Abstract
Purpose
Lowering a load could be associated with abnormal shoulder and scapular motion. We tested the hypothesis that lowering a load involves different shoulder muscle coordination strategies compared to lifting a load.
Methods
EMG activity of 13 muscles was recorded in 30 healthy volunteers who lifted and lowered a 6, 12 or 18 kg box between three shelves. Kinematics, EMG levels and muscle synergies, extracted using non-negative matrix factorization, were analyzed.
Results
We found greater muscle activity level during lowering in four muscles (+ 1–2% MVC in anterior deltoid, biceps brachii, serratus anterior and pectoralis major). The movements were performed faster during lifting (18.2 vs. 15.9 cm/s) but with similar hand paths and segment kinematics. The number of synergies was the same in both tasks. Two synergies were identified in ~ 75% of subjects, and one synergy in the others. Synergy #1 mainly activated prime movers’ muscles, while synergy #2 co-activated several antagonist muscles. Synergies’ structure was similar between lifting and lowering (Pearson’s r ≈ 0.9 for synergy #1 and 0.7–08 for synergy #2). Synergy #2 was more activated during lowering and explained the greater activity observed in anterior deltoid, serratus anterior and pectoralis.
Conclusion
Lifting and lowering a load were associated with similar synergy structure. In 3/4 of subjects, lowering movements involved greater activation of a “multiple antagonists” synergy. The other subjects co-contracted all shoulder muscles as a unit in both conditions. These inter-individual differences should be investigated in the occurrence of shoulder musculoskeletal disorders.
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Abbreviations
- BB:
-
biceps brachii
- DeltA:
-
deltoid (Anterior part)
- DeltM:
-
deltoid (Middle part)
- DeltP:
-
deltoid (Posterior part) of the deltoid
- InfE:
-
infraspinatus
- LD:
-
latissimus dorsi
- MVC:
-
Maximal voluntary contraction
- Pect:
-
pectoralis major
- SerrA:
-
serratus anterior
- SubS:
-
lower subscapularis
- SupE:
-
supraspinatus
- TB:
-
triceps brachii
- TraS:
-
trapezius (Superior part)
- TraL:
-
trapezius (Lower part)
- VAF:
-
Variance accounted for
References
Arborelius UP, Ekholm J, Nemeth G, Svensson O, Nisell R (1986) Shoulder joint load and muscular activity during lifting. Scand J Rehabil Med 18(2):71–82
Blache Y, Begon M (2017) Influence of shoulder kinematic estimate on joint and muscle mechanics predicted by musculoskeletal model. IEEE Trans Biomed Eng 65(4):715–722
Blache Y, Dal Maso F, Desmoulins L, Plamondon A, Begon M (2015) Superficial shoulder muscle co-activations during lifting tasks: influence of lifting height, weight and phase. J Electromyogr Kinesiol 25(2):355–362. https://doi.org/10.1016/j.jelekin.2014.11.004
Borstad JD, Ludewig PM (2002) Comparison of scapular kinematics between elevation and lowering of the arm in the scapular plane. Clin Biomech (Bristol, Avon) 17(9–10):650–659
Bouffard J, Martinez R, Plamondon A, Côté JN, Begon M (2019) Sex differences in glenohumeral muscle activation and coactivation during a box lifting task. Ergonomics 62(10):1327–1338. https://doi.org/10.1080/00140139.2019.1640396
Cheung VC, d'Avella A, Tresch MC, Bizzi E (2005) Central and sensory contributions to the activation and organization of muscle synergies during natural motor behaviors. J Neurosci 25(27):6419–6434
Christou EA, Carlton LG (2002) Motor output is more variable during eccentric compared with concentric contractions. Med Sci Sports Exerc 34(11):1773–1778. https://doi.org/10.1249/01.mss.0000035201.21310.cc
Cools AM, Declercq GA, Cambier DC, Mahieu NN, Witvrouw EE (2007) Trapezius activity and intramuscular balance during isokinetic exercise in overhead athletes with impingement symptoms. Scand J Med Sci Sports 17(1):25–33. https://doi.org/10.1111/j.1600-0838.2006.00570.x
