Implicit task switching in Parkinson’s disease is preserved when on medication

Autoři: Jacob A. Yaffe aff001;  Yair Zlotnik aff002;  Gal Ifergane aff002;  Shelly Levy-Tzedek aff003
Působiště autorů: Goldman Medical School, Faculty of Health Sciences, Ben-Gurion University of the Negev, Beer-Sheva, Israel aff001;  Neurology Department, Soroka University Medical Center, Beer-Sheva, Israel aff002;  Recanati School for Community Health Professions, Department of Physical Therapy, Ben-Gurion University of the Negev, Beer-Sheva, Israel aff003;  Zlotowski Center for Neuroscience, Ben-Gurion University of the Negev, Beer-Sheva, Israel aff004;  Freiburg Institute for Advanced Studies (FRIAS), University of Freiburg, Freiburg, Germany aff005
Vyšlo v časopise: PLoS ONE 15(1)
Kategorie: Research Article


People with Parkinson’s disease have been shown to have difficulty switching between movement plans. In the great majority of studies, the need to switch between tasks was made explicitly. Here, we tested whether people with Parkinson’s disease, taking their normal medication, have difficulty switching between implicitly specified tasks. We further examined whether this switch is performed predictively or reactively. Twenty five people with Parkinson’s disease continuously increased or decreased the frequency of their arm movements, inducing an abrupt–but unaware–switch between rhythmic movements (at high frequencies) and discrete movements (at low frequencies). We tested whether that precipitous change was performed reactively or predictively. We found that 56% of participants predictively switched between the two movement types. The ability of people with Parkinson’s disease, taking their regular medication, to predictively control their movements on implicit tasks is thus preserved.

Klíčová slova:

Cognitive impairment – Dopamine – Dopaminergics – Ellipses – Forearms – Musculoskeletal system – Parkinson disease – Walking


1. Rakitin BC, Stern Y. Parkinson Disease. In: Nadel L, editor. Encyclopedia of Cognitive Science. 2006. doi: 10.1002/0470018860.s00317

2. Pringsheim T, Jette N, Frolkis A, Steeves TDL. The prevalence of Parkinson's disease: A systematic review and meta-analysis. Mov Disord. 2014;29: 1583–1590. doi: 10.1002/mds.25945 24976103

3. Postuma RB, Berg D, Stern M, Poewe W, Olanow CW, Oertel W, et al. MDS clinical diagnostic criteria for Parkinson's disease. Mov Disord. 2015;30: 1591–1601. doi: 10.1002/mds.26424 26474316

4. Jankovic J. Parkinson’s disease: clinical features and diagnosis. J Neurol Neurosurg Psychiatr. 2008;79: 368.

5. Fahn S, Jankovic J, Hallett M. Chapter 4—Parkinsonism: Clinical features and differential diagnosis. Principles and Practice of Movement Disorders (Second Edition). 2011: 66–92.

6. Nonnekes J, Snijders AH, Nutt JG, Deuschl G, Giladi N, Bloem BR. Freezing of gait: a practical approach to management. The Lancet Neurology. 2015;14: 768–778. doi: 10.1016/S1474-4422(15)00041-1 26018593

7. Bloem BR, Hausdorff JM, Visser JE, Giladi N. Falls and freezing of gait in Parkinson's disease: A review of two interconnected, episodic phenomena. Mov Disord. 2004;19: 871–884. doi: 10.1002/mds.20115 15300651

8. Goetz CG, Tilley BC, Shaftman SR, Stebbins GT, Fahn S, Martinez-Martin P, et al. Movement Disorder Society-sponsored revision of the Unified Parkinson's Disease Rating Scale (MDS-UPDRS): Scale presentation and clinimetric testing results. Mov Disord. 2008;23: 2129–2170. doi: 10.1002/mds.22340 19025984

9. Levy-Tzedek S. Changes in Predictive Task Switching with Age and with Cognitive Load. Frontiers in Aging Neuroscience. 2017;9: 375. doi: 10.3389/fnagi.2017.00375 29213235

10. Porr B, Wörgötter F. Learning a forward model of a reflex. Advances in Neural Information Processing Systems. 2003; pp. 1555–1562.

11. Gilbert DT, Wilson TD. Prospection: Experiencing the future. Science. 2007;317: 1351–1354. doi: 10.1126/science.1144161 17823345

12. Weiss A, Herman T, Mirelman A, Shiratzky SS, Giladi N, Barnes LL, et al. The transition between turning and sitting in patients with Parkinson's disease: A wearable device detects an unexpected sequence of events. Gait & Posture. 2019;67: 224–229.

