Statistical Analysis of Motor Unit Firing Patterns in a Human Skeletal Muscle

A statistical analysis of the firing pattern of single motor units in the human brachial biceps muscle is presented. Single motor unit spike trains are recorded and analyzed. The statistical treatment of these spike trains is as stochastic point processes, the theory of which is briefly discussed. Evidence is presented that motor unit spike trains may be modelled by a renewal process with an underlying gaussian probability density. Statistical independence of successive interspike intervals is shown using scatter diagrams; the hypothesis of a gaussian distribution is accepted at the 99th percentile confidence limit, chi-square test, in 90% of the units tested. A functional relationship between the mean and standard deviation is shown and discussed; its implications in obtaining sample size are presented in an appendix.The results of higher order analysis in the form of autocorrelograms and grouped interval histograms are presented. Grouped interval histograms are discussed in the context of motor unit data, and used to confirm the hypothesis that a stable probability density function does not represent a good model of the data at this level of analysis.     

Motor unit firing rates during isometric voluntary contractions performed at different muscle lengths

Firing rates of motor units and surface EMG were measured from the triceps brachii muscles of able-bodied subjects during brief submaximal and maximal isometric voluntary contractions made at 5 elbow joint angles that covered the entire physiological range of muscle lengths. Muscle activation at the longest, midlength, and shortest muscle lengths, measured by twitch occlusion, averaged 98%, 97%, and 93% respectively, with each subject able to achieve complete activation during some contractions. As expected, the strongest contractions were recorded at 90 degrees of elbow flexion. Mean motor unit firing rates and surface EMG increased with contraction intensity at each muscle length. For any given absolute contraction intensity, motor unit firing rates varied when muscle length was changed. However, mean motor unit firing rates were independent of muscle length when contractions were compared with the intensity of the maximal voluntary contraction (MVC) achieved at each joint angle.     

Simulations of the alpha motoneuron pool electromyogram reflex at different preactivation levels in man

The alpha motoneuron pool and the surface electromyogram (EMG) of the human soleus muscle are modelled, respectively, by an alpha motoneuron pool model generating the firing patterns in the motor units of e muscle and by a muscle model using these discharge patterns to simulate the surface EMG. In the alpha motoneuron pool model, we use a population of motoneurons in which cellular properties like cell size and membrane conductance are distributed according to experimentally observed data. By calculating the contribution from each motor unit, the muscle model predicts the EMG. Wave forms of the motor unit action potentials in the surface EMG are obtained from experimental data. Using the model, we are able to give a quantitative prediction of the motoneuron pool activity and the reflex EMG output at different preactivation levels. The simulated data are consistent with experimentally obtained results in healthy humans. During static isometric muscle preactivations, the simulations show that the reflex strength is highly dependent on the intrinsic threshold properties of the alpha motoneuron pool. Received: 27 April 1993/Accepted in revised form: 8 September 1993     

Ia-afferent input to motoneurons during shortening and lengthening muscle contractions in humans.

The central nervous system employs different strategies to execute specific motor tasks. Because afferent feedback during shortening and lengthening muscle contractions differs, the neural strategy underlying these tasks may be quite distinct. Cortical drive may be adjusted or afferent input regulated. The exact mechanisms are not clear. Here, we examine the control of synaptic transmission across the Ia synapse during shortening and lengthening muscle contractions. Subjects were instructed to maintain isolated activity in a single tibialis anterior (TA) motor unit while muscle length was varied from flexion to extension and back. At a fixed interval after a firing of the active motor unit, a single electrical stimulus was applied to the common peroneal nerve to activate Ia afferents from the TA muscle. We investigated the stimulus-induced change in firing probability of 19 individual low-threshold TA motor units during shortening and lengthening contractions. Any change in firing probability depends on both pre- and postsynaptic mechanisms. In this experiment, motoneuron firing rate was similar during both contraction types. There was no difference in the firing probability between shortening and lengthening contractions (0.23 +/- 0.03 and 0.20 +/- 0.02, respectively). We suggest that there is no contraction type-specific control of Ia input to the motoneurons during shortening and lengthening muscle contractions. Cortical adjustments may have occurred.     

