys Med Rehabil Vol 90, July 2009

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H-REFLEX AFTER BICYCLE AND LOCOMOTOR TRAINING, Phadke

Fig 2. Comparison paired reflex depression between subjects withincomplete SCI pre- and posttraining and comparison between
pooled SCI pretraining and noninjured subjects. *Statistically significant differences pre- vs postbicycle training at 100ms interval;§Statistically significant difference between noninjured and SCI atinterstimulus interval of 200ms, 500ms, and 1s; vertical bars represent SE; SCI (nⴝ24; data were pooled from prebicycle training andprelocomotor training) and noninjured (nⴝ24; data pooled for all
subjects prebicycle training and prelocomotor training).

Paired Reflex Depression: Influence of Training Type in
Subjects With Incomplete SCI
No detectable change was observed in depression between
pre- and postlocomotor training at any interstimulus interval(P⬎.05); however, depression postbicycle training was greaterthan prebicycle training at all interstimulus intervals, butreached statistical significance for only the 100-millisecond
interval (P⫽.011) (see fig 2). On average, the depression
significantly increased from 58% pre- to 46% postbicycle training for the 100-millisecond interval, thus approaching theamount of depression seen in noninjured subjects (see fig 2).
The EMG data from the tibialis anterior and soleus muscles did
not show a consistent pattern of change during the course of 20
minutes of either type of training.
Paired Reflex Depression in Subjects With Spasticity
Versus No Spasticity
To compare the depression patterns between spastic andnonspastic subjects, we divided the subjects with incomplete
SCI based on scores on the MAS.42 We grouped all subjects
with an MAS score of 2 or higher into the spastic group (n⫽5)
and the rest of the subjects into the nonspastic group (MAS⬍2,n⫽5; MAS data not available in 2 subjects) (see table 1).

Fig 4. Effect of bicycle training in spastic and nonspastic; andchronic and subacute groups post-SCI at 100ms interstimulus interval. *Statistically significant difference (P<.025); SE bars shown;spastic and nonspastic groups each had nⴝ5; chronic group nⴝ7;subacute group nⴝ5.

Pretraining depression values for both types of training werepooled together, and at a 100-millisecond interval, we used a
Mann-Whitney U test to compare depression in the spastic(n⫽10) and nonspastic groups (n⫽10). The spastic group
showed less mean depression (73%) compared with the nonspastic group (49%; P⫽.04). Subsequently, we used a Wilcoxon signed-rank test to compare the depression postbicycle
training and postlocomotor training at 100-millisecond intervals in both the spastic and nonspastic groups. Subjects withspasticity showed a statistically significant approximately 19%
increase in depression postbicycle training (42%; n⫽5) compared with prebicycle training (62%; n⫽5) at 100-millisecond
interval (P⫽.020) (fig 4). In addition, the spastic group also
showed a significant increase in overground gait speed from
.61 to .74m/s (Wilcoxon signed-rank test; P⫽.021). Interestingly, 3 out of 5 subjects in the nonspastic group were receiving antispasticity medications (see table 1). The groups basedon spasticity, however, did not show any significant differencespre- versus postlocomotor training at all interstimulus intervals.
The nonspastic group did not show any change in walking
speed after any type of training.
Paired Reflex Depression in Subjects With Subacute
Verus Chronic Incomplete SCI
To evaluate the influence of injury duration on the level ofdepression, we subdivided the subjects into 2 groups: subacute(n⫽5; duration ⱕ12mo) and chronic (n⫽7; duration ⬎12mo).
We used the Wilcoxon signed-rank test to compare the effect ofbicycle training and locomotor training in these 2 groups. We
found a statistically significant increase in depression postbicycle training at 100-millisecond interstimulus interval in thechronic group (P⫽.009) (see fig 4). In addition, the chronic
group also increased their overground gait speed from .59 to.69m/s (Wilcoxon signed-rank test; P⫽.036). The subacutegroup did not show any change in walking speed after any typeof training.
Correlation: H-Reflex Amplitudes (Stance and Swing)
Versus Percentage of H-Reflex Depression
For the purpose of correlation, depression was calculated by
the following formula:(First H-reflex ⫺ second H-reflex)/First H-reflex

Fig 3. Effect of bicycle and locomotor training on paired reflex
depression in noninjured subjects. *Statistically significant difference between prebicycle training and postbicycle training; SE bars
shown.

