Synchronization of low- and high-threshold motor units

SYNCHRONIZATION OF LOW- AND HIGH-THRESHOLD MOTOR UNITSJASON M. DEFREITAS, PhD,1 TRAVIS W. BECK, PhD,1 XIN YE, MS,1 and MATT S. STOCK, PhD2

1 University of Oklahoma, 1401 Asp Avenue, Norman, Oklahoma 730192 Texas Tech University, Lubbock, Texas, USA

Accepted 16 July 2013

ABSTRACT: Introduction: We examined the degree of synchro-nization for both low- and high-threshold motor unit (MU) pairsat high force levels. Methods: MU spike trains were recordedfrom the quadriceps during high-force isometric leg extensions.Short-term synchronization (between 26 and 6 ms) was calcu-lated for every unique MU pair for each contraction. Results: Athigh force levels, earlier recruited motor unit pairs (low-thresh-old) demonstrated relatively low levels of short-term synchroni-zation (approximately 7.3% extra firings than would have beenexpected by chance). However, the magnitude of synchroniza-tion increased significantly and linearly with mean recruitmentthreshold (reaching 22.1% extra firings for motor unit pairsrecruited above 70% MVC). Conclusions: Three potential mech-anisms that could explain the observed differences in synchro-nization across motor unit types are proposed and discussed.

Muscle Nerve 49:575–583, 2014

The firing of motor units that innervate the samemuscle have a tendency to be synchronized in timemore often than could be expected from chancealone.1–3 Furthermore, when multiple motor unitsfire together there is a nonlinear, temporal sum-mation of their twitch forces4–6 which exceeds thealgebraic sum of the individual motor units. Conse-quently, the magnitude of motor unit synchroniza-tion may have an influence on the resultant forceoutput. Using a computer simulation model, Bakeret al.7 showed that synchronization of upper motorneurons descending from the motor cortexresulted in increased force production (see theirFig. 5). These findings are also supported byexperimental evidence, as Merton5 has demon-strated that synchronous excitation of a muscleresulted in larger and longer lasting twitches thanthose elicited from asynchronous excitation. Addi-tionally, the model by Baker et al.7 revealedanother potential benefit of synchronization inthat synchronized descending commands from themotor cortex require lesser firing rates to producethe same amount of force as asynchronousdescending commands. In other words, synchroni-zation of motor neurons allows the central nervoussystem (CNS) to be more efficient.

As such, it is quite possible, and has been sug-gested,8 that motor unit synchronization may be adeliberate neural strategy utilized to increase forceproduction (in addition to manipulating firingrate and recruitment). In support of this possiblestrategy is the fact that motor unit synchronizationis greater during maximal contractions than dur-ing submaximal contractions.9 Furthermore, if syn-chronization is indeed a deliberate strategy toincrease force, it stands that there would be anappropriate adaptation to habitually producinghigh levels of force (i.e., strength training). Suchan adaptation seems to occur, as more studies3,10,11

than not12 have demonstrated training-inducedincreases in either motor unit or motor neuronsynchronization. Multiple other studies13–15 havealso reported greater levels of synchrony instrength-trained individuals compared to eitheruntrained and/or skill-trained individuals. It isimportant to note, however, that not all of the evi-dence has supported an intentional control ofmotor unit synchronization. For example, Contessaet al.16 found no change in motor unit synchroni-zation in the vastus lateralis muscle after multiplesustained submaximal contractions. They con-cluded that motor unit synchronization could nothave caused the observed fatigue-induced changesin force variability.

