Skip to main content

Motor and Perceptual Timing in Parkinson’s Disease

  • Chapter
  • First Online:
Book cover Neurobiology of Interval Timing

Part of the book series: Advances in Experimental Medicine and Biology ((AEMB,volume 829))

Abstract

Neuroimaging has been a powerful tool for understanding the neural architecture of interval timing. However, identifying the critical brain regions engaged in timing was initially driven by investigation of human patients and animals. This chapter draws on the important contribution that the study of patients with Parkinson’s disease (PD) has made in identifying the basal ganglia as a key component of motor and perceptual timing. The chapter initially describes the experimental tasks that have been critical in PD (and non-PD) timing research before systematically discussing the results from behavioural studies. This is followed by a critique of neuroimaging studies that have given insight into the pattern of neural activity during motor and perceptual timing in PD. Finally, discussion of the effects of medical and surgical treatment on timing in PD enables further evaluation of the role of dopamine in interval timing.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 129.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  1. Rodriguez-Oroz MC, Jahanshahi M, Krack P, Litvan I, Macias R, Bezard E, Obeso JA. Initial clinical manifestations of Parkinson’s disease: features and pathophysiological mechanisms. Lancet Neurol. 2009;8(12):1128–39.

    Article  PubMed  CAS  Google Scholar 

  2. Wing AM, Keele SW, Margolin DI. Motor disorder and the timing of repetitive movements. In: Gibbon J, Allen L, editors. Timing and time perception, vol. 423. New York: Annals of the New York Academy of Science; 1984. p. 183–92.

    Google Scholar 

  3. Ivry RB. The representation of temporal information in perception and motor control. Curr Opin Neurobiol. 1996;6(6):851–7.

    Article  PubMed  CAS  Google Scholar 

  4. Coull JT, Cheng RK, Meck WH. Neuroanatomical and neurochemical substrates of timing. Neuropsychopharmacology. 2011;36(1):3–25.

    Article  PubMed  PubMed Central  Google Scholar 

  5. Keele SW, Pokorny RA, Corcos DM, Ivry R. Do perception and motor production share common timing mechanisms: a correctional analysis. Acta Psychol (Amst). 1985;60(2–3):173–91.

    Article  CAS  Google Scholar 

  6. Merchant H, Luciana M, Hooper C, Majestic S, Tuite P. Interval timing and Parkinson’s disease: heterogeneity in temporal performance. Exp Brain Res. 2008;184(2):233–48.

    Article  PubMed  Google Scholar 

  7. Cerasa A, Hagberg GE, Peppe A, Bianciardi M, Gioia M, Costa A, Castriota-Scanderbeg A, Caltagirone C, Sabatini U. Functional changes in the activity of cerebellum and frontostriatal regions during externally and internally timed movement in Parkinson’s disease. Brain Res Bull. 2006;71:259–69.

    Article  PubMed  Google Scholar 

  8. Claassen DO, Jones CR, Yu M, Dirnberger G, Malone T, Parkinson M, Giunti P, Kubovy M, Jahanshahi M. Deciphering the impact of cerebellar and basal ganglia dysfunction in accuracy and variability of motor timing. Neuropsychologia. 2013;51(2):267–74.

    Article  PubMed  Google Scholar 

  9. Duchek JM, Balota DA, Ferraro FR. Component analysis of a rhythmic finger tapping task in individuals with senile dementia of the Alzheimer type and in individuals with Parkinson’s disease. Neuropsychology. 1994;8(2):218–26.

    Article  Google Scholar 

  10. Elsinger CL, Rao S, Zimbelman JL, Reynolds NC, Blindauer KA, Hoffmann RG. Neural basis for impaired time reproduction in Parkinson’s disease: an fMRI study. J Int Neuropsychol Soc. 2003;9:1088–98.

    Article  PubMed  Google Scholar 

  11. Harrington DL, Haaland KY, Hermanowicz N. Temporal processing in the basal ganglia. Neuropsychology. 1998;12(1):3–12.

    Article  PubMed  CAS  Google Scholar 

  12. Ivry RB, Keele SW. Timing functions of the cerebellum. J Cogn Neurosci. 1989;1:136–52.

    Google Scholar 

  13. Jahanshahi M, Jones CRG, Zijlmans J, Katzenschlager R, Lee L, Quinn N, Frith CD, Lees AJ. Dopaminergic modulation of striato-frontal connectivity during motor timing in Parkinson’s disease. Brain. 2010;133:727–45.

