Arm load magnitude affects selective shoulder muscle activation

Frans Steenbrink 0 1 2 Carel G. M. Meskers 0 1 2 Bart van Vliet 0 1 2 Jorrit Slaman 0 1 2 H. E. J. Veeger 0 1 2 Jurriaan H. De Groot 0 1 2 Principal Action 0 1 2 0 H. E. J. Veeger Department of Biomechanical Engineering, Faculty of Mechanical, Maritime and Materials Engineering, Delft University of Technology , Delft, The Netherlands 1 B. van Vliet J. Slaman H. E. J. Veeger Department of Human Movement Sciences, Institute of Fundamental and Clinical Human Movement Sciences, Vrije Universiteit Amsterdam , Amsterdam, The Netherlands 2 F. Steenbrink (&) C. G. M. Meskers J. H. De Groot Laboratory for Kinematics and Neuromechanics, Departments of Orthopaedics and Rehabilitation Medicine, Leiden University Medical Center , Leiden, The Netherlands For isometric tasks, shoulder muscle forces are assumed to scale linearly with the external arm load magnitude, i.e., muscle force ratios are constant. Inverse dynamic modeling generally predicts such linear scaling behavior, with a critical role for the arbitrary load sharing criteria, i.e., the ''cost function''. We tested the linearity of the relation between external load magnitude exerted on the humerus and shoulder muscle activation. Six isometric force levels ranging from 17 to 100% of maximal arm force were exerted in 24 directions in a plane perpendicular to the longitudinal axis of the humerus. The direction of maximum muscle activation, the experimentally observed so called Principal Action (PA), was determined for each force magnitude in 12 healthy subjects. This experiment was also simulated with the Delft Shoulder and Elbow Model (DSEM) using two cost functions: (1) minimizing muscle stress and (2) a compound, energy related cost function. PA, both experimental (PAexp) and simulated (PAsim), was expected not to change with arm forces magnitudes. PAexp of the mm. trapezius pars descendens, deltoideus pars medialis and teres major changed substantially as a function of external force magnitude, indicating external load dependency of shoulder muscle activation. In DSEM simulations, using the stress cost function, small non-linearities in the muscle forceexternal load dependency were observed, originating from gravitational forces working on clavicular and scapular bone masses. More pronounced non-linearities were introduced by using the compound energy related cost function, but no similarity was observed between PAexp and PAsim. 1 Introduction Individual muscle forces change with armload direction. This load direction dependency was used to study muscle coordination in healthy subjects [1, 4, 10, 14, 18] and subjects with shoulder pathologies [5, 20]. The Principal Action (PA), which comprehends load direction dependent electromyography (EMG) parameters [4, 14], is used as a descriptive parameter for muscle coordination. In practice, repeated measurements are performed before and after an intervention, while maximum force around the shoulder may be altered by the intervention, e.g., by pain reduction or muscle tendon transfers [20]. In the comparison of these experiments, we assume that muscle forces scale linearly with external force magnitude. External forces may differ considerably in prepost measurements [5, 20] and interindividually [4, 18]. So linearity is a pre-requisite, or should be predictable if muscle contraction patterns are to be compared under these different loading conditions. In the jaw, linear scaling of muscle activity (EMG) and external load was indeed demonstrated [2, 25]. However, non-linear muscle activation scaling with external arm load was reported in the upper extremity [8]. In shoulder inverse dynamic modeling, linearity is generally assumed and incorporated in the load sharing criteria that are needed to mathematically solve the redundancy problem in order to reach a unique muscle activation pattern [3, 79, 21]. Praagman et al. [19] introduced a combination of a linear stress and a quadratic energy cost function, which turned out to fit best with non-linear in vivo obtained muscle energy expenditure around the elbow using near infrared spectroscopy. They stated that most cost functions are chosen rather arbitrary, mainly due to the fact that validation is difficult since muscle force cannot be measured accurately in vivo. The EMG based PA method offers an alternative method to compare in vivo observed activation simulated muscle activation, in order to interpret the experimental results and to predict possible load dependencies of shoulder muscle activation patterns in future studies [3, 4]. In the present study, we experimentally test the assumption that relative shoulder muscle forces do not change with armload magnitude. The experiment was numerically simulated, using the Delft Shoulder and Elbow Model (DSEM) with both a linear and an energy related cost function [19, 2224]. We used the PA, i.e. the direction of maximum muscle activation assessed by either EMG (experiment) or force (simulation), respectively PAexp and PAsim, as a parameter for muscle coordination. 2 Methods 2.1 Subjects Twelve healthy subjects (five female; three left handed) with a mean age of 26 (SD 2.9 years) took part in the study. The local medical ethical committee granted permission and all subjects gave informed consent. 2.2 Experimental setup Subjects were seated with the dominant arm in a splint with the elbow in 90 of flexion (Fig. 1). The set-up allowed for static, isometric contractions of shoulder muscles while loading the arm with a force of different magnitudes in different directions in a plane perpendicular to the humerus [3, 4, 18]. The humeral plane of elevation was approximately 60 rotated externally from the para-sagittal plane and the humerus was 60 abducted. The forearm was 45 externally rotated relative to the horizontal plane (see Fig. 1). The objective of the set-up was to record only forces perpendicular to the longitudinal axis of the humerus. In rest, the arm was fully supported by means of a weight and pulley system to compensate for all gravitational forces and moments [4, 18]. The arm splint was attached to a 3D force transducer (AMTI-300, Advanced Mechanical Technology, Inc., Watertown MA, USA) by means of a low friction ball and socket joint. The transducer was mounted on a low friction rail in line with the humerus. This construction allowed for movement of the arm along four degrees of freedom (three rotations and a translation), while translations along the axes perpendicular to the humerus long arm were constrained. These forces controlled the position of a cursor on a computer screen placed in front of the subjects [4, 18] (Fig. 1). EMG activity of 12 shoulder muscles was recorded (Table 1), and off-line post-processed [4, 18]. Nine shoulder muscles were recorded with the use of bipolar silver bar surface electrodes (DelSys, Bagnoli-16, Boston MA, USA, analog filter: 20 Hz high pass, 450 Hz low pass, 10 mm electrode length, inter-electrode distance of 10 mm). Fig. 1 Ex (...truncated)