The goal of the present study is to compare the electrophysiological correlates of the threshold to detection of passive motion (TTDPM) among three groups: healthy individuals (control group), professional volleyball athletes with atrophy of the infraspinatus muscle on the dominant side, and athletes with no shoulder pathologies. More specifically, the study aims at assessing the effects of infraspinatus muscle atrophy on the cortical representation of the TTDPM. A proprioception testing device (PTD) was used to measure the TTDPM. The device passively moved the shoulder and participants were instructed to respond as soon as movement was detected (TTDPM) by pressing a button switch. Response latency was established as the delay between the stimulus (movement) and the response (button press). Electroencephalographic (EEG) and electromyographic (EMG) activities were recorded simultaneously. An analysis of variance (ANOVA) and subsequent post hoc tests indicated a significant difference in latency between the group of athletes without the atrophy when compared both to the group of athletes with the atrophy and to the control group. Furthermore, distinct patterns of cortical activity were observed in the three experimental groups. The results suggest that systematically trained motor abilities, as well as the atrophy of the infraspinatus muscle, change the cortical representation of the different stages of proprioceptive information processing and, ultimately, the cortical representation of the TTDPM.
The atrophy of the infraspinatus has been clinically recognized as corresponding to a suprascapular nerve palsy [
The high incidence of this pathology in volleyball players suggests that the nature of the game plays an important role in the pathogenesis of the atrophy of the infraspinatus muscle [
Proprioceptive ability in the shoulder is essential for correctly positioning the hand during serving and spiking in a volleyball match. In our knowledge, no investigations were published about proprioceptive deficits in a group of individuals with suprascapular neuropathy and no studies were conducted about the pattern of these deficits in the central nervous system. The identification of suprascapular neuropathy in elite volleyball players has suggested that a combination of traction, friction, and kinking of the nerve at points of tethering may induce nerve injury [
In this study, we hypothesized that infraspinatus muscle atrophy secondary to suprascapular nerve injury could provide proprioception deficit in shoulder joint. The proprioceptive deficits can be defined through the measure of TTDPM [
Electrophysiology has also been employed in the study of proprioception. Specifically, electrophysiological studies have investigated the cortical representation of passive motion [
The sample of the study consisted of 58 right-handed male volunteers, with ages ranging from 18 to 26 years old: 18 professional volleyball players with atrophy (PAG) of the infraspinatus muscle on the dominant side (Figure
Demographic table comparing the three groups.
Volleyball players ( |
Control group (CG) ( |
||
---|---|---|---|
Athletes with atrophy |
Athletes without atrophy (PG) ( |
||
Age | 29.4 (4.7) | 32.5 (4.1) | 30.3 (4.3) |
Weight (Kg) | 92.1 (8.3) | 95.9 (9.2) | 76.2 (9.2) |
Height (cm) | 196.0 (6.8) | 198.4 (7.8) | 181.2 (6.7) |
Professional volleyball player with atrophy of the infraspinatus muscle on the dominant side.
A motor-driven, proprioception testing device (PTD), which was developed at the Neuromuscular Research Laboratory of the National Institute of Traumatology and Orthopaedics (INTO) [
The apparatus and participant position for the experiment procedure.
Electroencephalographic (EEG) activity was acquired during the task with a 20-channel Braintech-3000 (EMSA-Medical Instruments, Rio de Janeiro, Brazil). The International 10/20 System [
A light- and sound-attenuated room was prepared for data acquisition. Participants were comfortably seated on a reclining chair attached to the PTD, with the dominant shoulder abducted at 90 degrees and rotated forward by 30 degrees so that the arm was in the same plane as the scapula. The elbow was flexed at 90 degrees [
The software Data Acquisition developed at Neuromuscular Research Laboratory (INTO, Rio de Janeiro, Brazil) used to acquire the EEG signal was developed at the. Visual inspection was used to detect and eliminate artifacts in the recordings. The data acquired had total amplitude of less than 100
Data collected during the experiment were processed with Matlab 5.3 (MathWorks, M, USA). The data were first averaged for each participant and then across participants. Considering all passive movement repetitions, response latency (i.e., millisecond) was established as the delay between the onset of the stimulus (passive movement) and the response (button press). EEG epochs were aligned to the pressing of the button-switch (trigger). The presence of EMG activity was used as an exclusion criterion, only to detect voluntary movement, since it signalizes the volunteer did not remain relaxed. Root mean square (RMS), defined as the square root of the mean square value for the EMG was calculated [
Response latencies and absolute power at beta and alpha frequencies were the dependent variables of interest. Statistical analysis was performed using SPSS for Windows—version 17.0 (SPSS Inc., Chicago, USA) and we employed an ANOVA one-way with repeated measure with subsequent post hoc tests to assess possible differences among the experimental groups for response latencies. To assess cortical activity, we analyzed absolute power at beta and alpha frequencies on the electrodes F3, C3 and P3. We performed an ANOVA two-way with repeated measure to investigate the relationship between the factor group (3 levels: professional volleyball players with atrophy of the infraspinatus muscle on the dominant side; volleyball players without the atrophy of infraspinatus; and healthy nonathlete controls) and the factor moment (2 levels: moment 1 represents 2 s before pressing the button switch; moment 2 represents 2 s after pressing the button switch). The group differences were tested using Scheffè post hoc test if ANOVA was significant.
The behavioral measure demonstrated a statistical difference between the PG when compared both to the PAG and to the CG (Table
Mean and standard deviation of the variables dependents.
