Skip to content
Licensed Unlicensed Requires Authentication Published by De Gruyter February 5, 2018

Neuromuscular synergies in motor control in normal and poststroke individuals

Sharon Israely, Gerry Leisman and Eli Carmeli

Abstract

Muscle synergies are proposed to function as motor primitives that are modulated by frontal brain areas to construct a large repertoire of movement. This paper reviews the history of the development of our current theoretical understanding of nervous system-based motor control mechanisms and more specifically the concept of muscle synergies. Computational models of muscle synergies, especially the nonnegative matrix factorization algorithm, are discussed with specific reference to the changes in synergy control post-central nervous system (CNS) lesions. An alternative approach for motor control is suggested, exploiting a combination of synergies control or flexible muscle control used for gross motor skills and for individualized finger movements. Rehabilitation approaches, either supporting or inhibiting the use of basic movement patterns, are discussed in the context of muscle synergies. Applications are discussed for the use of advanced technologies that can promote the recovery and functioning of the human CNS after stroke.

References

Adler, S., Beckers, D., and Buck, M. (2007). PNF in Practice: An Illustrated Guide (Springer-Verlag, Berlin Heidenlberg).Search in Google Scholar

Alkadhi, H., Brugger, P., Boendermaker, S.H., Crelier, G., Curt, A., Hepp-Reymond, M., and Kollias, S.S. (2004). What disconnection tells about motor imagery: evidence from paraplegic patients. Cereb. Cortex 15, 131–140.10.1093/cercor/bhh116Search in Google Scholar PubMed

Bagnall, M.W. and McLean, D.L. (2014). Modular organization of axial microcircuits in zebrafish. Science 343, 197–200.10.1126/science.1245629Search in Google Scholar PubMed PubMed Central

Baker, S.N. and Perez, M.A. (2017). Reticulospinal contributions to gross hand function after human spinal cord injury. J. Neurosci. 37, 9778–9784.10.1523/JNEUROSCI.3368-16.2017Search in Google Scholar PubMed PubMed Central

Battig, W., Nagel, E., Voss, J.F., and Brogden, W. (1957). Transfer and retention of bidimensional compensatory tracking after extended practice. Am. J. Psychol. 70, 75–80.10.2307/1419232Search in Google Scholar PubMed

Berger, D.J. and d’Avella, A. (2014). Effective force control by muscle synergies. Front. Comput. Neurosci. 8, 46.10.3389/fncom.2014.00046Search in Google Scholar PubMed PubMed Central

Berger, D.J., Gentner, R., Edmunds, T., Pai, D.K., and d’Avella, A. (2013). Differences in adaptation rates after virtual surgeries provide direct evidence for modularity. J. Neurosci. 33, 12384–12394.10.1523/JNEUROSCI.0122-13.2013Search in Google Scholar PubMed PubMed Central

Bernstein, N. (1967). The Coordination and Regulation of Movements (Oxford: Pergamon Press).Search in Google Scholar

Bizzi, E. and Ajemian, R. (2015). A hard scientific quest: understanding voluntary movements. Daedalus 144, 83–95.10.1162/DAED_a_00324Search in Google Scholar

Bizzi, E. and Cheung, V.C. (2013). The neural origin of muscle synergies. Front. Comput. Neurosci. 7, 51.10.3389/fncom.2013.00051Search in Google Scholar PubMed PubMed Central

Bizzi, E., Mussa-Ivaldi, F.A., and Giszter, S. (1991). Computations underlying the execution of movement: a biological perspective. Science 253, 287–291.10.1126/science.1857964Search in Google Scholar PubMed

Bizzi, E., Cheung, V., d’Avella, A., Saltiel, P., and Tresch, M. (2008). Combining modules for movement. Brain Res. Rev. 57, 125–133.10.1016/j.brainresrev.2007.08.004Search in Google Scholar PubMed PubMed Central

Bobath, B. (1990). Adult Hemiplegia: Evaluation and Treatment (William Heinemann Medical Books Limited, London).Search in Google Scholar

Bortoff, G.A. and Strick, P.L. (1993). Corticospinal terminations in two new-world primates: further evidence that corticomotoneuronal connections provide part of the neural substrate for manual dexterity. J. Neurosci. 13, 5105–5118.10.1523/JNEUROSCI.13-12-05105.1993Search in Google Scholar PubMed

Brown, T.G. (1911). The intrinsic factors in the act of progression in the mammal. Proc. R. Soc. Lond. B Biol. Sci. 84, 308–319.10.1098/rspb.1911.0077Search in Google Scholar

