Sex differences in leg dexterity are not present in elite athletes

Abstract

We studied whether the time-varying forces that control unstable foot–ground interactions provide insight into the neural control of dynamic leg function. Twenty elite (10 F, 26.4 ± 3.5 yrs) and 20 recreational (10 F, 24.8 ± 2.4 yrs) athletes used an isolated leg to maximally compress a slender spring designed to buckle at low forces while seated. The foot forces during the compression at the edge of instability quantify the maximal sensorimotor ability to control dynamic foot–ground interactions. Using the nonlinear analysis technique of attractor reconstruction, we characterized the spatial (interquartile range IQR) and geometric (trajectory length TL, volume V, and sum of edge lengths SE) features of the dynamical behavior of those force time series. ANOVA confirmed the already published effect of sex, and a new effect of athletic ability, respectively, in TL (p = 0.014 and p < 0.001), IQR (p = 0.008 and p < 0.001), V (p = 0.034 and p = 0.002), and SE (p = 0.033 and p < 0.001). Further analysis revealed that, for recreational athletes, females exhibited weaker corrective actions and greater stochasticity than males as per their greater mean values of TL (p = 0.003), IQR (p = 0.018), V (p = 0.017), and SE (p = 0.025). Importantly, sex differences disappeared in elite athletes. These results provide an empirical link between sex, athletic ability, and nonlinear dynamical control. This is a first step in understanding the sensorimotor mechanisms for control of unstable foot–ground interactions. Given that females suffer a greater incidence of non-contact knee ligament injuries, these non-invasive and practical metrics of leg dexterity may be both indicators of athletic ability, and predictors of risk of injury.

Introduction

It is well accepted that female athletes have a four to ten times greater incidence of non-contact knee injury than their male counterparts, particularly in agility-based sports (Hewett, 1999, Huston and Wojtys, 1996, Stanley, 2016, Yoo, 2010). It is speculated that sex differences in anatomical structure and function including joint alignment (Q-angle), ligament laxity, strength, hormonal levels, and more recently, neuromuscular control are major contributors for the disproportionate number of injuries in females (Hewett, 2000, Hewett, 1999, Yoo, 2010). When considering an isolated joint (e.g., knee) during leg function, sensorimotor control is of considerable importance in terms of preventing injuries, particularly anterior cruciate ligament (ACL) tears. Males tend to exhibit muscle-dominant neuromuscular strategies to control joint stability, while females display ligament-dominant strategies (Hewett, 2000). This muscle-dominant strategy is described as a protective mechanism to reduce strain on the joint ligaments during dynamic motions. Sex differences in muscle recruitment patterns and synergies are also well reported and speculated to be contributors to the increased injury risk in female athletes (Hewett, 1999, Lephart, 2002, Tsai, 2012).

Neuromuscular and sensorimotor (e.g., plyometric and proprioceptive) training programs have been introduced to athletic training regimens because they have been shown to improve movement biomechanics and joint stability, thus reducing the likelihood of leg injury (Benjaminse, 2015, Hewett, 2000, Hewett, 1999, Mandelbaum, 2005, Myer, 2005, Yoo, 2010). For example, Hewett et al. reported decreased peak landing forces and ab/adduction moments at the knee, increased hamstring-to-quadriceps peak torque ratios, and corrections in hamstring strength imbalances during the landing phases of vertical jumps after a six-week plyometric training program (Hewett, 1996). Another neuromuscular training study showed increased flexion/extension knee range of motion and decreased varus and valgus knee moments during the landing phase of a vertical jump (Myer, 2005). While the biomechanical benefits of neuromuscular and sensorimotor training have been extensively documented, to our knowledge, the effect of long-term athletic-based neuromuscular training on sensorimotor processing for leg dexterity has not been investigated. We define “dexterity” as originally described by Valero-Cuevas (Valero-Cuevas, 2003). Namely, it is the ability to use movements and force vectors to stabilize a slender spring prone to buckling. It was originally developed for fingers (Dayanidhi, 2013, Dayanidhi and Valero-Cuevas, 2014, Venkadesan et al., 2007), and then adapted into a lower extremity dexterity test to quantify the dynamical ability to stabilize unstable foot-ground interactions (Lawrence, 2014, Lyle, 2013). We have previously reported sex differences in this leg version in young soccer players (Lyle, 2015) and across the lifespan (Lawrence, 2014) and proposed that may contribute to the disproportionate higher number of non-contact ACL injuries in female athletes compared to males. As such, it is important to understand the influence of athletic ability—likely, in part, a result of long-term exposure to athletic training regimens—on sensorimotor control for leg dexterity.

The integration of sensory and motor systems for whole-body dynamic activities is inherently complex. This makes quantification of the functional domain of sensorimotor processing difficult. Traditional measures of leg function during whole-body activity are confounded by the contribution of the functional domains of strength and/or limb coordination—let alone vestibular function, visual acuity, posture control, risk aversion, etc. However, we have shown that different versions of the Valero-Cuevas dexterity test quantify the functional domain of sensorimotor processing, as distinct from the functional domains of strength and limb coordination, in fingers (Dayanidhi, 2013, Dayanidhi and Valero-Cuevas, 2014, Lawrence, 2014, Valero-Cuevas, 2003) and legs (Lawrence, 2015) (Fig. 1). This simple, yet reliable, test requires participants to compress a slender spring prone to buckling at low forces to a maximal steady state level (Lyle, 2013, Valero-Cuevas, 2003). The spring becomes increasingly unstable as it is compressed (i.e., undergoes a bifurcation in instability (Venkadesan et al., 2007), and one’s ability to compress and hold the spring at the edge of instability is a measure of the person's sensorimotor control capabilities (Dayanidhi, 2013, Dayanidhi and Valero-Cuevas, 2014, Lawrence, 2014, Valero-Cuevas, 2003, Venkadesan et al., 2007). Unfortunately, the fact that subjects can reliably control the spring at the edge of instability only for the few seconds produces time series that are not well suited for many classical nonlinear dynamical measures (i.e., maximal Lyapunov Exponent, Correlation Dimension) that require longer time series (Kantz and Schreiber, 2004, Wolf, 1985). We recently showed that a nonlinear dynamical approach to the analysis of the time-varying compression forces at the edge of instability is more robust than traditional linear analyses (e.g., mean compression force, and root-mean square (RMS)) to quantify sensorimotor processing for finger dexterity, and can even distinguish the effects of healthy aging from those of mild-to-moderate degenerative neurologic conditions such as Parkinson's disease (Peppoloni, 2017). Here we extend that work and apply the delayed embedding theorem (Takens’ theorem (Takens, 1985), to reconstruct the phase portraits from time series of foot forces collected during the leg dexterity test from both elite (highly-skilled) and recreational (moderately-skilled) athletes. Our goal is to explore the influences of sex and athletic ability on sensorimotor processing for leg dexterity, and its implications for the risk of knee ligament injury.