Skip to main content
SpringerLink
Log in

Proprioceptive recalibration following implicit visuomotor adaptation is preserved in Parkinson’s disease

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

Abstract

Individuals with Parkinson’s disease (PD) and healthy adults demonstrate similar levels of visuomotor adaptation provided that the distortion is small or introduced gradually, and hence, implicit processes are engaged. Recently, implicit processes underlying visuomotor adaptation in healthy individuals have been proposed to include proprioceptive recalibration (i.e., shifts in one’s proprioceptive sense of felt hand position to match the visual estimate of their hand experienced during reaches with altered visual feedback of the hand). In the current study, we asked if proprioceptive recalibration is preserved in PD patients. PD patients tested during their “off” and “on” medication states and age-matched healthy controls reached to visual targets, while visual feedback of their unseen hand was gradually rotated 30° clockwise or translated 4 cm rightwards of their actual hand trajectory. As expected, PD patients and controls produced significant reach aftereffects, indicating visuomotor adaptation after reaching with the gradually introduced visuomotor distortions. More importantly, following visuomotor adaptation, both patients and controls showed recalibration in hand position estimates, and the magnitude of this recalibration was comparable between PD patients and controls. No differences for any measures assessed were observed across medication status (i.e., PD off vs PD on). Results reveal that patients are able to adjust their sensorimotor mappings and recalibrate proprioception following adaptation to a gradually introduced visuomotor distortion, and that dopaminergic intervention does not affect this proprioceptive recalibration. These results suggest that proprioceptive recalibration does not involve striatal dopaminergic pathways and may contribute to the preserved visuomotor adaptation that arises implicitly in PD patients.

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.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Adamovich SV, Berkinblit MB, Hening W, Sage J, Poizner H (2001) The interaction of visual and proprioceptive inputs in pointing to actual and remembered targets in Parkinson’s disease. Neuroscience 104(4):1027–1041

    Article  CAS  PubMed  Google Scholar 

  • Almeida QJ, Wishart LR, Lee TD (2002) Bimanual coordination deficits with Parkinson’s disease: the influence of movement speed and external cueing. Mov Disord 17(1):30–37

    Article  PubMed  Google Scholar 

  • Almeida QJ, Frank JS, Roy EA, Jenkins ME, Spaulding S, Patla AE et al (2005) An evaluation of sensorimotor integration during locomotion toward a target in Parkinson’s disease. Neuroscience 134(1):283–293

    Article  CAS  PubMed  Google Scholar 

  • Bedard P, Sanes JN (2011) Basal ganglia-dependent processes in recalling learned visual-motor adaptations. Exp Brain Res 209(3):385–393

    Article  PubMed  Google Scholar 

  • Block HJ, Bastian AJ (2012) Cerebellar involvement in motor but not sensory adaptation. Neuropsychologia 50:1766–1775

    Article  PubMed  PubMed Central  Google Scholar 

  • Clayton HA, Cressman EK, Henriques DYP (2014) The effect of visuomotor adaptation on proprioceptive localization: the contributions of perceptual and motor changes. Exp Brain Res 232(7):2073–2086

    Article  PubMed  Google Scholar 

  • Clower DM, Hoffman JM, Votaw JR, Faber TL, Woods RP, Alexander GE (1996) Role of posterior parietal cortex in the recalibration of visually guided reaching. Nature 383:618–621

    Article  CAS  PubMed  Google Scholar 

  • Contreras-Vidal JL, Buch ER (2003) Effects of Parkinson’s disease on visuomotor adaptation. Exp Brain Res 150(1):25–32

    Article  PubMed  Google Scholar 

  • Cressman EK, Henriques DY (2009) Sensory recalibration of hand position following visuomotor adaptation. J Neurophysiol 102(6):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(4):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(4):533–544

    Article  PubMed  Google Scholar 

  • Davidsdottir S, Wagenaar R, Young D, Cronin-Golomb A (2008) Impact of optic flow perception and egocentric coordinates on veering in Parkinson’s disease. Brain 131(Pt 11):2882–2893

    Article  PubMed  PubMed Central  Google Scholar 

  • Fahn S, Elton RL (1987) Unified Parkinson’s disease rating scale. In: Fahn S, Marsden CD, Goldstein M, Caine DB (eds) Recent developments in Parkinson’s disease, vol 2. Macmillan Healthcare Information, Florham Park, NJ, pp 153–163

    Google Scholar 

  • Fuentes CT, Bastian AJ (2010) Where is your arm? Variations in proprioception across space and tasks. J Neurophysiol 103(1):164–171

    Article  PubMed  Google Scholar 

  • Galea JM, Bestmann S, Beigi M, Jahanshahi M, Rothwell JC (2012) Action reprogramming in Parkinson’s disease: response to prediction error is modulated by levels of dopamine. Neuroscience 32(2):542–550

