Articles in PresS. J Appl Physiol (May 9, 2013). doi:10.1152/japplphysiol.00333.

2013

Contribution of central vs. peripheral factors to the force loss

induced by passive stretch of the human plantar flexors.

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Gabriel S. Trajano1, Laurent Seitz1, Kasunori Nosaka1 and Anthony J. Blazevich1

1 Centre for Exercise and Sports Science Research (CESSR), School of Exercise and Health

Sciences, Edith Cowan University, Australia.

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Running title: Central vs. peripheral factors on stretch-induced force loss

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Keywords: muscle stretch; muscle activity; excitation-contraction coupling

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Corresponding author:

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Anthony J. Blazevich

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Centre for Exercise and Sports Science Research (CESSR)

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School of Exercise and Health Sciences, Edith Cowan University

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270 Joondalup Drive, Joondalup, WA 6027, AUSTRALIA.

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Email: a.blazevich@ecu.edu.au

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Copyright 2013 by the American Physiological Society.

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ABSTRACT

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The purpose of the present research was to indentify the contribution of central vs. peripheral

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factors to the force loss after passive muscle stretching. Thirteen men randomly performed

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both a 5-min constant-torque stretch of the plantar flexors on an isokinetic dynamometer and

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a resting condition on two separate days. The triceps surae electromyogram (EMG) was

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recorded simultaneously with plantar flexor isometric torque. Measures of central drive,

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including the EMG amplitude normalized to the muscle compound action potential amplitude

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(EMG:M), percent voluntary activation (%VA) and first volitional wave amplitude (V:M),

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and measures of peripheral function, including the twitch peak torque, 20:80 Hz tetanic

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torque ratio and torque during 20 Hz stimulation preceded by a doublet, were taken before,

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and immediately and 15 min after each condition. Peak torque (-15.7%), EMG:M (-8.2%),

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and both twitch (-9.4%) and 20 Hz (-11.5%) peak torques were reduced immediately after

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stretch but recovered by 15 min. There were strong correlations between the torque loss and

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the reductions in central drive parameters (r=0.650.93). Torque recovery was also strongly

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correlated with the recovery in EMG:M and %VA (r=0.770.81). The moderate decreases in

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measures of peripheral function were not related to the torque loss or recovery. These results

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suggest that: 1) central factors were strongly related to the torque reduction immediately after

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stretch and during torque recovery; and 2) the muscles contractile capacity was moderately

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reduced, although these changes were not associated with the torque reduction and changes in

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E-C coupling efficiency were not observed.

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INTRODUCTION

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Prolonged (60 s) passive muscle stretch reduces maximal force production in human

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muscles (25). However the mechanisms underpinning this loss have not been fully elucidated

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and effective strategies for minimizing the force loss have not been developed. A post-stretch

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decrease in central (efferent) drive to the muscles has been considered to affect force

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production, evidenced by the reductions in electromyogram (EMG) amplitudes that are often

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observed (18, 27). However the EMG signal can be affected by peripheral factors, including

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changes in muscle fiber action potential amplitude and propagation velocity (3, 16), so

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factors other than central drive limitations could also explain these results.

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To better quantify changes in central drive other techniques could be used, including

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normalization of EMG amplitudes to the maximal muscle compound action potential (Mmax)

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amplitude (3), the use of the interpolated twitch technique to estimate percent voluntary

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activation(33, 40) and the measurement of V-wave amplitudes during maximum voluntary

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contractions (41). On the other hand, each of these measures is also considered potentially

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imperfect in some way (1, 3, 16, 40), so strong evidence for a central drive limitation

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subsequent to muscle stretch might only be indicated when a depression is observed in

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several simultaneously-obtained measures, and these depressions are related to (i.e. correlated

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with) the loss of force. As yet, such a detailed examination has not been completed so it is not

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clear whether a reduction in central drive is a key mechanism underpinning the force loss.

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In addition to central factors, peripheral factors might influence the loss of force after stretch.

