Journal of Gerontology: BIOLOGICAL SCIENCES
1998, Vol. 53A. No. 6, B425-B429
Copyright 1998 by The Gerontological Society of America
Normally Aging Older Adults Demonstrate the Bilateral
Deficit During Ramp and Hold Contractions
Tammy M. Owings and Mark D. Grabiner
Department of Biomedical Engineering, The Cleveland Clinic Foundation, Cleveland, Ohio.
The bilateral deficit results from the maximum voluntary force of a bilaterally performed task being smaller than
the sum of the maximum voluntary force of the unilaterally performed tasks. It is underlain by the limitation of the
neural drive during maximum bilateral contractions and has been hypothesized to reflect the inability to fully activate high threshold motor units. Because high threshold motor units atrophy in older adults, a smaller bilateral
deficit in older adults compared to young adults would further support the hypothesis. Indeed, K. Hakkinen et al. in
1995 and 1996 reported no bilateral deficit in older adults performing rapid maximum contractions. The present
study extends this investigation to slowly developed maximum contractions. The results demonstrated a bilateral
deficit (p < .05). This result, combined with the age related decrease in the number of high threshold motor units,
tends to refute the contention that selective restriction of high threshold motor units causes the bilateral deficit during maximum voluntary isometric ramp and hold contractions.
T
HE central nervous system normally seems to limit the
neural drive to skeletal muscle during conditions in
which bilateral, homologous muscles are simultaneously
and voluntarily intended to be maximally activated. This
phenomenon, known as the bilateral deficit, is manifested
by the maximum voluntary force of a bilaterally performed
task being smaller than the sum of the maximum voluntary
force of the unilaterally performed tasks. Generally, the
size of the deficit is between 10 and 25%. The bilateral
deficit in young adults has been demonstrated for small
muscles such as those of the hand (1) and for large muscles
of the lower extremity (2,3). It has been observed during
isometric contractions (3-5), isokinetic concentric contractions (2,6,7), and isokinetic eccentric contractions (8).
However, the bilateral deficit is not obligatory. Hakkinen et
al. (9,10) reported no bilaterial deficit in older adults performing rapid maximum contractions. Howard and Enoka
(11) showed that in some subjects the bilateral deficit can
be diminished, and even reversed, by training, underscoring the important influence of the central nervous system.
It has been suggested that the neural basis for the bilateral
deficit is caused by interhemispheric inhibition (1,12). However, it is not known whether the activation of motor units is
selectively restricted or, conversely, if the entire motor unit
pool is affected. The latter possibility has not received much
attention, but there are conflicting reports as to whether the
bilateral deficit results from selective restriction of low or
high threshold motor unit activation. Some authors have suggested that the bilateral deficit is caused by a restriction of
high threshold motor unit activation (2,3). In contrast, other
authors have suggested that the bilateral deficit is caused by
a restriction of low threshold motor unit activation (13,14).
Recently, Hakkinen et al. (10) investigated the bilateral
deficit for an isometric knee extension task (knee joint angle
of 107 degrees flexion) in middle-aged (44-57 years) and
older (59-75 years) men and women. Earlier work by
Hakkinen et al. (9) examined the bilateral deficit in young
(approximately 30 years), middle-aged (approximately 50
years), and older (approximately 70 years) men. In both
experiments, subjects generated their maximum effort knee
extension force in a "step" fashion, having been instructed
to generate force as rapidly as possible. The subjects in
these studies did not demonstrate a bilateral deficit. This is
notable because the normal aging process is generally associated with an atrophy of and/or a decrease in the number of
high threshold motor units (15-17), which are the motor
units most difficult to voluntarily activate. Thus, failure of
the older subjects to demonstrate a bilateral deficit combined with normal age-related atrophy of high threshold
motor units is consistent with an inability to fully activate
high threshold motor units during a bilateral condition.
The presently reported data were collected as part of two
other studies. One group of subjects were the controls for a onestage versus two-stage bilateral knee arthroplasty study (18),
and the other group of subjects were from an exercise training
program (only the pretraining data were used in the present
study). The analysis was prompted by the data of Hakkinen et
al. (10) and undertaken to extend the literature on the bilateral
deficit in older adults to include ramp and hold contractions.
