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Differential influence of vision and proprioception on control of movement distance

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Abstract

The purpose of this study was to investigate the contribution of proprioceptive and visual information about initial limb position in controlling the distance of rapid, single-joint reaching movements. Using a virtual reality environment, we systematically changed the relationship between actual and visually displayed hand position as subjects’ positioned a cursor within a start circle. No visual feedback was given during the movement. Subjects reached two visual targets (115 and 125° elbow angle) from four start locations (90, 95, 100, and 105° elbow angle) under four mismatch conditions (0, 5, 10, or 15°). A 2×4×4 ANOVA enabled us to ask whether the subjects controlled the movement distance in accord with the virtual, or the actual hand location. Our results indicate that the movement distance was mainly controlled according to the virtual start location. Whereas distance modification was most extensive for the closer target, analysis of acceleration profiles revealed that, regardless of target position, visual information about start location determined the initial peak in tangential hand acceleration. Peak acceleration scaled with peak velocity and movement distance, a phenomenon termed “pulse-height” control. In contrast, proprioceptive information about actual hand location determined the duration of acceleration, which also scaled with peak velocity and movement distance, a phenomenon termed “pulse-width” control. Because pulse-height and pulse-width mechanisms reflect movement planning and sensory-based corrective processes, respectively, our current findings indicate that vision is used primarily for planning movement distance, while proprioception is used primarily for online corrections during rapid, unseen movements toward visual targets.

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References

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

    PubMed  CAS  Google Scholar 

  • Bagesteiro LB, Sainburg RL (2003) Nondominant arm advantages in load compensation during rapid elbow joint movements. J Neurophysiol 90:1503–1513

    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 

  • Bennett DJ, Gorassini M, Prochazka A (1994) Catching a ball: contributions of intrinsic muscle stiffness, reflexes, and higher order responses. Can J Physiol Pharmacol 72:525–534

    PubMed  CAS  Google Scholar 

  • Bizzi E, Dev P, Morasso P, Polit A (1978) Effect of load disturbances during centrally initiated movements. J Neurophysiol 41:542–556

    PubMed  CAS  Google Scholar 

  • Bock O (1993) Early stages of load compensation in human aimed arm movements. Behav Brain Res 55:61–68

    Article  PubMed  CAS  Google Scholar 

  • Brown SH, Cooke JD (1981) Responses to force perturbations preceding voluntary human arm movements. Brain Res 220:350–355

    Article  PubMed  CAS  Google Scholar 

  • Brown SH, Cooke JD (1984) Initial agonist burst duration depends on movement amplitude. Exp Brain Res 55:523–527

    Article  PubMed  CAS  Google Scholar 

  • Brown SH, Cooke JD (1986) Initial agonist burst is modified by perturbations preceding movement. Brain Res 377:311–322

    Article  PubMed  CAS  Google Scholar 

  • Brown LE, Rosenbaum DA, Sainburg RL (2003a) Limb position drift: implications for control of posture and movement. J Neurophysiol 90:3105–3118

    Article  PubMed  Google Scholar 

  • Brown LE, Rosenbaum DA, Sainburg RL (2003b) Movement speed effects on limb position drift. Exp Brain Res 153:266–274

    Article  PubMed  Google Scholar 

  • Day BL, Rothwell JC, Marsden CD (1983) Interaction between the long-latency stretch reflex and voluntary electromyographic activity prior to a rapid voluntary motor reaction. Brain Res 270:55–62

    Article  PubMed  CAS  Google Scholar 

  • Desmedt JE, Godaux E (1979) Voluntary motor commands in human ballistic movements. Ann Neurol 5:415–421

    Article  PubMed  CAS  Google Scholar 

  • DiZio P, Lathan CE, Lackner JR (1993) The role of brachial muscle spindle signals in assignment of visual direction. J Neurophysiol 70:1578–1584

