Advertisement

The Cerebellum

, Volume 6, Issue 1, pp 18–23 | Cite as

The cerebellum and neural networks for rhythmic sensorimotor synchronization in the human brain

  • Marco MolinariEmail author
  • Maria G. Leggio
  • Michael H. Thaut
Original Article Scientific Papers

Abstract

Sensorimotor synchronization (SMS) is the rhythmic synchronization between a timed sensory stimulus and a motor response. This rather simple function requires complex cerebral processing whose basic mechanisms are far from clear. The importance of SMS is related to its hypothesized relevance in motor recovery following brain lesions. This is witnessed by the large number of studies in different disciplines addressing this issue. In the present review we will focus on the role of the cerebellum by referring to the general modeling of SMS functioning. Although at present no consensus exists on cerebellar timekeeping function it is generally accepted that cerebellar input and output flow process time information. Reviewed data are considered within the framework of the ‘sensory coordination’ hypothesis of cerebellar functioning. The idea that timing might be within the parameters that are under cerebellar control to optimize cerebral cortical functioning is advanced.

Key words

Timing motor learning lesion studies human motor recovery 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. 1.
    Thaut MH, Kenyon GP. Rapid motor adaptations to subliminal frequency shifts during syncopated rhytmic sensorimotor synchronization. Human Movement Sci. 2003;22:321–38.CrossRefGoogle Scholar
  2. 2.
    Thaut MH, Kenyon GP. Response to Bruno Repp’s comments on ‘Rapid motor adaptations to subliminal frequency shifts during syncopated rhythmic sensorimotor synchronization’ by Michael H. Thaut and Gary P. Kenyon (Human Movement Science 22 [2003] 321–38). Human Movement Sci. 2004;23(1):79–86.Google Scholar
  3. 3.
    Repp BH. Comments on ‘Rapid motor adaptations to subliminal frequency shifts during syncopated rhythmic sensorimotor synchronization’ by Michael H. Thaut and Gary P. Kenyon (Human Movement Science 22 [2003] 321–38). Human Movement Sci. 2004;23(1):61–77.Google Scholar
  4. 4.
    Repp BH. Sensorimotor synchronization: A review of the tapping literature. Psychon Bull Rev. 2005;12(6):969–92.PubMedGoogle Scholar
  5. 5.
    Ivry RB, Spencer RMC. Evaluating the role of the cerebellum in temporal processing: beware of the null hypothesis. Brain. 2004;127(8).Google Scholar
  6. 6.
    Harrington DL, Lee RR, Boyd LA, Rapcsak SZ, Knight RT. Reply to: Evaluating the role of the cerebellum in temporal processing: beware of the null hypothesis. Brain. 2004; 127(8).Google Scholar
  7. 7.
    Mates J. A model of synchronization of motor acts to a stimulus sequence. I. Timing and error corrections. Biol Cybern. 1994;70(5):463–73.PubMedCrossRefGoogle Scholar
  8. 8.
    Haken H, Kelso JAS, Bunz H. A theoretical model of phase transitions in human hand movements. Biol Cybern. 1985;51(5):347–56.PubMedCrossRefGoogle Scholar
  9. 9.
    Mitra S, Riley MA, Turvey MT. Chaos in human rhythmic movement. J Mot Behav. 1997;29(3):195–8.PubMedGoogle Scholar
  10. 10.
    Ivry RB. The representation of temporal information in perception and motor control. Curr Opin Neurobiol. 1996;6(6):851–7.PubMedCrossRefGoogle Scholar
  11. 11.
    Ivry RB, Spencer RM. The neural representation of time. Curr Opin Neurobiol. 2004;14(2):225–32.PubMedCrossRefGoogle Scholar
  12. 12.
    Tesche CD, Karhu JJ. Anticipatory cerebellar responses during somatosensory omission in man [see comments]. Hum Brain Mapp. 2000;9(3):119–42.PubMedCrossRefGoogle Scholar
  13. 13.
    Braitenberg V, Heck D, Sultan F. The detection and generation of sequences as a key to cerebellar function: Experiments and theory. Behaviour Brain Sci. 1997;20: 229–77.Google Scholar
  14. 14.
    Ohyama T, Nores WL, Murphy M, Mauk MD. What the cerebellum computes. Trends Neurosci. 2003;26(4):222–7.PubMedCrossRefGoogle Scholar