Effect of the tendon reflex on the silent period of motor units in man

The behavior of motor units functioning under different conditions was investigated during the patellar reflex. The reflex was elicited during regular firing of the motor units in connection with weak sustained voluntary effort without postural change. Under these conditions the firing rate of the motor units serves as a statistical characteristic of threshold: during the maintenance of an assigned level of contraction the mean firing rate of the low-threshold motor units was higher. The greater the mean spontaneous interspike interval of the motor units, the longer the duration of their silent period after reflex muscular contraction. The duration of the silent period of single motor units in many cases exceeded the longest duration of the aggregated silent period on the electromyogram. The instant frequency (the difference between the reciprocals of the mean interspike interval and silent period) was used as a measure of inhibitory action on the motoneuron. Positive correlation was observed between the change in the instant frequency and the spontaneous firing rate of the motor units. Within the population examined, those motoneurons whose frequency was higher (low-threshold) were more inhibited. The combination of spinal factors evoking inhibition of the motoneurons after the tendon reflex and the excitatory supraspinal influences causing recruiting of the motoneurons during voluntary contraction proved more effective under the conditions investigated for the same motoneurons.     

Recurrent inhibition of human firing motoneurons (experimental and modeling study)

Recurrent inhibition between tonically activated single human motoneurons was studied experimentally and by means of a computer simulation. Motor unit activity was recorded during weak isometric constant-force muscle contractions of brachial biceps (BB) and soleus (SOL) muscles. Three techniques (cross correlogram, frequencygram, and interspike interval analysis) were used to gauge the relations between single motor unit potential trains. Pure inhibition was detected in 5.6% of 54 BB motoneuron pairs and in 5.2% of 43 SOL motoneuron pairs. In 27.8% (BB) and 23.7% (SOL) presumed inhibition symptoms were accompanied by a synchrony peak; 37% (BB) and 48.8% (SOL) exhibited synchrony alone. The demonstrated inhibition was very weak, at the edge of detectability. Computer simulations were based on the threshold-crossing model of a tonically firing motoneuron. The model included synaptic noise as well as threshold and postsynaptic potential (PSP) amplitude change within interspike interval. Inhibition efficiency of the model neurons increased with IPSP amplitude and duration, and with increasing source firing rate. The efficiency depended on target motoneuron interspike interval in a manner similar to standard deviation of ISI. The minimum detectable amplitude estimated in the simulations was about 50V, which, compared with the experimental results, suggests that amplitudes of detectable recurrent IPSPs in human motoneurons during weak muscle contractions do not exceed this magnitude. Since recurrent inhibition is known to be progressively depressed with an increase in the force of voluntary contraction, it is concluded that the recurrent inhibition hardly plays any important role in the isometric muscle contractions of constant force.     

An EMG study of functional cortico-motoneuronal connections in humans.

We set out to decompose the EMG signal into its constituent motor unit action potential components to track motor unit firing rates with a high degree of accuracy and extract their average firing rate. We were able to show that this average firing rate tracks the subject's force trajectory from beginning to end. We propose that this average firing rate is a volitional control signal pointing to the existence of a 'volitional unit'. This volitional unit has to do with the projection of a group of functionally related cortico-motoneurons on a group of spinal motoneurons in the motoneuronal pool of a muscle. Our study of motor unit firing patterns during their steady state showed that spinal motoneurons respond to a descending central input in a Gaussian manner. We have further shown that the central drive itself, as represented by the average firing rate of the active motor units, also displays a Gaussian firing behavior. We have also described the existence of a 'translation factor', highly correlated to the motor unit size, which is unique to each spinal motoneuron and determines the motoneuronal response, and its resulting firing rate, to the descending inputs. As for force generation, we have shown that expressing the twitch force of a motor unit in a dynamic fashion using the 'electrotwitch' concept of firing rate x macro area, approximates motor unit force output better and accounts for firing rate related force changes more effectively than force estimates based on the mechanical twitch.     

