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Control of aperture closure initiation during reach-to-grasp movements under manipulations of visual feedback and trunk involvement in Parkinson’s disease

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Abstract

The present project was aimed at investigating how two distinct and important difficulties (coordination difficulty and pronounced dependency on visual feedback) in Parkinson’s disease (PD) affect each other for the coordination between hand transport toward an object and the initiation of finger closure during reach-to-grasp movement. Subjects with PD and age-matched healthy subjects made reach-to-grasp movements to a dowel under conditions in which the target object and/or the hand were either visible or not visible. The involvement of the trunk in task performance was manipulated by positioning the target object within or beyond the participant’s outstretched arm to evaluate the effects of increasing the complexity of intersegmental coordination under different conditions related to the availability of visual feedback in subjects with PD. General kinematic characteristics of the reach-to-grasp movements of the subjects with PD were altered substantially by the removal of target object visibility. Compared with the controls, the subjects with PD considerably lengthened transport time, especially during the aperture closure period, and decreased peak velocity of wrist and trunk movement without target object visibility. Most of these differences were accentuated when the trunk was involved. In contrast, these kinematic parameters did not change depending on the visibility of the hand for both groups. The transport-aperture coordination was assessed in terms of the control law according to which the initiation of aperture closure during the reach occurred when the hand distance-to-target crossed a hand-target distance threshold for grasp initiation that is a function of peak aperture, hand velocity and acceleration, trunk velocity and acceleration, and trunk-target distance at the time of aperture closure initiation. When the hand or the target object was not visible, both groups increased the hand-target distance threshold for grasp initiation compared to its value under full visibility, implying an increase in the hand-target distance-related safety margin for grasping. The increase in the safety margin due to the absence of target object vision or the absence of hand vision was accentuated in the subjects with PD compared to that in the controls. The pronounced increase in the safety margin due to absence of target object vision for the subjects with PD was further accentuated when the trunk was involved compared to when it was not involved. The results imply that individuals with PD have significant limitations regarding neural computations required for efficient utilization of internal representations of target object location and hand motion as well as proprioceptive information about the hand to compensate for the lack of visual information during the performance of complex multisegment movements.

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Notes

  1. An alternative method where trials are randomized across conditions has been found to induce a behavioral pattern where the participants always performed the reaching task as if they were reaching without vision, even in those trials where visual feedback was continuously available (Jakobson and Goodale 1991). For this reason, trial randomization does not seem suitable for revealing changes of kinematic characteristics produced by various vision-related manipulations.

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 104:1027–1041

    Article  CAS  PubMed  Google Scholar 

  • Alberts JL, Saling M, Adler CH, Stelmach GE (2000) Disruptions in the reach-to-grasp actions of Parkinson’s patients. Exp Brain Res 134:353–362

    Article  CAS  PubMed  Google Scholar 

  • Andersen RA, Buneo CA (2002) Intentional maps in posterior parietal cortex. Annu Rev Neurosci 25:189–220

    Article  CAS  PubMed  Google Scholar 

  • Baumann MA, Fluet MC, Scherberger H (2009) Context-specific grasp movement representation in the macaque anterior intraparietal area. J Neurosci 29:6436–6448

    Article  CAS  PubMed  Google Scholar 

  • Benecke R, Rothwell JC, Dick JP, Day BL, Marsden CD (1987) Simple and complex movements off and on treatment in patients with Parkinson’s disease. J Neurol Neurosurg Psychiatry 50:296–303

    Article  CAS  PubMed  Google Scholar 

  • Bertram CP, Lemay M, Stelmach GE (2005) The effect of Parkinson’s disease on the control of multi-segmental coordination. Brain Cogn 57:16–20

    Article  PubMed  Google Scholar 

  • Binkofski F, Dohle C, Posse S, Stephan KM, Hefter H, Seitz RJ, Freund HJ (1998) Human anterior intraparietal area subserves prehension: a combined lesion and functional MRI activation study. Neurology 50:1253–1259

    CAS  PubMed  Google Scholar 

  • Bursztyn LL, Ganesh G, Imamizu H, Kawato M, Flanagan JR (2006) Neural correlates of internal-model loading. Curr Biol 16:2440–2445

