644 IEEE TRANSACTIONS ON BIOMEDICAL ENGINEERING, VOL. 36, NO.
7, JULY 1989
Tetanic Responses of Electrically Stimulated
Paralyzed Muscle at Varying Interpulse
Intervals
Abstract-The influence of stimulus interpulse interval (IPI) on
torque output during electrically-evoked contractions was investigated
for the knee extensor muscles of paralyzed subjects. The parameters
measured were the rise time, magnitude, and relaxation time of the
contraction at stimulus IPI’s ranging from 62 to 7 ms. Torque output
increased as IPI’s were decreased from 62 to 15 ms. Peak torques were
recorded at IPI’s of 12-15 ms; IPI’s less than these resulted in an in-
significant loss of torque. Rise times decreased as IPI’s were decreased.
Relaxation time generally increased as IPI’s were decreased with the
longest relaxation times occurring with stimulation at an IPI of 12 ms.
To demonstrate the influence of IPI on muscle fatigue, the effect of
prolonged stimulation at short (12 ms) and long (50 ms) IPI’s was also
compared. After 30 s of stimulation with an IPI of 12 ms, mean torque
had declined to 5 f 3 percent and after 30 s of stimulation with an IPI
of 50 ms, mean torque had declined to 82 f 4 percent of the initial
value. Knowledge of how stimulus IPI influences the response of par-
alyzed muscle to electrical stimulation may assist in the development
of rehabilitation devices which utilize these technologies.
INTRODUCTION
I N recent years there has been increasing interest in the
utilization of functional neuromuscular stimulation
(FNS) for augmenting or restoring function in patients suf-
fering from upper motor neuron lesions [4],[7], [22].
Since 1983, we have worked with thoracic level spinal
cord-injured volunteers to develop an FNS system using
percutaneous intramuscular electrodes [ 181. In total, eight
subjects have been able to ambulate with the aid of a
walker and, of these, three are able to ascend and descend
stairs. Progress in the areas of electrode design and im-
plantation techniques, and the increasing sophistication of
hardware and software has enabled some of these individ-
uals to walk at speeds which begin to approach normal.
As ambulation speed increases, less time is available for
Manuscript received June 8, 1988; revised November 8, 1988. This work
was supported by the Rehabilitation Research and Development Service of
the Veterans Administration.
S. G . Carroll was with the Motion Study Laboratory, Veterans Admin-
istration Medical Center, Cleveland, OH 44106. She is now with the De-
partment of Physiotherapy, Austin Hospital, Heidelburg, Victoria, Aus-
tralia.
R. .I.Triolo is with Shriners Hospital for Crippled Children, Philadel-
phia, PA.
H. J. Chizeck is with the Departments of Systems and Biomedical En-
gineering, Case Western Reserve University, Cleveland, OH 44106.
R. Kobetic is with the Motion Study Laboratory, Veterans Administra-
tion Medical Center, Cleveland, OH 44106.
E. B. Marsolais is with the Department of Orthopaedics, Case Western
Reserve University, Cleveland, OH 44106.
IEEE Log Number 8927445.
.OO
0018-9294/89/0700-0644$01
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achieving the muscle contractions needed to complete
each phase of the gait cycle. In other words, the time taken
for the generation of torque in part determines the speed
of ambulation. Coordination and timing of muscle con-
tractions have therefore become key aspects in the design
of open-loop stimulation sequences for gait and other
functional tasks.
In order to assist in the design of such sequences, we
undertook a study of the responses of paralyzed quadri-
ceps muscles. This study was designed to compare the
rate and magnitude of torque development and relaxation
at the knee during tetanic stimulation at a wide range of
interpulse intervals (IPI’s). A brief study contrasting the
rate of torque loss during prolonged stimulation at short
and long IPI’s was also performed. The results of this
work and the implications with respect to the development
of FNS systems are discussed.
Outline
METHODS
Two phases of experiments were required for this study.
In the initial phase, the response time of the torque-mea-
suring device was determined to verify its adequacy for
measuring the rise time of muscular contractions. Exper-
iments to measure the response time of the system alone,
the response time of the system with the unstimulated leg
of a subject attached, and, finally, the combined response
time of the system and the subject’s leg during an electri-
cally-evoked contraction of the quadriceps muscles were
performed. The results revealed that this system was ad-
equate for measurements of muscle rise times. Details of
the methods used, the equipment and the results of these
experiments are given at the end of the “Methods” sec-
tion. The goal of the second and major phase of experi-
ments was to characterize the responses of the paralyzed
quadriceps muscle to stimulation at varying IPI’s.
Subjects
Data were collected from two subjects who were par-
ticipants in a project to restore functional tasks in para-
lyzed individuals. Both had suffered complete spinal cord
lesions at the level of T-7/T-8 at least five years previ-
ously and had been involved in the project for a minimum
of four years. Percutaneous intramuscular electrodes were
O 1989 IEEE

