Experimental Brain Research

, Volume 194, Issue 1, pp 39–58

New insights into action–perception coupling

Research Article


According to a view that has dominated the field for over a century, the brain programs muscle commands and uses a copy of these commands [efference copy (EC)] to adjust not only resulting motor action but also ongoing perception. This view was helpful in formulating several classical problems of action and perception: (1) the posture-movement problem of how movements away from a stable posture can be made without evoking resistance of posture-stabilizing mechanisms resulting from intrinsic muscle and reflex properties; (2) the problem of kinesthesia or why our sense of limb position is good despite ambiguous positional information delivered by proprioceptive and cutaneous signals; (3) the problem of visual space constancy or why the world is perceived as stable while its retinal image shifts following changes in gaze. On closer inspection, the EC theory actually does not solve these problems in a physiologically feasible way. Here solutions to these problems are proposed based on the advanced formulation of the equilibrium-point hypothesis that suggests that action and perception are accomplished in a common spatial frame of reference selected by the brain from a set of available frames. Experimental data suggest that the brain is also able to translate or/and rotate the selected frame of reference by modifying its major attributes—the origin, metrics and orientation—and thus substantially influence action and perception. Because of this ability, such frames are called physical to distinguish them from symbolic or mathematical frames that are used to describe system behavior without influencing this behavior. Experimental data also imply that once a frame of reference is chosen, its attributes are modified in a feedforward way, thus enabling the brain to act in an anticipatory and predictive manner. This approach is extended to sense of effort, kinesthetic illusions, phantom limb and phantom body phenomena. It also addresses the question of why retinal images of objects are sensed as objects located in the external, physical world, rather than in internal representations of the brain.


  1. Adamovich SV, Levin MF, Feldman AG (1997) Central modifications of reflex parameters may underlie the fastest arm movements. J Neurophysiol 77:1460–1469PubMedGoogle Scholar
  2. Archambault PS, Mihaltchev P, Levin MF, Feldman AG (2005) Basic elements of arm postural control analyzed by unloading. Exp Brain Res 164:225–241PubMedCrossRefGoogle Scholar
  3. Arshavsky YI, Gelfand IM, Orlovsky GN, Pavlova GA (1978) Messages conveyed by spinocerebellar pathways during scratching in the cat. II. Activity of neurons of the ventral spinocerebellar tract. Brain Res 151:493–506PubMedCrossRefGoogle Scholar
  4. Arzy S, Seeck M, Ortigue S, Spinelli L, Blanke O (2006) Induction of an illusory shadow person. Nature 443(7109):287PubMedCrossRefGoogle Scholar
  5. Asatryan DG, Feldman AG (1965) Functional tuning of the nervous system with control of movements or maintenance of a steady posture: I. Mechanographic analysis of the work of the joint on execution of a postural task. Biophysics 10:925–935Google Scholar
  6. Belen’kiĭ VE, Gurfinkel’ VS, Pal’tsev EI (1967) Control elements of voluntary movements. Biofizika 12:135–141PubMedGoogle Scholar
  7. Bigland B, Lippold OCJ (1954) The relation between force, velocity and integrated electrical activity in human muscles. J Physiol 123:214–224PubMedGoogle Scholar
  8. Bridgeman B (2007) Efference copy and its limitations. Comput Biol Med 37:924–929PubMedCrossRefGoogle Scholar
