SHORT REPORT ABSTRACT: Force production may be influenced by the phase of ventila-tion during which force is exerted. To examine the potential influences ofventilation on variability in maximal force measurements, we recorded peakisometric forces of the finger flexors during normal breathing, forced inspi-ration, forced expiration, and the Valsalva maneuver in 14 healthy adultsubjects. The peak force increased significantly from forced inspiration toforced expiration (about 10%). Both forced expiration and inspiration re-sulted in increases in the flexor/extensor cocontraction ratio, whereas theValsalva maneuver had no significant effects on maximal force or cocon-traction ratio. Thus, this study clearly demonstrates the effects of ventilationon maximal finger force-generating capability. Ventilation needs to be con-trolled for accurate assessments of maximal force.

Muscle Nerve 34: 651–655, 2006

INFLUENCES OF VENTILATION ON MAXIMALISOMETRIC FORCE OF THE FINGER FLEXORS

SHENG LI, MD, PhD, and JAMES J. LASKIN, PhD

Motor Control Laboratory, School of Physical Therapy and Rehabilitation Science,University of Montana, Missoula, Montana 59812, USA

Accepted 21 April 2006

Control of breathing has been used to enhanceforce production during strength exercise and train-ing. If maximal force is exerted while inhaling, ex-haling, or making a forced expiration against theclosed glottis (the Valsalva maneuver), the forcemagnitude is expected to increase from inspirationto expiration to the Valsalva maneuver.19 The effects,however, have not been quantified, and the under-lying mechanisms remain unknown. Although itmight be considered a useful breathing techniquefor ultimate force production, the Valsalva maneu-ver causes increased intrathoracic pressure with con-comitant decreased venous return to the heart andalterations in arterial pressure and heart rate.8,15,19,20

These systemic responses might be harmful andtherefore contraindicated in individuals with cardiacdisease.

The magnitude of maximal voluntary contrac-tion (MVC) is often viewed as a reliable measure ofmuscle strength and is often used to assess neuro-

muscular and musculoskeletal functions. Many fac-tors, however, may influence accurate measurementof this value, resulting in large variability within sub-jects1 and among patient populations.9 These factorsinclude biomechanical factors (e.g., joint angle10

and transducer position18), time of day,14 and phaseof the menstrual cycle.17 Even when these factors arecontrolled, large variability may still occur in MVCmeasurements between trials by the same subject.3

Different phases of ventilation could influence themaximal force-generating capabilities of muscles.19

Therefore, to provide accurate assessment of maxi-mal muscle strength, it is necessary to quantify theeffects of different phases of ventilation on maximalstrength. The purpose of the present study was toassess the effects of different phases of ventilation onthe maximal force-generating capability of distal-limb muscles.

METHODS

Fourteen healthy volunteers (5 men, 9 women; age,26.8 � 6.6 years; age range, 22–42 years) took part inthe experiments. All subjects gave written informedand the study was approved by our institutional re-view board.

During testing, subjects sat on an adjustable chairand breathed through a facemask connected to apneumotach system (Series 1110A; Hans Rudolph,Kansas City, Missouri). After skin preparation, differ-ential surface electrodes (DelSys, Boston, Massachu-

Abbreviations: ANOVA, analysis of variance; EDC, extensor digitorum com-munis; EMG, electromyography; FDS, flexor digitorum superficialis; MVC,maximal voluntary contraction; MVCN, MVCE, MVCI, MVCV, MVC during nor-mal breathing, forced expiration, forced inspiration, and Valsalva maneuver,respectivelyKey words: finger flexion; isometric force; maximal voluntary contraction(MVC); respiration; Valsalva maneuverCorrespondence to: S. Li; e-mail: sheng.li@umontana.edu

© 2006 Wiley Periodicals, Inc.Published online 12 June 2006 in Wiley InterScience (www.interscience.wiley.com). DOI 10.1002/mus.20592

Short Reports MUSCLE & NERVE November 2006 651

setts) were placed over the muscle bellies of theflexor digitorum superficialis (FDS) and extensordigitorum communis (EDC) to record electromy-graphic (EMG) signals. The two upper limbs weresymmetrical with respect to the body midline, withthe upper arms at approximately 45° of abduction inthe frontal plane and 45° of flexion in the sagittalplane, and the elbow joints at approximately 135° offlexion. The forearm was stabilized at the proximaland distal sites by two adjustable vertical bars. Sub-jects placed their fingertips on four force sensorswith fingers slightly curved (about 20° flexion ofinterphalangeal joints). Four unidirectional piezo-electric force sensors (208C02; PCB Piezotronics,Depew, New York) were used to measure individualfinger forces. The position of the sensors could beadjusted within a steel frame (140 mm � 90 mm) tofit the individual. Subjects were asked to relax priorto a trial, and the weights of fingers were offset tozero at the beginning of a trial. The data acquisitionsystem for finger force measurement has been de-scribed previously.11–13 Airflow, EMG, and force sig-nals were sampled at 1000 Hz by a 16-bit analog-to-digital converter (PCI-6229; National Instruments,Austin, Texas) using customized LabView software(National Instruments). All signals were saved foroffline analysis using a customized Matlab (TheMathWorks, Natick, Massachusetts) program.

