Share this article on:

Etiology and Recovery of Neuromuscular Fatigue after Simulated Soccer Match Play


Medicine & Science in Sports & Exercise: May 2017 - Volume 49 - Issue 5 - p 955–964
doi: 10.1249/MSS.0000000000001196
Applied Sciences

Purpose: We profiled the etiology and recovery of neuromuscular fatigue after simulated soccer match play.

Methods: Fifteen semiprofessional players completed a 90-min simulated soccer match. Before, immediately after, and at 24, 48, and 72 h, participants completed a battery of neuromuscular, physical, and perceptual tests. Perceived fatigue and muscle soreness were assessed via visual analog scales. Maximum voluntary contraction (MVC) and twitch responses to electrical (femoral nerve) and magnetic (motor cortex) stimulation during isometric knee extensor contractions and at rest were measured to assess central (voluntary activation) and peripheral (quadriceps potentiated twitch force, Qtw,pot) fatigue, and responses to single and paired magnetic stimuli were assessed to quantify corticospinal excitability and short intracortical inhibition, respectively. Countermovement jump, reactive strength index, and sprint performance were assessed to profile the recovery of physical function.

Results: Simulated match play elicited decrements in MVC that remained unresolved at 72 h (P = 0.01). Central fatigue was prominent immediately postexercise (−9% reduction in voluntary activation) and remained depressed at 48 h (−2%, P = 0.03). Qtw,pot declined by 14% postexercise, remained similarly depressed at 24 h, and had not fully recovered 72 h after (−5%, P = 0.01). Corticospinal excitability was reduced at 24 h (P = 0.047) only, and no change in short intracortical inhibition was observed. Measures of jump performance and self-reported fatigue followed a similar time course recovery to neuromuscular fatigue.

Conclusion: Central processes contribute significantly to the neuromuscular fatigue experienced in the days after soccer match play, but the magnitude and slower recovery of peripheral fatigue indicates that it is the resolution of muscle function that primarily explains the recovery of neuromuscular fatigue after soccer match play.

1Faculty of Health and Life Sciences, Northumbria University, Newcastle upon Tyne, UNITED KINGDOM; and 2Water Research Group, School of Environmental Sciences and Development, Northwest University, Potchefstroom, SOUTH AFRICA

Address for correspondence: Kevin Thomas, Ph.D., Faculty of Health and Life Sciences, Department of Sport, Exercise and Rehabilitation, Northumbria University, Newcastle upon Tyne, NE1 8ST, United Kingdom; E-mail:

Submitted for publication October 2016.

Accepted for publication December 2016.

Supplemental digital content is available for this article. Direct URL citations appear in the printed text and are provided in the HTML and PDF versions of this article on the journal’s Web site (

Association football (soccer) is an intermittent sprint sport that places significant physical demand on players (1,31). An inevitable consequence of this physical demand is fatigue, a debilitating symptom that manifests in negative physiological, functional, and perceptual outcomes, which can persist in the days postexercise (26). For example, marked changes in biochemical factors indicative of exercise-induced muscle damage persist for at least 72 h postmatch (17,25), and decrements in physical performance considered to reflect neuromuscular function (maximum voluntary contraction [MVC] force, vertical jump height, and sprint speed) are present postmatch and for 24–96 h thereafter (17,26,31). The physiological consequences of fatigue in the days after soccer match play have typically been studied at a peripheral level, with recovery of impairments in skeletal muscle function (termed “peripheral fatigue”) the primary concern (17,26). The level at which fatigue-induced changes present along the motor pathway can also be central in origin, reflected in a reduction in the capacity of the central nervous system (CNS) to activate skeletal muscle (termed “central fatigue”). Few studies have assessed the contribution, and recovery, of central fatigue after soccer match play. The prolonged reduction in soccer performance measures that are thought to reflect neuromuscular function (17,26,31), and a disconnect in the temporal pattern of recovery of voluntary force compared with markers of exercise-induced muscle damage (24,30), suggests a contribution of central processes to fatigue after soccer match play (23,32). Although the evidence supporting this posit is limited, one study has demonstrated reductions in voluntary activation (VA), using motor nerve stimulation and a measure of central fatigue, for up to 48 h after soccer match play (31). In addition, VA was shown to be depressed after just two repetitions of a repeated-sprint running protocol (12 × 30 m), reaching a nadir after sprint 10 (13). These studies suggest that the recovery of the impairments in the CNS function is likely to contribute to the recovery of physical performance after soccer match play, but there remains a paucity of data to substantiate this premise (23).

The application of transcranial magnetic stimulation (TMS) to assess the CNS function could potentially reveal new information on the etiology of central fatigue induced by intermittent exercise. The stimulation of motor cortical cells in single- and paired-pulse paradigms elicit motor evoked potentials (MEP) in the muscle of interest, the characteristics of which can be studied to quantify the excitability of the brain-to-muscle pathway, and the status of inhibitory intracortical neurons (9). Single-pulse TMS has been previously used to demonstrate acute and chronic modulations in corticospinal excitability as a result of resistance training (4,29,45), single-limb submaximal (46) and maximal (6) muscle actions, and whole body locomotor exercise (37). Paired-pulse TMS has previously revealed changes in intracortical activity (specifically the activity of gamma-aminobutyric acid type A–mediated inhibitory interneurons) in response to resistance exercise (45,47), fatiguing single-limb contractions (21), and locomotor exercise (38). Collectively, these data demonstrate that the use of single- and paired-pulse TMS paradigms has the potential to provide novel information on the neurophysiological basis of fatigue and recovery from intermittent exercise (23,32).