    PubMed  CAS  Google Scholar 

  • Georgopoulos AP (1994) Population activity in the control of movement. Int Rev Neurobiol 37:103–119; discussion 121–123

    Google Scholar 

  • Georgopoulos AP (1995) Current issues in directional motor control. Trends Neurosci 18:506–510

    Article  PubMed  CAS  Google Scholar 

  • Georgopoulos AP (1996) Arm movements in monkeys: behavior and neurophysiology. J Comp Physiol [A] 179:603–612

    Article  CAS  Google Scholar 

  • Georgopoulos AP (2000) Neural aspects of cognitive motor control. Curr Opin Neurobiol 10:238–241

    Article  PubMed  CAS  Google Scholar 

  • Ghez C (1979) Contributions of central programs to rapid limb movement in the cat. In: Asanuma H, Wilson VJ (eds) Integration in the nervous system. Igaku-Shoin, Tokyo, pp 305–319

    Google Scholar 

  • Ghez C, Gordon J (1987) Trajectory control in targeted force impulses. I. Role of opposing muscles. Exp Brain Res 67:225–240

    Article  PubMed  CAS  Google Scholar 

  • Ghez C, Vicario D (1978) The control of rapid limb movement in the cat. II. Scaling of isometric force adjustments. Exp Brain Res 33:191–202

    PubMed  CAS  Google Scholar 

  • Ghez C, Hening W, Gordon J (1991) Organization of voluntary movement. Curr Opin Neurobiol 1:664–671

    Article  PubMed  CAS  Google Scholar 

  • Ghez C, Favilla M, Ghilardi MF, Gordon J, Bermejo R, Pullman S (1997) Discrete and continuous planning of hand movements and isometric force trajectories. Exp Brain Res 115:217–233

    Article  PubMed  CAS  Google Scholar 

  • Gordon J, Ghez C (1984) EMG patterns in antagonist muscles during isometric contraction in man: relations to response dynamics. Exp Brain Res 55:167–171

    Article  PubMed  CAS  Google Scholar 

  • Gordon J, Ghez C (1987) Trajectory control in targeted force impulses. III. Compensatory adjustments for initial errors. Exp Brain Res 67:253–269

    Article  PubMed  CAS  Google Scholar 

  • Gordon J, Ghez C (1987a) Trajectory control in targeted force impulses. II. Pulse height control. Exp Brain Res 67:241–252

    PubMed  CAS  Google Scholar 

  • Gordon J, Ghez C (1987b) Trajectory control in targeted force impulses. III. Compensatory adjustments for initial errors. Exp Brain Res 67:253–269

    PubMed  CAS  Google Scholar 

  • Gordon J, Ghilardi MF, Ghez C (1994) Accuracy of planar reaching movements. I. Independence of direction and extent variability. Exp Brain Res 99:97–111

    PubMed  CAS  Google Scholar 

  • Graziano MS (1999) Where is my arm? The relative role of vision and proprioception in the neuronal representation of limb position. Proc Natl Acad Sci USA 96:10418–10421

    Article  PubMed  CAS  Google Scholar 

  • Kakei S, Hoffman DS, Strick PL (1999) Muscle and movement representations in the primary motor cortex. Science 285:2136–2139

    Article  PubMed  CAS  Google Scholar 

  • Kalaska JF (1988) The representation of arm movements in postcentral and parietal cortex. Can J Physiol Pharmacol 66:455–463

    PubMed  CAS  Google Scholar 

  • Kalaska JF, Caminiti R, Georgopoulos AP (1983) Cortical mechanisms related to the direction of two-dimensional arm movements: relations in parietal area 5 and comparison with motor cortex. Exp Brain Res 51:247–260

    Article  PubMed  CAS  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  CAS  Google Scholar 

  • Lackner JR, Levine MS (1979) Changes in apparent body orientation and sensory localization induced by vibration of postural muscles: vibratory myesthetic illusions. Aviat Space Environ Med 50:346–354

