vations (Desmedt and Godaux 198 1; Thomas et al. 1986;. Thomas et al. ..... tigue test required not only maintained isolation of the single motor unit, but also ...
JOURNA LOFNEUROPHYSIOLOGY Vol. 62, No. 6, December 1989. Printtd
Task and Fatigue Effects on Low-Threshold Motor Units in Human Hand Muscle ROGER
M. ENOKA,
Departments
SUMMARY
GRANT
A. ROBINSON,
AND
of Exercise and Sport Sciences and Physiology,
AND
CONCLUSIONS
R. KOSSEV
University of Arizona, Tucson, Arizona 85 72 I
INTRODUCTION
1. The activity of single motor units was recorded in the first dorsal interosseus muscle of human subjects while they performed an isometric ramp-and-hold maneuver. Motor-unit activity was characterized before and after fatigue by the use of a branched bipolar electrode that was positioned subcutaneously over the test muscle. Activity was characterized in terms of the forces of recruitment and derecruitment and the discharge pattern. The purpose was to determine, before and after fatigue, whether motor-unit activity was affected by the direction in which the force was exerted. 2. Regardless of the task during prefatigue trials, inter-impulse intervals were 1) more variable during increases or decreases in force than when force was held constant at the target value (4-6% above the recruitment force), and 2) more clustered around an arbitrary central value than would be expected with a normal (Gaussian) distribution. Both effects were seen during the flexion and abduction tasks. The behavior of low-threshold motor units in first dorsal interosseus is thus largely unaffected by the direction of the force exerted by the index finger. The absence of a task (i.e., a direction of force) effect suggests that the resultant force vector about the metacarpophalangeal joint of the index finger is not coded in terms of discrete populations of motor units, but, rather, it is based on the net muscle activity about the joint. 3. Motor-unit behavior during and after fatigue showed that the relatively homogeneous behavior seen before fatigue could be severely disrupted. The fatiguing protocol involved the continuous repetition, to the endurance limit, of a 15-s ramp-and-hold maneuver in which the abduction target force was 50% of maximum and was held for 1O-s epochs (ramps up and down were ~2 s each). Motor-unit threshold was assessed by the forces of recruitment and derecruitment associated with each cycle of the fatigue test. Changes in recruitment force during the protocol were either minimal or, when present, not systematic. In contrast, the derecruitment force of all units exhibited a marked and progressive increase over the course of the test. 4. After the fatigue test, when the initial threshold tasks were repeated, the behavior of most motor units changed. These changes included the derecruitment of previously active motor units, the recruitment of additional motor units, and an increased discharge variability of units that remained recruited. The variation in recruitment order seemed to be much greater than that reported previously for nonfatiguing conditions. For those units that remained recruited, the forces of recruitment and derecruitment were largely unaffected, whereas discharge rates were generally slower and more variable. Despite several dominant fatiguerelated effects, a significant feature of the data was the diversity of responses exhibited by motor units. These low-threshold units of first dorsal interosseus were not affected by the fatigue test as a homogeneous population, but, rather, they exhibited a wide range of adaptations.
1344
ANDON
0022-3077/f@
$1 SO Copyright
For at least 50 years, we have known that the activation of motor units can be described by the orderly recruitment phenomenon (Denny-Brown and Pennybacker 1938). Considerable evidence suggeststhat the pattern of motorunit recruitment is determined by spinal mechanisms (Burke 1987; Gustafsson and Pinter 1985; Liischer et al. 1979), thereby relieving higher centers of the need to be concerned with some of the details associatedwith the execution of the motor performance (Henneman et al. 1974). There has been much interest in identifying both the determinants of a recruitment pattern (e.g., Burke 1981; Henneman and Mendell 1981) and the limits of operation of a particular recruitment pattern (e.g., Datta and Stephens 198 1; Desmedt and Godaux 198 1; Garnett and Stephens 198 1; Kanda et al. 1977; Smith et al. 1980). This paper addressesthe general issueof the reliability of an activation pattern by examining the behavior of single motor units when a muscle contributes to different tasks and after the muscle has been fatigued. Since the formulation of the Size Principle (Henneman 1957), investigators have attempted to identify experimental conditions that alter an expected recruitment order. In general, alterations in recruitment order have been observed in three types of experiments: 1) an abnormal excitation of motoneurons by repetitive electrical activation of selected structures in the motor cortex, red nucleus, Dieters’ nucleus, and sural nerve; 2) variations in afferentinput conditions; and 3) the involvement of a muscle in different motor tasks (for review: Stuart and Enoka 1983). The latter condition, variable task requirements, may represent the most common cause for alterations in recruitment order that is encountered by the motor system. Seyffarth (1940) and Denny-Brown (1949) were among the first to suggestthat the firing patterns of motor units were dependent on whether the muscle, such as biceps brachii, was functioning as a prime mover or as a stabilizer. This possibility has been substantiated by reports of variations in recruitment order among the motor units of rectus femoris for the tasks of thigh flexion versus upper leg rotation (Person 1974), among the motor units of abductor pollicis brevis during abduction-adduction versus flexionextension (Thomas et al. 1978), and among the motor units of extensor digitorum communis during wrist extension versus individual and combined extension of the fingers (Thomas et al. 1978). Furthermore, Denier van der Gon and colleagues have provided convincing evidence that the behavior of motor units in biceps brachii depends
0 1989 The American Physiological
Society
TASK AND FATIGUE
EFFECTS ON MOTOR
not only on the task but also on the anatomic location of the motor unit in the muscle (Denier van der Gon et al. 1985; ter Haar Romeny et al. 1982, 1984). In contrast to these observations, measurements of recruitment force, recruitment order, twitch size, and contraction time of motor
UNITS
1345
Young and Mayer 198 l), which has shown that low-thresh-
old motor units are uniformly
fatigue resistant, we antici-
pated that the responsesof low-threshold motor units of
first dorsal interosseus woulci not be affected by a fatigue test.
units in first dorsal interosseus have indicated that task-related alterations in the expected recruitment order occur infrequently in this muscle, in lessthan -8% of the observations (Desmedt and Godaux 198 1; Thomas et al. 1986; Thomas et al. 1978). However, these analyses have not
muscle acted as a prime mover compared with when it assistedas a synergist. The term “low threshold” refers to
included a detailed consideration
motor units that are recruited at forces up to 15% of maxi-
of motor-unit
behavior,
such as the potential effects of task direction and fatigue on patterns of discharge.
The behavior of a motor unit is known to be profoundly influenced by its activation history. One convincing example of these effects is the adaptation that occurs in motorunit discharge during a sustained contraction. Several groups have shown that, under such conditions, there is a fatigue-related decline in motor-unit discharge (BiglandRitchie et al. 1983b; Grimby et al. 198 1; Gydikov and Kosarov 1974). Bigland-Ritchie and colleagues (BiglandRitchie et al. 1983a, 1986; Woods et al. 1987) have pro-
posed that this decline is mediated by afferent feedback for the purpose of optimizing the motor-unit
activity to the
changing mechanical state of the muscle. Given this effect, we wondered whether motor-unit behavior during a prescribed threshold task might be different immediately after an episode of fatiguing activity. Furthermore, based on the motor unit-classification literature (e.g., Grimby et al. 198 1; Kato et al. 198 1; Stephens and Usherwood 1977;
[Flexor
I
The purpose of the study was to determine, before and
after a fatigue test, whether the behavior of Iow-threshold motor units in first dorsal interosseus differed when the
mum. Such units have been shown to be uniformly fatigue
resistant in first dorsal interosseus (Stephens and Usherwood 1977). Motor-unit behavior was defined in terms of the forces of recruitment and derecruitment and the dis-
charge pattern of action potentials.
had diverse effects on motor-unit
i I
rFDl
1.
Position
of the subject
in the manipulandum
and
mined by the net muscle activity about the joint.
In con-
trast, the fatigue results indicate that the effects of activation history on individual motor units are heterogeneous, that is, fatigue disrupts the consistent discharge characteristics of unfatigued motor unit behavior. Preliminary re-
Subcutaneous EMG
of the
the
langeal joint of the index finger is not coded in terms of discrete populations of motor units but rather it is deter-
FDI Surface EMG
the source
during
motor units of first dorsal interosseus suggests that the vector representing resultant force about the metacarpopha-
Force Force
FIG.
behavior
threshold task. The absence of a task effect among the
Digitorum Surface EMG
I-------
We found that the be-
havior of low-threshold motor units was independent of whether the muscle contributed to its prime mover (abduction) or its synergist (flexion) function but that fatigue
5 data
signals.
Arm
and
hand
were
restrained
to focus on the contribution of first dorsal interosseus to the abduction and flexion forces about the metacarpophalangeal joint of the index finger. Data on the right are from the threshold task when force was exerted in the flexion direction. Subject was required to keep the abduction force near 0 and to employ similar rates of change in force when the force was increased and when it was decreased. When force was exerted in this direction, first dorsal interosseus acted as a synergist to the larger flexor digitorum muscle. In this example, the target force was low, and the EMG record obtained from the surface bipolar electrodes over flexor digitorum was dominated by the discharge of a single motor unit. EMG records from first dorsal interosseus were acquired with a monopolar electrode (surface) and with a “branched” bipolar electrode (subcutaneous). Force was measured with 2 transducers that were positioned at the level of the proximal interphalangeal joint of the index finger.
1346
R. M.
ports have appeared previously et al. 1987).