A better understanding of the etiology of neuromuscular fatigue could assist in the management of the training and recovery process in soccer, an area of particular importance given that the congested competitive schedules and the subsequent accumulation of fatigue in players have been linked with an increased incidence of injury (7,11). Accordingly, the primary aim of this study was to profile the etiology and recovery of neuromuscular fatigue, quantified with laboratory based tests, after simulated soccer match play. A secondary aim of the study was to study the time course recovery of a range of simple measures of physical and perceptual function to provide information on the appropriateness of these tools as markers of a players readiness to train and compete. We hypothesized that soccer match play would induce significant neuromuscular fatigue, both central and peripheral in origin, which would persist in the days postexercise and be concurrent with decrements in physical function.

Back to Top | Article Outline



After ethical approval from the Northumbria University Faculty of Health and Life Sciences Ethics committee, 15 male soccer players gave written informed consent to participate (age = 21 ± 1 yr, stature = 1.83 ± 0.07 m, mass = 77 ± 9 kg, predicted maximum oxygen uptake = 55.0 ± 2.9 mL·kg−1·min−1). All participants were current players with teams at Level 9 of the Football Association soccer league system, a semiprofessional league consisting of 22 teams in the Northern region of England. The participant's competitive season ran from August to May, where teams play 42 league games and compete in five knockout domestic cup competitions (three local and two national). Consequently, teams at this level will typically play 50–60 competitive matches for a season, and periods of fixture congestion (where two to three matches are scheduled per week, separated by 48–96 h) are frequent. Testing took place in the late off-season to early preseason phase of the players training year (n = 12) and midseason (n = 3).

Back to Top | Article Outline


Participants first completed two practice trials for habituation to the measurement tools of the study and a preliminary assessment of aerobic fitness. The experimental trial required participants to visit the laboratory on four consecutive days, separated by 24 h. On the first day, participants completed a simulated soccer match protocol on an indoor synthetic track, in a temperature-controlled environment (ambient temperature = 18°C ± 1°C, relative humidity = 38% ± 6%). Before, immediately after, and on subsequent days at 24, 48, and 72 h postexercise, participants completed a series of assessments to measure neuromuscular, physical, and perceptual function to ascertain the time course recovery of these variables after the simulated soccer match (see Figure, Supplemental Digital Content 1, Schematic of experimental protocol, Participants were instructed to avoid food (>2 h), caffeine and alcohol (>24 h), and strenuous exercise (>48 h) before the first visit and were instructed to refrain from caffeine, alcohol, and any exercise other than that completed for the study for the duration of their participation.

Back to Top | Article Outline


Practice trials

Participants visited the laboratory on two separate occasions for practice trials. On both occasions, after a standardized 10-min warm-up, participants were habituated to all of the neuromuscular, functional, and perceptual measures used in the study (described in the next section). Subsequent to this on the first practice trial, participants completed the multistage fitness test to measure aerobic fitness and to determine appropriate intensities for the simulated soccer match protocol (28). On the second practice trial, participants completed 15 min of the simulated soccer match (described in the next section) to habituate to the demands of the test.

Back to Top | Article Outline

Experimental Trials

Simulated soccer match

On the first day of the experimental trial, participants reported to the laboratory 2 h postprandial and, after baseline measurement (described in detail in the next section), completed a 90-min simulated soccer match. The simulated match consisted of 2 × 45 min halves of varying intensity exercise requiring walking, jogging (55% V˙O2max), backpedaling, and running (95% V˙O2max) 20-m shuttles in time to an audible beep, interspersed with maximum effort 20-m sprints. This protocol has been previously demonstrated to induce a physical demand and associated metabolic response consistent with a 90-min soccer match (19,28). After each 20-m sprint, participants were required to forcibly decelerate to a target line situated 5 m from the finish. This procedure was included to more accurately reflect the demands of soccer match play (1) and to induce muscle damage consistent with the mechanical demands of soccer (16,18). In total, participants completed 42 maximal sprints with forced decelerations across the 90 min.

Back to Top | Article Outline

Outcome measures

A range of measures were assessed before and after simulated soccer match play, and at 24-h intervals for 72 h postexercise, to ascertain the time course recovery after the simulated match. Details of each are outlined in the next section. For the postexercise measurement, the assessment of central and peripheral neuromuscular fatigue measured with motor nerve and motor cortical stimulation was completed within 2.5 min of exercise cessation. This is in accordance with previous similar investigations (35,39,43,44) and is necessary to capture the extent of neuromuscular fatigue before it dissipates. Further details on these procedures are provided in the next section.

Back to Top | Article Outline

Fatigue and perceptions of muscle soreness

Fatigue was measured at each time point via visual analog scales, where participants were required to draw a vertical line on a 15-cm horizontal line in response to the question “How fatigued do you feel?” Visual analog scales were also completed to assess perceptions of muscle soreness in passive (while seated) and active (while performing three repetitions of a bodyweight squat) conditions and readiness to train after warm-up. The scales were anchored by verbal descriptors as follows: “extremely fatigued” to “not fatigued at all,” “extremely sore” to “no soreness,” and “not ready/tired/fatigued” to “ready/alert/focused.”