The question specifically posed by this analysis was, "Do older
adults demonstrate a bilateral deficit during maximum voluntary isometric knee extensions performed in a ramp- and- hold
fashion?" Based on the assumptions that the bilateral deficit is
caused by a restriction of high threshold motor units and that the
normal aging process is generally associated with an atrophy of
and/or a decrease in the number of high threshold motor units, it
was hypothesized that older adults would not demonstrate a
bilateral deficit during maximum voluntary isometric knee
extensions performed in a ramp-and-hold fashion.
METHODS
Subjects.—Two experiments were conducted in which 35
older adults (mean age ± SD: 72.1 ± 5.7 ys; Table 1) volunB425
OWINGSAND GRABINER
B426
teered to participate and provided informed consent. All
subjects were right leg dominant, as indicated by their preference for kicking a ball. An important difference between
the protocols was the knee flexion angle at which the isometric knee extension task was performed. All subjects were
healthy and living independently, but not involved in recreational activities associated with bilateral contractions (i.e.,
rowing, weight lifting). Exclusion criteria included musculoskeletal, neurological, and cardiovascular pathologies that
would have interfered with the ability to perform the tasks.
Instrumentation.—A Kin-Corn isokinetic dynamometer
(Chattanooga Corporation, Chattanooga, TN), customized
for bilateral force measurements, was used in this study.
The knee extension forces produced by the left and right
legs during a bilateral contraction were measured individually using strain gauge load cells (Figure 1; model MC3-3500, AMTI, Newton, MA). The signals from the strain
gauge load cells were used as input to an A/D circuit (Data
Translation, 2801 A, Marlboro, MA). The signals were digitized at 100 Hz and stored for processing.
Table 1. Descriptive Statistics (mean ± SD)
of Subject Physical Characteristics by Group/Sex
Subjects
Age (yrs)
Height (m) Weight (kg)
4
5
9
70.0 ± 4.8
66.6 ± 7.0
68.1 ±6.0
1.72 ±0.08
1.63 ±0.07
1.67 ±0.08
91.5 ±18.5
76.9 ± 6.6
83.4 ± 14.4
8
18
26
74.3 ± 3.3
73.2 ± 5.5
73.5 ± 4.9
1.71 ±0.06
1.57 ±0.08
1.62 ±0.10
77.3 ± 9.1
66.9 ±10.2
70.1 ± 10.9
35
72.1 ±5.7
1.63 ±0.10
73.5 ±13.1
Group I *
Men
Women
Total
Protocol.—Subjects were seated upright in the Kin-Corn
and stabilized with Velcro straps across their waist and each
thigh (Figure 2). The axes of rotation of the Kin-Corn were
aligned with the putative flexion-extension axis of both knee
joints. The pad of each load cell was placed over the distal
shank, proximal to the ankle joint. For Group I, the isometric contractions were performed with the knee joint at 45
degrees of flexion (full extension = 0 degrees). For Group II,
isometric contractions were performed with the leg vertical
to the floor (knee flexion angle approximately 90 degrees).
Subjects performed maximum voluntary isometric contractions (MVC) of the knee extensor muscles under three
different conditions (right leg only, left leg only, and both
legs). Three trials for each condition were collected. The
collection order was randomized, and subjects were given a
practice trial prior to each condition. Subjects were instructed to generate an MVC over a period of 3 seconds.
Upon achieving MVC, the subject indicated that to the
experimenter (either by a verbal "okay" or by a nod of the
head), and data were collected for one second. One minute
of rest was allowed between each trial.
Data Analysis.—The digitized force data were smoothed
using a recursive Butterworth filter (cutoff frequency = 10
Hz) and converted to moments. The peak knee extension
moment and the average knee extension moment were
extracted for the one-second data collection period. The
Group lit
Men
Women
Total
Combined groups
*Knee angle 45 degrees.
fKnee angle 90 degrees.