    PubMed  CAS  Google Scholar 

  • Lateiner JE, Sainburg RL (2003) Differential contributions of vision and proprioception to movement accuracy. Exp Brain Res 151:446–454

    Article  PubMed  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Pick HL Jr, Hay JC, Martin R (1969) Adaptation to split-field wedge prism spectacles. J Exp Psychol 80:125–132

    Article  PubMed  Google Scholar 

  • Rosenbaum DA (1980) Human movement initiation: specification of arm, direction, and extent. J Exp Psychol Gen 109:444–474

    Article  PubMed  CAS  Google Scholar 

  • Rossetti Y, Desmurget M, Prablanc C (1995) Vectorial coding of movement: vision, proprioception, or both? J Neurophysiol 74:457–463

    PubMed  CAS  Google Scholar 

  • Sainburg RL (2002) Evidence for a dynamic-dominance hypothesis of handedness. Exp Brain Res 142:241–258

    Article  PubMed  Google Scholar 

  • Sainburg RL, Schaefer SY (2004) Interlimb differences in control of movement extent. J Neurophysiol 92:1374–1383

    Article  PubMed  Google Scholar 

  • Sainburg RL, Wang J (2002) Interlimb transfer of visuomotor rotations: independence of direction and final position information. Exp Brain Res 145:437–447

    Article  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  CAS  Google Scholar 

  • Sainburg RL, Lateiner JE, Latash ML, Bagesteiro LB (2003) Effects of altering initial position on movement direction and extent. J Neurophysiol 89:401–415

    Article  PubMed  Google Scholar 

  • Sarlegna F, Blouin J, Bresciani J-P, Bourdin C, Vercher J-L, Gauthier GM (2003) Target and hand position information in the online control of goal-directed arm movements. Exp Brain Res 151:524–535

    Article  PubMed  Google Scholar 

  • Shapiro MB, Gottlieb GL, Moore CG, Corcos DM (2002) Electromyographic responses to an unexpected load in fast voluntary movements: descending regulation of segmental reflexes. J Neurophysiol 88:1059–1063

    PubMed  Google Scholar 

  • Sober SJ, Sabes PN (2003) Multisensory integration during motor planning. J Neurosci 23:6982–6992

    PubMed  CAS  Google Scholar 

  • Van Beers RJ, Sittig AC, Denier van der Gon JJ (1996) How humans combine simultaneous proprioceptive and visual position information. Exp Brain Res 111:253–261

    Article  PubMed  Google Scholar 

  • Van Beers RJ, Sittig AC, Denier van der Gon JJ (1998) The precision of proprioceptive position sense. Exp Brain Res 122:367–377

    Article  PubMed  Google Scholar 

  • Van Beers RJ, Sittig AC, Denier van der Gon JJ. (1999) Integration of proprioceptive and visual position-information: an experimentally supported model. J Neurophysiol 81:1355–1364

    PubMed  Google Scholar 

  • Warren DH, Cleaves WT (1971) Visual-proprioceptive interaction under large amounts of conflict. J Exp Psychol 90:206–214

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

This research was supported by National Institute of Child Health and Human Development Grant R01HD-39311.

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Authors and Affiliations

  1. Department of Kinesiology, The Pennsylvania State University, 29 Recreation Bldg, University Park, PA, 16802, USA

    Leia B. Bagesteiro, Fabrice R. Sarlegna & Robert L. Sainburg

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  1. Leia B. Bagesteiro
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  2. Fabrice R. Sarlegna
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  3. Robert L. Sainburg
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Correspondence to Robert L. Sainburg.

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Bagesteiro, L.B., Sarlegna, F.R. & Sainburg, R.L. Differential influence of vision and proprioception on control of movement distance. Exp Brain Res 171, 358–370 (2006). https://doi.org/10.1007/s00221-005-0272-y

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  • DOI: https://doi.org/10.1007/s00221-005-0272-y

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