  9. Bridgeman B, Hendry D, Stark L (1975) Failure to detect displacement of the visual world during saccadic eye movements. Vision Res 15:719–722PubMedCrossRefGoogle Scholar
  10. Capaday C (1995) The effects of baclofen on the stretch reflex parameters of the cat. Exp Brain Res 104:287–296PubMedCrossRefGoogle Scholar
  11. Chan BL, Witt R, Charrow AP, Magee A, Howard R, Pasquina PF (2007) Mirror therapy for phantom limb pain. N Engl J Med 357:2206–2207PubMedCrossRefGoogle Scholar
  12. Colby CL (1998) Action-oriented spatial reference frames in cortex. Neuron 20:15–24PubMedCrossRefGoogle Scholar
  13. Currie CB, McConkie GW, Carlson-Radvansky LA, Irwin DE (2000) The role of the saccade target object in the perception of a visually stable world. Percept Psychophys 62:673–683PubMedGoogle Scholar
  14. Dancause N, Taylor MD, Plautz EJ, Radel JD, Whittaker T, Nudo RJ, Feldman AG (2007) A stretch reflex in extraocular muscles of species purportedly lacking muscle spindles. Exp Brain Res 180:15–21PubMedCrossRefGoogle Scholar
  15. Deliagnina TG, Feldman AG, Gelfand IM, Orlovsky GN (1975) On the role of central program and afferent inflow in the control of scratching movements in the cat. Brain Res 100:297–313PubMedCrossRefGoogle Scholar
  16. Deubel H, Bridgeman B, Schneider WX (2004) Different effects of eyelid blinks and target blanking on saccadic suppression of displacement. Percept Psychophysics 66:772–778Google Scholar
  17. Fechner GT (1860) Elemente der Psychophisik, vol 2. Leipzig, Breitkopf und Härtel. English translation (vol 1 only): lements of Psychophysics (1966) Adler HE (ed), NY, Holt, Rinehartand, WinstonGoogle Scholar
  18. Fedirchuk B, Dai Y (2004) Monoamines increase the excitability of spinal neurones in the neonatal rat by hyperpolarizing the threshold for action potential production. J Physiol 557:355–561PubMedCrossRefGoogle Scholar
  19. Feldman AG (1966) Functional tuning of the nervous system with control of movement or maintenance of a steady posture. III. Mechanomyographic analysis of execution by man of the simplest motor task. Biophysics 11:667–675Google Scholar
  20. Feldman AG, Latash ML (1982) Afferent and efferent components of joint position sense: interpretation of kinaesthetic illusions. Biol Cybern 42:205–214PubMedGoogle Scholar
  21. Feldman AG, Latash ML (2005) Testing hypotheses and the advancement of science: recent attempts to falsify the equilibrium point hypothesis. Exp Brain Res 161:91–103PubMedCrossRefGoogle Scholar
  22. Feldman AG, Levin MF (1995) The origin and use of positional frames of reference in motor control. Behav Brain Sci 18:723–806CrossRefGoogle Scholar
  23. Feldman AG, Orlovsky GN (1972) The influence of different descending systems on the tonic stretch reflex in the cat. Exp Neurol 37:481–494PubMedCrossRefGoogle Scholar
  24. Feldman AG, Ostry DJ, Levin MF, Gribble PL, Mitnitski AB (1998) Recent tests of the equilibrium-point hypothesis (λ model). Motor Control 2:189–205PubMedGoogle Scholar
  25. Feldman AG, Goussev V, Sangole A, Levin MF (2007) Threshold position control and the principle of minimal interaction in motor actions. Prog Brain Res 165C:267–281CrossRefGoogle Scholar
  26. Foisy M, Feldman AG (2006) Threshold control of arm posture and movement adaptation to load. Exp Brain Res 175:726–744PubMedCrossRefGoogle Scholar
  27. Forget R, Lamarre Y (1990) Anticipatory postural adjustment in the absence of normal peripheral feedback. Brain Res 508:176–179PubMedCrossRefGoogle Scholar
  28. Gallistel CR (1980) The organization of action: a new synthesis. Lawrence Elbaum Associates/Wiley, Hillisdale/New JerseyGoogle Scholar
  29. Gandevia SC (1996) Kinesthesia roles for afferent signals and motor commands. In: Rowell L, Shepherd JT (eds) Handbook of physiology, exercise: regulation and integration of multiple systems. American Physiol Society, New York, pp 128–172 (Section 12)Google Scholar