Brown, T.G. (1914). On the nature of the fundamental activity of the nervous centres; together with an analysis of the conditioning of rhythmic activity in progression, and a theory of the evolution of function in the nervous system. J. Physiol. (Lond.) 48, 18–46.10.1113/jphysiol.1914.sp001646Search in Google Scholar PubMed PubMed Central

Brunnström, S. (1970). Movement therapy in hemiplegia: a neurophysiological approach, facts and comparisons.Search in Google Scholar

Caggiano, V., Cheung, V.C., and Bizzi, E. (2016). An optogenetic demonstration of motor modularity in the mammalian spinal cord. Sci. Rep. 6, 35185.10.1038/srep35185Search in Google Scholar PubMed PubMed Central

Cappellini, G., Ivanenko, Y.P., Poppele, R.E., and Lacquaniti, F. (2006). Motor patterns in human walking and running. J. Neurophysiol. 95, 3426–3437.10.1152/jn.00081.2006Search in Google Scholar PubMed

Carmichael, S.T. (2006). Cellular and molecular mechanisms of neural repair after stroke: making waves. Ann. Neurol. 59, 735–742.10.1002/ana.20845Search in Google Scholar PubMed

Cheung, V.C., d’Avella, A., Tresch, M.C., and Bizzi, E. (2005). Central and sensory contributions to the activation and organization of muscle synergies during natural motor behaviors. J. Neurosci. 25, 6419–6434.10.1523/JNEUROSCI.4904-04.2005Search in Google Scholar PubMed PubMed Central

Cheung, V.C., d’Avella, A., and Bizzi, E. (2009a). Adjustments of motor pattern for load compensation via modulated activations of muscle synergies during natural behaviors. J. Neurophysiol. 101, 1235–1257.10.1152/jn.01387.2007Search in Google Scholar PubMed PubMed Central

Cheung, V.C., Piron, L., Agostini, M., Silvoni, S., Turolla, A., and Bizzi, E. (2009b). Stability of muscle synergies for voluntary actions after cortical stroke in humans. Proc. Natl. Acad. Sci. USA. 106, 19563–19568.10.1073/pnas.0910114106Search in Google Scholar PubMed PubMed Central

Cheung, V.C., Turolla, A., Agostini, M., Silvoni, S., Bennis, C., Kasi, P., Paganoni, S., Bonato, P., and Bizzi, E. (2012). Muscle synergy patterns as physiological markers of motor cortical damage. Proc. Natl. Acad. Sci. USA. 109, 14652–14656.10.1073/pnas.1212056109Search in Google Scholar PubMed PubMed Central

Cheung, V.C., DeBoer, C., Hanson, E., Tunesi, M., D’Onofrio, M., Arisi, I., Brandi, R., Cattaneo, A., and Goosens, K.A. (2013). Gene expression changes in the motor cortex mediating motor skill learning. PLoS One 8, e61496.10.1371/journal.pone.0061496Search in Google Scholar PubMed

Chvatal, S.A., Torres-Oviedo, G., Safavynia, S.A., and Ting, L.H. (2011). Common muscle synergies for control of center of mass and force in nonstepping and stepping postural behaviors. J. Neurophysiol. 106, 999–1015.10.1152/jn.00549.2010Search in Google Scholar PubMed

Clark, D.J., Ting, L.H., Zajac, F.E., Neptune, R.R., and Kautz, S.A. (2010). Merging of healthy motor modules predicts reduced locomotor performance and muscle coordination complexity post-stroke. J. Neurophysiol. 103, 844–857.10.1152/jn.00825.2009Search in Google Scholar PubMed

Corbetta, D., Sirtori, V., Castellini, G., Moja, L., and Gatti, R. (2015). Constraint-induced movement therapy for upper extremities in people with stroke. Cochrane Database Syst. Rev. Art. No.: CD004433. DOI: 10.1002/14651858.CD004433.pub3.10.1002/14651858.CD004433.pub3Search in Google Scholar

Danion, F., Varraine, E., Bonnard, M., and Pailhous, J. (2003). Stride variability in human gait: the effect of stride frequency and stride length. Gait Posture 18, 69–77.10.1016/S0966-6362(03)00030-4Search in Google Scholar PubMed

d’Avella, A. and Lacquaniti, F. (2013). Control of reaching movements by muscle synergy combinations. Front. Comput. Neurosci. 7, 42.10.3389/fncom.2013.00042Search in Google Scholar PubMed PubMed Central

d’Avella, A., Saltiel, P., and Bizzi, E. (2003). Combinations of muscle synergies in the construction of a natural motor behavior. Nat. Neurosci. 6, 300–308.10.1038/nn1010Search in Google Scholar PubMed

d’Avella, A., Portone, A., Fernandez, L., and Lacquaniti, F. (2006). Control of fast-reaching movements by muscle synergy combinations. J. Neurosci. 26, 7791–7810.10.1523/JNEUROSCI.0830-06.2006Search in Google Scholar PubMed PubMed Central

d’Avella, A., Fernandez, L., Portone, A., and Lacquaniti, F. (2008). Modulation of phasic and tonic muscle synergies with reaching direction and speed. J. Neurophysiol. 100, 1433–1454.10.1152/jn.01377.2007Search in Google Scholar PubMed