(Enoka
ENOKA,
G. A. ROBINSON,
et al. 1987; Kossev
METHODS
Six human subjects (2 l-55 yr of age) gave their informed consent for participation in the study. The experiments were performed on the first dorsal interosseus muscle of the left hand of the subjects. First dorsal interosseus is a bipennate muscle with a central tendon and fibers arising from the ulnar aspect of metacarpal I and the radial aspect of metacarpal II and inserts, on the radial side, into the metacarpophalangeal joint capsule and the base of the proximal phalanx of the index finger (Brand 1985; Landsmeer 1965; Valentin 198 1). The fibers from metacarpal II have a uniform length of 1.6 cm, whereas the fibers from metacarpal I vary from 2.5 to 3.5 cm, with an average of 3.1 cm (Brand et al. 198 1). As a result of this arrangement, first dorsal interosseus is the only muscle to exert an abduction force on the index finger, but it is one of several muscles to exert a flexion force about the metacarpophalangeal joint of the index finger (Eyler and Markee 1954; Garnett and Stephens 198 1; Landsmeer 1965). First dorsal interosseus does not contribute to extension of the interphalangeal joints (Brand 1985; Valentin 198 1). Based on cadaver estimates (n = 12; 22-54 yr), first dorsal interosseus comprises - 119 motor units, with an average of 340 muscle fibers in each motor unit (Feinstein et al. 1955). The present studies concern 1) the normal discharge characteristics of motor units when the index finger exerts a force in either the abduction or flexion direction, and 2) fatigue-induced changes in the same discharge characteristics.
AND
Mechanical
A. R. KOSSEV
recording
The study was conducted with the subjects in a seated position. The left arm was abducted to a horizontal plane so that the hand and forearm were pronated and resting on a manipulandum, the elbow joint was at about a right angle, and the upper arm was in a frontal plane (Fig. 1). The forearm and hand were immobilized in the manipulandum by several restraints: 1) a forearm strap; 2) a support for the thumb that held the angle between metacarpals I and II at - 1 .O rad; 3) a strap over fingers II-IV; and 4) a brace that minimized flexion at the metacarpophalangeal joint of the index finger. Furthermore, the index finger was placed in an individualized mold (polyvinyl silicone) and strapped to an L-shaped aluminium bar that was positioned along the radial and palmar surfaces of the finger and kept the interphalangeal joints extended. The hand was placed in the manipulandum so that the proximal interphalangeal joint was aligned with the two force transducers (Sensotec model 13; capacity 220 N). The aluminum bar served as an interface between the finger and the transducers so that one transducer sensed the abduction force and the other sensed the flexion force. The signals from both transducers were displayed on an oscilloscope and recorded on analog FM tape (bandwidth DC- 10 kHz).
Electrical
recording
Electromyographic (EMG) signals were obtained from three sources: 1) subcutaneous electrode over first dorsal interosseus; 2) surface electrode over first dorsal interosseus; and 3) surface electrodes over the wrist and finger flexors located in the forearm, principally flexor digitorum. The subcutaneous procedure has
A
Subcutaneous EMG
Force
FIG. 2. Determination of the recruitment and derecruitment forces during the fatigue test. A: abduction force during 2 cycles of the fatigue test. Subject graded the force from 0 to 50% of maximum, held the target force for 10 s, graded the force back to 0, then repeated this sequence until the target force could no longer be attained. This subject used a target force of 12 N and was able to perform 9 cycles of the fatigue test. B: variation in the subcutaneous EMG associated with the gradation of force. When the force approached 0, it was possible to determine the force at which the unit was derecruited and subsequently the force at which it was recruited. These decisions were made from chart records that displayed the data with a much faster time base (100 mm/s) than that shown in the figure (10 mm/s).
TASK
n E 2
AND
FATIGUE
EFFECTS
ON
MOTOR
UNITS
1347
l~:~e---•=e=e---•~o-o-e-o-e
50 40
l
25 20
n \” 17
I5 IO 5
Fatigue Test Cycle FIG. 3. Variation in recruitment force, derecruitment force, and the rate of change in force during the fatigue test. A: 2 units that were isolated during a single experiment. Because recruitment and derecruitment forces of single motor units are known to be influenced by the rate of change in force, subjects were required to grade force relatively slowly and at a consistent rate throughout the test. The lowest panel shows the variation in the rate of change in force during the fatigue test when force was graded between 0 and the target value (2 1 N). Solid line represents the increase in force (recruitment phase), and dashed line indicates the decrease in force (derecruitment phase). The 2 units had initial recruitment forces of 10 (-) and 7% (- - -) of maximum. These values declined slightly during the fatigue test. Initial derecruitment forces were 23 and 0% of maximum, respectively, and these values increased markedly during the test. B: another 2 units from a different experiment. The rate of change in force remained consistent throughout the test. Target force was 23 N. The 2 units were initially recruited at 2 1 ( -) and 35% (- - -) o f maximum. Recruitment force varied but did not change systematically during the fatigue test, although, at cycle 8, 1 unit (- - -) ceased contributing to the performance. The 2 units were derecruited while the target force was being maintained at 50% of maximum. These 4 units indicated the general behavior observed in the study, that recruitment force may decline slightly during the fatigue test or it may vary unsystematically, but derecruitment force invariably increases.
been described previously (Enoka et al. 1988). Briefly, a branched bipolar electrode was inserted between the skin and the fascia of first dorsal interosseus. The electrode consisted of two stainless steel, Formvar-insulated wires (50 pm) that had the insulation removed circumferentially in three equidistant bands. Each band was - 100 pm across and 1 mm from an adjacent band. Two bands were on one wire, the so-called “branched” wire (Gydikov et al. 1986), and the third band was on the other wire but located longitudinally between the two bands on the branched wire. The bands were - 10 cm from the end of the wires. The electrode was inserted with a 25gauge needle over the proximal end of first dorsal interosseus and oriented so that it was perpendicular to TABLE
1.
fibers arising from metacarpal I. The needle penetrated the skin in two places so that the electrode was located under the skin for -2-3 cm. The subcutaneous track was approximately parallel to metacarpal I. Once inserted, the needle was removed, and both ends of the electrode remained outside the skin, whereas the uninsulated region (i.e., the three bands) was subcutaneous and lying over first dorsal interosseus. Given this arrangement, it was possible to carefully maneuver the electrode to optimize the isolation of a single motor unit. The branched bipolar electrode, which had an impedance in the range of 0.74-2.08 MS2 at 100 Hz and 0.16-0.48 Ma at 1.O kHz, was used to measure the potentials of isolated motor units.
Number ofcycles and decrementsin maximum voluntary contractionsfor fatigue test Day Abduction
1
Day 2 Flexion
Flexion
Abduction s
Number Decrease Decrease
of cycles in abduction force in flexion force
11.2 k 2.3 -19.3 + 8.3 -21.2 -t 14.4
5.1 f 1.5 -28.2 7.6 -29.9 k 11.4 zk
12.1 I!I 3.8 -25.3 9.4 -22.4 k 11.4 k
4.3 1.7 -27.3 5.5 -31.4 + 5.8 -t
I!I
Values are expressed in percentages and are means + SD for 3 subjects who performed the fatigue test twice on 2 different days. On day 1, the fatigue test was first done in the abduction direction and then, immediately, in the flexion direction. On day 2, the order was reversed.
1348
R. M.
ENOKA,
G. A. ROBINSON,
Abduction
AND
A. R. KOSSEV
Force
Flexion Force
Subcutaneous
EMG
Motor Unit Potential
IOOJN
FIG. 4. Typical data for a single motor unit during the threshold task. Data on the left are from a trial when force was exerted in the abduction direction, and data on the rightare from a trial when force was exerted in the flexion direction. For the abduction trial, recruitment force was 6% of maximum, the target force was 8% of maximum, the derecruitment force was 8% of maximum, and force increased and decreased at a rate of 3% of maximum/s. For the flexion trial, recruitment force was 5% of maximum, the target force was 8% of maximum, the derecruitment force was 8% of maximum, and the force increased and decreased at a rate of 3% of maximum/s. Maximum force was 2 1 N in the abduction direction and 27 N in the flexion direction. Bottom: spike-triggered average (n = 64) of the potential as recorded by the subcutaneous electrode during several trials in each direction. Similarity in the shape of the averaged potential confirms that the same motor unit was examined in the 2 directions. Furthermore, the subcutaneous EMG records show that the behavior of the motor unit (i.e., recruitment force, discharge rate, and derecruitment force) was similar when force was exerted independently in the two directions.
The signal from the electrode was amplified (2,500- 10,000X), led through a band-pass filter (300 Hz- 10 kHz; roll-off at 48 dB/octave), displayed on an oscilloscope, and stored on analog FM tape. The amplitude of the motor-unit potentials was in the range of 0.04-0.49 mV. Identification of a single motor-unit potential was based on waveform shape, as seen on-line with a waveform digitizer (5 ms/Div.). Once identified, the potential of a single motor unit was discriminated (BAK DIS-l), and the logic pulse was led to an audio unit for an on-line account of the discharge of the unit. A monopolar surface electrode (4-mm diam; silver-silver chloride) was fixed over the belly of first dorsal interosseus to provide a global record of the EMG activity in the muscle. The reference electrode was placed on the dorsolateral aspect of the hand. Similarly, a bipolar surface electrode @-mm diam; silver-silver chloride) was placed on the ulnar side of the forearm to measure the EMG activity of the muscles, principally flexor digitorum, involved in flexion of the wrist and fingers. Because these muscles provide the major flexion force exerted by the index finger, the TABLE
Abduction Flexion
2.
purpose of this signal was to provide a global EMG record that could be compared qualitatively to the surface EMG for first dorsal interosseus (Fig. 1). Both surface EMG signals were bandpass filtered ( 10 Hz- 10 kHz), displayed on an oscilloscope, and stored on analog FM tape.
Experimental
procedures
Although the protocol simply involved the isometric gradation of force exerted at the proximal interphalangeal joint of the index finger, it was necessary for subjects to participate in several practice sessions to achieve a high degree of accuracy in the prescribed tasks. All tasks involved the ramp increase in isometric force to some prescribed target, maintenance of the target force for several seconds, and the ramp decrease in force back to base line. Subjects were instructed to match the rate of change in force for the ramp increase and decrease in force. The goal of the practice sessions was to familiarize the subjects with both the timing and the performance criteria for each task.