Back to Top | Article Outline

Assessment of neuromuscular function

The evoked force and EMG responses of the quadriceps musculature to TMS of the motor cortex and electrical stimulation of the femoral nerve were assessed to ascertain fatigue-induced changes in CNS and muscle function. A calibrated load cell (MuscleLab Force Sensor 300; Ergotest Technology, Norway), attached via a noncompliant strap and positioned superior to the ankle malleoli of the participants' dominant leg recorded muscle force (N) during isometric knee extensor contractions. All knee extensor contractions were performed in a custom-built chair. Participants sat upright with hip and knee angles at 90° flexion and were encouraged to grasp the handles of the chair for support during contractions. The force transducer was adjusted for each participant to ensure a direct line of applied force; this position was recorded for replication on repeat trials. Surface EMG activity of the rectus femoris (RF) and biceps femoris (BF) was recorded from surface electrodes (Ag/AgCl; Kendall H87PG/F; Covidien, Mansfield, MA) placed 2 cm apart over the muscle bellies, with a reference electrode placed on the patella. Electrodes were used to record the root-mean-square (RMS) amplitude for submaximal and maximal voluntary contractions, the compound muscle action potential (M-wave) from electrical stimulation of the femoral nerve, and the MEP elicited by TMS. Further details on these methods are provided in the next section.

Back to Top | Article Outline

Motor nerve stimulation

Single electrical stimuli (200 μs) were delivered via a constant-current stimulator (DS7AH; Digitimer Ltd., Hertfordshire, UK) using self-adhesive surface electrodes (Nidd Valley Medical Ltd., North Yorkshire, UK). The cathode was positioned superficially on the skin in the femoral triangle. The anode was placed midway between the greater trochanter and the iliac crest. Electrical stimuli were administered manually by the experimenter at rest, in 20-mA stepwise increments from 100 mA until the maximum quadriceps twitch amplitude (Qtw, N) and muscle compound action potential (Mmax, mV) were elicited. To ensure a consistent, supramaximal stimulus and account for any fatigue-induced changes in axonal excitability, the resulting stimulation intensity was increased by 30% (mean current = 215 ± 40 mA). Participants subsequently completed six isometric MVC of the knee extensors, separated by 60 s rest. For the final three MVC, single electrical stimuli were delivered during and 2 s after to assess VA and potentiated quadriceps twitch force (Qtw,pot), respectively.

Back to Top | Article Outline

Motor cortical stimulation

Single and paired pulse TMS of 1-ms duration were delivered to the left motor cortex over Brodmann area 4 (position relative to the vertex: ~1–2 cm), using a concave double cone coil (posteroanterior intracranial current flow, 110 mm diameter, maximum output 1.4 T) powered by two linked monopulse magnetic stimulators (Magstim 200; The Magstim Company Ltd., Whitland, UK). The coil position that elicited a large MEP in the knee extensors and concurrent small MEP in the antagonist muscle was marked with indelible ink.

Back to Top | Article Outline

VA with TMS

Single-pulse TMS was delivered during brief (3–5 s) contractions at 100%, 75%, and 50% MVC, separated by 5 s of rest, for determination of VA with TMS (VATMS). This procedure was repeated three times with 90 s rest between each set. The stimulation intensity (66% ± 7%) was set at the stimulator output that elicited the maximum superimposed twitch force during a 50% MVC (39).

Back to Top | Article Outline

CNS excitability and inhibition

Single- and paired-pulse TMS were delivered during submaximal contraction (10% MVC) to elicit unconditioned (single-pulse) and conditioned (paired-pulse) MEP at each time point. The ratio of the unconditioned MEP to the maximum M-wave was used as an index of corticospinal excitability. The ratio of the unconditioned to conditioned MEP was used as an index of short intracortical inhibition (SICI). Ten unconditioned and 10 conditioned MEP were elicited in two sets of 10 stimuli, delivered in random order, with each stimuli separated by 4–6 s and each set separated by 60 s. The stimulator output was set relative to active motor threshold (AMT, 43% ± 6%), which was determined before each trial as the stimulus intensity required to elicit an MEP of at least 0.2 mV in the rectus femoris in three of five consecutive stimulations during a submaximal (10% MVC) contraction. Single-pulse TMS was delivered at 1.2 × AMT. Paired stimuli, to induce SICI, consisted of a subthreshold (0.7 × AMT) conditioning stimulus followed by a suprathreshold (1.2 × AMT) test stimulus, with an interstimulus interval of 3 ms. Postexercise and at 24, 48, and 72 h if MVC force differed from baseline by >10% responses were elicited at two contraction strengths: (i) at 10% of the nonfatigued MVC recorded at baseline (absolute) and (ii) at 10% of the fatigued MVC recorded on the day of the test (relative).

Back to Top | Article Outline

Assessment of physical function

Participants completed tests of linear speed (10- and 20-m sprint) and jumping performance (countermovement jump, broad jump [BJ], and drop jump for reactive strength index [DJ-RSI]) to measure physical function in variables relevant to optimal soccer performance. Linear speed was recorded during three maximum effort sprints with electronic timing gates recording splits at 10 and 20 m (TC Timing Systems, Brower Timing Systems, Draper). Vertical jumping performance was recorded using an optical timing system (Optojump Next, Microgate, Milan, Italy). For CMJ, participants were instructed to jump as high as possible, with hands akimbo. For reactive strength index (DJ-RSI), participants were instructed to keep hands akimbo, step off a 30-cm box, and jump as quickly and, as maximally as possible. To ensure the DJ-RSI protocol was assessing fast stretch-shortening cycle function, participants were required to attain ground contract times of <200 ms. Visual feedback of ground contact time and jump height was provided via a computer monitor after each jump. Reactive strength index was calculated as the ratio between jump height (cm) and ground contact time (s). For the assessment of BJ performance, participants stood with their toes behind a marked line and jumped maximally in a horizontal direction. Jump distance was recorded at the heel of the backmost foot (m). All participants completed three maximal attempts at each jump, with 60 s separating each repetition. The best score was used for analysis.

Back to Top | Article Outline

Creatine kinase

Fingertip samples of capillary blood were obtained at each time point and immediately assayed for creatine kinase (CK) concentration (Reflotron, Roche Diagnostics, Germany).

