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Learning a visuomotor rotation: simultaneous visual and proprioceptive information is crucial for visuomotor remapping

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Abstract

Visuomotor adaptation is mediated by errors between intended and sensory-detected arm positions. However, it is not clear whether visual-based errors that are shown during the course of motion lead to qualitatively different or more efficient adaptation than errors shown after movement. For instance, continuous visual feedback mediates online error corrections, which may facilitate or inhibit the adaptation process. We addressed this question by manipulating the timing of visual error information and task instructions during a visuomotor adaptation task. Subjects were exposed to a visuomotor rotation, during which they received continuous visual feedback (CF) of hand position with instructions to correct or not correct online errors, or knowledge-of-results (KR), provided as a static hand-path at the end of each trial. Our results showed that all groups improved performance with practice, and that online error corrections were inconsequential to the adaptation process. However, in contrast to the CF groups, the KR group showed relatively small reductions in mean error with practice, increased inter-trial variability during rotation exposure, and more limited generalization across target distances and workspace. Further, although the KR group showed improved performance with practice, after-effects were minimal when the rotation was removed. These findings suggest that simultaneous visual and proprioceptive information is critical in altering neural representations of visuomotor maps, although delayed error information may elicit compensatory strategies to offset perturbations.

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References

  • Bagesteiro LB, Sainburg RL (2002) Handedness: dominant arm advantages in control of limb dynamics. J Neurophysiol 88:2408–2421

    Article  PubMed  Google Scholar 

  • Bagesteiro LB, Sarlegna FR, Sainburg RL (2006) Differential influence of vision and proprioception on control of movement distance. Exp Brain Res 171:358–370

    Article  PubMed  Google Scholar 

  • Baraduc P, Wolpert DM (2002) Adaptation to a visuomotor shift depends on the starting posture. J Neurophysiol 88:973–981

    PubMed  Google Scholar 

  • Bedford FL (1989) Constraints on learning new mappings between perceptual dimensions. J Exp Psychol Hum Percept Perform 15:232–248

    Article  Google Scholar 

  • Bedford FL (1993) Perceptual and cognitive spatial learning. J Exp Psychol Hum Percept Perform 19:517–530

    Article  CAS  PubMed  Google Scholar 

  • Bock O (2005) Components of sensorimotor adaptation in young and elderly subjects. Exp Brain Res 160:259–263

    Article  PubMed  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 

  • Caithness G, Osu R, Bays P, Chase H, Klassen J, Kawato M, Wolpert DM, Flanagan JR (2004) Failure to consolidate the consolidation theory of learning for sensorimotor adaptation tasks. J Neurosci 24:8662–8671

    Article  CAS  PubMed  Google Scholar 

  • Choe CS, Welch RB (1974) Variables affecting the intermanual transfer and decay of prism adaptation. J Exp Psychol 102:1076–1084

    Article  CAS  PubMed  Google Scholar 

  • Cohen RG, Sternad D (2008) Variability in motor learning: relocating, channeling and reducing noise. Exp Brain Res 193:69–83

    Article  PubMed  Google Scholar 

  • Cunningham HA, Welch RB (1994) Multiple concurrent visual-motor mappings: implications for models of adaptation. J Exp Psychol Hum Percept Perform 20:987–999

    Article  CAS  PubMed  Google Scholar 

  • Desmurget M, Pelisson D, Rossetti Y, Prablanc C (1998) From eye to hand: planning goal-directed movements. Neurosci Biobehav Rev 22:761–788

    Article  CAS  PubMed  Google Scholar 

  • Deutsch KM, Newell KM (2004) Changes in the structure of children’s isometric force variability with practice. J Exp Child Psychol 88:319–333

    Article  PubMed  Google Scholar 

  • Ghahramani Z, Wolpert DM, Jordan MI (1996) Generalization to local remappings of the visuomotor coordinate transformation. J Neurosci 16:7085–7096

    CAS  PubMed  Google Scholar 

  • Ghilardi MF, Gordon J, Ghez C (1995) Learning a visuomotor transformation in a local area of work space produces directional biases in other areas. J Neurophysiol 73:2535–2539

    CAS  PubMed  Google Scholar 

  • Ghilardi M, Ghez C, Dhawan V, Moeller J, Mentis M, Nakamura T, Antonini A, Eidelberg D (2000) Patterns of regional brain activation associated with different forms of motor learning. Brain Res 871:127–145

    Article  CAS  PubMed  Google Scholar 

  • Heuer H, Hegele M (2008) Adaptation to visuomotor rotations in younger and older adults. Psychol Aging 23:190–202

    Article  PubMed  Google Scholar 

  • Hinder MR, Tresilian JR, Riek S, Carson RG (2008) The contribution of visual feedback to visuomotor adaptation: how much and when? Brain Res 1197:123–134

    Article  CAS  PubMed  Google Scholar 

  • Hinder MR, Riek S, Tresilian JR, de Rugy A, Carson RG (2010) Real-time error detection but not error correction drives automatic visuomotor adaptation. Exp Brain Res 201:197–207

    Google Scholar 

  • Kagerer FA, Contreras-Vidal JL, Stelmach GE (1997) Adaptation to gradual as compared with sudden visuo-motor distortions. Exp Brain Res 115:557–561

    Article  CAS  PubMed  Google Scholar 

  • Klassen J, Tong C, Flanagan JR (2005) Learning and recall of incremental kinematic and dynamic sensorimotor transformations. Exp Brain Res 164:250–259

