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Two modes of error processing in reaching

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Abstract

Several processes are devoted to error reduction for the production of purposeful actions. When motor responses deviate from their goal, online corrections can be performed either under voluntary control with additional sub-movements or under fast automatic control with smooth velocity profiles. When errors cannot be corrected online and are repeated over trials, subsequent responses can be improved iteratively through adaptation, a progressive adjustment of motor commands that acts to reduce the magnitude of error. It has been argued that reaching adaptation results essentially from a conflict between actual sensory feedback and expected sensory feedback. Here, we specifically compare two innovative hand-reaching paradigms that provide the subject with undistorted hand sensory feedback. Both paradigms induce motor planning errors unknown to the subjects. Experiment 1 yields a continuous retinal and visuomotor feedback which allows fast and complete automatic online corrections. In experiment 2, all visual feedback is eliminated during movement execution. This prevents online correction and provides information on hand-to-target visual error at movement end only. Despite a reiterated motor planning error and an automatic online correction of the whole error, experiment 1 shows a complete lack of adaptation. In contrast, experiment 2 which yields the same motor planning error exhibits a robust and generalized adaptation, although devoid of limb inter-sensory mismatch. These results demonstrate independence between the induced motor adaptation and automatic online correction, both characterized by the lack of any cognitive interference. Despite these quite different processes acting upon either motor planning or motor control, the general structure of the movement kinematics remains unaltered. A putative visuomotor cerebro-cerebellar network accounting for our results is proposed.

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References

  • Bahill AT, McDonald JD (1983) Frequency limitations and optimal step size for the two-point central difference derivative algorithm with applications to human eye movement data. IEEE Trans Biomed Eng 30:191–194

    Article  PubMed  CAS  Google Scholar 

  • Baizer JS, Kralj-Hans I, Glickstein M (1999) Cerebellar lesions and prism adaptation in Macaque monkeys. J Neurophysiol 81:1960–1965

    PubMed  CAS  Google Scholar 

  • Bard C, Turrell Y, Fleury M, Teasdale N, Lamarre Y, Martin O (1999) Deafferentation and pointing with visual double-step perturbations. Exp Brain Res 125:410–416

    Article  PubMed  CAS  Google Scholar 

  • Bedford FL (2007) Can a space-perception conflict be solved with three sense modalities? Perception 36:508–515

    Article  PubMed  Google Scholar 

  • Bekkering H, Abrams RA, Pratt J (1995) Transfer of saccadic adaptation to the manual system. Hum Mov Sci 14:155–164

    Article  Google Scholar 

  • Bridgeman B, Lewis S, Heit G, Nagle M (1979) Relation between cognitive and motor-oriented systems of visual position perception. J Exp Psychol Hum Percept 5:692–700

    Article  PubMed  CAS  Google Scholar 

  • Brodal P (1979) The pontocerebellar projection in the rhesus monkey: an experimental study with retrograde axonal transport of horseradish peroxidase. Neuroscience 4:193–208

    Article  PubMed  CAS  Google Scholar 

  • Chen H, Hua SE, Smith MA, Lenz FA, Shadmehr R (2005) Effects of human cerebellar thalamus disruption on adaptive control of reaching. Cereb Cortex 16:1462–1473

    Article  PubMed  Google Scholar 

  • Coello Y, Orliaguet JP, Prablanc C (1996) Pointing movement in an artificial perturbing inertial field: a prospective paradigm for motor control study. Neuropsychologia 34:879–892

    Article  PubMed  CAS  Google Scholar 

  • Day BL, Thompson PD, Harding AE, Marsden CD (1998) Influence of vision on upper limb reaching movements in patients with cerebellar ataxia. Brain 121:357–372

    Article  PubMed  Google Scholar 

  • De Graaf JB, Pelisson D, Prablanc C, Goffart L (1995) Modifications in end positions of arm movements following short-term saccadic adaptation. Neuroreport 6:1733–1736

    Article  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Desmurget M, Grea 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

    PubMed  CAS  Google Scholar 

  • Desmurget M, Gaveau V, Vindras P, Turner RS, Broussolle E, Thobois S (2004) On-line motor control in patients with Parkinson’s disease. Brain 127:1755–1773