CARROLL PI al ’ RESPONSES OF ELECTRICALLY STIMULATED PARALYZED MUSCLE
implanted at the motor points of most of their major lower
limb muscles [17] and both subjects had performed daily
electrical exercise of their lower limbs for at least 30 min
in the forms of ambulation, stair climbing, standing, and/
or a seated exercise program during their years of partic-
ipation in this project [ 191.
Stimulation Equipment and Procedures
The subjects were seated on a Cybex I1 dynamometer
bench (Cybex, Lumex, Ronkonkoma, NY) with the knee
of the test leg fixed securely in 30” of flexion. This angle
was chosen as it fell within the range of angles shown to
permit generation of maximal voluntary torque in normal
subjects [14], [21]. A total of nine electrodes implanted
in the vastus medialis, vastus lateralis, and/or vastus in-
termedius muscles of both subjects were tested. Isometric
contractions were evoked by a laboratory-built, micropro-
cessor-controlled, portable stimulator [27] which utilized
constant-current pulses of 20 mA in amplitude and a fixed
pulsewidth of 150 p s .
The experimental protocol was designed to produce
steady-state tetanic contractions without inducing signif-
icant potentiation or fatigue. Prior to the commencement
of data collection, each muscle was “warmed up” with
ten isometric contractions. The duty cycle was 2 s on/
3 s off and the stimulus frequency was 25 Hz. The mus-
cles were then rested for at least 5 min to allow any effects
of potentiation to dissipate [9]. The experimental protocol
consisted of 10 trains of stimulation; each being 900 ms
in duration and each utilizing a different IPI. In all cases,
900 ms of stimulation was sufficient to allow the muscle
to reach a steady-state torque output. The intertrain inter-
val was 30 s and IPI’s of 7, 10, 12, 15, 18, 20, 40, 50,
5 5 , and 62 ms were chosen as they corresponded to fre-
quencies within the ranges recorded in discharging motor
units during voluntary contractions of normal muscles
[lo], [ 151. To cancel out any effect of fatigue or potentia-
tion, the IPI’s were tested in the ascending order in ap-
proximately half of the experiments while the descending
order was used in the remaining experiments. The trial-
to-trial and day-to-day reliabilities of the results were as-
sessed by repeating the experiment on a minimum of three
occasions using two electrodes. No less than ten minutes
or three days elapsed between tests of trial-to-trial and
day-to-day repeatability, respectively.
Fatigue Study
The influence of IPI on torque decline during continu-
ous quadriceps stimulation was performed on a total of
seven electrodes from both subjects. IPI’s of 12 and 50
ms were chosen to represent stimulation with high and
low frequencies, respectively. The fatiguing procedure,
consisting of 150 s of continuous stimulation with a pulse
duration of 150 p s , was performed on each of the seven
electrodes at the two test IPI’s on separate occasions. The
experimental setup including the stimulator, torque mea-
suring system, and angle of testing was identical to that
described above. The fatigue experiments were per-
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-
645
formed at least one week apart and the order of testing
was at random.
Recording
Torque was detected using a Cybex dynamometer which
had been instrumented with strain gauges. The strain
gauge output was amplified, filtered at 50 Hz, and stored
by a MINC 11/23 microcomputer (Digital Corp., May-
nard, MA). The sampling rate employed in the fatigue
experiments was 50 Hz; for all other experiments, a sam-
pling rate of 250 Hz was utilized. A two-point calibration
was employed and testing of the system using known
weights showed that the output voltage versus torque was
linear at all positions. After completion of each experi-
ment, the data were transferred onto a MicroVax I1 com-
puter (Digital Corp., Maynard, MA) for plotting and
analysis.
Characterization of the Torque Measriring
System: Methods
The transfer function of the instrumented Cybex appa-
ratus was determined by recording the system response to
a step change in torque. A step input, beginning at an
initial negative level, passing through zero to a final pos-
itive steady-state value, was used to simulate the action
of the quadriceps muscles during an isometric contrac-
tion. Weights were suspended below the arm of the Cybex
with a thin wire, and above the arm by a wire looped
through a pulley attached to the ceiling. The weight below
the arm was always larger than that suspended above the
arm so that the net torque acted downwards. The step in-
put was created by cutting the wire suspending the bottom
weight, resulting in a net torque acting in the upward di-
rection. The response of the system to this “instanta-
neous” change in torque was recorded using the same
procedures as described above. The wire was also instru-
mented to provide a timing signal which indicated the ex-
act instant the step was applied for delay and rise time
calculations. All strain gauge measurements were syn-
chronized to this timing signal for averaging. Step re-
sponses were collected in this manner from 1) the instru-
mented Cybex arm alone, and 2) with the passive,
unstimulated leg of a paraplegic subject fixed firmly to the
apparatus. In all cases, the Cybex arm was held at a con-
stant position, 30” below the horizontal.
The responses from stimulated muscle were determined
in a second series of experiments. In addition to the pas-
sive mechanical tests, step responses were generated ac-
tively by stimulating the quadriceps muscles while the
subject’s leg was attached to the Cybex arm. The stimu-
lator was modified to produce a timing signal which cor-
responded exactly to the onset and cessation of stimula-
tion for delay and rise time calculations and for
synchronization purposes. All analyses were repeated on
the downward step associated with the removal of stim-
ulation during relaxation of the muscle to further charac-
terize the system.
The step responses recorded from the strain gauges un-
der each of the test conditions were averaged to eliminate
 IEEE TRANSACTIONS ON BIOMEDICAL ENGINEERING. VOL. 36. NO. 7. J U L Y '980

