Sex differences in torque steadiness, accuracy and activation of the shoulder girdle muscles during isometric shoulder scaption

Sex is a biological risk factor for musculoskeletal disorders that has been highlighted in both the work and sport contexts (Côté, 2012, Theberge, 2012). The prevalence of neck/shoulder musculoskeletal disorders is higher among females than males (Arvidsson et al., 2006, Hooftman et al., 2009). Females and males without neck/shoulder musculoskeletal disorders may have different muscle activation strategies. Females have higher levels of trapezius activation than males during dynamic scaption (Szucs and Borstad, 2013). Moreover, in shoulder efforts, males have shown a focused recruitment of primary agonistic muscles, while females proportionally activate more accessory muscles (Anders et al., 2004, Otto et al., 2018). Sex differences have also been reported in the variability of the upper trapezius activation, with females showing lower variability than males (Srinivasan et al., 2016). Different muscle activation strategies are an important neuromuscular control mechanism to ensure adequate performance and joint stability (Riemann and Lephart, 2002). However, a recent review highlighted the meaningful lack of knowledge on sex differences in this field (Lulic-Kuryllo and Inglis, 2022). Moreover, whether sex differences in neuromuscular control of the shoulder muscles originates from sex differences in neural commands of the integrated sensorimotor system is a question largely unexplored.

Sensorimotor system centrally integrates and processes sensory, visual and motor components (Riemann and Lephart, 2002). In the clinical setting, sensorimotor control can be evaluated using a torque steadiness test (Bandholm et al., 2006). This test quantifies fluctuations in the torque produced during a submaximal contraction performed with visual feedback (Enoka et al., 2003). Fluctuations in torque result from adjustments in the activation of motor units in response to afferent information (Tracy, 2007). These fluctuations can be measured in amplitude based on standard deviation (SD) and coefficient of variation (CV) values and in the frequency domain by median frequency (MF) values (Camargo et al., 2009).

Efforts to investigate sex differences in torque steadiness and their possible causes have received recent attention (Jakobi et al., 2018). Females were shown to have higher torque CV values than males during submaximal isometric dorsiflexion associated with a higher incidence of doublet motor unit discharges, indicating that neural strategies may result in less steadiness in females (Inglis and Gabriel, 2021). In the upper body, higher CV values (i.e. higher torque fluctuations) were found in females compared to males during submaximal isometric flexion of the elbow (Brown et al., 2010, Harwood et al., 2014). On the other hand, Svendsen and Madeleine (2010) observed the opposite when elbow flexion torque fluctuations were quantified using SD values. Furthermore, these last authors did not observe sex differences in CV values. Therefore, sex differences in torque steadiness also depend on whether torque fluctuations are measured in absolute (SD) or normalized (CV) manner.

The sensorimotor system can also be explored through accuracy of the motor output. Accuracy reflects how the target is represented in the nervous system (Vafadar et al., 2015). The magnitude of the error can be quantified by absolute error (AE) values, and its direction by the constant error (CE) values (Vafadar et al., 2015). Minn and Côté (2018) showed no sex difference for shoulder joint error before and after performing a fatiguing task. However, females had less variability in the shoulder position relocation trials and tended to mostly overestimate the target than males, as males tended to both overestimate and underestimate the target (Vafadar et al., 2015), reinforcing the discrepancy in past results on this topic.

To our knowledge, sex comparisons in the torque steadiness and accuracy evaluation of the neck/shoulder region have not yet been studied. Knowing possible sex differences in the strategies adopted by the sensorimotor system in terms of steadiness and accuracy can help to understand part of the neural and biomechanics mechanisms related to sex differences in development of neck/shoulder musculoskeletal disorders. Thus, this study investigated sex differences in torque steadiness and accuracy with simultaneous recording of surface electromyographic signals (sEMG) of the shoulder girdle muscles during isometric shoulder scaption performed by healthy subjects. We hypothesized that females would have greater torque steadiness and accuracy that would equate to higher amplitude and lower variability of muscle activation, compared to males. The torque steadiness was measured based on SD, CV and MF values, while torque accuracy was quantified through the AE and CE values.

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