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Movement curvature planning through force field internal models

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Abstract

Human motion studies have focused primarily on modeling straight point-to-point reaching movements. However, many goal-directed reaching movements, such as movements directed towards oneself, are not straight but rather follow highly curved trajectories. These movements are particularly interesting to study since they are essential in our everyday life, appear early in development and are routinely used to assess movement deficits following brain lesions. We argue that curved and straight-line reaching movements are generated by a unique neural controller and that the observed curvature of the movement is the result of an active control strategy that follows the geometry of one’s body, for instance to avoid trajectories that would hit the body or yield postures close to the joint limits. We present a mathematical model that accounts for such an active control strategy and show that the model reproduces with high accuracy the kinematic features of human data during unconstrained reaching movements directed toward the head. The model consists of a nonlinear dynamical system with a single stable attractor at the target. Embodiment-related task constraints are expressed as a force field that acts on the dynamical system. Finally, we discuss the biological plausibility and neural correlates of the model’s parameters and suggest that embodiment should be considered as a main cause for movement trajectory curvature.

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References

  • Admiraal MA, Kusters MJMAM, Gielen SCAM (2004) Modeling kinematics and dynamics of human arm movements. Motor Control 8(3): 312–338

    PubMed  Google Scholar 

  • Ajemian R, Bullock D, Grossberg S (2001) A model of movement coordinates in the motor cortex: posture-dependent changes in the gain and direction of single cell tuning curves. Cereb Cortex 11(12): 1124–1135

    Article  PubMed  CAS  Google Scholar 

  • Atkeson CG, Hollerbach JM (1985) Kinematic features of unrestrained vertical arm movements. J Neurosci 5(9): 2318–2330

    PubMed  CAS  Google Scholar 

  • Bernstein NA (1947) On the construction of movements. Medgiz, Moscow

    Google Scholar 

  • Bernstein NA (1996) Levels of construction of movements. In: Latash ML, Turvey MT(eds) Dexterity and its development. Lawrence Erlbaum Associates, Mahwah, pp 115–170

    Google Scholar 

  • Biess A, Liebermann DG, Flash T (2007) A computational model for redundant human three dimensional pointing movements: integration of independant spatial and temporal motor plans simplifies movement dynamics. J Neurosci 27(48): 13045–13064

    Article  PubMed  CAS  Google Scholar 

  • Bizzi E, Accornero N, Chapple W, Hogan N (1982) Arm trajectory formation in monkeys. Exp Brain Res 46(1): 139–143

    Article  PubMed  CAS  Google Scholar 

  • Brenner E, Smeets JBJ (1995) Moving one’s finger to a visually specified position: target orientation influences the finger’s path. Exp Brain Res 105(2): 318–320

    Article  PubMed  CAS  Google Scholar 

  • Brown SH, Cooke JD (1990) Movement-related phasic muscle activation. I. Relations with temporal profile of movement. J Neurophysiol 63(3): 455–464

    PubMed  CAS  Google Scholar 

  • Bullock D, Grossberg S (1988) Neural dynamics of planned arm movements: emergent invariants and speed-accuracy properties during trajectory formation. Psychol Rev 95(1): 49–90

    Article  PubMed  CAS  Google Scholar 

  • Bullock D, Grossberg S, Mannes C (1993) A neural network model for cursive script production. Biol Cybern 70(1): 15–28

    Article  Google Scholar 

  • Bullock D, Cisek P, Grossberg S (1998) Cortical networks for control of voluntary arm movements under variable force conditions. Cereb Cortex 8(1): 48–62

    Article  PubMed  CAS  Google Scholar 

  • Christel MI, Billard A (2002) Comparison between macaques’ and humans’ kinematics of prehension: the role of morphological differences and control mechanisms. Behav Brain Res 131(1–2): 169–184

    Article  PubMed  Google Scholar 

  • Cisek P, Grossberg S, Bullock D (1998) A cortico-spinal model of reaching and proprioception under multiple task constraints. J Cogn Neurosci 10(4): 425–444

    Article  PubMed  CAS  Google Scholar 

  • Clamman HP (1969) Statistical analysis of motor unit firing pattern in human skeletal muscle. Biophys J 9: 1233–1251

    Article  Google Scholar 

  • Clancy EA, Hogan N (1999) Probability density of the surface electromyogram and its relation to amplitude detectors. IEEE Trans Biomed Eng 46(6): 730–739

    Article  PubMed  CAS  Google Scholar 

  • Conditt MA, Gandolfo F, Mussa-Ivaldi FA (1997) The motor system does not learn the dynamics of the arm by rote memorization of past experience. J Neurophysiol 78(1): 554–560

    PubMed  CAS  Google Scholar 

  • Cruse H, Brüwer M (1987) The human arm as a redundant manipulator: the control of path and joint angles. Biol Cybern 57(1–2): 134–144

