Abstract
We revisit the concept of synergy based on the recently translated classical book by Nikolai Bernstein (On the construction of movements, Medgiz, Moscow 1947; Latash, Bernstein’s Construction of Movements, Routledge, Abingdon 2020b) and progress in understanding the physics and neurophysiology of biological action. Two aspects of synergies are described: organizing elements into stable groups (modes) and ensuring dynamical stability of salient performance variables. The ability of the central nervous system to attenuate synergies in preparation for a quick action—anticipatory synergy adjustments—is emphasized. Recent studies have demonstrated synergies at the level of hypothetical control variables associated with spatial referent coordinates for effectors. Overall, the concept of synergies fits naturally the hierarchical scheme of control with referent coordinates with an important role played by back-coupling loops within the central nervous system and from peripheral sensory endings. Further, we review studies showing non-trivial changes in synergies with development, aging, fatigue, practice, and a variety of neurological disorders. Two aspects of impaired synergic control—impaired stability and impaired agility—are introduced. The recent generalization of the concept of synergies for non-motor domains, including perception, is discussed. We end the review with a list of unresolved and troubling issues.
Similar content being viewed by others
Data availability
The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.
References
Aeles J, Kelly LA, Yoshitake Y, Cresswell AG (2020) Fine-wire recordings of flexor hallucis brevis motor units up to maximal voluntary contraction reveal a flexible, non-rigid mechanism for force control. J Neurophysiol 123:1766–1774
Ambike S, Zatsiorsky VM, Latash ML (2015) Processes underlying unintentional finger force changes in the absence of visual feedback. Exp Brain Res 233:711–721
Ambike S, Mattos D, Zatsiorsky VM, Latash ML (2016a) Synergies in the space of control variables within the equilibrium-point hypothesis. Neurosci 315:150–161
Ambike S, Mattos D, Zatsiorsky VM, Latash ML (2016b) Unsteady steady-states: central causes of unintentional force drift. Exp Brain Res 234:3597–3611
Ambike S, Pinedo T, Kulkarni A, Santinelli FP, Barbieri FA (2021) Step length synergy while crossing obstacles is weaker in patients with Parkinson’s disease. Gait Posture 84:340–345
Babinski F (1899) De L’asynergie Cerebelleuse. Rev Neurologique 7:806–816
Berger DJ, Masciullo M, Molinari M, Lacquaniti F, D’Avella A (2020) Does the cerebellum shape the spatiotemporal organization of muscle patterns? Insights from subjects with cerebellar ataxias. J Neurophysiol 123:1691–1710
Bernstein NA (1935) The problem of interrelation between coordination and localization. Archs Biol Sci 38:1–35 (in Russian)
Bernstein NA (1947) On the construction of movements. Medgiz: Moscow (in Russian). English translation in Latash 2020b
Bernstein NA (1967) The co-ordination and regulation of movements. Pergamon Press, Oxford
Bernstein NA (1996) On dexterity and its development. In: Latash ML, Turvey MT (eds) Dexterity and its development. Erlbaum Publ, Mahwah, NJ, pp 1–244
Bizzi E, Ajemian R (2020) From motor planning to execution: a sensorimotor loop perspective. J Neurophysiol 124:1815–1823
Bobath B (1978) Adult hemiplegia: evaluation and treatment. William Heinemann, London
Booth FW, Weeden SH, Tseng BS (1994) Effect of aging on human skeletal muscle and motor function. Med Sci Sport Exer 26:556–560
Botzheim L, Laczko J, Torricelli D, Mravcsik M, Pons JP, Oliveiro Barroso F (2021) Effects of gravity and kinematic constraints on muscle synergies in arm cycling. J Neurophysiol 125:1367–1381
Bowler RM, Nakagawa S, Drezgic M, Roels HA, Park RM, Diamond E, Mergler D, Bouchard M, Bowler RP, Koller W (2007) Sequelae of fume exposure in confined space welding: a neurological and neuropsychological case series. Neurotoxicol 28:298–311
