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New insights into action–perception coupling

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Abstract

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.

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References

  • Adamovich SV, Levin MF, Feldman AG (1997) Central modifications of reflex parameters may underlie the fastest arm movements. J Neurophysiol 77:1460–1469

    PubMed  CAS  Google Scholar 

  • Archambault PS, Mihaltchev P, Levin MF, Feldman AG (2005) Basic elements of arm postural control analyzed by unloading. Exp Brain Res 164:225–241

    Article  PubMed  Google Scholar 

  • 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 151:493–506

    Article  PubMed  CAS  Google Scholar 

  • Arzy S, Seeck M, Ortigue S, Spinelli L, Blanke O (2006) Induction of an illusory shadow person. Nature 443(7109):287

    Article  PubMed  CAS  Google Scholar 

  • 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 10:925–935

    Google Scholar 

  • Belen’kiĭ VE, Gurfinkel’ VS, Pal’tsev EI (1967) Control elements of voluntary movements. Biofizika 12:135–141

    PubMed  Google Scholar 

  • Bigland B, Lippold OCJ (1954) The relation between force, velocity and integrated electrical activity in human muscles. J Physiol 123:214–224

    PubMed  CAS  Google Scholar 

  • Bridgeman B (2007) Efference copy and its limitations. Comput Biol Med 37:924–929

    Article  PubMed  Google Scholar 

  • Bridgeman B, Hendry D, Stark L (1975) Failure to detect displacement of the visual world during saccadic eye movements. Vision Res 15:719–722

    Article  PubMed  CAS  Google Scholar 

  • Capaday C (1995) The effects of baclofen on the stretch reflex parameters of the cat. Exp Brain Res 104:287–296

    Article  PubMed  CAS  Google Scholar 

  • Chan BL, Witt R, Charrow AP, Magee A, Howard R, Pasquina PF (2007) Mirror therapy for phantom limb pain. N Engl J Med 357:2206–2207

    Article  PubMed  CAS  Google Scholar 

  • Colby CL (1998) Action-oriented spatial reference frames in cortex. Neuron 20:15–24

    Article  PubMed  CAS  Google Scholar 

  • 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 62:673–683

    PubMed  CAS  Google Scholar 

  • 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 180:15–21

    Article  PubMed  Google Scholar 

  • 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 100:297–313

    Article  PubMed  CAS  Google Scholar 

  • Deubel H, Bridgeman B, Schneider WX (2004) Different effects of eyelid blinks and target blanking on saccadic suppression of displacement. Percept Psychophysics 66:772–778

    Google Scholar 

  • 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, Winston

  • 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 557:355–561

    Article  PubMed  CAS  Google Scholar 

  • 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 11:667–675

    CAS  Google Scholar 

  • Feldman AG, Latash ML (1982) Afferent and efferent components of joint position sense: interpretation of kinaesthetic illusions. Biol Cybern 42:205–214

    PubMed  CAS  Google Scholar 

  • Feldman AG, Latash ML (2005) Testing hypotheses and the advancement of science: recent attempts to falsify the equilibrium point hypothesis. Exp Brain Res 161:91–103

    Article  PubMed  Google Scholar 

  • Feldman AG, Levin MF (1995) The origin and use of positional frames of reference in motor control. Behav Brain Sci 18:723–806

    Article  Google Scholar 

  • Feldman AG, Orlovsky GN (1972) The influence of different descending systems on the tonic stretch reflex in the cat. Exp Neurol 37:481–494

    Article  PubMed  CAS  Google Scholar 

  • Feldman AG, Ostry DJ, Levin MF, Gribble PL, Mitnitski AB (1998) Recent tests of the equilibrium-point hypothesis (λ model). Motor Control 2:189–205

    PubMed  CAS  Google Scholar 

  • 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:267–281

    Article  Google Scholar 

  • Foisy M, Feldman AG (2006) Threshold control of arm posture and movement adaptation to load. Exp Brain Res 175:726–744

    Article  PubMed  Google Scholar 

  • Forget R, Lamarre Y (1990) Anticipatory postural adjustment in the absence of normal peripheral feedback. Brain Res 508:176–179

    Article  PubMed  CAS  Google Scholar 

  • Gallistel CR (1980) The organization of action: a new synthesis. Lawrence Elbaum Associates/Wiley, Hillisdale/New Jersey

  • 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 

  • Gibson JJ (1968) The senses considered as perceptual systems. George Allen and Unwin, London

    Google Scholar 

  • Glansdorf P, Prigogine I (1971) Thermodynamic theory of structures stability and fluctuations. Wiley, New York

    Google Scholar 

  • Gomi H, Kawato M (1996) Equilibrium point control hypothesis examined by measured arm stiffness during multi joint movement. Science 272:117–120

