1Department of Biomedical Engineering, Lerner Research Institute; 2Department of Physical Medicine and Rehabilitation, The Cleveland Clinic Foundation, Cleveland 44195; and 3Program of Applied Biomedical Engineering, Fenn College of Engineering, Cleveland State University, Cleveland, Ohio 44114
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ABSTRACT |
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Fang, Yin,
Vlodek Siemionow,
Vinod Sahgal,
Fuqin Xiong, and
Guang H. Yue.
Greater Movement-Related Cortical Potential During Human
Eccentric Versus Concentric Muscle Contractions.
J. Neurophysiol. 86: 1764-1772, 2001.
Despite abundant
evidence that different nervous system control strategies may exist for
human concentric and eccentric muscle contractions, no data are
available to indicate that the brain signal differs for eccentric
versus concentric muscle actions. The purpose of this study was to
evaluate electroencephalography (EEG)-derived movement-related cortical
potential (MRCP) and to determine whether the level of MRCP-measured
cortical activation differs between the two types of muscle activities.
Eight healthy subjects performed 50 voluntary eccentric and 50 voluntary concentric elbow flexor contractions against a load equal to
10% body weight. Surface EEG signals from four scalp locations
overlying sensorimotor-related cortical areas in the frontal and
parietal lobes were measured along with kinetic and kinematic
information from the muscle and joint. MRCP was derived from the EEG
signals of the eccentric and concentric muscle contractions. Although
the elbow flexor muscle activation (EMG) was lower during eccentric
than concentric actions, the amplitude of two major MRCP
componentsone related to movement planning and execution and the
other associated with feedback signals from the peripheral systems
was
significantly greater for eccentric than for concentric actions. The
MRCP onset time for the eccentric task occurred earlier than that for
the concentric task. The greater cortical signal for eccentric muscle actions suggests that the brain probably plans and programs eccentric movements differently from concentric muscle tasks.
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INTRODUCTION |
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All motor actions involving skeletal muscle activities are accomplished by three types of muscle contractions: concentric (shortening), eccentric (lengthening), and isometric (constant length). Of the three, isometric and concentric contractions are more widely studied, and the neural mechanisms that mediate isometric and concentric actions are better understood. Eccentric muscle contractions, which generate a significant proportion of our daily-living movements [e.g., walking upstairs (concentric) and downstairs (eccentric); raising a water glass to the mouth (concentric) and returning it to the table (eccentric)], are less well understood.
Eccentric muscle actions are employed in many medical rehabilitation
programs, such as those for anterior knee pain (Bennett and
Stauber 1986), pitching shoulder injury (Pappas et al.
1985
), and patellar tendinitis (Jensen and Fabio
1989
). Numerous athletic training and recreational conditioning
programs also include eccentric muscle activities as a major component
of these programs (Alfredson et al. 1999
; Bobbert
1990
; Chandler et al. 1989
; Wilk et al.
1993
). A major advantage of eccentric muscle actions is that
this type of muscle activity develops greater tension than concentric
actions (Bigland and Lippold 1954
; Doss and
Karpovich 1965
; Lacerte et al. 1992
;
Olson et al. 1972
). In addition, eccentric training induces adaptive changes in the muscle, which may reduce future tissue
damage and pain (Clarkson et al. 1992
;
Fridén et al. 1983a
; Hortobágyi et
al. 1996
). Eccentric contractions require less energy
expenditure, and such energy efficiency may improve the functional
capacity of an individual with limited physiological reserves
(Asmussen 1952
; Bigland-Ritchie and Woods
1976
; Dean 1988
). Yet, little is known about how
eccentric training or exercise affects the CNS.
The results of many studies suggest that the CNS may control concentric
and eccentric muscle actions differently. One of the most reported
observations is that for a given force to be generated, electromyographic (EMG) activities are lower during eccentric than
concentric contractions (e.g., Bigland and Lippold 1954; Moritani et al. 1988
; Tesch et al. 1990
).
A lower level of EMG in an eccentric contraction is a result of fewer
motor units being recruited and a lower discharge rate of the active
motor units (Moritani et al. 1988
). Nardone et
al. (1989)
reported that motor unit recruitment order during
eccentric contractions of human triceps surae muscles was reversed
compared with isometric and concentric contractions. High-threshold
motor units were selectively recruited (Howell et al.
