Skip to main content
SpringerLink
Log in

The internal model and the leading joint hypothesis: implications for control of multi-joint movements

  • Review
  • Published:
Experimental Brain Research Aims and scope Submit manuscript

Abstract

This article presents a theoretical generalization of recent experimental findings accumulated in support of two concepts of inter-segmental dynamics regulation during multi-joint movements. The concepts are the internal model of inter-segmental dynamics and the leading joint hypothesis (LJH). The internal model of limb dynamics is a well-established interpretation of feed-forward control. Recent experiments have generated new information about the organization of the internal model and its role in regulation of inter-segmental dynamics. The LJH, which proposes a simplified principle of the regulation of inter-segmental dynamics, is at the beginning stage of development. This paper outlines major results obtained in these two research directions and demonstrates that the two groups of findings complement and augment each other, suggesting a simple and robust hierarchical strategy of multi-joint movement control that exploits specific mechanical properties of human limbs.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

Notes

  1. In the latest interpretations, the inputs of lookup tables include the movement trajectory together with a neighborhood of the trajectory in the trajectory manifold (Poggio and Bizzi 2004). Possible implementation of this principle is Gaussian tuning of the trajectory (Thoroughman and Shadmehr 2000)

  2. If novel inter-segmental dynamics are practiced and structured algorithms are available for only a limited number of discrete locations in the intrinsic space, motion in intermediate locations may be performed with use of interpolation of the constant estimates of A and B obtained for neighboring structured algorithms (Malfait et al. 2005).

References

  • Ariff G, Donchin O, Nanayakkara T, Shadmehr R (2002) A real-time state predictor in motor control: study of saccadic eye movements during unseen reaching movements. J Neurosci 22:7721–7729

    PubMed  Google Scholar 

  • Atkeson CG (1989) Learning arm kinematics and dynamics. Ann Rev Neurosci 12:157–183

    Article  PubMed  Google Scholar 

  • Baev KV, Shimansky YP (1992) Principles of organization of neural systems controlling automatic movements in animals. Prog Neurobiol 39:45–112

    Article  PubMed  Google Scholar 

  • Bagesteiro LB, Sainburg RL (2005) Interlimb transfer of load compensation during rapid elbow joint movements. Exp Brain Res 161:155–165

    Article  PubMed  Google Scholar 

  • Bastian AJ, Martin TA, Keating JG, Thach WT (1996) Cerebellar ataxia: abnormal control of interaction torques across multiple joints. J Neurophysiol 76:492–509

    PubMed  Google Scholar 

  • Bastian AJ, Zackowski KM, Thach WT (2000) Cerebellar ataxia: torque deficiency or torque mismatch between joints?. J Neurophysiol 83:3019–3030

    PubMed  Google Scholar 

  • Beer RF, Dewald JPA, Rymer WZ (2000) Deficits in the coordination of multijoint arm movements in patients with hemiparesis: evidence for disturbed control of limb dynamics. Exp Brain Res 131:305–319

    Article  PubMed  Google Scholar 

  • Berardelli A, Hallett M, Rothwell JC, Agostino R, Manfredi M, Thompson PD, Marsden CD (1996) Single-joint rapid arm movements in normal subjects and in patients with motor disorders. Brain 119:661–674

    PubMed  Google Scholar 

  • Bernstein N (1967) The co-ordination and regulation of movements. Pergamon Press, Oxford, UK

    Google Scholar 

  • Bhushan N, Shadmehr R (1999) Computational nature of human adaptive control during learning of reaching movements in force fields. Biol Cyber 81:39–60

    Article  Google Scholar 

  • Bizzi E, Hogan N, Mussa-Ivaldi FA, Giszter S (1992) Does the nervous system use equilibrium-point control to guide single and multiple joint movements?. Behav Brain Sci 15:603–613

    Google Scholar 

  • Buchanan JJ (2004) Learning a single limb multijoint coordination pattern: the impact of a mechanical constraint on the coordination dynamics of learning and transfer. Exp Brain Res 156:39–54

