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Keywords:

  • EIMD ;
  • muscle pain;
  • cortical alpha activity;
  • central regulator;
  • top-down control;
  • EEG

Abstract

  1. Top of page
  2. Abstract
  3. Methods
  4. Results
  5. Discussion
  6. Perspectives
  7. Conflict of interest
  8. Acknowledgements
  9. Funding
  10. Ethical approval
  11. References

Exercise-induced muscle damage (EIMD) is characterized by pain, swelling, and shortening of the muscle; increased serum creatine kinase; decreased force output; and altered neuromuscular function. The aim of this study was to investigate the effects of EIMD to determine the relationship between the peripheral symptoms, neuromuscular changes, and delayed pain sensation during a submaximal movement of the biceps brachii on cortical alpha (α) activity. In contrast to the control (n = 12) group, the experimental (n = 16) group participated in an EIMD protocol, and both groups were monitored for 132 h post-EIMD protocol. At 12 h, neuromuscular functioning was already disturbed while the sensation of pain was perceived, but not fully developed. Muscle pain scores in the experimental group peaked after 36 h with the lowest torque reported at 12 h. α-1 activity increased significantly in the motor and somatosensory area 12 h post-EIMD while α-2 activity increased in the contralateral fronto-central area. At 36 h, pain had further increased and neuromuscular function improved while α-1 and α-2 activities had decreased. We hypothesize that α-1 activity over the motor and somatosensory cortex of the experimental group displays a compensatory increase in response to the changes in neuromuscular function during movement, while an increase in α-2 activity is related to the suppression of pain experienced within the first 12 h.

Exercise-induced muscle damage (EIMD) is a phenomenon that occurs after unaccustomed exercise, especially exercise where the muscles are lengthened under tension. Symptoms include structural damage to the muscle (Fridén & Lieber, 1992), development of pain (Plattner et al., 2011), and changes in neuromuscular function including electromygraphy activity (EMG) (Semmler et al., 2007; Plattner et al., 2011) and force production (Semmler et al., 2007).

Interestingly, while there is a decrease in EMG activity during a maximal voluntary contraction (MVC), submaximal EMG is increased within the first 12 h after an EIMD protocol. This is of interest because the sensation of pain is only perceived 12–24 h after an EIMD protocol (Plattner et al., 2011). Collectively, these data suggest that the changes observed in the neuromuscular function after EIMD are driven by an upstream regulator situated in the brain, which is guided by peripheral bottom-up input (i.e., symptoms of pain, inflammation, intramuscular enzyme leakage, and tissue damage) (Semmler et al., 2007; Plattner et al., 2011).

It has been shown with functional magnetic resonance imaging (fMRI) and positron emission tomography scans that a pain stimulus activates several areas of the brain, the primary somatosensory cortex (SI), secondary somatosensory cortex (SII), premotor cortex, and cingulate gyrus (limbic system) contralateral to the stimulus (Vogt, 2005). These areas integrate the information arising from the periphery to create an emotional, behavioral and/or motor response, depending on the circumstances (Melzack, 1999; Vogt, 2005).

As fMRI does not allow for movement during the measurement or precise time resolution of the data (Sato et al., 2010), electroencephalography (EEG) is a preferred method to measure brain activity during movement (Thompson et al., 2008). EEG is measured on the scalp with multiple low-amplitude sensitive electrodes and measures electrical activity produced by the neuronal firing in cortical and subcortical areas of the brain (Niedermeyer, 2005; Thompson et al., 2008). An outcome of the EEG measurement is spectral power in different frequencies, also known as frequency band activity. The 8–13-Hz band, which represents the alpha (α) activity, is known to be influenced by pain (Chang et al., 2001, 2003), movement (Stancak et al., 2000), attention (Sauseng et al., 2006), and arousal (Chang et al., 2005).

The most common response of an α activity to a painful, cognitive, or motor stimulus is a decrease in activity at the onset of the stimulus, followed by an increase in activity once the stimulus has lasted for several minutes (Stancak et al., 2000; Chang et al., 2003) or ended (Chang et al., 2001; Anderson & Ding, 2011). However, recent research has shown that α activity can also increase during focused attention and cognitive processes (Palva & Palva, 2007). von Stein et al. (2000) showed that the increase in α-activity, especially α-2 activity, was due to interactions between the frontal and parietal areas, and that the increase appears to be acting as a top-down regulator. A similar top-down regulatory process has been suggested by Chen and Herrmann (Chen and Herrmann, 2001) to control the sensation of pain. The notion of the top-down suppression of pain is further supported by studies showing that meditation increases the global α-activity while decreasing the subjective sensation of pain (Kakigi et al., 2005; Lagopoulos et al., 2009).