Davidson, A.G. and Buford, J.A. (2006). Bilateral actions of the reticulospinal tract on arm and shoulder muscles in the monkey: stimulus triggered averaging. Exp. Brain Res. 173, 25–39.10.1007/s00221-006-0374-1Search in Google Scholar PubMed

Davies, P.M. (2000). Steps to Follow: The Comprehensive Treatment of Patients With Hemiplegia (Springer-Verlag, Berlin Heidenlberg New York Tokyo).10.1007/978-3-642-57022-3Search in Google Scholar

Delis, I., Berret, B., Pozzo, T., and Panzeri, S. (2013). Quantitative evaluation of muscle synergy models: a single-trial task decoding approach. Front. Comput. Neurosci. 7, 8.10.3389/fncom.2013.00008Search in Google Scholar PubMed

Delis, I., Panzeri, S., Pozzo, T., and Berret, B. (2014). A unifying model of concurrent spatial and temporal modularity in muscle activity. J. Neurophysiol. 111, 675–693.10.1152/jn.00245.2013Search in Google Scholar PubMed

Della-Maggiore, V., Landi, S.M., and Villalta, J.I. (2014). Sensorimotor adaptation: multiple forms of plasticity in motor circuits. Neuroscientist 21, 109–125.10.1177/1073858414545228Search in Google Scholar PubMed

Detrembleur, C., Dierick, F., Stoquart, G., Chantraine, F., and Lejeune, T. (2003). Energy cost, mechanical work, and efficiency of hemiparetic walking. Gait Posture 18, 47–55.10.1016/S0966-6362(02)00193-5Search in Google Scholar PubMed

Dickstein, R., Hocherman, S., Pillar, T., and Shaham, R. (1986). Stroke rehabilitation: three exercise therapy approaches. Phys. Ther. 66, 1233–1238.10.1093/ptj/66.8.1233Search in Google Scholar PubMed

Dionísio, A., Duarte, I.C., Patrício, M., and Castelo-Branco, M. (2017). The use of repetitive transcranial magnetic stimulation for stroke rehabilitation: a systematic review. J. Stroke Cerebrovasc. Dis. 27, 1–31.10.1016/j.jstrokecerebrovasdis.2017.09.008Search in Google Scholar PubMed

Dominici, N., Ivanenko, Y.P., Cappellini, G., d’Avella, A., Mondi, V., Cicchese, M., Fabiano, A., Silei, T., Di Paolo A., Giannini C., et al. (2011). Locomotor primitives in newborn babies and their development. Science 334, 997–999.10.1126/science.1210617Search in Google Scholar PubMed

Drew, T., Kalaska, J., and Krouchev, N. (2008). Muscle synergies during locomotion in the cat: a model for motor cortex control. J. Physiol. (Lond.) 586, 1239–1245.10.1113/jphysiol.2007.146605Search in Google Scholar PubMed PubMed Central

Faber, D.S., Fetcho, J.R., and Korn, H. (1989). Neuronal networks underlying the escape response in goldfish. Ann. N.Y. Acad. Sci. 563, 11–33.10.1111/j.1749-6632.1989.tb42187.xSearch in Google Scholar PubMed

Forssberg, H. (1985). Ontogeny of human locomotor control I. Infant stepping, supported locomotion and transition to independent locomotion. Exp. Brain Res. 57, 480–493.10.1007/BF00237835Search in Google Scholar PubMed

Fourkas, A.D., Ionta, S., and Aglioti, S.M. (2006). Influence of imagined posture and imagery modality on corticospinal excitability. Behav. Brain Res. 168, 190–196.10.1016/j.bbr.2005.10.015Search in Google Scholar PubMed

García-Cossio, E., Broetz, D., Birbaumer, N., and Ramos-Murguialday, A. (2014). Cortex integrity relevance in muscle synergies in severe chronic stroke. Front. Hum. Neurosci. 8, 744.10.3389/fnhum.2014.00744Search in Google Scholar PubMed PubMed Central

Gentner, R., Gorges, S., Weise, D., aufm Kampe, K., Buttmann, M., and Classen, J. (2010). Encoding of motor skill in the corticomuscular system of musicians. Curr. Biol. 20, 1869–1874.10.1016/j.cub.2010.09.045Search in Google Scholar PubMed

