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 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 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.
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 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).