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.

  • Letter
  • Published:

Action plans used in action observation

Abstract

How do we understand the actions of others? According to the direct matching hypothesis, action understanding results from a mechanism that maps an observed action onto motor representations of that action1,2,3,4. Although supported by neurophysiological1,5,6,7,8,9,10,11,12,13 and brain-imaging3,14,15,16,17,18 studies, direct evidence for this hypothesis is sparse. In visually guided actions, task-specific proactive eye movements are crucial for planning and control19,20,21,22. Because the eyes are free to move when observing such actions, the direct matching hypothesis predicts that subjects should produce eye movements similar to those produced when they perform the tasks. If an observer analyses action through purely visual means, however, eye movements will be linked reactively to the observed action. Here we show that when subjects observe a block stacking task, the coordination between their gaze and the actor's hand is predictive, rather than reactive, and is highly similar to the gaze–hand coordination when they perform the task themselves. These results indicate that during action observation subjects implement eye motor programs directed by motor representations of manual actions and thus provide strong evidence for the direct matching hypothesis.

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

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

Figure 1: Gaze–hand coordination in action and action observation.
Figure 2: Gaze behaviour in the block observation task.

Similar content being viewed by others

References

  1. Gallese, V., Fadiga, L., Fogassi, L. & Rizzolatti, G. Action recognition in the premotor cortex. Brain 119, 593–609 (1996)

    Article  Google Scholar 

  2. Rizzolatti, G., Fadiga, L., Gallese, V. & Fogassi, L. Premotor cortex and the recognition of motor actions. Brain Res. Cogn. Brain Res. 3, 131–141 (1996)

    Article  CAS  Google Scholar 

  3. Iacoboni, M. et al. Cortical mechanisms of human imitation. Science 286, 2526–2528 (1999)

    Article  CAS  Google Scholar 

  4. Rizzolatti, G., Fogassi, L. & Gallese, V. Neurophysiological mechanisms underlying the understanding and imitation of action. Nature Rev. Neurosci. 2, 661–670 (2001)

    Article  CAS  Google Scholar 

  5. di Pellegrino, G., Fadiga, L., Fogassi, L., Gallese, V. & Rizzolatti, G. Understanding motor events: a neurophysiological study. Exp. Brain Res. 91, 176–180 (1992)

    Article  CAS  Google Scholar 

  6. Fadiga, L., Fogassi, L., Pavesi, G. & Rizzolatti, G. Motor facilitation during action observation: a magnetic stimulation study. J. Neurophysiol. 73, 2608–2611 (1995)

    Article  CAS  Google Scholar 

  7. Hari, R. et al. Activation of human primary motor cortex during action observation: a neuromagnetic study. Proc. Natl Acad. Sci. USA 95, 15061–15065 (1998)

    Article  ADS  CAS  Google Scholar 

  8. Nishitani, N. & Hari, R. Temporal dynamics of cortical representation for action. Proc. Natl Acad. Sci. USA 97, 913–918 (2000)

    Article  ADS  CAS  Google Scholar 

  9. Strafella, A. P. & Paus, T. Modulation of cortical excitability during action observation: a transcranial magnetic stimulation study. NeuroReport 11, 2289–2292 (2000)

    Article  CAS  Google Scholar 

  10. Gangitano, M., Mottaghy, F. M. & Pascual-Leone, A. Phase-specific modulation of cortical motor output during movement observation. NeuroReport 12, 1489–1492 (2001)

    Article  CAS  Google Scholar 

  11. Umiltà, M. A. et al. I know what you are doing: a neurophysiological study. Neuron 31, 155–165 (2001)

    Article  Google Scholar 

  12. Avikainen, S., Forss, N. & Hari, R. Modulated activation of the human SI and SII cortices during observation of hand actions. NeuroImage 15, 640–646 (2002)

    Article  Google Scholar 

  13. Kohler, E. et al. Hearing sounds, understanding actions: action representation in mirror neurons. Science 297, 846–848 (2002)