    Article  PubMed  CAS  Google Scholar 

  • Diedrichsen J, Hashambhoy Y, Rane T, Shadmehr R (2005) Neural correlates of reach errors. J Neurosci 25:9919–9931

    Article  PubMed  CAS  Google Scholar 

  • Flash T, Henis E (1991) Arm trajectory modifications during reaching towards visual targets. J Cogn Neurosci 3:220–230

    Article  Google Scholar 

  • Fujita M, Amagai A, Minakawa F, Aoki M (2002) Selective and delay adaptation of human saccades. Brain Res Cogn Brain Res 13:41–52

    Article  PubMed  Google Scholar 

  • Georgopoulos AP, Kalaska JF, Massey JT (1981) Spatial trajectories and reaction times of aimed movements: effects of practice, uncertainty, and change in target location. J Neurophysiol 46:725–743

    PubMed  CAS  Google Scholar 

  • Gielen CC, Van den Heuvel PJ, van Gisbergen JA (1984) Coordination of fast eye and arm movements in a tracking task. Exp Brain Res 56:154–161

    Article  PubMed  CAS  Google Scholar 

  • Gilbert PF, Thach WT (1977) Purkinje cell activity during motor learning. Brain Res 128:309–328

    Article  PubMed  CAS  Google Scholar 

  • Goodale MA, Pelisson D, Prablanc C (1986) Large adjustments in visually guided reaching do not depend on vision of the hand or perception of target displacement. Nature 320:748–750

    Article  PubMed  CAS  Google Scholar 

  • Gréa H, Pisella L, Rossetti Y, Desmurget M, Tilikete C, Grafton S, Prablanc C, Vighetto A (2002) A lesion of the posterior parietal cortex disrupts on-line adjustments during aiming movements. Neuropsychologia 40:2471–2480

    Article  PubMed  Google Scholar 

  • Held R (1961) Exposure-history as a factor in maintaining stability of perception and coordination. J Nerv Ment Dis 132:26–32

    Article  PubMed  CAS  Google Scholar 

  • Held R, Freedman SJ (1963) Plasticity in human sensorimotor control. Science 142:455–462

    Article  PubMed  CAS  Google Scholar 

  • Hopp JJ, Fuchs AF (2004) The characteristics and neuronal substrate of saccadic eye movement plasticity. Prog Neurobiol 72:27–53

    Article  PubMed  Google Scholar 

  • Horak FB, Diener HC (1994) Cerebellar control of postural scaling and central set in stance. J Neurophysiol 72:479–493

    PubMed  CAS  Google Scholar 

  • Ito M (2001) Cerebellar long-term depression: characterization, signal transduction, and functional roles. Physiol Rev 81:1143–1195

    PubMed  CAS  Google Scholar 

  • Jakobson LS, Goodale MA (1989) Trajectories of reaches to prismatically displaced targets: evidence for “automatic” visuomotor recalibration. Exp Brain Res 78:575–587

    Article  PubMed  CAS  Google Scholar 

  • Kitazawa S, Kohno T, Uka T (1995) Effects of delayed visual information on the rate and amount of prism adaptation in the human. J Neurosci 15:7644–7652

    PubMed  CAS  Google Scholar 

  • Kitazawa S, Kimura T, Yin PB (1998) Cerebellar complex spikes encode both destinations and errors in arm movements. Nature 392:494–497

    Article  PubMed  CAS  Google Scholar 

  • Kornheiser AS (1976) Adaptation to laterally displaced vision: a review. Psychol Bull 83:783–816

    Article  PubMed  CAS  Google Scholar 

  • Krakauer JW, Pine ZM, Ghilardi MF, Ghez C (2000) Learning of visuomotor transformations for vectorial planning of reaching trajectories. J Neurosci 20:8916–8924

    PubMed  CAS  Google Scholar 

  • Kroller J, De Graaf JB, Prablanc C, Pelisson D (1999) Effects of short-term adaptation of saccadic gaze amplitude on hand-pointing movements. Exp Brain Res 124:351–362