Nevertheless, there is enough evidence to main-tain the possibility that motor unit synchronizationmay be a deliberate neural strategy utilized toincrease force production. Despite this possibility,motor units of varying force-producing capabilitieshave not been investigated thoroughly. It isaccepted widely that earlier recruited motor units(i.e., low-threshold) produce low levels of twitchforce and that the force-producing capabilities ofmotor units linearly increase with recruitmentthreshold.17 However, due mostly to technical limi-tations, the high-threshold and high-force produc-ing motor units have been largely neglected in thesynchronization literature. Many studies haverelied on use of indwelling electrodes for record-ing of 2 separate single-motor unit action potentialtrains.1,18–20 As a result, most studies have beenrestricted to very low force levels that correspondto less than 10% of a subject’s maximum voluntarycontraction (MVC).12,18,21 Although a few stud-ies1,3,19,22 have attempted to compare the degreeof motor unit synchronization of low-threshold

Abbreviations: CI, confidence interval; CNS, central nervous system;EPSP, excitatory postsynaptic potential; MUAPT, motor unit action poten-tial train; MVC, maximum voluntary contraction; VL, vastus lateralis muscleKey words: Synchrony; motor neuron; recruitment threshold; decompo-sition; common inputsCorrespondence to: J.M. DeFreitas; e-mail: [email protected]

VC 2013 Wiley Periodicals, Inc.Published online 28 July 2013 in Wiley Online Library (wileyonlinelibrary.com). DOI 10.1002/mus.23978

Synchronization of Low- and High-Threshold Motor Units MUSCLE & NERVE April 2014 575

pairs versus high-threshold pairs, there remainsuncertainty in their findings, since all of thesestudies limited their subjects to very low force lev-els. The cutoff between low- and high-thresholdmotor units in these studies would equate toapproximately 1–5% MVC.

The aim of this study was to examine thedegree of synchronization across motor unit pairsof widely varying recruitment thresholds and force-producing capabilities during sufficiently highforce contractions. We hypothesized that high-threshold motor units would have greater degreesof synchronization at high force levels than theirlow-threshold counterparts, thereby further sup-porting the possibility that synchronization is adeliberate neural strategy intended to helpincrease force production.

EXPERIMENTAL PROCEDURES

Subjects. Fifteen healthy men and women (5men, 10 women; mean 6 SD age 5 20.6 6 2.9 years;stature 5 1.7 6 0.1 m; body mass 5 62.6 6 11.3 kg)volunteered to participate in this investigation.Each participant provided informed consent andcompleted a pre-exercise health and exercise statusquestionnaire prior to testing. Subjects wererequired to have no current or recent (within thepast 6 months) neuromuscular or musculoskeletalproblems in the knees, hips, or lower back to beconsidered eligible for the study. The study wasapproved by the University Institutional ReviewBoard for Human Subjects Research prior to test-ing and conformed to the standards set by the lat-est revision of the Declaration of Helsinki.

Isometric Testing. Each subject made 1 visit to thelaboratory and was tested for unilateral isometricstrength of the dominant (based on kicking prefer-ence) leg extensors. The subjects were seated in acustomized chair with the leg attached to a loadcell (Model SSM-AJ-500, Interface Inc., Scottsdale,Arizona) to measure isometric leg extension force(N). All isometric contractions were performed ata joint angle of 120� between the thigh and thelower leg (180�5 full extension). Following awarm-up of 4 15-s submaximal isometric contrac-tions at approximately 50% of each subject’s maxi-mum, they performed 3 MVCs. Each MVC wasseparated by 2–3 min of rest, and the highest forcevalue of the 3 trials was designated as the subject’strue MVC. After an additional 2–3 min of rest, thesubjects performed a 15 s, submaximal, trapezoidalcontraction. The trapezoid ramped force linearlyfrom zero force to 80% MVC over 5 s, remainedconstant at 80% MVC for 5 s, and then rampedlinearly back down to zero force over 5 s. Visualfeedback of the real-time force level was providedto the subjects along with a target template. This

helped minimize error and ensure that the subjectwas as close to 80% of MVC as possible. The sub-ject had practiced tracing a template trajectoryduring the warm-ups. Contractions were later vali-dated by assuring that the mean of the 5-s constantforce region was within 2% of the 80% target (i.e.,the range of all the contractions were within 78–82% MVC).