Brooks SV, Faulkner JA (1994) Skeletal muscle weakness in old age: underlying mechanisms. Med Sci Sport Exer 26:432–439
Bruton M, O’Dwyer N (2018) Synergies in coordination: a comprehensive overview of neural, computational, and behavioral approaches. J Neurophysiol 120:2761–2774
Cheng EJ, Loeb GE (2008) On the use of musculoskeletal models to interpret motor control strategies from performance data. J Neural Eng 5:232–253
Cossu G, Pau M (2017) Subthalamic nucleus stimulation and gait in Parkinson’s disease: a not always fruitful relationship. Gait Posture 52:205–210
Côté JN, Mathieu PA, Levin MF, Feldman AG (2002) Movement reorganization to compensate for fatigue during sawing. Exp Brain Res 146:394–398
Côté JN, Feldman AG, Mathieu PA, Levin MF (2008) Effects of fatigue on intermuscular coordination during repetitive hammering. Mot Control 12:79–92
Cuadra C, Latash ML (2019) Exploring the concept of iso-perceptual manifold (IPM): a study of finger force matching. Neurosci 401:130–141
Cuadra C, Wojnicz W, Kozinc Z, Latash ML (2020) Perceptual and motor effects of muscle co-activation in a force production task. Neurosci 437:34–44. https://doi.org/10.1016/j.neuroscience.2020.04.023
Cuadra C, Corey J, Latash ML (2021a) Distortions of the efferent copy during force perception: a study of force drifts and effects of muscle vibration. Neurosci 457:139–154
Cuadra C, Gilmore R, Latash ML (2021b) Finger force matching and verbal reports: testing predictions of the Iso-Perceptual Manifold (IPM) concept. J Mot Behav 53:598–610
Cuadra C, Gilmore R, Latash ML (2021c) Finger force matching and verbal reports: testing predictions of the Iso-Perceptual Manifold (IPM) concept. J Motor Behav 53:598–610
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, Degani AM, Latash ML (2008) Flexible muscle modes and synergies in challenging whole-body tasks. Exp Brain Res 189:171–187
De Freitas PB, Freitas SMSF, Reschechtko S, Corson T, Lewis MM, Huang X, Latash ML (2020a) Synergic control of action in levodopa-naïve Parkinson’s disease patients: I. Multi-finger interaction and coordination. Exp Brain Res 238:229–245
DeWald JP, Pope PS, Given JD, Buchanan TS, Rymer WZ (1995) Abnormal muscle coactivation patterns during isometric torque generation at the elbow and shoulder in hemiparetic subjects. Brain 118:495–510
Dingwell JB, Cusumano JP, Cavanagh PR, Sternad D (2001) Local dynamic stability versus kinematic variability of continuous overground and treadmill walking. J Biomech Eng 123:27–32
Dinse HR (2006) Cortical reorganization in the aging brain. Prog Brain Res 157:57–80
Dominici N, Ivanenko YP, Cappellini G et al (2011) Locomotor primitives in newborn babies and their development. Science 334:997–999
Domkin D, Laczko J, Jaric S, Johansson H, Latash ML (2002) Structure of joint variability in bimanual pointing tasks. Exp Brain Res 143:11–23
Duysens J, De Groote F, Jonkers I (2013) The flexion synergy, mother of all synergies and father of new models of gait. Front Comput Neurosci 7:14
Eisen A, Entezari-Taher M, Stewart H (1996) Cortical projections to spinal motoneurons: changes with aging and amyotrophic lateral sclerosis. Neurology 46:1396–1404
Enoka RM, Duchateau J (2008) Muscle fatigue: what, why and how it influences muscle function. J Physiol 586:11–23
Erim Z, Beg FM, Burke DT, De Luca CJ (1999) Effects of aging on motor-unit control properties. J Neurophysiol 82:2081–2091
Falaki A, Huang X, Lewis MM, Latash ML (2016) Impaired synergic control of posture in Parkinson’s patients without postural instability. Gait Posture 44:209–215
Falaki A, Huang X, Lewis MM, Latash ML (2017a) Dopaminergic modulation of multi-muscle synergies in postural tasks performed by patients with Parkinson’s disease. J Electromyogr Kinesiol 33:20–26