    Google Scholar 

  • d’Avella A, Saltiel P, Bizzi E (2003) Combinations of muscle synergies in the construction of a natural motor behavior. Nat Neurosci 6(3): 300–308

    Article  PubMed  Google Scholar 

  • de Graaf JB, Sittig AC, Denier von der Gon JJ (1991) Misdirections in slow goal-directed arm movements and pointer-setting tasks. Exp Brain Res 84(2): 434–438

    Article  PubMed  Google Scholar 

  • de Graaf JB, Sittig AC, Denier von der Gon JJ (1994) Misdirections in slow, goal-directed arm movements are not primarily visually based. Exp Brain Res 99(3): 464–472

    Article  PubMed  Google Scholar 

  • Dalby JT, Gibson D, Grossi V, Schneider RD (1980) Lateralized hand gesture during speech. J Motor Behav 12(4): 292–297

    CAS  Google Scholar 

  • De Renzi E, Lucchelli F (1988) Ideational apraxia. Brain 111(Pt 5): 1173–1185

    Article  PubMed  Google Scholar 

  • Desmurget M, Grafton S (2000) Forward modeling allows feedback control for fast reaching movements. Trends Cogn Sci 4(11): 423–431

    Article  PubMed  Google Scholar 

  • Desmurget M, Jordan M, Prablanc C, Jeannerod M (1997) Constrained and unconstrained movements involve different control strategies. J Neurophysiol 77(3): 1644–1650

    PubMed  CAS  Google Scholar 

  • Fitts PM (1954) The information capacity of the human motor system in controlling the amplitude of movement. J Exp Psychol 47(6): 381–391

    Article  PubMed  CAS  Google Scholar 

  • Flash T (1987) The control of hand equilibrium trajectories in multi-joint arm movements. Biol Cybern 57(4–5): 257–274

    Article  PubMed  CAS  Google Scholar 

  • Flash T, Hogan N (1985) The coordination of arm movements: an experimentally confirmed mathematical model. J Neurosci 5(7): 1688–1703

    PubMed  CAS  Google Scholar 

  • Gandolfo F, Mussa-Ivaldi FA, Bizzi E (1996) Motor learning by field approximation. Proc Natl Acad Sci USA 93(9): 3843–3846

    Article  PubMed  CAS  Google Scholar 

  • Gielen CCAM, van den Oosten K, Pull ter Gunne F (1985) Relation between EMG activation patterns and kinematic properties of aimed arm movements. J Mot Behav 17(4): 421–442

    PubMed  CAS  Google Scholar 

  • Goldenberg G, Hagmann S (1997) The meaning of meaningless gestures: a study of visuo-imitative apraxia. Neuropsychologia 35(3): 333–341

    Article  PubMed  CAS  Google Scholar 

  • Graziano MSA, Cooke DF, Taylor CSR (2000) Coding the location of the arm by sight. Science 290(5497): 1782–1786

    Article  PubMed  CAS  Google Scholar 

  • Graziano MSA, Taylor CSR, Moore T (2002) Complex movements evoked by microstimulation of precentral cortex. Neuron 34(5): 841–851

    Article  PubMed  CAS  Google Scholar 

  • Graziano MSA, Aflalo TNS, Cooke DF (2005) Arm movements evoked by electrical stimulation in the motor cortex of monkeys. J Neurophysiol 94(6): 4209–4223

    Article  PubMed  Google Scholar 

  • Guigon E, Baraduc P, Desmurget M (2007) Computational motor control: redundancy and invariance. J Neurophysiol 97(1): 331–347

    Article  PubMed  Google Scholar 

  • Hamilton AFC, Wolpert DM (2002) Controlling the statistics of action: obstacle avoidance. J Neurophysiol 87(5): 2434–2440

    PubMed  Google Scholar 

  • Harris CM, Wolpert DM (1998) Signal-dependent noise determines motor planning. Nature 394(6695): 780–784

    Article  PubMed  CAS  Google Scholar 

  • Hersch M, Billard A (2007) Reaching with multi-referential dynamical systems. Auton Robot 25(1–2): 71–83

    Google Scholar 

  • Hoos H, Stützle T (2004) Stochastic local search: Foundations and applications. Elsevier/Morgan Kaufmann, San Francisco

    Google Scholar 

  • Klein Breteler MD, Meulenbroek RGJ, Gielen SCAM (1998) Geometric features of workspace and joint-space paths of 3D reaching movements. Acta Psychol 100(1–2): 37–53

    Article  CAS  Google Scholar 

  • Lacquaniti F, Terzuolo C, Viviani P (1983) The law relating the kinematic and figural aspects of drawing movements. Acta Psychol 54(1–3): 115–130