EIMD provides an interesting model for investigating the effect of structural damage and acute pain on α-activity, particularly in the first 12 h after EIMD when neuromuscular changes occur with minor symptoms of pain (Plattner et al., 2011). Therefore, the aim of this study was to investigate the effects of EIMD and determine whether there is a relationship between the peripheral symptoms, the neuromuscular changes and delayed pain sensation and cortical α-1 and α-2 activity.

We hypothesize that a compensatory increase in α-1 activity will be displayed over the motor and somatosensory cortex of the experimental group compared with the control group in response to changes in neuromuscular function. We further hypothesize that an increase in α-2 activity is associated with the suppression of the sensation of pain experienced within the first 12 h after the EIMD-inducing protocol was performed.

Methods

  1. Top of page
  2. Abstract
  3. Methods
  4. Results
  5. Discussion
  6. Perspectives
  7. Conflict of interest
  8. Acknowledgements
  9. Funding
  10. Ethical approval
  11. References

Thirty-seven right-handed male participants, aged 21–40 years, were recruited for this study. Handedness was determined by the Edinburgh handedness inventory (Oldfield, 1971). Participants matched for age, height, weight, body fat, and skinfold thickness, were allocated to the experimental or control group. All participants had to be free of any upper body injuries and were not participating in any upper body training during the last 12 weeks before the study. This included the engagement in exercises involving specific muscle lengthening under tension movements.

Prior to being informed about the study design and familiarization with the equipment, participants had to sign an informed consent form and complete a Physical Activity Readiness Questionnaire (American College of Sports Medicine, 2007). They were also asked to complete questionnaires about their injury and training history. Participants were informed about the study design, familiarized with the equipment, and signed the consent form before starting the study. The study was approved by the Human Ethics Committee of the Faculty of Health Science, University of Cape Town. The principles outlined by the Declaration of Helsinki for the use of humans were adopted in this study (World Medical Association, 2002).

Study design

Before the start of the study, all participants were familiarized with the testing equipment and different test protocols. Figure 1 is a time line depicting the order of tests performed over the 7-day testing period. To minimize the effect of circadian rhythm on any of the outcome measures, all tests were scheduled at the same time of the day (within 60 min). This however, was not possible for the measurement at 12 h after the exercise protocol.

figure

Figure 1. Timeline of measurements. The exercise-induced muscle damage (EIMD) indicators include, pain, arm circumference, elbow angle, and creatine kinase activity. EEG, electroencephalography.

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Twelve hours before the start of exercise protocol (see also Fig. 1), stature, body mass, body fat percentage, and skinfolds of each participant was measured. In addition, resting elbow angle, elbow muscle function (MVC), biceps girth, and pain scores were measured. A blood sample was taken to determine creatine kinase (CK) activity.

EEG activity was measured during a self-initiated self-paced flexion–extension movement. In contrast to all the measurements mentioned earlier, that were conducted at −12, 12, 36, 60, 84, 108, and 132 h, EEG measurements were only captured at −12, 12, 36, and 132 h (Fig. 1). These measurements were time consuming for the participants and there was concern about poor compliance if they were required to be tested more frequently.

Exercise protocol

Twelve hours after baseline testing, the subjects in the experimental group completed an exercise protocol designed to induce muscle damage (EIMD protocol). In brief, participants were asked to resist the lengthening movement of the left biceps [five sets of 25 movements; see also “muscle function tests” section for set up of the Biodex (Biodex Pro 3, New York, NY, USA)]. The resistance to these movements was set on a Biodex dynamometer at 80% of each subject's maximum isometric contraction torque, as this has been shown to induce EIMD (Plattner et al., 2011). The control group did not perform this exercise protocol.

Muscle function tests

The muscle function tests consisted of a MVC measurement and a self-paced submaximal flexion–extension movement. The experimental and the control group performed these muscle function tests.

The MVC was measured using a Biodex dynamometer when performing elbow flexion of the left arm. For this, the participant sat on the chair of the Biodex dynamometer with their upper body and left upper arm securely strapped to the dynamometer, while the left forearm was only able to move in the sagittal plane (flexion/extension), In this position, participants were able to freely flex and extend their elbow over a range of approximately 120°, without hyperextending the elbow. The rotation axis of the dynamometer was aligned with the lateral epicondyle of the humerus, while the forearm was fixed into a fully supinated position. This ensured that the flexion–extension movement was carried out in the transversal axis and sagittal plane. Participants were asked to perform three 5-s isometric elbow contractions at maximal effort, with a fixed dynamometer arm angle of 45°. This setup will result in an elbow angle at about 60°, which is within the optimal length tension curve range (Saxton & Donnelly, 1996; Chang et al., 1999). Participants were asked to perform three 5-s MVCs interspaced by 60-s recovery periods, as previously described (Plattner et al., 2011).