Falaki A, Huang X, Lewis MM, Latash ML (2017b) Motor equivalence and structure of variance: Multi-muscle postural synergies in Parkinson’s disease. Exp Brain Res 235:2243–2258
Falaki A, Jo HJ, Lewis MM, O’Connell B, De Jesus S, McInerney J, Huang X, Latash ML (2018) Systemic effects of deep brain stimulation on synergic control in Parkinson’s disease. Clin Neurophysiol 129:1320–1332
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. Neurosci 5:81–90
Feldman AG (1986) Once more on the equilibrium-point hypothesis (λ–model) for motor control. J Mot Behav 18:17–54
Feldman AG (2009) New insights into action-perception coupling. Exp Brain Res 194:39–58
Feldman AG (2015) Referent control of action and perception: challenging conventional theories in behavioral science. Springer, New York
Feldman AG (2016) Active sensing without efference copy: referent control of perception. J Neurophysiol 116(3):960–976. https://doi.org/10.1152/jn.00016.2016
Feldman AG, Latash ML (1982) Afferent and efferent components of joint position sense: interpretation of kinaesthetic illusions. Biol Cybern 42:205–214
Feldman AG, Latash ML (2005) Testing hypotheses and the advancement of science: recent attempts to falsify the equilibrium-point hypothesis. Exp Brain Res 161:91–103
Freitas SMSF, de Freitas PB, Falaki A, Corson T, Lewis MM, Huang X, Latash ML (2020b) Synergic control of action in levodopa-naïve Parkinson’s disease patients. II. Multi-muscle synergies stabilizing vertical posture. Exp Brain Res 238:2931–2945
Gelfand IM, Latash ML (1998) On the problem of adequate language in movement science. Mot Control 2:306–313
Gera G, Freitas SM, Scholz JP (2016a) Relationship of diminished interjoint coordination after stroke to hand path consistency. Exp Brain Res 234:741–751
Gera G, McGlade KE, Reisman DS, Scholz JP (2016b) Trunk muscle coordination during upward and downward reaching in stroke survivors. Mot Control 20:50–69
Gersosimo MG, Koller WS (2006) The diagnosis of manganese-induced parkinsonism. Toxicology 27:340–346
Golenia L, Schoemaker MM, Otten E, Mouton LJ, Bongers RM (2018) Developing of reaching during mid-choldhood from a developmental systems perspective. PLoS ONE 13(2):e0193463
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
Grabiner MD, Enoka RM (1995) Changes in movement capabilities with aging. Exerc Sport Sci Rev 23:65–104
Gribble PL, Ostry DJ, Sanguineti V, Laboissiere R (1998) Are complex control signals required for human arm movements? J Neurophysiol 79:1409–1424
Hasanbarani F, Latash ML (2020) Performance-stabilizing synergies in a complex motor task: analysis based on the uncontrolled manifold hypothesis. Mot Control 24:238–252
Hausdorff JM, Purdon PL, Peng CK, Ladin Z, Wei JY, Goldberger AL (1985) Fractal dynamics of human gait: stability of long-range correlations in stride interval of human gail. J Appl Physiol 80:1448–1457
Hoehn M, Yahr M (1967) Parkinsonism: onset, progression and mortality. Neurology 17:427–442
Houk JC (2005) Agents of the mind. Biol Cybern 92:427–437
Houk JC, Buckingham JT, Barto AG (1996) Models of the cerebellum and motor learning. Behav Brain Sci 19:368–383
Hughlings Jackson J (1889) On the comparative study of disease of the nervous system. Brit Med J 17:355–362
Hultborn H, Brownstone RB, Toth TI, Gossard JP (2004) Key mechanisms for setting the input-output gain across the motoneuron pool. Prog Brain Res 143:77–95
Inglin B, Woollacott MH (1988) Anticipatory postural adjustments associated with reaction time arm movements: a comparison between young and old. J Gerontol 43:M105–M113
Ioffe ME, Chernikova LA, Ustinova KI (2007) Role of cerebellum in learning motor tasks. Cerebellum 6:87–94
Ivanenko YP, Poppele RE, Lacquaniti F (2006) Motor control programs and walking. Neuroscientist 12:339–348