    Article  PubMed  Google Scholar 

  14. Jones CRG, Claassen DO, Minhong Y, Spies JR, Malone T, Dirnberger G, Jahanshahi M, Kubovy M. Modeling accuracy and variability of motor timing in treated and untreated Parkinson’s disease and healthy controls. Front Integr Neurosci. 2011;5(81). doi:10.3389/fnint.2011.00081.

  15. Joundi RA, Brittain JS, Green AL, Aziz TZ, Jenkinson N. High-frequency stimulation of the subthalamic nucleus selectively decreases central variance of rhythmic finger tapping in Parkinson’s disease. Neuropsychologia. 2012;50(10):2460–6.

    Article  PubMed  Google Scholar 

  16. O’Boyle DJ, Freeman JS, Cody FW. The accuracy and precision of timing of self-paced, repetitive movements in subjects with Parkinson’s disease. Brain. 1996;119(1):51–70.

    Article  PubMed  Google Scholar 

  17. Pastor MA, Jahanshahi M, Artieda J, Obeso JA. Performance of repetitive wrist movements in Parkinson’s disease. Brain. 1992;115:875–91.

    Article  PubMed  Google Scholar 

  18. Spencer RM, Ivry RB. Comparison of patients with Parkinson’s disease or cerebellar lesions in the production of periodic movements involving event-based or emergent timing. Brain Cogn. 2005;58(1):84–93.

    Article  PubMed  Google Scholar 

  19. Wojtecki L, Elben S, Timmermann L, Reck C, Maarouf M, Jorgens S, Ploner M, Südmeyer M, Groiss SJ, Sturm V, Niedeggen M, Schnitzler A. Modulation of human time processing by subthalamic deep brain stimulation. PLoS One. 2011;6(9):12.

    Google Scholar 

  20. Guehl D, Burbaud P, Lorenzi C, Ramos C, Bioulac B, Semal C, Demany L. Auditory temporal processing in Parkinson’s disease. Neuropsychologia. 2008;46(9):2326–35.

    Article  PubMed  Google Scholar 

  21. Harrington DL, Castillo GN, Greenberg PA, Song DD, Lessig S, Lee RR, Rao SM. Neurobehavioural mechanisms of temporal processing deficits in Parkinson’s disease. PLoS One. 2011;6(2):e17461. doi:10.1371/journal.pone.0017461.

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  22. Hellström A, Lang H, Portin R, Rinne J. Tone duration discrimination in Parkinson’s disease. Neuropsychologia. 1997;35(5):737–40.

    Article  PubMed  Google Scholar 

  23. Rammsayer T, Classen W. Impaired temporal discrimination in Parkinson’s disease: temporal processing of brief durations as an indicator of degeneration of dopaminergic neurons in the basal ganglia. Int J Neurosci. 1997;91(1–2):45–55.

    Article  PubMed  CAS  Google Scholar 

  24. Riesen JM, Schnider A. Time estimation in Parkinson’s disease: normal long duration estimation despite impaired short duration discrimination. J Neurol. 2001;248(1):27–35.

    Article  PubMed  CAS  Google Scholar 

  25. Wearden JH, Smith-Spark JH, Cousins R, Edelstyn NM, Cody FW, O’Boyle DJ. Stimulus timing by people with Parkinson’s disease. Brain Cogn. 2008;67(3):264–79.

    Article  PubMed  CAS  Google Scholar 

  26. Malapani C, Rakitin B, Levy R, Meck WH, Deweer B, Dubois B, Gibbon J. Coupled temporal memories in Parkinson’s disease: a dopamine-related dysfunction. J Cogn Neurosci. 1998;10(3):316–31.

    Article  PubMed  CAS  Google Scholar 

  27. Malapani C, Deweer B, Gibbon J. Separating storage from retrieval dysfunction of temporal memory in Parkinson’s disease. J Cogn Neurosci. 2002;14(2):311–22.

    Article  PubMed  Google Scholar 

  28. Smith JG, Harper DN, Gittings D, Abernethy D. The effect of Parkinson’s disease on time estimation as a function of stimulus duration range and modality. Brain Cogn. 2007;64(2):130–43.

    Article  PubMed  Google Scholar 

  29. Lange KW, Tucha O, Steup A, Gsell W, Naumann M. Subjective time estimation in Parkinson’s disease. J Neural Transm Suppl. 1995;46:433–8.