    Article  ADS  CAS  Google Scholar 

  14. Grafton, S. T., Arbib, M. A., Fadiga, L. & Rizzolatti, G. Localization of grasp representations in humans by positron emission tomography. 2. Observation compared with imagination. Exp. Brain Res. 112, 103–111 (1996)

    Article  CAS  Google Scholar 

  15. Rizzolatti, G. et al. Localization of grasp representations in humans by PET: 1. Observation versus execution. Exp. Brain Res. 111, 246–252 (1996)

    Article  CAS  Google Scholar 

  16. Decety, J. et al. Brain activity during observation of actions. Influence of action content and subject's strategy. Brain 120, 1763–1777 (1997)

    Article  Google Scholar 

  17. Iacoboni, M. et al. Reafferent copies of imitated actions in the right superior temporal cortex. Proc. Natl Acad. Sci. USA 98, 13995–13999 (2001)

    Article  ADS  CAS  Google Scholar 

  18. Koski, L. et al. Modulation of motor and premotor activity during imitation of target-directed actions. Cereb. Cortex 12, 847–855 (2002)

    Article  Google Scholar 

  19. Land, M. F. & Furneaux, S. The knowledge base of the oculomotor system. Phil. Trans. R. Soc. Lond. Biol. 352, 1231–1239 (1997)

    Article  ADS  CAS  Google Scholar 

  20. Land, M., Mennie, N. & Rusted, J. The roles of vision and eye movements in the control of activities of daily living. Perception 28, 1311–1328 (1999)

    Article  CAS  Google Scholar 

  21. Land, M. F. & McLeod, P. From eye movements to actions: how batsmen hit the ball. Nature Neurosci. 3, 1340–1345 (2000)

    Article  CAS  Google Scholar 

  22. Johansson, R. S., Westling, G., Bäckström, A. & Flanagan, J. R. Eye-hand coordination in object manipulation. J. Neurosci. 21, 6917–6932 (2001)

    Article  CAS  Google Scholar 

  23. Ballard, D. H., Hayhoe, M. M., Li, F. & Whitehead, S. D. Hand-eye coordination during sequential tasks. Phil. Trans. R. Soc. Lond. Biol. 337, 331–338 (1992)

    Article  ADS  CAS  Google Scholar 

  24. Ballard, D. H., Hayhoe, M. M. & Pelz, J. B. Memory representations in natural tasks. J. Cogn. Neurosci. 7, 66–80 (1995)

    Article  CAS  Google Scholar 

  25. Becker, W., (ed. Carpenter, R. H. S.)) 95–137 (Macmillan, London, 1991)

  26. Rizzolatti, G., Fadiga, L., Fogassi, L. & Gallese, V. Resonance behaviors and mirror neurons. Arch. Ital. Biol. 137, 85–100 (1999)

    CAS  PubMed  Google Scholar 

  27. Perrett, D. I. et al. Frameworks of analysis for the neural representation of animate objects and actions. J. Exp. Biol. 6, 87–113 (1989)

    Google Scholar 

  28. Allison, T., Puce, A. & McCarthy, G. Social perception from visual cues: role of the STS region. Trends Cogn. Sci. 4, 267–278 (2000)

    Article  CAS  Google Scholar 

  29. Johansson, R. S. & Cole, K. J. Sensory-motor coordination during grasping and manipulative actions. Curr. Opin. Neurobiol. 2, 815–823 (1992)

    Article  CAS  Google Scholar 

  30. Mataric, M. J. & Pomplun, M. Fixation behavior in observation and imitation of human movement. Brain Res. Cogn. Brain Res. 7, 191–202 (1998)

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We thank G. Westling and A. Bäckström for engineering and software support. This study was supported by the Canadian Institutes of Health Research, the Swedish Medical Research Council, the Göran Gustafsson Foundation for Research in Natural Sciences and Medicine, and the 5th Framework Program of European Union.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to J. Randall Flanagan.

Ethics declarations

Competing interests

The authors declare that they have no competing financial interests.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Flanagan, J., Johansson, R. Action plans used in action observation. Nature 424, 769–771 (2003). https://doi.org/10.1038/nature01861

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nature01861

This article is cited by

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.

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