Figure 1. Kin-Com attachment allowing for collection of left and right
forces during a bilateral contraction. (From Owings & Grabiner, ref. 21.
Reprinted with permission.)
Figure 2. Positioning of subject in the modified isokinetic dynamometer.
BILATERAL DEFICIT IN OLDER ADULTS
value for each condition was determined by averaging
across the three trials.
The bilateral index was determined for each leg and was
calculated as defined by Howard and Enoka (11):
[100 X (bilateral value of x /unilateral value of x)] - 100
in which x represented the knee extension moment for
either the left or the right leg. A negative value indicated a
bilateral deficit, such that a smaller moment was generated
during the bilateral condition than during the unilateral condition. A positive value indicated a bilateral facilitation,
such that a larger moment was generated during the bilateral condition than during the unilateral condition.
Statistical Analysis.—A 2 X 2 X 2 (Group by Leg [i.e,
left vs right] by Condition [i.e., unilateral vs bilateral])
analysis of variance (ANOVA) was used to determine intercondition and interleg differences for the knee extension
moments generated. The leg and condition factors were
repeated measures. A 2 X 2 (Group by Leg) ANOVA was
used to determine intergroup and interleg differences for
the calculated bilateral indices. Paired samples t tests were
used to compare the knee extension moments of the unilateral conditions to the bilateral condition. One-sample t tests
were used to indicate if the bilateral indices were different
from zero. A probability level of .05 was used as the maximum acceptable value indicating significant differences.
RESULTS
The analysis performed on the maximum knee extension
moments and the analysis performed on the computed bilateral indices confirmed the presence of a bilateral deficit in
older adults. The bilateral indices were not different between the peak and averaged values, so only the averaged
values will be reported. The ANOVA revealed a significant
decrease in maximum knee extension moment when the
contractions were performed bilaterally (p < .001). This was
true for both the right and left legs (Table 2). The differences between the two groups of subjects, which effectively
tested the effect of knee joint angle, were not significant.
The interaction terms were not significant.
B427
The ANOVA performed on the bilateral indices revealed
that the differences between the right and left legs were not
significant (p = .282). Further, the differences between the
two groups of subjects were not significant (p = .222) The
Group by Leg interaction term was not significant. One-sample t test revealed that the bilateral index was significantly
different than zero for each of the four comparisons (p < .05).
Of the 70 calculated bilateral indices, only 12 showed a positive value (bilateral facilitation) with an additional four having an index approximately equal to zero (Figure 3). Three
subjects showed a bilateral facilitation in both legs.
DISCUSSION
Based upon the work by Hakkinen et al. (10), using maximum voluntary knee extension contractions performed in a
step fashion, we performed an analysis of data from two
other studies that allowed evaluation of the bilateral deficit
in older adults performing the task in a ramp-and-hold fashion. It has been suggested that the bilateral deficit reflects
increased difficulty of activating large motor units during
bilateral contractions activation (2,3). The work by Hakkinen et al. (10), in which the bilateral deficit was not
detected in older adults, supported this hypothesis. Because
normal aging is expected to be associated with atrophy of
high threshold motor units (15,16), the potential contribution of these motor units during bilaterally performed maximum effort contractions is also expected to be reduced. A
neurally mediated restriction of these motor units during
bilateral maximum contractions would effectively reduce
the size of the bilateral deficit. Based on older adults' data
that were collected as part of two other studies, the question
specifically addressed in the present study was, "Do older
adults demonstrate a bilateral deficit during maximum voluntary isometric knee extension performed in a ramp-andhold fashion?" The results of the analysis confirmed the
presence of a bilateral deficit under these conditions.
