Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Article
  • Published:

Central cancellation of self-produced tickle sensation

Nature Neuroscience volume 1, pages 635–640 (1998)Cite this article

Abstract

A self-produced tactile stimulus is perceived as less ticklish than the same stimulus generated externally. We used fMRI to examine neural responses when subjects experienced a tactile stimulus that was either self-produced or externally produced. More activity was found in somatosensory cortex when the stimulus was externally produced. In the cerebellum, less activity was associated with a movement that generated a tactile stimulus than with a movement that did not. This difference suggests that the cerebellum is involved in predicting the specific sensory consequences of movements, providing the signal that is used to cancel the sensory response to self-generated stimulation.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Figure 1: Diagram of experimental set-up.
Figure 2: Areas of activation in the main effects of movement and tactile stimuli.
Figure 3
Figure 4: Significantly decreased activity (p < 0.05, corrected for multiple comparisons) in bilateral secondary somatosensory cortex associated with the interaction between the effects of self-generated movement and tactile stimulation.
Figure 5: Significantly decreased activity (p < 0.05, corrected for multiple comparisons) in right anterior cerebellar cortex associated with the interaction between the effects of self-generated movement and tactile stimulation.
Figure 6: Significantly decreased activity (p < 0.05 corrected for multiple comparisons) in anterior cingulate cortex associated with the interaction between the effects of self-generated movement and tactile stimulation.

Similar content being viewed by others

References

  1. Decety, J. Neural representation for action. Rev. Neurosci. 7, 285–297 (1996).

    Article  CAS  Google Scholar 

  2. Jeannerod, M. The Neural and Behaviourial Organisation of Goal-Directed Movements (Oxford Univ. Press, 1988).

  3. Jeannerod, M. The Cognitive Neuroscience of Action (Blackwell, Cambridge, 1997).

    Google Scholar 

  4. Wolpert, D. M., Ghahramani, Z. & Jordan, M. I. An internal model for sensorimotor integration. Science 269, 1880–1882 ( 1995).

    Article  CAS  Google Scholar 

  5. Wolpert, D. M. Computational approaches to motor control. Trends Cog. Sci. 1, 209–216 (1997).

    Article  CAS  Google Scholar 

  6. Frith, C. D. The Cognitive Neuropsychology of Schizophrenia (Lawrence Erlbaum, Hove, UK, 1992).

    Google Scholar 

  7. Von Holst, E. Relations between the central nervous system and the peripheral organs. Brit. J. Anim. Behav. 2, 89–94 (1954).

    Article  Google Scholar 

  8. Sperry, R. W. Neural basis of spontaneous optokinetic responses produced by visual inversion. J. Comp. Physiol. Psychol. 43, 482– 489 (1950).

    Article  CAS  Google Scholar 

  9. Weiskrantz, L., Elliot, J. & Darlington, C. Preliminary observations of tickling oneself. Nature 230, 598–599 ( 1971).

    Article  CAS  Google Scholar 

  10. Claxton, G. Why can't we tickle ourselves? Percept. Motor Skills 41, 335–338 (1975).

    Article  CAS  Google Scholar 

  11. Chapin, J. K. & Woodward, D. J. Somatic sensory transmission to the cortex during movement: gating of single cell responses to touch. Exp. Neurol. 78, 654–669 (1982).

    Article  CAS  Google Scholar 

  12. Jiang, W., Chapman, C. E. & Lamarre, Y. Modulation of the cutaneous responsiveness of neurones in the primary somatosensory cortex during conditioned arm movements in the monkey. Exp. Brain Res. 84, 342– 354 (1991).

    Article  CAS  Google Scholar 

  13. Chapman, C. E. Active versus passive touch: factors influencing the transmission of somatosensory signals to primary somatosensory cortex. Can. J. Physiol. Pharmacol . 72, 558–570 ( 1994).

    Article  CAS  Google Scholar 

  14. Ito, M. Neurophysiological aspects of the cerebellar motor control system. Int. J. Neurol. 7, 162–176 ( 1970).

    CAS  PubMed  Google Scholar 

  15. Paulin, M. G. in Dynamic Interactions in Neural Networks: Models and Data (eds Arbib, E. M. A. & Amari, E. S.) 241–259 (Springer, 1989).

  16. Miall, R. C., Weir, D. J., Wolpert, D. M. & Stein, J. F. Is the cerebellum a Smith predictor? J. Motor Behav. 25, 203–216 (1993).

    Article  CAS  Google Scholar 

  17. Wolpert, D. M., Miall, R. C. & Kawato, M. Internal models in the cerebellum. Trends Cog. Sci. 2, 338–347 ( 1998).

    Article  CAS  Google Scholar 

  18. Oscarsson, O. in The Inferior Olivary Nucleus: Anatomy and Physiology (eds Courville, J., DeMontigny, C. & Lamarre, Y) 279– 289 (Raven, New York, 1980).

  19. Gellman, R., Gibson, A. R. & Houk, J. C. Inferior olivary neurons in the awake cat: detection of contact and passive body displacement. J. Neurophysiol. 54, 40–60 (1985).

    Article  CAS  Google Scholar 

  20. Andersson, G. & Armstrong, D. M. Climbing fibre input to b zone Purkinje cells during locomotor perturbation in the cat. Neurosci. Lett. Supp. 22, S27 (1985).

  21. Andersson, G. & Armstrong, D. M. Complex spikes in Purkinje cells in the lateral vermis of the cat cerebellum during locomotion. J. Physiol. (Lond.) 385, 107–134 (1987).