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For example, research using animal models has shown that passive muscle stretch can

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increase intracellular calcium concentration via stretch-activated channel activation

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disturb calcium homeostasis (4). Such a disturbance can negatively affect the synergistic

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interaction

between

the

and

calcium-release ryanodine receptor and voltage-sensitive

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dihydropyridine receptors, impairing excitation-contraction (E-C) coupling (6). In humans it

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is possible to estimate the efficiency of this process by comparing the torque produced during

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low- vs. high-frequency electrical motor nerve stimulation trains (23, 32). In fact, it is also

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reasonable to expect changes in a muscles response to short-interval double-spike stimuli

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when they precede a train of constant-frequency stimuli (i.e. a catch-inducing train) (7, 11)

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if calcium homeostasis is disrupted, because this response is thought to be influenced by the

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Ca2+ binding sensitivity to troponin (2, 35). Thus, decreases in force production might occur

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even if no significant changes in central drive are produced and no metabolic disturbances are

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elicited. To date, the effect of static muscle stretch on muscle contractile properties remains

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relatively unexplored, so it is not clear if these are potential targets for intervention.

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Given the above, the purpose of the present study was to establish the relative contribution of

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central vs. peripheral factors to the stretch-induced force loss after a 5-min continuous

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passive plantar flexor muscle stretch. We tested the hypothesis that impairments would be

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detected at both central and peripheral levels, and that these changes would be similarly

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correlated with changes in muscle force production. Three different examinations of central

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drive were completed (EMG:M ratio, percent voluntary activation [interpolated twitch

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technique; ITT] and V-wave amplitude) in order to more robustly quantify potential central

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changes, whilst muscle and nerve stimulation procedures were used to gain information with

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regards to peripheral changes.

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METHODS

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Subjects

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Thirteen healthy men (mean SD: age, 26.5 5.0 yr; height, 1.72 0.9 m; body mass, 71.1

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13.8 kg) with no previous neuromuscular impairment volunteered for the study. The subjects

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reported not being engaged in flexibility training for at least 6 months prior to the study and

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refrained from such training during data collection period. The procedures performed during

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this research were approved by the Edith Cowan University Human Research Ethics

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Committee and were in agreement to the Declaration of Helsinki. All participants read and

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signed an informed consent document.

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Study design and overview

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Subjects visited the laboratory on three occasions at the same time of day separated at least

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by 48 hours. A full familiarization of the stretch protocol and test procedures was provided in

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the first session whilst the subsequent two visits were used for the completion of the

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following experimental conditions in a randomized order: 1) control (or no stretch), and 2) 1

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set of 5 min passive plantar flexor stretching. The subjects were assessed immediately before,

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and immediately and 15 minutes after each intervention (Figure 1). During familiarization the

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muscle stimulation intensities for all electrically evoked measurements were determined and

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both the maximum tolerable passive torque during stretch and the maximal voluntary

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contraction torque (MVC) were measured. In the experimental trials, the subjects performed a

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warm-up on a Monark cycle for 5 min by cycling at 60 rpm with a 1-kg load to produce a

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power output of 60 W. The subjects were then seated upright in the chair of an isokinetic

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dynamometer (Biodex System 3 Pro, Biodex Medical System, Shirley, New York, USA) with

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the knee fully extended (0), the ankle in the neutral position (90) with the sole of the foot

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perpendicular to the shank, and the lateral malleolus aligned to the centre of rotation of the

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dynamometer. We placed the knee in an extended position to better assess the full plantar

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flexor torque (13), minimize the risk of muscle cramp during muscle stimulation and to allow

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for muscles to be more completely stretched during the muscle dorsiflexion rotations (i.e.

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plantar flexor stretches).

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Muscle Stretching Protocol

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All stretch procedures were performed on an isokinetic dynamometer with the muscles

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relaxed. The plantar flexors were stretched for 5 min by rotating the ankle into dorsiflexion at

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5s-1 until a passive resistance equal to 90% of the maximal tolerable stretch torque (assessed

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during familiarization) was achieved. Muscle stretch elicits a viscoelastic stress relaxation

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response, resulting in a rapid reduction in stretch intensity when the joint position is held

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constant (31). In order to avoid this response, the joint angle was continually adjusted

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(increase of dorsiflexion) so that the passive torque always remained within 5 Nm of the

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initial stretch torque level. Standard stretching practices are somewhat analogous to the

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constant torque design so the present results should be of practical significance.

