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1The Miami Project to Cure Paralysis, Department of Neurological Surgery, and 2Department of Physiology and Biophysics, University of Miami Miller School of Medicine, Miami, Florida; and 3Physiology Section, IMB, Umeå University, Umeå, Sweden
Submitted 2 September 2005; accepted in final form 29 October 2005
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ABSTRACT |
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INTRODUCTION |
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; Dum and Kennedy 1980; Kernell et al. 1975). Likewise, during muscle fatigue, the EMG may not change, may increase, or may decline for units that show large or intermediate force declines. In units that are more fatigue resistant, either no change or potentiation of EMG may accompany the decline in force (Burke et al. 1973; Celichowski et al. 1991; Enoka et al. 1992; Gardiner and Olha 1987; Hamm et al. 1989; Sandercock et al. 1985). Furthermore, changes in EMG potentials, when present, usually recover before the force is restored (Sandercock et al. 1985). In summary, these data suggest different processes account for the changes in motor unit EMG and force.
Largely because of technical difficulties, few studies have examined activity-dependent changes in the relationships between EMG and force in human muscles at the level of single motor units. In particular, it is difficult to follow the activity of the same motor unit during prolonged contractions that involve strong forces. Thus most previous studies on long-term changes in EMG and force have been restricted to weak voluntary contractions and to changes in either the force or the EMG of low threshold units rather than on the relationships between these parameters (e.g., Carpentier et al. 2001; Christensen and Sjogaard 1999; Nordstrom and Miles 1990; Stephens and Usherwood 1977). However, simultaneous recording of single motor unit force and EMG during weak and strong contractions have been made in spinal cord–injured individuals in whom only a few motor units in a muscle remained under voluntary control. In repeated voluntary contractions that elicited fatigue in these motor units, the unit EMG was either well maintained or declined (Thomas and del Valle 2001).
Intraneural stimulation of individual motor axons in healthy humans (Westling et al. 1990) has been applied in one previous study to examine the force-EMG relationship. Fuglevand et al. (1999) report that the EMG potentials of motor units in intrinsic and extrinsic hand muscles were unchanged despite depression of force. In contrast, using trains of pulses at 40 Hz and stimulation of the median nerve through the skin, Chan et al. (1998) found that the amplitude and area of the evoked potentials from thenar motor units more than doubled for fatigable units. Fatigue resistant units showed little change in EMG.
Using intraneural stimulation, we have previously characterized single human thenar motor units with respect to their potentiation of twitch force and fatigue of tetanic force (Thomas et al. 1990, 1991a,b; Westling et al. 1990). In this study, we analyze the changes in unit EMG that accompany these changes in force.
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METHODS |
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). All subjects gave their written informed consent to participate in these experiments, conducted in accordance with the Declaration of Helsinki. Experimental setup
As described previously (Westling et al. 1990), each subject reclined in a dental chair with the right forearm supinated, extended, and resting in a vacuum cast supported by a platform (Fig. 1). Clay was molded to the shape of the hand to stabilize it, and U-shaped metal clamps were pressed into the clay to restrain the fingers. Three electrodes made of braided strands of copper wire picked up EMG from the proximal and distal thenar muscle surfaces. A common electrode, 3–4 cm long, was placed transversely over the muscle belly. The other two electrodes were close to the distal and proximal tendons. One, 
2 cm long, lay across the volar aspect of the metacarpophalangeal joint, and the other over 3 cm of the base of the thenar eminence. Although unconventional, these electrode placements permitted recording of the small EMG responses evoked by stimulation of just one thenar motor axon in the median nerve in the otherwise relaxed and electrically silent muscle. A ground electrode spanned the arm just proximal to the wrist. A custom-made transducer was aligned along the length of the thumb so that 0.5 N of resting tension was applied in both the abduction and flexion directions. Force was registered in both of these directions at right angles. An optical pulse detector attached around the middle finger recorded the pulse pressure wave.
