Long-term physical exercise and somatosensory event-related potentials
We have compared the occurrence patterns of somatosensory event-related potentials (ERPs) in athletes (soccer players) and non-athletes. ERPs were elicited by two oddball tasks following separate somatosensory stimulation at the median nerve (upper-limb task) and at the tibial nerve (lower-limb task). In the athlete group the N140 amplitudes were larger during upper- and lower-limb tasks and the P300 amplitude and latency were larger and shorter, respectively, during the lower-limb task compared with non-athletes. On the other hand, no significant differences in the P300 amplitude and latency during the upper-limb task were observed between the athlete and non-athlete groups. These results indicate that plastic changes in somatosensory processing might be induced by performing physical exercises that require attention and skilled movements.
KeywordsEvent-related potentialsPhysical exerciseSkilled movementSomatosensory stimulation
Peripheral input is known to play an important role in the acquisition of motor skills. It has been demonstrated that the acquisition of new skills is very difficult for cats (Sakamoto et al. 1989) and monkeys (Pavlides et al. 1993) following ablation of their somatosensory cortex. In particular, corticocortical projections from the somatosensory cortex to the motor cortex (Waters et al. 1982; Mori et al.1989) contribute to motor learning by producing long-term potentiation in the motor cortex (Asanuma and Pavlides 1997).
Most physical exercises include the acquisition and execution of complicated motor skills. However, very few studies have examined the relationship between physical exercise and somatosensory processing (Thomas and Mitchell 1996).
On the other hand, it has been demonstrated that the P300 component of event-related potentials (ERPs), but not the other ERP components, are modulated during visual or auditory stimulation tasks by the execution of physical exercise (Rossi et al. 1992; Polich and Lardon 1997). However, we are not aware of any study that has examined these effects on ERPs during somatosensory stimulation tasks.
In the present study we examined somatosensory ERPs following lower-limb stimulation in soccer players. These athletes perform skilled lower-limb movements during a soccer game or their daily training. Therefore, their ERP patterns might differ from those of non-athletes. We also studied the effects on somatosensory ERPs following upper-limb stimulation in the same athletes.
Materials and methods
Seven male athletes performing soccer and seven male non-athletes were examined. The athletes belonged to the soccer club of their college, and had participated in the intercollegiate competitions. The non-athletes did not participate regularly in any physical sports activity. Individuals from the athlete and the non-athlete group were matched for age (21.8 years vs.18.7 years, respectively) and body mass index (22.05 vs. 21.61, respectively). However, the average time spent performing vigorous physical exercise over the previous 1-year period differed significantly between the two groups (9.85 h/week vs. 0.5 h/week for the athlete and non-athlete groups, respectively). Both groups were assessed during their typical weekly schedules, which included periods of exercise. No subjects reported any neurological or psychiatric problems. All subjects gave informed consent prior to the study. This study was approved by the local ethics review board.
The subjects were seated in a reclining armchair in a quiet and electrically shielded room. Somatosensory ERPs were elicited by two oddball tasks. In session 1 ERPs were obtained by applying electrical stimuli to the left median nerve at the wrist (upper-limb task). In session 2, ERPs were obtained by applying electric stimuli to the left posterior tibial nerve at the ankle (lower-limb task). These stimulation tasks were composed of two kinds of electric pulse, each with a duration of 0.2 ms: a weak stimulus (1.5 times the sensory threshold) and a strong stimulus (1.1 times the motor threshold). The probability of the strong stimulus being a target was 20%, and that of the weak stimulus being standard was 80%. The rate of repetition was 2–4 s at random.