The flexion–extension movement was not performed on the Biodex, but rather, the participants were seated on a standard armless-chair. Their arms were relaxed and hanging by their sides. For the submaximal self-paced flexion and extension movements, all participants wore a 1-kg wrist strap and movements were performed in the sagittal plane between elbow angles of 180° and 90°. During the movements, subjects were asked to look at a fixed point at the wall to reduce the interference of eye movements on the EEG measurement (see also EEG evaluation). In addition, the upper body and upper arm were positioned as described in the MVC setup for standardization purposes. Participants were asked to perform 75 repetitions, which were interspaced by 5- to 10-s recovery periods with slightly longer rest periods after each 25 repetitions, while EEG data were captured.

EEG study procedure

The EEG data were obtained in a darkened, sound-attenuated, temperature-controlled room to minimize the effect of confounding factors. Participants were instructed how to perform the self-paced flexion and extension movements. EEG activity was measured during the 75 submaximal, fast self-paced flexion and extension movements. In addition, subjects were asked to keep their eyes open and focused on a fixed spot on the wall during the submaximal self-paced movements.

EEG recording

An EEG net with 128 recording sites plus a vertex reference electrode (electrode 129) Electrical Geodesic ™ system [Electrical Geodesics, Inc (EGI), Eugene, OR, USA] (Bernier et al., 2007), which measures the electrical activity on the surface of the scalp, was fitted onto each participant (see Fig. 2 for an electrode layout). The impedance of all electrodes was maintained below 50 kΩ as suggested by the manufacturer of the EGI system and different technical references (Bernier et al., 2007; Murias et al., 2007; Keil & Muller, 2010) because of the high input resistance of the EEG amplifier. Specially designed amplifiers processed the high impedance signal. EEG was recorded using a 0.1–50 Hz bandpass filter (3 dB attenuation) (Murias et al., 2007). The signals were sampled at 250 Hz (Bernier et al., 2007; Murias et al., 2007). All recordings were initially referenced to the central reference electrode (Cz/129) (Bernier et al., 2007; Murias et al., 2007). The EEG system was connected to an experimental workstation (Net Station software 4.2.3, EGI; Apple Inc desktop, Cupertino, CA, USA) (Bernier et al., 2007).

figure

Figure 2. A layout of the EGI 129 channel system overlaid by the 10:20 electrode system (dark grey circles). Ellipses represent the following gross cortical areas: grey (frontal), green (premotor), orange (supplementary motor), blue (motor), red (somatosensory), yellow (parietal), and purple (occipital).

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EEG data analysis

The raw EEG data were 50 Hz notch filtered as well as 1–40 Hz bandpass filtered. Following this, the data for each trial were segmented into 3-s epochs (Thompson et al., 2008). Data were collected continuously during the premovement, movement and rest phase and therefore represent the common state of the brain during a biceps brachii movement protocol rather than a movement-induced change.

The EEG was re-referenced against an average reference (Bertrand et al., 1985; Bernier et al., 2007; Keil & Muller, 2010), which made data recorded in the reference electrode (Cz/129) available for analysis. The EEG recording was monitored for movement, eye movement, blink artifacts, and noise by an amplitude threshold criterion. Epochs were excluded if the eye blink threshold exceeded 140 μV and the eye movement threshold exceeded 55 μV. Ocular artifacts were also detected by a slope threshold, if the slope of a channel increased more than than 14 μV/ms, that channel was discarded within that epoch. The amplitude of a given channel was excluded in that epoch if it exceeded ±150 μV, and in such a case is replaced by an estimated calculation of the values of the surrounding channels. This was performed by computer algorithms built into the Net Station software version 4.2.3 (Murias et al., 2007).

After the automated artifact rejection algorithm, all epochs were also visually inspected offline and the recordings in which artifacts could not be removed were manually discarded before further data analysis took place.

While shorter epochs might reveal the relationship between, for example, spectral estimates or time-locked events, our intent was to characterize background brain states (induced activity) rather than specific components of event related processing (Travis et al., 2002). Subjects who had less than 40 usable, artifact-free epochs per trial day were excluded from further analysis. A fast Fourier transform (FFT) with a Welchen window was performed to obtain the spectral information of an epoch of each subject. Hereafter the data were exported to Microsoft Excel© (Microsoft, Redmont, WA, USA) and each subject's data were averaged before further analysis.

The different frequency bands used in this study were as follows: α-1 (7.81–9.77 Hz) and α-2 (10.74–12.7 Hz). Thereafter the relative power (activity) for each frequency on each day was calculated with the following formula: {[Power(12 or 36 or 132 h] − Power(0 h)/Power(0 h)}*100. The different relative power values for each subject on the different testing days were used to calculate the statistical differences between the two different groups on the four different testing days.