Back to Top | Article Outline

Data Analysis

MVC force was quantified as the mean of the two highest MVC attempts at each time point. The peak-to-peak amplitudes of the evoked M-wave and MEP responses, measured as the absolute difference between the minimum and the maximum points of the biphasic waveform, were quantified offline. Corticospinal excitability was quantified as the ratio between the average unconditioned MEP elicited during 10% MVC and the maximum M-wave. The average of the conditioned paired-pulse MEP was expressed relative to the averaged unconditioned MEP to quantify SICI. In addition, the RMS EMG amplitude and average force were measured across 80 ms before TMS to ensure a similar level of background muscle activity was present immediately before stimulation for unconditioned and conditioned MEP. The interpolated twitch technique was used to quantify VA (22). In brief, the amplitude of the superimposed twitch force (SIT) measured during MVC was compared with the Qtw,pot elicited 2 s post-MVC at rest (VA, % = (1 – [SIT/Qtw,pot] × 100). For motor cortical stimulation, VATMS was assessed by measurement of the superimposed twitch responses to TMS at 100%, 75%, and 50% MVC. As corticospinal excitability increases during voluntary contraction, it was necessary to estimate the amplitude of the resting twitch in response to motor cortex stimulation. The amplitude of the estimated resting twitch (ERT) was calculated as the y-intercept of the linear regression between the mean amplitude of the superimposed twitches evoked by TMS at 100%, 75%, and 50% MVC and the voluntary force; regression analyses confirmed the existence of a linear relationship at each time point (r2 range = 0.86 ± 0.08 to 0.91 ± 0.04). VA measured with TMS (VATMS, %) was subsequently calculated as (1 – [SIT/ERT] × 100).

Back to Top | Article Outline

Statistical Analysis

Descriptive statistics are presented as means ± SD. One-way repeated-measures ANOVA was used for all outcome measures, with a priori–defined Tukey-adjusted pairwise comparisons with the pretest, or baseline, score as the control category. Using the baseline score as the control category focuses the analysis on ascertaining how long the responses measured remain significantly depressed compared with baseline, and therefore how long it took for participants to fully recover from the simulated match. The assumptions of these procedures, including data distribution, were verified as per the guidelines of Newell et al. (27). Standardized effect sizes (Cohen's d) were calculated for focused pairwise comparisons and interpreted as small (≥0.2), moderate (≥0.6), and large (≥1.2). Statistical analysis was conducted using GraphPad Prism (version 5; GraphPad Software Inc., La Jolla, CA). Statistical significance was accepted at P < 0.05.

Back to Top | Article Outline


Back to Top | Article Outline

Fatigue and perceptual responses

Fatigue and perceptions of passive and active muscle soreness were similarly affected by the simulated soccer match (Fig. 1). Fatigue and perceptions of muscle soreness peaked postexercise (all P < 0.05 and d > 2.65) and remained depressed at 24 and 48 h (all P < 0.05 and d > 1.13; Fig. 1). All variables had recovered to baseline values by 72 h postexercise (all P > 0.05 and d < 0.54; Fig. 1). However, perceptions of readiness to train, measured before and at 24-h intervals postexercise before assessment of physical function and after a standardized warm-up, were not affected by the simulated game at any time point (all P > 0.05, d range from 0.12 to 0.61).

Back to Top | Article Outline

Neuromuscular function

Maximum voluntary force (MVC) was significantly reduced from pre- to postexercise (632 ± 54 vs 527 ± 64 N, P < 0.001, d = 1.77) and had not fully recovered by 72 h postexercise (614 ± 53 N, P = 0.01, d = 0.33; Fig. 2A). VA measured with motor nerve stimulation decreased from pre- to postexercise (91.8% ± 3.0% vs 83.3% ± 4.0%, P < 0.001, d = 2.41), remained depressed at 24 h (88.0% ± 3.4%, P < 0.001, d = 1.18) and 48 h (89.8% ± 4.1%, P = 0.03, d = 0.56), but recovered by 72 h (90.3% ± 3.6%, P = 0.09, d = 0.46 Fig. 2B). VA measured with motor cortical stimulation (VATMS) decreased pre- to postexercise (92.5% ± 2.9% vs 82.2% ± 6.3%, d = 2.23), remained depressed at 24 h (89.4% ± 4.2%, d = 0.85), but recovered by 48 h (P = 0.44, d = 0.25, Fig. 2C). Quadriceps potentiated twitch force was reduced from pre- to postexercise (197 ± 22 vs 170 ± 26 N, P < 0.001, d = 1.11), remained similarly depressed at 24 h (171 ± 21 N, P < 0.001, d = 1.19), and continued to be different from baseline at 48 h (181 ± 23 N, P < 0.001, d = 0.71) and 72 h postexercise (188 ± 30 N, P = 0.01, d = 0.33, Fig. 2D).

Back to Top | Article Outline

CNS inhibition and excitability

Short intracortical inhibition was unchanged after soccer match play and was not different to the baseline value at any time point (Fig. 3A). Corticospinal excitability (unconditioned MEP/Mmax) was reduced at 24 h compared with baseline when measured during a submaximal contraction at both absolute (−5% ± 9%, P = 0.047) and relative (−6% ± 10%, P = 0.04) contraction strengths (Fig. 3B). The reduction in corticospinal excitability was explained by a small reduction in the amplitude of the MEP, concurrent with a small increase in Mmax (Table 1). No other differences were observed at any other time point. Full details regarding the EMG responses to TMS and femoral nerve stimulation procedures are provided in Table 1.