EMG Signal Acquisition and Processing. Four sepa-rate bipolar surface EMG signals were detectedfrom the vastus lateralis (VL) muscle during thetrapezoid muscle action with a specialized 5-pinsurface array sensor (Delsys, Inc., Boston, Massa-chusetts). This sensor is described in more detailby Nawab et al.23 (see their Fig. 1). The skin wasshaved and cleansed with isopropyl alcohol priorto securing the sensor over the belly of the VLwith surgical tape. The sensor was placed at 2/3 ofthe line from the anterior superior iliac spine tothe lateral patella in accordance with the recom-mendations from the SENIAM project.24 A refer-ence electrode was placed on the patella. The VLwas chosen because of its high force-producingcapabilities and its wide motor unit recruitmentrange (motor units in the VL can be recruited upto 90–95% MVC).25 The analog EMG signals werecollected with a modified Bagnoli desktop EMGsystem (Delsys Inc, Boston, Massachusetts), high-pass filtered (cutoff frequency 5 20 Hz), low-passfiltered (cutoff frequency 5 1,750 Hz), sampled at20 kHz, and stored for subsequent analysis. Theraw EMG signals were decomposed into their con-stituent motor unit action potential trains(MUAPTs) using the Precision Decomposition(PD) III algorithm recently described by De Lucaet al.26 and improved by Nawab et al.23 TheMUAPTs were then tested for accuracy using theDecompose-Synthesize-Decompose-Compare(DSDC) test described by De Luca and Contessa.27

To reduce the potential influence of false positiveand false negative firings, any motor unit that didnot demonstrate an accuracy of 95.0% or greaterwas eliminated from further analysis. Figure 1Ashows an example of the firings for 21 motor unitsdetected during a trapezoid contraction up to 80%MVC for subject 11. Mean firing rate and recruit-ment threshold were also calculated for eachmotor unit. Recruitment threshold is defined asthe force level (% MVC) at which the motor unitfirst started firing. Mean firing rate curves werecomputed for each MUAPT by low-pass filteringthe impulse train with a 1-s unit-area Hanning win-dow. Low-threshold motor units were consideredto be those recruited below 30% MVC. Subse-quently, motor units recruited at or above 30%MVC were designated as high-threshold. Previously

576 Synchronization of Low- and High-Threshold Motor Units MUSCLE & NERVE April 2014

used cutoffs to distinguish between low- and high-threshold motor units have been 20% MVC,28 25%MVC,29–31 and 30% MVC.32 Furthermore, it hasbeen demonstrated that the biceps brachii, whichhas been shown to have similar firing propertiesand maximal motor unit recruitment ranges (upto 90–95% MVC) to the VL25,33 has recruited closeto 50% (23 of 49) of its motor units at 30%MVC.33

Motor Unit Synchronization. The synchronizationbetween firings of motor unit pairs was examinedby constructing cross-interval histograms in accord-ance with the technique first applied by De Lucaet al.2 and again by Contessa et al.16 The cross-interval histograms (see Fig. 2C) were constructedfrom each possible unique pairing of MUAPTs bymeasuring only the first-order forward and back-ward recurrence times (see Fig. 1C). The firingsused for this analysis were pulled from the centerapproximately flat portion of the mean firing rateplot (Fig. 1B) for each motor unit. When the flatportion of a motor unit’s mean firing rate wasselected, the same portion was pulled from all pre-vious motor units for comparison. For example,

after selecting the appropriate firings from themotor unit # 4 mean firing rate plot, the same por-tion was pulled from motor units 1–3 for compari-son (i.e., 4 vs. 3, 4 vs. 2, and 4 vs. 1). A separateportion was then selected for motor unit #5 forcomparisons of 5 versus 4, 5 versus 3, etc… Theanalyses were performed using these descending-order comparisons, because the region of stablemean firing rates becomes progressively smallerwith increases in recruitment threshold (see Fig.1B). For any given motor unit pair, the motor unitwith the lowest number of firings in the selectedregion was designated as the reference motor unit.The second was designated as the test motor unit.For each motor unit comparison, 2 separate cross-interval histograms were constructed: one with theoriginal, observed firings and a second in whichthe firings of the reference motor unit were shuf-fled randomly. The shuffled histogram representsthe between-firing latencies if the 2 motor unitswere completely independent of each other (i.e.,no common synaptic inputs). The width of the his-tograms was limited to 6 the mean interpulse inter-val for the reference motor unit (e.g., histogramx-axis ranges from 250 to 50 ms for a reference