13. Hulbert S, Ashburn A, Robert L, Verheyden G. A narrative review of turning deficits in people with Parkinson’s disease. Disability and Rehabilitation. 2015;37: 1382–1389. doi: 10.3109/09638288.2014.961661 25255298

14. Mancini M, Smulders K, Cohen RG, Horak FB, Giladi N, Nutt JG. The clinical significance of freezing while turning in Parkinson’s disease. Neuroscience. 2017;343: 222–228. doi: 10.1016/j.neuroscience.2016.11.045 27956066

15. Levy-Tzedek S, Krebs HI, Shils JL, Apetauerova D, Arle JE. Parkinson's disease: a motor control study using a wrist robot. Advanced Robotics. 2007;21: 1201–1213.

16. Taylor AE, Saint‐Cyr JA. The Neuropsychology of Parkinsons-Disease. Brain and Cognition. 1995;28: 281–296. doi: 10.1006/brcg.1995.1258 8546855

17. Cools R, Barker RA, Sahakian BJ, Robbins TW. Mechanisms of cognitive set flexibility in Parkinson's disease. Brain. 2001;124: 2503–2512. doi: 10.1093/brain/124.12.2503 11701603

18. Meiran N, Friedman G, Yehene E. Parkinson’s disease is associated with goal setting deficits during task switching. Brain and Cognition. 2004;54: 260–262. doi: 10.1016/j.bandc.2004.02.043 15050789

19. Crescentini C, Mondolo F, Biasutti E, Shallice T. Preserved and impaired task-switching abilities in non-demented patients with Parkinson's disease. Journal of Neuropsychology. 2012;6: 94–118. doi: 10.1111/j.1748-6653.2011.02018.x 22257678

20. Johansson RS, Flanagan JR. Coding and use of tactile signals from the fingertips in object manipulation tasks. Nature Reviews Neuroscience. 2009;10: 345–359. doi: 10.1038/nrn2621 19352402

21. Flanagan JR, Tresilian JR. Grip-load force coupling: a general control strategy for transporting objects. Journal of Experimental Psychology: Human Perception and Performance. 1994;20: 944. doi: 10.1037//0096-1523.20.5.944 7964530

22. Mawase F, Karniel A. Evidence for predictive control in lifting series of virtual objects. Experimental brain research. 2010;203: 447–452. doi: 10.1007/s00221-010-2249-8 20428856

23. Kashi S, Levy-Tzedek S. Smooth leader or sharp follower? Playing the Mirror Game with a Robot. Restorative neurology and neuroscience. 2018;36: 147–159. doi: 10.3233/RNN-170756 29036853

24. Noy L, Dekel E, Alon U. The mirror game as a paradigm for studying the dynamics of two people improvising motion together. Proceedings of the National Academy of Sciences. 2011;108: 20947–20952.

25. Slijper H, Latash ML, Mordkoff JT. Anticipatory postural adjustments under simple and choice reaction time conditions. Brain Res. 2002;924: 184–197. doi: 10.1016/s0006-8993(01)03233-4 11750904

26. Kanekar N, Aruin AS. Aging and balance control in response to external perturbations: role of anticipatory and compensatory postural mechanisms. Age. 2014;36: 9621. doi: 10.1007/s11357-014-9621-8 24532389

27. Jacobs JV, Lou J, Kraakevik JA, Horak FB. The supplementary motor area contributes to the timing of the anticipatory postural adjustment during step initiation in participants with and without Parkinson's disease. Neuroscience. 2009;164: 877–885. doi: 10.1016/j.neuroscience.2009.08.002 19665521

28. Hall LM, Brauer SG, Horak F, Hodges PW. The effect of Parkinson’s disease and levodopa on adaptation of anticipatory postural adjustments. Neuroscience. 2013;250: 483–492. doi: 10.1016/j.neuroscience.2013.07.006 23867768

29. Lin C, Creath RA, Rogers MW. Variability of anticipatory postural adjustments during gait initiation in individuals with Parkinson’s disease. Journal of neurologic physical therapy: JNPT. 2016;40: 40. doi: 10.1097/NPT.0000000000000112 26630325

30. Jacobs JV, Nutt JG, Carlson-Kuhta P, Stephens M, Horak FB. Knee trembling during freezing of gait represents multiple anticipatory postural adjustments. Exp Neurol. 2009;215: 334–341. doi: 10.1016/j.expneurol.2008.10.019 19061889

31. Hogan N, Sternad D. On rhythmic and discrete movements: reflections, definitions and implications for motor control. Experimental Brain Research. 2007;181: 13–30. doi: 10.1007/s00221-007-0899-y 17530234

32. Levy-Tzedek S, Tov MB, Karniel A. Early switching between movement types: indication of predictive control? Brain Res Bull. 2011;85: 283–288. doi: 10.1016/j.brainresbull.2010.11.010 21115104

33. Levy-Tzedek S, Krebs HI, Song D, Hogan N, Poizner H. Non-monotonicity on a spatio-temporally defined cyclic task: evidence of two movement types? Experimental brain research. 2010;202: 733–746. doi: 10.1007/s00221-010-2176-8 20169338

34. Ben-Tov M, Levy-Tzedek S, Karniel A. The effects of rhythmicity and amplitude on transfer of motor learning. PloS one. 2012;7: e46983. doi: 10.1371/journal.pone.0046983 23056549

35. Valyear KF, Fitzpatrick AM, Dundon NM. Now and then: Hand choice is influenced by recent action history. Psychonomic bulletin & review. 2018: 1–10.