TABLE 1
SUMMARY
O F INSTRUMENTED
CYBEX
APPARATUS
STEPRESPONSES
A N D TRANSFER
FLSCTIONS

Bandwidth
(Hz) Resonant Rise
Peak Time Percent Delay
Stat 3 dB (Hz) (ms) Overshoot (ms)

Cybex ( n = 7 ) 18.8 18.2 15.8 24 44.5 4

Cybex plus leg ( n = 6 ) 10.7 7.3 6.2 32 29.2 4
Stimulation ( n = 9 ) 7.7 2.1 - 88 4.5 40
Relaxation ( n = 8 ) 7.4 4.9 - 84 19.3 64

Normalized Torque
1.6

1.2

n - 9

-0.2' I 1 I I I I 1 1 I
-0.2 -0.1 0.0 0.1 0.2 0.3 0.4 0.5 0.6 0.7
Time (seconds)
(a)

Normalized Torque

1.4

n - 6

1
-0.2 I I 1 1 1 I I I 1

-0.2 -0.1 0.0 0.1 0.2 0.3 0.4 0.5 0.6 0.7
Time (seconds)
(b)
Fig. 1, Normalized average step responses of the instrumented Cybex ap-
paratus. ( a ) The mechanical response of the Cybex system including the
passive mass of an unstimulated leg, (b) the step response of the system
with constant stimulation of the quadriceps. Note the differences in rate
of rise, overshoot, and delay. All responses are synchronized to the ap-
plication of the step input and normalized to a steady state value before
averaging [mean values for (a) and (b) were 29.2 and 56.4 N ' m . re-
spectively]. Plots show mean. maximum. and minimum values at each
instant of time.