Gentner, R., Edmunds, T., Pai, D.K., and d’Avella, A. (2013). Robustness of muscle synergies during visuomotor adaptation. Front. Comput. Neurosci. 7, 120.10.3389/fncom.2013.00120Search in Google Scholar PubMed PubMed Central

Giszter, S.F. (2015). Motor primitives – new data and future questions. Curr. Opin. Neurobiol. 33, 156–165.10.1016/j.conb.2015.04.004Search in Google Scholar PubMed PubMed Central

Gizzi, L., Nielsen, J.F., Felici, F., Ivanenko, Y.P., and Farina, D. (2011). Impulses of activation but not motor modules are preserved in the locomotion of subacute stroke patients. J. Neurophysiol. 106, 202–210.10.1152/jn.00727.2010Search in Google Scholar PubMed

Graham, J.V., Eustace, C., Brock, K., Swain, E., and Irwin-Carruthers, S. (2009). The Bobath concept in contemporary clinical practice. Top. Stroke Rehabil. 16, 57–68.10.1310/tsr1601-57Search in Google Scholar PubMed

Grillner, S. and Wallen, P. (1985). Central pattern generators for locomotion, with special reference to vertebrates. Annu. Rev. Neurosci. 8, 233–261.10.1146/annurev.ne.08.030185.001313Search in Google Scholar PubMed

Hall, K.G. and Magill, R.A. (1995). Variability of practice and contextual interference in motor skill learning. J. Mot. Behav. 27, 299–309.10.1080/00222895.1995.9941719Search in Google Scholar PubMed

Hart, C.B. and Giszter, S.F. (2004). Modular premotor drives and unit bursts as primitives for frog motor behaviors. J. Neurosci. 24, 5269–5282.10.1523/JNEUROSCI.5626-03.2004Search in Google Scholar PubMed

Hashiguchi, Y., Ohata, K., Kitatani, R., Yamakami, N., Sakuma, K., Osako, S., Yamada, S., Aga, Y., Watanabe, A., and Yamada, S. (2016). Merging and fractionation of muscle synergy indicate the recovery process in patients with hemiplegia: the first study of patients after subacute stroke. Neural Plast. 2016, Article ID 5282957, 7 pages. http://dx.doi.org/10.1155/2016/5282957.10.1155/2016/5282957Search in Google Scholar

Heffner, R.S. and Masterton, R.B. (1983). The role of the corticospinal tract in the evolution of human digital dexterity. Brain Behav. Evol. 23, 165–183.10.1159/000121494Search in Google Scholar PubMed

Hobo, K., Kawase, J., Tamura, F., Groher, M., Kikutani, T., and Sunakawa, H. (2014). Effects of the reappearance of primitive reflexes on eating function and prognosis. Geriatr. Gerontol. Int. 14, 190–197.10.1111/ggi.12078Search in Google Scholar PubMed

Hsu, A., Tang, P., and Jan, M. (2003). Analysis of impairments influencing gait velocity and asymmetry of hemiplegic patients after mild to moderate stroke. Arch. Phys. Med. Rehabil. 84, 1185–1193.10.1016/S0003-9993(03)00030-3Search in Google Scholar PubMed

Israely, S. and Carmeli, E. (2016). Handwriting performance versus arm forward reach and grasp abilities among post-stroke patients, a case-control study. Top. Stroke Rehabil. 24, 5–11.10.1080/10749357.2016.1183383Search in Google Scholar PubMed

Israely, S., Leisman, G., Machluf, C., Shnitzer, T., and Carmeli, E. (2017). Direction modulation of muscle synergies in a hand-reaching task. IEEE Trans. Neural Syst. Rehabil. Eng. 25, 2427–2440.10.1109/TNSRE.2017.2769659Search in Google Scholar PubMed

Ivanenko, Y.P., Grasso, R., Zago, M., Molinari, M., Scivoletto, G., Castellano, V., Macellari, V., and Lacquaniti, F. (2003). Temporal components of the motor patterns expressed by the human spinal cord reflect foot kinematics. J. Neurophysiol. 90, 3555–3565.10.1152/jn.00223.2003Search in Google Scholar PubMed

Ivanenko, Y.P., Poppele, R.E., and Lacquaniti, F. (2004). Five basic muscle activation patterns account for muscle activity during human locomotion. J. Physiol. (Lond.) 556, 267–282.10.1113/jphysiol.2003.057174Search in Google Scholar PubMed PubMed Central

Jongbloed-Pereboom, M., Janssen, A.J., Steenbergen, B., and Nijhuis-van der Sanden, M.W.G. (2012). Motor learning and working memory in children born preterm: a systematic review. Neurosci. Biobehav. Rev. 36, 1314–1330.10.1016/j.neubiorev.2012.02.005Search in Google Scholar PubMed