41
2§
Table 2. The Bilateral Indices and the Right and Left Leg
Unilateral and Bilateral Knee Extension MVC Averages
(mean ± SD) for Each Group (3 trials per subject)
Bilateral
Index
Unilateral
Condition
(Nm)
Bilateral
Condition
(Nm)
Group I
Left leg
Right leg
-12.9 ±5.3*
-11.1 ±6.8*
82.3 ±18.4
94.7 ± 24.8
71.6 ±15.8**
83.0 ±17.3**
Group II
Left Leg
Right leg
-8.9 ± 15.4*
-6.5 ± 13.7*
76.1 ±29.9
85.0 ± 35.2
68.3 ±25.7**
77.7 ± 29.0**
Note: Group I knee angle 45 degrees; Group II knee angle 90 degrees.
•Statistically different from zero (p < .05).
••Statistically less than corresponding unilateral condition [p < .05).
00
Knee extension MVC (Nm)
during unilateral condition
Figure 3. The moment generated during a unilateral maximum voluntary
contraction (MVC) plotted against the moment of the same leg during the
bilateral MVC for each subject. The circles (O) represent the left leg and
the triangles (A) represent the right leg. The diagonal line is a line of identity. Data below the line of identity show a bilateral deficit. Data above the
line of identity show a bilateral facilitation. Nm = newton-meter.
B428
OWINGSAND GRABINER
By showing that the bilateral deficit did occur in older
men and women, the results of the present study are consistent with what we believe to be the dominant number of
published studies on this topic involving younger adults.
The size of the bilateral deficit in our older adults (ranging
from 6.5 ± 13.7% to 12.9 ± 5.3%) was comparable to the
9.5 ± 6.8% (11) and 17.0 ± 7.4% (3) measured in young
adults under similar conditions. Because the magnitudes of
the unilateral and bilateral forces were greater for the
younger adults, it seems that the degree of the bilateral
deficit is independent of strength.
The present findings are contradictory to those of the
heretofore only published studies on the bilateral deficit in
older adults (9,10). This naturally raises questions about
those factors that may have caused such differences. Based
on simple descriptions of the subjects, it does not seem that
this would be the source of differences. The subjects in each
study seem reasonably matched for age, height, and weight.
Further, the subjects in each study seemed similar regarding
their independent living lifestyles and, on average, participation in recreational activities. One can not discount the
importance of the differences afforded by the different countries in which the studies were performed but similarly,
there is no precedent to expect differences in the bilateral
deficit based upon this factor. Interestingly, the younger subjects in Hakkinen et al. (9) also failed to produce a bilateral
deficit. This is contradictory to numerous studies involving
younger adults (2,4,5), and specifically Koh et al. (3), in
which young subjects performed step contractions.
Not unexpectedly, the differences between how the bilateral deficit was computed in the current study as well as
Hakkinen et al. (9,10) are not a factor. We were able to
recompute the bilateral deficit in our older adults using the
equation of Hakkinen et al. (10) [(bilateral force / sum of
unilateral forces) X 100]. The mean and standard deviation
(n = 35) were found to be 91.5 ± 10.6. A t test revealed that this value was significantly different from 100.
An interesting possibility that may have contributed to the
differences in the two studies was provided by Vint and Hinrichs (19). Their data suggest that the size of the bilateral
deficit for maximum voluntary knee extension force is significantly affected by the time separating the onset of force
generated in one leg from that of the other leg. Specifically,
when bilateral knee extension force was generated asynchronously (on an average of 267 msec), the bilateral deficit
was absent. But a synchronously generated bilateral knee
extension force (within 18 msec) produced a bilateral deficit.
Therefore, although this was not investigated, one can not
discount the possibility that the findings of Hakkinen et al.
(10) were influenced to some extent by asynchronous timing
of bilateral force onset. This may also account for the
absence of the bilateral deficit in not only older, but also
young and middle-aged, men and women (9,10,20), yet not
all studies involving step contractions have failed to produce
a bilateral deficit in younger adults (3). It would seem that
during a ramp-and-hold contraction, asynchronous onset
would not have likely been an issue. A more comprehensive
study of the bilateral deficit in older adults is necessary and
should include both step and ramp-and-hold conditions. Such
a design could more effectively address the questions raised
by the differences between the present results and those of
Hakkinen et al. (10).
