Shoulder Kinematic and Muscle Activity Compensations to Scapular Stabilizer Weakness: An Optimal Control Framework

Shoulder Kinematic and Muscle Activity Compensations to Scapular Stabilizer Weakness: An Optimal Control Framework

Abstract

Purpose Shoulder kinematic and muscular redundancy promotes considerable variability, obscuring possible insights into neuromuscular control and compensation mechanisms for muscle weakness or fatigue. The current study harnessed recent advancements in optimal control formulations for computational musculoskeletal models to determine potential neuromuscular control strategies to compensate for isolated muscle weakness.

Methods A computational shoulder model characterized by independent clavicular, scapular, and humeral kinematics and one hundred thirty-eight muscle elements was used. Optimal control-predicted thoracohumeral elevation kinematics were validated against published empirical kinematics. Force-generating capacity of the upper trapezius, middle trapezius, and lower trapezius, and serratus anterior were individually limited to seventy-five percent, fifty percent, and twenty-five percent maximal capacity to generate subsequent optimal control predictions of scapulothoracic kinematic changes associated with muscle weakness. Combined limited maximal force-generating capacity of lower trapezius and serratus anterior was also explored.

Results Model-predicted scapulothoracic kinematics showed good agreement with reference data, yet some significant differences were identified below fifty-five degrees thoracohumeral elevation. Fatigue-mediated kinematic changes were most apparent during sagittal plane elevation. Serratus anterior weakness displayed the largest scapulothoracic kinematic changes at all thresholds of limited force-generating capacity. It also prompted the largest compensatory muscle activity changes from other shoulder muscles, while upper trapezius weakness prompted very little compensatory changes in muscle activity.

Conclusion Optimal control simulations were used to identify potential compensation mechanisms for shoulder muscle weakness and predict their effects on scapular kinematics. Findings suggest that thoracohumeral elevation in the scapular plane displayed less trapezius coactivity, both when 'weakened' and 'unweakened.' Thus, scapular plane tasks may isolate serratus anterior, while frontal plane tasks may achieve more balanced coactivation.

Introduction

High interindividual (between individuals) and intraindividual (within an individual) variability in shoulder muscle activity and control precludes the ability to make inferences on the effects of targeted muscle stimuli on upper limb kinematics. This variability is likely consequent of the seemingly highly redundant muscular and kinematic degrees of freedom at the shoulder that affords primates a wide landscape of potential solutions to nearly every upper limb task. Scapulothoracic kinematic variability has challenged the characterization of normal/healthy and abnormal/unhealthy scapulothoracic kinematics and muscle synergies. Recent works propose a critical perspective that muscle coactivation patterns associated with scapular stability (upper trapezius dominance, lower trapezius, and serratus anterior weakness) which were long considered to be 'unhealthy' by clinicians and researchers may in fact be a product of the morphological and anthropomorphic variability in scapular shape and muscle moment arms which promote a vast distribution of 'normal/healthy' shoulder muscle activity and kinematics.

A caveat of the inherent variability in scapulothoracic kinematics is that it can be difficult to characterize the kinematic contributions of individual shoulder muscles, which could otherwise help identify how the redundant set of shoulder joint effectors characterize the landscape of available motor control solutions. Muscle fatigue can sometimes provide an ecologically valid framework for assessing muscle control and compensation schemes in otherwise 'healthy' individuals, by observing how they respond to disruptions in muscle force-generating capacity. This framework is complex and multifaceted, however, as several peripheral and central adaptations occur due to fatigue, which are difficult to fully characterize. Scapulothoracic kinematics changes associated with fatiguing stimuli - stimuli that would transiently reduce the force-generating capacity of muscles that attach to the scapula - are frequently reported in the literature. However, interventions that attempt to fatigue an isolated set of one or more of the scapular stabilizer muscles (upper trapezius, middle trapezius, lower trapezius, and serratus anterior), rotator cuff muscles (supraspinatus, infraspinatus, subscapularis, teres minor), or tasks that stress the global shoulder musculature frequently report inconclusive findings, obscured by unclear trends swathed in variable responses. As we previously reported, individuals may even adopt opposing or bimodal scapulothoracic kinematic responses to fatigue following an overhead drilling task, illustrating how the landscape of redundancy in shoulder control may be so broad as to encompass completely opposing kinematic effects of fatigue. While intraindividual variability is a less commonly reported metric, Mulla et al. provided further evidence of opposing kinematic changes with fatigue, reporting scapular plane kinematic differences within individuals of up to ten degrees in the opposite direction across successive completions of a rotator cuff fatigue task. Similar levels of variability are consistent with other reports, which is considerable given that changes in static scapulothoracic angle of only five degrees may be clinically meaningful for injury risk. Importantly, such magnitudes of muscular and kinematic variability have the potential to obscure significant fatigue-related relationships in a very practical sense, by decreasing the calculated P-value of traditional hypothesis-based statistical tests.

While high variability may obscure shoulder muscle compensations to fatigue, comparisons of shoulder muscle fatigue-related effects across the literature are also complicated by the many different fatigue protocols employed. In addition, methodological limitations including the apparent error in skin-based scapular motion tracking, EMG artifacts and errors between the sensor and the muscle of interest due to muscle movement underneath the skin, and the difficulty in capturing and characterizing the full breadth of muscles which contribute to shoulder motion due to their number, many partitions, and depth may limit a comprehensive understanding of the kinematic-muscular relationship at the shoulder.

Computational musculoskeletal modeling tools may offer comprehensive insights into the muscular-kinematic relationship at the shoulder. Such models replace observations of empirical data from an in vivo model with simulated data which are derived from a set of biomechanical equations, constraints, and assumptions about the biomechanical system. One of the most extensively cited computational shoulder models, the Delft Shoulder and Elbow Model, is well regarded for its anatomical fidelity, which has been bolstered with three decades of model validation and updates. An implicit method for rapidly formulating optimal control problems as ordinary differential equations, harnessed with standard non-linear program solvers, has been integrated with a current version of the DSEM to offer upper limb optimal control solutions within six to twenty-four hours. Such timeframes were previously unachievable, hindered by mechanically stiff musculoskeletal elements which required timesteps one thousand five hundred times smaller to solve using explicit ordinary differential equations. Such advancements in optimal control formulation and stability make problems with low mass and high stiffness elements like the clavicle and scapula more accessible for exploring the muscle-kinematic relationship at the shoulder.

The purpose of this study was to use a computational musculoskeletal model of the shoulder to predict scapulothoracic kinematics changes associated with isolated reduced force-generating capacity of the scapular stabilizer muscles. A secondary aim of this study was to determine the model-predicted scapular stabilizer muscle activity compensations associated with isolated reductions in force-generating capacity of the scapular stabilizer muscles. We hypothesize that progressively reduced force-generating capacity will result in progressively altered scapulothoracic kinematics, and that scapular stabilizer muscle activity will progressively increase to compensate for simulated weakness.