  15. 15.
    Xu D, Liu T, Ashe J, Bushara KO. Role of the olivocerebellar system in timing. J Neurosci. 2006;26(22):5990–5.PubMedCrossRefGoogle Scholar
  16. 16.
    Lang EJ, Sugihara I, Llinas R. Olivocerebellar modulation of motor cortex ability to generate vibrissal movements in rat. J Physiol. 2006;571(Pt 1):101–20.PubMedCrossRefGoogle Scholar
  17. 17.
    Malapani C, Dubois B, Rancruel G, Gibbon J. Cerebellar dysfunction of temporal processing in the second range in humans. Neuroreport. 1998;9:3907–12.PubMedCrossRefGoogle Scholar
  18. 18.
    Nichelli P, Alway D, Grafman J. Perceptual timing in cerebellar degeneration. Neuropsychologia. 1996;34(9): 863–71.PubMedCrossRefGoogle Scholar
  19. 19.
    Lewis PA, Miall RC. Distinct systems for automatic and cognitively controlled time measurement: Evidence from neuroimaging. Curr Opin Neurobiol. 2003;13(2):250–5.PubMedCrossRefGoogle Scholar
  20. 20.
    Jantzen KJ, Steinberg FL, Kelso JA. Functional MRI reveals the existence of modality and coordination-dependent timing networks. Neuroimage. 2005;25(4): 1031–42.PubMedCrossRefGoogle Scholar
  21. 21.
    Renoult L, Roux S, Riehle A. Time is a rubberband: Neuronal activity in monkey motor cortex in relation to time estimation. Eur J Neurosci. 2006;23(11):3098–108.PubMedCrossRefGoogle Scholar
  22. 22.
    Ivry RB, Spencer RM, Zelaznik HN, Diedrichsen J. The cerebellum and event timing. Ann N Y Acad Sci. 2002;978:302–17.PubMedCrossRefGoogle Scholar
  23. 23.
    Ito M. Bases and implications of learning in the cerebellum-adaptive control and internal model mechanism. Prog Brain Res. 2005;148:95–109.PubMedGoogle Scholar
  24. 24.
    Molinari M, Filippini V, Leggio MG. Neuronal plasticity of interrelated cerebellar and cortical networks. Neuroscience. 2002;111(4):863–70.PubMedCrossRefGoogle Scholar
  25. 25.
    Riecker A, Kassubek J, Groschel K, Grodd W, Ackermann H. The cerebral control of speech tempo: Opposite relationship between speaking rate and BOLD signal changes at striatal and cerebellar structures. Neuroimage. 2006;29(1):46–53.PubMedGoogle Scholar
  26. 26.
    Salman MS. The cerebellum: It’s about time! But timing is not everything-new insights into the role of the cerebellum in timing motor and cognitive tasks. J Child Neurol. 2002;17(1):1–9.PubMedCrossRefGoogle Scholar
  27. 27.
    Diener HC, Hore J, Ivry R, Dichgans J. Cerebellar dysfunction of movement and perception. Can J Neurological Sci. 1993;20[Suppl. 3]:S62–9.Google Scholar
  28. 28.
    McNaughton S, Timmann D, Watts S, Hore J. Overarm throwing speed in cerebellar subjects: Effect of timing of ball release. Exp Brain Res. 2004;154:470–8.PubMedCrossRefGoogle Scholar
  29. 29.
    Ivry RB, Keele SW, Diener HC. Dissociation of the lateral and medial cerebellum in movement timing and movement execution. Exp Brain Res. 1988;73(1):167–80.PubMedCrossRefGoogle Scholar
  30. 30.
    Molinari M, Leggio MG, Filippini V, Gioia MC, Cerasa A, Thaut MH. Sensorimotor transduction of time information is preserved in subjects with cerebellar damage. Brain Res Bull. 2005;67(6):448–58.PubMedCrossRefGoogle Scholar
  31. 31.
    Nawrot M, Rizzo M. Motion Perception deficits from midline cerebellar lesions in human. Vision Res. 1995;35(5):723–31.PubMedCrossRefGoogle Scholar
  32. 32.
    Spencer RM, Zelaznik HN, Diedrichsen J, Ivry RB. Disrupted timing of discontinous but not continuos movements by cerebellar lesions. Science. 2003;300:1437–9.PubMedCrossRefGoogle Scholar
  33. 33.
    Jueptner M, Flerich L, Weiller C, Mueller SP, Diener HC. The human cerebellum and temporal information processing results from a PET experiment. Neuroreport. 1996;7(15-17):2761–5.PubMedCrossRefGoogle Scholar
  34. 34.
    Penhune VB, Zattore RJ, Evans AC. Cerebellar contributions to motor timing: A PET study of auditory and visual rhythm reproduction. J Cogn Neurosci. 1998;10(6):752–65.PubMedCrossRefGoogle Scholar
  35. 35.
    Bower JM, Parsons LM. Rethinking the “lesser brain”. Sci Am. 2003;289(2):50–7.PubMedCrossRefGoogle Scholar