Detection and analysis of recurrent inhibition of firing motoneurons in man

During regular firing of "small" motor units, activated during weak voluntary contraction of the human soleus muscle, thick efferent fibers of n. tibialis were stimulated (a small M response was evoked, in which the small units did not participate). Peristimulus histograms of potentials of single motor units were constructed and the effect of stimulation on interspike interval duration was analyzed. The firing rate of the motor units was 4.5–7.6 spikes/sec. Stimulation of the nerve led to a sharp decrease in probability of their discharge or even complete temporary cessation of firing, i.e., it had a well marked inhibitory effect (lasting 10–20 msec). The latent period of inhibition (35–40 msec) was only a little longer than the latent period of the monosynaptic reflex of the soleus muscle. The effect of an inhibitory volley on duration of the interspike interval of the motor units depended on the time when the volley arrived during the interval. Lengthening of the interval was observed only if the inhibitory volley arrived in the second half or at the end of the interval. It is concluded that inhibition of firing of small motor units is due to Renshaw cells, activated on stimulation of axons of large motoneurons. The efficiency of a short (compared with the duration of the interspike interval) inhibitory volley reaching a motoneuron firing at low frequency characteristic of its adequate activation, is discussed.Institute for Problems of Information Transmission, Academy of Sciences of the USSR, Moscow. Translated from Neirofiziologiya, Vol. 16, No. 1, pp. 88–96, January–February, 1984.     

Effects of evoked and spontaneous motoneuronal firing on synapse competition and elimination in skeletal muscle

Synapse elimination is a general feature of the development of neural connections, including the connections of motoneurons to skeletal muscle fibers. Our work addressed two questions: (1) how the action potentials generated in the set of motoneurons innervating an individual muscle (i.e., in a motor pool) are correlated in time during development in vivo; (2) what influence different firing patterns exert on the processes of polyneuronal innervation and synapse elimination which characterize the establishment of muscle innervation. We recorded the spontaneous electromyographic activity of the tibialis anterior and soleus muscles of late embryonic and neonatal rats, identifying the firing of at least two single motor unit signals in each record. We found that a striking switch occurs a few days after birth from a highly synchronous type of firing to an asynchronous one, the first thus characterizing embryonic while the second one adult motoneurons. We also investigated the effects of an evoked synchronous type of discharge on neuromuscular synapse formation, measuring polyneuronal innervation and synapse elimination. This was done in an adult in vivo model of de novo synapse formation, while a chronic TTX nerve conduction block, placed centrally with respect to the stimulating electrodes, eliminated the natural activity of motoneurons. We found that the imposed synchronous activity greatly inhibits synapse elimination, causing polyneuronal innervation to persist. We conclude that the early synchronous firing, favors the establishment of polyneuronal innervation while the subsequent switch to an asynchronous one promotes synapse elimination.     

Work organization of a group of human motoneurons during voluntary muscular contraction

Needle electrodes were used to record action potentials of motor units of the rectus femoris muscle during isometric contraction (up to 50% of maximal). Up to 10 motor units working simultaneously could be identified. Under strictly stable conditions of muscular contraction the recruitment order of the motoneurons was constant. The firing rate was inversely proportional as a rule to this recruitment order. As a rule the changes in frequency connected with voluntary contraction of measured strength were in the same direction for different motoneurons. Statistical analysis of the frequency fluctuations observed during contraction of constant strength revealed direct correlation between them. The behavior of the motoneurons as described above is regarded as the result of the diffuse, indeterminate distribution of the synaptic input in the group of motoneurons innervating the muscle studied. It was also shown that even under stable conditions individual motoneurons or groups of them sometimes fired independently. During the performance of different types of movements, the firing rates of the recruited motoneurons varied in different directions and some motoneurons were replaced by others. This shows that when motoneurons function under natural conditions they use not only a common (indeterminate) but also a determinate input.Institute of Problems of Information Transmission, Academy of Sciences of the USSR, Moscow. Translated from Neirofiziologiya, Vol. 5, No. 1, pp. 77–87, January–February, 1973.     

Does the frequency content of the surface mechanomyographic signal reflect motor unit firing rates? A brief review.

The purpose of this review is to examine the literature that has investigated the potential relationship between mechanomyographic (MMG) frequency and motor unit firing rates. Several different experimental designs/methodologies have been used to address this issue, including: repetitive electrical stimulation, voluntary muscle actions in muscles with different fiber type compositions, fatiguing and non-fatiguing isometric or dynamic muscle actions, and voluntary muscle actions in young versus elderly subjects and healthy individuals versus subjects with a neuromuscular disease(s). Generally speaking, the results from these investigations have suggested that MMG frequency is related to the rate of motor unit activation and the contractile properties (contraction and relaxation times) of the muscle fibers. Other studies, however, have reported that MMG mean power frequency (MPF) does not always follow the expected pattern of firing rate modulation (e.g. motor unit firing rates generally increase with torque during isometric muscle actions, but MMG MPF may remain stable or even decrease). In addition, there are several factors that may affect the frequency content of the MMG signal during a voluntary muscle action (i.e. muscle stiffness, intramuscular fluid pressure, etc.), independent of changes in motor unit firing rates. Despite the potential influences of these factors, most of the evidence has suggested that the frequency domain of the MMG signal contains some information regarding motor unit firing rates. It is likely, however, that this information is qualitative, rather than quantitative in nature, and reflects the global motor unit firing rate, rather than the firing rates of a particular group of motor units.     