  30. Gibson JJ (1968) The senses considered as perceptual systems. George Allen and Unwin, LondonGoogle Scholar
  31. Glansdorf P, Prigogine I (1971) Thermodynamic theory of structures stability and fluctuations. Wiley, New YorkGoogle Scholar
  32. Gomi H, Kawato M (1996) Equilibrium point control hypothesis examined by measured arm stiffness during multi joint movement. Science 272:117–120PubMedCrossRefGoogle Scholar
  33. Goodale MA, Westwood DA (2004) An evolving view of duplex vision: separate but interacting cortical pathways for perception and action. Curr Opin Neurobiol 14:203–211PubMedCrossRefGoogle Scholar
  34. Gribble PL, Ostry DJ, Sanguineti V, Laboissière R (1998) Are complex control signals required for human arm movement? J Neurophysiol 79:1409–1424PubMedGoogle Scholar
  35. von Helmholtz H (1866/1963) Hanbuch der Physiologischen Optik (Handbook of physiological optics). In: Southall JPC (ed. 2nd Trans.) Helmholtz’s treatise on physiological optics, vol 3, pp 247–270. Dover, New York (Original published 1866; English translation originally published 1925)Google Scholar
  36. Hinder MR, Milner TE (2003) The case for an internal dynamics model versus equilibrium point control in human movement. J Physiol 549:953–963PubMedCrossRefGoogle Scholar
  37. Holdefer RN, Miller EL (2002) Primary motor cortical neurons encode functional muscle synergies. Exp Brain Res 146:233–243PubMedCrossRefGoogle Scholar
  38. Honrubia FM, Elliott JH (1970) Efferent innervation of the retina. II. Morphologic study of the monkey retina. Invest Ophthalmol Vis Sci 9:971–976Google Scholar
  39. Houk JC (1988) Control strategies in physiological systems. FASEB J 2:97–107PubMedGoogle Scholar
  40. Hufschmidt HJ, Hufschmidt T (1954) Antagonist inhibition as the earliest sign of a sensory-motor reaction. Nature 174:607PubMedCrossRefGoogle Scholar
  41. Hulliger M, Nordh E, Vallbo AB (1982) The absence of position response in spindle afferent units from human finger muscles during accurate position holding. J Physiol 322:167–179PubMedGoogle Scholar
  42. Kawato M (1999) Internal models for motor control and trajectory planning. Curr Opin Neurobiol 9:718–727PubMedCrossRefGoogle Scholar
  43. Krawitz S, Fedirchuk B, Dai Y, Jordan LM, McCrea DA (2001) State-dependent hyperpolarization of voltage threshold enhances motoneuron excitability during fictive locomotion in the cat. J Physiol 532(Pt 1):271–281PubMedCrossRefGoogle Scholar
  44. Lackner JR (1988) Some proprioceptive influences on the perceptual representation of body shape and orientation. Brain 111:281–297PubMedCrossRefGoogle Scholar
  45. Lackner JR, Dizio P (1994) Rapid adaptation to Coriolis force perturbations of arm trajectory. J Neurophysiol 72:299–313PubMedGoogle Scholar
  46. Latash ML, Gottlieb GL (1991) An equilibrium-point model of dynamic regulation of fast single-joint movements. J Mot Behav 23:179–191PubMedGoogle Scholar
  47. Lepelley MC, Thullier F, Koral J, Lestienne FG (2006) Muscle coordination in complex movements during Jeté in skilled ballet dancers. Exp Brain Res 175:321–331PubMedCrossRefGoogle Scholar
  48. Lestienne FG, Thullier F, Archambault P, Levin MF, Feldman AG (2000) Multi-muscle control of head movements in monkeys: the referent configuration hypothesis. Neurosci Lett 283:65–68PubMedCrossRefGoogle Scholar
  49. Levin MF, Dimov M (1997) Spatial zones for muscle coactivation and the control of postural stability. Brain Res 757:43–59PubMedCrossRefGoogle Scholar
  50. Levin MF, Lamarre Y, Feldman AG (1995) Control variables and proprioceptive feedback in fast single-joint movement. Can J Physiol Pharmacol 73:316–330PubMedGoogle Scholar