Ivanenko YP, Dominici N, Cappellini G, Di Paolo A, Giannini C, Poppele RE, Lacquaniti F (2013) Changes in the spinal segmental motor output for stepping during development from infant to adult. J Neurosci 33:3025–3036
Jo HJ, Park J, Lewis MM, Huang X, Latash ML (2015) Prehension synergies and hand function in early-stage Parkinson’s disease. Exp Brain Res 233:425–440
Jo HJ, Maenza C, Good DC, Huang X, Park J, Sainburg RL, Latash ML (2016) Effects of unilateral stroke on multi-finger synergies and their feed-forward adjustments. Neuroscience 319:194–205
Jo HJ, Lucassen E, Huang X, Latash ML (2017) Changes in multi-digit synergies and their feed-forward adjustments in multiple sclerosis. J Motor Behav 49:218–228
Jordan K, Challis JH, Newell KM (2007) Speed influences on the scaling behavior of gait cycle fluctuations during treadmill running. Hum Move Sci 26:87–102
Jordan K, Challis JH, Cusumano JP, Newell KM (2009) Stability and time-dependent structure of gait variability in walking and running. Hum Move Sci 28:113–128
Kang N, Shinohara M, Zatsiorsky VM, Latash ML (2004) Learning multi-finger synergies: an uncontrolled manifold analysis. Exp Brain Res 157:336–350
Kang N, Roberts LM, Aziz C, Cauraugh JH (2019) Age-related deficits in bilateral motor synergies and force coordination. BMC Geriatr 19(1):287
Kawato M (1999) Internal models for motor control and trajectory planning. Curr Opin Neurobiol 9:718–727
Kinoshita H, Francis PR (1996) A comparison of prehension force control in young and elderly individuals. European J Appl Physiol 74:450–460
Klishko AN, Farrell BJ, Beloozerova IN, Latash ML, Prilutsky BI (2014) Stabilization of cat paw trajectory during locomotion. J Neurophysiol 112:1376–1391
Krishnamoorthy V, Goodman SR, Latash ML, Zatsiorsky VM (2003) Muscle synergies during shifts of the center of pressure by standing persons: identification of muscle modes. Biol Cybern 89:152–161
Lacquaniti F, Ivanenko YP, Zago M (2012a) Development of human locomotion. Curr Opin Neurobiol 22:822–828
Lacquaniti F, Ivanenko YP, Zago M (2012b) Patterned control of human locomotion. J Physiol 590:2189–2199
Latash ML (1992) Virtual trajectories, joint stiffness, and changes in natural frequency during single-joint oscillatory movements. Neurosci 49:209–220
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). Hum Move Sci 217:1–5
Latash ML (2018) Stability of kinesthetic perception in efferent-afferent spaces: the concept of iso-perceptual manifold. Neurosci 372:97–113
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 construction of movements. Routledge, Abingdon
Latash ML (2021) Laws of nature that define biological action and perception. Phys Life Rev 36:47–67
Latash ML, Gottlieb GL (1991) Reconstruction of elbow joint compliant characteristics during fast and slow voluntary movements. Neurosci 43:697–712
Latash ML, Huang X (2015) Neural control of movement stability: Lessons from studies of neurological patients. Neurosci 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, Aruin AS, Zatsiorsky VM (1999) The basis of a simple synergy: reconstruction of joint equilibrium trajectories during unrestrained arm movements. Hum Move Sci 18:3–30
Latash ML, Yarrow K, Rothwell JC (2003) Changes in finger coordination and responses to single pulse TMS of motor cortex during practice of a multi-finger force production task. Hum Move Sci 151:60–71
Latash ML, Shim JK, Smilga AV, Zatsiorsky V (2005) A central back-coupling hypothesis on the organization of motor synergies: a physical metaphor and a neural model. Biol Cybern 92:186–191
Latash ML, Scholz JP, Schöner G (2007) Toward a new theory of motor synergies. Mot Control 11:276–308
Lewis MM, Lee E-Y, Jo HJ, Park J, Latash ML, Huang X (2016) Synergy as a new and sensitive marker of basal ganglia dysfunction: a study of asymptomatic welders. Neurotoxicol 56:76–85
Loeb GE (1999) What might the brain know about muscles, limbs and spinal circuits? Prog Brain Res 123:405–409