During the recording period, the subjects were instructed to keep their eyes open and to look at a small fixation point positioned approximately 1 m in front of them. The subjects were instructed to respond by pressing a button with the thumb of their right hand as quickly as possible whenever a deviant stimulus was presented. A common response pattern was used for target stimulation in the upper- and lower-limb tasks, because the P3 amplitude for a button-pressing response is affected by the overlapping of movement-related cortical potentials (MRCPs) (Barret et al. 1987). If the response pattern of the lower-limb task was different from that of the upper-limb task, it would have been impossible to distinguish differences between the P300 amplitudes during lower-limb tasks between the athlete and non-athlete groups from those related to the MRCPs. Therefore, a common response pattern for both tasks was used to investigate the effects of physical exercise on the P300 amplitudes.
Electroencephalograms (EEGs) recordings and data analyses
EEGs were recorded using Ag–AgCl electrodes placed on the scalp at Fz, Cz, Pz, C3, and C4, according to the international 10/20 system. Each scalp electrode was referenced to linked earlobes. The electro-oculogram was recorded bipolarly from the right outer canthus and the suborbital region to monitor eye movements or blinks. The electrode impedance was kept below 5 kΩ, the amplifier band pass was set at 0.1–300 Hz, and the digitization rate was 1 kHz.
The analysis epoch for the ERPs was 800 ms, which included a prestimulus baseline period of 200 ms. The peak latencies of the N140 and P300 components measured from the time window, were 144–195 ms and 299–423 ms, respectively, for the upper-limb task and 163–242 ms and 332–450 ms, respectively, for the lower-limb task. The waveforms were averaged with an evoked EEG analysis program (Eplyzer II, Kissei-Comtec) with off-line processing. Response errors were excluded from the analysis. One ERP trial block consisted of 40 artifact-free target stimuli presented for each stimulus task.
The peak amplitudes and latencies of the ERP components were analyzed using a three-way mixed-type analysis of variance (ANOVA) with group (athlete group, non-athlete group), task (upper-limb task, lower-limb task), and electrode (Fz, Cz, Pz, C3, C4) as subject variables. The percentage of correct answers was analyzed using a two-way mixed type ANOVA for group (athlete group, non-athlete group) and task (upper-limb task, lower-limb task). The reported significances for the F values were obtained after Greenhouse–Geisser correction. In addition, a post hoc paired t-test adjusted for differences in amplitudes and latencies was used to compare data from the athlete group and the non-athlete group. Statistical significance was set at P<0.05.
Mean amplitudes and latencies for each task in the athlete and non-athlete groups. Data are expressed as means (standard deviations)
Upper limb task
Lower limb task
The percentage of correct answers for the upper-limb task in the athlete and non-athlete groups was 96.4±2.5% and 93.3±4.8%, respectively, while that for the lower-limb task was 90.5±16.6% and 82.5±12.1%, respectively. The response accuracies of the athlete and non-athlete groups were not different (F(1,12)=1.912, P=0.19).
Peak latency and amplitude analysis
A significant group–electrode interaction was observed for the N140 amplitude (F(2.8,33.7)=4.689, P<0.01). Further analysis of the effect of group on each electrode showed that the N140 amplitude in the athlete group was more negative than in the non-athlete group at Fz, C3, and C4 (P<0.05 for each electrode).
A significant main-task effect was also observed for N140 latency (F(1,12)=22.107, P<0.001). This result shows that the N140 latency was longer for the lower-limb task than for the upper-limb task.
A significant main-group effect was observed for the P300 amplitude (F(1,12)=19.948, P<0.001). This result shows that the P300 amplitude was larger in the athlete group than in the non-athlete group. In addition, a post hoc test showed that the P300 amplitude was larger in the athlete group than in the non-athlete group at Fz, Cz, Pz, C3, and C4 during the lower-limb task (P<0.01 for each electrode), but no significant differences were observed during the upper-limb task.
A significant group–task interaction was also observed for the P300 latency (F(1,12)=11.303, P<0.01). Further analysis of the effect of group on each task showed that the P300 latency was longer in the non-athlete group than in the athlete group during the lower-limb task (F(1,12)=5.152, P<0.05), but no significant differences were observed during the upper-limb task (F(1,12)=0.076, P=0.78).