Arch Phys Med Rehabil Vol 90, July 2009

Spearman’s bivariate correlation coefficient was calculated,
and the correlation was moderately strong between stance
H-reflex amplitudes and reflex depression (␳⫽–.47; P⫽.09)

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H-REFLEX AFTER BICYCLE AND LOCOMOTOR TRAINING, Phadke

Fig 5. Correlation between walking H-reflexes (stance and swing)
and percentage of paired H-reflex depression.

and between swing H-reflex amplitudes and reflex depression(␳⫽–.55; P⫽.05) (fig 5).
Overground Gait Speed
The gait speeds tested before and after training in bothconditions are listed in table 2. The mean posttraining gait
speed was significantly greater compared with mean pretraining speed in both training conditions (P⫽.008 bicycle training
and .002 locomotor training).
Patterns of Electromyography Activity Postspinal Cord
Injury: Bicycle Versus Locomotor Training
Although the EMG did not show a consistent pattern ofchange during the course of 20 minutes of either type oftraining, there were key differences in EMG activity between
the 2 training conditions. Surface EMG data were collectedduring training in 10 subjects with SCI. Three subjects showedno EMG activity and 4 subjects low muscle activity in either
the left or right tibialis anterior in the bicycle training condition; however, these same subjects showed good rhythmic
firing of bilateral tibialis anterior muscles in the locomotor
training environment. In general, the EMG activity in the lower
limbs was lower in the bicycle training condition comparedwith the locomotor training condition (fig 6). During bicycle
training, soleus EMG activity was either low/absent (tibialis
anterior 5 of 10 subjects; soleus, quadriceps, and hamstrings
muscles in 3 of 10 subjects) or comparable to EMG activity inthe locomotor training condition. Although some muscles
showed lower activation compared with locomotor training, in
general, the bicycle training condition was not passive andrequired active participation from the subjects. The medianmotor score of the SCI subjects was 85 (range, 47– 88; score
out of 100), and thus most subjects were able to actively
participate in both types of training.
Overground H-Reflexes
Mean H-reflex amplitude was almost identical pre- andposttraining in both swing and stance phase in both types oftraining (not significantly different; P⬎.05) (fig 7).
DISCUSSION
The major findings of this study are: (1) Subjects withincomplete SCI had significantly less depression than noninjured subjects at all interstimulus intervals (except 100ms). (2)Noninjured subjects showed a significant increase in depression postlocomotor training (at 500ms and 100ms interstimulusinterval) and a robust trend toward an increase in depression
postbicycle training (at 100ms interstimulus interval). (3) Subjects with incomplete SCI displayed significantly greater depression postbicycle training (⬇21% greater) at the 100-millisecond interstimulus interval. (4) The spastic incomplete SCI
group had a significant increase in depression postbicycle training (⬇32%), in contrast with the nonspastic group, which did
not show any significant difference before versus after for
either type of training. (5) The chronic group showed a significant increase in depression postbicycle training at 100-millisecond interstimulus interval. (6) In SCI subjects, overgroundwalking speed was significantly different before versus after
for either type of training. (7) H-reflexes tested over groundwere not significantly different before versus after types oftraining. (8) There was a moderate negative correlation between reflex depression and walking H-reflexes.
As reported in earlier studies, we found that depression was
significantly lower post-SCI compared with noninjured controls.25,27,49,50 The fact that the average level of depression in
noninjured subjects increased 18.3% and 19.5% postlocomotor
training and postbicycle training, respectively, suggests thatboth types of training can induce a robust neurologic effect.
Although we did not anticipate a change in reflex depression
posttraining in noninjured subjects, this result demonstrates theinherent neuroplastic capacity of the uninjured spinal cord in
response to repetitive sensory input. Reflex depression has
been previously reported to be modulated after a short duration
bicycle training task.46 Meunier et al46 also reported that noninjured subjects who were used to regularly exercising the
locomotor muscles (such as in treadmill walking) showedlarger reflex modulation posttraining compared with sedentary
subjects.46 It has been suggested that modulation of reflex
depression may be related to the task-specific pattern of sensory feedback.46
An unexpected finding of this study was that although asingle bout of both types of training resulted in a significant
increase in overground walking speed, only bicycle training—
but not locomotor training group—showed increased depression in subjects with incomplete SCI. Comparison of the EMG
activity during the 2 training conditions revealed that EMG
activity was greater in the locomotor training condition. In a
recent study, Stein et al51 reported that when the soleus muscle
is voluntarily activated, the phenomenon of paired reflex depression was diminished or lost. They argued on the basis of
their results that paired reflex depression may not have any
functional significance or relevance to an active task that reTable 2: Overground Walking Speed (m/s)
Bicycle Training