Maximum voluntary force and theforce characteristicsof the thresholdtask Maximum Force, N
Recruitment Force, %
Rate of Force Increase, %/s
31 -+ 8 (19-42) 41 * 10 (23-58)
5.6 AI 3.6 (2-16) 9.0 k 5.6 (2-28)
3.0 + 1.4 (l-6) 3.9 AI 2.8 (1-14)
Values are means k SD with range in the index finger. First dorsal interosseus flexion force. The % (relative) values are involved at least 2 maximum-force and
Target
Force,
%
9.9 t 5.2 (4-20) 14.5 -t 6.8 (5-34)
Derecruitment Force, %
Rate of Force Decrease, %/s
6.4 k 49(0-19) 6.9 k 6.6 (O-28)
2.5 IL 1.6 (l-8) 3.9 k 2.6 (1-13)
parentheses and represent the force and rate of change in force exerted at the proximal interphalangeal joint of is the only muscle that contributes to the abduction force, whereas it is one of several that contributes to the expressed as a percentage of the maximum force. These data were derived from 26 experiments, each of which 7-12 threshold trials in both the abduction and flexion directions.
TASK
AND
FATIGUE
EFFECTS
TABLE 3. Performance .features associated with the maintenanceof the targetforce during the thresholdtask
% Abduction Flexion
Target
4 -t 3 (O-l 1) 6 IL 4 (O-13)
Duration,
Interimpulse Interval, ms
s
4.02 + 1.22 (2.26-7.60) 3.43 IL 0.59 (1.74-4.23)
87 + 17 (50-120) 82 t 27 (55-152)
Values are means -t SD with range in parentheses. Force difference refers to the difference between the recruitment and target forces (% of maximum). Target duration indicates the time that the target force was maintained. The statistics on the interimpulse intervals were performed on the mean values (n = 70-682) of the 7-12 trials for each motor unit (n = 23).
Because several trials of each task were performed (n = 2- 12), it was critical that the temporal aspects of each performance remained as consistent as possible. The timing of each task was based on a verbal count (spaced at 1-s intervals) given by one investigator. The performances elicited by this procedure proved reliable enough to meet the aims of the study. The behavioral requirements included the unfamiliar criteria of functional isolation of the test muscle and the exertion of force in a single desired direction (i.e., abduction or flexion). During each experiment, one investigator provided the count for each task, another watched for functional isolation of the test muscle, and a third monitored the two force signals. The subject was informed of the extent to which the performance met the experimental criteria. Trials that did not meet these criteria were discarded. The following three ramp-up, hold, ramp-down tasks were used: 1) Maximum voluntary abduction and flexion forces. The maximum voluntary capacity in each direction was tested independently by having the subject grade the force, first only in Recruitment
30
0 24
18 //
/
/
//
/
/
//
/
//
/
/
/
/
MOTOR
UNITS
c
/’
Derecruitment 0
/ a
0/
/
”
1
1
I
,
0
6
12
18
24
I
30
,’ e
0
/
//
/
/
/
//
/
/
/
/
/
/’
/c
a
e’ 0
I349
abduction and then only in the flexion direction, from zero up to maximum. The force was increased to maximum in -2 s while the subject observed the signal on the oscilloscope to ensure a constant rate of change in force. The maximum force was maintained for 2-3 s. 2) Motor-unit threshold force for abduction and flexion. The target was set at a value that was sufficient to sustain a slow but steady discharge of a selected motor unit. The target force was set at a level that was 5- 10% greater than the recruitment force, where the recruitment force was defined as the force at which the unit was recruited. Because the rate of change in force is known to affect recruitment force (Budingen and Freund 1976; Desmedt and Godaux 1978), it was critical that the performance of this task remain consistent for each subject. The ramp parts of the task lasted -2 s, whereas target force was maintained for - 3 s. Subjects were instructed to employ similar rates for the increase and decrease in force. Furthermore, because the time between trials can influence recruitment force (Denier van der Gon et al. 1985), subjects rested 5-30 s between trials to minimize history-dependent effects. 3) Fatigue test. In the course of prescribing a fatigue test that would enable us to address the aims of the study, we considered several designs that ranged from a sustained maximum voluntary contraction to a series of low-force, rhythmic contractions. Our choice was an intermediate task that would induce fatigue within a few minutes and would allow us to monitor a functional index of motor-unit excitability (viz. forces of recruitment and derecruitment) as the muscle became fatigued. To this end, the subjects performed a cyclic ramp-and-hold task, without rest between cycles, with abduction force held at 50% of maximum for 10-s epochs (Fig. 24. The task required that the abduction force be carefully graded up to the target value and back to base line (taking -2 s each), so that the magnitude of the rate of change in force remained relatively constant throughout the test (Figs. 2 and 3). Given this condition, it was then possible to ascribe variation in the forces of recruitment and derecruitment to fatigue-related
Force Difference,
ON
0 m
l 1
1
1
6
12
18
Abduction Force (% of maximum) FIG. 5. Associations between the abduction and flexion recruitment and derecruitment forces. Line of identity for each relationship (recruitment on the left and derecruitment on the right) is indicated by the dashed line. For this sample of low-threshold motor units, recruitment force (percent of maximum) in the abduction direction was highly correlated with the recruitment force in the flexion direction (r2 = 0.60, P < 0.05). Similarly, derecruitment force (percent of maximum) in the abduction direction was highly correlated with the derecruitment force in the flexion direction (r2 = 0.63, P < 0.05). Data are for 19 units for which there were secure measures of the recruitment and derecruitment forces in both the abduction and flexion directions. These data indicate that the relative force at which a unit was recruited and derecruited during the threshold task was related for the 2 directions of the task.
I
24
I
30
1350
R. M.
ENOKA,
G. A. ROBINSON,
AND
A. R. KOSSEV
Abduction
lexisn
0
-2.5
_-.A---A
-.--
-2.0
-1.5
-.-l--_------L_---.
-1.0
--.-_L---------L
-0.5
0
0.5
----1 .o Time (s) -
1.0
. II ~_-_--L_-L ____._ -0.5
0
0.5
.I 1.0
._____I-- -- -.---.-------I-----1.5
2.0
2.5
2 3.0
FIG. 6. Temporal variation in interimpulse interval during the increase and decrease in force of the threshold task. The 4 panels represent the variation in interimpulse intervals for the abduction and flexion directions during 7 trials for the same motor unit. Line figure at the bottom represents the ramp-up, hold, ramp-down threshold task. Zero time is represented twice at the transition points between the ramp portions of the threshold task and the target force. For abduction, maximum force was 37 N, recruitment force was 3 t 1% of maximum, rate of increase in force was 2 + 0% of maximum/s, target force was 14% of maximum, derecruitment force was 4 -+ 2% of maximum, and rate of decrease in force was 1 of: 0% of maximum/s. For flexion, maximum force was 45 N, recruitment force was 8 t 3% of maximum, rate of increase in force was 3 + 1% of maximum/s, target force was 2 1% of maximum, derecruitment force was 1 t 1% of maximum, and rate of decrease in force was 2 -t 0% of maximum/s. For both abduction and flexion directions, the average derecruitment force was less than the recruitment force and there appeared to be no systematic variation in interimpulse interval.
processes rather than rate-dependent effects. Most subjects were able to perform 10-20 cycles before the test was terminated. The effect of task (i.e., abduction vs. flexion) on fatigue-test performance was studied in three subjects (Table 1). They performed the fatigue test, in a blind design, twice on two different days. On one day, the subjects performed, on average, 11.2 cycles of the test in the abduction direction until the abduction endurance limit was reached and then immediately were able to do 5.1 cycles of the test in the flexion direction before reaching the flexion endurance limit. On the other day, the order was reversed, and the criterion was again the endurance limit in each direction. On this occasion, the subjects performed an average of 12.2 cycles in the flexion direction followed by 4.3 cycles in the abduction direction. It is apparent in Table 1 that the reduction in maximum force was similar in both directions after a single fatigue test (viz. -19.3 vs. --21.2, --28.2 vs. -29.9, --25.3 vs. -22.4, and -27.3 vs. --3 1.4% of maximum). In addition, although the endurance limit was assessed subjectively (i.e., failure of the subject to maintain the target force), the number of fatigue-test cycles that were needed to meet this criterion was similar for all three subjects. Because subject performance was similar regardless of task, abduction was arbitrarily chosen for the fatigue test. The overall experimental protocol involved the performance of the maximum-voluntary-force and the threshold-force tasks be-
fore and after the fatigue test. Subjects performed two trials of the maximum voluntary contraction in each direction. If the maxima in these two trials were not within 5% of each other, a third trial was performed. Brief rest periods were given between each trial. Next, the subject did 7-12 trials of the threshold task, first in the abduction direction and then in the flexion direction. Based on the audio signal of motor-unit discharge during contiguous trials, it was possible to define rest intervals for the threshold task that minimized the effects of repetitive activity. In contrast, the goal of the fatigue test and the subsequent threshold- and maximumforce trials was to determine the effect of prior repetitive activity on the recruitment force and the discharge characteristics of the motor unit. The fatigue test was performed until the endurance limit was reached, and then, with no rest periods, the subject repeated the threshold- and maximum-force tasks. The number, count, and target levels (i.e., absolute force) for the threshold trials after the fatigue test were the same as those before the fatigue test. To maintain fatigue in first dorsal interosseus, a few cycles (M = 2-6) of the fatigue test were repeated after every third trial of the threshold task. After the threshold trials, one maximum-force trial was done in each direction. If the motor unit was not recruited during the threshold trials after the fatigue test, then another test was performed to verify that the electrode had not moved. Either the threshold task was
TASK
AND
FATIGUE
EFFECTS
repeated immediately and the target force gradually increased until the unit was recruited, or else the threshold task was repeated after the muscle had been allowed to recover for several minutes.