    Article  PubMed  Google Scholar 

  • Buchanan JJ, Kelso SA, de Guzman GC (1997) Self-organization of trajectory formation. I. Experimental evidence. Biol Cybern 76:257–273

    Article  PubMed  Google Scholar 

  • Chaffin DB, Andersson GBJ (1984) Occupational biomechanics. Wiley, New York, pp 64–75

    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 78:554–560

    PubMed  Google Scholar 

  • Criscimagna-Hemminger SE, Donchin O, Gazzaniga MS, Shadmehr R (2003) Learned dynamics of reaching movements generalize from dominant to nondominant arm. J Neurophysiol 89:168–176

    PubMed  Google Scholar 

  • Debicki DB, Gribble PL (2004) Inter-joint coupling strategy during adaptation to novel viscous loads in human arm movements. J Neurophysiol 92:754–765

    Article  PubMed  Google Scholar 

  • Diedrich FJ, Warren WH (1995) Why change gaits-dynamics of the walk run transition. J Exp Psychol Human Percept Perform 21:183–202

    Article  Google Scholar 

  • DiZio P, Lackner JR (1995) Motor adaptation to Coriolis force perturbations of reaching movements: endpoint but not trajectory adaptation transfers to the nonexposed arm. J Neurophysiol 74:1787–1792

    PubMed  Google Scholar 

  • Doonskaya NV (1998) The artificial potential method for control of robot constrained motion. IEEE Trans Syst Man Cybernetic 28:447–453

    Article  Google Scholar 

  • Dounskaia N, Swinnen SP, Walter CB, Spaepen AJ, Verschueren SMP (1998) Hierarchical control of different elbow-wrist coordination patterns. Exp Brain Res 121:239–254

    Article  PubMed  Google Scholar 

  • Dounskaia N, Swinnen SP, Walter CB (2000) A principle of control of rapid multijoint movements: the leading joint hypothesis. In: Winter JM, Crago PE (eds) Biomechanics and neural control of posture and movement. Springer-Verlag, New York Inc., pp 390–403

    Google Scholar 

  • Dounskaia N, Ketcham CJ, Stelmach GE (2002a) Commonalities and differences in control of a large set of drawing movements. Exp Brain Res 146:11–25

    Article  PubMed  Google Scholar 

  • Dounskaia N, Ketcham CJ, Stelmach GE (2002b) Influence of biomechanical constraints on horizontal arm movements. Motor Control 6:366–387

    PubMed  Google Scholar 

  • Dounskaia N, Ketcham CJ, Leis BC, Stelmah GE (2005) Disruptions in joint control during drawing arm movements in Parkinson’s dicease. Exp Brain Res. On-line

  • Feldman AG (1986) Once more for the equilibrium point hypothesis (λ model). J Mot Behav 18:17–54

    PubMed  Google Scholar 

  • Flanagan JR, Wing AM (1997) The role of internal models in motion planning and control evidence from grip force adjustments during movements of hand-held loads. J Neurosci 17(4):1519–1528

    PubMed  Google Scholar 

  • Fukson OI, Berkinblit MB, Feldman AG (1980) The spinal frog takes into account the scheme of its body during the wiping reflex. Science 209:1261

    PubMed  Google Scholar 

  • Galloway JC, Koshland GF (2002) General coordination of shoulder, elbow and wrist dynamics during multijoint arm movements. Exp Brain Res 142:163–180

    Article  PubMed  Google Scholar 

  • Galloway JC, Bhat A, Heathcock JC, Manal K (2004) Shoulder and elbow joint power differ as a general feature of vertical arm movements. Exp Brain Res 157:391–396

    Article  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Ghez C, Krakauer JW, Sainburg RL, Ghilardi M-F (2000) Spatial representations and internal models of limb dynamics in motor learning. In: Gazzaniga MS (ed) The new cognitive neurosciences. MIT, Cambridge, MA, pp 501–514

    Google Scholar 

  • Gordon PC, Meyer DE (1987) Control of serial order in rapidly spoken syllable sequences. J Memory Lang 26:300–321