Back to Top | Article Outline

Physical function

Countermovement jump performance was reduced from pre- to postexercise (38.8 ± 4.3 vs 34.0 ± 5.0 cm, P < 0.001, d = 1.04), and there were moderate, statistically significant effects thereafter at 24 h (36.8 ± 4.3 cm, P < 0.001, d = 0.46), 48 h (36.9 ± 4.2 cm, P < 0.001, d = 0.44), and 72 h postexercise (37.3 ± 4.1 cm, P = 0.009, d = 0.36, Fig. 4A). For DJ measurements, ground contact time averaged 180 ± 16 ms at baseline and was successfully maintained on subsequent days (range 180–186 ms). Reactive strength index (DJ height/ground contact time) was impaired postexercise (161 ± 22 vs 126 ± 19 cm·s−1, P < 0.001, d = 1.73), remained depressed at 24 h (144 ± 24 cm·s−1, P < 0.001, d = 0.74) and 48 h (144 ± 23 cm·s−1, P < 0.001, d = 0.75), and had recovered by 72 h (156 ± 26 cm·s−1, P = 0.11, d = 0.24; Fig. 4B). BJ performance decreased pre- to postexercise (2.38 ± 0.11 vs 2.23 ± 0.11 m, P < 0.001, d = 1.36), remained reduced at 24 h (2.32 ± 0.14 m, P = 0.03, d = 0.47), but had recovered from 48 h onward (2.37 ± 0.13 m, P = 0.24, d = 0.24; Fig. 4C). Maximal sprint performance was reduced pre- to postexercise for both 10 m (1.87 ± 0.08 vs 1.92 ± 0.07 s, P = 0.01, d = 0.62) and 20 m (3.15 ± 0.09 vs 3.26 ± 0.10 s, P < 0.001, d = 1.18) but was not different at any other time point (all P > 0.05).

Back to Top | Article Outline

Creatine kinase

Creatine kinase (IU·L−1) increased from pre- to postexercise (215 ± 125 vs 563 ± 368 IU·L−1, P < 0.001, d = 1.62), peaked at 24 h after (813 ± 391 IU·L−1, P < 0.001, d = 2.40), and remained elevated at 48 (577 ± 250 IU·L−1, P < 0.001, d = 1.80) and 72 h postexercise (442 ± 189 IU·L−1, P < 0.001, d = 1.36).

Back to Top | Article Outline


The aims of the study were 1) to ascertain the etiology and recovery of neuromuscular fatigue after simulated soccer match play and 2) to investigate the potential of physical and perceptual assessments to profile recovery after soccer match play, to provide practitioners with suitable tools to monitor recovery and inform the assessment of a players readiness to train. Simulated soccer match play resulted in substantial fatigue that persisted for up to 72 h postexercise. Central fatigue (reduction in VA) was substantial immediately postexercise and, although markedly recovered by 24 h, remained significantly depressed for 48 h postexercise. Supraspinal fatigue, a subset of central fatigue attributable to a suboptimal output from the motor cortex, was evident for up to 24 h postexercise but recovered thereafter. Peripheral fatigue was substantial immediately postexercise, remained similarly depressed at 24 h, and was still below baseline at 72 h. This marked and prolonged nature of peripheral fatigue indicates that changes in skeletal muscle function primarily explained the resolution of neuromuscular fatigue in the days after soccer match play. The similar decline and the subsequent time course recovery of physical and perceptual function suggest these might be appropriate tools to indirectly assess the recovery of neuromuscular fatigue after soccer match play. Collectively, these data have significant implications for managing the training and competition load experienced by players through appropriate intervention and scheduling of matches.

Back to Top | Article Outline

Neuromuscular fatigue after simulated match play

The simulated soccer match elicited neuromuscular fatigue that was both central and peripheral in origin. Maximum voluntary force and potentiated twitch force were reduced postexercise and remained below baseline at 72 h after. VA was depressed for 48 h but had recovered by 72 h. This U-shaped time course recovery of neuromuscular function is similar to findings reported after prolonged intermittent sprint exercise (24,30). VA assessed with TMS, a subset of central fatigue attributable to changes in corticospinal function, was depressed postexercise at 24 h but had recovered by 48 h after. Therefore, although VA (measured with motor nerve stimulation) remained depressed for 48 h, the earlier recovery of VATMS suggests the origin of central fatigue observed from 24 h onward was unlikely due to suboptimal output from the motor cortex. One previous study profiling the time course recovery of neuromuscular function after soccer match play reported a similar pattern of response to the present study, but with a faster return to baseline where central and peripheral markers of neuromuscular fatigue had recovered by 48 h after (31). Rampinini et al. (31) examined fatigue in professional academy players, during the competition phase of the season after a “friendly” match, rather than a simulated soccer match. These differences might explain the faster recovery of neuromuscular function observed and emphasize the need for further study.

Although it is not possible to accurately quantify the relative contribution of central and peripheral processes to the observed decrease in maximal voluntary force, a comparison of the magnitude of the decrement of each with previous work provides some insight. For central fatigue, the decrease immediately postexercise (−9% ± 4% for VA, −10% ± 5% for VATMS) is comparable with previous data from our laboratory examining fatigue after repeat sprint exercise (13), self-paced time trial cycling exercise exceeding 30 min (44), and constant-load cycling exercise of 30–45 min (43). This suggests that central fatigue was prominent immediately postexercise and is consistent with other previous observations of long-duration running (20,33,42) and cycling (10) exercise. At 24 and 48 h postexercise, there was evidence of a residual activation deficit, but the magnitude of this depression was relatively small in comparison with the postexercise decrease (−4% ± 2% for VA, −3% ± 4% for VATMS at 24 h, and −2% ± 3% for VA at 48 h), suggesting a rapid resolution of central fatigue. Although statistically significant, and representing moderate to large effects, the functional relevance of such small differences in VA is not possible to accurately quantify and could be questioned.