  36. 36.
    Rao SM, Mayer AR, Harrington DL. The evolution of brain activation during temporal processing. Nat Neurosci. 2001;4(3):317–23.PubMedCrossRefGoogle Scholar
  37. 37.
    Harrington DL, Lee RC, Boyd LA, Rapcsak SZ, Knight RT. Does the representation of time depend on the cerebellum? Effects of cerebellar stroke. Brain. 2004;127:561–74.PubMedCrossRefGoogle Scholar
  38. 38.
    Sanes JN, De Martin M, Weckelf J, Thaut MH. Brain activation patterns for producing symmetrically and asymmetrically synchronized movement rhythms. Neuroimage. 2001;13(6):1249.CrossRefGoogle Scholar
  39. 39.
    Parsons LM. Exploring the functional neruoanatomy of music performance, perception and comprehension. Ann N Y Acad Sci. 2001;930:211–29.PubMedGoogle Scholar
  40. 40.
    Stephan KM, Thaut MH, Schicks W, Wunderlich G, Tellmann L, Herzog H, et al. Cortico-cerebellar circuits and temporal adjustments of motor behaviour. Washington, DC: Society for Neuroscience, 2002. Online. Program 2002 Abstract Viewer/Itinerary Planner., No. 462.8, 2002.Google Scholar
  41. 41.
    Stephan KM, Thaut MH, Wunderlich G, Schicks W, Tian B, Tellmann L, et al. Conscious and subconscious sensorimotor synchronization-prefrontal cortex and the influence of awareness. Neuroimage. 2002; 15 (2): 345–52.PubMedCrossRefGoogle Scholar
  42. 42.
    Apps R, Garwicz M. Anatomical and physiological foundations of cerebellar information processing. Nat Rev Neurosci. 2005;6(4):297–311.PubMedCrossRefGoogle Scholar
  43. 43.
    Boyden ES, Katoh A, Raymond JL. Cerebellum-dependent learning: The role of multiple plasticity mechanisms. Ann Rev Neurosci. 2004;27(1):581–609.PubMedCrossRefGoogle Scholar
  44. 44.
    Cooke SF, Attwell PJE, Yeo CH. Temporal properties of cerebellar-dependent memory consolidation. J Neurosci. 2004;24(12):2934–41.PubMedCrossRefGoogle Scholar
  45. 45.
    Marr D. A theory of cerebellar cortex. J Physiol. 1969; 202(2):437–70.PubMedGoogle Scholar
  46. 46.
    Albus JS. A theory of cerebellar function. Math Biosci. 1971;10:25–61.CrossRefGoogle Scholar
  47. 47.
    Ito M. A new physiological concept on cerebellum. Rev Neurol. 1990;146(10):564–9.PubMedGoogle Scholar
  48. 48.
    Davidson PR, Wolpert DM. Motor learning and prediction in a variable environment. Curr Opin Neurobiol. 2003; 13 (2): 232–7.PubMedCrossRefGoogle Scholar
  49. 49.
    Wolpert DM, Miall RC, Kawato M. Internal models in the cerebellum. Trends Cognit Sci. 1998;2(9):338–47.CrossRefGoogle Scholar
  50. 50.
    Platel H, Price C, Baron JC, Wise R, Lambert J, Frackowiak RS, et al. The structural components of music perception. A functional anatomical study. Brain. 1997;120(2):229–43.PubMedCrossRefGoogle Scholar
  51. 51.
    Bower JM. Control of sensory data acquisition. Int Rev Neurobiol. 1997;41:489–513.PubMedGoogle Scholar
  52. 52.
    Parsons LM, Fox PT. Sensory and cognitive functions. Int Rev Neurobiol. 1997;41:255–71.PubMedCrossRefGoogle Scholar
  53. 53.
    Yarom Y, Cohen D. The olivocerebellar system as a generator of temporal patterns. Ann NY Acad Sci. 2002;978: 122–34.PubMedCrossRefGoogle Scholar
  54. 54.
    Andre P, Arrighi P. Hipnic modulation of cerebellar information processing: Implications for the cerebro-cerebellar dialogue. Cerebellum. 2003;2(2):84–95.PubMedCrossRefGoogle Scholar
  55. 55.
    Raymond JL, Lisberger SG, Mauk MD. The cerebellum: A neuronal learning machine. Science. 1996;272(5265): 1126–31.PubMedCrossRefGoogle Scholar

Copyright information

© Taylor & Francis 2007

Authors and Affiliations

  • Marco Molinari
    • 1
    Email author
  • Maria G. Leggio
    • 1
    • 2
  • Michael H. Thaut
    • 1
    • 3
  1. 1.Experimental Neurorehabilitation LabI.R.C.C.S. Santa Lucia FoundationRomeItaly
  2. 2.Department of PsychologyUniversity of Rome “La Sapienza”RomeItaly
  3. 3.Molecular, Cellular, and Integrative Neuroscience ProgramColorado State UniversityUSA

Personalised recommendations