    Article  Google Scholar 

  • Gordon J, Ghilardi MF, Cooper SE, Ghez C (1994) Accuracy of planar reaching movements. II. Systematic extent errors resulting from inertial anisotropy. Exp Brain Res 99:112–130

    PubMed  Google Scholar 

  • Gottlieb GL (1998) Muscle activation patterns during two types of voluntary single-joint movements. J Neurophysiol 80:1860–1867

    PubMed  Google Scholar 

  • Graham KM, Moore KD, Cabel DW, Gribble PL, Cisek P, Scott SH (2003) Kinematics and kinetics of multijoint reaching in nonhuman primates. J Neurophysiol 89:2667–2677

    PubMed  Google Scholar 

  • Greene PH (1972) Problems of organization of motor systems. In: Rosen R, Snell FM (eds) Progress in theoretical biology, vol 2. Academic Press, New York

  • Gribble PL, Ostry DJ (1999) Compensation for interaction torques during single- and multijoint limb movement. J Neurophysiol 82:2310–2326

    PubMed  Google Scholar 

  • Grillner S, Zangger P (1974) Locomotor movements generated by the deafferented spinal cord. Acta Physiol Scand 91:38A–39A

    Google Scholar 

  • Hasan Z (1991) Biomechanics and study of multijoint movements. In: Humphrey DR, Freund HJ (eds) Motor control: concepts and issues, pp 75–84

  • Hatzitaki V, Hoshizaki TB (1998) Dynamic joint analysis as a method to document coordination disabilities associated with Parkinson’s disease. Clin Biomech 13:182–189

    Article  Google Scholar 

  • Hirashima M, Kudo K, Ohtsuki T (2003) Utilization and compensation torques during ball-throwing movements. J Neurophysiol 89:1784–1796

    PubMed  Google Scholar 

  • Hollerbach JM (1982) Computers, brains, and the control of movement. Trends Neurosci 6:189–192

    Article  Google Scholar 

  • Hollerbach JM, Flash T (1982) Dynamic interactions between limb segments during planar arm movement. Biol Cyber 44:67–77

    Article  Google Scholar 

  • Hoy MG, Zernicke RF (1985) Modulation of limb dynamics in the swing phase of locomotion. J Biomech 18:49–60

    Article  PubMed  Google Scholar 

  • Imamizu H, Uno Y, Kawato M (1995) Internal representations of the motor apparatus: implications from generalization in visuomotor learning. J Exp Psychol Hum Percept Perform 21:1174–1198

    Article  PubMed  Google Scholar 

  • Kaminski T, Gentile AM (1989) A kinematic comparison of single and multijoint movements. Exp Brain Res 78:547–556

    Article  PubMed  Google Scholar 

  • Kawato M (1999) Internal models for motor control and trajectory planning. Curr Opinions Neurobiol 9:718–727

    Article  Google Scholar 

  • Ketcham CJ, Dounskaia N, Stelmach GE (2004) Age-related differences in the control of multijoint movements. Motor Contr 8:422–436

    Google Scholar 

  • Konczak J, Dichgans J (1997) The development toward stereotypic arm kinematics during reaching in the first 3 years of life. Exp Brain Res 117:346–354

    Article  PubMed  Google Scholar 

  • Koshland GE, Hasan Z (1994) Selection of muscles for initiation of planar, three-joint arm movements with different final orientations of the hand. Exp Brain Res 98:157–162

    Article  PubMed  Google Scholar 

  • Koshland GF, Galloway JC, Nevoret-Bell CJ (2000) Control of the wrist in three-joint arm movements to multiple directions in the horizontal plane. J Neurophysiol 83:3188–3195

    PubMed  Google Scholar 

  • Krakauer JW, Ghilardi MF, Ghez C (1999) Independent learning of internal models for kinematic and dynamic control of reaching. Nat Neurosci 2:1026–1031

    Article  PubMed  Google Scholar 

  • Lackner JR, DiZio P (1994) Rapid adaptation to Coriolis force perturbations of arm trajectory. J Neurophysiol 72:299–313

    PubMed  Google Scholar 

  • Lashley KS (1951) The problem of serial order in behavior. In: Jeffress LA (ed) Cerebral mechanisms in behavior. Wiley, New York, pp 112–13