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 C A R R O L L er U/. RESPONSES OF ELECTRICALLY S T I M U L A T E D P A R A L Y 7 E D M U S C L E
Frequency (Logarithmic scale)
(a)
10-1 100 10'
Frequency (Logarithmic scale)
(b)
Fig. 2 . Average transfer functions of the instrumented Cybex apparatus.
(a) System response of Cybex with passive, unstimulated leg attached.
(bj transfer function of the system with active contraction of the quad-
riceps muscles. The transfer function of the passive system is consist-
ently characterized by a flat response up to a resonance and followed by
a prominent null. The response of the stimulated system begins to atten-
uate at frequencies above 2 Hz. Statistical bandwidths are indicated.
fluctuations due to random noise. Transfer functions were
calculated by differentiating the average step responses to
obtain the impulse responses of the system, and then com-
puting the power spectral density. A differentiating filter
with a bandwidth of 50 Hz was used, after which a digital
low-pass filter with a bandwidth of 50 Hz cutoff was ap-
plied to prevent the introduction of high frequency noise.
Equivalent statistical and half-power ( 3 dB ) bandwidths
[2] were computed for the transfer functions of the Cybex
alone, the Cybex and the unstimulated leg, and the Cybex
and the actively contracting leg during both the generation
and relaxation of knee extensor torque. Rise times,
overshoots, and delays were also compiled from each of
the average step responses.
Characterization of the Torque Measuring
System: Results
The characteristics of the instrumented Cybex appa-
ratus are summarized in Table I . The Cybex arm alone
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647
exhibited a flat response out to a frequency of approxi-
mately 8 Hz at which point a prominent null was observed
in the spectrum. This was consistently followed by a flat
response at the same level and a resonant peak at approx-
imately 16 Hz. The half power and statistical bandwidths
were both between 18 and 19 Hz in this case. Addition of
the passive leg resulted in a shift to lower frequencies out
to a resonant peak at about 6 Hz, followed by a major null
at 8 Hz. The statistical and half-power bandwidths in this
case were 8 and 11 Hz smaller than those characteristic
of the system without the mass of the leg. The average
step responses of the system with and without stimulation
are shown in Fig. 1. Fig. l(a) illustrates the step response
of the Cybex and the unstimulated leg while Fig. l(b)
shows the average step response obtained by stimulating
the quadriceps muscles. The step responses produced by
the contracting muscle displayed longer rise times, larger
delays, and smaller overshoots than those seen in the sys-
tem with the unstimulated leg.
The responses elicited by stimulation of the quadriceps
muscles were characterized by transfer functions which
showed an additional shift to lower frequencies. Fig. 2
shows the transfer functions associated with each step re-
sponse pictured in Fig. 1 . The transfer function of the
Cybex arm and the passive leg is presented in Fig. 2(a)
while that of the system during stimulation is given in
Fig. 2(b). The statistical bandwidth of the system during
stimulation was 7.7 Hz compared to the 10.7 Hz band-
width of the passive system. In addition, the stimulated
10' and passive systems exhibited half power bandwidths of
approximately 2.1 and 7.3 Hz, respectively, as shown in
Table I. These results indicate that the instrumented Cy-
bex apparatus is capable of passing all frequencies of in-
terest in the stimulated muscle response without distor-
tion. The instrumentation, including the mass of the leg,
is of sufficient bandwidth to measure the responses of the
quadriceps muscles to stimulation.
RESULTS
Parameters
Fig. 3(a) shows typical responses from one electrode at
IPI's of 12, 20, 50, and 62 ms. An initial overshoot with
several secondary oscillations was seen for all electrodes
during stimulation with IPI's of and less than 40 ms.
Maximum torque was therefore defined as the average
steady-state output occurring during a 100 ms window.
beginning 750 ms after the onset of stimulation. The de-
gree of fusion induced by stimulation at each IPI was as-
sessed by measuring the amplitude of the ripple and ex-
pressing it as a percentage of maximum torque [6]. Tetanic
response time was defined as the time taken for torque to
rise from 10-90 percent of maximum ( t 10-yOpercent ). To as-
sess rise time independently of changes in torque, rise time
was also expressed in units of time per Newton meter.
Relaxation time was similarly defined as the time taken
for torque to decay from 90 to 10 percent of maximum
( t y O ~ I o p e r c and
c n t ) also expressed in units of time per New-
 648 IEEE TRANSACTIONS ON BIOMEDlCAL ENGINEERING. VOL. 36, NO. 7, IULY 1989

: IPI-I2

a-
IW 7 IPI=*O

I-
n
E IPI=SO
I 1-
Z
v
u
3
Y =-
I-

*-

e-

-* ; 1 I I I 1 I I I
0 U I4 U U I I1 I4 I6 I
Time (Second)

(a)

(b)
Fig. 3. (a) The response of one electrode to stimulation at IPI’s of 62, 50,
20, and 12 ms. Note the initial overshoot during contractions at IPI’s of
20 and 12 ms and the incomplete fusion during stimulation at IPI’s of
50 and 62 ms. (b) The method for measuring rise time, relaxation time,
and the 100 ms window used for calculating maximum torque. The onset
of stimulation is marked by an arrow.

ton meter. Definitions and measurements of the above pa-
rameters are shown in Fig. 3(b). Repeatability was deter-
mined by calculating the mean percentage error at each
IPI for two electrodes tested on a minimum of three oc-
casions.
As absolute values for torque, rise time, and relaxation
time varied considerably from electrode to electrode for
both subjects, pooled results from the electrodes have been
presented as normalized values. The mean response for
each electrode following stimulation at all test IPI’s was
given the value of 100 percent and the value for each IPI
was normalized with respect to this mean. The normal-
ized data from the individual electrodes were then pooled
for each IPI. The ranges of absolute values for torque,

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 CARROLL et al. : RESPONSES OF ELECTRICALLY STIMULATED PARALYZED MUSCLE 649

TABLE 11 % Max Torque

RANGE OF ABSOLUTE VALUES FOR MAXIMUM TORQUE,RISETIME,AND 120 r

RELAXATIONT I M EFOR EACH ELECTRODE TESTED OVER A N IPI RANGE OF

1-62 ms. LAT = VASTUS LATERALIS; MED = VASTUS MEDIALIS; INT =
VASTUSINTERMEDIUS. WHENTwo MUSCLES A R E LISTED PER ELECTRODE,
THE FIRSTMENTIONED MUSCLE IS T H E PRIMARY CONTRIBUTER TO TORQUE

Range of Range of

: l i
Range of Rise Relaxation
Torques Times Times
Subject Muscle ( N - m) (ms) (ms)

