Abstract
Visuomotor adaptation to a kinematic distortion was investigated in Parkinson's disease (PD) patients and age-matched controls. Participants performed pointing movements in which the visual feedback of hand movement, displayed as a screen cursor, was normal (pre-exposure condition) or rotated by 90° counterclockwise (exposure condition). Aftereffects were assessed in a post-exposure condition in which the visual feedback of hand movement was set back to normal. In pre- and early-exposure trials, both groups showed similar initial directional error (IDE) and movement straightness (RMSE, root mean square error), but the PD group showed reduced movement smoothness (normalized jerk, NJ) and primary submovement to total movement distance ratios (PTR). During late-exposure the PD subjects, compared with controls, showed larger IDE, RMSE, NJ, and smaller PTR scores. Moreover, PD patients showed smaller aftereffects than the controls during the post-exposure condition. Overall, the PD group showed both slower and reduced adaptation compared with the control group. These results are discussed in terms of reduced signal-to-noise ratio in feedback signals related to increased movement variability and/or disordered kinesthesia, deficits in movement initiation, impaired selection of initial movement direction, and deficits in internal model formation in PD patients. We conclude that Parkinson's disease impairs visuomotor adaptation.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Notes
Generally speaking, "internal models are neural representations of how, for instance, the arm would respond to a neural command, given its current position and velocity" and thus, in the context of this study, they "are expected to represent the altered relationship between the cursor movement and the mouse [or hand] movement (forward and/or inverse kinematics model)" (p 194 of Imamizu et al. 2000). In the context of the present experiment, other researchers have used the term to describe "neural principles which represent positions in such a way that they are accessible by both the sensory and motor system" (Abeele and Bock 2001)
References
Abeele S, Bock O (2001) Sensorimotor adaptation to rotated visual input: different mechanisms for small versus large rotations. Exp Brain Res 140:407–410
Boraud T, Bezard E, Bioulac B, Gross CE (2000) Ratio of inhibited-to-activated pallidal neurons decreases dramatically during passive limb movement in the MPTP-treated monkey. J Neurophysiol 83:1760–1763
Carter CS, Braver TS, Barch DM, Botvinick MM, Noll D, Cohen JD (1998) Anterior cingulate cortex, error detection, and the online monitoring of performance. Science 280:747–749
Clower DM, Boussaoud D (2000) Selective use of perceptual recalibration versus visuomotor skill acquisition. J Neurophysiol 84:2703–2708
Falkenstein M, Hielscher H, Dziobek I, Schwarzenau P, Hoormann J, Sunderman B, Hohnsbein J (2001) Action monitoring, error detection, and the basal ganglia: an ERP study. Neuroreport 12:157–161
Filion M, Tremblay L, Bedard PJ (1988) Abnormal influences of passive limb movement on the activity of globus pallidus neurons in parkinsonian monkeys. Brain Res 444:165–176
Gao JH, Parsons LM, Bower JM, Xiong JH, Li JQ, Fox PT (1996) Cerebellum implicated in sensory acquisition and discrimination rather than motor control. Science 272:545–547
Ghilardi MF, Alberoni M, Rossi M, Franceschi M, Mariani C, Fazio F (2000a) Visual feedback has differential effects on reaching movements in Parkinson's and Alzheimer's disease. Brain Res 876:112–123
Ghilardi, MF, Ghez CV, Dhawan V, Moeller J, Mentis M, Nakamura T, Antonini A, Eidelberg D (2000b) Patterns of regional brain activation associated with different forms of motor learning. Brain Res 871:127–145
Grafton ST, Fagg AH, Woods RP, Arbib MA (1996) Functional anatomy of pointing and grasping in humans. Cereb Cortex 6:226–237