    Article  PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • MacAskill MR, Anderson TJ, Jones RD (2000) Suppression of displacement in severely slowed saccades. Vision Res 40:3405–3413

    Article  PubMed  CAS  Google Scholar 

  • Magescas F, Prablanc C (2006) Automatic drive of limb motor plasticity. J Cogn Neurosci 18:75–83

    Article  PubMed  CAS  Google Scholar 

  • Malfait N, Ostry DJ (2004) Is interlimb transfer of force-field adaptation a cognitive response to the sudden introduction of load? J Neurosci 24:8084–8089

    Article  PubMed  CAS  Google Scholar 

  • Martin TA, Keating JG, Goodkin HP, Bastian AJ, Thach WT (1996) Throwing while looking through prisms. I. Focal olivocerebellar lesions impair adaptation. Brain 119:1183–1198

    Article  PubMed  Google Scholar 

  • Michel C, Pisella L, Prablanc C, Rode G, Rossetti Y (2007) Enhancing visuomotor adaptation by reducing error signals: single-step (aware) versus multiple-step (unaware) exposure to wedge prisms. J Cogn Neurosci 19:341–350

    Article  PubMed  Google Scholar 

  • Morton SM, Bastian AJ (2004) Prism adaptation during walking generalizes to reaching and requires the cerebellum. J Neurophysiol 92:2497–2509

    Article  PubMed  Google Scholar 

  • Morton SM, Bastian AJ (2006) Cerebellar contributions to locomotor adaptations during splitbelt treadmill walking. J Neurosci 26:9107–9116

    Article  PubMed  CAS  Google Scholar 

  • Mussa-Ivaldi FA, Hogan N, Bizzi E (1985) Neural, mechanical, and geometric factors subserving arm posture in humans. J Neurosci 5:2732–2743

    PubMed  CAS  Google Scholar 

  • Optican LM (1985) Adaptive properties of the saccadic system. Rev Oculomot Res 1:71–79

    PubMed  CAS  Google Scholar 

  • Pélisson D, Prablanc C, Goodale MA, Jeannerod M (1986) Visual control of reaching movements without vision of the limb. II. Evidence of fast unconscious processes correcting the trajectory of the hand to the final position of a double-step stimulus. Exp Brain Res 62:303–311

    Article  PubMed  Google Scholar 

  • Pisella L, Grea H, Tilikete C, Vighetto A, Desmurget M, Rode G, Boisson D, Rossetti Y (2000) An ‘automatic pilot’ for the hand in human posterior parietal cortex: toward reinterpreting optic ataxia. Nat Neurosci 3:729–736

    Article  PubMed  CAS  Google Scholar 

  • Prablanc C, Martin O (1992) Automatic control during hand reaching at undetected two-dimensional target displacements. J Neurophysiol 67:455–469

    PubMed  CAS  Google Scholar 

  • Prablanc C, Echallier JE, Jeannerod M, Komilis E (1979) Optimal response of eye and hand motor systems in pointing at a visual target. II. Static and dynamic visual cues in the control of hand movement. Biol Cybern 35:183–187

    Article  PubMed  CAS  Google Scholar 

  • Prablanc C, Desmurget M, Grea H (2003) Neural control of on-line guidance of hand reaching movements. Prog Brain Res 142:155–170

    Article  PubMed  Google Scholar 

  • Redding GM, Wallace B (1992) Adaptative eye–hand coordination: implication of prism adaptation for perceptual-motor organization. In: Proteau L, Elliott D (eds) Vision and motor control. Elsevier Science Publishers, Amsterdam, pp 105–127

  • Sarlegna F, Blouin J, Vercher JL, Bresciani JP, Bourdin C, Gauthier GM (2004) Online control of the direction of rapid reaching movements. Exp Brain Res 157:468–471

    Article  PubMed  Google Scholar 

  • Saunders JA, Knill DC (2003) Humans use continuous visual feedback from the hand to control fast reaching movements. Exp Brain Res 152:341–352