    Article  CAS  PubMed  Google Scholar 

  • Caminiti R, Johnson PB (1992) Internal representations of movement in the cerebral cortex as revealed by the analysis of reaching. Cereb Cortex 2:269–276

    Article  CAS  PubMed  Google Scholar 

  • Castiello U, Bennett K, Bonfiglioli C, Lim S, Peppard RF (1999) The reach-to-grasp movement in Parkinson’s disease: response to a simultaneous perturbation of object position and object size. Exp Brain Res 125:453–462

    Article  CAS  PubMed  Google Scholar 

  • Castiello U, Bennett KM, Bonfiglioli C, Peppard RF (2000) The reach-to-grasp movement in Parkinson’s disease before and after dopaminergic medication. Neuropsychologia 38:46–59

    Article  CAS  PubMed  Google Scholar 

  • Chen H, Hua SE, Smith MA, Lenz FA, Shadmehr R (2006) Effects of human cerebellar thalamus disruption on adaptive control of reaching. Cereb Cortex 16:1462–1473

    Article  PubMed  Google Scholar 

  • Clower DM, Dum RP, Strick PL (2005) Basal ganglia and cerebellar inputs to ‘AIP’. Cereb Cortex 15:913–920

    Article  PubMed  Google Scholar 

  • Connolly JD, Andersen RA, Goodale MA (2003) FMRI evidence for a ‘parietal reach region’ in the human brain. Exp Brain Res 153:140–145

    Article  PubMed  Google Scholar 

  • Cooke JD, Brown JD, Brooks VB (1978) Increased dependence on visual information for movement control in patients with Parkinson’s disease. Can J Neurol Sci 5:413–415

    CAS  PubMed  Google Scholar 

  • Davare M, Montague K, Olivier E, Rothwell JC, Lemon RN (2009) Ventral premotor to primary motor cortical interactions during object-driven grasp in humans. Cortex 45:1050–1057

    Article  PubMed  Google Scholar 

  • DeLong MR, Wichmann T (2007) Circuits and circuit disorders of the basal ganglia. Arch Neurol 64:20–24

    Article  PubMed  Google Scholar 

  • Dounskaia N, Ketcham CJ, Leis BC, Stelmach GE (2005) Disruptions in joint control during drawing arm movements in Parkinson’s disease. Exp Brain Res 164:311–322

    Article  PubMed  Google Scholar 

  • Doya K (1999) What are the computations of the cerebellum, the basal ganglia and the cerebral cortex? Neural Netw 12:961–974

    Article  PubMed  Google Scholar 

  • Ferraina S, Brunamonti E, Giusti MA, Costa S, Genovesio A, Caminiti R (2009) Reaching in depth: hand position dominates over binocular eye position in the rostral superior parietal lobule. J Neurosci 29:11461–11470

    Article  CAS  PubMed  Google Scholar 

  • Flash T, Inzelberg R, Schechtman E, Korczyn AD (1992) Kinematic analysis of upper limb trajectories in Parkinson’s disease. Exp Neurol 118:215–226

    Article  CAS  PubMed  Google Scholar 

  • Flowers KA (1976) Visual “closed-loop” and “open-loop” characteristics of voluntary movement in patients with Parkinsonism and intention tremor. Brain 99:269–310

    Article  CAS  PubMed  Google Scholar 

  • Fogelson N, Williams D, Tijssen M, van Bruggen G, Speelman H, Brown P (2006) Different functional loops between cerebral cortex and the subthalmic area in Parkinson’s disease. Cereb Cortex 16:64–75

    Article  PubMed  Google Scholar 

  • Galvan A, Wichmann T (2008) Pathophysiology of Parkinsonism. Clin Neurophysiol 119:1459–1474

    Article  CAS  PubMed  Google Scholar 

  • Gentilucci M, Negrotti A (1999) The control of an action in Parkinson’s disease. Exp Brain Res 129:269–277

    Article  CAS  PubMed  Google Scholar 

  • Georgiou N, Bradshaw JL, Iansek R, Phillips JG, Mattingley JB, Bradshaw JA (1994) Reduction in external cues and movement sequencing in Parkinson’s disease. J Neurol Neurosurg Psychiatry 57:368–370