Locomotor Training

Subject

Pre

Post

Pre

Post

1
2
3
4
5
6
7
8
9
10
11
12
Mean

0.71
0.23
0.60
0.57
1.00
0.21
0.23
1.43
0.83
0.16
1.12
0.06
0.60

0.73
0.24
0.71
0.52
0.99
0.30
0.28
1.83
0.87
0.26
1.23
0.07
0.67

0.50
0.21
0.69
0.50
0.99
0.19
0.21
1.27
0.76
0.18
0.88
0.11
0.54

0.98
0.26
0.69
0.93
1.48
0.36
0.27
1.84
1.24
0.24
1.59
0.12
0.83

Arch Phys Med Rehabil Vol 90, July 2009

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H-REFLEX AFTER BICYCLE AND LOCOMOTOR TRAINING, Phadke

Fig 6. Surface EMG activity
from a representative subject
with SCI collected during a
10s interval during bicycle andlocomotor training. Abbreviations: FS, foot switch; Hams,
hamstrings; L, left; Quads,
quadriceps; R, right; S, soleus;TA, tibialis anterior.

quires active firing of muscles. It is likely that the greater
muscle activation during the locomotor training condition,compared with the bicycle training condition (see fig 5), may
have resulted in a loss of sensitivity to changes in reflex
depression. We did not record ankle movement velocity andankle angles, which may have produced specific effects wehave not accounted for during the 2 types of training. Thus, itappears that paired reflex depression may not be a sensitive
measure to detect changes postlocomotor training.
Our previous work shows an increase in depression of Hreflex amplitude in the locomotor training environment postSCI8,30; thus, it is possible that changes in presynaptic inhibition may have led to improvement in walking speed
postlocomotor training. Training principles for locomotor
training have been established and continue to be refined52;
a primary target of these training protocols is to provide optimal sensory cues for activating the central pattern generators.
In light of the rehabilitation potential of training locomotor
activity with bicycle and treadmill, it will be important to

Fig 7. Overground walking H-reflexes pre- vs posttraining. NOTE:
H/Mmax on the y-axis represents mean H-reflex normalized tomaximum M wave; vertical SE bars shown.

Arch Phys Med Rehabil Vol 90, July 2009

continue considering the similarities and differences of these 2
training environments. Bicycling does not typically require as
much loading as locomotor training; hence, we anticipatedgreater H-reflex depression posttraining on the treadmill. On
the other hand, cycling is a relatively rhythmical, constant,repetitive task, alternating between flexion and extension without the added element of postural control. With a more structured, controlled task such as cycling (with trainer assistance tomaintain cadence; feet strapped to pedals), the afferent input
may be more consistent, providing a better opportunity forreorganization around this afferent information. In contrast,walking is a complex task that requires postural control (evenwith 40% BWS), relative control over hip/knee/ankle movements (even with trainers assisting), and some consideration
for foot placement. Accordingly, this level of supraspinal attention and control with stepping may have reduced the consistency of alternating flexion/extension input to the nervous
system. In addition, a recent report shows that the soleus
H-reflex amplitude is directly proportional to the level of
postural threat during walking on a treadmill.53 The bicycle
training environment was clearly less of a postural threat compared with walking in the locomotor training environment.
Animal studies have provided the rationale for the use of
bicycle training; 2 separate studies reported that passive exercise can normalize H-reflex depression in a rat SCI model.54,55
Subsequently, Kiser et al56 reported normalization of frequency
dependent H-reflex depression after a passive cycling regime ina human SCI single case study; this increase in depression was
also correlated with a decrease in spasticity. Recently, Motl et
al57 reported a decrease in both spasticity and H-reflex amplitude after 20 minutes of cycling exercise in people with multiple sclerosis. In the current study, we found that spastic
subjects had a greater loss of depression and responded tobicycle training better than the nonspastic subjects (see fig 4).
Thus, it appears from our results that bicycle training could
potentially be used as a modality to decrease spasticity.
Our subject population was heterogeneous in their chronicity, which ranged from 3 to 88 months (see table 1). We
analyzed H-reflex depression in groups on the basis of chronicity of SCI (subacute and chronic). Thompson et al12 re-H-REFLEX AFTER BICYCLE AND LOCOMOTOR TRAINING, Phadke