    Article  CAS  PubMed  Google Scholar 

  • Henriques DY, Soechting JF (2003) Bias and sensitivity in the haptic perception of geometry. Exp Brain Res 150(1):95–108

    Article  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Hoehn MM, Yahr MD (1967) Parkinsonism: onset, progression and mortality. Neurology 17(5):427–442

    Article  CAS  PubMed  Google Scholar 

  • Isaias IU, Moisello C, Marotta G, Schiavella M, Canesi M, Perfetti B, Ghilardi MF (2011) Dopaminergic striatal innervation predicts interlimb transfer of a visuomotor skill. J Neuroscience 31(41):14458–14462

    Article  CAS  Google Scholar 

  • Jacobs JV, Horak FB (2006) Abnormal proprioceptive-motor integration contributes to hypometric postural responses of subjects with Parkinson’s disease. Neuroscience 141(2):999–1009

    Article  CAS  PubMed  Google Scholar 

  • Jones SA, Cressman EK, Henriques DY (2010) Proprioceptive localization of the left and right hands. Exp Brain Res 204(3):373–383

    Article  PubMed  Google Scholar 

  • Kesten H (1958) Accelerated stochastic approximation. Ann Math Stat 29(1):41–59

    Article  Google Scholar 

  • Konczak J, Li KY, Tuite PJ, Poizner H (2008) Haptic perception of object curvature in Parkinson’s disease. PLoS ONE 3(7):e2625

    Article  PubMed  PubMed Central  Google Scholar 

  • Konczak J, Corcos DM, Horak F, Poizner H, Shapiro M, Tuite P, Volkmann J, Maschke M (2009) Proprioception and motor control in Parkinson’s disease. J Mot Behav 41(6):543–552

    Article  PubMed  Google Scholar 

  • Lee AC, Harris JP, Atkinson EA, Fowler MS (2001) Disruption of estimation of body-scaled aperture width in Hemiparkinson’s disease. Neuropsychologia 39(10):1097–1104

    Article  CAS  PubMed  Google Scholar 

  • Lee D, Henriques DY, Snider J, Song D, Poizner H (2013) Reaching to proprioceptively defined targets in Parkinson’s disease: effects of deep brain stimulation therapy. Neuroscience 244:99–112

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lewis SJ, Slabosz A, Robbins TW, Barker RA, Owen AM (2005) Dopaminergic basis for deficits in working memory but not attentional set-shifting in Parkinson’s disease. Neuropsychologia 43(6):823–832

    Article  PubMed  Google Scholar 

  • Li KY, Pickett K, Nestrasil I, Tuite P, Konczak J (2010) The effect of dopamine replacement therapy on haptic sensitivity in Parkinson’s disease. Neurology 257(12):1992–1998

    Article  CAS  Google Scholar 

  • Mancini M, Rocchi L, Horak FB, Chiari L (2008) Effects of Parkinson’s disease and levodopa on functional limits of stability. Clin Biomech 23(4):450–458

    Article  Google Scholar 

  • Marinelli L, Crupi D, Di Rocco A, Bove M, Eidelberg D, Abbruzzese G, Ghilardi MF (2009) Learning and consolidation of visuo-motor adaptation in Parkinson’s disease. Parkinsonism Relat Disord 15(1):6–11

    Article  PubMed  Google Scholar 

  • Maschke M, Tuite PJ, Krawczewski K, Pickett K, Konczak J (2006) Perception of heaviness in Parkinson’s disease. Mov Disord 21(7):1013–1018

    Article  PubMed  Google Scholar 

  • McEntee WJ, Mair RG, Langlais PJ (1987) Neurochemical specificity of learning: dopamine and motor learning. Yale J Biol Med 60(2):187–193

    CAS  PubMed  PubMed Central  Google Scholar 

  • McNeely ME, Duncan RP, Earhart GM (2012) Medication improves balance and complex gait performance in Parkinson disease. Gait Posture 36(1):144–148

    Article  PubMed  PubMed Central  Google Scholar 

  • Messier J, Adamovich S, Jack D, Hening W, Sage J, Poizner H (2007) Visuomotor learning in immersive 3D virtual reality in Parkinson’s disease and in aging. Exp Brain Res 179:457–474

    Article  PubMed  Google Scholar 

  • Modchalingam S, Vachon CM, ‘t Hart BM, Henriques DYP (2019) The effects of awareness of the perturbation during motor adaptation on hand localization. PLoS ONE 14(8):e0220884

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mongeon D, Blanchet P, Messier J (2009) Impact of Parkinson’s disease and dopaminergic medication on proprioceptive processing. Neuroscience 158(2):426–440