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Voluntary and Evoked Torque Measurements

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Peak isometric plantar flexor torque (TPeak) was assessed during MVCs with the ankle in a

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neutral position (90). Maximal force is usually reduced by the anticipation of discomfort

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caused by the electrical stimulation (12). To avoid the effect of stimulus anticipation two

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MVCs were performed at each time point: the first MVC was used to calculate TPeak and

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measure muscle activity (EMG; see below), the second MVC included tibial nerve

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stimulation in order to measure muscle activation (ITT) and V-wave amplitude (Figure 1).

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Participants were instructed to produce a force against the dynamometer by rotating foot plate

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the ankle as fast and as hard as possible. Verbal encouragement and visual feedback were

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provided during all MVCs.

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Stimulation procedures

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Muscle Stimulation (20:80 ratio, constant vs. catch-inducing train stimulation)

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A constant current electrical stimulator (DS7, Digitimer Ltd, Welwyn Garden City, UK) was

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used to deliver an electrical square-wave stimulus (0.5-ms pulse width) to the plantar flexor

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muscle belly through two self-adhesive electrodes (9 5 cm, Dura-Stick II, Chattanooga

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Group, Hixon, USA). The cathode was placed distal to the popliteal crease and the anode

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over the distal myotendinous junction of the soleus. For all tetanic stimulations, the intensity

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necessary to reach 50% of MVC with a 0.5-s 80 Hz tetanic stimulation was used. Three

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tetanic stimulations with the same duration were delivered to test for E-C coupling efficiency:

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1) 20 Hz train of 11 pulses (0.05 s interpulse interval); 2) catch-inducing train (i.e. 2 pulses at

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0.01 s plus 10 pulses at 0.05 s interpulse interval); and 3) 80 Hz train of 36 pulses (0.0125 s

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interpulse interval). The peak torque produced by the 20 Hz and 80 Hz stimulations were

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used to calculate the 20:80 ratio, which was used as a measure of E-C coupling efficiency

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(32). The catch-inducing train was used to assess the muscles capacity to increase force

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production under this specific condition, when compared to a constant-frequency train

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(20:catch ratio).

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Nerve Stimulation (Twitch, ITT, V-wave)

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The same electrical stimulator was used to deliver the electrical square wave 1-ms pulse

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width stimuli to the posterior tibial nerve via a cathode electrode (Ag-AgCl, 10 mm) fixed to

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the popliteal fossa and an anode electrode of large size (9 5 cm, Dura-Stick II,

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Chattanooga Group, Hixon, USA) placed on the anterior surface of the knee. ITT was used to

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estimate the percentage voluntary activation (%VA) of the muscle. The intensity for a single

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twitch was set at 120% of the intensity required to elicit Mmax, to ensure a supramaximal

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current stimulus was used. Supra-maximal twitches were elicited before, during and 2 s after

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an isometric plantar flexor MVC (33). A comparison of the interpolated twitch to the resting

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potentiated (i.e. post-MVC) twitch was completed, with %VA being calculated using the

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equation (39):

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%VA = [1-(superimposed twitch/potentiated twitch)] 100.

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The superimposed twitch was also used to capture the V-wave; decreases in amplitude were

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considered as evidence of a decrease in efferent drive to the motor neuron (1). Although,

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multiple assessments are ideal to improve the methods reliability, only one stimulation was

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provided at each time point in order to minimize the effects of fatigue. Thus, the balance

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between an optimum number of stimulations and the minimization of muscle fatigue was

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considered. The V-wave peak-to-peak amplitude was measured and then normalized to the

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M-wave amplitude measured prior to the MVC (V:M ratio).

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Measurement of muscle activity (EMG)

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Surface EMG was recorded from soleus and lateral gastrocnemius using a bipolar electrode

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configuration at a 4000 Hz analogue-digital conversion rate (bandwidth 10 to 500 Hz) using

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the Bagnoli-8 Main Unit EMG system (DelSys, Inc., MA, USA). The inter-electrode distance

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was 1 cm and a reference electrode was placed on the lateral malleolus. Further, to obtain

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clearer M- and V-wave data, surface EMG was recorded from soleus in a pseudo-monopolar

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configuration (sample rate 4000 Hz) using the BioAmp EMG system (PowerLab System,

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ADInstruments, NSW, Australia), with one electrode placed on the medial aspect of soleus