1995
; Karapondo et al. 1993
; Nardone et
al. 1989
), and the activation was shifted from a slow (soleus) to a fast (gastrocnemius) muscle when an eccentric contraction was
performed (Nardone and Schieppati 1988
). One interesting
observation is that the motor unit pool of a muscle cannot be fully
activated during maximal voluntary eccentric contractions, as assessed
by the twitch interpolation technique, whereas almost all motor units are active during concentric contractions (Sale 1988
;
Westing et al. 1990
). The amplitude of motor-evoked
potential in muscle by transcranial magnetic stimulation differs for
concentric and eccentric contractions. With comparable EMG levels, the
motor-evoked potential in an elbow flexor muscle was less for eccentric
contractions than for concentric and isometric contractions
(Abbruzzese et al. 1994
). Relative activation levels
among synergistic muscles change as the activity shifts from concentric
to eccentric muscle actions (Nakazawa et al. 1993
).
Despite these differences, which have led a number of investigators to
suggest that eccentric muscle actions have unique neural control
strategies (Enoka 1996), no direct evidence is available to indicate that the CNS signal for controlling an eccentric muscle contraction differs from that for controlling a concentric action. The
purpose of this study was to measure electroencephalography (EEG)-derived movement-related cortical potential (MRCP) during the two
types of muscle actions and determine if the level and timing of
cortical activation differ between eccentric and concentric human elbow
flexor contractions. Preliminary results have been reported in abstract
form (Siemionow et al. 1999
).
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METHODS |
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Subject
Eight right-handed volunteers (6 men and 2 women, 27.75 ± 7.21 yr old, range 20-44 yr) participated in the study. All individuals were healthy and had no known neuromuscular disorders. All individuals gave informed consent prior to their participation. The experimental procedures were approved by the Institutional Review Board at the Cleveland Clinic Foundation.
Mechanical recording
Subjects were seated comfortably in an experimental chair in an electrically shielded data-recording room. The subject's left arm was held at shoulder height, then placed and restrained on a wooden board that could be freely rotated. The forearm was in a neutral position between supination and pronation. The upper arm rotated ~30° forward from a straight line connecting the left and right shoulders. The subject's torso, shoulders, and left upper arm were all stabilized so that only movements at the left elbow joint were allowed (Fig. 1). A load of 10% of the subject's body weight was attached to the left wrist through a nonelastic cable and a pulley fixed on the wall (Fig. 1). Subjects could perform concentric contraction of the elbow flexor muscles by lifting the weight and eccentric contraction by lowering the weight. The wooden board on which the arm rested was connected to a potentiometer that measured the position of the arm and the angle of the elbow joint. A concentric or eccentric contraction consisted of a 30° rotation of the elbow joint. A trigger signal was generated as soon as the rotation reached a threshold (3°). This trigger signal was later used for the triggered data averaging during data processing and analysis. A button-type strain gauge force transducer (subminiature load cell, Sensotec, Columbus, OH) was built between two metal plates; one was attached to one side of the cable holding the weight and the other to the opposite side of the cable fixed to the subject's arm. When the weight was lifted or lowered, the transducer was pressed and force recorded. The position and force signals were digitized (100 samples/s) by a Spike 2 data acquisition and analysis system (Cambridge Electronic Design Limited, Cambridge, UK) and recorded on-line on the hard drive of a personal computer. The position and force signals were displayed on an oscilloscope located in front of the subject.
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Electrical recording
EEG RECORDING.
Monopolar EEG data were recorded from four locations using Ag-AgCl cup
electrodes (10-mm diam). Positioning of the electrodes was based on the
International 10-20 System (Jasper 1958). One electrode
(Cz) was placed on the scalp overlying the supplementary motor area
(SMA). Another (Fz) was over the center region of the prefrontal
cortex. C3 and C4 electrodes were positioned on the scalp overlying the
sensorimotor areas of the left and right hemispheres, respectively.
These four active electrodes (Cz, C3, C4, and Fz) were referenced to
the common linked earlobes (A1 and A2). Impedance of each electrode was
maintained 5000
. The EEG signal was amplified (20,000 times) using
EEG amplifiers (Grass Neurodata Amplifier System, Astro-Med, West
Warwick, RI). The time constant of the EEG recording was 2s, with
a low-pass cutoff frequency of 100 Hz. The output signal from the EEG
amplifiers was digitized (200 samples/s) using the Spike 2 system and
recorded on the hard disk of the personal computer.