d'Avella A, Fernandez L, Portone A, Lacquaniti F (2008) Modulation of phasic and tonic muscle synergies with reaching direction and speed. J Neurophysiol 100(3):1433–1454. https://doi.org/10.1152/jn.01377.2007
Dal Maso F, Marion P, Begon M (2016) Optimal combinations of isometric normalization tests for the production of maximum voluntary activation of the shoulder muscles. Arch Phys Med Rehabil 97(9):1542–1551 e1542. https://doi.org/10.1016/j.apmr.2015.12.024
Duchateau J, Enoka RM (2008) Neural control of shortening and lengthening contractions: influence of task constraints. J Physiol 586(24):5853–5864. https://doi.org/10.1113/jphysiol.2008.160747
Duchateau J, Enoka RM (2016) Neural control of lengthening contractions. J Exp Biol 219(Pt 2):197–204. https://doi.org/10.1242/jeb.123158
Ebaugh D, Finley M (2017) Muscle activation associated with scapular function and dysfunction. In: Kibler W, Sciascia A (eds) Disorders of the scapula and their role in shoulder injury. Springer, Cham. https://doi.org/10.1007/978-3-319-53584-5
Ebaugh DD, Spinelli BA (2010) Scapulothoracic motion and muscle activity during the raising and lowering phases of an overhead reaching task. J Electromyogr Kinesiol 20(2):199–205. https://doi.org/10.1016/j.jelekin.2009.04.001
Faria CD, Teixeira-Salmela LF, Gomes PF (2009) Applicability of the coactivation method in assessing synergies of the scapular stabilizing muscles. J Shoulder Elb Surg 18(5):764–772. https://doi.org/10.1016/j.jse.2009.02.019
Faulkner JA (2003) Terminology for contractions of muscles during shortening, while isometric, and during lengthening. J Appl Physiol (1985) 95(2):455–459. https://doi.org/10.1152/japplphysiol.00280.2003
Gaudet S, Tremblay J, Begon M (2018) Muscle recruitment patterns of the subscapularis, serratus anterior and other shoulder girdle muscles during isokinetic internal and external rotations. J Sports Sci 36(9):985–993. https://doi.org/10.1080/02640414.2017.1347697
Gribble PL, Mullin LI, Cothros N, Mattar A (2003) Role of cocontraction in arm movement accuracy. J Neurophysiol 89(5):2396–2405. https://doi.org/10.1152/jn.01020.2002
Hagen DA, Valero-Cuevas FJ (2017) Similar movements are associated with drastically different muscle contraction velocities. J Biomech 59:90–100
Hawkes DH, Alizadehkhaiyat O, Fisher AC, Kemp GJ, Roebuck MM, Frostick SP (2012a) Normal shoulder muscular activation and co-ordination during a shoulder elevation task based on activities of daily living: an electromyographic study. J Orthop Res 30(1):53–60. https://doi.org/10.1002/jor.21482
Hawkes DH, Alizadehkhaiyat O, Kemp GJ, Fisher AC, Roebuck MM, Frostick SP (2012b) Shoulder muscle activation and coordination in patients with a massive rotator cuff tear: an electromyographic study. J Orthop Res 30(7):1140–1146. https://doi.org/10.1002/jor.22051
Helwig NE, Hong S, Hsiao-Wecksler ET, Polk JD (2011) Methods to temporally align gait cycle data. J Biomech 44:561–566
Herzog W (2014) Mechanisms of enhanced force production in lengthening (eccentric) muscle contractions. J Appl Physiol (1985) 116(11):1407–1417. https://doi.org/10.1152/japplphysiol.00069.2013
Hudak PL, Amadio PC, Bombardier C, Beaton D, Cole D, Davis A, Hawker G, Katz JN, Makela M, Marx RG (1996) Development of an upper extremity outcome measure: the DASH (disabilities of the arm, shoulder, and head). Am J Ind Med 29(6):602–608
Hug F (2011) Can muscle coordination be precisely studied by surface electromyography? J Electromyogr Kinesiol 21(1):1–12
Hug F, Turpin NA, Couturier A, Dorel S (2011) Consistency of muscle synergies during pedaling across different mechanical constraints. J Neurophysiol 106(1):91–103. https://doi.org/10.1152/jn.01096.2010
Kopec JA, Esdaile JM, Abrahamowicz M, Abenhaim L, Wood-Dauphinee S, Lamping DL, Williams JI (1996) The Quebec back pain disability scale: conceptualization and development. J Clin Epidemiol 49(2):151–161
Kronberg M, Brostrom LA (1995) Electromyographic recordings in shoulder muscles during eccentric movements. Clin Orthop Relat Res 314:143–151