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An insulated tungsten microelectrode (0.2 mm diam with a fine uninsulated tip; impedance: 200–400 k
) was inserted into the median nerve 10 cm proximal to the elbow. It was moved in small steps until weak negative current pulses (0.2-ms duration) delivered through the electrode evoked EMG and force in a thenar motor unit in an all-or-none manner. Thus below threshold, neither EMG nor force was produced. With small increases in current over a particular range, thenar EMG and force signals of consistent magnitude and shape were evoked simultaneously, showing the excitation of a single motor unit. Further increments in current resulted in larger and more complex EMG and force signals because additional motor units were activated. After verifying that only one thenar motor axon was stimulated (for details, see Westling et al. 1990), the following stimuli were delivered to the axon: 1) 5–10 single pulses to elicit initial twitches (Thomas et al. 1990); 2) trains of stimuli at variable interpulse intervals to determine the series of pulses that maximized unit force (Thomas et al. 1999) and/or trains of pulses at 5, 8, and 10 Hz (each for 2 s) and 15, 20, 30, 50, and 100 Hz (each for 1 s) in ascending then descending order of frequency, or vice versa, to determine the force evoked at different stimulation frequencies (Thomas et al. 1991a); 3) 5–10 single pulses to elicit twitches after posttetanic potentiation (Thomas et al. 1990); 4) 2 min of stimulation at 40 Hz (13 pulses each second) to induce fatigue (Burke et al. 1973; Thomas et al. 1991b); 5) postfatigue responses including single pulses and trains of pulses at 5–100 Hz as before fatigue.
Baseline fluctuations from the pulse pressure and respiration were minimized in two ways (Westling et al. 1990). First, using signals from the pulse detector, all single stimuli and trains of stimuli were delivered to the thenar motor axons during periods when the force baseline remained relatively flat (typically 50–100 ms after peak pulse pressure). Second, the force baseline was reset electronically to a defined level just before the delivery of single stimuli or just before the first stimulus in a train of pulses.
Data collection and analysis
EMG recorded from the distal and proximal surfaces of the thenar muscles, and the abduction and flexion forces were each sampled on-line at 3,200 and 400 Hz, respectively, using SC/Zoom (Physiology Section, IMB, Umeå University, Sweden). All data analyses were done off-line. The vector sum of the measured abduction and flexion force components represented the magnitude of the evoked forces.
Up to 10 twitches recorded before and after the series of pulse trains at different tetanic frequencies were averaged and are referred to as initial and potentiated twitches, respectively, because these tetanic stimuli increased the twitch force significantly (Thomas et al. 1990). We characterized EMG potentials obtained from both the distal and the proximal channels by amplitude, duration, and area. The sum of the durations and areas measured for the first and second phase of an EMG potential (as defined by isoelectric crossings) represented the duration and area of the potential, respectively. EMG amplitude was calculated as the peak-to-peak voltage (Fig. 2A). The corresponding EMG parameters and the peak twitch force of each unit obtained after stimulation at different frequencies were normalized to the respective initial values to show the changes in twitch EMG and force induced by this stimulation.
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Time-dependent changes in the EMG amplitude, duration, and area for the first potential in the train were calculated by normalizing the values at 20, 40, 60, 80, 100, and 120 s to the respective values at 0 s. Changes in the parameters of the last EMG potential in these same trains were assessed by normalizing the values to the respective parameters for the first EMG potential at 0 s. Thus at 120 s, these data represent the changes in EMG parameters after the delivery of 1,560 pulses. Fatigue (force decline) was calculated by dividing the peak force measured every 20 s by the force measured at 0 s.
Statistics
Separate repeated measures ANOVAs with EMG channel (distal vs. proximal) and test point (initial vs. potentiated) as factors were used to compare EMG amplitude, duration, and area before and after tetanic stimulation at frequencies between 5 and 100 Hz. Likewise, repeated-measures ANOVAs with EMG channel (distal vs. proximal) and train number (7 levels corresponding to 7 times) were used to assess EMG changes during the fatigue protocol. One-way repeated-measures ANOVAs were used to examine effects of the tetanic stimulation and the fatigue protocol on twitch forces. Tukey HSD tests were used in posthoc analyses that involved pairwise comparisons of data. Relationships between parameters were analyzed using Pearson or product-moment correlations. Use of other statistical analyses is indicated in the Results section. Mean ± SD values are given, and the threshold for statistical significance was P < 0.05.