    Article  CAS  PubMed  Google Scholar 

  • Ghasia FF, Meng H, Angelaki DE (2008) Neural correlates of forward and inverse models for eye movements: evidence from three-dimensional kinematics. J Neurosci 28:5082–5087

    Article  CAS  PubMed  Google Scholar 

  • Haber SN (2003) The primate basal ganglia: parallel and integrative networks. J Chem Neuroanat 26:317–330

    Article  PubMed  Google Scholar 

  • Hamidi M, Tononi G, Postle BR (2009) Evaluating the role of prefrontal and parietal cortices in memory-guided response with repetitive transcranial magnetic stimulation. Neuropsychologia 47:295–302

    Article  PubMed  Google Scholar 

  • Hoover JE, Strick PL (1993) Multiple output channels in the basal ganglia. Science 259:819–821

    Article  CAS  PubMed  Google Scholar 

  • Hoshi E (2006) Functional specialization within the dorsolateral prefrontal cortex: a review of anatomical and physiological studies of non-human primates. Neurosci Res 54:73–84

    Article  PubMed  Google Scholar 

  • Hoshi E, Tanji J (2007) Distinctions between dorsal and ventral premotor areas: anatomical connectivity and functional properties. Curr Opin Neurobiol 17:234–242

    Article  CAS  PubMed  Google Scholar 

  • Imamizu H, Higuchi S, Toda A, Kawato M (2007) Reorganization of brain activity for multiple internal models after short but intensive training. Cortex 43:338–349

    Article  PubMed  Google Scholar 

  • Jackson SR, Jackson GM, Rosicky J (1995) Are non-relevant objects represented in working memory? The effect of non-target objects on reach and grasp kinematics. Exp Brain Res 102:519–530

    Article  CAS  PubMed  Google Scholar 

  • Jackson GM, Jackson SR, Hindle JV (2000) The control of bimanual reach-to-grasp movements in hemiparkinsonian patients. Exp Brain Res 132:390–398

    Article  CAS  PubMed  Google Scholar 

  • Jakobson LS, Goodale MA (1991) Factors affecting higher-order movement planning: a kinematic analysis of human prehension. Exp Brain Res 86:199–208

    Article  CAS  PubMed  Google Scholar 

  • Keijsers NL, Admiraal MA, Cools AR, Bloem BR, Gielen CC (2005) Differential progression of proprioceptive and visual information processing deficits in Parkinson’s disease. Eur J Neurosci 21:239–248

    Article  CAS  PubMed  Google Scholar 

  • Khudados E, Cody FW, O’Boyle DJ (1999) Proprioceptive regulation of voluntary ankle movements, demonstrated using muscle vibration, is impaired by Parkinson’s disease. J Neurol Neurosurg Psychiatr 67:504–510

    Article  CAS  PubMed  Google Scholar 

  • Klockgether T, Dichgans J (1994) Visual control of arm movement in Parkinson’s disease. Mov Disord 9:48–56

    Article  CAS  PubMed  Google Scholar 

  • Leis BC, Rand MK, Van Gemmert AWA, Longstaff MG, Lou JS, Stelmach GE (2005) Movement precues in planning and execution of aiming movements in Parkinson’s disease. Exp Neurol 194:393–409

    Article  CAS  PubMed  Google Scholar 

  • Ma S, Feldman AG (1995) Two functionally different synergies during arm reaching movements involving the trunk. J Neurophysiol 73:2120–2122

    CAS  PubMed  Google Scholar 

  • Majsak MJ, Kaminski T, Gentile AM, Flanagan JR (1998) The reaching movements of patients with Parkinson’s disease under self-determined maximal speed and visually cues conditions. Brain 121:755–766

    Article  PubMed  Google Scholar 

  • Majsak MJ, Kaminski T, Gentile AM, Gordon AM (2008) Effects of a moving target versus a temporal constraint on reach and grasp in patients with Parkinson’s disease. Exp Neurol 210:479–488

    Article  PubMed  Google Scholar 

  • Marteniuk RC, Bertram CP (2001) Contributions of gait and trunk movements to prehension: perspectives from world- and body-centered coordination. Mot Control 2:151–165