EMG RECORDING. Surface EMG signals were simultaneously recorded from the biceps brachii (BB), brachioradialis (BR), triceps brachii (TB), and deltoid (DL) muscles. The skin was cleaned with alcohol prior to electrode attachment. Bipolar electrodes (8-mm recording diameter) were attached to the skin overlying the belly of each muscle. The reference electrode was fixed on the skin overlying the lateral epicondyle near the elbow joint. The EMG signals were amplified (1,000 times), filtered (10-3,000 Hz), digitized (1,000 samples/s), and recorded on the hard disk of the computer.
Experimental procedures
After the scalp was cleaned with alcohol pads, EEG electrodes
were attached to the scalp with electrode paste. The impedance of each
electrode was measured after the electrodes were secured on the scalp.
If the impedance for a given electrode was >5,000 , the electrode
was removed and the scalp was further prepared until the impedance was
lowered to <5,000
. The left elbow and forearm rested on the padded
wooden board after the EMG electrodes were attached. The forearm was
secured between two vertical wooden boards that could be tightly
screwed onto the horizontal board (Fig. 1, right). Soft
cushions were provided between the forearm and vertical boards.
Each subject performed 50 concentric and 50 eccentric contractions of the elbow flexor muscles of the left arm. Four subjects performed the concentric contractions first, and the other four performed the eccentric trials first. Subjects rested for 5 min after the first 50 contractions were completed. During this time, they were released from the chair and arm restraints, but with the EEG and EMG electrodes still attached, to allow them to stretch. During each concentric contraction, the elbow flexors shortened and the elbow joint rotated from the 155° position to the 125° position (180° with the elbow being fully extended). During each eccentric contraction, the muscles lengthened and the elbow joint rotated from the 125° position to the 155° position (Fig. 1, left). Both the beginning arm position (155° for concentric and 125° for eccentric) and target position (125° for concentric and 155° for eccentric) were displayed on an oscilloscope. The subject moved the forearm (rotated the elbow) from the beginning position to the target position and the weight was either caught by the experimenter (concentric) or touched down on the padded floor (eccentric) after the target position was passed. After each contraction, the experimenter supported the weight (concentric) or the weight was on the floor (eccentric) for ~10 s, during which the subject rested. After the rest, the weight and subject's arm were moved back to the beginning position by the experimenter and the subject began the isometric contraction (~5 s) that preceded each concentric or eccentric movement. The speed of movement was ~25°/s for both actions.
Subjects gauged the range and speed of each movement by viewing the position cursor on the oscilloscope. They were told to avoid eye blinks during each contraction, but eye blinks were allowed during the time when the weight was supported by the experimenter. At the end of the experiment, maximal isometric elbow flexion, extension and shoulder abduction contractions were performed to record maximal EMG values of the BB, BR, TB, and DL muscles. These maximal EMG values were later used to normalize the EMG data of these muscles during the concentric and eccentric contractions.
Analysis
All raw EEG data were inspected visually. Trials that contained eye blinks or other signal artifacts were excluded. For both concentric and eccentric contractions, each trigger signal triggered a 10-s window (5 s before the trigger and 5 s after). The Spike 2 data analysis software performed EEG signal averaging over the 50 trials of each type of contractions. Similarly, after all EMG signals were rectified, the force and EMG signals were trigger-averaged across the 50 trials. After averaging, the baseline force, EMG, and EEG data were measured. Baseline data were defined as the data obtained during the isometric contraction (the holding phase). During the concentric and eccentric contractions, mean force and EMG were determined within 1.2 s from the time of trigger. Force fluctuation (standard deviation of the mean force) was measured for the first five and last five trials of concentric and the first five and last five trials of eccentric contractions. In each trial, it was calculated in a period during the movement when the force was stable (Fig. 2A). In each subject, the fluctuation was measured from each of the 10 trials first, then an average of the 10 trials was obtained.
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MRCP was divided into two major components, negative potential
(NP) and positive potential (PP). These components were measured separately. In general, NP is thought to be related to movement preparation, planning, and execution, whereas PP is associated with
brain signals processing feedback information from the sensory system
(Deecke et al. 1976; Hallet 1994
;
Siemionow et al. 2000
). Mean and peak values were
determined for the NP. The mean NP was calculated as an average from
the beginning of NP to its peak, and the peak NP was determined from
the baseline to the peak (Fig. 2B). In addition, the onset
time of NP was analyzed to reveal possible differences in the timing of
the NP between the two motor tasks. The NP onset time was calculated
from the trigger to the beginning of NP and from the onset of the
biceps brachii EMG to the onset of NP. The beginning of the NP was
determined by a curve-fitting procedure
a straight line was drawn
along the baseline potential and another line along the NP. The
intercept of the baseline and the line crossing NP was taken as the
beginning of the NP (Siemiomow et al. 2000
).