Subjects performed the following four tasks: (1)MVCN, subjects pressed against the force sensors ashard as they could without specific instructions onventilatory patterns; (2) MVCI, subjects pressedagainst the force sensors as hard as they could whilesynchronizing force production with rapid forcedinspiration; (3) MVCE, similar to MVCI, but forceproduction was synchronized with rapid forced ex-piration; and (4) MVCV, subjects again pressed theforce sensors as hard as they could while performingthe Valsalva maneuver.

Subjects always performed the MVCN task first asa baseline to minimize the influence of instructionson their performance. The other three tasks wereperformed in random order. Five to eight practicetrials were allowed to familiarize subjects with exper-imental settings and instructions. Subjects restedtheir fingertips on the force sensors prior to a trial.Two computer-generated tones indicated the begin-ning of a 10-s trial. Subjects initiated force produc-tion in a self-paced manner within the first 3 s of thetrial and were verbally encouraged to maintain max-imal force production. They did not receive feed-back on force production during the experiment.Each task was repeated four times. To avoid fatigue,the interval between two consecutive trials was ap-

proximately 60 s. All subjects performed the tasks ata similar time of day to minimize the potential effectof testing time.14

Airflow signals were used to confirm subjects’performance for each task through visual inspection.The EMG signals were rectified, and the resultingsignals were low-pass filtered at 10 Hz using a sec-ond-order, zero-lag Butterworth filter to create EMGenvelopes used to quantify muscle activity. Fingerforces were summed to calculate the total force.

The peak force, defined as FMVC, was calculatedas the force averaged over a 100-ms period, centeredabout the instance of the maximal force. The FMVC

was averaged across trials for each subject. To com-pare the effect of ventilation on maximal force-gen-erating capability of the same muscles, the averagedFMVC for MVCI, MVCE, and MVCV was normalized tothe averaged FMVC for MVCN, respectively.

Similarly, peak EMG parameters recorded fromFDS and EDC, defined as EMGFDS and EMGEDC,respectively, were calculated as an average of a100-ms window centered about the instance of themaximal force for FDS and EDC, respectively. EMGFDS

and EMGEDC were then averaged and normalized asfor FMVC. From the normalized EMGFDS andEMGEDC, a ratio of FDS/EDC was calculated to in-dicate cocontraction of the FDS and EDC duringfinger flexion.

Repeated-measures one-way analysis of variance(ANOVA) with a factor task (four levels: MVCN,MVCI, MVCE, MVCV) was used to compare peakforce and EMG during different tasks. Another fac-tor, ventilation (three levels: MVCI, MVCE, MVCV),was used to examine the effect of ventilation onmaximal force production and muscle cocontrac-tion. Whenever necessary, post hoc Tukey’s honestlysignificant difference tests were used to compare thevarious levels of a factor. The level of significance wasset at P � 0.05.

RESULTS

Figure 1 represents typical trials from the same sub-ject, who showed mixed inspiration and expirationduring MVCN. However, other subjects demon-strated different forms of respiration, such as expi-ration only or breath-holding during MVCN. Figure1 shows that FMVC was larger during MVCE thanduring MVCN. This change in FMVC was accompa-nied by changes in EMGFDS. Peak forces occurred atthe beginning of the expiration and inspiration ef-forts, followed by a relatively steady phase of forceproduction during MVCE and MVCI. The initialpeak force was not obvious during MVCV.

652 Short Reports MUSCLE & NERVE November 2006

Ventilatory phases clearly influenced maximalforce-generating capability, showing a main effect oftask (F[3,39] � 4.15, P � 0.012). According to the posthoc analysis, FMVC during MVCE (85.1 N) was largerthan FMVC during MVCI (78.5 N) and MVCN (78.3N), respectively (P � 0.026). The latter two were notsignificantly different. FMVC during MVCV (81.9 N)was not significantly different from the others. Fig-ure 2A demonstrates the normalized FMVC duringdifferent tasks. A one-way ANOVA showed the maineffect of breath on the normalized FMVC (F[2,26] �4.74, P � 0.017). On average, FMVC was larger duringMVCE (110.1%) than during MVCI (101.5%) (P �0.013), whereas FMVC (105.8%) during MVCV wasnot significantly different from the other two. Wealso used the best effort trial from four trials (highestpeak force) as an estimate of MVC for each of thebreathing conditions. This analysis showed the samepattern of results.