    Article  PubMed  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

    CAS  PubMed  Google Scholar 

  • Krakauer JW, Ghez C, Ghilardi MF (2005) Adaptation to visuomotor transformations: consolidation, interference, and forgetting. J Neurosci 25:473–478

    Article  CAS  PubMed  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 

  • Mazzoni P, Krakauer JW (2006) An implicit plan overrides an explicit strategy during visuomotor adaptation. J Neurosci 26:3642–3645

    Article  CAS  PubMed  Google Scholar 

  • Miall RC, Jenkinson N, Kulkarni K (2004) Adaptation to rotated visual feedback: a re-examination of motor interference. Exp Brain Res 154:201–210

    Article  PubMed  Google Scholar 

  • Mosier KM, Scheidt RA, Acosta S, Mussa-Ivaldi FA (2005) Remapping hand movements in a novel geometrical environment. J Neurophysiol 94:4362–4372

    Article  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Pine ZM, Krakauer JW, Gordon J, Ghez C (1996) Learning of scaling factors and reference axes for reaching movements. Neuroreport 7:2357–2361

    Article  CAS  PubMed  Google Scholar 

  • Prager AD, Contreras-Vidal JL (2003) Adaptation to display rotation and display gain distortions during drawing. Hum Mov Sci 22:173–187

    Article  PubMed  Google Scholar 

  • Redding GM, Wallace B (1996) Adaptive spatial alignment and strategic perceptual-motor control. J Exp Psychol Hum Percept Perform 22:379–394

    Article  CAS  PubMed  Google Scholar 

  • Redding GM, Wallace B (2002) Strategic calibration and spatial alignment: a model from prism adaptation. J Mot Behav 34:126–138

    Article  PubMed  Google Scholar 

  • Roby-Brami A, Burnod Y (1995) Learning a new visuomotor transformation: error correction and generalization. Brain Res Cogn Brain Res 2:229–242

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

    CAS  PubMed  Google Scholar 

  • Sarlegna FR, Sainburg RL (2007) The effect of target modality on visual and proprioceptive contributions to the control of movement distance. Exp Brain Res 176:267–280

    Article  PubMed  Google Scholar 

  • Saunders JA, Knill DC (2004) Visual feedback control of hand movements. J Neurosci 24:3223–3234

    Article  CAS  PubMed  Google Scholar 

  • Schaefer SY, Haaland KY, Sainburg RL (2009) Dissociation of initial trajectory and final position errors during visuomotor adaptation following unilateral stroke. Brain Res 1298:78–91

    Article  CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Sober SJ, Sabes PN (2005) Flexible strategies for sensory integration during motor planning. Nat Neurosci 8:490–497

    CAS  PubMed  Google Scholar 

  • Soechting JF, Flanders M (1989) Sensorimotor representations for pointing to targets in three-dimensional space. J Neurophysiol 62:582–594

    CAS  PubMed  Google Scholar 

  • Tillery SI, Flanders M, Soechting JF (1991) A coordinate system for the synthesis of visual and kinesthetic information. J Neurosci 11:770–778

    CAS  PubMed  Google Scholar 

  • Tong C, Flanagan JR (2003) Task-specific internal models for kinematic transformations. J Neurophysiol 90:578–585

    Article  PubMed  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 

  • Vindras P, Viviani P (1998) Frames of reference and control parameters in visuomanual pointing. J Exp Psychol Hum Percept Perform 24:569–591

    Article  CAS  PubMed  Google Scholar 

  • Vindras P, Viviani P (2002) Altering the visuomotor gain. Evidence that motor plans deal with vector quantities. Exp Brain Res 147:280–295

    Article  PubMed  Google Scholar 

  • Wang J, Sainburg RL (2005) Adaptation to visuomotor rotations remaps movement vectors, not final positions. J Neurosci 25:4024–4030

    Article  CAS  PubMed  Google Scholar 

  • Wang J, Sainburg RL (2006) Interlimb transfer of visuomotor rotations depends on handedness. Exp Brain Res 175:223–230

    Article  PubMed  Google Scholar 

  • Wang X, Merzenich MM, Sameshima K, Jenkins WM (1995) Remodelling of hand representation in adult cortex determined by timing of tactile stimulation. Nature 378:71–75

    Article  CAS  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Zarahn E, Weston GD, Liang J, Mazzoni P, Krakauer JW (2008) Explaining savings for visuomotor adaptation: linear time-invariant state-space models are not sufficient. J Neurophysiol 100:2537–2548

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

We thank Marisa Alcaro for participant recruitment and scholarly discussions regarding this manuscript. This research was supported by the National Institutes of Health, National Institute of Child Health and Human Development Grant #R01HD39311.

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Authors and Affiliations

  1. The Huck Institutes of the Life Sciences, The Pennsylvania State University, University Park, PA, USA

    Britne A. Shabbott & Robert L. Sainburg

  2. The Department of Kinesiology, The Pennsylvania State University, 266 Recreation Building, University Park, PA, 16802, USA

    Robert L. Sainburg

  3. The Department of Neurology, Penn State Hershey Medical Center, Hershey, PA, USA

    Robert L. Sainburg

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  1. Britne A. Shabbott
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  2. Robert L. Sainburg
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Correspondence to Robert L. Sainburg.

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Shabbott, B.A., Sainburg, R.L. Learning a visuomotor rotation: simultaneous visual and proprioceptive information is crucial for visuomotor remapping. Exp Brain Res 203, 75–87 (2010). https://doi.org/10.1007/s00221-010-2209-3

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  • DOI: https://doi.org/10.1007/s00221-010-2209-3

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