    PubMed  CAS  Google Scholar 

  30. Pastor MA, Artieda J, Jahanshahi M, Obeso JA. Time estimation and reproduction is abnormal in Parkinson’s disease. Brain. 1992;115:211–25.

    Article  PubMed  Google Scholar 

  31. Jones CRG, Malone TJ, Dirnberger G, Edwards M, Jahanshahi M. Basal ganglia, dopamine and temporal processing: performance on three timing tasks on and off medication in Parkinson’s disease. Brain Cogn. 2008;68(1):30–41.

    Article  PubMed  Google Scholar 

  32. Perbal S, Deweer B, Pillon B, Vidailhet M, Dubois B, Pouthas V. Effects of internal clock and memory disorders on duration reproductions and duration productions in patients with Parkinson’s disease. Brain Cogn. 2005;58(1):35–48.

    Article  PubMed  Google Scholar 

  33. Wild-Wall N, Willemssen R, Falkenstein M, Beste C. Time estimation in healthy ageing and neurodegenerative basal ganglia disorders. Neurosci Lett. 2008;442:34–8.

    Article  PubMed  CAS  Google Scholar 

  34. Koch G, Brusa L, Caltagirone C, Oliveri M, Peppe A, Tiraboschi P, Stanzione P. Subthalamic deep brain stimulation improves time perception in Parkinson’s disease. Neuroreport. 2004;15(6):1071–3.

    Article  PubMed  Google Scholar 

  35. Koch G, Brusa L, Oliveri M, Stanzione P, Caltagirone C. Memory for time intervals is impaired in left hemi-Parkinson patients. Neuropsychologia. 2005;43(8):1163–7.

    Article  PubMed  Google Scholar 

  36. Koch G, Costa A, Brusa L, Peppe A, Gatto I, Torriero S, Lo Gerfo E, Salerno S, Oliveri M, Carlesimo GA, Caltagrione C. Impaired reproduction of second but not millisecond time intervals in Parkinson’s disease. Neuropsychologia. 2008;46(5):1305–13.

    Article  PubMed  Google Scholar 

  37. Torta DM, Castelli L, Latini-Corazzini L, Banche A, Lopiano L, Geminiani G. Dissociation between time reproduction of actions and of intervals in patients with Parkinson’s disease. J Neurol. 2010;257(8):3377–85.

    Article  Google Scholar 

  38. Kudlicka A, Clare L, Hindle JV. Executive functions in Parkinson’s disease: systematic review and meta-analysis. Mov Disord. 2011;26(13):2305–15.

    Article  PubMed  Google Scholar 

  39. Hinton SC, Rao SM. One-thousand one… one-thousand two…”: chronometric counting violates the scalar property in interval timing. Psychon Bull Rev. 2004;11:24–30.

    Article  PubMed  Google Scholar 

  40. Hinton SC, Harrington DL, Binder JR, Durgerian S, Rao SM. Neural systems supporting timing and chronometric counting: an fMRI study. Cogn Brain Res. 2004;21(2):183–92.

    Article  Google Scholar 

  41. Brown RG, Marsden CD. Dual task performance and processing resources in normal subjects and patients with Parkinson’s disease. Brain. 1991;114(1):215–31.

    PubMed  Google Scholar 

  42. Wing AM, Kristofferson AB. Response delays and timing of discrete motor responses. Percept Psychophys. 1973;14:5–12.

    Google Scholar 

  43. Wing AM, Kristofferson AB. Timing of interresponse intervals. Percept Psychophys 1973;13:455–60.

    Google Scholar 

  44. Collier GL, Ogden RT. Variance decomposition of tempo drift in isochronous rhythmic tapping. Ann N Y Acad Sci. 2001;930:405–8.

    Article  PubMed  CAS  Google Scholar 

  45. Madison G. Variability in isochronous tapping: higher order dependencies as a function of intertap interval. J Exp Psychol Hum Percept Perform. 2001;27(2):411–22.

    Article  PubMed  CAS  Google Scholar 

  46. Jahanshahi M, Jones CRG, Dirnberger G, Frith CD. The substantia nigra pars compacta and temporal processing. J Neurosci. 2006;26(47):12266–73.

    Article  PubMed  CAS  Google Scholar 

  47. Beudel M, Galama S, Leenders KL, de Jong BM. Time estimation in Parkinson’s disease and degenerative cerebellar disease. Neuroreport. 2008;19(10):1055–8.

