We explored the organization of motor units recorded in the flexor digitorum superficialis into stable groups (MU-modes) and force-stabilizing synergies in spaces of MU-modes. Young, healthy participants performed one-finger and three-finger accurate cyclical force production tasks. Two wireless sensor arrays (Trigno Galileo, Delsys, Inc.) were placed over the proximal and distal portions of the muscle for surface recording and identification of motor unit action potentials. Principal component analysis with Varimax rotation and factor extraction was used to identify MU-modes. The framework of the uncontrolled manifold hypothesis was used to analyze inter-cycle variance in the space of MU-modes and compute the index of force-stabilizing synergy. Multiple linear regression between the first MU-mode in the three-finger task and the first MU-modes in the three single-finger tasks showed no differences between the data recorded by the two electrodes suggesting that MU-modes were unlikely to be synonymous with muscle compartments. Multi-MU-mode synergies stabilizing task force were documented across all tasks. In contrast, there were no force-stabilizing synergies in the three-finger task analyzed in the space of individual finger forces. Our results confirm the synergic organization of motor units in single-finger tasks and, for the first time, expand this result to multi-finger tasks. We offer an interpretation of the findings within the theoretical scheme of control with spatial referent coordinates expanded to the analysis of individual motor units. The results confirm trade-offs between synergies at different hierarchical levels and expand this notion to intra-muscle synergies.
This is a preview of subscription content, access via your institution.
Buy single article
Instant access to the full article PDF.
Price includes VAT (USA)
Tax calculation will be finalised during checkout.
Availability of data and materials
The original data are available from the corresponding author at a reasonable request.
The original codes in Matlab are available from the corresponding author at a reasonable request.
Ambike S, Mattos D, Zatsiorsky VM, Latash ML (2016) Synergies in the space of control variables within the equilibrium-point hypothesis. Neurosci 315:150–161
Arbib MA, Iberall T, Lyons D (1985) Coordinated control programs for movements of the hand. In: Goodwin AW, Darian-Smith I (eds) Hand function and the neocortex. Springer Verlag, Berlin, pp 111–129
Asaka T, Wang Y, Fukushima J, Latash ML (2008) Learning effects on muscle modes and multi-mode synergies. Exp Brain Res 184:323–338
Bernstein NA (1947) On the construction of movements. Medgiz, Moscow (in Russian)
Bruton M, O’Dwyer N (2018) Synergies in coordination: a comprehensive overview of neural, computational, and behavioral approaches. J Neurophysiol 120:2761–2774
Burgar CG, Valero-Cuevas FJ, Hentz VR (1997) Fine-wire electromyographic recording during force generation: application to index finger kinesiologic studies. Amer J Phys Med Rehab 76:494–501
Butler TJ, Kilbreath SL, Gorman RB, Gandevia SC (2005) Selective recruitment of single motor units in human flexor digitorum superficialis muscle during flexion of individual fingers. J Physiol 567:301–309
Christova P, Kossev A (2001) Human motor unit recruitment and derecruitment during long lasting intermittent contractions. J Electromyogr Kinesiol 11:189–196
Contessa P, DeLuca CJ (2013) Neural control of muscle force: indications from a simulation model. J Neurophysiol 109:1548–1570
Cuadra C, Bartsch A, Tiemann P, Reschechtko S, Latash ML (2018) Multi-finger synergies and the muscular apparatus of the hand. Exp Brain Res 236:1383–1393
Danion F, Li S, Zatsiorsky VM, Latash ML (2002) Relations between surface EMG of extrinsic flexors and individual finger forces support the notion of muscle compartments. Eur J Appl Physiol 88:185–188
Danion F, Schöner G, Latash ML, Li S, Scholz JP, Zatsiorsky VM (2003) A force mode hypothesis for finger interaction during multi-finger force production tasks. Biol Cybern 88:91–98
Danna-Dos-Santos A, Slomka K, Zatsiorsky VM, Latash ML (2007) Muscle modes and synergies during voluntary body sway. Exp Brain Res 179:533–550
Danna-Dos-Santos A, Degani AM, Latash ML (2008) Flexible muscle modes and synergies in challenging whole-body tasks. Exp Brain Res 189:171–187
d’Avella A, Saltiel P, Bizzi E (2003) Combinations of muscle synergies in the construction of a natural motor behavior. Nature Neurosci 6:300–308
De Luca CJ, Mambrito B (1987) Voluntary control of motor units in human antagonist muscles: coactivation and reciprocal activation. J Neurophysiol 58:525–542
De Freitas PB, Freitas SMSF, Lewis MM, Huang X, Latash ML (2018) Stability of steady hand force production explored across spaces and methods of analysis. Exp Brain Res 236:1545–1562