Peripheral fatigue was also substantial postexercise (−14% ± 10% reduction in Qtw,pot), but in contrast to central fatigue recovered more slowly. The 14% reduction in Qtw,pot immediately after simulated soccer appears relatively small compared with previous observations in high-intensity single-leg (−44% ± 6%) vs double-leg cycling (−33% ± 7%) (34) and all-out repeat-sprint running exercise (−23% ± 9%) (13). However, the absolute magnitude of peripheral fatigue is dictated by the extent of the muscle mass involved (34,35), and the intensity of the exercise task (43), and in the aforementioned studies the higher absolute magnitude of peripheral fatigue in comparison with the current data can be explained by differences in these factors. Importantly, the magnitude of peripheral fatigue persisted 24 h postexercise (−13% ± 5%), where central fatigue had demonstrated a quicker recovery and remained slightly below baseline at 72 h (−5% ± 6%). This suggests the neuromuscular fatigue experienced in the days postexercise can be explained to a greater extent by processes occurring at the muscle that are likely related to muscle damage (as evidenced by the large increase in CK in the days postexercise) and the subsequent inflammatory response rather than processes within the CNS. Recent reviews have suggested that future research should focus more on the recovery of central factors of fatigue in the days postintermittent sprint exercise (23,32). Our data would suggest this to be a worthwhile endeavor given the significant activation deficit present in the days postexercise. However, the recovery of skeletal muscle function should remain the primary target of intervention aimed at optimizing recovery from soccer match play.

Back to Top | Article Outline

CNS excitability and inhibition

Corticospinal excitability, inferred from changes in the MEP to Mmax ratio, was different to baseline only at 24 h postexercise. This decrease was concurrent with a reduction in VATMS at the same time point, with both recovering by 48 h. There is a plausible theoretical link between changes in corticospinal excitability and supraspinal fatigue, but the functional relevance of changes in corticospinal excitability is questionable (5). Indeed, where supraspinal fatigue was highest in the present study (immediately postexercise), excitability was unchanged. The magnitude of SICI, inferred from changes in the unconditioned MEP expressed relative to the conditioned, paired-pulse, MEP, was not different at any time point. We hypothesized differences in these variables in the days postexercise could reflect residual, CNS fatigue, but the lack of change in excitability and SICI did not support this posit. That these measures were not sensitive to fatigue and recovery of neuromuscular function is not altogether surprising; the measurement of the MEP response to TMS is notoriously variable (15), and the size of the MEP is subject to modulation by multiple mechanisms and sites. These include premotor and motor supraspinal areas (5), the excitability of the spinal motoneuron pool (41), and afferent inputs at both motor and spinal sites (8). A detailed physiological underpinning to the MEP evoked by single- and paired-pulse TMS remains incompletely understood (5), but the present data suggest their use to understand any residual fatigue of the CNS in the days after soccer match play is limited.

Back to Top | Article Outline

Recovery of physical function

All measures of physical function were impaired immediately postexercise but recovered at different rates. Vertical jump performance (countermovement and drop jump for reactive strength index) followed a similar decline and recovery as measures of neuromuscular function, with countermovement jump height remaining reduced at 72 h after. This decrease and recovery of jump performance is similar to that previously reported in the days after soccer match play (17,26,31). BJ and sprint performance were less sensitive as markers of fatigue, suggesting their use to profile the recovery process after soccer match play is limited. These observations are supported by previous research demonstrating jump tests to be superior in their consistency and sensitivity to fatigue in the days postexercise compared with sprinting tests (12), and that the decrements in jumping performance after soccer match play are relatively consistent (remaining depressed for 48–72 h after) (2,19,25,31), whereas the effect on sprinting performance ranges from no effect (2) to full recovery by 24 h (31), 48 h (3), and >72 h (19,25).

Back to Top | Article Outline

Recovery of perceptual responses

Measures of perceptual function had a similar time course recovery pattern to the physical and neuromuscular responses studied. Perceptual scales such as those used within this study can be used daily and are a simple, noninvasive method of assessing an athlete's recovery status without disrupting their training schedule, and as a result might be a better alternative to a physical monitoring tool (36). Alongside an objective measure of physical performance, the assessment of the athlete's perceived recovery would, at the very least, offer valuable ancillary information in determining recovery status. Interestingly, perceptions of readiness to train assessed after a standardized warm-up were not significantly impaired at any time point within the study, despite the documented declines in neuromuscular and physical function. This suggests that a thorough warm-up might mask the deleterious effects of fatigue present in the days postmatch, which has implications for the timing of perceptual assessment for practitioners.

Back to Top | Article Outline

Limitations and future directions

The measurements of neuromuscular function were studied in the dominant knee extensor musculature at rest, and during submaximal and maximal isometric contractions, with evoked responses recorded from the rectus femoris. These procedures have been previously validated (14,22) and allow an assessment of voluntary and involuntary force capacity, and the magnitude of central and peripheral neuromuscular fatigue. However, the fatigue elicited by the physical demands of soccer, which requires complex whole-body maximal and submaximal multidirectional movements, might not be fully elucidated by studying the fatigue of a single muscle group in a single-limb isometric contraction. In addition, there is a significant cognitive component to successful soccer performance that is not present in a simulated match, which could contribute to impairments in performance by increasing mental fatigue and the perception of effort required during a match (40). Notwithstanding, the significant and prolonged neuromuscular fatigue and associated decrements in physical function provide support for the usefulness of the methods used in revealing new information on the etiology and recovery of fatigue after soccer match play. Further research is required with real soccer matches to further corroborate these findings in a more ecologically valid model.