Matlab 6.5 (The Mathworks Inc, Natick, MA, USA) and EEGlab v 5.02 (SCCN, University of California, San Diego, CA, USA) were used to create topographical maps of the relative power on each day in each frequency.

Recorded data are represented based on the 10:20 system. All electrodes are grouped according to electrode on the 10:20 system, which represents the same area. For example the 10:20 electrode Fz is represented by electrodes 5, 6, 11, and 12 in the Netstation system (Fig. 2).

Other measurements

Blood samples, biceps girth, resting elbow angle, and a pain score were measured daily as previously described by Plattner et al. (2011). For the blood sample 5 mL of blood were drawn from the right antecubital vein. These samples were stored (−20 °C) and later analyzed to determine the serum CK activity in the blood (Beckman DU-62, Beckman Instruments, Fullerton, CA, USA) as described previously (Lambert et al., 2002). The girth of the left biceps was measured with a tape measure midway between the acromion and radial bony landmarks, that was marked with a permanent marker for repeatability purposes (Lambert et al., 2002). Resting elbow angles, and by implication the resting length of the biceps muscle, were measured with a goniometer (Lambert et al., 2002). Current pain perception was measured on a daily basis before the muscle function test with the use of a 10-cm visual analog scale (VAS) (Svensson et al., 1998).

Statistical analysis

An independent t-test was used to compare the descriptive data between experimental and control group, using STATISTICA 8.0 data analysis software (StatSoft, Inc, Tulsa, OK, USA).

As some of the data sets in this study had an unequal variance, determined using Levene's test of homogeneity of variance, it was decided to use nonparametric statistical tests instead of the parametric analysis of variance test. A Kruskal–Wallis test (H) compared the differences between the control and experimental group on each of the testing days in each electrode separately. A Friedman's test (X2) was used to compare changes within each group over the repeated testing days in each electrode separately. A Dunn's test was used for post-hoc analysis. Statistical significance was accepted at P < 0.05.

Results

  1. Top of page
  2. Abstract
  3. Methods
  4. Results
  5. Discussion
  6. Perspectives
  7. Conflict of interest
  8. Acknowledgements
  9. Funding
  10. Ethical approval
  11. References

The Friedmann's and Kruskal–Wallis' statistical results are presented in the Results section. To keep the figures straightforward, only the P-values of the Kruskal–Wallis test were used.

Characteristics of subjects

One participant did not finish the entire trial and was excluded from the study. Seven other participants were also excluded because they did not have sufficient EEG data epochs for further analysis. The remaining 28 participants were divided into two groups similar in weight, height, age, skinfold thickness, and handedness (Table 1).

Table 1. Descriptive data for the control (n = 12) and experimental groups (n = 16)
VariableControlExperimental
  1. Data are expressed as mean ± standard deviation.

Age (years)23 ± 423 ± 3
Body mass (kg)71.1 ± 8.872.7 ± 11.3
Stature (cm)171.7 ± 6.8177.4 ± 8.0
Body fat (%)15.9 ± 4.913.4 ± 5.4
Skinfolds (mm)79 ± 3769 ± 38
Handedness (%)73 ± 2079 ± 19

Muscle soreness

The difference in pain in the left arm in the experimental and control group measured by the VAS scale is shown in Fig. 3(a). Peak pain in the experimental group occurred 36 h after the EIMD-inducing protocol (X2 = 53.66 P < 0.00001). A difference in pain between the two groups occurred at 12 (H = 7.48 P < 0.01), 36 (H = 14.32 P < 0.001), 60 (H = 10.21 P < 0.01), 84 (H = 8.03 P < 0.01), and 108 h (H = 8.37 P < 0.01). Significant changes in pain occurred in the experimental group compared with the baseline value at 12, 36, 60, 84, and 108 h (X2 = 53.66 P < 0.00001) (Fig. 3(a)).

figure

Figure 3. (a) The change in current pain measured with the visual analog scale (VAS). (b) The change in the difference in relaxed elbow girth (cm) between the left and right arm. (c) The change in the difference in elbow angle (degrees) between the left and right arm. (d) The change in creatine kinase activity (U/L1). (e) The maximal force output produced on seven consecutive days. *Indicates results of the Kruskal–Wallis nonparametric test in the control (•) and experimental (°) group on seven consecutive days. *P < 0.05; **P < 0.01; ***P < 0.001.

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Arm circumference

During the experiment, there was a significant increase in the difference in girth between the exercised and rested arm in the experimental group compared with the control group at 36 (H = 7.23 P < 0.01), 60 (H = 6.97 P < 0.01), 84 (H = 5.36 P < 0.05), and 108 h (H = 5.04 P < 0.05). Significant changes in arm circumference were also found over time in the experimental groupcompared with the baseline value at 36, 60, and 84 h (X2 = 27.04 P < 0.0001). The difference between the left and right biceps girth of the control group did not change throughout the experiment. The difference between the left and right biceps girth of the control group did not change throughout the experiment (Fig. 3(b)).