Jonkers, I., Delp, S., and Patten, C. (2009). Capacity to increase walking speed is limited by impaired hip and ankle power generation in lower functioning persons post-stroke. Gait Posture 29, 129–137.10.1016/j.gaitpost.2008.07.010Search in Google Scholar PubMed

Kimberley, T.J., Khandekar, G., Skraba, L.L., Spencer, J.A., Van Gorp, E.A., and Walker, S.R. (2006). Neural substrates for motor imagery in severe hemiparesis. Neurorehabil. Neural Repair 20, 268–277.10.1177/1545968306286958Search in Google Scholar PubMed

Kitago, T., Liang, J., Huang, V.S., Hayes, S., Simon, P., Tenteromano, L., Lazar, R.M., Marshall, R.S., Mazzoni, P., Lennihan, L., et al. (2013). Improvement after constraint-induced movement therapy: recovery of normal motor control or task-specific compensation? Neurorehabil. Neural Repair 27, 99–109.10.1177/1545968312452631Search in Google Scholar

Krouchev, N., Kalaska, J.F., and Drew, T. (2006). Sequential activation of muscle synergies during locomotion in the intact cat as revealed by cluster analysis and direct decomposition. J. Neurophysiol. 96, 1991–2010.10.1152/jn.00241.2006Search in Google Scholar PubMed

Kutch, J.J., Kuo, A.D., Bloch, A.M., and Rymer, W.Z. (2008). Endpoint force fluctuations reveal flexible rather than synergistic patterns of muscle cooperation. J. Neurophysiol. 100, 2455–2471.10.1152/jn.90274.2008Search in Google Scholar PubMed

Lamontagne, A., Richards, C.L., and Malouin, F. (2000). Coactivation during gait as an adaptive behavior after stroke. J. Electromyogr. Kinesiol. 10, 407–415.10.1016/S1050-6411(00)00028-6Search in Google Scholar PubMed

Lamontagne, A., Malouin, F., Richards, C., and Dumas, F. (2002). Mechanisms of disturbed motor control in ankle weakness during gait after stroke. Gait Posture 15, 244–255.10.1016/S0966-6362(01)00190-4Search in Google Scholar PubMed

Lang, C.E., Wagner, J.M., Bastian, A.J., Hu, Q., Edwards, D.F., Sahrmann, S.A., and Dromerick, A.W. (2005). Deficits in grasp versus reach during acute hemiparesis. Exp. Brain Res. 166, 126–136.10.1007/s00221-005-2350-6Search in Google Scholar PubMed

Langhorne, P., Coupar, F., and Pollock, A. (2009). Motor recovery after stroke: a systematic review. Lancet Neurol. 8, 741–754.10.1016/S1474-4422(09)70150-4Search in Google Scholar PubMed

Lee, W.A. (1984). Neuromotor synergies as a basis for coordinated intentional action. J. Mot. Behav. 16, 135–170.10.1080/00222895.1984.10735316Search in Google Scholar PubMed

Lee, D.D. and Seung, H.S. (1999). Learning the parts of objects by non-negative matrix factorization. Nature 401, 788–791.10.1038/44565Search in Google Scholar PubMed

Lee, D.D. and Seung, H.S. (2001). Algorithms for non-negative matrix factorization. Adv. Neural Inf. Process Syst. 556–562.Search in Google Scholar

Leisman, G. and Melillo, R. (2012). The development of the frontal lobes in infancy and childhood: symmetry and the nature of temperament and affect. Andrea E. Cavanna, ed. (Frontal Lobe/Anatomy, Functionas and Injury. Hauppauge, NY, Nova Scientifc Publishers), pp. 23–56.Search in Google Scholar

Leo, A., Handjaras, G., Bianchi, M., Marino, H., Gabiccini, M., Guidi, A., Scilingo, E.P., Pietrini, P., Bicchi, A., Santello, M., et al. (2016). A synergy-based hand control is encoded in human motor cortical areas. eLife 5, e13420.10.7554/eLife.13420Search in Google Scholar PubMed

Levin, M.F. (2016). Principles of motor recovery after neurological injury based on a motor control theory. Progress in Motor Control (Springer, Cham), pp. 121–140.10.1007/978-3-319-47313-0_7Search in Google Scholar

Levine, A.J., Hinckley, C.A., Hilde, K.L., Driscoll, S.P., Poon, T.H., Montgomery, J.M., and Pfaff, S.L. (2014). Identification of a cellular node for motor control pathways. Nat. Neurosci. 17, 586–593.10.1038/nn.3675Search in Google Scholar PubMed