36. Wu T, Hallett M, Chan P. Motor automaticity in Parkinson's disease. Neurobiology of Disease. 2015;82: 226–234. doi: 10.1016/j.nbd.2015.06.014 26102020

37. Woodward TS, Bub DN, Hunter MA. Task switching deficits associated with Parkinson’s disease reflect depleted attentional resources. Neuropsychologia. 2002;40: 1948–1955. doi: 10.1016/s0028-3932(02)00068-4 12207992

38. Hodgson TL, Sumner P, Molyva D, Sheridan R, Kennard C. Learning and switching between stimulus-saccade associations in Parkinson’s disease. Neuropsychologia. 2013;51: 1350–1360. doi: 10.1016/j.neuropsychologia.2013.03.026 23583972

39. de Bondt CC, Gerrits, Niels J. H. M., Veltman DJ, Berendse HW, van dH, van dW. Reduced task-related functional connectivity during a set-shifting task in unmedicated early-stage Parkinson’s disease patients. BMC Neuroscience. 2016;17: 20. doi: 10.1186/s12868-016-0254-y 27194153

40. Levy-Tzedek S, Krebs HI, Arle JE, Shils JL, Poizner H. Rhythmic movement in Parkinson’s disease: effects of visual feedback and medication state. Experimental Brain Research. 2011;211: 277. doi: 10.1007/s00221-011-2685-0 21526337

41. Levy-Tzedek S, Arbelle D, Forman D, Zlotnik Y. Improvement in upper-limb UPDRS motor scores following fast-paced arm exercise: A pilot study. Restorative Neurol Neurosci. 2018: 1–11.

42. Levy-Tzedek S, Tov MB, Karniel A. Rhythmic movements are larger and faster but with the same frequency on removal of visual feedback. J Neurophysiol. 2011;106: 2120–2126. doi: 10.1152/jn.00266.2011 21813746

43. Levy-Tzedek S. Motor errors lead to enhanced performance in older adults. Scientific reports. 2017;7: 3270. doi: 10.1038/s41598-017-03430-4 28607449

44. Folstein MF, Folstein SE, McHugh PR. “Mini-mental state”: A practical method for grading the cognitive state of patients for the clinician. Journal of Psychiatric Research. 1975;12: 189–198. doi: 10.1016/0022-3956(75)90026-6 1202204

45. Guiard Y. On Fitts's and Hooke's laws: Simple harmonic movement in upper-limb cyclical aiming. Acta Psychol. 1993;82: 139–159.

46. Guiard Y. Fitts' law in the discrete vs. cyclical paradigm. Human Movement Science. 1997;16: 97–131.

47. Buchanan JJ, Park J, Shea CH. Target width scaling in a repetitive aiming task: switching between cyclical and discrete units of action. Experimental Brain Research. 2006;175: 710–725. doi: 10.1007/s00221-006-0589-1 16917774

48. Buchanan JJ, Park J, Ryu YU, Shea CH. Discrete and cyclical units of action in a mixed target pair aiming task. Experimental Brain Research. 2003;150: 473–489. doi: 10.1007/s00221-003-1471-z 12739091

49. Buchanan JJ, Park J, Shea CH. Systematic scaling of target width: dynamics, planning, and feedback. Neurosci Lett. 2004;367: 317–322. doi: 10.1016/j.neulet.2004.06.028 15337257

50. Cole KJ, Rotella DL. Old age impairs the use of arbitrary visual cues for predictive control of fingertip forces during grasp. Experimental Brain Research. 2002;143: 35–41. doi: 10.1007/s00221-001-0965-9 11907688

51. Rosenbaum DA, Cohen RG, Jax SA, Weiss DJ, Van Der Wel R. The problem of serial order in behavior: Lashley’s legacy. Human movement science. 2007;26: 525–554. doi: 10.1016/j.humov.2007.04.001 17698232

52. Monsell S. Task switching. Trends Cogn Sci (Regul Ed). 2003;7: 134–140.

53. Hirsch P, Schwarzkopp T, Declerck M, Reese S, Koch I. Age-related differences in task switching and task preparation: Exploring the role of task-set competition. Acta Psychol. 2016;170: 66–73.