Resting elbow joint angle (muscle length)

The difference in resting joint angle between the left and right arms in the control and the experimental group are shown in Fig. 3(c). There was a significant decrease in elbow joint angle in the experimental group until 84 h after the EIMD protocol (X2 = 42.46 P < 0.0001). The difference in joint angle decreased in the experimental group compared with the control group and reached its minimum 36 h (H = 7.34 P < 0.01) after the exercise protocol. It remained decreased until 108 h (H = 6.71 P = 0.01) after the exercise protocol. No changes in the resting elbow joint angle over time were observed in the control group (Fig. 3(c)).

Serum CK activity

The serum CK activity in the experimental group increased at 36 h (H = 3.90 P < 0.05) and reached its highest values compared with the control group at 84 (H = 3.99 P < 0.05), 108 (H = 4.87 P < 0.05) and 132 h (H = 5.27 P < 0.05) after the EIMD protocol. CK activity in the experimental group was only significantly increased compared with baseline at 108 and 132 h (X2 = 20.27 P < 0.01). The serum CK activity in the control group did not change during the experiment (Fig. 3(d)).

Muscle function

Muscle function, as measured by MVC (Fig. 3(e)), decreased significantly in the experimental group compared with the control group on all but one visit to the laboratory after the EIMD-inducing protocol (P < 0.05). The largest decrease in maximal force output was observed within the first 12 h after the EIMD protocol in the experimental group (H = 14.14 P < 0.001) while there were no changes in the control group throughout the experiment. The force output in the experimental group remained different to that of the control group until the end of the trial (H = 5.61 P < 0.05) (Fig. 3(e)).

A difference was also observed in the force output of the experimental group over time at 12, 36, 60, and 84 h compared with the baseline measurement (X2 = 48.3 P < 0.0001). There were no changes in the control group over time.

Alpha 1

Figures 4 and 6 show significant differences between the control and experimental group at 12 and 36 h after the exercise protocol. The most increases are seen 12 h after the exercise protocol, although changes remain at 36 h especially in the electrodes overlying the motor and somatosensory areas (Cz, C3, and C4).

figure

Figure 4. The global change (%) of α-1 activity measured with 129 electrodes over the scalp is shown in the control (a) and experimental (b) group. An outline of the electrodes showing significant differences between the two groups (c) at each time point is also shown.

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At 12 h after the EIMD protocol, there was a widespread increase in α-1 power over the motor and somatosensory area in the experimental group compared with the control group. This is seen especially atelectrodesrepresenting the central motor area surrounding C3, C4, and Cz.

Thirty-six hours after the exercise protocol, differences were still observed between the experimental and control groups, especially in the electrodes overlying the medial motor area.

To simplify the understanding of the results, electrodes have been placed into subgroups and labeled with the title of the closest electrode represented on the 10:20 system.

Frontal

12h
Fz and F4. 

Electrodes 6 and 113 (H > 4.56 P < 0.05) placed on the frontal area of the cortex show significant differences between the groups.

36 and 132h

No changes were seen in electrodes over the frontal area 36 or 132 h after the protocol, which induced the muscle damage.

Central

12h
T3. 

A significant differences was found in electrode 47 (H = 4.56 P < 0.05), which is located between C3 and T3.

C3. 

In the ipsilateral central area surrounding electrode C3 significant differences were seen in electrodes, 31, 32, 36, 37, 42, and 48 (H > 4.17 P < 0.05), and electrodes 38 and 43 (H > 7.76 P < 0.01) where α-1 activity increases were significant in the experimental vs the control group.

Cz. 

Significant changes between the two groups were also seen over the vertex (Cz) of the head in electrodes 7 (H = 6.28 P < 0.05) as well as 81 and 129 (H > 7.76 P < 0.01).

C4. 

Significant differences were also seen in the central area contralateral to the moving arm in electrodes 99 and 105 (H = 5.61 P < 0.05) as well as 104, 106, and 111 (H > 7.00 P < 0.01).

36h
Cz. 

The largest differences were recorded in the three electrodes surrounding the vertex area, electrodes 7, 107, and 129 (H > 4.17 P < 0.05).

C3. 

Differences occurred between the experimental and the control group at electrodes 32 and 38 (H > 4.76 P < 0.05) in the motor area ipsilateral to the movement (between C3 and Cz).

C4. 

Differences occurred between the groups in electrode 99 (H = 6.76 P < 0.01).

132h

No differences were observed in α-1 activity between the two groups at 132 h.