    Article  CAS  PubMed  Google Scholar 

  • Mongeon D, Blanchet P, Messier J (2013) Impact of Parkinson’s disease and dopaminergic medication on adaptation to explicit and implicit visuomotor perturbations. Brain Cogn 81(2):271–282

    Article  PubMed  Google Scholar 

  • Mongeon D, Blanchet P, Bergeron S, Messier J (2015) Impact of Parkinson’s disease on proprioceptively based on-line movement control. Exp Brain Res 233(9):2707–2721

    Article  PubMed  Google Scholar 

  • Morehead JR, Qasim SE, Crossley MJ, Ivry R (2015) Savings upon re-aiming in visuomotor adaptation. J Neurosci 35(42):14386–14396

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Neville KM, Cressman EK (2018) The influence of awareness on explicit and implicit contributions to visuomotor adaptation over time. Exp Brain Res 236(7):2047–2059

    Article  PubMed  Google Scholar 

  • O’Suilleabhain P, Bullard J, Dewey RB (2001) Proprioception in Parkinson’s disease is acutely depressed by dopaminergic medications. J Neurol Neurosurg Psychiatry 71(5):607–610

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Owen AM, Iddon JL, Hodges JR, Summers BA, Robbins TW (1997) Spatial and non-spatial working memory at different stages of Parkinson’s disease. Neuropsychologia 35(4):519–532

    Article  CAS  PubMed  Google Scholar 

  • Poizner H, Fookson OI, Berkinblit MB, Hening W, Feldman G, Adamovich S (1998) Pointing to remembered targets in 3-D space in Parkinson’s disease. Mot Control 2(3):251–277

    Article  CAS  Google Scholar 

  • Rickards C, Cody FW (1997) Proprioceptive control of wrist movements in Parkinson’s disease Reduced muscle vibration-induced errors. Brain 120(Pt 6):977–990

    Article  PubMed  Google Scholar 

  • Ruttle JE, ‘t Hart BM, Henriques DY (2018) The fast contribution of visual-proprioceptive discrepancy to reach aftereffects and proprioceptive recalibration. PLoS ONE 13(7):e0200621

    Article  PubMed  PubMed Central  Google Scholar 

  • Salomonczyk D, Cressman EK, Henriques DY (2011) Proprioceptive recalibration following prolonged training and increasing distortions in visuomotor adaptation. Neuropsychologia 49(11):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(2):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(3):313–325

    Article  PubMed  Google Scholar 

  • Seidler RD, Bernard JA, Burutolu TB, Fling BW, Gordon MT, Gwin JT, Kwak Y, Lipps DB (2010) Motor control and aging: links to age-related brain structural, functional, and biochemical effects. Neurosci Biobehav Rev 34(5):721–733

    Article  CAS  PubMed  Google Scholar 

  • Semrau JA, Perlmutter JS, Thoroughman KA (2014) Visuomotor adaptation in Parkinson’s disease: effects of perturbation type and medication state. J Neurophysiol 111(12):2675–2687

    Article  PubMed  PubMed Central  Google Scholar 

  • Shadmehr R, Krakauer JW (2008) A computational neuroanatomy for motor control. Exp Brain Res 185:359–381

    Article  PubMed  PubMed Central  Google Scholar 

  • Shadmehr R, Smith MA, Krakauer JW (2010) Error correction, sensory prediction, and adaptation in motor control. Ann Rev Neurosci 33:89–108

    Article  CAS  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(5):2827–2841

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Swinnen SP, Van Langendonk L, Verschueren S, Peeters G, Dom R, De Weerdt W (1997) Interlimb coordination deficits in patients with Parkinson’s disease during the production of two-joint oscillations in the sagittal plane. Mov Disord 12(6):958–968

    Article  CAS  PubMed  Google Scholar 

  • Takiyama K, Sakurada T, Shinya M, Sato T, Ogihara H, Komatsu T (2020) Larger, but not better, motor adaptation ability inherent in medicated parkinson’s disease patients revealed by a smart-device-based study. Scientific Reports 10(1):1–11

    Article  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Vachon CM, Modchalingam S, ’t Hart BM, Henriques DYP (2020) The effect of age on visuomotor learning processes. PLoS ONE 15(9):e0239032

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vahdat S, Darainy M, Milner TE, Ostry DJ (2011) Functionally specific changes in resting-state sensorimotor networks after motor learning. J Neuroscienc 31:16907–16915

    CAS  Google Scholar 

  • Van Beers RJ, Sittig AC, Van Der Gon JJD (1998) The precision of proprioceptive position sense. Exp Brain Res 122(4):367–377

    Article  PubMed  Google Scholar 

  • Van Beers RJ, Wolpert DM, Haggard P (2002) When feeling is more important than seeing in sensorimotor adaptation. Curr Biol 12(10):834–837