Evidence of self-sustained motoneuron firing in young and older adults.

Motoneurons demonstrate a type of self-sustained firing behavior that seems to be produced by a prolonged period of depolarization caused by intrinsic long-term changes in the motoneuron. Such self-sustained firing behavior has previously been reported in human motor units. The purpose of the present study was to investigate the occurrence of self-sustained firing behavior in older adults. Eight young (mean age 24 yrs) and eight older (mean age 73 yrs) individuals participated in the investigation. While subjects produced light dorsiflexion contractions, a brief vibration stimulus was applied to the tibialis anterior muscle. Motor unit recordings were also obtained from the tibialis anterior muscle. Self-sustained firing behavior was evidenced by the appearance of new motor unit recruitment following vibration, even as the motor units that fired before the vibratory stimulus maintained a steady firing rate. The proportion of motor units exhibiting self-sustained firing activity was similar in both young and older adults (approx. 23% of trials). We conclude that self-sustained firing behavior is a ubiquitous phenomenon that does not seem to be affected by the aging process.     

Firing rates of motor units in human vastus lateralis muscle during fatiguing isometric contractions.

We investigated the firing rate of motor units in the vastus lateralis muscle in five healthy young men (mean = 21.4 yr, SD = 0.9) during a sequence of isometric constant-torque contractions repeated to exhaustion. The contractions were sustained at 20% of the maximal voluntary level, measured at the beginning of the test sequence. Electromyographic (EMG) signals were recorded via quadrifilar fine-wire electrodes and subsequently decomposed into their constituent motor unit action potentials to obtain the motor unit firing times. In addition, we measured the whole muscle mechanical properties during the fatigue task using electrical stimulation. The firing rate of motor units first decreased within the first 10-20% of the endurance time of the contractions and then increased. The firing rate increase was accompanied by recruitment of additional motor units as the force output remained constant. The elicited twitch and tetanic torque responses first increased and then decreased. The two processes modulated in a complementary fashion at the same time. Our data suggest that, when the vastus lateralis muscle is activated to maintain a constant torque output, its motoneuron pool receives a net excitatory drive that first decreases to compensate for the short-lived potentiation of the muscle force twitch and then increases to compensate for the diminution of the force twitch. The underlying inverse relationship between the firing rate and the recruitment threshold that has been reported for nonfatigued contractions is maintained. We, therefore, conclude that the central nervous system control of vastus lateralis motor units remains invariant during fatigue in submaximal isometric isotonic contractions.     

Rate-coding of spinal motoneurons with high-frequency magnetic stimulation of human motor cortex

Rate-coding in spinal motoneurons was studied using high-frequency magnetic stimulation of the human motor cortex. The subject made a weak contraction to cause rhythmic (i.e., tonic) discharge of a single motor unit in flexor (or extensor) carpi radialis or tibialis anterior, while the motor cortical representation of that muscle was stimulated with brief trains of pulses from a Pyramid stimulator (4 Magstim units connected by 3 BiStim modules). An "m@n" stimulus train consisted of m number of pulses (1-4), with an interpulse interval (IPI) of n ms (1-6). Peristimulus time histograms were constructed for each stimulus condition of a given motor unit, and related to the average rectified surface electromyography (EMG) from that muscle. Surface EMG responses showed markedly more facilitation than single-pulse stimulation, with increasing numbers of pulses in the train; responses also tended to increase in magnitude for the longer IPI values (4 and 6 ms) tested. Motor-unit response probability increased in a manner comparable to that of surface EMG. In particular, motoneurons frequently responded twice to a given stimulus train. In addition to recruitment of new motor units, the increased surface EMG responses were, in part, a direct consequence of short-term rate-coding within the tonically discharging motoneuron. Our results suggest that human corticomotoneurons are capable of reliably following high-frequency magnetic stimulation rates, and that this activity pattern is carried over to the spinal motoneuron, enabling it to discharge at extremely high rates for brief periods of time, a pattern known to be optimal for force generation at the onset of a muscle contraction.     

