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Proprioceptive recalibration arises slowly compared to reach adaptation

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Abstract

When subjects reach in a novel visuomotor environment (e.g. while viewing a cursor representing their hand that is rotated from their hand’s actual position), they typically adjust their movements (i.e. bring the cursor to the target), thus reducing reaching errors. Additionally, research has shown that reaching with altered visual feedback of the hand results in sensory changes, such that proprioceptive estimates of hand position are shifted in the direction of the visual feedback experienced (Cressman and Henriques in J Neurophysiol 102:3505–3518, 2009). This study looked to establish the time course of these sensory changes. Additionally, the time courses of implicit sensory and motor changes were compared. Subjects reached to a single visual target while seeing a cursor that was either aligned with their hand position (50 trials) or rotated 30° clockwise relative to their hand (150 trials). Reach errors and proprioceptive estimates of felt hand position were assessed following the aligned reach training trials and at seven different times during the rotated reach training trials by having subjects reach to the target without visual feedback, and provide estimates of their hand relative to a visual reference marker, respectively. Results revealed a shift in proprioceptive estimates throughout the rotated reach training trials; however, significant sensory changes were not observed until after 70 trials. In contrast, results showed a greater change in reaches after a limited number of reach training trials with the rotated cursor. These findings suggest that proprioceptive recalibration arises more slowly than reach adaptation.

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References

  • Allen TJ, Proske U (2006) Effect of muscle fatigue on the sense of limb position and movement. Exp Brain Res 170:30–38

    Article  CAS  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 

  • Benson BL, Anguera JA, Seidler RD (2011) A spatial explicit strategy reduces error but interferes with sensorimotor adaptation. J Neurophysiol 105:2843–2851

    Article  PubMed  PubMed Central  Google Scholar 

  • Berniker M, Kording K (2008) Estimating the sources of motor errors for adaptation and generalization. Nat Neurosci 11:1454–1461

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Buch ER, Young S, Contreras-Vidal JL (2003) Visuomotor adaptation in normal aging. Learn Mem 10:55–63

    Article  PubMed  PubMed Central  Google Scholar 

  • Cameron BD, Franks IM, Inglis T, Chua R (2012) The adaptability of self-action perception and movement control when the limb is passively versus actively moved. Conscious Cogn 21:4–17

    Article  PubMed  Google Scholar 

  • Clayton HA, Cressman EK, Henriques DY (2014) The effect of visuomotor adaptation on proprioceptive localization: the contributions of perceptual and motor changes. Exp Brain Res 232:2073–2086

    Article  PubMed  Google Scholar 

  • Cressman EK, Henriques DY (2009) Sensory recalibration of hand position following visuomotor adaptation. J Neurophysiol 102:3505–3518

    Article  PubMed  Google Scholar 

  • Cressman EK, Henriques DY (2010) Reach adaptation and proprioceptive recalibration following exposure to misaligned sensory input. J Neurophysiol 103:1888–1895

    Article  PubMed  Google Scholar 

  • Cressman EK, Salomonczyk D, Henriques DY (2010) Visuomotor adaptation and proprioceptive recalibration in older adults. Exp Brain Res 205:533–544

    Article  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 

  • Diedrichsen J, White O, Newman D, Lally N (2010) Use-dependent and error-based learning of motor behaviors. J Neurosci 30:5406–5409

    Article  Google Scholar 

  • Flanders M, Tillery SI, Soechting JF (1992) Early stages in a sensorimotor transformation. Behav Brain Sci 15:209–320

    Article  Google Scholar 

  • Hadjiosif AM, Smith MA (2013a) Savings is restricted to the temporally labile component of motor adaptation. Translational and Computational Motor Control

  • Hadjiosif AM, Smith MA (2013b) Generalization of temporally-labile and temporally stable components of motor memory. Abstract submitted to Society for Neuroscience

  • Henriques DY, Cressman EK (2012) Visuomotor adaptation and proprioceptive recalibration. J Motor Behav 44:435–444

    Article  Google Scholar 

  • Henriques DY, Soechting JF (2003) Bias and sensitivity in haptic perception of geometry. Exp Brain Res 150:95–108

    PubMed  Google Scholar 

  • Henriques DY, Filippopulos F, Straube A, Effert T (2014) The cerebellum is not necessary for visually driven recalibration of hand proprioceptive. Neuropsychologia 64:195–204

    Article  Google Scholar 

  • Izawa J, Criscimagna-Hemminger SE, Shadmehr R (2012) Cerebellar contributions to reach adaptation and learning sensory consequences of action. J Neurosci 32:4230–4239

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jeannerod M (1988) The neural and behavioural organization of goal-directed movements. Clarendon Press, Oxford, UK

    Google Scholar 

  • Kesten H (1958) Accelerated stochastic approximation. Ann Math Stat 29:41–59

    Article  Google Scholar 

  • Kitago T, Ryan SL, Mazzoni P, Krakauer JW, Haith AM (2013) Unlearning versus savings in visuomotor adaptation: comparing effects of washout, passage of time, and removal of errors on motor memory. Front Hum Neurosci 7:307

    Article  PubMed  PubMed Central  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  CAS  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 forgetting. J Neurosci 25:473–478