Data analysis
RESULTS
of task on motor-unit
MOTOR
UNITS
1351
Abduction 80 60
The force and EMG data stored on analog FM tape were replayed and recorded on a chart recorder (Gould ES-2000) that was operated at a paper speed of 100 mm/s. Because a single motor unit had been isolated during the experiment by the appropriate positioning of the subcutaneous electrode, it was possible to use amplitude discrimination for the identification of motor units on the chart paper. With the use of this method, the record provided a resolution of ~5 ms and 3% of the maximum voluntary force. The following measurements were made from the chart record: 1) maximum-voluntary-abduction and flexion forces (IV); 2) recruitment and derecruitment forces (percent of maximum) for each motor unit during threshold trial; 3) rate of change in force (percent of maximum per second) during the increase and decrease in threshold force; 4) interimpulse intervals (milliseconds) during the threshold trials; and 5) recruitment and derecruitment forces (percent of maximum) for each motor unit during the fatigue test. Comparisons of motor-unit behavior before and after the fatigue test required not only maintained isolation of the single motor unit, but also similar pre- and postfatigue threshold performances. The extent to which each subject could satisfy the latter criterion was determined by comparing the magnitude of the target force and the rate of change in force in the two instances. All subjects were able to satisfy this criterion for most trials; unacceptable trials were discarded. The isolation of a single motor unit was regarded as secure when the shape of the action potential, as determined by spike-triggered averaging (e.g., Fig. 4 for averages during threshold tasks), was the same before and after the fatigue test. Each subject was afforded ample practice time before the day of the experiment to ensure a reliable performance. Statistical tests included linear regressions, the KolmogorovSmirnov goodness-of-fit test, and measures of kurtosis and symmetry. Significance is reported at P < 0.05.
Efict
ON
behavior
After two to three training sessions,it was possible for all subjects to exert a force in one direction (e.g., abduction) while force in the other direction (e.g., flexion) was kept near zero (Figs. 1 and 4). Although it was also possible to meet this criterion while exerting substantial forces, subjects were permitted to exert small forces in the nontest direction during maximum-force trials because this tended to result in the greatest forces. The maximum voluntary force (mean +- SD) was usually lessin the abduction direction (3 1 & 8 N) than in the flexion direction (4 1 t 10 N). The average ratio of the abduction force relative to the flexion force was 0.78 t 0.13 (range: 0.54-l .OO). In the performance of the threshold task, force was slowly increased (3.0 and 3.9% of maximum/s for abduction and flexion, respectively) to the target value, held at the target for several seconds, and then slowly decreased (2.5 and 3.9% of maximum/s, respectively) back to base line (Table 2). The target force was held for 4.02 t 1.22 s in the abduction task and 3.40 -t 0.59 s in the flexion task (Table 3). The average target forces were relatively low (9.9
40
Flex ion 40 30 20 IQ I
ml
I
150
Interimpulse
Interva ,I (ms)
FIG. 7. Histograms of the interimpulse inter rvals when force was maintained at the target level for the 2 directions. Data are from the same motor unit shown in Fig. 6. Based on the Kolmogorov-Smirnov goodness-of-fit test, neither of the distributions, as for all motor units in the study, were Gaussian (P < 0.000 1) because of varying degrees of kurtosis and skewness. Absence of a Gaussian distribution was present in both the abduction and the flexion directions. Flexion distribution was characterized by a marked kurtosis. Abduction: interimpulse interval statistics (median, mean t SD, and range) were 60 ms, 64.3 -t 14.8 ms, and 20- 130 ms. Distribution (n = 450) was positively skewed (skewness = 0.907) and was more peaked (kurtosis = 1.845) than for a Gaussian distribution. Flexion: interimpulse interval statistics were 60 ms, 57.8 2 10.3 ms, and 40-130 ms. Distribution (n = 223) contained a marked positive skew (skewness = 1.555) and was substantially more peaked (kurtosis = 9.593) than normal. Because the most dominant feature of the distributions was the marked kurtosis, the data emphasize that the interimpulse intervals were more similar to the central value than might be expected based on a normal distribution.
and 14.5% of maximum for abduction and flexion, respectively) and were set, on average, at values of 4 +- 3% (abduction) and 6 t 4% (flexion) of maximum above the recruitment force (i.e., the force at which the motor unit was recruited; Table 3) Subjects performed 5-l 2 trials of the threshold task in each direction. A typical contribution of a motor unit to these isometric force-time profiles is shown in Fig. 4. On the left are shown the forces (abduction and flexion), subcutaneous EMG, and averaged motor-unit potential during the performance of the threshold task in the abduction direction. The companion performa rice, force exerted in the flexion direction, is shown on the right side of Fig. 4. The bottom traces in Fig. 4 are spike-triggered averages (n = 64) of the motorunit potential when force was exerted in each direction; the
1352
R. M.
ENOKA,
G. A. RQBINSON,
similarity in shape of the potential confirms that the same motor unit was examined in each task. This criterion was also used to ensure that the same motor unit was studied before and after the fatigue test. BEHAVIOR DURING FORCE GRADATION. Although the average recruitment force of motor units in the abduction direction was slightly lessthan that in the flexion direction (2.9%), this difference was at the limit of our measurement resolution. Similarly, a paired-sample analysis of derecruitment forces (Table 2) revealed no significant differences for the two directions. The force at which a motor unit was recruited in the abduction direction was a good predictor (Fig. 5) of the recruitment force in the flexion direction (r2 = 0,60, P < 0.05) and, similarly, derecruitment forces were significantly correlated for the two directions (Fig. 5; r2 = 0.63, P < 0.05). Because the target force was set above the recruitment force, the contribution of discharge rate to the increase in force above the recruitment value was examined by plotting interimpulse interval against time during the ramp-up and ramp-down phasesof the threshold task (Fig. 6). For
AND
this motor unit, both in abduction and flexion, there appeared to be no obvious systematic variation in interpulse interval during the gradation of force over this range. Furthermore, displays of the data as joint-interval histograms (Fig. 1014)(Clamann 1969; Ivanova et al. 1986) indicated no unusual discharge patterns during this phase of the threshold task; that is, because the data in Fig. 1OA are distributed symmetrically about the line of identity, successive intervals are considered to be independent (Rodieck et al. 1962). Because the average difference between recruitment force and target force was only 4% in the abduction task and 6% in the flexion task, most of the motor units exhibited the typical pattern shown in Fig. 6. BEHAVIORATTARGETFORCE. Asindicatedin Figs. 1 and 3, visual feedback of the force signals on the oscilloscope made it possible for the subjects to reliably maintain the target force for several seconds(Table 3)” The distributions of interimpulse intervals while force was maintained at the target level were analyzed with a Kolmogorov-Smirnov goodness-of-fit test. It was found that none of the distributions were Gaussian (P < 0.00 1) becauseof a greater degree
12N
2
3
II
4
I I
1
5
6
! 7
III i/
I I
I I
I 1’1
II
II I,
III I,’
A. R. KOSSEV
behavior of a motor unit that FIG. 8. Threshold-task was substantially affected by the fatigue test. Data show the discharge pattern of a single motor unit during the performance of the threshold task before (top 7 trials) and after (bottom 7 ha/s) the fatigue test. Action potentials were plotted with a computer graphics package. Target force for the threshold task was 15% of maximum; the maximum force was 3 1 N. Trials were aligned C- - -) at the instant that the target force was attained. L@ hit of each trial indicates the time when force began increasing from 0. Recruitment force was 12 + 3% of maximum before the fatigue test, and the derecruitment force was 7 + 3% of maximum before the fatigue test. ‘4lthough the force record in the middk of the figure was from 1 trial, the performance in all 14 abduction trials (i.e., before and after the fatigue test) was similar. It is apparent that, although the target force for the threshold task remained the same before and after the fatigue test, the contribution of a single motor unit to the task could be altered markedly.
TASK AND FATIGUE
EFFECTS ON MOTOR
of kurtosis and a skew toward longer intervals (positive skew) than normal. These characteristics applied to the distributions associated with both the abduction and flexion directions (Fig. 7). Statistical measuresof kurtosis and skew indicated that the degree of kurtosis was the more prominent effect, which meant that the interimpulse intervals tended to be more clustered around a central value than would be expected with a normal distribution; that is, there was lessvariability in the interimpulse interval than would be expected with a normal distribution. Table 3 reports the mean interimpulse intervals (*SD; range) for the two directions while target force was maintained. These values are based on the averages of the 5-12 trials of the threshold task for each motor unit. On average, the interimpulse intervals were similar for the abduction (87 t 17 ms) and flexion (82 t 27 ms) directions (r* = 0.4 1, P < 0.05). For each motor unit, there was some variability in the interimpulse interval while force was maintained at the target level. As with the average values, this variability, as expressed by the coefficient of variation (mean t SD; range), was similar for the abduction (0.29 t 0.09; 0.15-0.49) and flexion (0.28 t 0.08; 0.18-0.4 1) directions. Although there were significant negative correlations between force difference (target force minus recruitment force) and mean interimpulse interval for both abduction (r = -0 43 P < 0 .05) and flexion (r = -0.55, P < 0.05), this association only accounted for 18 and 30%, respectively, of the variability in interimpulse interval. Taken together, the data indicate that when the biomechanical features of the threshold task remained consistent for the two directions, the behavior of individual motor units was largely unaffected by the task; that is, whether the muscle acted as a prime mover (abduction) or as a synergist (flexion).