Liu, K.P., Chan, C.C., Wong, R.S., Kwan, I.W., Yau, C.S., Li, L.S., and Lee, T.M. (2009). A randomized controlled trial of mental imagery augment generalization of learning in acute poststroke patients. Stroke 40, 2222–2225.10.1161/STROKEAHA.108.540997Search in Google Scholar PubMed

McMorland, A.J., Runnalls, K.D., and Byblow, W.D. (2015). A neuroanatomical framework for upper limb synergies after stroke. Front. Hum. Neurosci. 9, 82.10.3389/fnhum.2015.00082Search in Google Scholar PubMed

Melillo, R. and Leisman, G. (2010). Neurobehavioral Disorders of Childhood: An evolutionary Perspective (Springer Science and Business Media, New York).10.1007/978-1-4419-1231-2Search in Google Scholar

Mogenson, G.J., Jones, D.L., and Yim, C.Y. (1980). From motivation to action: functional interface between the limbic system and the motor system. Prog. Neurobiol. 14, 69–97.10.1016/0301-0082(80)90018-0Search in Google Scholar PubMed

Muceli, S., Boye, A.T., d’Avella, A., and Farina, D. (2010). Identifying representative synergy matrices for describing muscular activation patterns during multidirectional reaching in the horizontal plane. J. Neurophysiol. 103, 1532–1542.10.1152/jn.00559.2009Search in Google Scholar PubMed

Mukherjee, A. and Chakravarty, A. (2010). Spasticity mechanisms – for the clinician. Front. Neurol. 1, 149.10.3389/fneur.2010.00149Search in Google Scholar PubMed PubMed Central

Mulroy, S., Gronley, J., Weiss, W., Newsam, C., and Perry, J. (2003). Use of cluster analysis for gait pattern classification of patients in the early and late recovery phases following stroke. Gait Posture 18, 114–125.10.1016/S0966-6362(02)00165-0Search in Google Scholar PubMed

Munzert, J., Lorey, B., and Zentgraf, K. (2009). Cognitive motor processes: the role of motor imagery in the study of motor representations. Brain Res. Rev. 60, 306–326.10.1016/j.brainresrev.2008.12.024Search in Google Scholar PubMed

Neptune, R.R., Clark, D.J., and Kautz, S.A. (2009). Modular control of human walking: a simulation study. J. Biomech. 42, 1282–1287.10.1016/j.jbiomech.2009.03.009Search in Google Scholar PubMed PubMed Central

Overduin, S.A., d’Avella, A., Carmena, J.M., and Bizzi, E. (2012). Microstimulation activates a handful of muscle synergies. Neuron 76, 1071–1077.10.1016/j.neuron.2012.10.018Search in Google Scholar PubMed PubMed Central

Overduin, S.A., d’Avella, A., Roh, J., Carmena, J.M., and Bizzi, E. (2015). Representation of muscle synergies in the primate brain. J. Neurosci. 35, 12615–12624.10.1523/JNEUROSCI.4302-14.2015Search in Google Scholar PubMed PubMed Central

Page, S.J., Szaflarski, J.P., Eliassen, J.C., Pan, H., and Cramer, S.C. (2009a). Cortical plasticity following motor skill learning during mental practice in stroke. Neurorehabil. Neural Repair 23, 382–388.10.1177/1545968308326427Search in Google Scholar PubMed PubMed Central

Page, S.J., Levine, P., and Khoury, J.C. (2009b). Modified constraint-induced therapy combined with mental practice: thinking through better motor outcomes. Stroke 40, 551–554.10.1161/STROKEAHA.108.528760Search in Google Scholar PubMed

Perry, J., Garrett, M., Gronley, J.K., and Mulroy, S.J. (1995). Classification of walking handicap in the stroke population. Stroke 26, 982–989.10.1161/01.STR.26.6.982Search in Google Scholar PubMed

Pollock, A., Farmer, S.E., Brady, M.C., Langhorne, P., Mead, G.E., Mehrholz, J., and van Wijck, F. (2013). Interventions for improving upper limb function after stroke (Protocol). Cochrane Database Syst. Rev. Art. No.: CD010820. DOI: 10.1002/14651858.CD010820.10.1002/14651858.CD010820Search in Google Scholar

Quattrocchi, G., Greenwood, R., Rothwell, J.C., Galea, J.M., and Bestmann, S. (2017). Reward and punishment enhance motor adaptation in stroke. J. Neurol. Neurosurg. Psychiatry 88, 730–736.10.1136/jnnp-2016-314728Search in Google Scholar PubMed

Redlich, R., Opel, N., Bürger, C., Dohm, K., Grotegerd, D., Förster, K., Zaremba, D., Meinert, S., Repple, J., Enneking, V., et al. (2017). The limbic system in youth depression: brain structural and functional alterations in adolescent in-patients with severe depression. Neuropsychopharmacology. 43, 546–554.10.1038/npp.2017.246Search in Google Scholar PubMed PubMed Central