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below the distal gastrocnemius junction and the other placed at the Achilles tendon-soleus

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muscle-tendon junction 3 cm superior to the malleolus (9). The skin under the electrodes

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was shaved, abraded and cleaned with alcohol to reduce the inter-electrode resistance below 5

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k. EMG data were also recorded during the stretching maneuvers to ensure that muscle

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activation remained below 5% of the maximal value; a small activity response is often seen

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even when the subjects are asked to remain completely relaxed (8). Muscle activity was

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expressed as root mean square EMG amplitude (500-ms averaging window) and normalized

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to the M-wave amplitude measured before the contraction (EMG:M) to account for the

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possible influence of peripheral factors. The EMG:M quantified from SOL (EMG:MSOL) and

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LG (EMG:MLG) were summed and considered as a measure of neural efferent drive to the

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triceps surae (EMG:MTS). Ankle joint torque, joint angle and EMG data were simultaneously

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recorded using LabChart v.6.1.3 Software (PowerLab System, ADInstruments, NSW,

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Australia).

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Statistical analysis

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Separate two-way repeated measures ANOVAs were performed to compare changes in all

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variables between conditions (stretch vs. control) over time (before, after and 15 min after).

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Pairwise comparisons with Bonferroni corrections were performed when significant

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interaction effect was detected. Pearsons product-moment correlation coefficient were

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computed to determine the relationships between changes in torque and changes in central

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(EMG:M; %VA; V-wave) and peripheral (20:80 ratio, 20:catch ratio, peak twitch torque)

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mechanisms. Statistical significance was set at an level of 0.05.

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RESULTS

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There was a significant interaction (time condition) effect for Tpeak (p<0.05). Post-hoc

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analyses revealed a significant reduction of 15.7% immediately after stretch with no

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significant difference from the baseline being found at 15 minutes, and no changes in the

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control condition (Figure 2).

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Similarly, a significant interaction effect was found for EMG:MSOL (p<0.05) and EMG:MTS

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(p<0.05). Post-hoc analyses revealed a reduction of 13.2% for EMG:MSOL and 8.2% for

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EMG:MTS immediately after stretch but no difference at 15 min, indicating that EMG:M was

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fully recovered by 15 min. Both %VA and V:M ratio were not significantly different to the

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control condition at any time point (Table 1).

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There were moderate-strong correlations between changes in torque and changes in central

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drive measurements, including EMG:MSOL (r=0.93, p<0.001), EMG:MLG (r=0.82, p=0.001),

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EMG:MTS (r=0.88, p<0.001), as well as %VA (r=0.76, p=0.002) and V:M ratio (r=0.65,

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p=0.017) immediately after stretch (Figure 3). Thus, greater decrements in torque were

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observed in subjects who had greater reductions in measures of central drive. Interestingly,

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the recovery of peak torque within 15 min of stretch (Figure 4) was also correlated strongly

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with EMG:MSOL (r=0.81, p=0.001), EMG:MLG (r=0.79, p=0.001), EMG:MTS (r=0.80

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p=0.001) and %VA (r=0.77, p=0.003) recovery. These results indicate that a similar temporal

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response occurred in torque production and central drive.

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There was a significant interaction effect for torque elicited by the 20 Hz, catch-inducing

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train and twitch peak torque (Tpeak) (p<0.05). Post-hoc analyses revealed that reductions in

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peak torque in response to 20 Hz (11.5%), catch-inducing (10.8%) and twitch (9.4%)

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stimulations occurred only immediately after stretch, with no further change to 15 min. There

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was a trend towards a reduction in torque elicited by 80 Hz stimulation (p<0.1), but no

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significant interaction effect was found. In addition, no interaction effect or correlation was

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found for 20:80 (p>0.05) or 20:catch (p>0.05) ratios, suggesting that muscle force production

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was affected somewhat by the stretch protocol, but it could not be explained by changes in E-

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C coupling efficiency. There were no changes in Mmax amplitude detected, when compared to

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the control condition (p>0.05), indicating that muscle excitability was not affected by the

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stretch protocol (Table 1).