The effects of ventilation on EMG revealed a dif-ferent pattern. No significant differences in EMGFDS

or EMGEDC were found among different stages ofventilation (P � 0.17). The effect of ventilation onFDS/EDC ratio was close to significance (F[3,39] �2.67, P � 0.06). The ratios were 5.3, 6.2, 6.0, and 5.2for MVCN, MVCE, MVCI, and MVCV, respectively.The normalized FDS/EDC ratio, however, showed asignificant effect of ventilation (Fig. 2B) (F[2,26] �5.52, P � 0.01). Tukey’s post hoc tests (P � 0.04)revealed that the FDS/EDC ratio was significantlylarger during MVCE (123.3%) and MVCI (119.7%)than during MVCV (102.3%). The ratio was not sig-nificantly different during MVCE and MVCI.

DISCUSSION

We observed that the MVC force developed in thefinger flexors increased significantly from forced in-

spiration to forced expiration (by about 10%). Bothexpiration and inspiration led to increases in FDS/EDC cocontraction ratio during attempted MVCs.The Valsalva maneuver had no significant effects onmaximal force production or FDS/EDC cocontrac-tion.

FIGURE 1. Representative trials recorded from the same subject during different breathing conditions. (A) Normal; (B) forced expiration;(C) forced inspiration; and (D) Valsalva maneuver. Channel 1: total finger force; 2: airflow (inspiration: positive; expiration: negative); 3:rectified and filtered EMG signals from the flexor digitorum superficialis (FDS); 4: rectified and filtered EMG signals from the extensorsdigitorum communis (EDC).

FIGURE 2. Normalized maximal forces (A) and FDS/EDC cocon-traction ratio (B). Mean and standard error bars are presented.The MVC force (FMVC) increases significantly from forced inspi-ration (MVCI) to forced expiration (MVCE). Both MVCE and MVCI

lead to increased FDS/EDC cocontraction ratio. The Valsalvamaneuver (MVCE) has no significant effect on the MVC force ormuscle cocontraction ratio.

Short Reports MUSCLE & NERVE November 2006 653

To our surprise, we did not observe a significanteffect of the Valsalva maneuver on FMVC or FDS/EDC cocontraction ratio. This may relate to the factthat small muscles were tested, because a Valsalvamaneuver is usually performed when large musclesare involved during strength training. Our resultsnevertheless contribute to a better understanding ofthe functional consequence of this maneuver. Theabsence of significant changes in the FDS/EDC co-contraction ratio implies that proportional changesoccur in flexor/extensor contraction, which maymaintain stability in the wrist and metacarpalphalan-geal and interphalangeal joints during the course ofthe Valsalva maneuver. In contrast to the significantincreases occurring in the FDS/EDC ratio duringforced expiration and inspiration, the preservedjoint stability could be an advantage of the Valsalvamaneuver, allowing subjects to produce a stableMVC output over a relatively long period of time,such as when lifting a heavy object.

Forced inspiration and expiration is synchro-nized with enhanced respiratory-related neuronalactivity at many cortical sites, including the primarymotor cortex, premotor cortex, and supplementarymotor area.4,5,16 It is likely that such enhanced neu-ronal activities in the motor cortex act in concertwith the motor drive to the exercising, nonrespira-tory skeletal muscles (for review, see Guz7). Thisrespiratory–motor enhancement mechanism couldexplain, in part, the obtained results, such as signif-icant increases in FMVC during MVCE. Significantincreases in the FDS/EDC ratio could also be attrib-uted to transient increases in respiratory-related neu-ronal activity favoring exercising finger flexors, re-sulting in disproportional increases in activation forfinger flexors. As such, initiation of forced inspira-tion and expiration exerted a considerable impact atthe initial phase of force production, that is, theinitial force peak (Fig. 1B and C).

In addition to the proposed respiratory–motorenhancement mechanism, we propose an expira-tion–flexion inspiration–extension coupling hypoth-esis to explain otherwise contradictory results of noeffect on FMVC during MVCI. According to this hy-pothesis, inspiration facilitates finger extension andinhibits finger flexion. During finger-flexion MVCattempts, inspiration-imposed inhibition on maxi-mal finger flexion is balanced by the respiratory-related overall increase in cortical activities due tothe aforementioned mechanism, with the net resultof no change in FMVC. Expiration-imposed facilita-tion is likely to integrate with the expiration–flexioncoupling effect, resulting in significant increases inmaximal finger flexion force. This hypothesis is pro-

posed based on published evidence indicating thatforceful respiration influences the motor drive. Forinstance, resistive loaded inspiration significantly en-hanced tonic vibratory response in the extensor digi-torum,2 but did not affect contraction of biceps bra-chialis.6 Further evidence is required to corroboratethis hypothesis.

The study was supported in part by start-up funds (S.L.) from theUniversity of Montana. The authors thank Professor V. M. Zatsi-orsky, Pennsylvania State University, and Professor C. T. Leonard,University of Montana, for their valuable comments.

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