    Google Scholar 

  • Latash ML (1999) Mirror writing: learning, transfer, and implications for internal inverse models. J Mot Behav 31:107–111

    PubMed  Google Scholar 

  • Latash ML, Aruin AS, Shapiro MB (1995) The relation between posture and movement: study of a simple synergy in a two-joint task. Hum Mov Sci 14:79–107

    Article  Google Scholar 

  • Levin O, Ouamer M, Steyvers M, Swinnen SP (2001) Directional tuning effects during cyclical two-joint arm movements in the horizontal plane. Exp Brain Res 141:471–484

    Article  PubMed  Google Scholar 

  • MacKay DG (1987) The organization of perception and action: a theory for language and other cognitive skills. Springer-Verlag, New York

    Google Scholar 

  • Malfait N, Gribble PL, Ostry DJ (2005) Generalization of motor learning based on multiple field exposures and local adaptation. J Neurophysiol 93:3327–3338

    Article  PubMed  Google Scholar 

  • Malfait N, Shiller DM, Ostry DJ (2002) Transfer of motor learning across arm configurations. J Neurosci 22:9656–9660

    PubMed  Google Scholar 

  • Marr D (1982) Vision. A computational investigation into the human representation and processing of visual information. W.H. Freeman and Company, San Francisco

    Google Scholar 

  • Meulenbroek RGJ, Rosenbaum DA, Thomassen AJWM, Schomaker LRB (1993) Limb-segment selection in drawing behavior. Q J Exp Psychol 46A:273–299

    Google Scholar 

  • Morton SM, Lang CE, Bastian AJ (2001) Inter- and intra-limb generalization of adaptation during catching. Exp Brain Res 141:438–445

    Article  PubMed  Google Scholar 

  • Ostry DJ, Feldman AG (2003) A critical evaluation of the force control hypothesis in motor control. Exp Brain Res 153:275–288

    Article  PubMed  Google Scholar 

  • Pigeon P, Bortolami SB, DiZio P, Lackner JR (2003) Coordinated turn-and-reach movements. I. Anticipatory compensation for self-generated coriolis and interaction torques. J Neurophysiol 89:276–289

    PubMed  Google Scholar 

  • Poggio T, Bizzi E (2004) Generalization in vision and motor control. Nature 431:768–774

    Article  PubMed  Google Scholar 

  • Rosenbaum DA (1987) Hierarchical organization of motor programs. In: Wise S (ed) Neural and behavioral approaches to higher brain functions. Wiley, New York, pp 45–66

    Google Scholar 

  • Sainburg RL, Poizner H, Ghez C (1993) Loss of proprioception produces deficits in interjoint coordination. J Neurophysiol 70:2136–2147

    PubMed  Google Scholar 

  • Sainburg RL, Ghilardi MF, Poizner H, Ghez C (1995) Control of limb dynamics in normal subjects and patients without proprioception. J Neurophysiol 73:820–835

    PubMed  Google Scholar 

  • Sainburg RL, Ghez C, Kalakanis D (1999) Intersegmental dynamics are controlled by sequential anticipatory, error correction, and postural mechanisms. J Neurophysiol 81:1045–1056

    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 136:60–72

    Article  PubMed  Google Scholar 

  • Scheidt RA, Rymer WZ (2000) Control strategies for the transition from multijoint to single-joint arm movements studied using a simple mechanical constraint. J Neurophysiol 83:1–12

    PubMed  Google Scholar 

  • Schmidt RA (1975) A schema theory of discrete motor skill learning. Psychol Rev 82:225–260

    Google Scholar 

  • Schmidt RA, Lee TD (1999) Motor control and learning: a behavioral emphasis. Human Kinetics, Champaign, IL

    Google Scholar 

  • Schneider K, Zernicke RF, Ulrich BD, Jensen JL, Thelen E (1990) Understanding movement control in infants through the analysis of limb intersegmental dynamics. J Mot Behav 22:493–520