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DISCUSSION

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The present research examined the contributions of central vs. peripheral factors to the

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stretch-induced force loss in the human plantar flexors. The main findings were that: 1)

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decreases in EMG:M, voluntary activation and V-wave amplitude (i.e. central factors) were

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strongly related to both the torque reduction after stretch and the torque recovery, indicating

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that central drive modification influenced the loss and recovery of muscle force; and 2) the

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muscles contractile capacity was moderately reduced, but these changes were not associated

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with the loss or recovery of torque and there was no evidence of a change in E-C coupling

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efficiency after the stretch protocol utilized in the present study.

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The present data provide the clearest evidence of a reduced central drive influencing force

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production after stretch. As shown in Figure 1, three different parameters (EMG:M, %VA

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and V-wave) were investigated in order to detect central changes, and reductions in these

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parameters were strongly correlated with reductions in torque after stretch. Moreover,

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recovery of EMG:M and %VA were strongly correlated with force recovery, suggesting that

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recovery of efferent drive may have been important in the return of muscle force to baseline.

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It has been suggested that the force reduction might be caused by a decrease in central drive

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because decreases in EMG amplitude have been reported and relationships between changes

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in EMG amplitudes and changes in torque have been demonstrated (18, 27). However, EMG

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amplitude can be influenced by peripheral, in addition to central, factors so some caution was

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exercised in the interpretation of these results. Although the EMG:M ratio, as measured in

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the present study, can still be influenced by factors other than the absolute magnitude of

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central drive (e.g. motor unit synchronization), the simultaneous depression of voluntary

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activation and V-wave amplitude is strongly suggestive of a central depression, and the

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correlations between EMG:M, voluntary activation and the torque recovery to 15 min

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provides substantial additional support for the hypothesis (Figure 3). Thus, the findings of

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the present study strongly support the proposition that a reduced central drive is a major

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factor contributing to the torque loss caused by acute passive muscle stretch.

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From the current data it is not possible to determine the site/s of origin of the central drive

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limitation. Descending output from the motor cortex can exert significant executive control

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over muscle force so changes in supraspinal command are clearly a potentially important

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factor. To the best of our knowledge there is no clear evidence that muscle stretching can

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affect supraspinal outflow, however this possibility is particularly worthy of exploration

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because the mild pain response elicited by the stretch might have been sufficient to reduce

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motor cortical drive to the muscle (28, 37) and thus reduce motor unit firing frequency (14,

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15). Studies imposing muscle stretch whilst pharmacologically blocking the pain response

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may be useful in testing this hypothesis. Spinal-level inhibition is also a candidate site for

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examination. Spinal interneurons can modulate both Ia afferent feedback and motor neuron

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excitability through inhibitory and excitatory mechanisms (22). In particular, the soleus Ia

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inhibitory interneuron is thought to be excited by both agonist and synergist Ia afferents (17,

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38). Thus, the stretch protocol used in the present experiments may have promoted an

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autogenic inhibition of soleus and a subsequent decrease in its activity level. Finally, motor

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neuron disfacilitation is a possible mechanism. Alpha motor neurons are strongly dependent

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upon facilitatory inputs to achieve maximal discharge frequency, and thus to produce high

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levels of muscular force (20). This facilitatory modulation occurs at the motor neuron

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dendrites and is controlled by the interaction between descending monoaminergic drive and

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spinal circuits, especially including the Ia afferents (19). For instance, changes in muscle

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length directly affect the level of dendritic amplification to the motor neuron (21), so the

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prolonged increase in muscle length during the stretch may have reduced Ia afferent input

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onto -motor neuron. Indeed, a reduction in Ia afferent efficiency (measured as decrease in

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H-reflex amplitude) concomitant with a decrease in force has previously been reported

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immediately after prolonged passive stretching (5); a reduction in Ia afferent input could

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affect the motor neuron facilitatory process preventing maximal discharge rates being

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attained during force production. Interestingly, both the H-reflex amplitude and maximal

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force production were shown to recover within 15 minutes of the stretch (5). The temporal

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match with our data is suggestive that central drive might be reduced immediately after

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stretch, and then recover relatively rapidly and simultaneously with force.