Back to Top | Article Outline


Simulated soccer match play induced significant neuromuscular fatigue that was both central and peripheral in origin and persisted for up to 72 h postexercise. Central processes contribute significantly to the neuromuscular fatigue experienced in the days postexercise, but the magnitude and slower recovery of peripheral fatigue indicates that processes relating to the resolution of muscle function primarily explain the recovery of neuromuscular fatigue after games. That the recovery of neuromuscular fatigue can persist for up to 72 h postmatch has significant practical implications for the training process and the scheduling of matches, particularly during congested fixture periods. The assessment of fast stretch–shortening cycle function via measurement of the reactive strength index provides a promising surrogate measurement of neuromuscular fatigue, but it is recommended practitioners use a range of tools, including simple assessments of perceived recovery, when assessing recovery status.

The study was funded by the UEFA Research grant program. The authors thank Mr. Paul Parker, Mr. Chris Ferriter, Mr. Ryan Stewart, and Mr. John Benz for their assistance during data collection. The authors have no competing interests to declare. The results of the study are presented clearly, honestly, and without fabrication, falsification, or inappropriate data manipulation. The results of the study do not constitute endorsement by the American College of Sports Medicine.

Back to Top | Article Outline


1. Akenhead R, Hayes PR, Thompson KG, French D. Diminutions of acceleration and deceleration output during professional football match play. J Sci Med Sport. 2013;16(6):556–61.
2. Andersson H, Raastad T, Nilsson J, Paulsen G, Garthe I, Kadi F. Neuromuscular fatigue and recovery in elite female soccer: effects of active recovery. Med Sci Sports Exerc. 2008;40(2):372–80.
3. Ascensao A, Rebelo A, Oliveira E, Marques F, Pereira L, Magalhaes J. Biochemical impact of a soccer match—analysis of oxidative stress and muscle damage markers throughout recovery. Clin Biochem. 2008; 41(10–11):841–51.
4. Beck S, Taube W, Gruber M, Amtage F, Gollhofer A, Schubert M. Task-specific changes in motor evoked potentials of lower limb muscles after different training interventions. Brain Res. 2007; 1179:51–60.
5. Bestmann S, Krakauer JW. The uses and interpretations of the motor-evoked potential for understanding behaviour. Exp Brain Res. 2015;233(3):679–89.
6. Butler JE, Taylor JL, Gandevia SC. Responses of human motoneurons to corticospinal stimulation during maximal voluntary contractions and ischemia. J Neurosci. 2003;23(32):10224–30.
7. Carling C, McCall A, Le Gall F, Dupont G. The impact of short periods of match congestion on injury risk and patterns in an elite football club. Br J Sports Med. 2016;50(12):764–8.
8. Carroll TJ, Selvanayagam VS, Riek S, Semmler JG. Neural adaptations to strength training: moving beyond transcranial magnetic stimulation and reflex studies. Acta Physiol (Oxf). 2011;202(2):119–40.
9. Chen R. Excitatory and inhibitory effects of transcranial magnetic stimulation. Biocybern Biomed Eng. 2011;31(2):93–105.
10. Decorte N, Lafaix PA, Millet GY, Wuyam B, Verges S. Central and peripheral fatigue kinetics during exhaustive constant-load cycling. Scand J Med Sci Sports. 2012;22(3):381–91.
11. Dellal A, Lago-Peñas C, Rey E, Chamari K, Orhant E. The effects of a congested fixture period on physical performance, technical activity and injury rate during matches in a professional soccer team. Br J Sports Med. 2015;49(6):390–4.
12. Gathercole R, Sporer B, Stellingwerff T, Sleivert G. Alternative countermovement-jump analysis to quantify acute neuromuscular fatigue. Int J Sports Physiol Perform. 2015;10(1):84–92.
13. Goodall S, Charlton K, Howatson G, Thomas K. Neuromuscular fatigability during repeated-sprint exercise in male athletes. Med Sci Sports Exerc. 2015;47(3):528–36.
14. Goodall S, Romer LM, Ross EZ. Voluntary activation of human knee extensors measured using transcranial magnetic stimulation. Exp Physiol. 2009;94(9):995–1004.
15. Héroux ME, Taylor JL, Gandevia SC. The use and abuse of transcranial magnetic stimulation to modulate corticospinal excitability in humans. PLoS One. 2015;10(12):e0144151.
16. Howatson G, Milak A. Exercise-induced muscle damage following a bout of sport specific repeated sprints. J Strength Cond Res. 2009; 23(8):2419–24.
17. Ispirlidis I, Fatouros IG, Jamurtas AZ, et al. Time-course of changes in inflammatory and performance responses following a soccer game. Clin J Sport Med. 2008;18(5):423–31.
18. Leeder JDC, van Someren KA, Gaze D, et al. Recovery and adaptation from repeated intermittent-sprint exercise. Int J Sports Physiol Perform. 2014;9(3):489–96.
19. Magalhães J, Rebelo A, Oliveira E, Silva JR, Marques F, Ascensão A. Impact of Loughborough Intermittent Shuttle Test versus soccer match on physiological, biochemical and neuromuscular parameters. Eur J Appl Physiol. 2010;108(1):39–48.