    Google Scholar 

  • Matelli M, Luppino G (2001) Parietofrontal circuits for action and space perception in the macaque monkey. Neuroimage 14:S27–S32

    Article  CAS  PubMed  Google Scholar 

  • McFarland NR, Haber SN (2002) Thalamic relay nuclei of the basal ganglia form both reciprocal and nonreciprocal cortical connections, linking multiple frontal cortical areas. J Neurosci 22:8117–8132

    CAS  PubMed  Google Scholar 

  • Middleton FA, Strick PL (2000) Basal ganglia and cerebellar loops: motor and cognitive circuits. Brain Res Brain Res Rev 31:236–250

    Article  CAS  PubMed  Google Scholar 

  • Moroney R, Heida C, Geelen J (2008) Increased bradykinesia in Parkinson’s disease with increased movement complexity: elbow flexion-extension movements. J Comput Neurosci 25:501–519

    Article  PubMed  Google Scholar 

  • Nakamura K, Sakai K, Hikosaka O (1998) Neuronal activity in medial frontal cortex during learning of sequential procedures. J Neurophysiol 80:2671–2687

    CAS  PubMed  Google Scholar 

  • Nakayama Y, Yamagata T, Tanji J, Hoshi E (2008) Transformation of a virtual action plan into a motor plan in the premotor cortex. J Neurosci 28:10287–10297

    Article  CAS  PubMed  Google Scholar 

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

    CAS  Google Scholar 

  • Poizner H, Feldman AG, Levin MF, Berkinblit MB, Hening WA, Patel A, Adamovich SV (2000) The timing of arm-trunk coordination is deficient and vision-dependent in Parkinson’s patients during reaching movements. Exp Brain Res 133:279–292

    Article  CAS  PubMed  Google Scholar 

  • Rand MK, Stelmach GE (1999) Effects of increased stroke number on sequential arm movements in Parkinson’s disease subjects. Parkinsonism Relat Disord 5:27–35

    Article  CAS  PubMed  Google Scholar 

  • Rand MK, Van Gemmert AWA, Stelmach GE (2002) Segment difficulty in two-stroke movements in patients with Parkinson’s disease. Exp Brain Res 143:383–393

    Article  PubMed  Google Scholar 

  • Rand MK, Smiley-Oyen AL, Shimansky YP, Bloedel JR, Stelmach GE (2006a) Control of aperture closure during reach-to-grasp movements in Parkinson’s disease. Exp Brain Res 168:131–142

    Article  CAS  PubMed  Google Scholar 

  • Rand MK, Squire LM, Stelmach GE (2006b) B) Effect of speed manipulation on the control of aperture closure during reach-to-grasp movements. Exp Brain Res 174:74–85

    Article  PubMed  Google Scholar 

  • Rand MK, Lemay M, Squire LM, Shimansky YP, Stelmach GE (2007) Role of vision in aperture closures control during reach-to-grasp movements. Exp Brain Res 181:447–460

    Article  PubMed  Google Scholar 

  • Rand MK, Shimansky Y, Hossain ABM, Stelmach GE (2008) Quantitative model of transport-aperture coordination during reach-to-grasp movements. Exp Brain Res 174:74–85

    Article  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Rizzolatti G, Luppino G, Matelli M (1988) The organization of the cortical motor system: new concepts. Electroencephalogr Clin Neurophysiol 106:283–296

    Google Scholar 

  • Saling M, Stelmach GE, Mescheriakov S, Berger M (1996) Prehension with trunk assisted reaching. Behav Brain Res 80:153–160

    Article  CAS  PubMed  Google Scholar 

  • Samuel M, Ceballos-Baumann AO, Blin J, Uema T, Boecker H, Passingham RE, Brooks DJ (1997) Evidence for lateral premotor and parietal overactivity in Parkinson’s disease during sequential and bimanual movements. A PET study. Brain 120:963–976

    Article  PubMed  Google Scholar 

  • Schenk T, Baur B, Steude U, Bötzel K (2003) Effects of deep brain stimulation on prehensile movements in PD patients are less pronounced when external timing cues are provided. Neuropsychologia 41:783–794

