Skip to main content
SpringerLink
Log in

Coordination deficits during trunk-assisted reach-to-grasp movements in Parkinson’s disease

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

Abstract

The present study investigated how Parkinson’s disease (PD) affects temporal coordination among the trunk, arm, and fingers during trunk-assisted reach-to-grasp movements. Seated participants with PD and healthy controls made prehensile movements. During the reach to the object, the involvement of the trunk was altered based on the instruction; the trunk was not involved, moved forward (flexion), or moved backward (extension) in the sagittal plane. Each of the trunk movements was combined with an extension or flexion motion of the arm during the reach. For the transport component, the individuals with PD substantially delayed the onset of trunk motion relative to that of arm motion in conditions where the trunk was moved in the direction opposite from the arm reaching toward the object. At the same time, variability of intervals between the onsets and intervals between the velocity peaks of the trunk and wrist movements was increased. The magnitudes of the variability measures were significantly correlated with the severity of PD. Regarding the grasp component, the individuals with PD delayed the onset of finger movements during reaching. These results imply that PD impairs temporal coordination between the axial and distal body segments during goal-directed skilled actions. When there is a directional discrepancy between the trunk and wrist motions, individuals with PD appear to prioritize wrist motion that is tied to the task goal over the trunk motion. An increase in disease severity magnifies the coordination deficits.

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.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

Notes

  1. We are interested in the neural control of the movement in the correct direction because the current task was to perform specific combinations of motion directions between the trunk and arm based on instructions. If individuals initially move in the wrong direction, they have to reprocess their movement, and the time spent for moving in the wrong direction is possibly used to plan and prepare the movement in the correct direction. For this reason, the current study focuses on analyzing the onset time of the trunk movement in the correct (instructed) direction.

References

  • 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 

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

    Article  PubMed  Google Scholar 

  • Almeida QJ, Wishart LR, Lee TD (2003) Disruptive influences of a cued voluntary shift on coordinated movement in Parkinson’s disease. Neuropsychologia 41:442–452

    Article  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 (1986) Performance of simultaneous movements in patients with Parkinson’s disease. Brain 109:739–757

    Article  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

    Article  CAS  PubMed  Google Scholar 

  • Bloem BR, Grimbergen YA, van Dijk JG, Munneke M (2006) The “posture second” strategy: a review of wrong priorities in Parkinson’s disease. J Neurol Sci 248:196–204

    Article  PubMed  Google Scholar 

  • Brown RG, Marsden CD (1991) Dual task performance and processing resources in normal subjects and patients with Parkinson’s disease. Brain 114:215–231

    PubMed  Google Scholar 

  • Byblow WD, Summers JJ, Lewis GN, Thomas J (2002) Bimanual coordination in Parkinson’s disease: deficits in movement frequency, amplitude, and pattern switching. Mov Disord 17:20–29

    Article  PubMed  Google Scholar 

  • Canning CG (2005) The effect of directing attention during walking under dual-task conditions in Parkinson’s disease. Parkinsonism Relat Disord 11:95–99

    Article  PubMed  Google Scholar 

  • Castiello U, Stelmach GE, Lieberman AN (1993) Temporal dissociation of the prehension pattern in Parkinson’s disease. Neuropsychologia 31:395–402

    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 

  • Chung KA, Lobb BM, Nutt JG, Horak FB (2010) Effects of a central cholinesterase inhibitor on reducing falls in Parkinson disease. Neurology 75:1263–1269

    Article  CAS  PubMed  Google Scholar 

  • Churchill A, Hopkins B, Rönnqvist L, Vogt S (2000) Vision of the hand and environmental context in human prehension. Exp Brain Res 134:81–89

    Article  CAS  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 

  • Connor NP, Abbs JH (1991) Task-dependent variations in parkinsonian motor impairments. Brain 114:321–332

    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 

  • Fahn S, Elton R, Members of the UPDRS Development Committee (1987) Unified Parkinsons disease rating scale. In: Fahn S, Marsden CD, Calne DB, Goldstein M (eds) Recent developments in Parkinson’s disease. Macmillan Health Care Information, Florham Park, vol 2, pp 153–163

  • 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 

  • Folstein M, Folstein S, McHugh P (1975) “Mini-mental state” A practical method for grading the cognitive state of patients for the clinician. J Psychiatr Res 12:189–198

    Article  CAS  PubMed  Google Scholar 

  • Fradet L, Lee G, Stelmach G, Dounskaia N (2009) Joint-specific disruption of control during arm movements in Parkinson’s disease. Exp Brain Res 195:73–87

