Experimental Brain Research

, Volume 185, Issue 3, pp 399–409 | Cite as

Inference of complex human motion requires internal models of action: behavioral evidence

  • Ghislain SaunierEmail author
  • Charalambos Papaxanthis
  • Claudia D. Vargas
  • Thierry Pozzo
Research Article


Previous behavioral investigation from our laboratory (Pozzo et al. in Behav Brain Res 169:75–82, 2006) suggests that the kinematic features influence the subject’s capacity to estimate the final position of simple arm movement in which the last part of the trajectory is hidden. The authors argue the participation of internal information, as the kinematic parameters, to compensate the lack of the visual input. The purpose of this report was to verify if the dependency of visual motion inference to biological displays can be generalized for intransitive and complex human motions. To answer this question, the subjects were asked to estimate the vanishing and final position of the shoulder trajectory of Sit to Stand (STS) or Back to Sit (BTS) motion performed in the sagittal plane, according to a biological or nonbiological kinematics. The last part of the trajectory (i.e., 35%) was occluded. We observed a kinematic effect on the precision of individuals’ estimation. The subjects were more precise and less variable to estimate the end trajectory with biological velocity profiles. Moreover, impoverished visual information appeared sufficient to evaluate the final position of an intransitive complex human motion. These results suggest the participation of internal representations to infer the final part of complex motion. We discuss the results in the light of possible neural substrates involved during the inference task.


Motion inference Internal models Simulation Mirror neurons Complex intransitive motion 



This work was supported by CNES (Centre National d’Etudes Spatiales) and the Conseil Régional de Bourgogne, France. G. Saunier is supported by the French ministry of the Foreign Affairs (Collège Doctoral Franco-Brésilien).


