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

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Abstract

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.

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References

  • Actis-Grosso R, Stucchi N (2003) Shifting the start: backward mislocation of the initial position of a motion. J Exp Psychol Hum Percept Perform 29:675–691

    Article  PubMed  Google Scholar 

  • 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 140:375–381

    Article  PubMed  CAS  Google Scholar 

  • Barnes GR, Barnes DM, Chakraborti SR (2000) Ocular pursuit responses to repeated, single-cycle sinusoids reveal behavior compatible with predictive pursuit. J Neurophysiol 84:2340–2355

    PubMed  CAS  Google Scholar 

  • Buccino G, Binkofski F, Riggio L (2004) The mirror neuron system and action recognition. Brain Lang 89:370–376

    Article  PubMed  Google Scholar 

  • 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 16:1905–1910

    Article  PubMed  CAS  Google Scholar 

  • Casile A, Giese MA (2006) Nonvisual motor training influences biological motion perception. Curr Biol 16:69–74

    Article  PubMed  CAS  Google Scholar 

  • Chaminade T, Meary D, Orliaguet JP, Decety J (2001) Is perceptual anticipation a motor simulation? A PET study. Neuroreport 12:3669–3674

    Article  PubMed  CAS  Google Scholar 

  • Cochin S, Barthelemy C, Roux S, Martineau J (1999) Observation and execution of movement: similarities demonstrated by quantified electroencephalography. Eur J Neurosci 11:1839–1842

    Article  PubMed  CAS  Google Scholar 

  • Daprati E, Wriessnegger S, Lacquaniti F (2006) Kinematic cues and recognition of self-generated actions. Exp Brain Res (in press)

  • 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):1763–1777

    Article  PubMed  Google Scholar 

  • De Valois RL, De Valois KK (1991) Vernier acuity with stationary moving Gabors. Vision Res 31:1619–1626

    Article  PubMed  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Erlhagen W (2003) Internal models for visual perception. Biol Cyber 88:409–417

    Article  Google Scholar 

  • Fadiga L, Fogassi L, Gallese V, Rizzolatti G (2000) Visuomotor neurons: ambiguity of the discharge or ‘motor’ perception? Int J Psychophysiol 35:165–177

    Article  PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Fadiga L, Craighero L, Olivier E (2005) Human motor cortex excitability during the perception of others’ action Curr Opin Neurobiol 15:213–218

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Gangitano M, Mottaghy FM, Pascual-Leone A (2001) Phase-specific modulation of cortical motor output during movement observation. Neuroreport 12:1489–1492

    Article  PubMed  CAS  Google Scholar 

  • Gangitano M, Mottaghy FM, Pascual-Leone A (2004) Modulation of premotor mirror neuron activity during observation of unpredictable grasping movements. Eur J Neurosci 20:2193–2202

    Article  PubMed  Google Scholar 

  • Giorello G, Sinigaglia C (2007) Perception in action. Acta Biomed 78:49–57

    PubMed  Google Scholar 

  • Graf M, Reitzner B, Corves C, Casile A, Giese M, Prinz W (2007) Predicting point-light actions in real-time. Neuroimage 36:22–32

    Article  Google Scholar 

  • 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 13:775–785

    Article  PubMed  CAS  Google Scholar 

  • Grossman ED, Blake R (2001) Brain activity evoked by inverted and imagined biological motion. Vision Res 41:1475–1482

    Article  PubMed  CAS  Google Scholar 

  • 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 95:15061–15065

    Article  PubMed  CAS  Google Scholar 

  • Iacoboni M (2005) Neural mechanisms of imitation. Curr Opin Neurobiol 15:632–637

    Article  PubMed  CAS  Google Scholar 

  • Indovina I, Maffei V, Bosco G, Zago M, Macaluso E, Lacquaniti F (2005) Representation of visual gravitational motion in the human vestibular cortex. Science 308:416–419

    Article  PubMed  CAS  Google Scholar 

  • Jeannerod M (1994) The representing brain: neural correlates of motor intention and imagery. Behav Brain Sci 17:187–245

    Article  Google Scholar 

  • Jeannerod M (2001) Neural simulation of action: a unifying mechanism for motor cognition. NeuroImage 14:103–109

    Article  Google Scholar 

  • Kalaska JF, Cohen DA, Prud’homme M, Hyde ML (1990) Parietal area 5 neuronal activity encodes movement kinematics, not movement dynamics. Exp Brain Res 80:351–364

    Article  PubMed  CAS  Google Scholar 

  • Kao GW, Morrow MJ (1994) The relationship of anticipatory smooth eye movement to smooth pursuit initiation. Vision Res 34:3027–3036

    Article  PubMed  CAS  Google Scholar 

  • 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 27:829–840

    Article  PubMed  CAS  Google Scholar 

  • 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 2:158–166

    Article  Google Scholar 

  • Knoblich G, Flach R (2001) Predicting the effects of actions: interactions of perception and action. Psychol Sci 12:467–472

    Article  PubMed  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • McIntyre J, Zago M, Berthoz A, Lacquaniti F (2001) Does the brain model Newton’s laws? Nat Neurosci 4:693–694

    Article  PubMed  CAS  Google Scholar 

  • Miall RC (2003) Connecting mirror neurons and forward models. Neuroreport 14:2135–2137