Imamizu H, Miyauchi S, Tamada T, Sasaki Y, Takino R, Putz B, Yoshioka T, Kawato M (2000) Human cerebellar activity reflecting an acquired internal model of a new tool. Nature 403:192–195
Ingram HA, van Donkelaar P, Cole J, Vercher JL, Gauthier GM, Miall RC (2000) The role of proprioception and attention in a visuomotor adaptation task. Exp Brain Res 132:114–126
Jones DL, Phillips JG, Bradshaw JL, Iansek R, Bradshaw JA (1993) Coding of movement direction and amplitude in Parkinson's disease: are they differentially impaired (or unimportant)? J Neurol Neurosurg Psychiatry 56:419–22
Jueptner M, Weiller C (1998) A review of differences between basal ganglia and cerebellar control of movements as revealed by functional imaging studies. Brain 121:1437–1449
Kagerer FA, Contreras-Vidal JL, Stelmach GE (1997) Adaptation to gradual as compared with sudden visuo-motor distortions. Exp Brain Res 115:557–561
Kawato M, Wolpert D (1998) Internal models for motor control. Novartis Found Symp 218:291–304
Kitazawa S, Goto T, Urushihara Y (1993) Quantitative evaluation of reaching movements in cats with and without cerebellar lesions using normalized integral of jerk. In: Mano N, Hamada I, DeLong MR (eds) Role of the cerebellum and basal ganglia in voluntary movement. Elsevier, Amsterdam, pp 11–19
Klockgether T, Dichgans J (1994) Visual control of arm movement in Parkinson's disease. Mov Disord 9:48–56
Krakauer JW, Pine ZM, Ghilardi MF, Ghez C (2000) Learning of visuomotor transformations for vectorial planning of reaching trajectories. J Neurosci 20:8916–8924
Manolakis DG, Ingle VK, Kogon S (2000) Statistical and adaptive signal processing: spectral estimation, signal modeling, adaptive filtering, and array processing. McGraw Hill, New York
Pratt J, Chasteen AL, Abrams RA (1994) Rapid aimed limb movements: age differences and practice effects in component submovements. Psychol Aging 9:325–34
Rickards C, Cody FW (1997) Proprioceptive control of wrist movements in Parkinson's disease. Reduced muscle vibration-induced errors. Brain 120:977–990
Robertson EM, Miall RC (1999) Visuomotor adaptation during inactivation of the dentate nucleus. Neuroreport 10:1029–1034
Roby-Brami A, Burnod Y (1995) Learning of a new visuomotor transformation: error correction and generalization. Cognit Brain Res 2:229–242
Schugens MM, Daum I, Richter S, Scholz E, Canavan AGM (1993) Proximal and distal reaction times (RTs) are not differentially affected in Parkinson's disease. Mov Disord 8:367–370
Stern Y, Mayeux R, Hermann A, Rosen J (1988) Prism adaptation in Parkinson's disease. J Neurol Neurosurg Psychiatry 51:1584–1587
Teulings HL, Contreras-Vidal JL, Stelmach GE, Adler CH (2002) Handwriting size adaptation under distorted feedback in Parkinson's disease, elderly, and young controls. J Neurol Neurosurg Psychiatry 72:315–324
Touge T, Werhahn KJ, Rothwell JC, Marsden CD (1995) Movement-related cortical potentials preceding repetitive and random-choice hand movements in Parkinson's disease. Ann Neurol 37:791–799
Tremblay L, Filion M, Bedard PJ (1989) Responses of pallidal neurons to striatal stimulation in monkeys with MPTP-induced parkinsonism. Brain Res 498:17–33
van Beers RJ, Sittig AC, Gon JJ (1999) Integration of proprioceptive and visual position-information: an experimentally supported model. J Neurophysiol 81:1355–1364
Weiner MJ, Hallett M, Funkenstein HH (1983) Adaptation to lateral displacement of vision in patients with lesions of the central nervous system. Neurology 33:766–77
Acknowledgements
This research has been supported in part by the US National Institute on Aging, NIA AG019148-01. The authors would like to thank the reviewers for valuable comments on earlier versions of this manuscript.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Contreras-Vidal, J.L., Buch, E.R. Effects of Parkinson's disease on visuomotor adaptation. Exp Brain Res 150, 25–32 (2003). https://doi.org/10.1007/s00221-003-1403-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00221-003-1403-y