  1. Actis-Grosso R, Stucchi N (2003) Shifting the start: backward mislocation of the initial position of a motion. J Exp Psychol Hum Percept Perform 29:675–691PubMedCrossRefGoogle Scholar
  2. Baker CI, Keysers C, Jellema T, Wicker B, Perrett DI (2001) Neuronal representation of disappearing and hidden objects in temporal cortex of the macaque. Exp Brain Res 140:375–381PubMedCrossRefGoogle Scholar
  3. Barnes GR, Barnes DM, Chakraborti SR (2000) Ocular pursuit responses to repeated, single-cycle sinusoids reveal behavior compatible with predictive pursuit. J Neurophysiol 84:2340–2355PubMedGoogle Scholar
  4. Buccino G, Binkofski F, Riggio L (2004) The mirror neuron system and action recognition. Brain Lang 89:370–376PubMedCrossRefGoogle Scholar
  5. Calvo-Merino B, Grezes J, Glaser DE, Passingham RE, Haggard P (2006) Seeing or doing? Influence of visual and motor familiarity in action observation. Curr Biol 16:1905–1910PubMedCrossRefGoogle Scholar
  6. Casile A, Giese MA (2006) Nonvisual motor training influences biological motion perception. Curr Biol 16:69–74PubMedCrossRefGoogle Scholar
  7. Chaminade T, Meary D, Orliaguet JP, Decety J (2001) Is perceptual anticipation a motor simulation? A PET study. Neuroreport 12:3669–3674PubMedCrossRefGoogle Scholar
  8. Cochin S, Barthelemy C, Roux S, Martineau J (1999) Observation and execution of movement: similarities demonstrated by quantified electroencephalography. Eur J Neurosci 11:1839–1842PubMedCrossRefGoogle Scholar
  9. Daprati E, Wriessnegger S, Lacquaniti F (2006) Kinematic cues and recognition of self-generated actions. Exp Brain Res (in press)Google Scholar
  10. Decety J, Grezes J, Costes N, Perani D, Jeannerod M, Procyk E, Grassi F, Fazio F (1997) Brain activity during observation of actions. Influence of action content and subject’s strategy. Brain 120(Pt 10):1763–1777PubMedCrossRefGoogle Scholar
  11. De Valois RL, De Valois KK (1991) Vernier acuity with stationary moving Gabors. Vision Res 31:1619–1626PubMedCrossRefGoogle Scholar
  12. di Pellegrino G, Fadiga L, Fogassi L, Gallese V, Rizzolatti G (1992) Understanding motor events: a neurophysiological study. Exp Brain Res 91:176–180PubMedCrossRefGoogle Scholar
  13. Erlhagen W (2003) Internal models for visual perception. Biol Cyber 88:409–417CrossRefGoogle Scholar
  14. Fadiga L, Fogassi L, Gallese V, Rizzolatti G (2000) Visuomotor neurons: ambiguity of the discharge or ‘motor’ perception? Int J Psychophysiol 35:165–177PubMedCrossRefGoogle Scholar
  15. Fadiga L, Fogassi L, Pavesi G, Rizzolatti G (1995) Motor facilitation during action observation: a magnetic stimulation study. J Neurophysiol 73:2608–2611PubMedGoogle Scholar
  16. Fadiga L, Craighero L, Olivier E (2005) Human motor cortex excitability during the perception of others’ action Curr Opin Neurobiol 15:213–218PubMedCrossRefGoogle Scholar
  17. Gallese V, Fadiga L, Fogassi L, Rizzolatti G (1996) Action recognition in the premotor cortex. Brain 119:593–609PubMedCrossRefGoogle Scholar
  18. Gangitano M, Mottaghy FM, Pascual-Leone A (2001) Phase-specific modulation of cortical motor output during movement observation. Neuroreport 12:1489–1492PubMedCrossRefGoogle Scholar
  19. Gangitano M, Mottaghy FM, Pascual-Leone A (2004) Modulation of premotor mirror neuron activity during observation of unpredictable grasping movements. Eur J Neurosci 20:2193–2202PubMedCrossRefGoogle Scholar
  20. Giorello G, Sinigaglia C (2007) Perception in action. Acta Biomed 78:49–57PubMedGoogle Scholar
  21. Graf M, Reitzner B, Corves C, Casile A, Giese M, Prinz W (2007) Predicting point-light actions in real-time. Neuroimage 36:22–32CrossRefGoogle Scholar
  22. Grezes J, Fonlupt P, Bertenthal B, Delon-Martin C, Segebarth C, Decety J (2001) Does perception of biological motion rely on specific brain regions? Neuroimage 13:775–785PubMedCrossRefGoogle Scholar
  23. Grossman ED, Blake R (2001) Brain activity evoked by inverted and imagined biological motion. Vision Res 41:1475–1482PubMedCrossRefGoogle Scholar