UNITS
1353
1 2
3
5 6
7
I
2N
2.0 s I
2
I I i 1
3
i
Efect offatigue on motor-unit
behavior
CHANGES DURING THE FATIGUE TEST. The data shown in Fig. 3 outline both the range of threshold forces observed in the study and the effects of the fatigue test on the forces of recruitment and derecruitment. Although the study primarily focused on motor units that were recruited at low forces (10 and 7% of maximum in Fig. 3A), the fatigue-test data included some motor units that were recruited at higher forces (2 1 and 35% of maximum in Fig. 3B). The force of recruitment tended to decreaseslightly during the fatigue test for the low-force units and, although it did vary for the high-force units, this variation did not appear to be monotonic. In contrast, over the course of the fatigue-test, there was a marked increase in the derecruitment force of all units that were derecruited below the target force (Fig. 3). THRESHOLD
POST-FATIGUE TEST CHANGES DURING THRESHOLD TASK. Changes in motor-unit behavior during postfatigue
threshold trials were not surprising given the changesfound during the fatigue test. However, we did not anticipate the heterogeneity of post-fatigue test effects on motor unit behavior, which included the complete cessation of discharge, the recruitment of other units, and changesin the variability of di-scharge.The post-fatigue test database consisted of 27 tests of the threshold task on 15 motor units in the
6
7
FIG. 9. Threshold-task behavior of a motor unit that was minimally affected by the fatigue test. Data show the discharge pattern of a single motor unit during the performance of the threshold task before (top 7 trials) and after (bottom 7 trials) the fatigue test. Action potentials were plotted with a computer graphics package. Target force for the threshold task was 7% of maximum; the maximum force was 21 N. Trials were aligned (- - -) at the instant that the target force was attained. Left limit of each trial indicates the time when force began increasing from 0. Recruitment force was 3 + 1% of maximum both before and after the fatigue, whereas the derecruitment force was 6 f. 1% of maximum before the fatigue test and 7 * 1% of maximum after the test. For this motor unit, the recruitment and derecruitment forces during the threshold task were largely unaffected by the fatigue test.
abduction and flexion directions. For 10 of these tests, the motor unit exhibited the most extreme effect, cessation of discharge after the fatigue test, as shown in Fig. 8. In the remaining 17 tests, motor-unit behavior was similar to that depicted in Fig. 9. There were no significant differences in the threshold forces (5 t 3 vs. 7 t 3% of maximum, respectively) for the units that were derecruited after the fatigue test compared with those that remained active. For the unit shown in Fig. 8, the absolute force exerted
1354
R. M.
ENOKA,
G. A. ROBINSON,
by the proximal interphalangeal joint of the index finger during the threshold task was essentially the same before and after the fatigue test; the rate of force increase (mean t SD) was 1.9 t 0.3 versus 2.0 t 0.3 N/s (before vs. after), the target force was 4.7 t 0.3 versus 4.8 t 0.4 N, and the rate of force decrease was 2.2 t 0.9 versus 2.2 t 0.6 N/s. Accompanying this consistent performance of the threshold task was a markedly different contribution by the motor unit to the task. Before the fatigue test, the unit was recruited at a force of 3.7 t 0.9 N during the threshold task and derecruited at a force of 2.2 t 0.9 N; and the interimpulse interval was 81 t 29 ms during the 3.7 t 0.8 s that the target force was maintained. After the fatigue test, however, the motor unit did not contribute to the task until trial 7, when the muscle had experienced some recovery from the fatigue regimen. Although these absolute values for the target force and the rate of change in force for the threshold task were similar before and after the fatigue test, the target forces were actually a much greater proportion of the maximum after the fatigue test. Average maximum abduction force after the fatigue test was 67% of the initial value, whereas the final flexion force averaged 79% of the initial maximum. Furthermore, because these maxima were obtained after the threshold task when some recovery from the fatigue test would have occurred, the actual maximum capability of the muscle would have been even less during the performance of the post-fatigue test threshold task. In all instances involving the cessation of discharge, however, the motor unit was recruited again after - 15 min of recovery or when the target force was raised 3- 10% of maximum above the value used before the fatigue test. Furthermore, accompanying the motor units that ceased discharge during the post-fatigue test threshold task, there were other units that were silent before the fatigue test but were re-
AND
A. R. KOSSEV
cruited during the threshold task after the fatigue test. It is unlikely that these newly recruited units simply appeared in the record because of electrode movement, because they were evident in records containing other motor units whose action potentials had the same shape (as determined by spike-triggered averaging) before and after the fatigue test. In contrast to the marked effect of the fatigue test on the discharge of some motor units (Fig. S), there were other motor units that showed fewer changes (Fig. 9). For the example shown in Fig. 9, the performance met the necessary criteria, and the force exerted at the proximal interphalangeal joint of the index finger during the threshold task was essentially the same before and after the fatigue test; the rate of force increase was 0.6 t 0.2 versus 1.1 t 0.2 N/s (before vs. after), the target force was 1.5 t 0.2 versus 1.5 t 0.2 N, and the rate of force decrease was 0.4 t 0.2 versus 0.8 t 0.2 N/s. Furthermore, the average recruitment force was 0.6 t 0.2 N both before and after the fatigue test, whereas the derecruitment force was 1.3 t 0.2 N before and 1.5 t 0.2 N after the test. Close inspection of the data in Fig. 9, however, suggests that although the forces of recruitment and derecruitment were unaffected by the fatigue test, the discharge pattern seems to have been altered. This effect is shown more clearly in a joint-interval histogram (Fig. 10). Differences in the discharge pattern were quantified with measures of the distribution. The mean t SD of the interimpulse interval when force was at the target value was 75 t 37 ms (n = 324) before the fatigue test and 112 t 8 1 ms (n = 257) after the fatigue test. Based on a Kolmogorov-Smirnov goodness-of-fit test, both distributions (Fig. 10, A and B) were found to be non-Gaussian (P < 0.0001). However, the two distributions were also significantly different (P < 0.000 1; Kolmogorov-Smirnov
A 300 250 00
{
200
0
/ /
=z &
150
c T .’
100
/
/
/ /
/ //
//
/
/
/
/’
/
l /
/’
50
0
50
100
150
200
250
300
i Interval
I50
200
250
(ms>
FIG. 10. Joint-interval histograms based on the discharge of the single motor unit shown in Fig. 9. Intervals plotted in the histogram are those that occurred while the target force was maintained. A: joint-interval histogram for the 7 trials of the threshold task that were done before the fatigue test (i.e., the top 7 trials in Fig. 5). B: joint-interval histogram for the 7 trials of the threshold task that were done after the fatigue test (i.e., the bottom 7 trials in Fig. 5). Both histograms exhibit a non-Gaussian distribution. Greater dispersion in B indicates a decreased kurtosis in the distribution after the fatigue test, that is, less tendency for the discharge rate to cluster around a central value.
300
TASK
AND
FATIGUE
EFFECTS
ON
MOTOR
UNITS
1355
A
>
I
”
Before
I
0.6
0
After
I Before
I After
Threshold Task FIG. 1 1. Comparison of interimpulse intervals during the threshold task before and after the fatigue test. Data are limited to those units that were consistently active during the threshold task after the fatigue test and include both abduction (-) and flexion (- - -) trials. A: mean interimpulse intervals for 17 sets of trials ( 11 abduction and 6 flexion) before and after the fatigue test. Each set of trials consisted of 7-12 performances of the threshold task. Mean interimpulse interval increased significantly (P < 0.05) in 14 out of the 17 instances after the fatigue test. For 2 sets of trials (identified with + on the right side of the graph), the mean interimpulse interval decreased significantly after the fatigue test; the mean values went from 120 to 92 ms and 88 to 78 ms. For the other 2 sets of trials (identified with + on the L& side of the graph), the mean interimpulse interval was not significantly different before and after the fatigue test: 85 vs. 89 ms and 88 vs. 8 1 ms. B: coefficients of variation for the 17 sets of trials before and after the fatigue test. In 10 of these 17 sets of trials, there was a marked increase in the coefficient of variation after the fatigue test. For these units that remained consistently active during the threshold task after the fatigue test, the most common response was an increase in the mean interimpulse interval and an increase in the coefficient of variation.
2-sample test and x2 test) to each other, largely because of a greater kurtosis (3.76 vs. 0.48) in the pre-fatigue test distribution. The greater kurtosis is apparent in the joint-interval histogram by lessdispersion in the values (Fig. 10, A vs. B). Both distributions exhibited similar amounts of positive skew (1.6 1 and 1.02 for before and after, respectively). The typical behavior of units that were consistently active during the threshold task after the fatigue test was similar to that shown in Figs. 9 and 10 and is characterized in Fig. 11. The data compare 17 sets of trials before and after the fatigue test- 11 sets in the abduction direction and 6 in the flexion direction. Each set consisted of 5- 12 performances of the threshold task. In 14 of these 17 sets, the mean interimpulse interval increased significantly (t test, P < 0.05) after the fatigue test (Fig. 1IA). For two sets of trials, the mean interimpulse interval decreased significantly from 120 to 92 and 88 to 78 ms, respectively. For the other two setsof trials, the mean inter-impulse interval was not significantly different before and after the fatigue test (85 vs. 89 and 88 vs. 8 1 ms). Accompanying these changes in the mean interimpulse intervals were increases in the variability of discharge after the fatigue test (viz. Fig. 10). This is shown in Fig. 11B by the marked increase in the coefficient of variation after the fatigue test for 10 of the 17 sets of trials. Although the correlation between interimpulse interval and coefficient of variation was not significant before fatigue (r2 = O.OS), after fatigue a significant proportion of the variability in discharge was explained by changes in interimpulse interval (r2 = 0.38, P < 0.05). In contrast to these effects on discharge rate, the fatigue
test had a minimal effect on the forces of recruitment and derecruitment of the units that were active during the threshold task. The recruitment force of these units ranged from 2 to 12% of maximum, and the derecruitment force ranged from 1 to 14% of maximum. For only 1 of the 17 sets of trials shown in Fig. 11 was the mean recruitment force significantly different (5% increase) after the fatigue test. Furthermore, only for 6 of the 17 sets was the derecruitment force significantly different (4-6% increase) after the fatigue test. Thus, for units that remained active during postfatigue threshold trials, the data suggest that I) their mean firing rates decreased; 2) their firing patterns were more variable; and 3) their thresholds for recruitment and derecruitment were generally unchanged. Taken together, the fatigue data demonstrate that although the absolute forces of the threshold task remained the same before and after the fatigue test, the contributions of low-threshold motor units to the task were variable, including the derecruitment of some units, the recruitment of other units, an increased variability of discharge, and a decrease in the average discharge rate. There were, however, some units that had a similar average discharge rate before and after the fatigue test and other units that exhibited an increase in discharge rate. DISCUSSION
Pre-jdigue behavior These observations on motor-unit activity relate to previous studies in at least three respects: the control of activ-
1356
R. M. ENOKA,
G. A. ROBINSON,
AND A. R. KOSSEV
ity when force is exerted in different directions, the gradation of force, and discharge characteristics during steady state force. We will consider each issue separately.
that it is one of several muscles that contributes force during flexion and the only muscle that contributes to abduction.