RL L lnt/Lat 54-79 233-201 81-108 20

R Lat 30-44 165-93 70-95 10 5 10 15 20 25 30 35 40 45 50 55 60 65
L Med/Int 25-36 231-93 59-95
L Lat 35-51 240- 170 73-101
I P I las)
BK R Lat/Int 37-60 333-191 63-9 1
L Int 69-91 236-76 70-95 Fig. 4. Influence of stimulus IPI on maximum torque. Each point is the
L Lat 18-24 214-106 36-68 mean normalized response* of 9 electrodes f 1 standard deviation (SD).
R Med 28-63 103-65 69-91 * The mean response for each electrode following stimulation at all test
R Lat 36-61 95-60 61-89 IPIs was given the value of 100 percent and the value for each IPI was
normalized about this mean. The normalized data from the individual
electrodes was then pooled for each IPI.

rise time, and relaxation time together with a profile of

each electrode are given in Table 11. 200 -

180 -
Tetanic Torque
160 -
Despite the wide variation in the magnitude of torque
140 -
produced by the electrodes, a clear relationship between
120 -
IPI and maximum torque emerged (Fig. 4). For IPI’s be-
100 -
tween 55 and 20 ms, torque increased linearly as IPI was
decreased. No statistically significant changes in torque BO -
were obtained with IPI’s less than 20 ms although peak 60 -
torque was recorded at IPI’s of 12 or 15 ms for ail elec- 40 -
trodes. A consistent albeit insignificant decrease in torque 20 -
was observed when IPI’s less than 12 or 15 ms were used. 0
1. . . .1. . . .1. . . .1. . . . ’ . . . .1‘ . ‘ . ‘ . ‘ “ ‘ . ” .

The mean difference between minimum and maximum

relative torques was 37 i- 8 percent. No ripple was ob-
served during contractions using IPI’s of 20 ms and less.
At IPI’s of 40, 50, 5 5 , and 62 ms, the mean ripples were
3 f 1 percent, 4 i- 1 percent, 4 f 1 percent, and 7 f 2
percent of maximum torque, respectively. Tests of re-
peatability using two electrodes showed that mean trial-
to-trial errors were always less than the mean day-to-day
errors ( T - T : 2.4 f 1.9 percent versus D-D: 7.2 f 4.7
percent: p < 0.02). In addition, a clear effect of IPI on
the repeatability was observed for both trial-to-trial and
day-to-day errors. The average trial-to-trial mean per-
centage errors for stimulation at IPI’s equal or greater than
50 ms was significantly greater than for IPI’s less than 50
ms (IPI > 50, x = 4.8 k 1.5 percent versus IPI < 50,
x = 1.3 f 0.6 percent, p < 0.001). A similar pattern
was seen for day-to-day errors although the critical IPI
was 40 ms ( IPIs > 40, x = 12.5 i- 1.9 percent versus
IPI’s < 40, x = 3.6 f 1.3 percent, p < 0.001).
Rise Times
As was seen for torque output, considerable variations
in rise times were observed between the electrodes. In all
cases, however, the time required for torque to increase
from 10 to 90 percent of maximum increased in a linear
fashion as the stimulus IPI was lengthened so that the fast-
est responses were recorded with stimulation at the short-
est IPI’s (Fig. 5 ) . In addition to expressing rise time sim-
ply in units of time, it was also expressed as the rise time
per Newton meter. This permitted an assessment of the
influence of IPI on rise time without the confounding
variable of torque which, as we have seen, was also influ-
enced by IPI. Fig. 5 illustrates that the rise time was par-
ticularly sensitive to changes in IPI’s of 40 ms or more
when it was expressed for a constant level of torque. In-
deed, the mean differences between minimum and maxi-
mum relative values of rise time and rise time per Newton
meter were 59 It 27 percent and 95 f 38 percent, re-
spectively. Examination of trail-to-trial variations re-
vealed no influence of IPI. The average mean percentage
errors for all IPI’s was 3.8 f 1.5 percent. Day-to-day
variations were also small for all IPI’s except when the
IPI was 62 and 40 ms. The average mean percentage error
for all other IPI’s was 2.0 f 1.4 percent. For IPI’s of 62

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 650 IEEE T R A N S A C T I O N S ON B I O M E D I C A L E N G I N E E R I N G . VOL 36. N O 7. JULY 1989

contrast, a slow and incomplete loss of torque accom-

:I A
100 -
panied continuous stimulation at IPI’s of 50 ms. At the
5 s sampling point mean torque had declined to 97 f 2
90- percent and at the 30 s sampling point it had declined to
BO ~
82 f 4 percent. After 150 s of continuous stimulation, 20
70 - f 9 percent of the mean torque was still being generated.
60 -
I Fig. 7 illustrates a typical pattern of torque loss at both