Madarshahian S, Latash ML (2021) Synergies at the level of motor units in single-finger and multi-finger tasks. Exp Brain Res (in Press). https://doi.org/10.1007/s00221-021-06180-y
Madarshahian S, Letizi J, Latash ML (2021) Synergic control of a single muscle: the example of flexor digitorum superficialis. J Physiol 599:1261–1279
Mangalam M, Rein R, Fragaszy DM (2018) Bearded capuchin monkeys use joint synergies to stabilize the hammer trajectory while cracking nuts in bipedal stance. Proc Royal Soc Biol Sci 285:1889
Marconi R, Landi A, Valzania F (2008) Subthalamic nucleus stimulation in Parkinson’s disease. Neurol Sci 29(Suppl 5):S389-391
Martin V, Scholz JP, Schöner G (2009) Redundancy, self-motion, and motor control. Neural Comput 21:1371–1414
Martin JR, Budgeon MK, Zatsiorsky VM, Latash ML (2011) Stabilization of the total force in multi-finger pressing tasks studied with the ‘inverse piano’ technique. Hum Mov Sci 30:446–458
Martin V, Reimann H, Schöner G (2019) A process account of the uncontrolled manifold structure of joint space variance in pointing movements. Biol Cybern 113:293–307
Massion J (1992) Movement, posture and equilibrium—interaction and coordination. Prog Neurobiol 38:35–56
Mattos D, Latash ML, Park E, Kuhl J, Scholz JP (2011) Unpredictable elbow joint perturbation during reaching results in multijoint motor equivalence. J Neurophysiol 106:1424–1436
Mattos D, Kuhl J, Scholz JP, Latash ML (2013) Motor equivalence (ME) during reaching: is ME observable at the muscle level? Mot Control 17:145–175
Mattos D, Schöner G, Zatsiorsky VM, Latash ML (2015) Motor equivalence during accurate multi-finger force production. Hum Move Sci 233:487–502
Meyendorff J (1974) St. Gregory Palamas and orthodox spirituality. St. Vladimir’s Seminary Press, USA
Möhler F, Marahrens S, Ringhof S, Mikut R, Stein T (2020) Variability in running coordination in experts and novices: a 3D uncontrolled manifold analysis. Eur J Sport Sci 17:1–10
Morrison A, McGrath D, Wallace ES (2016) Motor abundance and control structure in the golf swing. Hum Mov Sci 46:129–147
Müller H, Sternad D (2003) A randomization method for the calculation of covariation in multiple nonlinear relations: illustrated with the example of goal-directed movements. Biol Cybern 89:22–33
Nichols TR (2018) Distributed force feedback in the spinal cord and the regulation of limb mechanics. J Neurophysiol 119:1186–1200
Olafsdottir H, Yoshida N, Zatsiorsky VM, Latash ML (2005) Anticipatory covariation of finger forces during self-paced and reaction time force production. Neurosci Lett 381:92–96
Olafsdottir H, Zhang W, Zatsiorsky VM, Latash ML (2007) Age related changes in multi-finger synergies in accurate moment of force production tasks. J Appl Physiol 102:1490–1501
Olafsdottir H, Kim SW, Zatsiorsky VM, Latash ML (2008) Anticipatory synergy adjustments in preparation to self-triggered perturbations in elderly individuals. J Appl Biomech 24:175–179
Ostry DJ, Feldman AG (2003) A critical evaluation of the force control hypothesis in motor control. Exp Brain Res 153:275–288
Park J, Wu Y-H, Lewis MM, Huang X, Latash ML (2012) Changes in multi-finger interaction and coordination in Parkinson’s disease. J Neurophysiol 108:915–924
Park J, Lewis MM, Huang X, Latash ML (2013) Effects of olivo-ponto-cerebellar atrophy (OPCA) on finger interaction and coordination. Clin Neurophysiol 124:991–998
Park J, Lewis MM, Huang X, Latash ML (2014) Dopaminergic modulation of motor coordination in Parkinson’s disease. Parkins Rel Disord 20:64–68
Parsa B, O’Shea DJ, Zatsiorsky VM, Latash ML (2016) On the nature of unintentional action: a study of force/moment drifts during multi-finger tasks. J Neurophysiol 116:698–708
Passos P, Lacasa E, Milho J, Torrents C (2020) Capturing interpersonal synergies in social setting: an example with a badminton cooperative task. Nonlinear Dyn Psychol Life Sci 24:59–78