A main finding was the similarity in behavior of individual motor units in first dorsal interosseusduring the threshold task when force was exerted either in abduction or in flexion. The data indicate that at these submaximal, relative (to maximum) forces, the control of motor-unit activity is independent of the task (i.e., prime mover vs. synergist) performed by the muscle. Based on the measurement of recruitment force, twitch tension, and the rank order of recruitment, Thomas et al. (1986) also concluded that the control of individual motor units in first dorsal interosseuswas essentially independent of the direction in which the muscle exerted a force. Desmedt and Godaux ( 1981) similarly found a significant correlation between twitch tension and recruitment force among the motor units of first dorsal interosseus for both the abduction and flexion directions. In both studies (Desmedt and Godaux 1981; Thomas et al. 1986), there was some variability in these relationships, but the general conclusion, based on recruitment force, twitch tension, and recruitment order, was that when first dorsal interosseus exerted a force in different directions, the control strategy for the motor units (i.e., the force and order of recruitment) was relatively similar. Our data add information on discharge rate and allow us to confirm the absence of a direction effect among the motor units of first dorsal interosseus when the muscle exerts low levels of force. The surprising aspect of these observations is the degree of coupling in motor-unit behavior, given the relative contribution of first dorsal interosseus to force in each direction. In the abduction direction, first dorsal interosseus is the only muscle to contribute to the force: it is the prime mover. In the flexion direction, however, first dorsal interosseusassumesthe role of a synergist as it assiststhe lumbricals and flexor digitorum (profundus and superficialis) with the flexion force. The contribution of first dorsal interosseus to the flexion force may be minimal with the finger in the test position (i.e., extension of the metacarpophalangeal and proximal interphalangeal joints). Based on preliminary data from another project, it seemsthat immobilization-induced atrophy of first dorsal interosseus causes a decline in the maximum voluntary abduction force but not the maximum flexion force (Robinson and Enoka, unpublished observation). The absenceof an effect on the maximum flexion force suggeststhat the contribution of first dorsal interosseus to this force is relatively minor. In a similar vein, Thomas et al. (1986) reported that the averaged twitch tension for each motor unit was considerably reduced (= 50%) when force was exerted in the flexion direction compared with twitch tension in the abduction direction. However, based on a seriesof nerve and muscle blocks with lidocaine, Ketchum et al. (1978) found that the intrinsic hand muscles (i.e., interossei and lumbricals) contributed 73% of the flexion force about the metacarpophalangeal joint of the index finger. Similar proportions have been reported by others (Landsmeer and Long 1965; Long et al. 1960). Although these observations suggest some uncertainty about the relative contribution of first dorsal interosseus to the flexion force, it is apparent
Milner-Brown et al. ( 1973) examined the interplay between recruitment and discharge modulation in the gradation of force by first dorsal interosseus and concluded that, at low forces, recruitment was the more dominant mechanism. In our study, motor-unit behavior during the gradation of force was characterized by the forces of recruitment and derecruitment and the temporal variation in interimpulse interval. Our observations on the interimpulse intervals during the threshold task indicate that, although variability was greater when force was being graded (Fig. 6), the variation was not systematic. This lack of a controlled variation in interimpulse interval suggests, as concluded by Milner-Brown et al. (1973) that motor-unit recruitment was the more dominant mechanism for the gradation of force at these low forces. Another feature of force gradation that has received attention has been the relative contribution of a motor unit to the increase and decreasein force; that is, the magnitude of the recruitment force relative to the derecruitment force. Several investigators have reported that the force at which a motor unit is derecruited is usually greater than the force at which the unit is recruited. This asymmetry has been reported previously for motor units in first dorsal interosseus (Freund et al. 1975), supinator, and brachialis (Denier van der Gon et al. 1985), but curiously the derecruitment force was generally lower for units located centrally and medially in biceps brachii (Denier van der Con et al. 1985). Our data on first dorsal interosseus indicated that the recruitment and derecruitment forces were about the same for the abduction direction but that the recruitment force was greater for the flexion direction (see also Desmedt and Godaux 198 1; Thomas et al. 1986).
DIRECTIONEFFECTS.
GRADATIONOFFORCE.
DISCHARGE CHARACTERISTICS. In addition to the variation in interimpulse interval associated with the gradation of force, the results of this study provided information on the discharge of motor units during constant, low levels of force. The average discharge rates were 11.5 Hz in abduction and 12.2 Hz in flexion, and these were associatedwith average target forces of 9.9 and 14.5% of maximum for abduction and flexion, respectively. These values are consistent with other reports on discharge rate in the literature at these force levels: adductor pollicis, 6- 16 Hz (Kukulka and Clamann 1981); biceps brachii, 5-22 Hz (Denier van der Gon et al. 1985) and 7-25 Hz (Gydikov and Kosarov 1974); extensor digitorum communis, 8-24 Hz (Monster and Chan 1977); first dorsal interosseus, 6-20 Hz (Freund et al. 1975); flexor pollicis brevis, 6- 15 Hz (Ivanova et al. 1986); rectus femoris, 5-2 1 Hz (Person and Kudina 1972); and tibialis anterior, 7- 16 Hz (Andreassen and Rosenfalck 1980). The average discharge rates were accompanied by some variability that was characterized by a coefficient of variation of 0.29 (0.15-0.49) in this study and a range of 0.12-0.25 in another study on first dorsal interosseus (Freund et al. 1972). To further characterize the variability, we examined the distributions of interimpulse intervals and found them all to be non-Gaussian because of increased kurtosis and skew. Gatev et al. (1986) similarly
TASK
AND
FATIGUE
EFFECTS
found a non-Gaussian distribution, but this was for a group of high-threshold motor units. Ivanova et al. (1986) observed two groups of low-threshold motor units that were distinguished on the basis of the absolute value of the interimpulse interval (mean values that were greater than or less than 100 ms) and the distributions of the interimpulse intervals (non-Gaussian and Gaussian respectively; see also Person and Kudina 1972). No such distinction was found among our data. Although Freund et al. (1975) suggested that their distributions were approximately normal, their histograms (see their Fig. 6) appeared to have a greater amount of kurtosis than normal and to match our results (Fig. 7). Consequently, our observation of a non-Gaussian distribution of interimpulse intervals during the period of constant force seems to be a common observation when appropriate statistical procedures are performed. Although the non-Gaussian distribution was because of an increase in both kurtosis and skew, it was dominated by the kurtosis effect. The increased kurtosis meant that the interimpulse intervals tended to be more clustered around a central value than would be expected with a normal distribution Given the rather stereotyped prefatigue behavior of the present sample of low-threshold motor units, it was expected that their behavior after the fatigue test would be similarly homogeneous because these units are reported to be fatigue resistant (Stephens and Usherwood 1977). These expectations were addressed by examining two issues, the behavior of single motor units during a fatigue test and the effect of the test on the contribution of the units to the threshold task. For the first issue, we assessed the effect of the fatigue test on two functional indexes of motor-unit excitability, the forces of recruitment and derecruitment. Of the two parameters, the force of derecruitment exhibited the most consistent and marked fatigue-related ef5ect. For all motor units that were derecruited at a force less than the target value (50% of maximum) during the fatigue test, the derecruitment force increased over the course of the test. This observation is consistent with evidence from motor-unit studies in animals (Gordon et al., In press) and whole-muscle studies in humans (Cooper et al. 1988; Dawson et al. 1980) that have recorded a progressive decline in the rate of relaxation during a fatigue regimen. Because a decline in the rate of relaxation indicates an increase in the time course of relaxation, a unit would have to be derecruited earlier for its mechanical effect to be dissipated within the same time frame. Apparently, low-threshold motor units are “informed” of this necessity, as derecruitment forces increased during the fatigue test, The second issue was addressed by comparing the behavior of individual motor units during the threshold task as it was performed before and after the fatigue test. The general observation was that the behavior of most motor units during the threshold task was affected by the fatigue test. These effects were variable, including the derecruitment of previously active units, the recruitment of additional units, and an increased variability of discharge. The post-fatigue test cessation of discharge by some units represented a substantial effect on recruitment order because these units failed to be recruited, even though the maximum capability of the muscle was significantly reduced after the fatigue
ON
MOTOR
UNITS
1357
test. Furthermore, there were additional motor units that were recruited after the fatigue test to complement the absence of activation of other motor units. These observations lead us to conclude that the fatigue test caused substantial changes in recruitment order and that this effect might be explained by two possibilities. First, among the low-threshold motor units of first dorsal interosseus, there may be some flexibility in the recruitment order that is influenced by the activation history of the motoneuron pool, including feedback-related effects from the periphery (cf. Bigland-Ritchie et al. 1986; Woods et al. 1987). Second, despite the subjects’ best efforts, the performance of the threshold task may not have been exactly the same before and after the fatigue test, and these differences may have been sufficient to cause some alterations in the reunits. cr uitm ent order among the low-threshold This second possibility, di fferences in the perfo rmance of the threshold task, might have been beta use of an insufficient resolution in the mechani cal system orani nability to determine which mu scles contributed to the force exerted by the index nnge r. It seems unlikely th at the 1ack o f resolution prevented us from detecting d ifferences in performan ce of the threshold task because the characteristics of the pre- and post-fatigue test performances of the threshold task were no different for the units that were not recruited than thevw were for the units that were recruited (e.g., Figs. 8 and 9). Similarly, considerable care was taken to constrain the task to the test muscle. Although we did not monitor the activity of other m uscles in the h and, one pe rformance criterion was to keep flexio n force zero when force was exerted in the abduct i on direction and vice versa. However, th is did n ot seem to be a confoundi ng factor because, whereas first dorsal interosseus is the only muscle that contributes to the abduction force, it is one of several muscles that contributes to the flexion force, yet the same effects were observed when the threshold task was performed in both the abduction and flexion directions (Fig. 11). Furthermore, Garnett and Stephens (198 1) reported that coactivation of antagonist muscles was minimal under similar conditions. For these reasons we tend to di scount the second possibi lity and favor the nterpretation that the variation in motor units recruited during the post-fatigue test performance of the threshold task reflects some degree of history-dependent flexibility in recruitment order among the low-threshold motor units of first dorsal interosseus. In the extent terms of relative forces (percent of maximum), order seems to be much of this variability in recruitment greater than that found with pair-wise compa risons of recruitment order during nonfatiguing conditions (Desmedt and Godaux 198 1; Thomas et al. 1986; Thomas et al. 1978). In addition to some variation in the motor units that were recruited during the threshold task after the fatigue test, the other most profound effect of the fatigue test was on the average value and the variability of the interimpulse interval. Most, but not all, motor units exhibited a decrease in the discharge rate and an increase in the variability of discharge. The post-fatigue test decline in motor-unit discharge during the threshold task is consistent with the fatigue-related decline reported by others (Bigland-Ritchie et al. 1983a; Grimby et al. 198 1; Gydikov and Kosarov 1974; Ivanova et al. 1986). Although the distributions of interim-