De Luca CJ, Chang SS, Roy SH, Kline JC, Nawab SH (2015) Decomposition of surface EMG signals from cyclic dynamic contractions. J Neurophysiol 113:1941–1951
Dominici N, Ivanenko YP, Cappellini G, d’Avella A, Mondì V, Cicchese M, Fabiano A, Silei T, Di Paolo A, Giannini C, Poppele RE, Lacquaniti F (2011) Locomotor primitives in newborn babies and their development. Science 334:997–999
Enoka RM, Robinson GA, Kossev AR (1989) Task and fatigue effects on low-threshold motor units in human hand muscle. J Neurophysiol 62:1344–1359
Feldman AG (1966) Functional tuning of the nervous system with control of movement or maintenance of a steady posture. II. Controllable parameters of the muscle. Biophysics 11:565–578
Feldman AG (1980) Superposition of motor programs. I. Rhythmic forearm movements in man. Neuroscience 5:81–90
Feldman AG (1986) Once more on the equilibrium-point hypothesis (λ–model) for motor control. J Motor Behav 18:17–54
Feldman AG (2015) Referent control of action and perception: Challenging conventional theories in behavioral science. Springer, NY
Fuglevand AJ, Dutoit AP, Johns RK, Keen DA (2006) Evaluation of plateau-potential-mediated “warm up” in human motor units. J Physiol 571:683–693
Gelfand IM, Tsetlin ML (1962) On certain methods of control of complex systems. Adv Math Sci 17:103 (in Russian)
Gelfand IM, Gurfinkel VS, Fomin SV, Tsetlin ML (eds) (1971) Models of the structural-functional organization of certain biological systems. MIT Press, Cambridge
Gorniak S, Zatsiorsky VM, Latash ML (2007) Hierarchies of synergies: an example of the two-hand, multi-finger tasks. Exp Brain Res 179:167–180
Gorniak S, Zatsiorsky VM, Latash ML (2009) Hierarchical control of static prehension: II. Multi-digit synergies. Exp Brain Res 194:1–15
Heckman CJ, Gorassini MA, Bennett DJ (2005) Persistent inward currents in motoneuron dendrites: implications for motor output. Muscle Nerve 31:135–156
Henneman E, Somjen G, Carpenter DO (1965) Excitability and inhibitibility of motoneurones of different sizes. J Neurophysiol 28:599–620
Ivanenko YP, Poppele RE, Lacquaniti F (2004) Five basic muscle activation patterns account for muscle activity during human locomotion. J Physiol 556:267–282
Ivanenko YP, Poppele RE, Lacquaniti F (2006) Motor control programs and walking. Neuroscientist 12:339–348
Jeneson JA, Taylor JS, Vigneron DB, Willard TS, Carvajal L, Nelson SJ, Murphy-Boesch J, Brown TR (1990) 1H MR imaging of anatomical compartments within the finger flexor muscles of the human forearm. Magn Reson Med 15:491–496
Kim SW, Shim JK, Zatsiorsky VM, Latash ML (2008) Finger interdependence: linking the kinetic and kinematic variables. Hum Move Sci 27:408–422
Krishnamoorthy V, Goodman SR, Latash ML, Zatsiorsky VM (2003a) Muscle synergies during shifts of the center of pressure by standing persons: identification of muscle modes. Biol Cybern 89:152–161
Krishnamoorthy V, Latash ML, Scholz JP, Zatsiorsky VM (2003b) Muscle synergies during shifts of the center of pressure by standing persons. Exp Brain Res 152:281–292
Krishnamoorthy V, Latash ML, Scholz JP, Zatsiorsky VM (2004) Muscle modes during shifts of the center of pressure by standing persons: effects of instability and additional support. Exp Brain Res 157:18–31
Krishnamoorthy V, Scholz JP, Latash ML (2007) The use of flexible arm muscle synergies to perform an isometric stabilization task. Clin Neurophysiol 118:525–537
Lang CE, Schieber MH (2003) Differential impairment of individuated finger movements in humans after damage to the motor cortex or the corticospinal tract. J Neurophysiol 90:1160–1170
Latash ML (2008) Synergy. Oxford University Press, New York
Latash ML (2010) Motor synergies and the equilibrium-point hypothesis. Mot Control 14:294–322
Latash ML (2012) The bliss (not the problem) of motor abundance (not redundancy). Exp Brain Res 217:1–5
Latash ML (2019) Physics of biological action and perception. Academic Press, New York
Latash ML (2020a) On primitives in motor control. Mot Control 24:318–346
Latash ML (ed) (2020b) Bernstein’s coordination of movements. Routledge, Abingdon
Latash ML (2021) Laws of nature that define biological action and perception. Phys Life Rev 36:47–67
Latash ML, Huang X (2015) Neural control of movement stability: lessons from studies of neurological patients. Neuroscience 301:39–48
Latash ML, Zatsiorsky VM (1993) Joint stiffness: myth or reality? Hum Move Sci 12:653–692
Latash ML, Zatsiorsky VM (2016) Biomechanics and motor control: defining central concepts. Academic Press, New York
Latash ML, Scholz JF, Danion F, Schöner G (2001) Structure of motor variability in marginally redundant multi-finger force production tasks. Exp Brain Res 141:153–165
Latash ML, Scholz JP, Schöner G (2007) Toward a new theory of motor synergies. Mot Control 11:276–308
Latash ML, Friedman J, Kim SW, Feldman AG, Zatsiorsky VM (2010) Prehension synergies and control with referent hand configurations. Exp Brain Res 202:213–229