    Article  PubMed  Google Scholar 

  48. Bareš M, Lungu OV, Husárová I, Gescheidt T. Predictive motor timing performance dissociates between early diseases of the cerebellum and Parkinson’s disease. Cerebellum. 2010;9(1):124–35.

    Article  PubMed  Google Scholar 

  49. Thomas EA, Weaver WB. Cognitive processing and time perception. Percept Psychophys. 1975;17:363–7.

    Article  Google Scholar 

  50. Grahn JA, Brett M. Impairment of beat-based rhythm discrimination in Parkinson’s disease. Cortex. 2009;45(1):54–61.

    Article  PubMed  Google Scholar 

  51. Wearden JH, Todd NP, Jones LA. When do auditory/visual differences in duration judgements occur? Q J Exp Psychol. 2006;59(10):1709–24.

    Article  CAS  Google Scholar 

  52. Zélanti PS, Droit-Volet S. Auditory and visual differences in time perception? An investigation from a developmental perspective with neuropsychological tests. J Exp Child Psychol. 2012;112:296–311.

    Article  PubMed  Google Scholar 

  53. Filippopoulos PC, Hallworth P, Lee S, Wearden JH. Interference between auditory and visual duration judgements suggests a common code for time. Psychol Res. 2013;77:708–15.

    Article  PubMed  Google Scholar 

  54. Wearden JH, Norton R, Martin S, Montford-Bebb O. Internal clock processes and the filled-duration illusion. J Exp Psychol Hum Percept Perform. 2007;33(3):716–29.

    Article  PubMed  Google Scholar 

  55. Santi A, Miki A, Hornyak S, Eidse J. The perception of empty and filled time intervals by rats. Behav Processes. 2005;70(3):247–63.

    Article  PubMed  Google Scholar 

  56. Logigian E, Hefter H, Reiners K, Freund HJ. Does tremor pace repetitive voluntary motor behavior in Parkinson’s disease? Ann Neurol. 1991;30(2):172–9.

    Article  PubMed  CAS  Google Scholar 

  57. Stegemöller EL, Simuni T, MacKinnon C. Effect of movement frequency on repetitive finger movements in patients with Parkinson’s disease. Mov Disord. 2009;24(8):1162–9.

    Article  PubMed  PubMed Central  Google Scholar 

  58. Yahalom G, Simon ES, Thorne R, Peretz C, Giladi N. Hand rhythmic tapping and timing in Parkinson’s disease. Parkinsonism Relat Disord. 2004;10(3):143–8.

    Article  PubMed  CAS  Google Scholar 

  59. Freeman JS, Cody FW, Schady W. The influence of external timing cues upon the rhythm of voluntary movements in Parkinson’s disease. J Neurol Neurosurg Psychiatry. 1993;56(10):1078–84.

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  60. Moreau C, Ozsancak C, Blatt JL, Derambure P, Destee A, Defebvre L. Oral festination in Parkinson’s disease: biomechanical analysis and correlation with festination and freezing of gait. Mov Disord. 2007;22(10):1503–6.

    Article  PubMed  Google Scholar 

  61. Nakamura R, Nagasaki H, Narabayashi H. Disturbances of rhythm formation in patients with Parkinson’s disease: part I. Characteristics of tapping response to the periodic signals. Percept Mot Skills. 1978;46(1):63–75.

    Article  PubMed  CAS  Google Scholar 

  62. Toma K, Mima T, Matsuoka T, Gerloff C, Ohnishi T, Koshy B, Andres F, Hallett M. Movement rate effect on activation and functional coupling of motor cortical areas. J Neurophysiol. 2002;88:3377–85.

    Article  PubMed  Google Scholar 

  63. Summers JJ, Anson JG. Current status of the motor program: revisited. Hum Mov Sci. 2009;28:566–77.

    Article  PubMed  Google Scholar 

  64. Jäncke L, Specht K, Mirzazade S, Loose R, Himmelbach M, Lutz K, Shah NJ. A parametric analysis of the “rate effect” in the sensorimotor cortex: a functional magnetic resonance imaging analysis in human subjects. Neurosci Lett. 1998;252(1):37–40.

    Article  PubMed  Google Scholar 

  65. Sadato N, Ibanez V, Campbell G, Deiber M-P, Le Bihan D, Hallett M. Frequency-dependent changes of regional cerebral blood flow during finger movements: functional MRI compared to PET. J Cereb Blood Flow Metab. 1997;17:670–9.