Parietal and temporal area

12h
P3 and Pz. 

There were significant differences in electrode 53 (H = 3.99 P < 0.05), representing P3, and also in electrode 55 (H = 8.28 P < 0.01) representing Pz.

T4. 

Further down in the temporal areas, there was a significant difference between groups (electrode 103; H = 7.77 P < 0.01).

36 and 132h

No differences were observed in α-1 activity in the parietal or temporal region between the two groups at 36 or 132 h.

Alpha 2

Figures 5 and 7 show that there are significant differences in the α-2 activity between the control and experimental groups at 12 and 36 h after the exercise protocol.

figure

Figure 5. The global change (%) of α-2 activity measured with 129 electrodes over the scalp is shown in the control (a) and experimental (b) group. An outline of the electrodes showing significant differences between the two groups (c) at each time point is also shown.

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Frontal

12h
F3. 

In the ipsilateral frontal area only one electrode was significantly different, electrode 29 (H = 4.56 P < 0.05).

Fz. 

In the medial frontal area, electrodes 4, 6, and 12 (H > 3.99 P < 0.05) were significantly different between the two groups.

F4. 

In the contralateral frontal area electrodes 112, 119, and 124 (H > 4.76 P < 0.05) as well as 113 and 118 (H > 7.25 P < 0.01), there were significant differences between the groups while in the ipsilateral frontal area, only one electrode (29) showed significant differences (H = 4.56 P < 0.05).

36 and 132h

No changes were seen in electrodes over the frontal area 36 or 132 h after the protocol, which induced muscle damage.

Central

12h
C3. 

Differences between groups occurred in the ipsilateral central area at electrode 42, 43 and 48 (H > 4.97 P < 0.05).

Cz. 

In the medial central area at electrodes 107 and 129 (H > 4.76 P < 0.05) there were differences between the groups.

C4. 

In the contralateral central area surrounding C4, there were differences between groups at electrodes 88, 105 (H > 5.17 P < 0.05), and 106 (H = 11.80 P = 0.001).

36h
C4. 

Significant differences between groups occurred in electrodes 88, 105, and 111 (H > 4.17 P < 0.05).

132h

No differences were observed in the central area between the two groups at 132 h.

Parietal

12h
P3. 

The difference between groups occurred in the parietal area at 52 (H = 7.50 P < 0.01), and 60 (H = 4.17 P < 0.05).

Pz. 

Of the electrodes representing Pz, only electrode 55 (H = 5.61 P < 0.05) showed significant differences between the groups.

36h
P4. 

There were significant differences between groups in electrode 87 (H = 6.28 P < 0.05).

132h

No differences were observed in the parietal area between the two groups at 132 h.

Discussion

  1. Top of page
  2. Abstract
  3. Methods
  4. Results
  5. Discussion
  6. Perspectives
  7. Conflict of interest
  8. Acknowledgements
  9. Funding
  10. Ethical approval
  11. References

The first finding of this study was that the EIMD protocol resulted in similar physiological responses (Fig. 3) reflecting muscle damage in the experimental group as previously reported (Plattner et al., 2011).

In particular, the symptoms of EIMD (swelling, muscle shortening, and CK activity) changed in the typical way for the duration of the experiment (Fig. 3(a–d)). Also, muscle function (force output) was impaired immediately after the EIMD protocol (Semmler et al., 2007; Plattner et al., 2011) and gradually recovered, but did not return to baseline by 132 h (Fig. 3(e)). On the other hand, pain progressively increased, peaking around 36–60 h and was decreasing at 132 h.

The following sections will discuss α-1 and α-2 activity separately, as the two bands have shown to be active in separate cortical areas between the groups. The authors acknowledge that deducing functional and anatomical associations from EEG data is challenging, but they do believe that the clustering of significant differences in certain areas do support the association with areas and functionality.

Alpha 1

The participants with symptoms of EIMD experienced an increase in cortical α-1 activity (Figs. 4 and 6) while performing a series of brisk biceps brachii contractions. The increase in the experimental group was most noticeable at 12 h post-EIMD induction (Fig. 4(b)), and activity had decreased, although still significantly different between the two groups, by 36 h post (Fig. 4(b, c)). The difference in activity between the groups was most pronounced in electrodes overlying the motor and somatosensory cortex (Fig. 4(c)).

figure

Figure 6. Nine different electrodes representative of the change (%) of α-1 activity in the frontal, central and parietal areas of the brain. Each of the electrodes represents a location on the 10:20 system. *Indicates results of the Kruskal–Wallis nonparametric test in the control (•) and experimental (°) group. *P < 0.05; **P < 0.01.