    Article  CAS  PubMed  Google Scholar 

  • Martin TA, Keating JG, Goodkin HP, Bastian AJ, Thach WT (1996) Throwing while looking through prisms. II. Specificity and storage of multiple gaze-throw calibrations. Brain 119:1199–1211

    Article  PubMed  Google Scholar 

  • Mattar AA, Darainy M, Ostry DJ (2013) Motor learning and its sensory effects: time course of perceptual change and its presence with gradual introduction of load. J Neurophys 109:782–791

    Article  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 

  • Miyamoto YR, Wang SX, Brennan AE, Smith MA (2014) Distinct forms of implicit learning that respond differentially to performance errors and sensory prediction errors. Translational and Computational Motor Control

  • Mostafa AA, Kamran-Disfani R, Bahari-Kashani G, Cressman EK, Henriques DY (2014a) Generalization of reach adaptation and proprioceptive recalibration at different distances in the workspace. Exp Brain Res 233:817–827

    Article  PubMed  Google Scholar 

  • Mostafa AA, Salomonczyk D, Cressman EK, Henriques DY (2014b) Intermanual transfer and proprioceptive recalibration following training with translated visual feedback of the hand. Exp Brain Res 232:1639

    Article  PubMed  Google Scholar 

  • Neva JL, Henriques DY (2013) Visuomotor adaptation and generalization with repeated and varied training. Exp Brain Res 226:363–372

    Article  PubMed  Google Scholar 

  • Nourouzpour N, Salomonczyk D, Cressman EK, Henriques DY (2015) Retention of proprioceptive recalibration following visuomotor adaptation. Exp Brain Res 233:1019–1029

    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 

  • Pisella L, Michel C, Grea H, Tilikete C, Vighetto A, Rossetti Y (2004) Preserved prism adaptation in bilateral optic ataxia: strategic versus adaptive reaction to prisms. Exp Brain Res 156:399–408

    Article  CAS  PubMed  Google Scholar 

  • Redding GM, Rossetti Y, Wallace B (2005) Applications of prism adaptation: a tutorial in theory and method. Neurosci Biobehav R 29:431–444

    Article  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 

  • Salomonczyk D, Cressman EK, Henriques DY (2011) Proprioceptive recalibration following prolonged training and increasing distortions in visuomotor adaptation. Neuropsychologia 49:3053–3062

    Article  PubMed  Google Scholar 

  • Salomonczyk D, Henriques DY, Cressman EK (2012) Proprioceptive recalibration in the right and left hands following abrupt visuomotor adaptation. Exp Brain Res 217:187–196

    Article  PubMed  Google Scholar 

  • Salomonczyk D, Cressman EK, Henriques DY (2013) The role of the cross-sensory error signal in visuomotor adaptation. Exp Brain Res 228:313–325

    Article  PubMed  Google Scholar 

  • Simani MC, McGuire LM, Sabes PN (2007) Visual-shift adaptation is composed of separable sensory and task-dependent effects. J Neurophysiol 98:2827–2841

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Smith MA, Ghazizadeh A, Shadmehr R (2006) Interacting adaptive processes with different timescales underlie short-term motor learning. PLoS Biol 4:e179

    Article  PubMed  PubMed Central  Google Scholar 

  • Taylor JA, Ivry RB (2011) Flexible cognitive strategies during motor learning. PLoS Comput Biol 7:e10001096

    Article  Google Scholar 

  • Taylor JA, Krakauer JW, Ivry RB (2014) Explicit and implicit contributions to learning in a sensorimotor adaptation task. J Neurosci 34:3023–3032

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Treutwein B (1995) Adaptive psychophysical procedures (2014). Vision Res 35:2503–2522

    Article  CAS  PubMed  Google Scholar 

  • Tseng Y, Diedrichsen J, Krakauer JW, shadmehre R, Bastian AJ (2007) Sensory Prediction Errors Drive Cerebellum-Dependent Adaptation of Reaching. J Neurophys 98:54–62

    Article  Google Scholar 

  • van Beers RJ, Wolpert DM, Haggard P (2002) When feeling is more important than seeing in sensorimotor adaptation. Curr Biol 12:834–837

    Article  PubMed  Google Scholar 

  • Wei K, Kording K (2009) Relevance of error: what drives motor adaptation? J Neurophys 101: 655-664

    Article  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Yamamoto K, Hoffman DS, Strick PL (2006) Rapid and long-lasting plasticity of input output mapping. J Neurophysiol 96:2797–2801

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

This research was supported by a Discovery Grant from the Natural Sciences and Engineering Research Council to EKC.

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Authors and Affiliations

  1. School of Human Kinetics, University of Ottawa, 125 University Private, Room 360, Ottawa, ON, K1N6N5, Canada

    Basel Zbib & Erin K. Cressman

  2. School of Kinesiology and Health Science, York University, Toronto, Canada

    Denise Y. P. Henriques

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  1. Basel Zbib
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  2. Denise Y. P. Henriques
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  3. Erin K. Cressman
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Correspondence to Erin K. Cressman.

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Zbib, B., Henriques, D.Y.P. & Cressman, E.K. Proprioceptive recalibration arises slowly compared to reach adaptation. Exp Brain Res 234, 2201–2213 (2016). https://doi.org/10.1007/s00221-016-4624-6

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  • DOI: https://doi.org/10.1007/s00221-016-4624-6

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