1358
R. M.
ENOKA,
G. A. ROBINSON,
pulse intervals were non-Gaussian both before and after the fatigue test, they were also significantly different from one another. Both distributions had a positive skew, but only the pre-fatigue test distribution had an increased kurtosis; that is, the post-fatigue test distribution was characterized by an increased variability in the interimpulse interval. Two features of the increased variability of discharge are intriguing: the mechanism underlying the increased variability and the reason for the increase. Based on the concepts of “muscle wisdom” (Cooper et al. 1988; Garland et al. 1988; Marsden et al. 1969) and force optimization (Zajac and Young 1980), we might explain the increased variability as an optimization of motor-unit discharge to the changing mechanical state of the muscle. However, it is unclear from these data whether the increased variability was a constructive adaptation (i.e., optimization) or simply an inconsequential by-product of the change in input to the motoneuron pool as a result of the fatigue test. Certainly some of the increased variability in discharge was because of a decrease in mean discharge rate, presumably associated with some units approaching their minimum repetitive firing threshold. Whatever the mechanism, it is probably responsible for changes in motor-unit discharge and for the recruitment changes observed with some motor units. In conclusion, this study extends on other reports in the literature and confirms that the responses of low-threshold motor units in first dorsal interosseus are similar for the two directions of force production. Low levels of force exerted by the index finger at the proximal interphalangeal joint appear to be coded in terms of net muscle activity rather than the direction-specific control of individual muscles. In contrast, fatigue-induced changes in motorunit behavior included almost every possible permutation. It was evident that these units did not respond as a homogeneous population to the demands of the fatigue test. Although it is possible, under more controlled experimental conditions, to identify groups of motor units that exhibit similar fatigue responses (e-g., Burke et al. 1973; McDonagh et al. 1980; Stephens and Usher-wood 1977), the lowthreshold and, presumably, fatigue-resistant motor units that were examined in this study exhibited a heterogeneous response to the fatigue test. This heterogeneity underscores the wide-ranging effects produced by the short-term adaptive processes associated with fatigue. We thank P. Worden and A. Tyler for technical assistance, Dr. John Cropper for statistical assistance, and Dr. Douglas G. Stuart for financial, moral, and editorial support. The project was supported by grants from National Institutes of Health (HL-07249 to the Department of Physiology, NS-07309 to the Motor Control Group, and NS-20544 to Drs. Stuart and Enoka) and from National Science Foundation (INT-8520863 to Dr. Stuart). Present address of A. R. Kossev: Central Laboratory for Biophysics, Bulgarian Academy of Sciences, Acad. G. Bontchev bl. 2 1, Sofia 1113, Bulgaria. Address for reprint requests: R. M. Enoka, Gittings Bldg., [Jniversity of Arizona, Tucson, AZ 8572 1. Received
17 February
1989; accepted
in final
form
3 1 July
1989.
REFERENCES AN, K. N., CHAO, E. Y., COONEY, Normative model of human hand
mech. 12: 775-788, 1979.
W. P. 111, AND for biomechanical
LINSCHEID, analysis.
R. L. J.
Bio-
AND
A. R. KOSSEV
AN, K. A., UEBA, Y., CHAO, E. Y., COONEY, W. P., AND LINSCHEID, R. L. Tendon excursion and moment arm of index finger muscles” J. Biomech. 16: 419-425, 1983. ANDREASSEN, S. AND ROSENFALCK, A. Regulation of the firing pattern of single motor units. J. Neural. Neurosurg. Psychiatry 43: 897-906, 1980. BIGL,AND-RITCHIE, B. R., DAWSON, N. J., JOHANSS~N, R. S., AND LIPPoL,D, 0. C. J. Reflex origin for the slowing of nrotoneurone firing rates in fatigue of human voluntary contractions. J. Physiol. Land. 379: 451-459, 1986. BIGLAND-RITCHIE, B., JOHANSSON, R., LIPPOL~D, 0. C. J., SMITH, S., AND WOODS, J. J. Changes in motoneurone firing rates during sustained maximal voluntary contractions J. Physiol. Lond. 340: 335-346, 1983a. BIGL,AND-RITCHIE, B., JOHANSSON, R., L,IPPOL,D, 0. C. J., AND Woons, J. J. Contractile speed and EMG changes during fatigue of sustained maximal voluntary contractions. J. Neurophysiol. 50: 3 13-324, 1983’0. BRAND, P. W. Clinical Mechanics o_f’the Hand. St. Louis, MO: Mosby, 1985. BRAND, P. W., BEACH, R. B., AND THOMPSON, I>. E. Relative tension and potential excursion of muscles in the forearm and hand. J. Hand Surg. 6: 209-219, 1981. BODINGEN, J. H. AND FRE~ND, H.-J. The relationship between the rate of rise of isometric tension and motor unit recruitment in a human forearm muscle. Pfluegers Arch. 362: 6 l-67, 1976. BURKE, R. E. Motor units: anatomy, physiology, and functional organization. In: Handbook oJ‘PhysiologyU The Nervous System. Motor Control. Bethesda, MD: Am. Physiol. Sot., 198 1, sect. 1, vol. 11, pt. 1, chapt. 10, p. 345-422. BURKE, R. E. Synaptic efficacy and the control of neuronal input-output relations. Trends Neurosci. 10: 42-45, 1987. BURKE, R. E., LEVINE, D. N., TSAIRIS, P., AND ZAJAC, F. E. III. Physiological types and histochemical profiles in motor units of the cat gastrocnemius. J. Physiol. L,ond. 234: 723-748, 1973. CL,AMANN, H. P. Statistical analysis of motor unit firing patterns in a human skeletal muscle. Biophys. J. 9: 1233- 125 1, 1969. COOPER, R. G., EDWARDS, R. H. T*, GIBSON, H., AND S-I’OKES, M. J. Human muscle fatigue: frequency dependence of excitation and force generation. J. Physiol. Lond. 397: 585-599, 1988. DATTA, A. K. AND STEPHENS, J. A. The effects of digital nerve stimulation on the firing of motor units in human first dorsal interosseus muscle. J. Physiol. Lond. 3 18: 50 l-5 10, 198 1. DAWSON, M. J., GADIAN, D. G., AND WILKIE, D. R. Mechanical relaxation rate and metabolism studied in fatiguing muscle by phosphorus nuclear magnetic resonance. J. Physiol. Land. 299: 465-484, 1980. DENIER VAN DER GON, J. J., TER HAAR ROMENY, B. M., AND VAN ZI_IYL,EN, E. J. Behaviour of motor units of human arm muscles: diff‘erences between slow isometric contraction and relaxation. J. Physiol. Land. 359: 107-l 18, 1985. DENNY-BROWN, D. Interpretation of the electromyogram. Arch. Neural. Psychiatry 61: 99-128, 1949. DENNY-BROWN, D. AND PENNYBA~KER, J. B. Fibrillation and fasciculation in voluntary muscle. Brain 61: 31 l-334, 1938. DESMED’T, J. E. AND GODAUX, E. Ballistic contractions in fast or slow human muscles: discharge patterns of single motor units. J. Physiol. L,ond. 285: 185-196, 1978. DESMEDT, J. E. ANr) GOr>AUx, E. Spinal motoneuron recruitment in man: rank deordering with direction but not with speed of voluntary movement. Science Wash. DC 2 14: 933-936, 198 1. ENOKA, R. M., ROBINSON, G. A., AND KOSSEV, A. R. Absence of direction-specific rate coding among low threshold motor units of first dorsal interosseus. Sot. Neurosci. Abstr. 13: 873, 1987. ENOKA, R. M., ROBINSON, G. A., AND KOSSEV, A. R. A stable, selective electrode for recording single motor-unit potentials in humans. E.xp. Neural. 99: 761-764, 1988. EYLER, D. L. AND MARKEE, J. E. The anatomy and function of the intrinsic musculature of the fingers. J. Bone Joint Surg. 36-A: l-9, 1954. FEINSTEIN, B., LINDEGARD, B., NYMAN, E., AND WOHLFARI-, G. Morphologic studies of motor units in normal human muscles. Acta Anat. 23: 127-142, 1955. FREUND, H.-J., BUDINGEN, H. J., AND DIETZ, V. Activity of single motor units from human forearm muscles during voluntary isometric contractions. J. Neurophysiol. 38: 933-946, 1975. FREIJND, H.-J., WITA, C. W., ANL> SPRUNG, C. Discharge properties and functional differentiation of single motor units in man. In: Neurophysi-
TASK
AND
FATIGUE
EFFECTS
ology Studied in Man, edited by G. Somjen.