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In the present study we also tested, for the first time, the hypothesis that passive stretch could

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affect E-C coupling efficiency by comparing the torque produced during low- and high-

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frequency tetanic stimulation. Reductions in tetanic torque were evident in 20 Hz and catch-

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inducing tetanic stimulation conditions, suggesting that the muscles contractile capacity was

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compromised. However, these reductions were relatively small and were not correlated with

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the changes in peak torque. Moreover, the lack of changes in 20:80 and 20:catch ratios

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suggest that calcium homeostasis was not affected significantly by the present stretch

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protocol and that any small changes in muscle or tendon mechanical properties also did not

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specifically influence torque induced by the high-frequency pair of pulses during the catch-

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inducing train. Additionally, no change in Mmax amplitude was found, indicating that

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sarcolemmal and t-tubular function was not significantly compromised. One might speculate

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that the moderate changes in muscle function could result from mechanical changes within

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the parallel elastic component. It has been proposed that parallel elastic components are

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responsible for epimuscular force transmission, which is an important factor contributing to

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maximal force production (29, 30), and connective tissues such as the perimysium might be

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affected by static muscle stretch (10, 36). Clearly, changes in the series elastic components,

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and particularly the Achilles tendon, are unlikely to have had a substantial influence (24, 26,

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27, 34). Regardless, the moderate changes in muscular function did not appear to have a

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notable effect on torque production in this study.

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With respect to the current data, some limitations should be highlighted. This study was

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designed to investigate the mechanisms underpinning the force loss, so a relatively long

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stretch duration was employed (5 min). However, short duration stretches (< 45 s), which are

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commonly performed in pre-exercise routines, are unlikely to negatively affect force

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production. Thus, it is possible that the neuromuscular changes observed in the present study

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would not be observed under shorter stretch conditions. Nonetheless, further research is

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needed to clarify the dose-response relationship between stretch duration and central drive

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depression. Second, mechanical properties of the muscle (e.g. changes in parallel elastic

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components) could not be measured, but may have influenced muscle force production

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without affecting the E-C coupling process. Further research is required to clearly determine

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the effects of changes in the mechanical properties of in particular, the parallel elastic

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components on neuromuscular measurements and whether muscle stretch might influence

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these. Third, using the present methodology we were unable to determine the site/s of origin

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of the central drive limitation. Research using brain imaging and cortical brain stimulation

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techniques could provide a clearer picture in this regard.

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In summary, the present data indicate that the torque decrement elicited by passive plantar

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flexor muscle stretch was strongly associated with a reduction in central (efferent) drive. This

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conclusion is based on the significant decrease and recovery of the EMG:M ratio, the strong

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correlation between the torque loss and decreases in EMG:M, %VA and V:M, and the

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association of torque recovery with EMG:M and %VA recovery; further research is required

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to determine the specific location of the central drive modification. The stretch protocol may

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have induced a deficit at the muscular level, however changes were not substantial and were

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not correlated with the torque loss or recovery. Notwithstanding the clear loss of force

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induced by the stretch, it is also important to note, from a practical perspective, that torque

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recovered quickly and certainly within 15 minutes. These changes occurred in response to 5-

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min muscle stretch and future studies should determine if shorter durations of stretch impair

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maximal force by the same mechanisms.

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Disclosures: The authors have no conflicts of interests to disclose. This research was funded

451

by the Edith Cowan University PhD fund.

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Table 1. Muscle activation and torque data (mean SD) before, and immediately and 15 min

454

after stretch. * Indicates changes significantly different from control group (p 0.05).

455
456

Figure 1. A: The experimental design and time course of measurements: subjects were

457

assessed before, and immediately and 15 minutes after the stretch or control (rest) period. B:

458

the order of measurements (20 Hz, 20 Hz tetanic stimulation; catch, catch-inducing tetanic

459

stimulation; 80 Hz, 80 Hz tetanic stimulation; MVC, maximal voluntary contraction; Twitch,

460

single pulse stimulation)

461

Figure 2. Torque loss immediately and 15 min after stretch. * Significantly greater change

462

compared to the control condition (p 0.05).

463

Figure 3. Relationship between changes in torque and changes in indicators of central drive.