    Article  PubMed  CAS  Google Scholar 

  66. Alexander GE, DeLong MR, Strick PL. Parallel organization of functionally segregated circuits linking basal ganglia and cortex. Annu Rev Neurosci. 1986;9:357–81.

    Article  PubMed  CAS  Google Scholar 

  67. Dušek P, Jech R, Sieger T, Vymazal J, Růžička E, Wackermann J, Mueller K. Abnormal activity in the precuneus during time perception in Parkinson’s disease: an fMRI study. PLoS One. 2012;7(1):e29635. doi:10.1371/journal.pone.0029635.

    Article  PubMed  PubMed Central  Google Scholar 

  68. Husárová I, Lungu OV, Mareček R, Mikl M, Gescheidt T, Krupa P, Bareš M. Functional imaging of the cerebellum and basal ganglia during motor predictive motor timing in early Parkinson’s disease. J Neuroimaging. 2011. doi:10.1111/j.1552-6569.2011.00663.x.

    PubMed  Google Scholar 

  69. Bradberry TJ, Metman LV, Contreras-Vidal JL, van den Munckhof P, Hosey LA, Thompson JL, Schulz GM, Lenz F, Pahwa R, Lyons KE, Braun AR. Common and unique responses to dopamine agonist therapy and deep brain stimulation in Parkinson’s disease: An H2 15O PET study. Brain Stimul. 2012;5(4):605–15.

    Article  PubMed  PubMed Central  Google Scholar 

  70. 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(11):1431–41.

    Article  PubMed  Google Scholar 

  71. Jahanshahi M, Ardouin CM, Brown RG, Rothwell JC, Obeso J, Albanese A, Rodriguez-Oroz MC, Benabid AL, Pollak P, Limousin-Dowsey P. The impact of deep brain stimulation on executive function in Parkinson’s disease. Brain. 2000;123(6):1142–54.

    Article  PubMed  Google Scholar 

  72. Chaudhuri KR, Healy DG, Schapira AH. Non-motor symptoms of Parkinson’s disease: diagnosis and management. Lancet Neurol. 2006;5(3):235–45.

    Article  PubMed  Google Scholar 

  73. Jankovic J, McDermott M, Carter J, Gauthier S, Goetz C, Golbe L, Huber S, Koller W, Olanow C, Shoulson I, Stern M, Tanner C, Weiner A, Parkinson Study Group. Variable expression of Parkinson's disease: a base-line analysis of the DATATOP cohort. Neurology. 1990;40(10):1529–34.

    Google Scholar 

  74. Schrag A, Quinn NP, Ben-Shlomo Y. Heterogeneity of Parkinson’s disease. J Neurol Neurosurg Psychiatry. 2006;77(2):275–6.

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  75. van Rooden SM, Colas F, Martínez-Martín P, Visser M, Verbaan D, Marinus J, Chaudhuri RK, Kok JN, van Hilten JJ. Clinical subtypes of Parkinson’s disease. Mov Disord. 2011;26(1):51–8.

    Article  PubMed  Google Scholar 

  76. Gibbon J. Scalar expectancy theory and Weber’s law in animal timing. Psychol Rev. 1977;84:279–325.

    Article  Google Scholar 

  77. Gibbon J, Church RM, Meck WH. Scalar timing in memory. Ann N Y Acad Sci. 1984;423:52–77.

    Article  PubMed  CAS  Google Scholar 

  78. Matell MS, Meck WH. Neuropsychological mechanisms of interval timing behaviour. Bioessays. 2000;22:94–103.

    Article  PubMed  CAS  Google Scholar 

  79. Matell MS, Meck WH. Cortico-striatal circuits and interval timing: coincidence detection of oscillatory processes. Brain Res Cogn Brain Res. 2004;21:139–70.

    Article  PubMed  Google Scholar 

  80. Yu H, Sternad D, Corcos DM, Vaillancourt DE. Role of hyperactive cerebellum and motor cortex in Parkinson’s disease. NeuroImage. 2007;35:222–33.

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Catherine R. G. Jones .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2014 Springer Science+Business Media New York

About this chapter

Cite this chapter

Jones, C.R.G., Jahanshahi, M. (2014). Motor and Perceptual Timing in Parkinson’s Disease. In: Merchant, H., de Lafuente, V. (eds) Neurobiology of Interval Timing. Advances in Experimental Medicine and Biology, vol 829. Springer, New York, NY. https://doi.org/10.1007/978-1-4939-1782-2_14

Download citation

Publish with us

Policies and ethics