Three amplitude values were measured for PP. The mean PP was the mean value from the negative peak or beginning of the PP to the end of movement (based on elbow angle measurement). The peak PP was the amplitude from the beginning of PP to the value at which the movement was ended. The baseline PP was measured from the pre-NP baseline to the value at which the movement was ended (Fig. 2B). These measurements were averaged across all subjects. Finally, the range and speed of movement for each type of contractions were measured.
Statistical analysis
Paired t-tests were performed to compare force, EMG,
range and rate of movement, and measurements of MRCP between the
concentric and eccentric muscle contractions. The mean force, EMG, and
EEG values during the baseline condition were also compared between the
two types of contractions using the paired t-tests.
Significance level was determined at P 0.05, and the data
are reported as means ± SD unless otherwise mentioned.
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RESULTS |
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Initial isometric contraction
Subjects held the weight for ~5 s (isometric contraction) before
each eccentric or concentric contraction. The mean isometric force
preceding the eccentric contraction (60.17 ± 7.98 N) was not
significantly different (P > 0.15) from that preceding
the concentric contraction (63.89 ± 8.68 N, Fig.
3A). Surface EMG data recorded
from the BB, BR, TB, and DL muscles during the isometric contraction
that preceded the concentric and eccentric contractions were similar
(P > 0.3, Fig. 3B). The isometric EMG data
(percent of MVC) of the BB, BR, TB, and DL muscles before the eccentric contraction were 27.68 ± 4.68, 26.83 ± 6.49, 7.10 ± 0.86, and 7.01 ± 0.23%, respectively. The same values for the
four muscles before the concentric contraction were 26.56 ± 6.38, 24.47 ± 6.60, 6.98 ± 0.84, and 7.21 ± 0.34%,
respectively (Fig. 3B). Similarly, the mean EEG amplitude
during the isometric contraction preceding the eccentric contraction
did not significantly differ (P > 0.2) from that
preceding the concentric contraction (Fig. 3C). The isometric EEG values for the four scalp locations (Cz, C3, C4, and Fz)
before the eccentric contraction were 0.72 ± 0.26,
0.13 ± 0.09,
0.50 ± 0.37, and
0.18 ± 0.09 µV,
respectively. The isometric EEG values for the four recording locations
before the concentric contraction were
0.64 ± 0.25,
0.12 ± 0.07,
0.52 ± 0.31, and
0.15 ± 0.08 µV,
respectively (Fig. 3C).
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Eccentric and concentric contractions
RANGE AND SPEED OF MOVEMENT. The range of movement for eccentric and concentric contractions was the same: 0.49 ± 0.09 and 0.49 ± 0.05 rad, respectively. The speed of movement for the eccentric contraction (0.40 ± 0.02 rad/s) was not significantly different (P > 0.1) from that for the concentric contraction (0.37 ± 0.03 rad/s). Figure 4 (top) presents an example of movement range and speed for concentric (left) and eccentric (right) contractions.
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FORCE AND EMG. Although the load (weight) applied during eccentric and concentric contractions was the same, the force exerted by the subjects during eccentric contractions (54.50 ± 6.03 N) was significantly lower (P < 0.01) than the force during concentric contractions (69.33 ± 8.30 N, Figs. 4, 2nd panel, and 5A). We recently moved the force transducer to the distal side of the pulley (between the pulley and weight) and found that the force was the same during eccentric and concentric contractions against the same weight. Thus the discrepancy in force under the same-load conditions arose from different friction force directions between the cable and pulley when the weight was lowered and lifted. If the friction force was the same, then the exerted force should also be equal between the two tasks.
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MRCP NEGATIVE POTENTIAL.