    Article  PubMed  Google Scholar 

  • Schettino LF, Rajaraman V, Jack D, Adamovich SV, Sage J, Poizner H (2004) Deficits in the evolution of hand preshaping in Parkinson’s disease. Neuropsychologia 42:82–94

    Article  PubMed  Google Scholar 

  • Schettino LF, Adamovich SV, Hening W, Tunik E, Sage J, Poizner H (2006) Hand preshaping in Parkinson’s disease: effects of visual feedback and medication state. Exp Brain Res 168:186–202

    Article  PubMed  Google Scholar 

  • Seidler RD, Stelmach GE (2000) Trunk-assisted prehension: specification of body segments with imposed temporal constraints. J Mot Behav 32:379–389

    Article  CAS  PubMed  Google Scholar 

  • Shima K, Tanji J (1998) Both supplementary and presupplementary motor areas are crucial for the temporal organization of multiple movements. J Neurophysiol 80:3247–3260

    CAS  PubMed  Google Scholar 

  • Teasdale N, Bard C, Fleury M, Young D, Proteau L (1993) Determining movement onsets from temporal series. J Mot Behav 25:97–106

    CAS  PubMed  Google Scholar 

  • Teulings HL, Stelmach GE (1991) Control of stroke size, peak acceleration, and stroke duration in Parkinsonian handwriting. Hum Mov Sci 1991(10):315–333

    Article  Google Scholar 

  • Teulings HL, Contreras-Vidal JL, Stelmach GE, Adler CH (1997) Parkinsonism reduces coordination of fingers, wrist, and arm in fine motor control. Exp Neurol 146:159–170

    Article  CAS  PubMed  Google Scholar 

  • Tresilian JR, Stelmach GE, Adler CH (1997) Stability of reach-to-grasp movement patterns in Parkinson’s disease. Brain 120:2093–2111

    Article  PubMed  Google Scholar 

  • Tunik E, Adamovich SV, Poizner H, Feldman AG (2004a) Deficits in rapid adjustments of movements according to task constraints in Parkinson’s disease. Mov Disord 19:897–906

    Article  PubMed  Google Scholar 

  • Tunik E, Poizner H, Adamovich SV, Levin MF, Feldman AG (2004b) Deficits in adaptive upper limb control in response to trunk perturbations in Parkinson’s disease. Exp Brain Res 159:23–32

    CAS  PubMed  Google Scholar 

  • Wang J, Stelmach GE (2001) Spatial and temporal control of trunk-assisted prehensile actions. Exp Brain Res 136:231–240

    Article  CAS  PubMed  Google Scholar 

  • Wang J, Bohan M, Leis BC, Stelmach GE (2006) Altered coordination patterns in parkinsonian patients during trunk-assisted prehension. Parkinsonism Relat Disord 12:211–222

    Article  CAS  PubMed  Google Scholar 

  • Wing AM, Turton A, Fraser C (1986) Grasp size and accuracy of approach in reaching. J Mot Behav 18:245–260

    CAS  PubMed  Google Scholar 

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Acknowledgments

This research was supported by grants from NINDS NS 39352 and 40266.

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  1. Martin Lemay

    Present address: Département de Kinanthropologie, Centre de Réadaptation Marie Enfant, CHU Sainte-Justine, Université du Québec à Montréal, 5200, rue Bélanger est, Montreal, QC, H1T 1C9, Canada

Authors and Affiliations

  1. Motor Control Laboratory, Department of Kinesiology, Arizona State University, Box 870404, Tempe, AZ, 85287-0404, USA

    Miya Kato Rand, Martin Lemay, Linda M. Squire & George E. Stelmach

  2. Harrington Department of Bioengineering, Arizona State University, Tempe, AZ, 85287-9709, USA

    Yury P. Shimansky

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  1. Miya Kato Rand
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Correspondence to Miya Kato Rand.

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Rand, M.K., Lemay, M., Squire, L.M. et al. Control of aperture closure initiation during reach-to-grasp movements under manipulations of visual feedback and trunk involvement in Parkinson’s disease. Exp Brain Res 201, 509–525 (2010). https://doi.org/10.1007/s00221-009-2064-2

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