In the present study the athlete group exhibited larger N140 amplitudes during both the upper- and lower-limb tasks compared to the non-athlete group. On the other hand, the P300 amplitude was significantly larger and the P300 latency was significant shorter in the athlete group than in the non-athlete group during the lower-limb task, although no significant differences were observed between the athlete and non-athlete groups during the upper-limb task.
A relationship between the N140 component and physical exercise has not been reported previously; however, the N140 component is known to be functionally analogous to the auditory or visual N1 component (Desmedt et al. 1977). The relationship between auditory or visual N1 components and history of intensive physical exercise has been studied previously (Polich and Lardon 1997), but no significant effects on amplitude or latency were observed between the exercise group and the non-exercise group. Therefore, the enhanced response observed in the athlete group in the present study might reflect the involvement of a different mechanism from that examined in the previous study. Many studies have reported that an increase in N140 amplitude is related to selective attention (Michie et al. 1987; Eimer and Forster 2003). In general, sports activities are greatly influenced by the state of attention. In particular, rapid shifts from broad to selective attention are important for the successful performance of open-skill activities (Fontani and Lodi 1999). In the present study, the attention abilities of the athletes, who play an open-skill game (soccer) might have been superior to those of the non-athletes because of the development of various attention styles that occurs during continuous sports training in athletes.
In the present study, the athlete group demonstrated significantly larger N140 amplitudes in bilateral frontal lobes during upper- and lower-limb tasks. Frontal N140 has been suggested to reflect activation of bilateral frontal lobes involving orbitofrontal cortex and lateral and mesial cortex (Allison et al. 1989, 1992). These results indicate that activation of the frontal cortex in athletes might be affected by the attentional ability associated with physical training.
The lack of a significant effect on the auditory or visual N1 components noted in the previous studies might be attributable to different characteristics of the exercise performed in the exercise group.
The P300 component, however, was significantly different between the athlete group and the non-athlete group during the lower-limb task but not during the upper-limb task. Previous studies have reported that P300 latency is related to stimulus evaluation (Kutas et al.1977) and that P300 amplitudes are related proportionally to the amount of attentional resources devoted to a given task (Wickens et al. 1983). Moreover, it has been demonstrated that P300 amplitude and latency are modulated by the improved attentional abilities achieved by athletes who regularly take part in open-skill games (Rossi et al. 1992; Fontani and Lodi 1999).
It has been suggested that temporal-parietal connection, frontal and posterior association cortex, and medial temporal region are responsible for the generation of the somatosensory P300 component (Yamaguchi and Knight 1991; Valeriani et al. 2001). In the present study, the athlete group demonstrated a significantly larger P300 amplitude and a shorter P300 latency in extensive regions during the lower-limb task. This observation might support to the need for extensive training to perform the complicated, skilled lower-limb movements used during soccer games or soccer daily training. These results indicate that projections between the somatosensory association area to the temporal and frontal areas might contribute to the acquisition and execution of compound motor skills. Indeed, primate studies have shown the existence of substantial anatomical connections between the posterior association cortex and these regions (Mesulam et al. 1977).
It has been demonstrated that the projection from somatosensory cortex to motor cortex plays an important role in learning motor skills in cats (Sakamoto et al. 1989) and monkeys (Pavlides et al. 1993). Furthermore, the somatosensory cortex was shown to be activated by physical exercise in humans (Thomas and Mitchell 1996) and other animals (Senturk et al. 2000).
We suggest that the increased P300 amplitudes and reduced latencies observed in the athlete group imply that plasticity might drive not only the somatosensory cortex but also somatosensory cognitive processing by the execution of physical exercise. These reinforced neuronal networks might be induced by acquisition and execution of compound motor skills during daily extensive training. These results indicate that plastic changes in somatosensory processing might be induced by performing physical exercises that require attention and skilled movements.