54. Berry AS, Shah VD, Jagust WJ. The Influence of Dopamine on Cognitive Flexibility Is Mediated by Functional Connectivity in Young but Not Older Adults. Journal of Cognitive Neuroscience. 2018;30: 1330–1344. doi: 10.1162/jocn_a_01286 29791298

55. Aarts E, Nusselein AAM, Smittenaar P, Helmich RC, Bloem BR, Cools R. Greater striatal responses to medication in Parkinson׳s disease are associated with better task-switching but worse reward performance. Neuropsychologia. 2014;62: 390–397. doi: 10.1016/j.neuropsychologia.2014.05.023 24912070

56. Cools R, Barker RA, Sahakian BJ, Robbins TW. l-Dopa medication remediates cognitive inflexibility, but increases impulsivity in patients with Parkinson’s disease. Neuropsychologia. 2003;41: 1431–1441. doi: 10.1016/s0028-3932(03)00117-9 12849761

57. Vaillancourt DE, Schonfeld D, Kwak Y, Bohnen NI, Seidler R. Dopamine overdose hypothesis: Evidence and clinical implications. Mov Disord. 2013;28: 1920–1929. doi: 10.1002/mds.25687 24123087

58. Karrer TM, Josef AK, Mata R, Morris ED, Samanez-Larkin GR. Reduced dopamine receptors and transporters but not synthesis capacity in normal aging adults: a meta-analysis. Neurobiology of Aging. 2017;57: 36–46. doi: 10.1016/j.neurobiolaging.2017.05.006 28599217

59. Cools R. Dopaminergic modulation of cognitive function-implications for l-DOPA treatment in Parkinson's disease. Neuroscience & Biobehavioral Reviews. 2006;30: 1–23.

60. Thorstensson A, Roberthson H. Adaptations to changing speed in human locomotion: speed of transition between walking and running. Acta Physiol Scand. 1987;131: 211–214. doi: 10.1111/j.1748-1716.1987.tb08228.x 3673618

61. Diedrich FJ, Warren WH Jr. Why change gaits? Dynamics of the walk-run transition. Journal of Experimental Psychology: Human Perception and Performance. 1995;21: 183. doi: 10.1037//0096-1523.21.1.183 7707029

62. Diedrich FJ, Warren WH. Dynamics of human gait transitions. Timing of behavior: Neural, psychological, and computational perspectives. 1998: 323–343.

63. Getchell N, Whitall J. Transitions to and from asymmetrical gait patterns. J Mot Behav. 2004;36: 13–27. doi: 10.3200/JMBR.36.1.13-27 14766485

64. Bastian AJ. Learning to predict the future: the cerebellum adapts feedforward movement control. Curr Opin Neurobiol. 2006;16: 645–649. doi: 10.1016/j.conb.2006.08.016 17071073

65. Galea JM, Bestmann S, Beigi M, Jahanshahi M, Rothwell JC. Action reprogramming in Parkinson's disease: response to prediction error is modulated by levels of dopamine. Journal of Neuroscience. 2012;32: 542–550. doi: 10.1523/JNEUROSCI.3621-11.2012 22238089

66. Fu Q, Zhang W, Santello M. Anticipatory planning and control of grasp positions and forces for dexterous two-digit manipulation. Journal of Neuroscience. 2010;30: 9117–9126. doi: 10.1523/JNEUROSCI.4159-09.2010 20610745

67. Rosenbaum DA, Gong L, Potts CA. Pre-Crastination: Hastening Subgoal Completion at the Expense of Extra Physical Effort. Psychol Sci. 2014;25: 1487–1496. doi: 10.1177/0956797614532657 24815613

68. Rosenbaum DA, Fournier LR, Levy-Tzedek S, McBride DM, Rosenthal R, Sauerberger K, et al. Sooner rather than later: Precrastination rather than procrastination. Current Directions in Psychological Science. 2019: 0963721419833652.

69. Zhu M, Yang Y, Hsee CK. The Mere Urgency Effect. J Consum Res. 2018;45: 673–690.

70. Fournier LR, Coder E, Kogan C, Raghunath N, Taddese E, Rosenbaum DA. Which task will we choose first? Precrastination and cognitive load in task ordering. Attention, Perception, & Psychophysics. 2019;81: 489–503.

71. Blinch J, DeWinne CR. Pre-crastination and procrastination effects occur in a reach-to-grasp task. Experimental brain research. 2019;237: 1129–1139. doi: 10.1007/s00221-019-05493-3 30783715

72. Lehtonen E, Lappi O, Summala H. Anticipatory eye movements when approaching a curve on a rural road depend on working memory load. Transportation Research Part F: Traffic Psychology and Behaviour. 2012;15: 369–377.

Článek vyšel v časopise


2020 Číslo 1
Nejčtenější tento týden