FIGURE 1. (A) Individual motor unit action potential trains during the isometric, trapezoid muscle action. Each vertical bar represents

a motor unit firing. The solid black line is the subject’s force output. (B) The mean firing rate curves for each of the motor units

depicted in A. The horizontal dashed line with the diamond ends represents the region of firings that was used for subsequent analysis

for motor unit 2. The horizontal dashed line with the circles represents the same region for motor unit 19. (C,D) Visual depiction of the

first-order forward and backward recurrence times (C) used to construct a cross-interval histogram (D).


motor unit with an interpulse interval of 50 ms). A95% confidence interval (CI) was calculated forthe shuffled histogram as the mean 1 1.96 stand-ard deviations and then overlaid on top of theobserved histogram. Because there are no negativecounts in a histogram, we would have been justi-fied to use the one-tailed value of 1.65 SD abovethe mean as our confidence interval. However, wedecided to take a more conservative approachusing the two-tailed value (1.96). Any peaks in theobserved histogram that fall below the 95% CIwere considered to have occurred by chance, andany peaks that exceeded the CI were subsequentlyconsidered to be significant. In other words, thepeak is considered to have more synchronous fir-ings at that latency than could be expected fromchance alone. The magnitude of synchronizationof the significant peaks was then calculated usingthe “Sync Index” (%) described by De Luca et al.(p 2014)2 In short, the index is the percentage ofextra events (i.e., percentage of firings beyondwhat would be expected from chance alone) nor-malized to the number of firings in the referencemotor unit. With short-term synchronization beingof particular interest in this study, a separate short-term Sync Index was also calculated maintainingthe entire histogram as total area, but only consid-ering the significant peaks that occurred between

26 and 6 ms. If no peaks exceeded the 95% CI,then the resulting Sync Index was 0% (i.e., no syn-chronization was present).

Statistical Analyses. Linear regression was used toassess 2 separate relationships: (a) the recruitmentthreshold and number of firings used for synchro-nization analysis for each motor unit, and (b) themean recruitment threshold and short-term syn-chronization index for each motor unit pair. Themean recruitment threshold/synchronization anal-yses were performed on group data and for eachindividual. Bin widths of 5% (e.g., 5–10%, 10–15%,etc.) were used to condense the group data. Thegroup linear regression was applied to the meansof each bin. An alpha level of 0.05 was used for allcomparisons. Only motor units which demon-strated at least 95.0% decomposition accuracy wereincluded in the statistical analyses. Additionally,the 30% recruitment threshold cutoff was used todichotomize the motor units into low-thresholdand high-threshold groups. Only motor unit pairsof similar threshold (low/low and high/high) wereused for the second regression analysis. The pur-pose of this separation, and removal of any low/high comparisons, was to improve the clarity of themotor units which provided moderate meanrecruitment thresholds. If low- and high-threshold

FIGURE 2. (A,B) Example cross-interval histograms from a pair of low-threshold motor units (A) and a pair of high-threshold motor

units (B). The magnitude of short-term synchronization was calculated as the Short-Term Sync Index (%). The vertical shaded area

depicts the region of short-term synchronization (26 to 6 ms). Significant peaks are those that exceed the 95% confidence interval

(CI). It should be noted that the x-axis of the lower histogram (B) originally spanned from 282 to 82 ms but was truncated for compari-

son with histogram A. Ref. 5 reference; MU 5 motor unit; RT 5recruitment threshold (as a % of maximal voluntary contraction).


comparisons were not eliminated, then it would beimpossible to determine if a pair of motor unitswith a moderate mean recruitment threshold weremotor units of similar types or drastically differenttypes. For example, without this separation, amotor unit pair with a mean recruitment thresholdof 34% MVC could have come from motor unitswith thresholds of 32% and 36% MVC, or frommotor units with thresholds of 4% and 64% MVC.Therefore, the elimination of low- and high-threshold pairings allowed for comparisons ofmotor unit types (i.e. motor units of similarrecruitment thresholds).