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Increased α-1 activity in the somatosensory and motor cortex has previously been associated with movement planning (Anderson & Ding, 2011), as well as increased consciousness and perception (Palva & Palva, 2007). Altered perception, reflected in the increased α-1 activity, might be a response to changed peripheral bottom-up feedback. Feedback about changes in peripheral neuromuscular function [greater movement unsteadiness, increased submaximal EMG activity and decreased force output (Semmler et al., 2007; Plattner et al., 2011)] is integrated and processed by the central nervous system.

The increase in α-1 activity could also be a result of precise movement planning and execution in the motor and somatosensory cortex to compensate (feedforward) for the loss in neuromuscular function while experiencing the symptoms of EIMD, indicated by the increased submaximal EMG activity.

We have previously shown (using the same protocol) that submaximal EMG activity increases within the first 12–36 h after the induction of EIMD, while maximal EMG and force output decrease (Plattner et al., 2011). It has been suggested that the increased submaximal EMG activity is due to increased neural drive initiated by the central nervous system (McAuley et al., 1997; Semmler et al., 2007). Thus our current findings of increased cortical α-1 activity in electrodes overlying the motor and somatosensory area together with the previous findings of increased submaximal and decreased maximal EMG activity at 12 and 36 h post-EIMD support our hypothesis that the motor and somatosensory cortex act as a compensatory upstream regulator of motor control while experiencing EIMD.

While it cannot be clearly stated what causes the increases in α-1 activity over the motor and somatosensory area in the EIMD group, it is suggested that increased cortical α-1 activity might be necessary to counteract the loss of movement steadiness and force output while experiencing EIMD. Because of the recording of α-1 activity in this proximal location, the authors assume it to be a top-down regulator of peripheral function. Therefore, the increased α-1activity could be part of an upstream regulatory mechanism of motor perception, activation, and neuromuscular function.

Alpha 2

While α-1 activity increased in the motor and somatosensory areas, α-2 activity increased in the ipsilateral fronto-parietal area as well as in the contralateral fronto-central areas.

α-2 activity peaked at 12 h (Figs. 5 and 7), when neuromuscular function was already disturbed, although the main sensation of pain was yet to develop. At 36 h post-EIMD induction, α-2 activity remained elevated in the contralateral centro-parietal area. Pain peaked at 36 h while α-2 activity decreased again toward pre-EIMD values.

figure

Figure 7. Nine different electrodes representative of the change (%) of α-2 activity in the frontal, central and parietal areas of the brain. Each of the electrodes represents a location on the 10:20 system. *Indicates results of the Kruskal–Wallis nonparametric test in the control (•) and experimental (°) group. *P < 0.05; **P < 0.01.

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It has previously been shown that α-2 activity increases because of interactions between the frontal and parietal cortical areas. Palva and Palva (2007) and Halgren et al. (2002) proposed that this fronto-parietal α synchrony is associated with focused attention, working memory, conscious perception, cognition, and action. As this is assumed to be the most proximal level of control, this fronto-parietal α synchrony is known to act as a top-down regulator in subcortical and peripheral information integration processes (von Stein et al., 2000).

Klimesch et al. (2007) have further suggested that increased α-2 activity in cortical areas causes an inhibition of information retrieval from the involved areas. Hence, the authors suggested the increase in α activity to be an inhibitory top-down control mechanism of information integration processes. A similar cortical top-down regulator has been suggested for pain (Chen & Herrmann, 2001), stating that the painful signal is perceived and incorporated at different frequency levels and areas of the cortex, with the somatosensory and the frontal cortex playing an important part.

Further research by Kakigi and Lagopoulos (Kakigi et al., 2005; Lagopoulos et al., 2009) showed that meditation increased α-2 activity while simultaneously decreasing the sensation of pain. Following this trend, Babiloni et al. (2005) showed that α-2 activity decreases in the contralateral hemisphere with the induction of a combined stimulus of pain and movement (Babiloni et al., 2005). In addition, the perception of pain, especially limb pain, has been further localized to the dorsolateral prefrontal, the primary somatosensory, motor, and supplementary motor cortex (Lorenz et al., 2003).

The earlier mentioned findings support the existence of a relationship between increased α-2 activity in the contralateral premotor, motor, and somatosensory cortex, and the subsequent inhibited perception of pain12 h post-EIMD induction (von Stein et al., 2000; Lorenz et al., 2003; Palva & Palva, 2007; Egsgaard et al., 2009). Therefore an increased α-2 activity in our cohort might be responsible for the dissociation between the sensation of pain and the changes in neuromuscular function caused by the exercise-induced muscle damage. This is of clinical importance as pain during the first 12 h after the induction of EIMD does not reflect on the amount of damage caused.

Therefore, we propose that an increased contralateral fronto-central α-2 activity acts as a cortical top-down regulator of the perception of pain 12 h post-EIMD induction and therefore leads to the delayed onset pain response associated with EIMD.