:I
40
50

10
0
I
5
, , 1 , , , , , 1 , , ~ , ~ , , , , , , , , , , , , , , , , , , , , , ,

10 15 20 25 30 35 40
~ ,,,,

65
LLLULLLLUILLV
50 55 60
1
65
IPI’s for one electrode. This trend was observed in all
electrodes tested.

IPI (msl
Fig. 6 . Influence of stimulus 1P1 on relaxation time. Relaxation time was
calculated as the time required for torque to decay from 90 to 10 percent
of maximum. Each point is the mean normalized* response from 9 elec-
trodes I SD.
Torque (N-m)
0 ‘ I
L..-
”
---_ ...~....,....
.-..,.*.
0 20 40 60
Tine (seconds o f stimulation1
Fig. 7. Comparison of rate of torque decline during continuous stimulation
of one electrode at IPI’s of 12 ms (dashed line) and 50 ms (solid line).
All seven electrodes displayed a similar pattern of torque decline.
and 40 ms, however, the average mean percentage error
was 10.4 f 0.4 percent.
Relaxation Time
The time taken for torque to decay from 90 to 10 per-
cent of maximum was generally inversely proportional to
the length of the IPI (Fig. 6). This trend was observed for
IPI’s from 62 to 12 ms; stimulation at IPI’s less than 12
ms resulted in a decrease in relaxation time. In contrast
to rise time, IPI showed no effect on relaxation time when
this parameter was expressed as time per Newton meter.
Assessment of trial-to-trial and day-to-day variations re-
vealed average mean percentage errors of 2.53
cent and 4.83 f 4.13 percent, respectively.
1.9 per-
Effect of IPI on Torque Decline During Fatigue
A very rapid decline of torque occurred during contin-
uous stimulation at IPI’s of 12 ms. After only 5 s of stim-
ulation, mean torque output had decreased to 81 k 24
percent and only 5 f 3 percent of torque was recorded at
the 30 s sampling point. No significant torque could be
measured during the remaining period of stimulation. In
DISCUSSION
The relationships observed between IPI and maximum
torque and IPI and rise time concur with previously pub-
lished studies of mammalian muscle 131, [25]. Specifi-
cally, our observation that torque output was inversely
proportional to the duration of the stimulus IPI was de-
scribed by Edwards and colleagues who examined the re-
sponses of normal quadriceps muscles to electrically
evoked contractions [9], [20] and by Peckham and col-
leagues who recorded responses of paralyzed forearm
muscles during electrical stimulation [24]. Moulds’ re-
sults are also in agreement with our finding that peak
torque occurs at IPI’s of 12-15 ms. The increase in rise
time in response to a lengthening IPI has been docu-
mented in vivo previously for isometric contractions of
adductor pollicis [ 161 but not for the quadriceps. Rise time
displayed a greater sensitivity to the stimulus IPI than did
torque. Although this sensitivity was more pronounced for
rise time per newton meter than for rise time, this obser-
vation is of little clinical value as one cannot separate the
---.-,--.-t...-C. .
* . - -.
. . effect of IPI on rise time from its effect on torque. To the
EO 100 120 140
best of the authors’ knowledge, the apparent absence of
effecr of IPI on relaxation time has not been documented
previously. In summary, the responses observed in the
quadriceps muscles of these two spinal cord-injured sub-
jects were not markedly different from responses recorded
in “normal” human muscles. A longitudinal study doc-
umenting changes in the contractile properties of quadri-
ceps muscles in paralyzed subjects is needed to elucidate
the magnitude and the rates of such changes. It is antici-
pated that these data will be collected from future subjects
who join this project.
Several findings relating to the generation of torque
should be of interest to developers of FNS systems. First,
the mean difference between minimal and maximal torque
output over the range of IPI’s tested was relatively small
(37 -t 8 percent) and a substafitial portion of this differ-
* ence was due to stimulation at an IPI of 62 ms. This find-
ing indicates that frequency modulation alone may not
provide the ranges of torque which would be needed to
achieve a variety of functional tasks and supports the
premise that a combination of recruitment and temporal
summation provides the most effective form of force mod-
ulation [6].
The phenomenon of “high-frequency fatigue,” char-
acterized by a rapid torque decline during stimulation at
high frequencies, is well documented 1121, [13], and has