RESULTS

Motor Unit Analyses. Initially, approximately 300motor units were detected, and approximately3,000 unique motor unit pairs were analyzed fromthe original 15 subjects. However, the contractionsof 4 subjects were eliminated from further analysisdue to either poor decomposition accuracy (i.e.,too many motor units below 95%) or because ofclustering of motor units within a small range ofrecruitment thresholds (e.g., all motor unitsdetected were recruited within 10% MVC of eachother). Of the remaining 11 participants, 165 ofthe detected motor units demonstrated the neces-sary decomposition accuracy (>95%). The numberof firings used for synchronization analysis foreach of the 165 motor units, as well as the distribu-tion of low-threshold pairs to high-threshold pairs,can be seen in Figure 3. The mean number of fir-ings per motor unit was 137. Using only the 165motor units with sufficient accuracy, 757 uniquemotor unit pairs of similar recruitment thresholds(i.e., low/low or high/high) were analyzed(approximately 68 motor unit pairs per subject).The average accuracy of the 165 motor units was96%.

Motor Unit Synchronization. Approximately 65.4%(495 of 757) of the motor unit pairs demonstrated

a significant amount of short-term synchronization(i.e., a central peak in the histogram exceeded the95% confidence interval). The grouped linearregression for the synchronized motor unit pairs(n 5 495) in all 11 subjects can be seen in Figure4. There was a significant (p 5 0.0002) positive rela-tionship between short-term synchronization andthe mean recruitment threshold for each motorunit pair (r 5 0.833). Individual analyses showedthat the same relationship was significant in 7 ofthe 11 subjects. The results of the individual sub-ject linear regressions are also shown in Figure 4(below the pooled data). The grouped regressionrevealed that motor unit pairs recruited between 5and 10% MVC exhibited 7.3% extra short-term fir-ings than would have been expected from chance,while pairs recruited above 70% MVC exhibited22.1% extra firings. As demonstrated in Figure 5,the percent of motor unit pairs that exhibited sig-nificant short-term synchronization was notdependent on mean recruitment threshold.

DISCUSSION

Synchronization of Low- and High-Threshold Motor

Unit Pairs. These results reveal that high-threshold motor unit pairs exhibit greater short-term synchronization than their low-thresholdcounterparts. No previous study has made thiscomparison using motor units recruited at higherforce outputs (up to 79.1% MVC). The previousstudies that attempted the comparison did so withhigh-threshold motor units that were recruited atvery low forces (<10% MVC).1,3,19,22 Nevertheless,our findings that high-threshold motor unit pairsdemonstrate significantly greater occurrences ofsynchronous firings than low-threshold pairs are inagreement with the conclusions developed frommost studies.1,19,22 Our results, however, conflictslightly with the findings of Milner-Brown et al.,3

who demonstrated only a weak relationship(r 5 0.34) between motor unit recruitment thresh-old and synchronization ratio. The difference inthe strength of the relationship might beexplained by the muscles and relative force out-puts examined. The findings of our study supportthe previously suggested hypothesis2,3,9,14 thatmotor unit synchronization may be a deliberateneural strategy intended to help increase forceproduction. However, as will be discussed, thereare other mechanisms that could also explain theresults, and are seemingly more likely.

Implications. The varying levels of motor unit syn-chronization demonstrated can be explainedpotentially by 3 distinct mechanisms: (a) variableCNS control schemes for different motor unittypes, (b) inherent differences in membrane prop-erties between the motor units, or (c) differences

FIGURE 3. The recruitment threshold (% MVC) and number of

firings used for synchronization analysis for each motor unit.