Riddle, C.N. and Baker, S.N. (2010). Convergence of pyramidal and medial brain stem descending pathways onto macaque cervical spinal interneurons. J. Neurophysiol. 103, 2821–2832.10.1152/jn.00491.2009Search in Google Scholar PubMed PubMed Central

Riddle, C.N., Edgley, S.A., and Baker, S.N. (2009). Direct and indirect connections with upper limb motoneurons from the primate reticulospinal tract. J. Neurosci. 29, 4993–4999.10.1523/JNEUROSCI.3720-08.2009Search in Google Scholar PubMed PubMed Central

Roh, J., Rymer, W.Z., and Beer, R.F. (2012). Robustness of muscle synergies underlying three-dimensional force generation at the hand in healthy humans. J. Neurophysiol. 107, 2123–2142.10.1152/jn.00173.2011Search in Google Scholar PubMed PubMed Central

Roh, J., Rymer, W., Perreault, E., Yoo, S., and Beer, R. (2013). Alterations in upper limb muscle synergy structure in chronic stroke survivors. J. Neurophysiol. 109, 768–781.10.1152/jn.00670.2012Search in Google Scholar PubMed PubMed Central

Roh, J., Rymer, W., and Beer, R. (2015). Evidence for altered upper extremity muscle synergies in chronic stroke survivors with mild and moderate impairment. Front. Hum. Neurosci. 9, 6.10.3389/fnhum.2015.00006Search in Google Scholar PubMed PubMed Central

Rombokas, E., Malhotra, M., and Matsuoka, Y. (2011). Task-specific demonstration and practiced synergies for writing with the ACT hand. 2011 IEEE International Conference on Robotics and Automation (ICRA), pp. 5363–5368 (Shanghai, China).10.1109/ICRA.2011.5980218Search in Google Scholar

Rosenblum, S. (2013). Handwriting measures as reflectors of executive functions among adults with developmental coordination disorders (DCD). Front. Psychol. 4, 357.10.3389/fpsyg.2013.00357Search in Google Scholar PubMed PubMed Central

Routson, R.L., Clark, D.J., Bowden, M.G., Kautz, S.A., and Neptune, R.R. (2013). The influence of locomotor rehabilitation on module quality and post-stroke hemiparetic walking performance. Gait Posture 38, 511–517.10.1016/j.gaitpost.2013.01.020Search in Google Scholar PubMed PubMed Central

Safavynia, S.A., Torres-Oviedo, G., and Ting, L.H. (2011). Muscle synergies: implications for clinical evaluation and rehabilitation of movement. Top. Spinal Cord Inj. Rehabil. 17, 16–24.10.1310/sci1701-16Search in Google Scholar PubMed PubMed Central

Saltiel, P., Wyler-Duda, K., D’Avella, A., Tresch, M.C., and Bizzi, E. (2001). Muscle synergies encoded within the spinal cord: evidence from focal intraspinal NMDA iontophoresis in the frog. J. Neurophysiol. 85, 605–619.10.1152/jn.2001.85.2.605Search in Google Scholar PubMed

Sawada, T., Kaneko, F., Aoyama, T., Ogawa, M., and Murakami, T. (2017). Analysis of reaching movements in stroke patients using average variability of electromyogram value. Asian J. Occup. Ther. 13, 13–21.10.11596/asiajot.13.13Search in Google Scholar

Sawers, A., Allen, J.L., and Ting, L.H. (2015). Long-term training modifies the modular structure and organization of walking balance control. J. Neurophysiol. 114, 3359–3373.10.1152/jn.00758.2015Search in Google Scholar PubMed

Seitz, R.J., Stephan, K.M., and Binkofski, F. (2000). Control of action as mediated by the human frontal lobe. Exp. Brain Res. 133, 71–80.10.1007/s002210000402Search in Google Scholar PubMed

Semprini, M., Cuppone, A.V., Delis, I., Squeri, V., Panzeri, S., and Konczak, J. (2016). Biofeedback signals for robotic rehabilitation: assessment of wrist muscle activation patterns in healthy humans. IEEE Trans. Neural Syst. Rehabil. Eng. 25, 883–892.10.1109/TNSRE.2016.2636122Search in Google Scholar PubMed

Sharfi, K. and Rosenblum, S. (2016). Executive functions, time organization and quality of life among adults with learning disabilities. PLoS One 11, e0166939.10.1371/journal.pone.0166939Search in Google Scholar PubMed

Sherrington, C. (1910). The integrative action of the nervous system. CUP Archive.10.1037/13798-000Search in Google Scholar