Amsterdam: Excerpta Med. 1972, p. 305-313. GARI_AND, S. J., GARNER, S. H., ANII) M~C~MAS, A. J. Relationship between numbers and frequencies of stimuli in human muscle fatigue. J. Appl. Physiol. 65: 89-93, 1988. GARNETT, R. AND STEPHENS, J. A. Changes in the recruitment threshold of motor units produced by cutaneous stimulation in man. J. Physiol. Lond. 3 11: 463-473, 198 1. GATEV, P., IVANOVA, T., AND GANTCHEV, G. N. Changes in the firing pattern of high-threshold motor units due to fatigue. Electromyogr. Clin. Neuroph.ysiol. 26: 83-93, 1986. GORDON, D., ENOKA, R. M., AND STUART, D. G. Force development and relaxation in single motor units of adult cats during a standard fatigue test. J. Physiol. Lond. In press. GRIMBY, L., HANNERZ, J., AND HEDMAN, B. The fatigue and voluntary discharge properties of single motor units in man. J. Physiol. L,ond. 3 16: 545-554, 1981. GUSTAFSSON, B. AND PINI’ER, M. J. On factors determining orderly recruitment of motor units: a role for intrinsic membrane properties. Trends Neurosci. 8: 43 l-433, 1985. GYDIKOV, A. AND KOSAROV, D. Some features of different motor units in human biceps brachii. Pfluegers Arch. 347: 75-88, 1974. GYDIKOV, A., KOSSEV, A., TRAYANOVA, N., AND RADICHEVA, N. Selective recording of motor unit potentials. Electromyogr. Clin. Neurophysiol. 26: 273-28 1, 1986. HENNEMAN, E. Relation between size of neurons and their susceptibility to discharge. Science Wash. DC 126: 1345-l 347, 1957. HENNEMAN, E., CLAMANN, H. P., GILLIES, J. D., AND SKINNER, R. D. Rank order of motoneurons within a pool: law of combination. J. Neurophysiol. 37: 1338- 1349, 1974. HENNEMAN, E. AND MENDELL, L. M. Functional organization of motoneuron pool and its inputs. In: Handbook of Physiology. The Nervous System. Motor Control. Bethesda, MD: Am. Physiol. Sot., 198 1, sect. 1, vol. 1 1, pt. 1, chapt. 11, p. 423-507. IVANOVA, T., GANTCHEV, G. N., AND POPIVANOV, D. Firing rate of low-threshold motor units after maximal voluntary contraction. Elec-
tromyogr. Clin. Neurophysiol. 26: 69-78, 1986. KANDA, K., BURKE, R. E., AND WALMESLY, B. Dift‘erential control of fast and slow twitch motor units in the decerebrate cat. Exp. Brain Rex 29: 57-74, 1977. KATO, M., MIIRAKAMI, S., TAKAHASHI, K., AND HIRAYAMA, H. Motor unit activities during maintained voluntary muscle contraction at constant levels in man. Neurosci. Lett. 25: 149- 154, 198 1. KETCHUM, L. D., THOMPSON, D., POC’OCK, G., AND WALLINGFORD, D. A clinical study of forces generated by the intrinsic muscles of the index finger and the extrinsic flexor and extensor muscles of the hand. J. Hand Surg. 3: 571-578, 1978. KOSSEV, A. R., ROBINSON, G. A., AND ENOKA, R. M. Fatigue-induced changes in the threshold forces of recruitment and derecruitment for low threshold motor units of first dorsal interosseus. Sot. Neurosci. Abstr. 13: 873, 1987. KUKULKA, C. G. AND CLAMANN, H. P. Comparison of the recruitment and discharge properties of motor units in human brachial biceps and adductor pollicis during isometric contractions. Brain Res. 2 19: 45-55, 1981. LANIXMEER, J. M. F. Anatomical and functional investigations on the articulation of the human fingers. Acta Anat. 24 Suppl.: 5-69, 1955. LANDSMEER, J. M. F. AND LONG, C. The mechanism of finger control, based on electromyograms and location analysis” Acta Anat. 60: 330-347, 1965. LONG, C., BROWN, M. E., ANI> WEISS, G. An electromyographic study of the extrinsic-intrinsic kinesiology of the hand: preliminary report. Arch. Phys. Med. Rehabil. 41: 175-18 1, 1960. LUSCHER, H.-R., RUENZEL,, P., AND HENNEMAN, E. How size of motoneurones determines their susceptibility to discharge. Nature Land. 282: 859-861, 1979. MARSDEN, C. D., MEADOWS, J. C., AND MERTON, P. A. Muscular wisdom (Abstract). J. Physiol. Lond. 200: 15P, 1969.
ON
MOTOR
UNITS
1359
MARSDEN, C. D., MEADOWS, J. C., AND MERJ‘C)N, P. A. “Muscular wisdom” that minimizes fatigue during prolonged eff’ort in man: peak rates of motoneuron discharge and slowing of discharge during fatigue. In: Motor Control Mechanisms in Health and Disease, edited by J. E. Desmedt. New York: Raven, 1983, p. 169-2 11. M~DONAGH, J. C., BINDER, M. D., REINKING, R. M., AND STUART, D. G. Tetrapartite classification of motor units of cat tibilias posterior. J. Neurophysiol. 44: 696-7 12, 1980. MILNER-BROWN, H. S., STEIN, R. B., AND YEMM, R. Changes in firing rate of human motor units during linearly changing voluntary contractions. J. Physiol. Land. 230: 37 l-390, 1973. MONSTER, A. W. AND CHAN, H. Isometric force production by motor units of extensor digitorum communis muscle in man. J. Neurophysiol. 40: 1432-1443, 1977. PALMER, S. S. AND FETE, E. E. Discharge properties of primate forearm motor units during isometric muscle activity. J. Neurophysiol. 54: 1178-1193, 1985. PERSON, R. S. Rhythmic activity of a group of human motoneurones during voluntary contraction of a muscle. Electroencephalogr. Clin. Neuroph-ysiol. 36: 585-595, 1974. PERSON, R. S. AND KUDINA, L. P. Discharge frequency and discharge pattern of human motor units during voluntary contraction of muscle.
Electroencephalogr. Clin. Neurophysiol. 32: 47 I-483, 1972. RODIECK, R. W., KIANG, N. Y.-S., AND GERSTEIN, G. L. Some quantitative methods for the study of spontaneous activity of single neurons. Biophys. .I. 2: 35 l-368, 1962. SEYFFARTH, H. The behaviour of motor-units in voluntary contraction.
Avhandlinger utgitt av det norske videnskap-akademi i Oslo. I: Matemat&k-Naturvidenskupelig Klasse. 4: l-63, 1940. SMITI~, R. J. Balance and kinetics of the fingers under normal and pathological conditions. Clin. Orthop. Relat. Res. 104: 92- 1 1 1, 1974. SMITH, J. L., BE-~~s: B., EDGF,R~;~N, V. R., AND ZERNICKE, R. F. Rapid ankle extension during paw shakes: selective recruitment of fast ankle extensors. J. Neuroph”vsiol. 43: 6 12-620, 1980. STEPHENS, J. A. AND USHERWOOD, T. P. The mechanical properties of human motor units with special reference to their fatiguability and recruitment threshold. Brain Rex 125: 9 l-97, 1977. STUART’, D. G. ANr> ENOKA, R. M. Motoneurons, motor units and the size principle. In: The Clinical Neurosciences, edited by R. N. Rosenberg. Section 5--Neurobiolog~y, edited by W. D. Willis. New York: Churchill Livingstone, 1983, p. 47 l-5 18. TER HAAR ROMENY, B. M., DENIER VAN DER GON, J. J., AND GIELEN, C. C. A. M. Changes in recruitment order of motor units in the human biceps muscle. Exp. Neurol. 78: 360-368, 1982. TER HAAR ROMFINY, B. M., DENIER VAN DER GON, J. J., AND GIELEN, C. C. A. M. Relation between location of a motor unit in the human biceps brachii and its critical firing levels for different tasks. Exp. Neurol. 85: 63 l-650, 1984. THOMAS, C. K., Ross, B. H., ANL> STEIN, R. B. Motor-unit recruitment in human first dorsal interosseous muscle for static contractions in three different directions. J. Neurophysiol. 5 5: 10 17- 1029, 1986. THOMAS, J. S., SCHMID-r, E. M., ANr> HAMBRECH-I’, F. T. Facility of motor unit control during tasks defined directly in terms of unit behaviors. Exp. Neural. 59: 384-395, 1978. VALENTIN, P. The interossei and the lumbricals. In: The Hund, edited by R. Tubiana. Philadelphia, PA: Saunders, 198 1, vol. 1, p. 244-254. WOODS, J. J., FURNISH, F., ANT> BIGLAND-RIJCHKE, B. Evidence for a fatigue-induced reflex inhibition of motoneuron firing rates. J. Neurophysiol. 58: 125-l 37, 1987. YOUNG, J. L. AND MAYER, R. F. Physiological properties and classification of single motor units activated by intramuscular microstimulation in first dorsal interosseus muscle in man. In: Motor Unit Types, Recruitment and Plasticity in Health and Disease, edited by J. E. Desmedt. Basel: Karger, 198 1, p. 17-25, ZAJAC, F. E. AND YOUNG, J. L. Properties of stimulus trains producing maximum tension-time area per pulse from single motor units in medial gastrocnemius muscle of the cat. J. Neurophysiol. 43: 1206-l 220, 1980.