This only includes the motor units that exhibited at least 95%

decomposition accuracy. MVC 5 maximal voluntary contraction


in synaptic strength from peripheral sources. Ifoption (a) were true, then it would suggest thatvarying levels of synchronization are the result of adeliberate strategy by the CNS to control force.

However, the collective evidence from other stud-ies suggests that the other options (b and c) mightbe more plausible. With regard to the CNS controlscheme, it is important to consider the role ofcommon drive. Multiple studies34–37 have shownthat the firing rates of different motor units aremodulated together by the CNS. Therefore, it isgenerally concluded that these motor units receivea “common drive,” which relieves the CNS fromthe necessity to regulate each individual motorunit separately. However, it is still unknown if com-mon drive, as measured by the cross-correlation offiring rates, varies with recruitment thresholds. It ispossible that common drive is stronger betweenmotor units of similar recruitment threshold andcould conceivably be weaker between low- andhigh-threshold motor units. Therefore, the exis-tence of common drive does not necessarily elimi-nate the possibility that the CNS may bedeliberately sending a more synchronized input tohigh-threshold motor units than to low-threshold

FIGURE 4. The larger plot is the grouped regression analysis for mean recruitment threshold (% MVC) and the short-term synchroni-

zation index (% extra firings between 26 and 6 ms) in all 11 subjects. Bin width is in 5% intervals. Vertical bars represent the standard

deviation within each bin. Above the vertical bars are the numbers of motor unit pairs within each bin. Below the main figure are the

data points for each individual. The individual subject data were not grouped into bins. Lines of best fit are shown for the 7 subjects

who exhibited a significant correlation. MVC 5 maximal voluntary contraction.

FIGURE 5. The mean recruitment threshold (% MVC) and the

percent of motor unit pairs that demonstrated significant short-

term synchronization (i.e. a Sync Index above 0). Bin widths

are shown below the data points. MVC 5 maximal voluntary

contraction.


motor units. It is important to note, however, thatthe relatively low number of extra firings demon-strated here (approximately 7–22%) could hardlybe considered optimal for force enhancement.

The second possible mechanism is that inher-ent properties of the motor units lead to differen-ces in their levels of synchronization. It is fairlywell established that motor neurons have a widerange of properties that affect their firing behav-ior, such as soma size, membrane permeability/resistance, and capacitance.38,39 These propertiesdictate neuronal recruitment threshold as well asits behavior after threshold has been reached.Additionally, it has been suggested that higher-threshold motor units are more sensitive tochanges in descending drive.40 Therefore, it is fea-sible that, if all motor units receive exactly thesame common drive, the high-threshold motorunits might be more susceptible to synchronizationand more closely follow the firing patterns of theinput drive than low-threshold motor units. Itshould be noted that this potential mechanism fordifferences in synchronization would seem to bemutually exclusive with the possibility of a deliber-ate CNS strategy sending varying levels ofsynchronized drive.

The third possible mechanism that we proposeis that the varying levels of synchronization acrossmotor units could be due to differences in thenumber and strength of synaptic inputs from sec-ondary sources (sources other than voluntary drivefrom the brain). It has been demonstrated previ-ously in multiple studies that recurrent inhibitionfrom Renshaw cell feedback has a desynchronizingeffect on the neighboring motor neuron pool.41–43

In turn, this opens up the possibility that second-ary excitatory inputs to motor neurons could alsohave a desynchronizing effect. In agreement,Negro and Farina44 have suggested that the exis-tence of a second excitatory common input (ofperipheral origin), in addition to descending com-mand, would have a decorrelating effect on themotor neuron pool. The only secondary excitatoryinputs that could have that strong an influence onmotor neuron firing behavior would likely be frommuscle spindles (Ia afferent neurons). It has beenshown that spindle afferents may be responsiblefor up to 1/3 of the excitation that motor neuronsreceive during voluntary contractions.45 The possi-bility that a desynchronizing effect from spindleafferents might be the cause of differences inmotor unit synchronization is supported by evi-dence that the number of projections from periph-eral afferent fibers on homonymous a-motorneurons is heterogeneous.46 In other words, the Iafibers from a muscle spindle (and possibly Ib andII afferents as well) do not exhibit equal synaptic