There was a visible increase in α-2 activity in the control group at 132 h (Fig. 5b), but this was not significant. We suggest that these changes are a consequence ofa learning or familiarization phenomenon, although we have no descriptive data to confirm this. As a result of repetitive testing sessions, control participants probably had a lower attentiveness and increased movement automation (Zhuang et al., 1997). An increase in α-1 and α-2 is associated with this lower attentiveness (Sauseng et al., 2006).

This novel study explored the relationship between the neuromuscular changes and the pain induced by an EIMD protocol and associated changes in EEG α-1 and α-2 activity. However, our study investigated changes in induced α activity, rather than event-related α activity, and therefore includes, pre movement, movement, and post movement recordings. The aim was to investigate the influence of pain and changed neuromuscular function on α activity during a movement task. Also, our data were not baseline corrected, but rather compared with pre-EIMD protocol values to identify differences in activity between the groups post- vs pre-EIMD induction, rather than comparing rest to movement on each recording day, as this would have removed the effect of the pain state on the data. Therefore, the authors cannot conclude if the described EEG changes are related to the pain or state or due to movement, but can only suggest that there are changes in EEG while subjects experienced EIMD compared with subjects who did not experience EIMD. The authors acknowledge that other factors such as changes in pain pathways or inflammatory processes could have lead to the dissociated response of neuromuscular changes and the delayed pain response, but the interest of this study was how EIMD and its associated symptoms affected the α-1 and α-2 activity measured over the cortical areas. Further research is needed to integrate not only the pain and neuromuscular response with the EEG recordings, but also possible inflammatory changes and adaptations in the pain pathways. Future studies should consider correlations between EMG and EEG, separate measurements during rest and movement as well as look at a broader spectrum of EEG frequencies (including beta, theta, and gamma).

Therefore, we propose that the increase in α-1 activity, 12 h after the EIMD protocol, may be part of a neurocognitive top-down regulator of neuromuscular function (Proske et al., 2004; Kakigi et al., 2005; Sauseng et al., 2005; Klimesch et al., 2007), and that α-2 activity may be a top-down regulator that suppresses the sensation of pain (Kakigi et al., 2005; Sauseng et al., 2005; Klimesch et al., 2007).

Perspectives

  1. Top of page
  2. Abstract
  3. Methods
  4. Results
  5. Discussion
  6. Perspectives
  7. Conflict of interest
  8. Acknowledgements
  9. Funding
  10. Ethical approval
  11. References

Over decades changes in peripheral symptoms associated with EIMD have been documented. Structural changes, increases in serum CK activity, inflammatory processes, swelling, and decreased neuromuscular functioning have been well reported, but none have provided adequate explanations for the delayed pain response associated with EIMD (Semmler et al., 2007; Plattner et al., 2011). Therefore, the novel approach of this study was to explore the response of the central nervous system, especially the cortical α-1 and α-2 activities, peripheral symptoms and delayed pain response to EIMD caused by the unaccustomed exercise. There is surmounting evidence that these brain areas and frequencies may regulate the pain response acutely (12 h) while experiencing the symptoms of EIMD during movement. Therefore, future research should investigate further associations between EIMD, delayed pain, and neuromuscular responses linking EEG, EMG, and fMRI measures to unravel the afferent and efferent interactions between the muscle and the brain during EIMD. In the future, the information could add to the understanding and management of EIMD in athletes.

Acknowledgements

  1. Top of page
  2. Abstract
  3. Methods
  4. Results
  5. Discussion
  6. Perspectives
  7. Conflict of interest
  8. Acknowledgements
  9. Funding
  10. Ethical approval
  11. References

The authors would like to thank all participants of this study. Robert Lamberts, PhD is thanked for his kind assistance with the figures.

Funding

  1. Top of page
  2. Abstract
  3. Methods
  4. Results
  5. Discussion
  6. Perspectives
  7. Conflict of interest
  8. Acknowledgements
  9. Funding
  10. Ethical approval
  11. References

This study was funded by the Medical Research Council of South Africa, Discovery Health and the University of Cape Town.

Ethical approval

  1. Top of page
  2. Abstract
  3. Methods
  4. Results
  5. Discussion
  6. Perspectives
  7. Conflict of interest
  8. Acknowledgements
  9. Funding
  10. Ethical approval
  11. References

The study was approved by the Human Ethics Committee of the Faculty of Health (REC REF: 090/2004), University of Cape Town, while the principles outlined by the Declaration of Helsinki were adopted in this study (World Medical Association, 2002).

References

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  3. Methods
  4. Results
  5. Discussion
  6. Perspectives
  7. Conflict of interest
  8. Acknowledgements
  9. Funding
  10. Ethical approval
  11. References
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