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 CARROLL et U / . : RESPONSES OF ELECl-RlCALLY STIMULATED P 4 R A L Y Z E D MUSCLE
been observed during contractions of less than a second’s
duration in the human adductor pollicis [16]. It appears
from our data that stimulation at IPI’s of 12 ms or less
induced high frequency fatigue even before the muscle
reached its maximal torque. The possible alternative ex-
planations that potentiation of the torque response at IPI’s
of 12-15 ms was responsible for the apparent decline in
the response at the shorter IPI’s or that the repeated brief
tetanic contractions induced a form of contractile fatigue
are negated by the observation that this phenomenon oc-
curred when IPI’s were tested both in ascending and de-
scending order.
Intrasubject variations in both the rate and magnitude
of the torque response should be of concern to the de-
signer and ultimately to the user of an FNS system for
whom safety and reliability are key issues. Three sources
of variation, namely intersubject, intrasubject, and intra-
electrode, were noted during this study. The variability of
torque output both within and between subjects generally
increased as IPI’s were increased, apparently reflecting
the inverse relationship between IPI and the degree of fu-
sion achieved. Studies of cat muscle have shown that this
variability at long IPI’s can be reduced if asynchronous
rather than synchronous stimulation is used [25]. Al-
though sequential stimulation of motor nerve roots has not
been performed in human subjects, a modified version of
this technique has been used with some success by Peck-
ham and colleagues in their FNS system designed to aug-
ment grasp in the paralyzed upper limb [23]. The wide
range of torque values recorded for electrodes implanted
in the same subject reflects one of the inherent problems
with the percutaneous method of implantation, namely the
difficult task of positioning the electrode so that a maxi-
mum number of muscle fibers lie within its electric field.
The intrasubject variation associated with measurement of
rise times, however, can hardly be explained by differ-
ences in the numbers of fibers recruited by each electrode.
One possible explanation is that the proportion of fiber
types varied from electrode to electrode within the same
subject according to the electrode’s depth of placement
[ 111 and its history of activation. While the “fast to slow
twitch” conversion of muscle fibers in animals by pro-
longed electrical stimulation has been examined exten-
sively in recent years [26], conclusive evidence of this
type of transformation occurring in human muscle, nor-
mal or paralyzed, is lacking.
Although measures were taken to avoid any effect of
potentiation, fatigue, or subject movement, it is possible
that one or all of these factors contributed to the small
trial-to-trial variations that were observed. Similarly, the
larger day-to-day variations could have been induced by
factors which proved difficult to completely control,
namely ensuring the exact repositioning of the subject on
the Cybex apparatus and avoiding any long term fatigue
induced by extensive activity on the day or days preceding
the experiments. In summary, because of the variation
seen between electrodes and between subjects, consider-
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65 I
able “fine tuning” of the stimulus parameters is neces-
sary if FNS patterns are to be successfully transferred from
one to another.
With ongoing progress towards the development of an
implantable FNS system, timing and coordination of mus-
cle contractions have become critical factors in the design
of open-loop stimulation sequences. The nearly two-fold
increase in the mean relative rise time observed for IPI’s
ranging from 7 to 62 ms highlights the importance of se-
lecting the appropriate IPI’s for each task or part thereof.
For example, to achieve a gait pattern which is cosmeti-
cally acceptable, functional with respect to speed, and
which requires minimal energy expenditure, advantage
must be taken of the momentum generated by the moving
body. Among the many actuators which generate and/or
conserve momentum during the gait cycle are the hip ex-
tensors during stance phase and the hip flexors during
swing phase. The former should be activated rapidly upon
detection of heel strike and the latter once weight transfer
to the stance leg has been accomplished. The above ex-
amples include the assumption that other paralyzed mus-
cles demonstrate the same pattern of response as seen with
the quadriceps. Although this is highly likely, the need to
investigate the responses of muscles such as the hip flex-
ors and extensors is acknowledged.
Closed-loop systems which permit prolonged standing
with minimal stimulation are designed to respond to an
increasing angle of knee flexion by stimulating the quad-
riceps to bring the knee back into full extension [l], [ 5 ] .
In such a case, the use of IPI’s in the range of 12-15 ms
would, based on our findings, provide a maximal re-
sponse within 200 ms.
If reliable generation of maximal torque in minimal time
was the sole requirement for successful FNS applications,
we would conclude from this paper that stimulus IPI’s in
the range of 12-15 ms should be used by designers of
open- and closed-loop stimulation sequences. This con-
clusion would be valid if only brief, intermittent contrac-
tions were required. Most of the FNS sequences designed
to augment or restore function, however, utilize continu-
ous or cyclical contractions over prolonged periods of
time. Our brief fatigue study was included to highlight the
much-studied observation that the rate of force loss during
continuous prolonged stimulation is inversely propor-
tional to the stimulus IPI used [ 131. To take advantage of