    Article  PubMed  CAS  Google Scholar 

  • Miall RC, Wolpert DM (1996) Forward models for physiological motor control. Neural Networks 9:1265–1279

    Article  PubMed  Google Scholar 

  • Mitrani L, Dimitrov G (1978) Pursuit eye movements of a disappearing moving target. Vision Res 18:537–539

    Article  PubMed  CAS  Google Scholar 

  • Mitrani L, Dimitrov G, Yakimoff N, Mateeff S (1979) Oculomotor and perceptual localization during smooth eye movements. Vision Res 19:609–612

    Article  PubMed  CAS  Google Scholar 

  • 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 27:137–146

    Article  PubMed  CAS  Google Scholar 

  • Mrotek LA, Flanders M, Soechting JF (2006) Oculomotor responses to gradual changes in target direction. Exp Brain Res 172:175–192

    Article  PubMed  Google Scholar 

  • Nijhawan R (1994) Motion extrapolation in catching. Nature 370:256–257

    Article  PubMed  CAS  Google Scholar 

  • Oztop E, Kawato M, Arbib MA (2006) Mirror neurons and imitation: a computationally guided review. Neural Networks 19:254–271

    Article  PubMed  Google Scholar 

  • Oztop E, Wolpert DM, Kawato M (2005) Mental state inference using visual control parameters. Cogn Brain Res 22:129–151

    Article  Google Scholar 

  • Papaxanthis C, Dubost V, Pozzo T (2003a) Similar planning strategies for whole-body and arm movements performed in the sagittal plane. Neuroscience 117:779–783

    Article  PubMed  CAS  Google Scholar 

  • 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 135:371–383

    Article  PubMed  CAS  Google Scholar 

  • 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 148:498–503

    PubMed  Google Scholar 

  • Papaxanthis C, Pozzo T, Stapley P (1998) Effects of movement direction upon kinematic characteristics of vertical arm pointing movements in man. Neuroscience Letters 253:103–106

    Article  PubMed  CAS  Google Scholar 

  • Patton JL, Lee WA, Pai YC (2000) Relative stability improves with experience in a dynamic standing task. Exp Brain Res 135:117–126

    Article  PubMed  CAS  Google Scholar 

  • Pozzo T, Papaxanthis C, Petit JL, Schweighofer N, Stucchi N (2006) Kinematic features of movement tunes perception and action coupling. Behav Brain Res 169:75–82

    Article  PubMed  Google Scholar 

  • Pozzo T, Papaxanthis C, Stapley P, Berthoz A (1998) The sensorimotor and cognitive integration of gravity. Brain Res Brain Res Rev 28:92–101

    Article  PubMed  CAS  Google Scholar 

  • Prinz W (1997) Perception and action planning. Eur J Cogn Psychol 9:129–154

    Article  Google Scholar 

  • 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 19:861–869

    Article  PubMed  Google Scholar 

  • Rizzolatti G (2005) The mirror neuron system and its function in humans. Anat Embryol (Berl) 210:419–421

    Article  Google Scholar 

  • Rizzolatti G, Craighero L (2004) The mirror-neuron system. Annu Rev Neurosci 27:169–192

    Article  PubMed  CAS  Google Scholar 

  • 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 247–266

    Google Scholar 

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

    Article  CAS  Google Scholar 

  • Rizzolatti G, Luppino G (2001) The cortical motor system. Neuron 31:889–901

    Article  PubMed  CAS  Google Scholar 

  • Rizzolatti G, Luppino G, Matelli M (1998) The organization of the cortical motor system: new concepts. Electroencephalogr Clin Neurophysiol 106:283–296

    Article  PubMed  CAS  Google Scholar 

  • Saygin AP, Wilson SM, Hagler Jr DJ, Bates E, Sereno MI (2004) Point-light biological motion perception activates human premotor cortex. J Neurosci 24:6181–6188

    Article  PubMed  CAS  Google Scholar 

  • Tai YF, Scherfler C, Brooks DJ, Sawamoto N, Castiello U (2004) The human premotor cortex is ‘mirror’ only for biological actions. Curr Biol 14:117–120

    Article  PubMed  CAS  Google Scholar 

  • Thompson JC, Clarke M, Stewart T, Puce A (2005) Configural processing of biological motion in human superior temporal sulcus. J Neurosci 25:9059–9066

    Article  PubMed  CAS  Google Scholar 

  • 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 31:155–165

    Article  PubMed  Google Scholar 

  • Vaina LM, Solomon J, Chowdhury S, Sinha P, Belliveau JW (2001) Functional neuroanatomy of biological motion perception in humans. Proc Natl Acad Sci USA 98:11656–11661

    Article  PubMed  CAS  Google Scholar 

  • Verfaillie K, Daems A (2002) Representing and anticipating human actions in vision. Visual Cogn 9:217–232

    Article  Google Scholar 

  • Viviani P, Stucchi N (1992) Biological movements look uniform: evidence of motor-perceptual interactions. J Exp Psychol Hum Percept Perform 18:603–623

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

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).

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Correspondence to Ghislain Saunier.

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Saunier, G., Papaxanthis, C., Vargas, C.D. et al. Inference of complex human motion requires internal models of action: behavioral evidence. Exp Brain Res 185, 399–409 (2008). https://doi.org/10.1007/s00221-007-1162-2

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