Mean and peak values of the NP were measured. For the eccentric
contraction, the mean NP values for the four scalp locations (Cz, C3,
C4, and Fz) were 1.60 ± 0.40,
0.85 ± 0.14,
1.41 ± 0.51, and
0.86 ± 0.28 µV, respectively. For the concentric
contraction, these four values were
1.04 ± 0.31,
0.56 ± 0.15,
1.00 ± 0.48, and
0.48 ± 0.31 µV, respectively
(Figs. 4, bottom, and
6A). The mean NP values for
the eccentric contraction were significantly greater than those for the
concentric contraction (Cz, P < 0.05; C3,
P < 0.005; C4, P < 0.02; and Fz,
P < 0.005). For the eccentric contraction, the peak NP
values for the four recording locations (Cz, C3, C4, and Fz) were
3.78 ± 0.74,
2.68 ± 0.22,
3.41 ± 0.59, and
3.21 ± 0.45 µV, respectively. The corresponding four values
for the concentric contraction were
2.80 ± 1.19,
2.02 ± 0.58,
2.76 ± 0.90, and
2.48 ± 0.71 µV, respectively
(Figs. 4, bottom, and 6B). The peak NP values for
the eccentric contraction were significantly greater than those for the
concentric contraction (Cz, P < 0.05; C3,
P < 0.02; C4, P = 0.05; and Fz,
P < 0.002).
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NP ONSET TIME.
The NP onset time was measured from the trigger to the beginning of NP.
The values of NP onset time for the eccentric task for the four
recording locations (Cz, C3, C4, and Fz) were 859 ± 48,
837 ± 58,
890 ± 89, and
842 ± 52 ms,
respectively. For the concentric task, the four values were
768 ± 62,
681 ± 83,
802 ± 43, and
758 ± 38 ms,
respectively (Fig. 7A). The
values of NP onset time for the eccentric contraction were
significantly longer than those for the concentric contraction (Cz,
P < 0.05; C3, P < 0.05; C4,
P < 0.05; and Fz, P < 0.05). The NP
onset time was also measured from the onset of NP to the onset of the
biceps brachii EMG. This value allowed us to determine the latency from the beginning of the cortical activity to the onset of muscle activation. For the eccentric task, the values of NP onset time from
the EMG activity for the four recording locations (Cz, C3, C4, and Fz)
were
546 ± 40,
535 ± 26,
538 ± 55, and
595 ± 30 ms, respectively. For the concentric task, the four
values were
458 ± 34,
430 ± 23,
451 ± 19, and
528 ± 25 ms, respectively (Fig. 7B). The onset time
values for the eccentric contraction were significantly longer than
those for the concentric contraction (Cz, P < 0.05;
C3, P < 0.05; C4, P < 0.05; and Fz,
P < 0.05).
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MRCP POSITIVE POTENTIAL. For the eccentric contraction, the mean PP values for the four recording locations (Cz, C3, C4, and Fz) were 0.84 ± 0.51, 1.45 ± 0.63, 0.77 ± 0.16, and 0.99 ± 0.39 µV, respectively. For the concentric contraction, the four values were 0.18 ± 0.07, 0.78 ± 0.17, 0.18 ± 0.09, and 0.09 ± 0.13 µV, respectively (Fig. 8A). The mean PP values for the eccentric contraction were significantly greater than those for the concentric contraction (Cz, P < 0.05; C3, P < 0.02; C4, P < 0.005; and Fz, P < 0.001). The peak PP values for the eccentric contraction at the four scalp locations were 6.06 ± 0.40, 6.13 ± 0.74, 6.38 ± 1.33, and 8.37 ± 3.45 µV, respectively. These four values for the concentric task were 4.74 ± 0.66, 4.41 ± 0.83, 3.89 ± 1.60, and 5.11 ± 1.62 µV, respectively (Fig. 8B). Three of the four peak PP values for the eccentric task were significantly greater than those for the concentric task (Cz, P < 0.05; C3, P < 0.05; C4, P < 0.05; and Fz, P = 0.08). The baseline PP values for the eccentric task at the four scalp locations were 2.29 ± 0.88, 3.46 ± 0.65, 2.97 ± 1.67, and 5.17 ± 3.39 µV, respectively. The four values for the concentric action were 1.94 ± 1.76, 2.39 ± 1.23, 1.13 ± 1.65, and 2.64 ± 1.72 µV, respectively (Fig. 8C). Two of the four baseline PP values for the eccentric task were significantly greater than those for the concentric task (Cz, P = 0.6; C3, P < 0.05; C4, P = 0.06; and Fz, P < 0.05).
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FORCE FLUCTUATION. The force fluctuation (SD) was 1.14 ± 0.61 N for the eccentric task and 0.76 ± 0.25 N for the concentric task. The two values were significantly different (P < 0.05).