    Article  PubMed  Google Scholar 

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

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Gentilucci M, Roy AC, Stefanini S (2004) Grasping an object naturally or with a tool: are these tasks guided by a common motor representation? Exp Brain Res 157:496–506

    Article  PubMed  Google Scholar 

  • Goetz CG, Poewe W, Rascol O, Sampaio C, Stebbins GT, Counsell C et al (2004) Movement disorder society task force report on the Hoehn and Yahr staging scale: status and recommendations. Mov Disord 19:1020–1028

    Article  PubMed  Google Scholar 

  • Haggard P (2008) Human volition: towards a neuroscience of will. Nat Rev Neurosci 9:934–946

    Article  CAS  PubMed  Google Scholar 

  • Heilman KM, Valenstein E (2012) Clinical neuropsychology, 5th edn. Oxford University Press, New York

    Google Scholar 

  • Hikosaka O, Isoda M (2010) Switching from automatic to controlled behavior: cortico-basal ganglia mechanisms. Trends Cogn Sci 14:154–161

    Article  PubMed Central  PubMed  Google Scholar 

  • Hikosaka O, Nakahara H, Rand MK, Sakai K, Lu X, Nakamura K, Miyachi S, Doya K (1999) Parallel neural networks for learning sequential procedures. Trends Neurosci 22:464–471

    Article  CAS  PubMed  Google Scholar 

  • Hikosaka O, Takikawa Y, Kawagoe R (2000) Role of the basal ganglia in the control of purposive saccadic eye movements. Physiol Rev 80:953–978

    CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Horstink MW, Berger HJ, van Spaendonck KP, van den Bercken JH, Cools AR (1990) Bimanual simultaneous motor performance and impaired ability to shift attention in Parkinson’s disease. J Neurol Neurosurg Psychiatry 53:685–690

    Article  CAS  PubMed  Google Scholar 

  • Isoda M, Hikosaka O (2011) Cortico-basal ganglia mechanisms for overcoming innate, habitual and motivational behaviors. Eur J Neurosci 33:2058–2069

    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 

  • Jeannerod M (1981) Intersegmental coordination during reaching at natural visual objects. In: Long J, Baddeley A (eds) Attention and performance IX. Erlbaum, Hillsdale, pp 153–168

    Google Scholar 

  • Jeannerod M (1984) The timing of finger grip during prehension: a cortically mediated visuomotor pattern. J Mot Behav 16:235–254

    Article  CAS  PubMed  Google Scholar 

  • Kaminski TR, Bock C, Gentile AM (1995) The coordination between trunk and arm motion during pointing movements. Exp Brain Res 106:457–466

    Article  CAS  PubMed  Google Scholar 

  • Kim SD, Allen NE, Canning CG, Fung VSC (2013) Postural instability in patients with Parkinson’s disease. CNS Drugs 27:97–112

    Article  PubMed  Google Scholar 

  • Levy-Tzedek S, Krebs HI, Arle JE, Shils JL, Poizner H (2011) Rhythmic movement in Parkinson’s disease: effects of visual feedback and medication state. Exp Brain Res 211:77–86

    Article  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 

  • Magill RA (2010) Motor learning and control: concepts and applications, 9th edn. McGraw-Hill, New York

    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 

  • Marteniuk RG, 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 

  • Ménoret M, Curie A, des Portes V, Nazir TA, Paulignan Y (2013) Simultaneous action execution and observation optimise grasping actions. Exp Brain Res 227:407–419

    Article  PubMed  Google Scholar 

  • Miyachi S, Hikosaka O, Miyashita K, Kárádi Z, Rand MK (1997) Differential roles of monkey striatum in learning of sequential hand movement. Exp Brain Res 115:1–5

    Article  CAS  PubMed  Google Scholar 

  • Pigeon P, Yahia LH, Mitnitski AB, Feldman AG (2000) Superposition of independent units of coordination during pointing movements involving the trunk with and without visual feedback. Exp Brain Res 131:336–349

    Article  CAS  PubMed  Google Scholar 

  • Pilon JF, De Serres SJ, Feldman AG (2007) Threshold position control of arm movement with anticipatory increase in grip force. Exp Brain Res 181:49–67

    Article  PubMed  Google Scholar 

  • Poizner H, Feldman AG, Levin MF, Berkinblit MB, Hening WA, Patel A et al (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, Shimansky Y, Stelmach GE, Bracha V, Bloedel JR (2000) Effects of accuracy constrains on reach-to-grasp movements in cerebellar patients. Exp Brain Res 135:179–188

    Article  CAS  PubMed  Google Scholar 

  • Rand MK, Shimansky Y, Stelmach GE, Bloedel JR (2004) Adaptation of reach-to-grasp movement in response to force perturbations. Exp Brain Res 154:50–65