  24. Hari R, Forss N, Avikainen S, Kirveskari E, Salenius S, Rizzolatti G (1998) Activation of human primary motor cortex during action observation: a neuromagnetic study. Proc Natl Acad Sci USA 95:15061–15065PubMedCrossRefGoogle Scholar
  25. Iacoboni M (2005) Neural mechanisms of imitation. Curr Opin Neurobiol 15:632–637PubMedCrossRefGoogle Scholar
  26. Indovina I, Maffei V, Bosco G, Zago M, Macaluso E, Lacquaniti F (2005) Representation of visual gravitational motion in the human vestibular cortex. Science 308:416–419PubMedCrossRefGoogle Scholar
  27. Jeannerod M (1994) The representing brain: neural correlates of motor intention and imagery. Behav Brain Sci 17:187–245CrossRefGoogle Scholar
  28. Jeannerod M (2001) Neural simulation of action: a unifying mechanism for motor cognition. NeuroImage 14:103–109CrossRefGoogle Scholar
  29. Kalaska JF, Cohen DA, Prud’homme M, Hyde ML (1990) Parietal area 5 neuronal activity encodes movement kinematics, not movement dynamics. Exp Brain Res 80:351–364PubMedCrossRefGoogle Scholar
  30. Kao GW, Morrow MJ (1994) The relationship of anticipatory smooth eye movement to smooth pursuit initiation. Vision Res 34:3027–3036PubMedCrossRefGoogle Scholar
  31. Kerzel D, Jordan JS, Musseler J (2001) The role of perception in the mislocalization of the final position of a moving target. J Exp Psychol Hum Percept Perform 27:829–840PubMedCrossRefGoogle Scholar
  32. Kilner JM, Hamilton AF, Blakemore SJ (2007) Interference effect of observed human movement on action is due to velocity profile of biological motion. Social Neurosci 2:158–166CrossRefGoogle Scholar
  33. Knoblich G, Flach R (2001) Predicting the effects of actions: interactions of perception and action. Psychol Sci 12:467–472PubMedCrossRefGoogle Scholar
  34. Mataric MJ, Pomplun M (1998) Fixation behavior in observation and imitation of human movement. Cogn Brain Res 7:191–202CrossRefGoogle Scholar
  35. McIntyre J, Zago M, Berthoz A, Lacquaniti F (2001) Does the brain model Newton’s laws? Nat Neurosci 4:693–694PubMedCrossRefGoogle Scholar
  36. Miall RC (2003) Connecting mirror neurons and forward models. Neuroreport 14:2135–2137PubMedCrossRefGoogle Scholar
  37. Miall RC, Wolpert DM (1996) Forward models for physiological motor control. Neural Networks 9:1265–1279PubMedCrossRefGoogle Scholar
  38. Mitrani L, Dimitrov G (1978) Pursuit eye movements of a disappearing moving target. Vision Res 18:537–539PubMedCrossRefGoogle Scholar
  39. Mitrani L, Dimitrov G, Yakimoff N, Mateeff S (1979) Oculomotor and perceptual localization during smooth eye movements. Vision Res 19:609–612PubMedCrossRefGoogle Scholar
  40. Mourey F, Pozzo T, Rouhier-Marcer I, Didier JP (1998) A kinematic comparison between elderly and young subjects standing up from and sitting down in a chair. Age Ageing 27:137–146PubMedCrossRefGoogle Scholar
  41. Mrotek LA, Flanders M, Soechting JF (2006) Oculomotor responses to gradual changes in target direction. Exp Brain Res 172:175–192PubMedCrossRefGoogle Scholar
  42. Nijhawan R (1994) Motion extrapolation in catching. Nature 370:256–257PubMedCrossRefGoogle Scholar
  43. Oztop E, Kawato M, Arbib MA (2006) Mirror neurons and imitation: a computationally guided review. Neural Networks 19:254–271PubMedCrossRefGoogle Scholar
  44. Oztop E, Wolpert DM, Kawato M (2005) Mental state inference using visual control parameters. Cogn Brain Res 22:129–151CrossRefGoogle Scholar
  45. Papaxanthis C, Dubost V, Pozzo T (2003a) Similar planning strategies for whole-body and arm movements performed in the sagittal plane. Neuroscience 117:779–783PubMedCrossRefGoogle Scholar
  46. Papaxanthis C, Pozzo T, McIntyre J (2005) Kinematic and dynamic processes for the control of pointing movements in humans revealed by short-term exposure to microgravity. Neuroscience 135:371–383PubMedCrossRefGoogle Scholar
  47. Papaxanthis C, Pozzo T, Schieppati M (2003b) Trajectories of arm pointing movements on the sagittal plane vary with both direction and speed. Exp Brain Res 148:498–503PubMedGoogle Scholar