    Article  PubMed  CAS  Google Scholar 

  • Goodale MA, Westwood DA (2004) An evolving view of duplex vision: separate but interacting cortical pathways for perception and action. Curr Opin Neurobiol 14:203–211

    Article  PubMed  CAS  Google Scholar 

  • Gribble PL, Ostry DJ, Sanguineti V, Laboissière R (1998) Are complex control signals required for human arm movement? J Neurophysiol 79:1409–1424

    PubMed  CAS  Google Scholar 

  • 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)

  • Hinder MR, Milner TE (2003) The case for an internal dynamics model versus equilibrium point control in human movement. J Physiol 549:953–963

    Article  PubMed  CAS  Google Scholar 

  • Holdefer RN, Miller EL (2002) Primary motor cortical neurons encode functional muscle synergies. Exp Brain Res 146:233–243

    Article  PubMed  CAS  Google Scholar 

  • Honrubia FM, Elliott JH (1970) Efferent innervation of the retina. II. Morphologic study of the monkey retina. Invest Ophthalmol Vis Sci 9:971–976

    CAS  Google Scholar 

  • Houk JC (1988) Control strategies in physiological systems. FASEB J 2:97–107

    PubMed  CAS  Google Scholar 

  • Hufschmidt HJ, Hufschmidt T (1954) Antagonist inhibition as the earliest sign of a sensory-motor reaction. Nature 174:607

    Article  PubMed  CAS  Google Scholar 

  • 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 322:167–179

    PubMed  CAS  Google Scholar 

  • Kawato M (1999) Internal models for motor control and trajectory planning. Curr Opin Neurobiol 9:718–727

    Article  PubMed  CAS  Google Scholar 

  • 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):271–281

    Article  PubMed  CAS  Google Scholar 

  • Lackner JR (1988) Some proprioceptive influences on the perceptual representation of body shape and orientation. Brain 111:281–297

    Article  PubMed  Google Scholar 

  • Lackner JR, Dizio P (1994) Rapid adaptation to Coriolis force perturbations of arm trajectory. J Neurophysiol 72:299–313

    PubMed  CAS  Google Scholar 

  • Latash ML, Gottlieb GL (1991) An equilibrium-point model of dynamic regulation of fast single-joint movements. J Mot Behav 23:179–191

    PubMed  CAS  Google Scholar 

  • Lepelley MC, Thullier F, Koral J, Lestienne FG (2006) Muscle coordination in complex movements during Jeté in skilled ballet dancers. Exp Brain Res 175:321–331

    Article  PubMed  Google Scholar 

  • 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 283:65–68

    Article  PubMed  CAS  Google Scholar 

  • Levin MF, Dimov M (1997) Spatial zones for muscle coactivation and the control of postural stability. Brain Res 757:43–59

    Article  PubMed  CAS  Google Scholar 

  • Levin MF, Lamarre Y, Feldman AG (1995) Control variables and proprioceptive feedback in fast single-joint movement. Can J Physiol Pharmacol 73:316–330

    PubMed  CAS  Google Scholar 

  • 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 853:269–352

    Article  Google Scholar 

  • Loeb GE, Brown IE, Cheng EJ (1999) A hierarchical foundation for models of sensorimotor control. Exp Brain Res 126:1–18

    Article  PubMed  CAS  Google Scholar 

  • Matin E (1974) Saccadic suppression: a review and an analysis. Psychol. Bull 81: 899–917

    Google Scholar 

  • Matthews PBC (1959) A study of certain factors influencing the stretch reflex of the decerebrated cat. J Physiol 147:547–564

    PubMed  CAS  Google Scholar 

  • Matthews PBC (1972) Mammalian muscle receptors and their central actions. Arnold, London

    Google Scholar 

  • 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., Bethesda

  • McConkie GW, Currie CB (1996) Visual stability across saccades while viewing complex pictures. J Exp Psychol Human Percept Perform 22:563–581

    Article  CAS  Google Scholar 

  • Melzack R (1990) Phantom limbs and the concept of a neuromatrix. Trends Neurosci 13:88–92

    Article  PubMed  CAS  Google Scholar 

  • Merriam EP, Genovese CR, Colby CL (2007) Remapping in human visual cortex. J Neurophysiol 97:1738–1755

    Article  PubMed  Google Scholar 

  • Merton PA (1953) Speculations on the servo-control of movement. In: Wolstenholme GEW (ed) The spinal cord. Churchill, London, pp 247–255

  • Milner AD, Goodale MA (1988) The visual brain in action. Oxford Psychology Series, No. 27, Oxford University Press, New York

  • Mitchell SW (1971) Phantom limbs. Lippincott’s Mag Pop Lit Sci 8:63–569

    Google Scholar 

  • Munoz DP, Pélisson D, Guitton D (1991) Movement of neural activity on the superior colliculus motor map during gaze shifts. Science 251:1358–1360