Takakusaki, K. (2013). Neurophysiology of gait: from the spinal cord to the frontal lobe. Mov. Disord. 28, 1483–1491.10.1002/mds.25669Search in Google Scholar PubMed

Takei, T., Confais, J., Tomatsu, S., Oya, T., and Seki, K. (2017). Neural basis for hand muscle synergies in the primate spinal cord. Proc. Natl. Acad. Sci. USA. 114, 8643–8648.10.1073/pnas.1704328114Search in Google Scholar

Teixeira-Salmela, L.F., Olney, S.J., Nadeau, S., and Brouwer, B. (1999). Muscle strengthening and physical conditioning to reduce impairment and disability in chronic stroke survivors. Arch. Phys. Med. Rehabil. 80, 1211–1218.10.1016/S0003-9993(99)90018-7Search in Google Scholar PubMed

Timmermans, A.A., Spooren, A.I., Kingma, H., and Seelen, H.A. (2010). Influence of task-oriented training content on skilled arm-hand performance in stroke: a systematic review. Neurorehabil. Neural Repair 24, 858–870.10.1177/1545968310368963Search in Google Scholar PubMed

Ting, L.H. and Macpherson, J.M. (2005). A limited set of muscle synergies for force control during a postural task. J. Neurophysiol. 93, 609–613.10.1152/jn.00681.2004Search in Google Scholar PubMed

Tresch, M.C. and Jarc, A. (2009). The case for and against muscle synergies. Curr. Opin. Neurobiol. 19, 601–607.10.1016/j.conb.2009.09.002Search in Google Scholar PubMed PubMed Central

Tresch, M.C., Saltiel, P., and Bizzi, E. (1999). The construction of movement by the spinal cord. Nat. Neurosci. 2, 162–167.10.1038/5721Search in Google Scholar PubMed

Tresch, M.C., Cheung, V.C., and d’Avella, A. (2006). Matrix factorization algorithms for the identification of muscle synergies: evaluation on simulated and experimental data sets. J. Neurophysiol. 95, 2199–2212.10.1152/jn.00222.2005Search in Google Scholar PubMed

Turpin, N.A., Guével, A., Durand, S., and Hug, F. (2011). No evidence of expertise-related changes in muscle synergies during rowing. J. Electromyogr. Kinesiol. 21, 1030–1040.10.1016/j.jelekin.2011.07.013Search in Google Scholar PubMed

Twitchell, T.E. (1951). The restoration of motor function following hemiplegia in man. Brain 74, 443–480.10.1093/brain/74.4.443Search in Google Scholar PubMed

Valero-Cuevas, F.J., Venkadesan, M., and Todorov, E. (2009). Structured variability of muscle activations supports the minimal intervention principle of motor control. J. Neurophysiol. 102, 59–68.10.1152/jn.90324.2008Search in Google Scholar PubMed PubMed Central

Vecchio, M., Gracies, J., Panza, F., Fortunato, F., Vitaliti, G., Malaguarnera, G., Cinone, N., Beatrice, R., Ranieri, M., and Santamato, A. (2017). Change in coefficient of fatigability following rapid, repetitive movement training in post-stroke spastic paresis: a prospective open-label observational study. J. Stroke Cerebrovasc. Dis. 26, 2536–2540.10.1016/j.jstrokecerebrovasdis.2017.05.046Search in Google Scholar PubMed

Weiss, E.J. and Flanders, M. (2004). Muscular and postural synergies of the human hand. J. Neurophysiol. 92, 523–535.10.1152/jn.01265.2003Search in Google Scholar PubMed

Winstein, C.J., Rose, D.K., Tan, S.M., Lewthwaite, R., Chui, H.C., and Azen, S.P. (2004). A randomized controlled comparison of upper-extremity rehabilitation strategies in acute stroke: a pilot study of immediate and long-term outcomes. Arch. Phys. Med. Rehabil. 85, 620–628.10.1016/j.apmr.2003.06.027Search in Google Scholar PubMed

Zafeiriou, D.I. (2004). Primitive reflexes and postural reactions in the neurodevelopmental examination. Pediatr. Neurol. 31, 1–8.10.1016/j.pediatrneurol.2004.01.012Search in Google Scholar PubMed

Zinger, N., Harel, R., Gabler, S., Israel, Z., and Prut, Y. (2013). Functional organization of information flow in the corticospinal pathway. J. Neurosci. 33, 1190–1197.10.1523/JNEUROSCI.2403-12.2013Search in Google Scholar PubMed PubMed Central

Received: 2017-07-24
Accepted: 2017-11-26
Published Online: 2018-02-05
Published in Print: 2018-08-28

©2018 Walter de Gruyter GmbH, Berlin/Boston

Scroll Up Arrow