  48. Papaxanthis C, Pozzo T, Stapley P (1998) Effects of movement direction upon kinematic characteristics of vertical arm pointing movements in man. Neuroscience Letters 253:103–106PubMedCrossRefGoogle Scholar
  49. Patton JL, Lee WA, Pai YC (2000) Relative stability improves with experience in a dynamic standing task. Exp Brain Res 135:117–126PubMedCrossRefGoogle Scholar
  50. Pozzo T, Papaxanthis C, Petit JL, Schweighofer N, Stucchi N (2006) Kinematic features of movement tunes perception and action coupling. Behav Brain Res 169:75–82PubMedCrossRefGoogle Scholar
  51. Pozzo T, Papaxanthis C, Stapley P, Berthoz A (1998) The sensorimotor and cognitive integration of gravity. Brain Res Brain Res Rev 28:92–101PubMedCrossRefGoogle Scholar
  52. Prinz W (1997) Perception and action planning. Eur J Cogn Psychol 9:129–154CrossRefGoogle Scholar
  53. Puce A, Syngeniotis A, Thompson JC, Abbott DF, Wheaton KJ, Castiello U (2003) The human temporal lobe integrates facial form and motion: evidence from fMRI and ERP studies. Neuroimage 19:861–869PubMedCrossRefGoogle Scholar
  54. Rizzolatti G (2005) The mirror neuron system and its function in humans. Anat Embryol (Berl) 210:419–421CrossRefGoogle Scholar
  55. Rizzolatti G, Craighero L (2004) The mirror-neuron system. Annu Rev Neurosci 27:169–192PubMedCrossRefGoogle Scholar
  56. Rizzolatti G, Fadiga L, Fogassi L, Gallese V (2002) From mirror neurons to imitation: facts and speculations. In: Meltzoff AN, Prinz W (eds) The imitative mind: development, evolution, and brain bases. Cambridge University Press, New York, pp 247–266Google Scholar
  57. Rizzolatti G, Fadiga L, Gallese V, Fogassi L (1996) Premotor cortex and the recognition of motor actions. Cogn Brain Res 3:131–141CrossRefGoogle Scholar
  58. Rizzolatti G, Luppino G (2001) The cortical motor system. Neuron 31:889–901PubMedCrossRefGoogle Scholar
  59. Rizzolatti G, Luppino G, Matelli M (1998) The organization of the cortical motor system: new concepts. Electroencephalogr Clin Neurophysiol 106:283–296PubMedCrossRefGoogle Scholar
  60. Saygin AP, Wilson SM, Hagler Jr DJ, Bates E, Sereno MI (2004) Point-light biological motion perception activates human premotor cortex. J Neurosci 24:6181–6188PubMedCrossRefGoogle Scholar
  61. Tai YF, Scherfler C, Brooks DJ, Sawamoto N, Castiello U (2004) The human premotor cortex is ‘mirror’ only for biological actions. Curr Biol 14:117–120PubMedCrossRefGoogle Scholar
  62. Thompson JC, Clarke M, Stewart T, Puce A (2005) Configural processing of biological motion in human superior temporal sulcus. J Neurosci 25:9059–9066PubMedCrossRefGoogle Scholar
  63. Umiltà MA, Kohler E, Gallese V, Fogassi L, Fadiga L, Keysers C, Rizzolatti G (2001) I know what are you doing: a neurophysiological study. Neuron 31:155–165PubMedCrossRefGoogle Scholar
  64. Vaina LM, Solomon J, Chowdhury S, Sinha P, Belliveau JW (2001) Functional neuroanatomy of biological motion perception in humans. Proc Natl Acad Sci USA 98:11656–11661PubMedCrossRefGoogle Scholar
  65. Verfaillie K, Daems A (2002) Representing and anticipating human actions in vision. Visual Cogn 9:217–232CrossRefGoogle Scholar
  66. Viviani P, Stucchi N (1992) Biological movements look uniform: evidence of motor-perceptual interactions. J Exp Psychol Hum Percept Perform 18:603–623PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2007

Authors and Affiliations

  • Ghislain Saunier
    • 1
    • 3
    Email author
  • Charalambos Papaxanthis
    • 1
    • 2
  • Claudia D. Vargas
    • 3
  • Thierry Pozzo
    • 1
    • 2
    • 4
  1. 1.INSERM-U887, Motricité-PlasticitéCampus UniversitaireDijonFrance
  2. 2.UFRSTAPS Campus UniversitaireUniversité de BourgogneDijonFrance
  3. 3.Laboratório de Neurobiologia II, Instituto de Biofísica Carlos Chagas FilhoUniversidade Federal de Rio de JaneiroRio de JaneiroBrazil
  4. 4.Italian Institute of TechnologyGenovaItaly

Personalised recommendations