    Article  PubMed  Google Scholar 

  • Venkatakrishnan A, Banquet JP, Burnod Y, Contreras-Vidal JL (2011) Parkinson’s disease differentially affects adaptation to gradual as compared to sudden visuomotor distortions. Hum Mov Sci 30(4):760–769

    Article  PubMed  PubMed Central  Google Scholar 

  • Verschueren SM, Swinnen SP, Dom R, De Weerdt W (1997) Interlimb coordination in patients with Parkinson’s disease: motor learning deficits and the importance of augmented information feedback. Exp Brain Res 113(3):497–508

    Article  CAS  PubMed  Google Scholar 

  • Wang J, Joshi M, Lei Y (2011) The extent of interlimb transfer following adaptation to a novel visuomotor condition does not depend on awareness of the condition. J Neurophysiol 106(1):259–264

    Article  PubMed  PubMed Central  Google Scholar 

  • Werner S, Van Aken BC, Hulst T, Frens MA, Van Der Geest JN, Strüder HK, Donchin O (2015) Awareness of sensorimotor adaptation to visual rotations of different size. PLoS ONE 10(4):1–18

    Article  Google Scholar 

  • Wiltshire K, Foster S, Kaye JA, Small BJ, Camicioli R (2005) Corpus callosum in neurodegenerative diseases: findings in Parkinson’s disease. Dement Geriatr Cogn Disord 20(6):345–351

    Article  PubMed  Google Scholar 

  • Zbib B, Henriques DY, Cressman EK (2016) Proprioceptive recalibration arises slowly compared to reach adaptation. Exp Brain Res 234(8):2201–2213

    Article  PubMed  Google Scholar 

  • Zia S, Cody F, O’Boyle D (2000) Joint position sense is impaired by Parkinson’s disease. Ann Neurol 47(2):218–228

    Article  CAS  PubMed  Google Scholar 

  • Zia S, Cody FW, O’Boyle DJ (2002) Identification of unilateral elbow-joint position is impaired by Parkinson’s disease. Clin Anat 15(1):23–31

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

This work was supported by the J. P. Bickell Foundation, granted to DYPH.

Author information

Authors and Affiliations

  1. School of Human Kinetics, University of Ottawa, Ottawa, Canada

    Erin K. Cressman

  2. Department of Psychology, York University, Toronto, Canada

    Danielle Salomonczyk

  3. Centre for Vision Research, York University, Toronto, Canada

    Danielle Salomonczyk, Alina Constantin & Denise Y. P. Henriques

  4. Morton and Gloria Shulman Movement Disorders Centre and the Edmond J Safra Program in Parkinson’s Disease, Toronto Western Hospital, Toronto, Canada

    Janis Miyasaki, Elena Moro, Robert Chen, Antonio Strafella, Susan Fox & Anthony E. Lang

  5. Institute for Neural Computation, University of California, San Diego, USA

    Howard Poizner

  6. Department of Kinesiology, School of Kinesiology and Health Science, York University, 4700 Keele Street, Toronto, ON, M3J 1P3, Canada

    Denise Y. P. Henriques

Authors
  1. Erin K. Cressman
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Danielle Salomonczyk
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Alina Constantin
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Janis Miyasaki
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Elena Moro
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Robert Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Antonio Strafella
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Susan Fox
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Anthony E. Lang
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Howard Poizner
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Denise Y. P. Henriques
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Denise Y. P. Henriques.

Additional information

Communicated by Winston D Byblow.

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

221_2021_6075_MOESM1_ESM.eps

Supplementary file1 S1. Visuomotor adaptation during reach training trials with an aligned and rotated cursor (Experiment 1). The mean angular deviation of the hand at peak velocity relative to the target is presented for each block (3 trials) of training when controls (diamonds), PD patients off meds (triangles), and PD patients on meds (circles) reached with an aligned (empty symbols) and rotated (filled symbols) cursor. Error bars reflect the standard error of the mean. (EPS 1608 KB)

221_2021_6075_MOESM2_ESM.eps

Supplementary file2 S2. Visuomotor adaptation during reach training trials with an aligned and translated cursor (Experiment 2). The mean lateral hand deviation at peak velocity relative to the target is presented for each block (3 trials) of training when controls (diamonds), PD patients off meds (triangles), and PD patients on meds (circles) reached with an aligned (empty symbols) and translated (filled symbols) cursor. Error bars reflect the standard error of the mean. (EPS 1239 KB)

Supplementary file3 (DOCX 25 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Cressman, E.K., Salomonczyk, D., Constantin, A. et al. Proprioceptive recalibration following implicit visuomotor adaptation is preserved in Parkinson’s disease. Exp Brain Res 239, 1551–1565 (2021). https://doi.org/10.1007/s00221-021-06075-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00221-021-06075-y

Keywords

Search

Navigation