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DISCUSSION |
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The purpose of this study was to determine whether EEG-measured brain activity associated with eccentric contractions of the elbow flexor muscles differs from that related to concentric contractions. The major findings were that MRCP NP values, which are related to cortical activities for movement preparation and execution, were greater during eccentric than concentric tasks; MRCP PP values, which are associated with the processing of feedback signals, were greater during eccentric than concentric actions; and the onset times of the NP were earlier for the eccentric than concentric muscle contractions.
EEG (MRCP) and EMG paradox
For the eccentric task, the MRCP NP measurements were greater but
the EMG and force of the elbow flexor muscles were lower than the
corresponding values of the concentric task (lower MRCP but higher EMG
and force). These observations are contradictory to current data
dealing with the relationship between cortical and muscle signals. In
monkey, a higher discharge rate of motor cortical neurons was
associated with greater exerted force (Cheney and Fetz
1980; Evarts 1968
; Hepp-Reymond et al.
1989
; Smith et al. 1975
). A number of studies
have shown a positive relationship between MRCP NP and muscle output in
human subjects (Becker and Kristeva 1980
; Kutas
and Donchin 1974
; Shibata et al. 1993
). A recent
study from this laboratory (Siemionow et al. 2000
)
reported a linear relationship between a major component of MRCP NP
(negative slope) recorded from scalp locations overlying the
sensorimotor and supplementary motor areas and human elbow flexion
force and elbow flexor muscle EMG. Based on these relationship data,
given greater MRCP NP for the eccentric action, we should expect
higher force and EMG for the eccentric contraction. This
expectation is based on the assumption that the NP is a measure of the
signal of the motor cortical output neurons that scales muscle output.
However, it is unlikely that the NP is related only to the cortical output signals. The NP onset time was >400 ms before onset of EMG activity for both the eccentric and concentric actions, during which early preparation and planning for the muscle action should also occur. The following section discusses possible explanations for greater NP that may be related to differential cortical programming/planning for an eccentric muscle contraction.
Possible explanations for greater MRCP NP during eccentric muscle actions
DEGREE OF DIFFICULTY.
Eccentric contractions are more difficult to perform than concentric
ones. This is supported by the result of higher eccentric than
concentric force fluctuations. Higher eccentric force fluctuation seems
consistent with the observation that high-threshold motor units are
selectively recruited and that they discharge action potentials at a
lower rate during submaximal eccentric contractions (Howell et
al. 1995; Nardone et al. 1989
). Because
high-threshold motor units exhibit greater twitch force and a lower
discharge rate makes less-complete fused motor unit force, it is not
surprising that force fluctuation is higher during eccentric than
concentric contractions. Owings and Grabiner (2000)
reported greater errors (force fluctuation) in controlling eccentric
than concentric knee extensor contractions. To control a movement with
a higher degree of difficulty, the brain may need to devote greater
effort or a more extensive neural network may be needed to participate
in the controlling process. Neuroimaging studies have shown that when
motor tasks with a higher degree of difficulty are performed, the level
of brain activation is higher (Roland et al. 1980
;
Yue et al. 2000
).
PREVENTING MUSCLE DAMAGE.
Eccentric muscle contractions are characterized by greater tissue
damage as compared with concentric ones (Newham et al.
1983; Shellock et al. 1991
;
Waterman-Storer 1991
). Histological and ultrastructural
muscle damage has been reported after eccentric exercise, including
sarcolemmal disruption, dilation of the transverse tubule system,
distortion of myofibrillar components, fragmentation of the
sarcoplasmic reticulum, lesions of the plasma membrane, cytoskeletal
damage, and changes in the extracellular myofiber matrix
(Fridén and Lieber 1992
;
Fridén et al. 1983b
; Stauber 1989
). Because of higher susceptibility of tissue to damage
from eccentric contractions, the CNS may need to plan ahead to modify the descending command to limit the damage. The additional planning activity in the cortex for the "damage reduction" may contribute to
the greater NP signal.
DIFFERENT CONTROL STRATEGY.
It has been reported that the motor unit recruitment pattern differs
from eccentric to concentric contractions (Hoffer et al.
1980; Moritani et al. 1988
; Schieppati et
al. 1987
). During an eccentric contraction, high-threshold
motor units are selectively recruited as compared with a concentric or
isometric contraction, in which low-threshold motor units are recruited
first (Howell et al. 1995
; Nardone et al.