    Article  CAS  Google Scholar 

  • Lacquaniti F, Soechting JF, Terzuolo SA (1986) Path constraints on point-to-point arm movements in three-dimensional space. Neuroscience 17(2): 313–324

    Article  PubMed  CAS  Google Scholar 

  • Lavergne J, Kimura D (1987) Hand movement asymmetry during speech: no effect of speaking topic. Neuropsychologia 25(4): 689–693

    Article  PubMed  CAS  Google Scholar 

  • Liebermann DG, Biess A, Gielen CCAM, Flash T (2006) Intrinsic joint kinematic planning. II: Hand-path predictions based on a Listing’s plane constraint. Exp Brain Res 171(2): 155–173

    Article  PubMed  CAS  Google Scholar 

  • Liebermann DG, Krasovsky T, Berman S (2008) Planning maximally smooth hand movements constrained to nonplanar workspaces. J Mot Behav 40(6): 516–531

    Article  PubMed  Google Scholar 

  • Matthews PBC (1996) Relationship of firing intervals of human motor units to the trajectory of post-spike after-hyperpolarization and synaptic noise. J Physiol 492(Pt 2): 597–628

    PubMed  CAS  Google Scholar 

  • McIntyre J, Gurfinkel EV, Lipshits MI, Droulez J, Gurfinkel VS (1995) Measurements of human force control during a constrained arm motion using a force-actuated joystick. J Neurophysiol 73(3): 1201–1222

    PubMed  CAS  Google Scholar 

  • Miall RC, Haggard PN (1995) The curvature of human arm movements in the absence of visual experience. Exp Brain Res 103(3): 421–428

    Article  PubMed  CAS  Google Scholar 

  • Moran DW, Schwartz AB (1999) Motor cortical activity during drawing movements: population representation during spiral tracing. J Neurophysiol 82(5): 2693–2704

    PubMed  CAS  Google Scholar 

  • Morasso P (1981) Spatial control of arm movements. Exp Brain Res 42(2): 223–227

    Article  PubMed  CAS  Google Scholar 

  • Nakano E, Imamizu H, Osu R, Uno Y, Gomi H, Yoshioka T, Kawato M (1999) Quantitative examinations of internal representations for arm trajectory planning: minimum commanded torque change model. J Neurophysiol 81(5): 2140–2155

    PubMed  CAS  Google Scholar 

  • Neter J, Kutner MH, Nachtsheim CJ, Wasserman W (1996) Applied linear statistical models. McGraw-Hill/Irwin, Chicago

    Google Scholar 

  • Nishikawa KC, Murray ST, Flanders M (1999) Do arm postures vary with the speed of reaching?. J Neurophysiol 81(5): 2582–2586

    PubMed  CAS  Google Scholar 

  • Okadome T, Honda M (1999) Kinematic construction of the trajectory of sequential arm movements. Biol Cybern 80(3): 157–169

    Article  PubMed  CAS  Google Scholar 

  • Oldfield RC (1971) The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 9(1): 97–113

    Article  PubMed  CAS  Google Scholar 

  • Osu R, Uno Y, Koike Y, Kawato M (1997) Possible explanations for trajectory curvature in multijoint arm movements. J Exp Psychol Hum Percept Perform 23(3): 890–913

    Article  PubMed  CAS  Google Scholar 

  • Osu R, Kamimura N, Iwasaki H, Nakano E, Harris CM, Wada Y, Kawato M (2004) Optimal impedance control for task achievement in the presence of signal-dependant noise. J Neurophysiol 92(2): 1199–1215

    Article  PubMed  Google Scholar 

  • Paine RW, Grossberg S, Van Gemmert AWA (2004) A quantitative evaluation of the AVITEWRITE model of handwriting learning. Hum Mov Sci 23(6): 837–860

    Article  PubMed  CAS  Google Scholar 

  • Papaxanthis C, Pozzo T, Popov KE, McIntyre J (1998) Hand trajectories of vertical arm movements in one-G and zero-G environments. Evidence for a central representation of gravitational force. Exp Brain Res 120(4): 496–502

    Article  PubMed  CAS  Google Scholar 

  • Pellegrini JJ, Flanders M (1996) Force path curvature and conserved features of muscle activation. Exp Brain Res 110(1): 80–90

    Article  PubMed  CAS  Google Scholar 

  • Petreska B, Adriani M, Blanke O, Billard AG (2007) Apraxia: a review. Prog Brain Res 164: 61–83

    Article  PubMed  Google Scholar 

  • Sabes PN, Jordan MI (1997) Obstacle avoidance and a perturbation sensitivity model of motor planning. J Neurosci 17(18): 7119–7128

    PubMed  CAS  Google Scholar 

  • Sauser E, Billard A (2006) Dynamic updating of distributed neural representations using forward models. Biol Cybern 95(6): 567–588