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RESULTS |
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, 1991a,b; Westling et al. 1990). We also address the changes in unit EMG that accompany the force changes, focusing on the 23 units that were subjected to brief trains of stimulation at frequencies between 5 and 100 Hz (Thomas et al. 1991a) and to fatigue (Thomas et al. 1991b). Figure 2A shows the EMG and twitch force recorded from a single thenar motor unit when single pulses were first delivered to its motor axon. These pulses were followed by a series of trains of pulses delivered at frequencies from 100 to 5 Hz (Fig. 2B) and by more single pulses (Fig. 2C). For this unit, the twitch force increased by 94% after these trains of stimuli compared with the force of the initial twitches, whereas there were only small changes in the corresponding EMG potentials. Overall, the potentials recorded from the distal muscle surface were similar in shape to those from the proximal muscle surface, but typically larger in amplitude. Furthermore, the distal and proximal EMG was of opposite polarity for 22 of the 23 units studied (96%). This suggested that the end plates of most motor units lay near the center of the muscles.
Changes in unit EMG with twitch force potentiation
Brief periods of stimulation at frequencies between 5 and 100 Hz caused significant increases in EMG amplitude (P < 0.05), duration (P < 0.001), and area (P < 0.001; Table 1). Increases in each EMG parameter were seen in all but four units (83% of units; Fig. 3). The EMG potentials recorded from the distal muscle surface were similar in duration (P = 0.31) to those recorded from the proximal muscle surface, but significantly larger in amplitude (P < 0.01) and area (P < 0.05). There was no interaction between EMG channel (distal vs. proximal) and test point (initial vs. potentiated) for any of the EMG variables. Initial and potentiated peak-to-peak EMG amplitudes for distal and proximal records were positively correlated, as were the respective EMG areas and durations (all r > 0.96).
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). There was a significant positive correlation between the initial and potentiated twitch forces (r = 0.82, P < 0.001). In relative terms, the potentiation of twitch force was greater than the increases in any of the EMG parameters (P < 0.05 in all instances, paired t-test; Fig. 3). However, across units, no significant relationships were evident between the relative changes in any of the EMG parameters and twitch force (Fig. 4). The r values for the EMG amplitude, duration, and area for the 23 units analyzed in this study were –0.23, 0.37, and 0.15, respectively. The lack of correlations between the changes in EMG parameters and force were further emphasized by a weakening of the corresponding correlations (r = 0.04, 0.26, and 0.14) when we included data from another seven units stimulated at frequencies between 5 and 100 Hz (Thomas et al. 1991a) but not subjected to the fatigue protocol.
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Fatigue was induced in each unit by stimulating its motor axon for 2 min with trains of 13 pulses at 40 Hz delivered once per second. Figure 5 exemplifies the changes in the EMG and force during this protocol for three motor units. For the more fatigable units (Fig. 5, A and B), the first EMG potentials of the trains increased in amplitude, duration, and area during the fatigue protocol. For the last train, the EMG amplitudes for these two units were 132 (Fig. 5A) and 110% (Fig. 5B) of that recorded for the first train. The corresponding values for the duration of the potentials were 114 and 118% initial. Area data were 144 and 111% initial. The evoked tetanic forces declined to 41 (Fig. 5A) and 49% of initial (Fig. 5B). In contrast, the force for the more fatigue resistant motor unit had only fallen by 8% after 2 min of stimulation (Fig. 5C). However, the amplitude, duration, and area of the first EMG potentials in the trains increased to 128, 103, and 136% initial, respectively. Figure 5 also shows changes in the last EMG potentials in the trains. For one of the more fatigable units, the amplitude of the last potential in the train at 120 s declined during the fatigue protocol, but its duration increased resulting in an increase in its area (Fig. 5A). The duration and area of the EMG also increased for the other fatigable unit, whereas the amplitude was maintained (Fig. 5B). The value of all three EMG parameters increased for the more fatigue-resistant unit (Fig. 5C).