1989
). An altered motor unit recruitment order may reflect a
unique nervous system control strategy for eccentric actions, and that
strategy may need greater cortical activity to carry it out. However, a
recent study (Bawa and Jones 1999
) suggested that
selective recruitment of high-threshold motor units does not occur
during eccentric contractions of human wrist flexor muscles. More
studies are needed to determine whether a reversal in motor unit
recruitment order is a robust phenomenon for eccentric muscle actions.
Influence of speed of movement on MRCP NP
It is expected that the amplitude of MRCP NP depends on the rate or speed of the movement because greater muscle (and presumably brain) activities are needed to move the same load at a faster speed (force-velocity relationship). In the present study, the speed of movement was the same during eccentric versus concentric contractions. Thus the greater NP for the eccentric task in the present study did not have a biased contribution from the speed of movement.
MRCP PP
The MRCP PP was greater for the eccentric than concentric
contractions. The PP was defined as the amplitude from the peak of the
NP and the baseline to the value corresponding to the time of movement
completion (right before the weight touched the floor). Because the
peak of the NP occurred ~350 ms after the onset of EMG and the entire
duration of PP was after this peak, this signal (PP) has little
relation to movement planning and execution but must be more closely
associated with feedback signals (e.g., sensory information from
muscles and joints) to be processed in the brain (Hallett
1994; Kornhuber and Deecke 1965
;
Shibasaki et al. 1980
; Tarkka and Hallett
1991
). As indicated by force fluctuation data, eccentric
movement is associated with higher force variability, which indicates
that the movement is more difficult to control. Consequently, a greater
amount of sensory information related to more variable eccentric
actions may be conveyed to the brain. The higher level of PP may be a
result of processing the eccentric-related sensory information. One
source of sensory information that is likely to be greater during an
eccentric (lengthening) than a concentric (shortening) muscle
contraction is Ia afferent activity, which results from stretching
muscle spindle receptors.
Experimental evidence has supported the view that the human stretch
reflex has a delayed "long latency" response that is a transcortical reflex (e.g., Matthews 1991;
Thilmann et al. 1991
; however, see Corden et al.
2000
). The notion of transcortical reflex implies that the
stretch-induced Ia afferent volley causes firing of cortical neurons
that, in turn, activate the muscle being stretched. It is very likely
that this reflex-related cortical activity contributes to the PP
because it occurs after the movement begins. On the contrary, there
should be no stretch reflex-related cortical activity during a
concentric muscle action because the muscle is not stretched.
Onset of NP
On average, the onset of NP for the eccentric task was ~100 ms earlier than that for the concentric contraction. The earlier NP onset time suggests that the brain began preparing for eccentric movement earlier than for the concentric task. The earlier onset time may be explained by additional cortical planning for more movement complexity, modulation of monosynaptic reflex excitability, and carrying out a different control (e.g., motor unit recruitment) strategy for an eccentric action.
Conclusions
It has long been speculated that the nervous system poses unique strategies for controlling eccentric muscle actions. This study shows, for the first time, that the brain plans eccentric movements and processes eccentric-related sensory information differently than it does for concentric muscle contractions. Because eccentric movements are more complex, make muscles more prone to damage, and perhaps require a unique motor unit recruitment strategy to carry out the actions, the greater NP may reflect additional cortical planning activities or effort to deal with these "special problems." The higher magnitude of MRCP PP for the eccentric contractions may indicate that a larger amount of sensory information is being processed in the brain and additional reflex-induced cortical activity resulted from stretching the muscles. The earlier NP onset time suggests that not only are the cortical activities associated with planning eccentric actions greater but also the neurons begin the planning activities earlier.
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ACKNOWLEDGMENTS |
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We thank the anonymous reviewers whose comments improved the manuscript.
This work was supported in part by National Institutes of Health Grants NS-35130, NS-37400, and HD-36725 to G. H. Yue and by research funds from the Department of Physical Medicine and Rehabilitation at the Cleveland Clinic Foundation.
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FOOTNOTES |
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Address for reprint requests: G. H. Yue, Dept. of Biomedical Engineering/ND20, The Cleveland Clinic Foundation, 9500 Euclid Ave., Cleveland, OH 44195 (E-mail: yue{at}bme.ri.ccf.org).
Received 19 January 2001; accepted in final form 22 June 2001.
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