Motor unit activation patterns during concentric wrist flexion in humans with different muscle fibre composition

Muscle activity was recorded from the flexor carpi radialis muscle during static and dynamic-concentric wrist flexion in six subjects, who had exhibited large differences in histochemically identified muscle fibre composition. Motor unit recruitment patterns were identified by sampling 310 motor units and counting firing rates in pulses per second (pps). During concentric wrist flexion at 30% of maximal exercise intensity the mean firing rate was 27 (SD 13) pps. This was around twice the value of 12 (SD 5) pps recorded during sustained static contraction at 30% of maximal voluntary contraction, despite a larger absolute force level during the static contraction. A similar pattern of higher firing rates during dynamic exercise was seen when concentric wrist flexion at 60% of maximal exercise intensity [30 (SD 14) pps] was compared with sustained static contraction at 60% of maximal voluntary contraction [19 (SD 8) pps]. The increase in dynamic exercise intensity was accomplished by recruitment of additional motor units rather than by increasing the firing rate as during static contractions. No difference in mean firing rates was found among subjects with different muscle fibre composition, who had previously exhibited marked differences in metabolic response during corresponding dynamic contractions. It was concluded that during submaximal dynamic contractions motor unit firing rate cannot be deduced from observations during static contractions and that muscle fibre composition may play a minor role. Accepted: 5 May 1998     

Differences between properties of male and female motor units in the rat medial gastrocnemius muscle.

Differences between motor units in hindlimb locomotor muscles of male and female Wistar rats were studied. The contractile and action potential properties of various types of motor units as well as proportions of these units in the medial gastrocnemius muscle were analyzed. Experiments were based on functional isolation and electrical stimulation of axons of single motor units. Composition of motor units was different for male and female subjects, with higher number of the fast fatigable and lower number of slow type units in male animals. The contraction and the half-relaxation times were significantly longer in male motor units, what might be due to differences in muscle size. Slower contraction of male motor units likely corresponds to lower firing rates of their motoneurons. On the other hand, no significant differences between sexes were observed with respect to force parameters of motor units (the twitch and the maximum tetanus forces), except the fast resistant units (higher force values in male muscles). The mass of the muscle was approximately 1.5 time bigger in male rats. However, the mean ratio of motor unit tetanus force to the muscle mass was almost twice smaller in this group, what indirectly suggests that muscles of male rats are composed of higher number of motor units. Finally, female muscles appeared to have higher fatigue resistance as the effect of higher proportion of resistant units (slow and fast resistant) and higher values of the fatigue index in respective motor unit types. The motor unit action potentials in female rats had slightly lower amplitudes and shorter time parameters although this difference was significant only for fast resistant units.     

A Simulation Study to Examine the Effect of Common Motoneuron Inputs on Correlated Patterns of Motor Unit Discharge

The influence of common oscillatory inputs to the motoneuron pool on correlated patterns of motor unit discharge was examined using model simulations. Motor unit synchronization, in-phase fluctuations in mean firing rates known as ‘common drive’, and the coefficient of variation of the muscle force were examined as the frequency and amplitude of common oscillatory inputs to the motoneuron pool were varied. The amount of synchronization, the peak correlation between mean firing rates and the coefficient of variation of the force varied with both the frequency and amplitude of the common input signal. Values for ‘common drive’ and the force coefficient of variation were highest for oscillatory inputs at frequencies less than 5 Hz, while synchronization reached a maximum when the frequency of the common input was close to the average motor unit firing rate. The frequency of the common input signal for which the highest levels of synchronization were observed increased as motoneuron firing rates increased in response to higher target force levels. The simulation results suggest that common low-frequency oscillations in motor unit firing rates and short-term synchronization result from oscillatory activity in different bands of the frequency spectrum of shared motoneuron inputs. The results also indicate that the amount of synchronization between motor unit discharges depends not only on the amplitude of the shared input signal, but also on its frequency in relation to the present firing rates of the individual motor units.     