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Rand MK, Lemay M, Squire LM, Shimansky YP, Stelmach GE (2010) 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

    Article  PubMed  Google Scholar 

  • Rand MK, Van Gemmert AWA, Hossain ABMI, Shimansky YP, Stelmach GE (2012) Control of aperture closure initiation during trunk-assisted reach-to-grasp movements. Exp Brain Res 219:293–304

    Article  PubMed  Google Scholar 

  • Redgrave P, Rodriguez M, Smith Y, Rodriguez-Oroz MC, Lehericy S, Bergman H et al (2010) Goal-directed and habitual control in the basal ganglia: implications for Parkinson’s disease. Nat Rev Neurosci 11:760–772

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Riehle A, Wirtssohn S, Grün S, Brochier T (2013) Mapping the spatio-temporal structure of motor cortical LFP and spiking activities during reach-to-grasp movements. Front Neural Circuits 7:48

    Article  PubMed Central  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

    Article  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 

  • 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 

  • Schneider W, Chein JM (2003) Controlled & automatic processing: behavior, theory, and biological mechanisms. Cogn Sci 27:525–559

    Google Scholar 

  • Seidler RD, Alberts JL, Stelmach GE (2001) Multijoint movement control in Parkinson’s disease. Exp Brain Res 140:335–344

    Article  CAS  PubMed  Google Scholar 

  • Smith Y, Surmeier DJ, Redgrave P, Kimura M (2011) Thalamic contributions to Basal Ganglia-related behavioral switching and reinforcement. J Neurosci 31:16102–16106

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Song YG, Yoo KS, Park KW, Park JH (2010) Coordinative and limb-specific control of bimanual movements in patients with Parkinson’s disease and cerebellar degeneration. Neurosci Lett 482:146–150

    Article  CAS  PubMed  Google Scholar 

  • Stegemöller EL, Simuni T, MacKinnon CD (2009) The effects of Parkinson’s disease and age on syncopated finger movements. Brain Res 1290:12–20

    Article  PubMed Central  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

    Article  CAS  PubMed  Google Scholar 

  • Terao Y, Fukuda H, Yugeta A, Hikosaka O, Nomura Y, Segawa M et al (2011) Initiation and inhibitory control of saccades with the progression of Parkinson’s disease: changes in three major drives converging on the superior colliculus. Neuropsychologia 49:1794–1806

    Article  PubMed  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 

  • Torres EB, Heilman KM, Poizner H (2011) Impaired endogenously evoked automated reaching in Parkinson’s disease. J Neurosci 31:17848–17863

    Article  CAS  PubMed Central  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, Poizner H, Adamovich SV, Levin MF, Feldman AG (2004) 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 

  • Tunik E, Feldman AG, Poizner H (2007) Dopamine replacement therapy does not restore the ability of Parkinsonian patients to make rapid adjustments in motor strategies according to changing sensorimotor contexts. Parkinsonism Relat Disord 13:425–433

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Ueda Y, Kimura M (2003) Encoding of direction and combination of movements by primate putamen neurons. Eur J Neurosci 18:980–994

    Article  PubMed  Google Scholar 

  • Van Gemmert AWA, Teulings HL, Stelmach GE (1998) The influence of mental and motor load on handwriting movements in parkinsonian patients. Acta Psychol 100:161–175

    Article  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

    Article  CAS  PubMed  Google Scholar 

  • Yang F, Feldman AG (2010) Reach-to-grasp movement as a minimization process. Exp Brain Res 201:75–92

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

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

Author information

Authors and Affiliations

  1. Leibniz Research Centre for Working Environment and Human Factors (IfADo), 67 Ardeystraße, 44139, Dortmund, Germany

    Miya K. Rand

  2. School of Kinesiology, Louisiana State University, 112 HP Long Fieldhouse, Baton Rouge, LA, 70803, USA

    Arend W. A. Van Gemmert

  3. Motor Control Laboratory, Arizona State University, Tempe, AZ, 85287-0701, USA

    Abul B. M. I. Hossain & George E. Stelmach

Authors
  1. Miya K. Rand
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Arend W. A. Van Gemmert
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Abul B. M. I. Hossain
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. George E. Stelmach
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Miya K. Rand.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Rand, M.K., Van Gemmert, A.W.A., Hossain, A.B.M.I. et al. Coordination deficits during trunk-assisted reach-to-grasp movements in Parkinson’s disease. Exp Brain Res 232, 61–74 (2014). https://doi.org/10.1007/s00221-013-3720-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00221-013-3720-0

Keywords

Search

Navigation