    Article  CAS  Google Scholar 

  22. Simpson, J. L., Wylie, D. R. & De Zeeuw, C. I. On climbing fiber signals and their consequence(s) Brain Behav. Sci. 19, 368– 383 (1995).

    Google Scholar 

  23. Morrissette, J. & Bower, J. M. Contribution of somatosensory cortex to responses in the rat cerebellar granule cell layer following peripheral tactile stimulation. Exp. Brain Res. 109, 240–250 (1996).

    Article  Google Scholar 

  24. Leiner, H. C., Leiner, A. L. & Dow, R. S. The underestimated cerebellum. Hum. Brain Mapp. 2, 244–254 ( 1995).

    Article  Google Scholar 

  25. Gao, J-H et al. Cerebellum implicated in sensory acquisition and discrimination rather than motor control. Science 272, 545–546 (1996).

    Article  CAS  Google Scholar 

  26. Bower, J. M. Is the cerebellum sensory for motor's sake, or motor for sensory's sake: the view from the whiskers of a rat? Prog. Brain Res. 114 , 463–496 (1997).

    Article  CAS  Google Scholar 

  27. Bower, J. M. Control of sensory data acquisition. Int. Rev. Neurobiol. 41, 489–513 (1997).

    Article  CAS  Google Scholar 

  28. Deiber, M.-P. et al. Cortical areas and the selection of movement: a study with positron emission tomography. Exp. Brain Res. 84, 393–402 (1991).

    Article  CAS  Google Scholar 

  29. Frith, C. D., Friston, K. J., Liddle, P. F. & Frackowiak, R. S. J. Willed action and the prefrontal cortex in man: a study with PET. Proc. R. Soc. Lond. B Biol. Sci. 244, 241– 246 (1991).

    Article  CAS  Google Scholar 

  30. Paulesu, E., Frackowiak, R. S. J. & Bottini, G. in Human Brain Function (eds Frackowiak, R. S. J., Friston, K. J., Frith, C. D., Dolan, R. J. & Mazziotta, J. C.) 183–242 (Academic, San Diego,California 1997).

  31. Krubitzer, L., Clarrey, J., Tweedale, R., Elston, G. & Calford, M. A redefinition of somatosensory areas in the lateral sulcus of macaque monkeys. J. Neurosci. 15, 3821–3839 (1995).

    Article  CAS  Google Scholar 

  32. Jansma, J. M., Ramsey, N. F. & Kahn, R. S. Tactile stimulation during finger opposition does not contribute to 3D fMRI brain activity pattern. Neuroreport 9, 501–505 (1998).

    CAS  PubMed  Google Scholar 

  33. Vogt, B. A., Finch, D. M. & Olson, C. R. Functional heterogeneity in cingulate cortex: the anterior executive and posterior evaluative regions. Cereb. Cortex 2, 435–443 ( 1992).

    CAS  PubMed  Google Scholar 

  34. Vogt, B. A. & Gabriel, M. eds Neurobiology of Cingulate Cortex and Limbic Thalamus (Birkauser, Boston, 1993).

    Book  Google Scholar 

  35. Coghill, R. C. et al. Distributed processing of pain and vibration by the human brain. J. Neurosci. 14, 4095– 4108 (1994).

    Article  CAS  Google Scholar 

  36. Porrino, L. J. Functional consequences of acute cocaine treatment depend on route of administration. Psychopharmacol. Berl. 112, 343– 351 (1993).

    Article  CAS  Google Scholar 

  37. Friston K. J. et al. Spatial registration and normalization of images. Hum. Brain Mapp. 3, 165–189 (1995).

    Article  Google Scholar 

  38. Talairach, J & Tournoux, P. Co-Planar Stereotaxic Atlas of the Human Brain (Thieme, New York, 1988).

    Google Scholar 

  39. Friston, K. J. et al. The relationship between global and local changes in PET scans. J. Cereb. Blood Flow Metab. 10, 458– 466 (1990).

    Article  CAS  Google Scholar 

  40. Friston, K. J. et al. Statistical parametric maps in functional imaging: a general linear approach. Hum. Brain Mapp. 2, 189 –210 (1995).

    Article  Google Scholar 

  41. Friston, K. J. in Human Brain Function (eds Frackowiak, R. S. J., Friston, K. J., Frith, C. D., Dolan, R. J. & Mazziotta, J. C.) 107– 126 (Academic, San Diego, California, 1997).

    Google Scholar 

Download references

Acknowledgements

We thank Richard Perry and Richard Frackowiak for comments, and the radiographers at the Wellcome Department for Cognitive Neurology for their help. This work was supported by the Wellcome Trust. S.-J.B. is supported by a Wellcome Trust four-year Ph.D. Programme in Neuroscience at University College London.

Author information

Authors and Affiliations

  1. Wellcome Department of Cognitive Neurology, 12 Queen Square , London, WC1N 3BG, UK

    Sarah-J. Blakemore & Chris D. Frith

  2. Sobell Department, Institute of Neurology, Queen Square, London, WC1N 3BG, UK

    Sarah-J. Blakemore & Daniel M. Wolpert

Authors
  1. Sarah-J. Blakemore
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Daniel M. Wolpert
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Chris D. Frith
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Sarah-J. Blakemore.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Blakemore, SJ., Wolpert, D. & Frith, C. Central cancellation of self-produced tickle sensation. Nat Neurosci 1, 635–640 (1998). https://doi.org/10.1038/2870

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1038/2870

This article is cited by

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing