Abstract
Recent reports indicate that rhythmic and discrete upper-limb movements are two different motor primitives which recruit, at least partially, distinct neural circuitries. In particular, rhythmic movements recruit a smaller cortical network than discrete movements. The goal of this paper is to compare the levels of disability in performing rhythmic and discrete movements after a stroke. More precisely, we tested the hypothesis that rhythmic movements should be less affected than discrete ones, because they recruit neural circuitries that are less likely to be damaged by the stroke. Eleven stroke patients and eleven age-matched control subjects performed discrete and rhythmic movements using an end-effector robot (REAplan). The rhythmic movement condition was performed with and without visual targets to further decrease cortical recruitment. Movement kinematics was analyzed through specific metrics, capturing the degree of smoothness and harmonicity. We reported three main observations: (1) the movement smoothness of the paretic arm was more severely degraded for discrete movements than rhythmic movements; (2) most of the patients performed rhythmic movements with a lower harmonicity than controls; and (3) visually guided rhythmic movements were more altered than non-visually guided rhythmic movements. These results suggest a hierarchy in the levels of impairment: Discrete movements are more affected than rhythmic ones, which are more affected if they are visually guided. These results are a new illustration that discrete and rhythmic movements are two fundamental primitives in upper-limb movements. Moreover, this hierarchy of impairment opens new post-stroke rehabilitation perspectives.
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References
Andersen RA, Cui H (2009) Intention, action planning, and decision making in parietal–frontal circuits. Neuron 63:568–583
Balasubramanian S, Melendez-Calderon A, Burdet E (2012) A robust and sensitive metric for quantifying movement smoothness. IEEE Trans Biomed Eng 59:2126–2136
Barbeau H, Visintin M (2003) Optimal outcomes obtained with body-weight support combined with treadmill training in stroke subjects. Arch Phys Med Rehabil 84:1458–1465
Brown TG (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 48:18–46
Buchanan JJ, Park J-H, Shea CH (2006) Target width scaling in a repetitive aiming task: switching between cyclical and discrete units of action. Exp Brain Res 175:710–725
Cirstea M, Levin MF (2000) Compensatory strategies for reaching in stroke. Brain 123:940–953
Cohen AH, Rossignol S, Grillner S (1988) Neural control of rhythmic movements in vertebrates. Wiley, New York
Collins JJ, Richmond S (1994) Hard-wired central pattern generators for quadrupedal locomotion. Biol Cybern 71:375–385
Dagnelie P (2013) Statistique théorique et appliquée, 1st edn. De Boeck, Bruxelles
De Rugy A, Sternad D (2003) Interaction between discrete and rhythmic movements: reaction time and phase of discrete movement initiation during oscillatory movements. Brain Res 994:160–174
Desmurget M, Epstein CM, Turner RS, Prablanc C, Alexander GE, Grafton ST (1999) Role of the posterior parietal cortex in updating reaching movements to a visual target. Nat Neurosci 2:563–567
Desmurget M, Gréa H, Grethe JS, Prablanc C, Alexander GE, Grafton ST (2001) Functional anatomy of nonvisual feedback loops during reaching: a positron emission tomography study. J Neurosci 21:2919–2928
Dietz V (2002) Proprioception and locomotor disorders. Nat Rev Neurosci 3:781–790
Dimitrijevic MR, Gerasimenko Y, Pinter MM (1998) Evidence for a spinal central pattern generator in humansa. Ann N Y Acad Sci 860:360–376
Dipietro L, Krebs HI, Fasoli SE, Volpe BT, Hogan N (2009) Submovement changes characterize generalization of motor recovery after stroke. Cortex 45:318–324
Diserens K, Perret N, Chatelain S, Bashir S, Ruegg D, Vuadens P, Vingerhoets F (2007) The effect of repetitive arm cycling on post stroke spasticity and motor control: repetitive arm cycling and spasticity. J Neurol Sci 253:18–24
Duysens J, Van de Crommert HW (1998) Neural control of locomotion; Part 1: the central pattern generator from cats to humans. Gait Posture 7:131–141
Fitts PM (1954) The information capacity of the human motor system in controlling the amplitude of movement. J Exp Psychol 47(6):381
Fugl-Meyer A, Jääskö L, Leyman I, Olsson S, Steglind S (1974) The post-stroke hemiplegic patient. 1. A method for evaluation of physical performance. Scand J Rehabil Med 7:13–31
Gilliaux M, Lejeune T, Detrembleur C, Sapin J, Dehez B, Stoquart G (2012) A robotic device as a sensitive quantitative tool to assess upper limb impairments in stroke patients: a preliminary prospective cohort study. J Rehabil Med 44:210–217
Gilliaux M, Lejeune TM, Detrembleur C, Sapin J, Dehez B, Selves C, Stoquart G (2014a) Using the robotic device REAplan as a valid, reliable, and sensitive tool to quantify upper limb impairments in stroke patients. J Rehabil Med 46:00–00
Gilliaux M, Renders A, Dispa D, Holvoet D, Sapin J, Dehez B, Detrembleur C, Lejeune TM, Stoquart G (2014b) Upper limb robot-assisted therapy in cerebral palsy: a single-blind randomized controlled trial. Neurorehabil Neural Repair. doi:10.1177/1545968314541172
Giszter SF (2015) Motor primitives—new data and future questions. Curr Opin Neurobiol 33:156–165
Glover S, Wall MB, Smith AT (2012) Distinct cortical networks support the planning and online control of reaching-to-grasp in humans: cortical planning and control. Eur J Neurosci 35:909–915
Goto Y, Jono Y, Hatanaka R, Nomura Y, Tani K, Chujo Y, Hiraoka K (2014) Different corticospinal control between discrete and rhythmic movement of the ankle. Front Hum Neurosci 8:578. doi:10.3389/fnhum.2014.00578
Gowland C, Basmajian JV, Plews N, Burcea I et al (1992) Agonist and antagonist activity during voluntary upper-limb movement in patients with stroke. Phys Ther 72:624–633
Guiard Y (1993) On Fitts’s and Hooke’s laws: simple harmonic movement in upper-limb cyclical aiming. Acta Psychol (Amst) 82:139–159
Haiss F, Schwarz C (2005) Spatial segregation of different modes of movement control in the whisker representation of rat primary motor cortex. J Neurosci 25:1579–1587
Hanakawa T, Dimyan MA, Hallett M (2008) Motor planning, imagery, and execution in the distributed motor network: a time-course study with functional MRI. Cereb Cortex 18:2775–2788
Hogan N, Sternad D (2007) On rhythmic and discrete movements: reflections, definitions and implications for motor control. Exp Brain Res 181:13–30
Hogan N, Sternad D (2009) Sensitivity of smoothness measures to movement duration, amplitude, and arrests. J Mot Behav 41:529–534
Hogan N, Sternad D (2012) Dynamic primitives of motor behavior. Biol Cybern 106:727–739
Hogan N, Sternad D (2013) Dynamic primitives in the control of locomotion. Front Comput Neurosci 7:71
Howard IS, Ingram JN, Wolpert DM (2011) Separate representations of dynamics in rhythmic and discrete movements: evidence from motor learning. J Neurophysiol 105:1722–1731
Ijspeert AJ (2008) Central pattern generators for locomotion control in animals and robots: a review. Neural Netw 21:642–653
Ikegami T, Hirashima M, Taga G, Nozaki D (2010) Asymmetric transfer of visuomotor learning between discrete and rhythmic movements. J Neurosci 30:4515–4521
Kamper DG, McKenna-Cole AN, Kahn LE, Reinkensmeyer DJ (2002) Alterations in reaching after stroke and their relation to movement direction and impairment severity. Arch Phys Med Rehabil 83:702–707
Kawashima N, Nozaki D, Abe MO, Akai M, Nakazawa K (2005) Alternate leg movement amplifies locomotor-like muscle activity in spinal cord injured persons. J Neurophysiol 93:777–785
Krebs HI, Hogan N, Volpe BT, Aisen ML, Diels C (1999) Overview of clinical trials with MIT-MANUS: a robot-aided neuro-rehabilitation facility. Technol Health Care 7:419–423
Langhorne P, Bernhardt J, Kwakkel G (2011) Stroke rehabilitation. Lancet 377:1693–1702
Levy-Tzedek S, Krebs HI, Song D, Hogan N, Poizner H (2010) Non-monotonicity on a spatio-temporally defined cyclic task: evidence of two movement types? Exp Brain Res 202:733–746
Levy-Tzedek S, Krebs HI, Arle JE, Shils JL, Poizner H (2011) Rhythmic movement in Parkinson’s disease: effects of visual feedback and medication state. Exp Brain Res 211:277–286
Luft AR, McCombe-Waller S, Whitall J, Forrester LW, Macko R, Sorkin JD, Schulz JB, Goldberg AP, Hanley DF (2004) Repetitive bilateral arm training and motor cortex activation in chronic stroke: a randomized controlled trial. JAMA 292:1853–1861
Marder E, Bucher D (2001) Central pattern generators and the control of rhythmic movements. Curr Biol 11:R986–R996
Mazzoni P, Hristova A, Krakauer JW (2007) Why don’t we move faster? Parkinson’s disease, movement vigor, and implicit motivation. J Neurosci 27:7105–7116
Nozaki D, Kurtzer I, Scott SH (2006) Limited transfer of learning between unimanual and bimanual skills within the same limb. Nat Neurosci 9:1364–1366
Rohrer B, Fasoli S, Krebs HI, Hughes R, Volpe B, Frontera WR, Stein J, Hogan N (2002) Movement smoothness changes during stroke recovery. J Neurosci 22:8297–8304
Ronsse R, Sternad D, Lefevre P (2009) A computational model for rhythmic and discrete movements in uni- and bimanual coordination. Neural Comput 21:1335–1370
Ronsse R, Puttemans V, Coxon JP, Goble DJ, Wagemans J, Wenderoth N, Swinnen SP (2011) Motor learning with augmented feedback: modality-dependent behavioral and neural consequences. Cereb Cortex 21:1283–1294
Schaal S, Kotosaka S, Sternad D (2000) Nonlinear dynamical systems as movement primitives. In: IEEE international conference on humanoid robotics, pp 1–11. http://wwwiaim.ira.uka.de/users/rogalla/WebOrdnerMaterial/schaal-ICHR2000.pdf. Accessed 17 Feb 2015
Schaal S, Sternad D, Osu R, Kawato M (2004) Rhythmic arm movement is not discrete. Nat Neurosci 7:1136–1143
Shadmehr R, Krakauer JW (2008) A computational neuroanatomy for motor control. Exp Brain Res 185:359–381
Shik ML, Severin FV, Orlovsky GN (1966) Control of walking and running by means of electric stimulation of the midbrain. Biofizika 11:659–666
Simkins M, Jacobs AB, Rosen J (2013) Rhythmic affects on stroke-induced joint synergies across a range of speeds. Exp Brain Res 229:517–524
Smits-Engelsman B, Swinnen S, Duysens J (2006) The advantage of cyclic over discrete movements remains evident following changes in load and amplitude. Neurosci Lett 396:28–32
Spencer RM, Zelaznik HN, Diedrichsen J, Ivry RB (2003) Disrupted timing of discontinuous but not continuous movements by cerebellar lesions. Science 300:1437–1439
Spencer RMC, Ivry RB, Zelaznik HN (2005) Role of the cerebellum in movements: control of timing or movement transitions? Exp Brain Res 161:383–396
Sternad D, Dean WJ (2003) Rhythmic and discrete elements in multi-joint coordination. Brain Res 989:152–171
Sternad D, Dean WJ, Schaal S (2000) Interaction of rhythmic and discrete pattern generators in single-joint movements. Hum Mov Sci 19:627–664
Sternad D, Marino H, Charles SK, Duarte M, Dipietro L, Hogan N (2013) Transitions between discrete and rhythmic primitives in a unimanual task. Front Comput Neurosci 7:90. doi:10.3389/fncom.2013.00090
Swinnen SP (2002) Intermanual coordination: from behavioural principles to neural-network interactions. Nat Rev Neurosci 3:348–359
Van Mourik AM, Beek PJ (2004) Discrete and cyclical movements: unified dynamics or separate control? Acta Psychol (Amst) 117:121–138
Whitall J, Waller SM, Silver KH, Macko RF (2000) Repetitive bilateral arm training with rhythmic auditory cueing improves motor function in chronic hemiparetic stroke. Stroke 31:2390–2395
White O, Bleyenheuft Y, Ronsse R, Smith AM, Thonnard J-L, Lefevre P (2008) Altered gravity highlights central pattern generator mechanisms. J Neurophysiol 100:2819–2824
Zehr EP, Duysens J (2004) Regulation of arm and leg movement during human locomotion. Neuroscientist 10:347–361
Zehr EP, Carroll TJ, Chua R, Collins DF, Frigon A, Haridas C, Hundza SR, Thompson AK (2004) Possible contributions of CPG activity to the control of rhythmic human arm movement. Can J Physiol Pharmacol 82:556–568
Zehr EP, Loadman PM, Hundza SR (2012) Neural control of rhythmic arm cycling after stroke. J Neurophysiol 108:891–905
Zondervan DK, Smith B, Reinkensmeyer DJ (2013) Lever-actuated resonance assistance (LARA): a wheelchair-based method for upper extremity therapy and overground ambulation for people with severe arm impairment. In: Rehabilitation robotics (ICORR), International conference on IEEE, pp 1–6. http://ieeexplore.ieee.org/xpls/abs_all.jsp?arnumber=6650400. Accessed 7 Oct 2014b
Zondervan DK, Palafox L, Hernandez J, Reinkensmeyer DJ (2013b) The resonating arm exerciser: design and pilot testing of a mechanically passive rehabilitation device that mimics robotic active assistance. J Neuroeng Rehabil 10:39
Acknowledgments
The authors would like to thank Catherine Rasse for her support with the statistics, the subjects for their availability to participate in the study and the physiotherapists who helped in recruitment of the patients.
Funding
This work was supported by the Belgian F.R.S.-FNRS (FRIA grant awarded to PL, Fonds pour la Recherche dans l’Industrie et l’Agriculture) and by the “Fondation van Goethem Brichant.”
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Glossary
- D-T
-
Discrete task with small targets
- FMA-UE
-
Fugl-Meyer assessment of the upper extremity
- H
-
Harmonicity index
- ID
-
Index of difficulty
- PEAK
-
Number of peaks in the velocity profile
- LDJ
-
Logarithmic dimensionless jerk
- R-T
-
Rhythmic task with large targets
- R-NT
-
Rhythmic task without targets
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Leconte, P., Orban de Xivry, JJ., Stoquart, G. et al. Rhythmic arm movements are less affected than discrete ones after a stroke. Exp Brain Res 234, 1403–1417 (2016). https://doi.org/10.1007/s00221-015-4543-y
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DOI: https://doi.org/10.1007/s00221-015-4543-y