ported that acute SCI injured rats show almost normal patternsof H-reflex rate depression (another measure of homosynaptic
depression) and that as they progress to the chronic stage, theylose the rate depression. Schindler-Ivens and Shields2 confirmed in human subjects that rate depression is relatively
unaffected in acute SCI, but as the subjects progress to thechronic SCI, they successively begin to lose rate depression.
Although not statistically different in the current study, within
the pretraining groups, there was a trend for the subacute
subgroup to have greater depression compared with the chronic
subgroup (subacute .51⫾.26; chronic .62⫾.24). Consistent
with earlier studies reporting a training effect of increased rate
depression,43,54,55 bicycle training in this study resulted ingreater depression in subjects with chronic SCI.
In a spinal cord–injured nervous system, reflex modulation is
impaired in both static state (such as in the semireclined position in the current study) and dynamic states (stance and swing
phases of walking). The impaired ability to modulate reflexes
in a task-specific manner is reflected in the findings of increased reflex amplitudes during walking post-SCI.7,8,30 Similarly, paired reflex depression is impaired post-SCI and thesecond H-reflex (percentage of the first) is not significantly
depressed (see fig 2). Thus, the inability to modulate reflexes
tested in 2 different ways (paired reflex depression paradigm
and phase specific H-reflex modulation in walking) and 2
different postures suggests the possibility of shared common
neural elements. We found a moderate negative correlation
between walking H-reflexes (dynamic state) and reflex depression tested in semireclined position (static state) in the current
study. Thus, in SCI subjects with greater than normal amplitudes of walking reflexes (dynamic position), a similar loss ofdepression is also seen in the semireclined static position. This
correlation between reflex depression and walking reflexes
suggests that the increased depression seen postbicycle training
may also be related to a concomitant decrease in H-reflex
amplitudes in walking; however, the design of our current
study did not allow us to test walking H-reflexes immediately
posttraining. In the current study, the H-reflexes tested during
walking did not change posttraining (locomotor and bicycle). It
has been previously reported that a single bout of bicycle
training58 and locomotor training30 increases soleus H-reflex
amplitude depression. In the current study, we did not test
overground H-reflexes immediately after training (reflex depression was tested immediately posttraining). It is conceivablethat any potential neurophysiologic changes in walking Hreflex modulation may not have persisted at approximately 1hour posttraining.
Training effects such as improvements in synaptic efficacy
and increase in H-reflex paired reflex depression46,59 andsmaller peak amplitude58 have been reported in noninjured
human subjects after a single bout of bicycle training. The
above studies, however, used a skilled bicycling task thatinvolved variable resistance, whereas we used a simple bicycling task with consistent cadence and no resistance. In thecurrent study, although we did not observe significant difference in depression pre- versus postbicycle training in noninjured subjects, there was a robust trend toward an increase indepression postbicycle training. It is likely that this study was
somewhat underpowered for statistical significance. The effectof bicycle training is not global but is targeted in the spinal
segments (motor and sensory) that are actively participating in
the task of bicycling.60 In addition, bicycling has been reported
to induce phase-specific modulation of transmission in thecorticospinal pathways (increases during early downstroke)
and the presynaptic inhibition (depressed soleus H-reflex during late downstroke and upstroke).9,61-63