Combining the presence of a similar bilateral deficit in
older adults compared to young adults with the expected
age-related atrophy of high threshold motor units, tends to
refute the contention that the inability to fully activate high
threshold motor units underlies the bilateral deficit. Recent
studies in our laboratory (21) also dispute this contention.
With similar assumptions, such as Vandervoort et al. (2),
this study investigated the effects of fatigue on bilateral
deficit and if these effects were speed dependent. Our findings showed that the size of bilateral deficit was not
affected by fatigue induced isokinetically at 150 degrees
per second, yet increased when fatigue was induced at 30
degrees per second. If a restriction of high threshold motor
units is the cause of the bilateral deficit, the size of the
deficit following fatigue should have diminished.
Most studies have focused on selective motor unit recruitment as the cause for the bilateral deficit, but could it
be possible that the bilateral deficit, in young and older
adults, is a result of the nervous system restricting the maximum discharge frequency of active motor units? That is,
the bilateral deficit represents the influence of altered rate
coding rather than recruitment. There is a precedence supporting this as a possible mechanism. Specifically, there is
accumulating evidence that the central nervous system uses
a different control strategy for concentric and eccentric
contractions. In particular, the discharge frequency of
motor units is lower during eccentric contractions than during concentric contractions (22-24). If the central nervous
system employs different motor unit discharge frequencies
for concentric and eccentric contractions, it would not be
unreasonable to suggest that different motor unit discharge
frequencies occur for bilateral and unilateral contractions.
Electromyographic activity (EMG) was not collected in
the present study, but those investigations recording EMG
have showed conflicting results. Some have shown a decline in the EMG that parallels the decline in force during a
bilateral contraction (2), whereas others have shown no
decline in EMG (5). It has been suggested that the changes
in the force between a bilateral and a unilateral condition
may not be large enough to detect changes in EMG (11).
More refined measures of EMG may be needed in order to
detect the small changes in either motor unit recruitment or
discharge frequency.
Returning to the findings of the present study, the purpose
of calculating the bilateral index was to compare the total
force generated by both legs during the bilateral condition to
the sum of unilaterally generated forces. The unique design
of our testing apparatus allowed for simultaneous, independent force measurements from the left and the right leg during the bilateral condition. Thus, the bilateral index could be
calculated for each leg separately. There were a total of 70
individual conditions (35 subjects X 2 legs each). Of these
70 conditions, 4 displayed no difference, and 12 demonstrated a bilateral facilitation. Although Figure 3 does not differentiate between subject groups, these 16 conditions were
from Group II. Three subjects showed a bilateral facilitation
in both legs, four subjects showed a facilitation in their right
leg only, and two subjects showed a facilitation in their left
BILATERAL DEFICIT IN OLDER ADULTS
leg only. Two subjects from Group II showed a bilateral
index of approximately zero in both legs. Although not statistically significant, the bilateral deficit was quantitatively
larger for Group I, which had a knee flexion angle of 45
degrees. Future investigations may include components to
probe the possibility of a joint angle specific bilateral deficit.
In summary, this analysis was undertaken to extend the
results of the only published article on the bilateral deficit
in older adults. Surprisingly, the results were quite different
from the previously published work of Hakkinen et al. (10)
although there was at least one methodological difference
between the protocols; specifically, the use of step versus
ramp-and-hold contractions. Thus, the general question of
the nature of central nervous system control of bilaterally
performed isometric knee extension tasks in older adults
remains open for discussion.
ACKNOWLEDGMENTS
This work was partially funded by the Chattanooga Corporation, Chattanooga, Tennessee. The authors thank Julee E. Kasprisin, Thomas M.
Lundin, and Julie E. Perry for their assistance in the data collection. This
work was presented in the conference proceedings of the 20th Annual
Meeting of the American Society of Biomechanics, Georgia Tech, Atlanta,
Georgia, 1996.
Address correspondence to Tammy M. Owings, Department of Biomedical Engineering / Wb3, The Cleveland Clinic Foundation, 9500 Euclid
Avenue, Cleveland, OH 44195. E-mail: [email protected]
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Received October 21, 1997
Accepted June 2, 1998