  51. Levin MF, Selles RW, Verheul MH, Meijer OG (2000) Deficits in the coordination of agonist and antagonist muscles in stroke patients: implications for normal motor control. Brain Res 853:269–352CrossRefGoogle Scholar
  52. Loeb GE, Brown IE, Cheng EJ (1999) A hierarchical foundation for models of sensorimotor control. Exp Brain Res 126:1–18PubMedCrossRefGoogle Scholar
  53. Matin E (1974) Saccadic suppression: a review and an analysis. Psychol. Bull 81: 899–917Google Scholar
  54. Matthews PBC (1959) A study of certain factors influencing the stretch reflex of the decerebrated cat. J Physiol 147:547–564PubMedGoogle Scholar
  55. Matthews PBC (1972) Mammalian muscle receptors and their central actions. Arnold, LondonGoogle Scholar
  56. McCloskey DI (1981) Corollary discharges: motor commands and perception. In Brookhart JM, Mountcastle VB (eds) Handbook of physiology: the nervous system, vol 2, Pt 2, pp 1415–1447. American Physiol. Soc., BethesdaGoogle Scholar
  57. McConkie GW, Currie CB (1996) Visual stability across saccades while viewing complex pictures. J Exp Psychol Human Percept Perform 22:563–581CrossRefGoogle Scholar
  58. Melzack R (1990) Phantom limbs and the concept of a neuromatrix. Trends Neurosci 13:88–92PubMedCrossRefGoogle Scholar
  59. Merriam EP, Genovese CR, Colby CL (2007) Remapping in human visual cortex. J Neurophysiol 97:1738–1755PubMedCrossRefGoogle Scholar
  60. Merton PA (1953) Speculations on the servo-control of movement. In: Wolstenholme GEW (ed) The spinal cord. Churchill, London, pp 247–255Google Scholar
  61. Milner AD, Goodale MA (1988) The visual brain in action. Oxford Psychology Series, No. 27, Oxford University Press, New YorkGoogle Scholar
  62. Mitchell SW (1971) Phantom limbs. Lippincott’s Mag Pop Lit Sci 8:63–569Google Scholar
  63. Munoz DP, Pélisson D, Guitton D (1991) Movement of neural activity on the superior colliculus motor map during gaze shifts. Science 251:1358–1360PubMedCrossRefGoogle Scholar
  64. Müller GE, Schumann F (1889) Über die psychologischen Grundlagen der Vergleichung gehobener Gewichte [On the psychological basis for the comparison of weights]. Pflüig Arch ges Physiol 45:37–112Google Scholar
  65. Musampa NK, Mathieu PA, Levin MF (2007) Relationship between stretch reflex thresholds and voluntary arm muscle activation in patients with spasticity. Exp Brain Res 181:579–593PubMedCrossRefGoogle Scholar
  66. Nichols TR, Houk JC (1976) Improvement in linearity and regulation of stiffness that results from actions of stretch reflex. J Neurophysiol 39:119–142PubMedGoogle Scholar
  67. Nichols TR, Steeves JD (1986) Resetting of resultant stiffness in ankle flexor and extensor muscles in the decerebrated cat. Exp Brain Res 62:401–410PubMedCrossRefGoogle Scholar
  68. Ostry DA, Feldman AG (2003) A critical evaluation of the force control hypothesis in motor control. Exp Brain Res 153:275–288PubMedCrossRefGoogle Scholar
  69. Paillard J (1991) Motor and representational framing of space. In: Paillard J (ed) Brain and Space, chap 10, Oxford University Press, Oxford, pp 163–182Google Scholar
  70. Pearson KG, Misiaszek JE, Hulliger M (2003) Chemical ablation of sensory afferents in the walking system of the cat abolishes the capacity for functional recovery after peripheral nerve lesions. Exp Brain Res 150:50–60PubMedGoogle Scholar
  71. Pilon JF, Feldman AG (2006) Threshold control of motor actions prevents destabilizing effects of proprioceptive delays. Exp Brain Res 174:229–239PubMedCrossRefGoogle Scholar
  72. Pilon JF, De Serres SJ, Feldman AG (2007) Threshold position control of arm movement with anticipatory increase in grip force. Exp Brain Res 181:49–67PubMedCrossRefGoogle Scholar
  73. Ramachandran VS, Hirstein W (1998) The perception of phantom limbs: the D.O. Hebb lecture. Brain 9:1603–1630CrossRefGoogle Scholar