Labriola JE, Lee TQ, Debski RE, McMahon PJ (2005) Stability and instability of the glenohumeral joint: the role of shoulder muscles. J Shoulder Elb Surg 14(1):S32–S38
Lee DD, Seung HS (2001) Algorithms for non-negative matrix factorization. In: Leen TK, Dietterich TG, Tresp V (eds) Advances in neural information processing systems 13. MIT Press, pp 556–562
Llewellyn M, Yang JF, Prochazka A (1990) Human H-reflexes are smaller in difficult beam walking than in normal treadmill walking. Exp Brain Res 83(1):22–28
Ludewig PM, Lawrence RL (2017) Mechanics of the scapula in shoulder function and dysfunction. In: Kibler W, Sciascia A (eds) Disorders of the scapula and their role in shoulder injury. Springer, Cham, pp 7–23
Madeleine P (2010) On functional motor adaptations: from the quantification of motor strategies to the prevention of musculoskeletal disorders in the neck–shoulder region. Acta Physiol 199(s679):1–46
Magarey ME, Jones MA (2003) Dynamic evaluation and early management of altered motor control around the shoulder complex. Man Ther 8(4):195–206
Moraes GF, Faria CD, Teixeira-Salmela LF (2008) Scapular muscle recruitment patterns and isokinetic strength ratios of the shoulder rotator muscles in individuals with and without impingement syndrome. J Shoulder Elb Surg 17(1):S48–S53
Muceli S, Falla D, Farina D (2014) Reorganization of muscle synergies during multidirectional reaching in the horizontal plane with experimental muscle pain. J Neurophysiol 111(8):1615–1630
Nieminen H, Takala E, Niemi J, Viikari-Juntura E (1995) Muscular synergy in the shoulder during a fatiguing static contraction. Clin Biomech 10(6):309–317
Roh J, Rymer WZ, Beer RF (2012) Robustness of muscle synergies underlying three-dimensional force generation at the hand in healthy humans. J Neurophysiol 107(8):2123–2142. https://doi.org/10.1152/jn.00173.2011
Rossi DM, Resende RA, da Fonseca ST, de Oliveira AS (2018) Scapulothoracic kinematic pattern in the shoulder pain and scapular dyskinesis: a principal component analysis approach. J Biomech 77:138–145. https://doi.org/10.1016/j.jbiomech.2018.07.010
Safavynia SA, Torres-Oviedo G, Ting LH (2011) Muscle synergies: implications for clinical evaluation and rehabilitation of movement. Top Spinal Cord Inj Rehabil 17(1):16–24. https://doi.org/10.1310/sci1701-16
Steele KM, Rozumalski A, Schwartz MH (2015a) Muscle synergies and complexity of neuromuscular control during gait in cerebral palsy. Dev Med Child Neurol 57(12):1176–1182
Steele KM, Tresch MC, Perreault EJ (2015b) Consequences of biomechanically constrained tasks in the design and interpretation of synergy analyses. J Neurophysiol 00769:02013. https://doi.org/10.1152/jn.00769.2013
Thomas S, Reading J, Shephard RJ (1992) Revision of the physical activity readiness questionnaire (PAR-Q). Can J Sport Sci 17(4):338–345
Tresch MC, Jarc A (2009) The case for and against muscle synergies. Curr Opin Neurobiol 19(6):601–607
Veeger HE, van der Helm FC (2007) Shoulder function: the perfect compromise between mobility and stability. J Biomech 40(10):2119–2129. https://doi.org/10.1016/j.jbiomech.2006.10.016
Zheng Z, Yang J, Zhu Y (2007) Initialization enhancer for non-negative matrix factorization. Eng Appl Artif Intell 20(1):101–110
Funding
This study was funded by IRSST (#2014-0045) and NSERC discovery grants program (RGPIN-2014-0391) in Canada.
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NAT, RM and MB wrote the paper. NAT analyzed the data. RM and MB performed the experiments. MB designed the study. All authors approved the final manuscript.
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Communicated by Toshio Moritani.
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Turpin, N.A., Martinez, R. & Begon, M. Shoulder muscle activation strategies differ when lifting or lowering a load. Eur J Appl Physiol 120, 2417–2429 (2020). https://doi.org/10.1007/s00421-020-04464-9
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DOI: https://doi.org/10.1007/s00421-020-04464-9