464

A strong correlation was found between the reduction in torque and decreases in A) the

465

soleus EMG:M ratio (r=0.93), B) percent voluntary activation (%VA; r=0.76), and C) V-

466

wave amplitude (V:M ratio; r=0.65). Force recovery was also strongly correlated with

467

recovery of D) the soleus EMG:M ratio (r=0.81) and E) %VA (r=0.77). The correlation

468

between the change in torque during recovery and changes V-wave amplitude (F) was not

469

statistically significant. Force loss = changes in torque from baseline to immediately after

470

stretch; Force recovery = changes in torque from immediately to 15 min after stretch.

471

Figure 4. Example of data obtained from one subject before (left column), and immediately

472

(middle column) and 15 min after (right column) the stretch protocol. A decrease in maximal

473

voluntary contraction (MVC) torque (first row), EMG amplitude (second row) and V wave

474

amplitude (last row), and an increase in the superimposed twitch torque (i.e. decreased

475

voluntary activation; third row) are visible immediately after stretch. (ITT; interpolated

476

twitch technique)

A
Before

Stretch

After

15 min

Control

B
60 s
30 s

30 s

60 s

Immediately after

15 min after

Tpeak (%)

-10

-20
Stretch
Control

-30

*
-40

EMG/M (%)

40

Force Recovery

100

50

-40

R = 0.85

-80
40

VA (%)

Force Loss

R = 0.66

-50

60

30

-40

R = 0.58

V:M ratio

-80
0.6

R = 0.49
-30
0.6

0.3

0.3

0.0

0.0

-0.3

R = 0.45
-60

-40

-20

-0.3
0

-20

torque (%)

20

40

60

Immediately
after

EMG (mV)

MVC (Nm)

Before

Rectified EMG
RMS EMG

V-wave (mV)

ITT (Nm)

Superimposed Twitch
Potentiated
Twitch

M wave
V wave

15 min after

Control

Stretch

Before

Immediately
after

15 min after

Before

Immediately
after

15 min after

Tpeak (Nm)

171.6 37.1

167.5 37.5

171.2 46.9

181.2 44.4

150.5 49.6*

175.1 40.1

EMG:MSOL

0.058 0.05

0.062 0.06

0.065 0.06

0.053 0.03

0.041 0.02*

0.048 0.02

EMG:MLG

0.114 0.05

0.127 0.06

0.121 0.05

0.094 0.05

0.087 0.05

0.105 0.06

EMG:MTS

0.17 0.09

0.19 0.1

0.19 0.1

0.15 0.06

0.13 0.07*

0.15 0.06

VA (%)

96.4 1.6

96.6 2

96.5 2.2

96.9 1.7

86.5 20.7

96.5 4.6

V:M

0.24 0.13

0.21 0.11

0.23 0.09

0.22 0.11

0.25 0.18

0.23 0.12

Twitch (Nm)

25.2 4.9

24.5 5.5

23.6 5.3

26.7 5.5

24.4 6.7*

25.0 6.6

20 Hz (Nm)

66.8 13.5

65.9 14.9

63.7 15.8

67.7 13.5

60.1 15.0*

62.1 13.5

Catch (Nm)

69.8 14.4

68.5 15.6

66.0 16.9

69.9 14.6

62.5 15.2*

64.8 13.3

80 Hz (Nm)

94.7 21.9

95.5 25.4

94.8 28.4

93.6 19.8

87.5 19.7

91.2 18.5

Mmax (mV)

26 7.1

25.4 6.4

25.6 6.9

25.1 7.8

23.7 8.5

25.0 7.8

20:80 ratio

0.71 0.04

0.70 0.04

0.68 0.05

0.73 0.04

0.68 0.05

0.68 0.06

20:catch ratio

0.96 0.02

0.96 0.02

0.97 0.03

0.97 0.02

0.96 0.03

0.96 0.03

Tpeak, peak torque during maximal voluntary contraction; EMG:M, EMG-to- Mmax amplitude, SOL, soleus;
LG, lateral gastrocnemius; TS, triceps surae; VA, voluntary activation; V:M; ratio between V-wave-to-Mmax
amplitude; Twitch, peak twitch torque; 20 Hz, peak torque during 20 Hz tetanic stimulation; Catch, peak
torque when 20 Hz is preceded by short-interval doublet; 80 Hz, peak torque during 80 Hz stimulation;
Mmax, maximal M-wave amplitude; 20:80 ratio, ratio between 20 Hz and 80 Hz; 20:catch ratio, ratio between
20 Hz and catch.