Pham BN, Luo J, Anand H, Kola O, Salcedo P, Nguyen C, Gaunt S, Zhong H, Garfinkel A, Tillakaratne N, Edgerton VR (2020) Redundancy and multifunctionality among spinal locomotor networks. J Neurophysiol 124:1469–1479
Reisman D, Scholz JP (2003) Aspects of joint coordination are preserved during pointing in persons with post-stroke hemiparesis. Brain 126:2510–2527
Reschechtko S, Latash ML (2017) Stability of hand force production: I. Hand level control variables and multi-finger synergies. J Neurophysiol 118:3152–3164
Rocchi L, Carlson-Kuhta P, Chiari L, Burchiel KJ, Hogarth P, Horak FB (2012) Effects of deep brain stimulation in the subthalamic nucleus or globus pallidus internus on step initiation in Parkinson disease: laboratory investigation. J Neurosurg 117:1141–1149
Rodgers MA, Evans WJ (1993) Changes in skeletal muscle with aging: effects of exercise training. Exerc Sport Sci Rev 21:65–102
Rosenblatt NJ, Hurt CP, Latash ML, Grabiner MD (2014) An apparent contradiction: increasing variability to achieve greater precision? Exp Brain Res 232:403–413
Rosenblatt NJ, Eckardt N, Kuhman D, Hurt CP (2020) Older but not younger adults rely on multijoint coordination to stabilize the swinging limb when performing a novel cued walking task. Exp Brain Res 238:1441–1454
Scholz JP, Schöner G (1999) The uncontrolled manifold concept: identifying control variables for a functional task. Exp Brain Res 126:289–306
Scholz JP, Schöner G (2014) Use of the uncontrolled manifold (UCM) approach to understand motor variability, motor equivalence, and self-motion. Adv Exp Med Biol 826:91–100
Scholz JP, Schöner G, Hsu WL, Jeka JJ, Horak F, Martin V (2007) Motor equivalent control of the center of mass in response to support surface perturbations. Exp Brain Res 180:163–179
Schöner G (1995) Recent developments and problems in human movement science and their conceptual implications. Ecol Psychol 8:291–314
Serrien B, Tassignon B, Verschueren J, Meeusen R, Baeyens J-P (2020) Short-term effects on differential learning and contextual interference in a goalkeeper-like task: visuomotor response time and motor control. Eur J Sport Sci 20:1061–1071
Shadmehr R (2017) Distinct neural circuits for control of movement vs. holding still. J Neurophysiol 117:1431–1460
Shadmehr R, Wise SP (2005) The computational neurobiology of reaching and pointing. MIT Press, Cambridge
Shaklai S, Mimouni-Bloch A, Levin M, Friedman J (2017) Development of finger force coordination in children. Exp Brain Res 235:3709–3720
Shim JK, Olafsdottir H, Zatsiorsky VM, Latash ML (2005) The emergence and disappearance of multi-digit synergies during force production tasks. Exp Brain Res 164:260–270
Singh T, Varadhan SKM, Zatsiorsky VM, Latash ML (2010a) Fatigue and motor redundancy: adaptive increase in force variance in multi-finger tasks. J Neurophysiol 103:2990–3000
Singh T, Varadhan SKM, Zatsiorsky VM, Latash ML (2010b) Adaptive increase in force variance during fatigue in tasks with low redundancy. Neurosci Lett 485:204–207
Sperry RW (1950) Neural basis of the spontaneous optokinetic response produced by visual inversion. J Comp Physiol Psychol 43:482–489
Spirduso WW, Francis K, Eakin T, Stanford C (2005) Quantification of manual force control and tremor. J Mot Behav 37:197–210
St. Gregory Palamas (1983) The Triads. Classics of Western Spirituality. Paulist Press, Mahwah, NJ
St. Gregory Palamas (1988) The One Hundred and Fifty Chapters. Pontifical Institute of Mediaeval Studies, Toronto
Sylos-Labini F, Zago M, Guertin PA, Lacquaniti F, Ivanenko YP (2017) Muscle coordination and locomotion in humans. Curr Pharm Des 23:1821–1833
Sylos-Labini F, La Scaleia V, Cappellini G et al (2020) Distinct locomotor precursors in newborn babies. Proc Natl Acad Sci USA 117:9604–9612
Thach WT, Goodkin HG, Keating JG (1992) Cerebellum and the adaptive coordination of movement. Ann Rev Neurosci 15:403–442