  74. Robinson DA (1970) Oculomotor unit behavior in the monkey. J Neurophysiol 33:393–404PubMedGoogle Scholar
  75. Sampanes AC, Tseng P, Bridgeman B (2008) The role of gist in scene recognition. Vision Res 21:2275–2283CrossRefGoogle Scholar
  76. Sherrington CS (1910) Flexion-reflex of the limb, crossed extension-reflex, and reflex stepping and standing. J Physiol 40:28–121PubMedGoogle Scholar
  77. Shik ML, Orlovsky GN (1976) Neurophysiology of locomotor automatism. Physiol Rev 56:465–501PubMedGoogle Scholar
  78. Sperry R (1950) Neural basis of the spontaneous optokinetic response produced by visual inversion. J Comp Psychol Physiol 43:482–489CrossRefGoogle Scholar
  79. St-Onge N, Feldman AG (2004) Referent configuration of the body: a global factor in the control of multiple skeletal muscles. Exp Brain Res 155:291–300PubMedCrossRefGoogle Scholar
  80. St-Onge N, Adamovich SV, Feldman AG (1997) Control processes underlying elbow flexion movements may be independent of kinematic and electromyographic patterns: experimental study and modelling. Neuroscience 79:295–316PubMedCrossRefGoogle Scholar
  81. Turvey M (2007) Action and perception at the level of synergies. Hum Mov Sci 26:657–697PubMedCrossRefGoogle Scholar
  82. Vallbo AB (1974) Human muscle spindle discharge during isometric voluntary contractions. Amplitude relations between spindle frequency and torque. Acta Physiol Scand 90:319–336PubMedCrossRefGoogle Scholar
  83. Von Holst E, Mittelstaedt H (1950) Daz reafferezprincip. Wechselwirkungen zwischen Zentralnerven-system und Peripherie, Naturwiss. 37:467–476. English translation (1973: The reafference principle. In: The behavioral physiology of animals and man. The collected papers of Erich von Holst. Martin R (translator) University of Miami Press, Coral Gables, Florida, pp 139–173Google Scholar
  84. Wachholder K, Altenburger H (1927/2002) Do our limbs have only one rest length? a contribution to the measurement of elastic forces in passive and active movements. Pflüger’s Archive für die gesamte Physiologie 215:627–640. English translation and comments by Sternad D in Motor control, 2002, 6:299–318Google Scholar
  85. Warr WB (2004) Olivocochlear and vestibular efferent neurons of the feline brain stem: their location, morphology and number determined by retrograde axonal transport and acetylcholinesterase histochemistry. Comp Neurol 161:159–181CrossRefGoogle Scholar
  86. Warren WH (2006) The dynamics of perception and action. Psychol Rev 113:358–389PubMedCrossRefGoogle Scholar
  87. Weber EH (1834) De Pulsu, Resorptione, Auditu et Tactu. Kohler CF, Lipsiae. English translation of chapters De Tactu and Der Tastsim in this book: E.H. Weber’s the sense of touch (1978) Ross HE, Marray DJ (editors and translators) Acad. Press, Erlbaum (UK) Taylor & FrancisGoogle Scholar
  88. Windhorst U (2007) Muscle proprioceptive feedback and spinal networks. Brain Res Bull 73:155–202PubMedCrossRefGoogle Scholar
  89. Wing AM, Flanagan JR, Richardson J (1997) Anticipatory postural adjustments in stance and grip. Exp Brain Res 116:122–130PubMedCrossRefGoogle Scholar
  90. Wolpert DM, Flanagan JR (2001) Motor prediction. Curr Biol 11:R729–R732PubMedCrossRefGoogle Scholar
  91. Wolpert DM, Ghahramani Z (2000) Computational principles of movement neuroscience. Nat Neurosci 3:1212–1217PubMedCrossRefGoogle Scholar
  92. Wolpert DM, Ghahramani Z, Jordan MI (1995) An internal model for sensorimotor integration. Science 269:1179–1182CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2008

Authors and Affiliations

  1. 1.Department of Physiology, Center for Interdisciplinary Research in RehabilitationUniversity of MontrealMontrealCanada

Personalised recommendations