strength to each homonymous motor neuron. Infact, multiple studies47,48 have demonstrated thatspindle afferent neurons have a stronger synapticstrength (and greater EPSP amplitude) withsmaller, low-threshold motor neurons than larger,high-threshold ones. Such a discrepancy in thestrength of excitatory peripheral input coulddesynchronize 2 motor neurons that were previ-ously going to fire simultaneously. Therefore, it isconceivable that all motor units receive the samesynchronized common drive from the brain, butlow-threshold motor units receive more input fromspindle afferents (which has a desynchronizingeffect) than high-threshold motor units. Such anarrangement could certainly account for the differ-ences in synchronization in motor units of varyingrecruitment thresholds demonstrated in this study.It should also be noted that this possible explana-tion is not mutually exclusive with the second pro-posed mechanism (inherent differences in motorneuron membrane properties).

Limitations. It is important that the limitations ofthis study be recognized and formally acknowl-edged. First and foremost, almost all previous syn-chronization studies have used sustained,submaximal contractions of much greater durationthan those in this study (usually provided> 1,000action potentials). Since we were interested in thepossibility that synchrony is an intentional neuralstrategy to increase force, it was integral to ourstudy to record the motor unit firings at high forcelevels. As such, we did not have the luxury of long,sustained contractions, as it is possible that, at 80%MVC, fatigue may have started to influence motorunit synchronization in as short as 10 s. However,because there is no reason to suspect a bias in theerror due to using shorter action potential trains,the large number of motor unit comparisonsshould have more than made up for the decreasednumber of action potentials within each train. Sec-ond, it has been suggested by Nordstrom et al.49

that some synchronization indices, including theone used in the present study, may be biased tochanges in firing rates. However, they based thisconclusion on a very weak relationship (r2 5 0.11for the index used here) between changes in syn-chronization and changes in firing rates.49 Addi-tionally, more recent studies50,51 have shown nodependence on firing rate for the index used inthis study (see index E in T€urker and Powers - Fig.8).51 Because motor units have varying firing rates,they will also have a varying number of firingswithin the region of analysis. Normalizing the extrafirings to the number of firings is the most logicalapproach, as it removes the influence of firingrates on the index. Furthermore, as demonstrated


in Figure 5, mean recruitment threshold did notaffect the probability of a motor unit pair exhibit-ing significant short-term synchronization. Conse-quently, we conclude that our findings were due todifferences in motor unit behavior and not an arti-fact of the index.

CONCLUSIONS

At high force levels, earlier recruited motorunit pairs (i.e., low-threshold) from the humanvastus lateralis demonstrated relatively low levels ofshort-term synchronization (approximately 7.3%extra firings between 26 and 6 ms than wouldhave been expected by chance). However, themagnitude of motor unit synchronization signifi-cantly, and linearly, increased with mean recruit-ment threshold (reaching approximately 22.1%extra firings for motor unit pairs recruited above70% MVC). Three potential mechanisms were pro-posed. First, it is possible that motor unit synchro-nization is manipulated deliberately by the CNS asa strategy to produce force. Second, the differen-ces in synchronization in motor unit types may bedue to differences in membrane properties ofmotor neurons. Finally, it was suggested that thedifferences across motor neurons in their synapticstrength from secondary sources, such as spindleafferents, could have led to greater desynchroniza-tion in smaller motor neurons than in larger ones.We have suggested that the latter 2 mechanismsare more plausible than the former (deliberateCNS strategy). However, further research needs tobe performed in healthy humans to systematicallycompare the synchrony that occurs with and with-out normally functioning afferent input to themotor unit pool.

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Synchronization of low- and high-threshold motor units