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). However, as shown in Fig. 7 A–C, there were no significant correlations between the relative changes in force and any of the EMG parameters (amplitude: P = 0.15, duration: P = 0.06, area: P = 0.22 for distal EMG).
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Figure 8, A–C, shows the EMG changes that occurred during the fatigue protocol by comparing EMG parameters obtained for the first and last potential of the last train (at 120 s) with the first potential of the first train (at 0 s). For the first EMG potential of the last train, the amplitude, duration, and area remained higher than their initial values for 100, 83, and 96% of units, respectively. The corresponding percentages for the last potential of the trains were 61, 48, and 65%.
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Units whose EMG potentials had slowed the most by the end of the fatigue test had greater reductions in EMG amplitude (Fig. 9A; P < 0.001), larger increases in EMG area (Fig. 9B; P = 0.014), and were the more fatigable units (Fig. 9C; P < 0.01). There were no significant correlations across units between the relative change in force and relative change in EMG amplitude or area. This together with the observation that the EMG area for most units exceeded the initial values at the end of the fatigue protocol (Fig. 8C) suggested that the force loss related to processes beyond the electrical excitation of the muscle fibers.
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DISCUSSION |
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Changes in unit EMG with twitch force potentiation
Stimulation at various frequencies between 5 and 100 Hz induced significant increases in EMG amplitude, duration, and area, changes that were accompanied by even greater increases in twitch force (Fig. 3). Significant increases in evoked EMG have also been seen in whole human muscles after a brief maximal voluntary contraction (e.g., Hicks et al. 1989) or maximal evoked contractions (e.g., Duchateau and Hainaut 1985). In cat hind limb or foot muscles, however, twitch force potentiation also occurred in almost all motor units examined, but no changes were reported for the EMG waveforms (Burke et al. 1973; Dum and Kennedy 1980; Kernell et al. 1975). Potentiation of EMG amplitude with muscle activity can result from increases in Na+K+ pump activity and from greater synchronization of muscle fiber potentials (Hicks and McComas 1989; McComas et al. 1994). Our results suggest that increased synchronization may not fully explain the potentiation of EMG amplitude in experiments on whole human thenar muscles since the duration of most of our unitary EMG potentials increased rather than decreased in response to brief stimulation at different frequencies (Figs. 3 and 4). Increases in EMG potential duration probably reflect the slowing of muscle fiber conduction velocity that occurs when extracellular K+ increases with exercise (Juel 1988). In comparison, potentiation of twitch force after repetitive stimulation is proposed to relate to phosphorylation of myosin regulatory light chains (Grange et al. 1998; Sweeney et al. 1993). That the EMG and force data changed to quite different extents further suggests that different mechanisms underlie the potentiation of thenar unit EMG and twitch force in response to stimulation at different frequencies (Fig. 3). Likewise, there were no reliable correlations between the changes in unit EMG parameters and twitch force (Fig. 4).
Changes in unit EMG with fatigue
Two minutes of intermittent stimulation at 40 Hz resulted in significant potentiation of all EMG parameters, whereas the force of the motor units decreased. That the changes in EMG parameters were largely unrelated to the changes in force show that the changes in EMG signals do not predict motor unit fatigue and vice versa. These results also show that excitation of the sarcolemma and transmission across the neuromuscular junctions was effective and changes in these processes cannot explain the force loss. Similar conclusions have been reached in studies of single cat and rat motor units (Burke et al. 1973; Celichowski et al. 1991; Enoka et al. 1992; Hamm et al. 1989; Sandercock et al. 1985), where it has been suggested that force loss relates to changes in phosphate metabolism, intercellular Ca2+ handling and altered cross-bridge kinetics (Edman 1995; Westerblad and Allen 1991; Westerblad et al. 1998).