Relationship between the discharge rate of a firing motoneuron and the effectiveness of excitatory la afferent volleys in man

The H-reflex was evoked after producing regular unit firing in the flexor carpi ulnaris set up by moderate voluntary isometric muscular contraction. The firing index was used to quantify the effectiveness of the monosynaptic afferent signal traveling to the firing motoneuron. An analysis was made of the 3.3–16.0 spikes/sec firing range characteristic of naturally occurring muscular contraction. Effectiveness of afferent signals for motor units in the "fast" muscles under study were found to depend on motoneuronal background firing rate; the former declined as the latter rose, as previously discovered during research into "slow" soleus muscle units [2]. Afferent signals were most effective for motoneurons belonging to the "fast" muscles over the entire range of firing rates. It was found from analyzing afferent signal efficacy in relation to its point of occurrence within the interspike interval that variations in motoneuronal excitability within this interval are the reason for this relationship.Institute for Research into Information Transmission, Academy of Sciences of the USSR, Moscow. Translated from Neirofiziologiya, Vol. 19, No. 5, pp. 595–600, September–October, 1987.     

Physiological and developmental implications of motor unit anatomy

There is increasing evidence that the architectural design and arrangement of the fibers within a motor unit have important physiological and developmental ramifications. Limited data, however, are available to directly address this issue. In the present study the physiological properties of one motor unit in each of seven cat tibialis anterior (TA) muscles were determined. Each of these units then was repetitively stimulated to deplete the glycogen in all muscle fibers within the unit. Subsequently, the length, type of ending, and spatial distribution of fibers sampled from these physiologically and histochemically typed motor units were determined. Four fast fatigable (FF), one fast, fatigue resistant (FR), and two slow (S) motor units (MU) were studied. The samples consisted of all those glycogen-depleted fibers (9-27) contained within a single fascicle or a circumscribed area of each of the motor unit territories. The mean fiber lengths for the two slow motor units were 35.9 and 45.5 mm. The mean fiber lengths for the fast motor unit samples ranged from 8.8 to 48.5 mm. Some fibers of both the fast and slow units reached lengths of 58 mm. Most of the fibers in the slow units extended the entire distance between the proximal and distal musculotendinous planes, had relatively constant cross-sectional areas, and terminated at the tendon as blunt endings. In contrast, the majority of the fibers in the fast units terminated intrafascicularly at one end, and the cross-sectional area decreased progressively along their lengths, that is, showed a tapering pattern for a significant proportion of their lengths. Therefore, the force generated by units that end midfascicularly would appear to be transmitted to connective tissue elements and/or adjacent fibers. All fibers of a fast unit within a fascicle were located at approximately the same proximo-distal location. Thus, developmentally the selection of muscle fibers by a motoneuron would seem to be influenced by their spatial distribution. The architectural complexities of motor units also have clear implications for the mechanical interactions of active and inactive motor units. For example, the tension capabilities of a motor unit may be influenced not only by the spatial arrangement of its own fibers, but also by the level of activation of neighboring motor units.     

A comparison of central aspects of fatigue in submaximal and maximal voluntary contractions.

Magnetic and electrical stimulation at different levels of the neuraxis show that supraspinal and spinal factors limit force production in maximal isometric efforts ("central fatigue"). In sustained maximal contractions, motoneurons become less responsive to synaptic input and descending drive becomes suboptimal. Exercise-induced activity in group III and IV muscle afferents acts supraspinally to limit motor cortical output but does not alter motor cortical responses to transcranial magnetic stimulation. "Central" and "peripheral" fatigue develop more slowly during submaximal exercise. In sustained submaximal contractions, central fatigue occurs in brief maximal efforts even with a weak ongoing contraction (<15% maximum). The presence of central fatigue when much of the available motor pathway is not engaged suggests that afferent inputs contribute to reduce voluntary activation. Small-diameter muscle afferents are likely to be activated by local activity even in sustained weak contractions. During such contractions, it is difficult to measure central fatigue, which is best demonstrated in maximal efforts. To show central fatigue in submaximal contractions, changes in motor unit firing and force output need to be characterized simultaneously. Increasing central drive recruits new motor units, but the way this occurs is likely to depend on properties of the motoneurons and the inputs they receive in the task. It is unclear whether such factors impair force production for a set level of descending drive and thus represent central fatigue. The best indication that central fatigue is important during submaximal tasks is the disproportionate increase in subjects' perceived effort when maintaining a low target force.