1225

The current study and others56,59 report an activity-dependent increase in paired reflex depression posttraining. It will be
important to examine the paired reflex depression in a dynamic
task such as bicycling. Serially examining reflex depression
during the course of several weeks of bicycle training insubjects with incomplete SCI may provide us with an opportunity to examine the functional correlation between reflex
depression and walking recovery. Although walking speed
increased significantly postbicycle training and postlocomotor
training, the change postlocomotor training (.29m/s) was clinically more significant compared with the increase postbicycle
training (.07m/s). Thus, it is clear that the magnitude of change
is greater postlocomotor training. It is unlikely that bicycle
training by itself will produce changes in walking speedof the magnitude such as that seen postlocomotor training.
However, the finding that bicycle training significantly increased reflex depression suggests that bicycling may have arole as an adjunct, complementary, and interactive effect withother walking retraining strategies, including locomotor training.
Possible Mechanisms
Impaired reflex depression in subjects with incomplete SCI
as compared with noninjured control subjects is in agreementwith earlier studies.13,25,27 The underlying mechanism forpaired reflex depression is believed to be presynaptic in nature4,12,18,20,23,64-67 and likely regulated by the probability ofneurotransmitter release in the Ia afferent nerve endings in the
spinal cord.18,27 It is believed that this presynaptic effect islikely controlled by activation of GABA-ergic interneurons68,69
through controlled release of synaptic transmitter.70
Treatment of spasticity with baclofen (a GABA-B agonist
that presumably produces a tonic presynaptic inhibition; antispastic) decreases muscle tone and/or increases voluntary motor control71 and has been reported to improve modulation of
the stretch reflex during walking.72 In the current study, 4
subjects were receiving antispastic medication and 5 subjects
were not. All SCI subjects receiving spasticity medication
showed greater depression compared with the subjects receiving no spasticity medication (antispastic medication .29; no
medication .69). In the medication group, the level of depression increased postbicycle training but not postlocomotor training. It is therefore possible that the impaired depression observed in the subjects with SCI in the current study may havebeen due to disruption of the normal GABAergic regulation ofpresynaptic processes. However, the reverse may not be true,and H-reflex has not been shown to be predictive of outcomes
post-SCI.
Synaptic efficiency is modulated by various neurotransmitters (eg, serotonin or 5-HT). It follows, then, that the damage
to the descending tracts from the brain stem that carry a steadysupply of neurotransmitter may cause an impaired depression
post-SCI. Paired reflex recordings performed in lampreys haverevealed that activity in spinal cord interneurons is either
depressed or potentiated based on physiologic frequencies ofstimulation (interstimulus interval range of 200ms to 50ms,
respectively). Interestingly, the presence of neuromodulatorssuch as substance P and 5-HT catalyzes the depression ofpaired-reflex amplitudes.73 Post-SCI, the 5-HT receptors caudal to injury level become hypersensitive to 5-HT, most likely
because of meager amounts of endogenous 5-HT below thelesion.74 On the basis of animal studies, it is possible thatin the current study, bicycle training (compared with training
on the treadmill) may have induced a greater release of 5-HTin the lumbar spinal cord, resulting in an increase in paired
reflex depression.75,76 Along with an increase in spinal excitArch Phys Med Rehabil Vol 90, July 2009

1226

H-REFLEX AFTER BICYCLE AND LOCOMOTOR TRAINING, Phadke

ability, concomitant reemergence of persistent inward currents
is seen after chronic SCI.77,78 The lower level of depression
post-SCI and the increase after bicycle training may be related
to alteration in the modulation of the persistent inward currents78,79; future studies need to explore this relationship.
CONCLUSIONS
On the basis of the results of bicycle training in the current
study, 2 important questions arise: first, could the increase indepression after a single bout of bicycling be due to theconsistency of movement kinematics, lack of weight bearing
on the legs, or the lesser demands placed on posture? Second,is there a direct correlation between level of depression andfunctional outcome measures?40 At the 100-millisecond interval, single-session bicycle training normalized (increased depression) to a level commensurate with noninjured subjects. In
order to understand its potential role in walking rehabilitation,
future studies need to examine the long-term effects of bicycle
training on subclinical measures of reflex activity. Soleus Hreflex amplitude has been correlated to locomotor function in
the rat SCI model80; similar relationships between H-reflex andfunctional outcomes need to be tested in human subjects with
SCI.
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