    Article  PubMed  Google Scholar 

  • Schaal S, Sternad D (2001) Origins and violations of the 2/3 power law in rhythmic three-dimensional arm movements. Exp Brain Res 136(1): 60–72

    Article  PubMed  CAS  Google Scholar 

  • Schmidt RA, Zelaznik H, Hawkins B, Frank JS, Quinn JT (1979) Motor-output variability: a theory for the accuracy of rapid motor acts. Psychol Rev 47(5): 415–451

    Article  PubMed  CAS  Google Scholar 

  • Scott SH, Sergio LE, Kalaska JF (1997) Reaching movements with similar hand paths but different arm orientations. II. Activity of individual cells in dorsal premotor cortex and parietal area 5. J Neurophysiol 78(5): 2413–2426

    PubMed  CAS  Google Scholar 

  • Sha D, Patton J, Mussa-Ivaldi FA (2006) Minimum jerk reaching movements of human arm with mechanical constraints at endpoint. Int J Comput Syst Signal 7(1): 41–50

    Google Scholar 

  • Shadmehr R, Brashers-Krug T (1997) Functional stages in the formation of human long-term motor memory. J Neurosci 17(1): 409–419

    PubMed  CAS  Google Scholar 

  • Shadmehr R, Mussa-Ivaldi FA (1994) Adaptive representation of dynamics during learning of a motor task. J Neurosci 14(5 Pt 2): 3208–3224

    PubMed  CAS  Google Scholar 

  • Soechting JF, Lacquaniti F (1981) Invariant characteristics of a pointing movement in man. J Neurosci 1(7): 710–720

    PubMed  CAS  Google Scholar 

  • Soechting JF, Buneo CA, Herrmann U, Flandres M (1995) Moving effortlessly in three dimensions: does Donders’ law apply to arm movement?. J Neurosci 15(9): 6271–6280

    PubMed  CAS  Google Scholar 

  • St-Amant Y, Rancourt D, Clancy EA (1998) Influence of smoothing window length on electromyogram amplitude estimates. IEEE Trans Biomed Eng 45(6): 795–800

    Article  PubMed  CAS  Google Scholar 

  • Sutton GG, Sykes K (1967) The variation of hand tremor with force in healthy subjects. J Physiol 191(3): 699–711

    PubMed  CAS  Google Scholar 

  • Thoroughman KA, Shadmehr R (2000) Learning of action through adaptive combination of motor primitives. Nature 407(6805): 742–747

    Article  PubMed  CAS  Google Scholar 

  • Todorov E (2004) Optimality principles in sensorimotor control. Nat Neurosci 7(9): 907–915

    Article  PubMed  CAS  Google Scholar 

  • Todorov E, Jordan MI (2002) Optimal feedback control as a theory of motor coordination. Nat Neurosci 5(11): 1226–1235

    Article  PubMed  CAS  Google Scholar 

  • Torres EB, Zipser D (2002) Reaching to grasp with a multi-joined arm. I. Computational model. J Neurophysiol 88(5): 2355–2367

    Article  PubMed  Google Scholar 

  • Uno Y, Kawato M, Suzuki R (1989) Formation and control of optimal trajectory in human multijoint arm movement. Minimum torque-change model. Biol Cybern 61(2): 89–101

    Article  PubMed  CAS  Google Scholar 

  • Vetter P, Flash T, Wolpert DM (2002) Planning movements in a simple redundant task. Curr Biol 12(6): 488–491

    Article  PubMed  CAS  Google Scholar 

  • Wada Y, Kaneko Y, Nakano E, Osu R, Kawato M (2001) Quantitative examinations for multi joint arm trajectory planning—using a robust calculation algorithm of the minimum commanded torque change trajectory. Neural Netw 14(4–5): 381–393

    Article  PubMed  CAS  Google Scholar 

  • Wang W, Chan SS, Heldman DA, Moran DW (2007) Motor cortical representation of position and velocity during reaching. J Neurophysiol 97(6): 4258–4270

    Article  PubMed  Google Scholar 

  • Wolpert DM, Ghahramani Z, Jordan MI (1994) Perceptual distortion contributes to the curvature of human reaching movements. Exp Brain Res 98(1): 153–156

    Article  PubMed  CAS  Google Scholar 

  • Wolpert DM, Ghahramani Z, Jordan MI (1995) Are arm trajectories planned in kinematic or dynamic coordinates? An adaptation study. Exp Brain Res 103(3): 460–470

    Article  PubMed  CAS  Google Scholar 

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Correspondence to Aude Billard.

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Petreska, B., Billard, A. Movement curvature planning through force field internal models. Biol Cybern 100, 331–350 (2009). https://doi.org/10.1007/s00422-009-0300-2

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