    Article  PubMed  Google Scholar 

  • Schweighofer N, Spoelstra J, Arbib MA, Kawato M (1998) Role of the cerebellum in reaching movements in humans. II. A neural model of the intermediate cerebellum. Eur J Neurosci 10:95–105

    Article  PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Smith MA, Shadmehr R (2005) Intact ability to learn internal models of arm dynamics in Huntington’s disease but not cerebellar degeneration. J Neurophysiol 93:2809–2821

    Article  PubMed  Google Scholar 

  • Smith MA, Brandt J, Shadmehr R (2000) Motor disorder in Huntington’s disease begins a dysfunction in error feedback control. Nature 403:544–549

    Article  PubMed  CAS  Google Scholar 

  • Soechting JF, Lacquaniti F (1983) Modification of trajectory of a pointing movement in response to a change in target location. J Neurophysiol 49:548–564

    PubMed  CAS  Google Scholar 

  • Tseng Yw, Diedrichsen J, Krakauer JW, Shadmehr R, Bastian AJ (2007) Sensory prediction errors drive cerebellum-dependent adaptation of reaching. J Neurophysiol 98:54–62

    Article  PubMed  Google Scholar 

  • Van Kan PL, Gibson AR, Houk JC (1993a) Movement-related inputs to intermediate cerebellum of the monkey. J Neurophysiol 69:74–94

    PubMed  Google Scholar 

  • Van Kan PL, Houk JC, Gibson AR (1993b) Output organization of intermediate cerebellum of the monkey. J Neurophysiol 69:57–73

    PubMed  Google Scholar 

  • Vetter P, Goodbody SJ, Wolpert DM (1999) Evidence for an eye-centered spherical representation of the visuomotor map. J Neurophysiol 81:935–939

    PubMed  CAS  Google Scholar 

  • Von Holst E, Mittelstaed H (1950) Das reafferenzprinzip. Wechelwirkung Zwischen Zentralnerven system und peripherie. Naturwis 37:464–476

    Article  Google Scholar 

  • Weiner MJ, Hallett M, Funkenstein HH (1983) Adaptation to lateral displacement of vision in patients with lesions of the central nervous system. Neurology 33:766–772

    PubMed  CAS  Google Scholar 

  • Wolpert DM, Miall RC (1996) Forward models for physiological motor control. Neural Netw 9:1265–1279

    Article  PubMed  Google Scholar 

  • Wolpert DM, Miall RC, Kawato M (1998) Internal models in the cerebellum. Trends Cogn Sci 2:338–347

    Article  Google Scholar 

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Acknowledgments

This work was supported by INSERM and Région Rhône Alpes. It was carried out on the “Plateforme Mouvement et Handicap, Hospices Civils de Lyon/Institut Fédératif des Neurosciences de Lyon”. We thank Jean-Louis Borach for the illustrations and David Ostry for his final read-through.

Conflict of interest statement

The authors declare that they have no competing financial interests.

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Authors and Affiliations

  1. Espace et Action, INSERM, U864, 16 Avenue Lépine, 69500, Bron, France

    Frederic Magescas, Christian Urquizar & Claude Prablanc

  2. Université de Lyon, 69003, Lyon, France

    Frederic Magescas, Christian Urquizar & Claude Prablanc

  3. Biologie Humaine, Université Lyon 1, 69003, Lyon, France

    Frederic Magescas, Christian Urquizar & Claude Prablanc

  4. Hospices Civils de Lyon, Mouvement et Handicap, Hôpital Neurologique, 69003, Lyon, France

    Frederic Magescas, Christian Urquizar & Claude Prablanc

  5. Institut Fédératif des Neurosciences de Lyon, IFR19, 69003, Lyon, France

    Frederic Magescas, Christian Urquizar & Claude Prablanc

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  1. Frederic Magescas
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  2. Christian Urquizar
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  3. Claude Prablanc
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Correspondence to Claude Prablanc.

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Magescas, F., Urquizar, C. & Prablanc, C. Two modes of error processing in reaching. Exp Brain Res 193, 337–350 (2009). https://doi.org/10.1007/s00221-008-1629-9

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  • DOI: https://doi.org/10.1007/s00221-008-1629-9

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