20. Martin V, Kerhervé H, Messonnier LA, et al. Central and peripheral contributions to neuromuscular fatigue induced by a 24-h treadmill run. J Appl Physiol (1985). 2010;108(5):1224–33.
21. Maruyama A, Matsunaga K, Tanaka N, Rothwell JC. Muscle fatigue decreases short-interval intracortical inhibition after exhaustive intermittent tasks. Clin Neurophysiol. 2006;117(4):864–70.
22. Merton PA. Voluntary strength and fatigue. J Physiol. 1954;123(3): 553–64.
23. Minett GM, Duffield R. Is recovery driven by central or peripheral factors? A role for the brain in recovery following intermittent-sprint exercise. Front Physiol. 2014;5:24.
24. Minett GM, Duffield R, Billaut F, Cannon J, Portus MR, Marino FE. Cold-water immersion decreases cerebral oxygenation but improves recovery after intermittent-sprint exercise in the heat. Scand J Med Sci Sports. 2014;24(4):656–66.
25. Nedelec M, McCall A, Carling C, Legall F, Berthoin S, Dupont G. The influence of soccer playing actions on the recovery kinetics after a soccer match. J Strength Cond Res. 2014;28(6):1517–23.
26. Nédélec M, McCall A, Carling C, Legall F, Berthoin S, Dupont G. Recovery in soccer: part I—post-match fatigue and time course of recovery. Sports Med. 2012;42(12):997–1015.
27. Newell J, Aitchison T, Grant S. Statistics for Sports and Exercise Science: A Practical Approach. Harlow: Pearson Education; 2010. p. 427.
28. Nicholas CW, Nuttall FE, Williams C. The Loughborough Intermittent Shuttle Test: a field test that simulates the activity pattern of soccer. J Sports Sci. 2000;18(2):97–104.
29. Nuzzo JL, Barry BK, Gandevia SC, Taylor JL. Acute strength training increases responses to stimulation of corticospinal axons. Med Sci Sports Exerc. 2016;48(1):139–50.
30. Pointon M, Duffield R, Cannon J, Marino FE. Cold water immersion recovery following intermittent-sprint exercise in the heat. Eur J Appl Physiol. 2012;112(7):2483–94.
31. Rampinini E, Bosio A, Ferraresi I, Petruolo A, Morelli A, Sassi A. Match-related fatigue in soccer players. Med Sci Sports Exerc. 2011;43(11):2161–70.
32. Rattray B, Argus C, Martin K, Northey J, Driller M. Is it time to turn our attention toward central mechanisms for post-exertional recovery strategies and performance? Front Physiol. 2015;6:79.
33. Ross EZ, Goodall S, Stevens A, Harris I. Time course of neuromuscular changes during running in well-trained subjects. Med Sci Sports Exerc. 2010;42(6):1184–90.
34. Rossman MJ, Garten RS, Venturelli M, Amann M, Richardson RS. The role of active muscle mass in determining the magnitude of peripheral fatigue during dynamic exercise. Am J Physiol Regul Integr Comp Physiol. 2014;306(12):R394–40.
35. Rossman MJ, Venturelli M, McDaniel J, Amann M, Richardson RS. Muscle mass and peripheral fatigue: a potential role for afferent feedback? Acta Physiol (Oxf). 2012;206(4):242–50.
36. Saw AE, Main LC, Gastin PB. Monitoring the athlete training response: subjective self-reported measures trump commonly used objective measures: a systematic review. Br J Sports Med. 2016;50(5):281–91.
37. Sidhu SK, Cresswell AG, Carroll TJ. Motor cortex excitability does not increase during sustained cycling exercise to volitional exhaustion. J Appl Physiol (1985). 2012;113(3):401–9.
38. Sidhu SK, Lauber B, Cresswell AG, Carroll TJ. Sustained cycling exercise increases intracortical inhibition. Med Sci Sports Exerc. 2013;45(4):654–62.
39. Sidhu SK, Weavil JC, Venturelli M, et al. Spinal μ-opioid receptor-sensitive lower limb muscle afferents determine corticospinal responsiveness and promote central fatigue in upper limb muscle. J Physiol. 2014;592(22):5011–24.
40. Smith MR, Marcora SM, Coutts AJ. Mental fatigue impairs intermittent running performance. Med Sci Sports Exerc. 2015;47(8): 1682–90.
41. Taylor JL. Stimulation at the cervicomedullary junction in human subjects. J Electromyogr Kinesiol. 2006;16(3):215–23.
42. Temesi J, Rupp T, Martin V, et al. Central fatigue assessed by transcranial magnetic stimulation in ultratrail running. Med Sci Sports Exerc. 2014;46(6):1166–75.
43. Thomas K, Elmeua M, Howatson G, Goodall S. Intensity-dependent contribution of neuromuscular fatigue after constant-load cycling. Med Sci Sports Exerc. 2016;48(9):1751–60.
44. Thomas K, Goodall S, Stone M, Howatson G, St Clair Gibson A, Ansley L. Central and peripheral fatigue in male cyclists after 4-, 20-, and 40-km time trials. Med Sci Sports Exerc. 2015;47(3): 537–46.
45. Weier AT, Pearce AJ, Kidgell DJ. Strength training reduces intracortical inhibition. Acta Physiol (Oxf). 2012;206(2):109–19.
46. Williams PS, Hoffman RL, Clark BC. Cortical and spinal mechanisms of task failure of sustained submaximal fatiguing contractions. PLoS One. 2014;9(3):e93284.
47. Zult T, Goodall S, Thomas K, Hortobágyi T, Howatson G. Mirror illusion reduces motor cortical inhibition in the ipsilateral primary motor cortex during forceful unilateral muscle contractions. J Neurophysiol. 2015;113(7):2262–70.


Supplemental Digital Content

Back to Top | Article Outline
© 2017 American College of Sports Medicine