The aim of the present study was to describe the infraspinatus muscle cortical representation, in terms of excitability and location, as well as to assess its symmetry between the dominant and non-dominant sides in healthy individuals. In addition, the influence of age and gender on motor excitability was also explored. Data from healthy males and females from a wide range of ages are reported, which is important to inform future research in populations with impaired shoulder function. Our results on the symmetry of cortical representations indicate no significant difference between the dominant and non-dominant sides. No effect of age or gender was found on motor excitability.
Some authors have reported dominance and age as factors influencing motor excitability [17, 18]. However, the evidence on the effect of these variable remains conflicting, with more recent studies showing no impact for these variables, as well as no influence from gender [19, 20]. Most importantly, these studies all focused on intrinsic hand muscles. The present results extend these findings by demonstrating that the motor representation of a proximal muscle is similar between sides in healthy individuals, both in terms of excitability and location.
TMS measurements were performed with the muscle slightly contracted (5% MVC). Responses elicited in proximal muscles, such as RC muscles, with the arm at rest are very slight and require high intensities of stimulation [21]. Pilot experiments revealed that it was impossible to map the infraspinatus at rest (and to stimulate at 120 and 140% of resting MT) in several individuals because of high thresholds. It is noteworthy to mention that the posture and level of contraction used for active motor mapping in the present study were determined in order to be easily achievable in most patients with impaired/painful shoulder. A previous study by our research group showed that resting and active cortical maps are similar for hand muscles in healthy individuals, and that both methods provide reliable measures [15].
The infraspinatus is a humeral lateral rotator that has its origins on the infraspinatus fossa of the scapula and its insertion on the greater tubercle of the humerus. One of its primary functions is to depress the humeral head during arm elevation, which prevents subacromial impingement. The infraspinatus is the only RC muscle for which there are no other muscles located between its own muscle tissue and the skin [2]. Therefore, it provides the most direct recording of all RC muscles. EMG activity of the supraspinatus and teres minor could also be evaluated by using surface electrodes, providing the feasibility of evaluating their M1 representations using TMS; however, EMG crosstalk is a bigger issue in this case. The site for recording the supraspinatus using surface electrodes is located over a window where the tendon of the trapezius lies between the muscle and the skin [2]. Therefore, as suggested by Brown et al. [2], the recording may pick up some end-propagating activation from the trapezius. As for the teres minor, it lies deep into the infraspinatus and is assessed from the infraspinatus surface electrode site [2]. Still, Brown et al. [2] have shown that the correlations between skin surface and fine-wire electrodes were high for the supraspinatus and teres minor; however, they were lower than the ones found for the infraspinatus. Possibility of performing cortical mapping of the supraspinatus and teres minor might be explored in the future. Finally, it is not possible to evaluate the subscapularis using surface electrodes as the muscle has its origin from the subscapularis fossa of the scapula, which provides no site for surface electrodes.
Moreover, alterations in infraspinatus muscle activity have been found in populations with shoulder disorders. For instance, in individuals with RC tendinopathy, EMG activity of the infraspinatus has been shown to be significantly decreased between 30 and 60° of shoulder elevation [3]; while during shoulder lateral rotation, significantly less infraspinatus EMG activity was observed on the symptomatic shoulder [4]. Furthermore, a study evaluating the most common location of degenerative RC tears reported that most degenerative cuff tears initiate from a region near the junction of the supraspinatus and infraspinatus tendons [5]. It proves the significant role of the infraspinatus in the stabilization of the glenohumeral joint and in the etiology of chronic RC disorders.
It has been hypothesized that a reorganization of the motor cortex could explain part of the motor control deficits linked to RC disorders [11, 22, 23]. These central changes could contribute to the chronicity of symptoms. This hypothesis of central changes is based on previous studies that have shown reorganization in the central nervous system in patients with other MSK disorders [24, 25]. For example, in patients with patellofemoral pain, On et al. found that the amplitude of MEP produced in quadriceps was significantly increased compared to healthy individuals [6]. Tsao et al. [7] found that the CoG of motor cortical map of the transversus abdominis was more posterior and lateral in patients with recurrent low back pain. Locations of the CoG and map volumes were also correlated with the onset of transversus abdominis EMG during rapid arm movements, suggesting that changes in motor cortical organization could be linked to altered motor control. Therefore, as a fundamental muscle for shoulder stability, better knowledge of the cortical representation of infraspinatus muscle in healthy individuals is important.
Particular concerns for the assessment of changes in cortical representation in MSK disorders affecting the upper limbs relate to the fact that some asymmetry might be related to dominance, an aspect particularly important to control, given that the incidence of RC tendinopathy is higher on the dominant side [11]. The present results suggest that dominance should not be a concern when comparing the motor representation of affected vs. unaffected shoulders in clinical studies. However, this does not indicate that a unilateral MSK disorder cannot affect both hemispheres. An interesting illustration of such bilateral impacts of a MSK lesion was recently provided by Langer et al. [26]. They showed that immobilization (≥14 days) after an upper limb injury resulted not only in a decrease in cortical thickness in the primary motor and somatosensory area corresponding to the injured side, but in an improvement of the motor skills of the non-injured hand that was related to an increase in cortical thickness in the motor cortex corresponding to the non-injured side.
One possible limitation of the present study is that the EMG activity of the infraspinatus was recorded using surface electrodes. The infraspinatus could be seen as a challenging muscle to record with surface electrodes, given that there is only a small window overlying the infraspinatus process where it is possible to directly record EMG activity. Therefore, crosstalk by the trapezius and deltoid is highly probable if the electrode placement is not done accurately. In order to minimize crosstalk, we used standardized procedures for electrode placement that have proven to lead to EMG data in high correlation with data recorded with fine-wire electrodes [2]. Furthermore, verification of electrodes placement and EMG signal quality was done by visual monitoring of signals while subjects performed voluntary contractions. Nevertheless, future studies could validate the present results by using fine-wire electrodes. Finally, the use of surface electrodes simplifies the evaluation of motor representation, which is important to consider if TMS evaluation is to be used in clinical settings.