    Article  PubMed  CAS  Google Scholar 

  • 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 45:37–112

    Google Scholar 

  • Musampa NK, Mathieu PA, Levin MF (2007) Relationship between stretch reflex thresholds and voluntary arm muscle activation in patients with spasticity. Exp Brain Res 181:579–593

    Article  PubMed  Google Scholar 

  • Nichols TR, Houk JC (1976) Improvement in linearity and regulation of stiffness that results from actions of stretch reflex. J Neurophysiol 39:119–142

    PubMed  CAS  Google Scholar 

  • Nichols TR, Steeves JD (1986) Resetting of resultant stiffness in ankle flexor and extensor muscles in the decerebrated cat. Exp Brain Res 62:401–410

    Article  PubMed  CAS  Google Scholar 

  • Ostry DA, Feldman AG (2003) A critical evaluation of the force control hypothesis in motor control. Exp Brain Res 153:275–288

    Article  PubMed  Google Scholar 

  • Paillard J (1991) Motor and representational framing of space. In: Paillard J (ed) Brain and Space, chap 10, Oxford University Press, Oxford, pp 163–182

  • 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 150:50–60

    PubMed  CAS  Google Scholar 

  • Pilon JF, Feldman AG (2006) Threshold control of motor actions prevents destabilizing effects of proprioceptive delays. Exp Brain Res 174:229–239

    Article  PubMed  Google Scholar 

  • Pilon JF, De Serres SJ, Feldman AG (2007) Threshold position control of arm movement with anticipatory increase in grip force. Exp Brain Res 181:49–67

    Article  PubMed  Google Scholar 

  • Ramachandran VS, Hirstein W (1998) The perception of phantom limbs: the D.O. Hebb lecture. Brain 9:1603–1630

    Article  Google Scholar 

  • Robinson DA (1970) Oculomotor unit behavior in the monkey. J Neurophysiol 33:393–404

    PubMed  CAS  Google Scholar 

  • Sampanes AC, Tseng P, Bridgeman B (2008) The role of gist in scene recognition. Vision Res 21:2275–2283

    Article  Google Scholar 

  • Sherrington CS (1910) Flexion-reflex of the limb, crossed extension-reflex, and reflex stepping and standing. J Physiol 40:28–121

    PubMed  CAS  Google Scholar 

  • Shik ML, Orlovsky GN (1976) Neurophysiology of locomotor automatism. Physiol Rev 56:465–501

    PubMed  CAS  Google Scholar 

  • Sperry R (1950) Neural basis of the spontaneous optokinetic response produced by visual inversion. J Comp Psychol Physiol 43:482–489

    Article  CAS  Google Scholar 

  • St-Onge N, Feldman AG (2004) Referent configuration of the body: a global factor in the control of multiple skeletal muscles. Exp Brain Res 155:291–300

    Article  PubMed  Google Scholar 

  • 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 79:295–316

    Article  PubMed  CAS  Google Scholar 

  • Turvey M (2007) Action and perception at the level of synergies. Hum Mov Sci 26:657–697

    Article  PubMed  CAS  Google Scholar 

  • Vallbo AB (1974) Human muscle spindle discharge during isometric voluntary contractions. Amplitude relations between spindle frequency and torque. Acta Physiol Scand 90:319–336

    Article  PubMed  CAS  Google Scholar 

  • 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 139–173

  • 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, 6:299–318

  • 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 161:159–181

    Article  Google Scholar 

  • Warren WH (2006) The dynamics of perception and action. Psychol Rev 113:358–389

    Article  PubMed  Google Scholar 

  • 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 & Francis

  • Windhorst U (2007) Muscle proprioceptive feedback and spinal networks. Brain Res Bull 73:155–202

    Article  PubMed  CAS  Google Scholar 

  • Wing AM, Flanagan JR, Richardson J (1997) Anticipatory postural adjustments in stance and grip. Exp Brain Res 116:122–130

    Article  PubMed  CAS  Google Scholar 

  • Wolpert DM, Flanagan JR (2001) Motor prediction. Curr Biol 11:R729–R732

    Article  PubMed  CAS  Google Scholar 

  • Wolpert DM, Ghahramani Z (2000) Computational principles of movement neuroscience. Nat Neurosci 3:1212–1217

    Article  PubMed  CAS  Google Scholar 

  • Wolpert DM, Ghahramani Z, Jordan MI (1995) An internal model for sensorimotor integration. Science 269:1179–1182

    Article  Google Scholar 

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Acknowledgments

I thank Mark Latash for many valuable comments on the paper. Supported by CIHR, CHRP, NSERC and FQRNT (Canada).

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  1. Department of Physiology, Center for Interdisciplinary Research in Rehabilitation, University of Montreal, Montreal, Canada

    Anatol G. Feldman

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Feldman, A.G. New insights into action–perception coupling. Exp Brain Res 194, 39–58 (2009). https://doi.org/10.1007/s00221-008-1667-3

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