Li ZM, Latash ML, Zatsiorsky VM (1998) Force sharing among fingers as a model of the redundancy problem. Exp Brain Res 119:276–286
Madarshahian S, Letizi J, Latash ML (2021) Synergic control of a single muscle: the example of flexor digitorum superficialis. J Physiol 599:1261–1279
Mariappan YK, Manduca A, Glaser KJ, Chen J, Amrami KK, Ehman RL (2010) Vibration imaging for localization of functional compartments of the extrinsic flexor muscles of the hand. J Magn Reson Imaging 31:1395–1401
Marzke MW (1992) Evolutionary development of the human thumb. Hand Clin 8:1–8
Mirakhorlo M, Van Beek N, Wesseling M, Maas H, Veeger HEJ, Jonkers I (2018) A musculoskeletal model of the hand and wrist: model definition and evaluation. Comput Methods Biomech Biomed Eng 21:548–557
Nawab SH, Chang SS, De Luca CJ (2010) High-yield decomposition of surface EMG signals. Clin Neurophysiol 121:1602–1615
Negro F, Holobar A, Farina D (2009) Fluctuations in isometric muscle force can be described by one linear projection of low-frequency components of motor unit discharges. J Physiol 587:5925–5938
Nichols TR (1994) A biomechanical perspective on spinal mechanisms of coordinated muscular action: an architecture principle. Acta Anat 151:1–13
Nichols TR (2018) Distributed force feedback in the spinal cord and the regulation of limb mechanics. J Neurophysiol 119:1186–1200
Olatsdottir H, Zatsiorsky VM, Latash ML (2005) Is the thumb a fifth finger? A study of digit interaction during force production tasks. Exp Brain Res 160:203–213
Pilon J-F, De Serres SJ, Feldman AG (2007) Threshold position control of arm movement with anticipatory increase in grip force. Exp Brain Res 181:49–67
Reschechtko S, Latash ML (2017) Stability of hand force production: I. Hand level control variables and multi-finger synergies. J Neurophysiol 118:3152–3164
Santello M, Bianchi M, Gabiccini M, Ricciardi E, Salvietti G, Prattichizzo D, Ernst M, Moscatelli A, Jorntell H, Kappers AM, Kyriakopoulos K, Schaeffer AA, Castellini C, Bicchi A (2016) Hand synergies: Integration of robotics and neuroscience for understanding the control of biological and artificial hands. Phys Life Rev 17:1–23
Schieber MH, Santello M (2004) Hand function: peripheral and central constraints on performance. J Appl Physiol 96:2293–2300
Scholz JP, Schöner G (1999) The uncontrolled manifold concept: identifying control variables for a functional task. Exp Brain Res 126:289–306
Scholz JP, Danion F, Latash ML, Schöner G (2002) Understanding finger coordination through analysis of the structure of force variability. Biol Cybern 86:29–39
Shinohara M, Latash ML, Zatsiorsky VM (2003) Age effects on force production by the intrinsic and extrinsic hand muscles and finger interaction during maximal contraction tasks. J App Physiol 95:1361–1369
Ting LH, Macpherson JM (2005) A limited set of muscle synergies for force control during a postural task. J Neurophysiol 93:609–613
Ting LH, McKay JL (2007) Neuromechanics of muscle synergies for posture and movement. Curr Opin Neurobiol 17:622–628
Tresch MC, Jarc A (2009) The case for and against muscle synergies. Curr Opin Neurobiol 19:601–607
Tresch MC, Cheung VC, d’Avella A (2006) Matrix factorization algorithms for the identification of muscle synergies: evaluation on simulated and experimental data sets. J Neurophysiol 95:2199–2212
Vandenberk MS, Kalmar JM (2014) An evaluation of paired motor unit estimates of persistent inward current in human motoneurons. J Neurophysiol 111:1877–1884
Zatsiorsky VM, Latash ML (2008) Multi-finger prehension: an overview. J Mot Behav 40:446–476
Zatsiorsky VM, Li ZM, Latash ML (2000) Enslaving effects in multi-finger force production. Exp Brain Res 131:187–195
We are very much grateful to Paola Contessa and Nicholas Ducey for the important discussions and insights.
The Galileo system used in the study was on loan from Delsys, Inc. Shirin Madarshahian was supported for two months in 2019 by a fellowship from Delsys, Inc.
Conflict of interest
No conflict of interest is claimed by any of the authors.
All the procedures were approved by the Office for Research Protection of the Pennsylvania State University (protocol #33393) in accordance with the ethical standards laid down in the 1964 Declaration of Helsinki.
Consent to participate
All of the subjects provided their informed consent based on the procedures approved by the Office for Research Protection of Pennsylvania State University.
Consent for publication
The authors and participants gave their consent to publish these data.
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Communicated by Francesco Lacquaniti.
About this article
Cite this article
Madarshahian, S., Latash, M.L. Synergies at the level of motor units in single-finger and multi-finger tasks. Exp Brain Res 239, 2905–2923 (2021). https://doi.org/10.1007/s00221-021-06180-y
- Uncontrolled manifold
- Referent coordinate