Volleyball players ( |
Control group (CG) ( |
||
---|---|---|---|
Athletes with atrophy |
Athletes without atrophy (PG) ( |
||
Latency (ms) | 4,180 (260) | 2,237 (260) | 4,202 (247) |
Alpha-frequency ( |
|||
F3 | 23.78 (1.924) | 39.77 (1.785) | 34.66 (1.879) |
C3 | 11.51 (0.802) | 15.68 (0.744) | 11.36 (0.783) |
P3 | 31.34 (2.679) | 45.42 (2.486) | 32.92 (2.617) |
Beta-frequency ( |
|||
F3 | 17.17 (0.753) | 25.84 (0.699) | 10.38 (0.736) |
C3 | 8.12 (0.358) | 12.28 (0.332) | 4.50 (0.349) |
P3 | 11.98 (0.91) | 16.99 (0.844) | 12.05 (0.888) |
Latency variations among groups. The statistical analysis revealed that PG differs from PAG and CG (
Alpha Frequency. For the left frontal cortex (F3), we found a main effect for group with an absolute alpha power increase for the PG and an absolute alpha power decrease for the PAG (
Mean and standard deviation of absolute alpha power. The statistical analysis revealed a main effect for group (
Beta Frequency. We found a main effect for group in the three electrodes investigated, that is, F3 (
Mean and standard deviation of absolute beta power. The statistical analysis revealed a main effect for group (
The goal of the present study is to assess proprioception through the characterization of the TTDPM during internal rotation of the shoulder in professional volleyball athletes with atrophy of the infraspinatus muscle, and to assess the effects of the atrophy on the cortical representation of the TTDPM. We hypothesized that (1) athletes with atrophy of the infraspinatus show a greater delay in the detection of passive motion when compared to their peers without muscle atrophy. Pap et al. [
Researches have been conducted in the attempt to study proprioceptive deficits as assessed by the TTDPM. Lephart et al. [
The present study, therefore, substantiates these previous findings by showing that the PAG also presents proprioceptive deficits as assessed by the TTDPM. The PAG showed a significant delay in motion detection when compared to the PG and the CG. Moreover, PAG athletes have a behavior response similar to the CG. The two athlete groups were not different, a priori, with respect to two factors: training level and technical expertise. However, the two groups of athletes differed with respect to the presence of atrophy of the infraspinatus. The results indicate that there are significant differences in latency. Specifically, the PG detected the stimulus (i.e., passive motion) faster when compared to the PAG. This result supports the view that atrophy of the infraspinatus is a limiting factor for athletes, increasing the time of response to a sensory stimulus and, in this case, of passive motion detection.
The results indicate a significant difference between the two groups, the PG responded significantly faster, confirming that level of training and technical expertise are key factors in reducing the latency of detection of passive motion. Finally, when the PAG and the CG are compared, the results show no significant differences between groups. This result suggests that atrophy of the infraspinatus is a significant factor in the TTDPM increase and in the consequent speed reduction of the stimulus processing.
Our electrophysiological results showed a greater absolute beta and alpha power for the PG on the three electrodes investigated (i.e., C3, F3 and P3). The C3 and F3 electrodes represent the primary motor cortex and the premotor cortex, respectively. They are part of the sensorimotor cortex and are responsible for the movement planning and control [
Beta frequency is more sensible to sequencial and repetitive movement than alpha frequency [
The PG shows a high frequency oscillation concentrated around the motor response, suggesting that this group needed less time to detect the stimulus (i.e., passive motion) and started to prepare for the motor response (pressing the button switch) earlier in time. These data interpretations are supported by the latency results mentioned above, which showed that the PG was significantly faster in detecting passive motion when compared to the other two groups. In the CG, on the other hand, the oscillations pattern was spread and sustained in time, suggesting that this group needed more time to detect the stimulus, process the sensory information, and respond.
In the frontal (F3) and central (C3) regions, we found difference among the three groups (CG, PG, and PAG). The frontal region (F3) close related to the premotor cortex and the central area (C3) associated primary motor cortex were able to discriminate among the three groups. Specifically, these two regions which are associated directly with motor aspects could detect the difference between PG and PAG. Differently, the parietal region which traditionally is responsible to integrate different sources of information was not able to detect the difference between PG and PAG. The left parietal cortex in the absence of sensory information associated with infraspinatus muscle atrophy considered CG equals to PAG. Considering all the results together, beta absolute power supports our hypothesis on the sense that we can correlate different aspects of the pathology (e.g., infraspinatus muscle atrophy) with electrophysiological changes.
Overall, the results suggest that both consistently trained motor skills and the atrophy of the infraspinatus muscle alter the cortical representation of the various stages of proprioceptive information processing and, ultimately, the TTDPM cortical representation. In sum, by taking into account the different analyses of this study, we suggest that the dynamics of proprioceptive processing between the PAG and the PG is quantitatively different, as reflected by the significant difference in latency, and alpha and beta frequencies values. Future studies are necessary to thoroughly understand the effects of infraspinatus muscle atrophy as well as other pathologies on the proprioceptive abilities of athletes. Understanding the effects of this and other pathologies is fundamental for more adaptive training and treatment strategies of professional athletes. Future studies are also necessary to further explore the issue of the cortical representation of sensory deficits in different populations.
Our study has limitations related to clinical evaluation of infraspinatus atrophy and how to explain the pathophysiology of this condition. In the methodology proposed, we just define the presence of infraspinatus atrophy, once this clinical find cannot be quantified by physical exam, so we just did a qualitative analysis. We believe to quantify this atrophy is necessary the use of images of magnetic resonance, so that it could be graduate. Certainly it would be part of other study. Other issue is related to the pathophysiology of this isolated infraspinatus muscle atrophy. The literature states that isolated infraspinatus atrophy suggests selective suprascapular nerve injuries, specifically at the spinoglenoid notch, in the infraspinatus branch [