    PubMed  Google Scholar 

  • Seidler RD, Alberts JL, Stelmach GE (2001) Multijoint movement control in Parkinson’s disease. Exp Brain Res 140:335–344

    Article  PubMed  Google Scholar 

  • Seidler-Dobrin RD, Alberts JL, Stelmach GE (2002) Changes in multi-joint control patterns with age. Mot Contr 6:19–31

    Google Scholar 

  • Shadmehr R, Moussavi ZMK (2000) Spatial generalization from learning dynamics of reaching movements. J Neurosci 20:7807–7815

    PubMed  Google Scholar 

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

    PubMed  Google Scholar 

  • Sherrington CS (1906) Observations on the scratch-reflex in the spinal dog. J Physiol (Lond) 34:1–50

    Google Scholar 

  • Shimansky YP (2000) Spinal motor control system incorporates an internal model of limb dynamics. Biol Cybern 83:379–389

    Article  PubMed  Google Scholar 

  • Shimansky YP, Wang JJ, Bauer RA, Bracha V, Bloedel JR (2004) On-line compensation for perturbations of a reaching movement is cerebellar dependent: support for the task dependency hypothesis. Exp Brain Res 155:156–172

    Article  PubMed  Google Scholar 

  • Soechting JF, Lacquaniti F, Terzuolo CA (1986) Coordination of arm movements in three-dimensional space. Sensorimotor mapping during drawing movement. Neuroscience 17:295–311

    Article  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Ulrich BD, Jensen JL, Thelen E, Schneider K, Zernicke RF (1994) Adaptive dynamics of the leg movement patterns of human infants: II. Treadmill stepping in infants and adults. J Mot Behav 26:313–324

    PubMed  Google Scholar 

  • Van Galen GP (1991) Handwriting: issues for a psychomotor theory. Human Mov Sci 10:165–191

    Article  Google Scholar 

  • Virji-Babul N, Cooke JD (1995) Influence of joint interactional effects on the coordination of planar two-joint arm movements. Exp Brain Res 103:451–459

    Article  PubMed  Google Scholar 

  • Vorberg D, Hambuch R (1987) On the temporal control of rhythmic performance. In: Requin J (ed) Attention and performance, vol VII. Erlbaum, Hillsdale, NJ, pp 535–555

  • Wada Y, Kawato M (1993) A neural network model for arm trajectory formation using forward and inverse dynamics models. Neural Networks 6: 919–932

    Google Scholar 

  • Wang J, Sainburg RL (2004) Limitations in interlimb transfer of visuomotor rotations. Exp Brain Res 155:1–8

    Article  PubMed  Google Scholar 

  • Witney AG, Wolpert DM (2003) Spatial representation of predictive motor learning. J Neurophysiol 89:1837–1843

    PubMed  Google Scholar 

  • Wolpert DM, Ghahramani Z (2000) Computational principles of movement neuroscience. Nat Neurosci 3:1212–1217

    Article  PubMed  Google Scholar 

  • Wolpert DM, Kawato M (1998) Multiple paired forward and inverse models for motor control. Neural Networks 11:1317–1329

    Article  PubMed  Google Scholar 

  • Wolpert DM, Ghahramani Z, Jordan MI (1995) An internal model for sensorimotor integration. Science 269:1880–1882

    PubMed  Google Scholar 

  • Zernicke RF, Schneider K (1993) Biomechanics and developmental neuromotor control. Child Dev 64:982–1004

    PubMed  Google Scholar 

Download references

Acknowledgments

I thank Y. Shimansky and the two anonymous reviewers for helpful suggestions on the manuscript. The study was supported by NIH grant NS 43502.

Author information

Authors and Affiliations

  1. Department of Kinesiology, Arizona State University, P.O. Box 870404, Tempe, AZ, 85287-0404, USA

    Natalia Dounskaia

Authors
  1. Natalia Dounskaia
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Natalia Dounskaia.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Dounskaia, N. The internal model and the leading joint hypothesis: implications for control of multi-joint movements. Exp Brain Res 166, 1–16 (2005). https://doi.org/10.1007/s00221-005-2339-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00221-005-2339-1

Keywords

Search

Navigation