Tillman M, Ambike S (2018) Cue-induced changes in the stability of finger force-production tasks revealed by the uncontrolled manifold analysis. J Neurophysiol 119:21–32
Tillman M, Ambike S (2020) The influence of recent actions and anticipated actions on the stability of finger forces during a tracking task. Mot Control 24:365–382
Ting LH, McKay JL (2007) Neuromechanics of muscle synergies for posture and movement. Curr Opin Neurobiol 17:622–628
Tomita Y, Turpin NA, Piscitelli D, Feldman AG, Levin MF (2020) Stability of reaching during standing in stroke. J Neurophysiol 123:1756–1765
Tresch MC, Jarc A (2009) The case for and against muscle synergies. Curr Opin Neurobiol 19:601–607
Turvey MT (1990) Coordination. Amer Psychol 45(8):938–953. https://doi.org/10.1037/0003-066X.45.8.938
Turvey MT (2007) Action and perception at the level of synergies. Hum Move Sci 26:657–697
Uchiyama T, Johansson H, Windhorst U (2003) Static and dynamic input-output relations of the feline medial gastrocnemius motoneuron-muscle system subjected to recurrent inhibition: a model study. Biol Cybern 89:264–273
Vaillancourt DE, Russell DM (2002) Temporal capacity of short-term visuomotor memory in continuous force production. Exp Brain Res 145:275–285
Van Heijst JJ, Vos JE, Bullock D (1998) Development in a biologically inspired spinal neural network for movement control. Neur Networks 11:1305–1316
Von Holst E, Mittelstaedt H (1950/1973) Daz reafferezprincip. Wechselwirkungen zwischen Zentralnerven-system und Peripherie, Naturwiss. 37: 467–476, 1950. The reafference principle. In: The Behavioral Physiology of Animals and Man. The Collected Papers of Erich von Holst. Martin R (trans) University of Miami Press, Coral Gables, Florida, 1 pp 139–173
Vandekerckhove I, De Beukelaer N, Van den Hauwe M et al (2020) Muscle weakness has a limited effect on motor control of gait in Duchenne muscular dystrophy. PLoS ONE 15(9):e0238445
Vereijken B, van Emmerick REA, Whiting HTA, Newell KM (1992) Free(z)ing degrees of freedom in skill acquisition. J Mot Behav 24:133–142
Verrel J, Lövden M, Lindenberger U (2012) Normal aging reduces motor synergies in manual pointing. Neurobiol Aging 33:200.e1–10
Wang Y, Watanabe K, Asaka T (2017) Aging effect on muscle synergies in stepping forth during a forward perturbation. Eur J Appl Physiol 117:201–211
Welsh JP, Llinas R (1997) Some organizing principles for the control of movement based on olivocerebellar physiology. Prog Brain Res 114:449–461
Wolpert DM, Miall RC, Kawato M (1998) Internal models in the cerebellum. Trends Cogn Sci 2:338–347
Wu Y-H, Pazin N, Zatsiorsky VM, Latash ML (2012) Practicing elements vs. practicing coordination: changes in the structure of variance. J Mot Behav 44:471–478
Wu Y-H, Pazin N, Zatsiorsky VM, Latash ML (2013) Improving finger coordination in young and elderly persons. Exp Brain Res 226:273–283
Zatsiorsky VM, Li ZM, Latash ML (1998) Coordinated force production in multi-finger tasks: finger interaction and neural network modeling. Biol Cybern 79:139–150
Zelik KE, La Scaleia V, Ivanenko YP, Lacquaniti F (2014) Can modular strategies simplify neural control of multidirectional human locomotion. J Neurophysiol 111:1686–1702
Acknowledgements
Studies reviewed in this paper have been supported by several NIH grants over the past 25 years: HD030128, NS035032, AG018751, AR048563, and NS095873. The author is grateful to all the students and visiting scholars who took part in the cited studies.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
There is no conflict of interest.
Additional information
Communicated by Winston D Byblow.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Latash, M.L. One more time about motor (and non-motor) synergies. Exp Brain Res 239, 2951–2967 (2021). https://doi.org/10.1007/s00221-021-06188-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00221-021-06188-4