As for motor units in cat or rat hind limb muscles, the duration and area of the EMG potentials increased with fatigue in human thenar units, consistent with data of Chan et al. (1998). However, for thenar units, there was usually an increase in the amplitude of the first EMG potential in each train of stimuli (Fig. 6A), whereas more variable amplitude effects have been observed in cat units exposed to the same fatigue protocol (Enoka et al. 1992; Sandercock et al. 1985). These results may reflect differences in relative contraction intensity. Trains of pulses at 40 Hz evoke near maximal force in human thenar units (Thomas et al. 1991a) but cause unfused contractions in most cat motor units (Botterman et al. 1986; Kernell et al. 1983). Thenar units are also relatively fatigue resistant compared with the units in many cat hind limb muscles (Thomas et al. 1991b), so the largest changes in EMG parameters do not necessarily occur in fatigable units (force <75% of the initial force after 2 min of stimulation), as is typical for motor units in cat and rat muscles (Celichowski et al. 1991; Enoka et al. 1992; Gardiner and Olha 1987; Hamm et al. 1989; Sandercock et al. 1985).
Although Enoka et al. (1992) suggested that measurements of either EMG amplitude and duration or area are adequate to assess EMG changes, further comparison of results across studies is difficult because of the general lack of consensus on how to analyze EMG signals. Sometimes an entire train of potentials is averaged, which masks possible EMG changes occurring within the train (Figs. 5 and 8). The increases in unit EMG duration and area during fatiguing contractions may reflect slowing of muscle conduction velocity or fatigue-induced variability in conduction velocity across the different fibers of a motor unit (Gydikov et al. 1979; Stalberg 1966). Both these factors, in turn, will influence the amplitude of the unitary EMG potential. Furthermore, during high-frequency stimulation, a temporal overlap between succeeding EMG potentials may result in marked signal attenuation (Day and Hulliger 2001; Fuglevand 1995; Keenan et al. 2005). Indeed, during stimulation at 50 and 100 Hz, we observed a decrease in the recorded EMG amplitude for thenar units (Fig. 2), although the force generally increased. Thus rather than reflecting a reduced efficacy of electrical transmission, the decrements in unit EMG amplitude observed within a train of potentials during the fatigue protocol (Figs. 5A and 9) and in fatigable motor units in cat or rat muscles (Enoka et al. 1992; Gardiner and Olha 1987; Hamm et al. 1989) may be an artifact caused by signal attenuation.
General implications
These data show that thenar unit EMG signals usually became larger both when twitch force potentiated and when additional stimulation induced declines in tetanic force. These activity-dependent dissociations between EMG and force must underlie some of the discrepancies in EMG–force relationships seen at the whole muscle level. For example, early increases in M-wave amplitude accompany force declines that result from repeated brief maximal voluntary contractions of thenar muscles (Hicks et al. 1989), whereas M-waves are maintained at initial levels as force declines during sustained maximal voluntary contractions (Bigland-Ritchie et al. 1982). After small daily amounts of chronic stimulation, the force of cat muscles declines in response to repeated stimulation but the EMG is maintained well (Kernell et al. 1987). These motor unit and whole muscle data emphasize that changes in EMG signals are poor indicators of motor unit and muscle force or vice versa. Thus inappropriate adjustments in force may occur when electrical stimulation is used to restore behaviors in paralyzed muscles if changes in EMG are used to control the stimulation parameters. Furthermore, when interpreting surface EMG data obtained during voluntary muscle contractions, it is important to consider that the magnitude of motor unit potentials may change in addition to alterations in motor unit recruitment and firing rate.
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GRANTS |
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ACKNOWLEDGMENTS |
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FOOTNOTES |
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Address for reprint requests and other correspondence: C. K. Thomas, The Miami Project to Cure Paralysis, Univ. of Miami Miller School of Medicine, 1095 NW 14 Terrace, R48, Miami, FL 33136-2104 (E-mail: cthomas{at}miami.edu)
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REFERENCES |
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ABSTRACT
INTRODUCTION
), duration (
), area (
), and twitch force (
), expressed as a percentage of the respective initial values (n = 23 units). Dotted line at 100 represents no change in a parameter as a result of stimulation at frequencies between 5 and 100 Hz.