the rate, magnitude, and reliability of the forces generated
by shorter IPI’s, without inducing immediate fatigue, the
stimulus IPI should be modulated throughout each burst
of stimulation. We recommend an initial IPI of 15 ms
which is progressively increased over the duration of the
contraction. The slowing of the rate of relaxation which
accompanies fatigue [8] would lower the fusion frequency
of the muscle thus increasing the reliability of the re-
sponse at the longer IPI’s. To minimize fatigue further,
adequate rest periods must be incorporated into any stim-
ulation sequence. An investigation of the interaction be-
tween IPI, duty cycle, and fatigue is currently in progress.
 652 IEEE TRANSACTIONS ON BIOMEDICAL ENGINEERING, VOL. 36. NO. 7. JULY 1989
ACKNOWLEDGMENT
We gratefully acknowledge the contributions of Dr. J.
Lau for assistance in the implantation of electrodes, and
J. Abbas, G. Borges, and I. Zamir for their technical sup-
port.
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Sara G . Carroll was born on December 2 , 1959
in Subiaco, Western Australia. She received the
Bachelor of Applied Science degree in physio-
therapy with distinction in 1981 from the Western
Australian lnstitute of Technology, and the M.S.
degree in neurosciences in 1983 from McMaster
University in Hamilton, Ont., Canada.
In November 1985 she joined the staff of the
Cleveland Veterans Administration Motion Study
Laboratory where she collaborated on develop-
ment of FNS systems for restoring functional
movement in paralyze:d people. In July 1988 she returned to Australia where
she plans to continue research and teaching in the field of FNS.
Ronald J. Triolo (S’77-M’8O-S’81-M’86) re-
ceived the B . S . degree in electrical engineering
Summa Cum Laude from Villanova University,
Villanova, PA in June, 1980, the M.S. degree in
biomedical engineering, the M.S. degree in elec-
trical engineering, and the Ph.D. degree in
biomedical engineering from Drexel University,
Philadelphia, PA in 1982, 1984, and 1986, re-
spectively.
He is the Director of Research at the Philadel-
phia Unit of Shriners Hospital for Crippled Chil-
dren where he has been investigating the application of functional neuro-
muscular stimulation to pediatric patients with spinal cord injuries for the
purpose of restoring standing and walking function. His research interests
include biomechanics, EMG signal processing, and neural control of pos-
ture and locomotion.
Dr. Triolo was named a Calhoun Fellow at Drexel and selected to Sigma
Xi, the Scientific Research Society. He is a member of Tau-Beta-Pi Engi-
neering Honor Society and Eta-Kappa-Nu Electrical Engineering Honor
Society.
Howard J. Chizeck (S’74-M’79-M’81) was born
on March 27, 1952 in Columbus, OH. He re-
ceived the B.S. and M.S degrees in systems and
control engineering from Case Western Reserve
University, Cleveland, OH, in 1974 and 1976, re-
spectively, and the Sc.D. i n electrical engineering
and computer science from the Massachusetts In-
stitute of Technology in 1982
He is an Associate Professor in the Systems
Engineering and Biomedical Engineenng Depart-
ments at Case Western Reserve University His
research interests involve applications of control engineering to biomedical
problems. Current projects include the design and analysis of controllers
for the electrical stimulation of paralyzed muscle, adaptive control of drug
delivery, identification and control of cerebral ventricle volume dynamics
for hydrocephalus management, algebraic modeling of DNA sequence-ge-
 CARROLL et al. : RESPONSES OF ELECTRICALLY STIMULATED PARALYZED MUSCLE
ometry relationships and applications of algebraic systems theory to cod-
ing.
Dr. Chizeck is a member of the AAAS, Sigma Xi and the Rehabilitation
Society of North America (RESNA). He is also a member of the Interna-
tional Federation of Automatic Control (IFAC) Technical Committee on
Biomedical Engineering.
Rudi Kobetic received both undergraduate and
graduate degrees in biomedical engineering from
Case Westem Reserve University, Cleveland, OH.
Since 1980, he has been Head Biomedical En-
gineer of the Motion Study Laboratory of the
Cleveland VA Medical Center where he super-
vises the efforts of engineers who are researching
the restoration of ambulatory functions in para-
plegic subjects by using functional electrical stim-
ulation.
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653
E. Byron Marsolais received the M.D. and Ph.D.
degrees from the University of Iowa, Iowa City.
He interned at St. Luke’s Hospital in New York
City, and did his orthopedic residency at the Uni-
versity of Iowa. His Ph.D. studies were in the en-
gineering fields of mechanics and hydraulics. In
1970 he came to Case Western Reserve University
Medical School, Cleveland, OH, where he began
his association with the Veterans Administration
Medical Center. At Case Western Reserve Uni-
versity, he has been a Senior Instructor in or-
thopedic surgery, a Project Director in the biomechanics laboratory, As-
sistant Professor of orthopedic surgery, Assistant Professor in Solid
Mechanics, Structural, and Mechanical Design, and Adjunct Assistant Pro-
fessor in the Engineering Design Center. Since 1972 he has been Chief of
the Rehabilitation Medicine Service at the Veterans Administration Medi-
cal Center; and since 1974 Director of the Motion Study Laboratory of the
Center. Since 1975 he has been chief of the University Hospitals Problem
Low Back Team. For the past 15 years, he has been increasingly involved,
along with other investigators at Case Western Reserve University, in re-
search on functional electrical stimulation of paralyzed muscle. Since 1983
he has headed a 25-member interdisciplinary team at the Cleveland Vet-
erans Administration Medical Center, working on restoration of walking
function in the complete thoracic paraplegic.