Advertisement

Neuronal Correlates of the Simulation, Execution, and Perception of Limb Movements

  • Eiichi Naito

Abstract

Humans and animals can control only what they can sense. We therefore cannot precisely control voluntary movements that require elaborate motor control of our body parts unless we can perceive those movements. The neuronal correlates of the mental representation of the “body image”—our perception of the size, shape, movements, and relative configuration of our body parts (Head and Holms 1911)—have long been uncertain. Because brain damage often causes one’s body image to be distorted (Berlucchi and Aglioti 1997; Berti et al. 2005; Sellal et al. 1996), the body image represented as neuronal activity in our brain must be the result of neuronal computation and the integration of multisensory information (somatosensory and visual) about our body (Graziano and Gross 1998). Because people can sense and move body parts without the aid of vision, however, the body image must largely depend on somatic input. Recent neuroimaging techniques such as functional magnetic resonance imaging (fMRI) allow us to investigate the neuronal representations that are related to various types of our body image by measuring brain activity while people perceive limb movements (Naito 2004) or experience changing body configurations (Ehrsson et al. 2005). This chapter introduces neuronal representations underlying the somatic perception of various types of limb movements (particularly hand movements) and discusses how people perceive these movements and how this perception is related to the control of those movements.

Keywords

Motor Imagery Limb Movement Supplementary Motor Area Muscle Spindle Inferior Parietal Lobule 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Annett J (1995) Motor imagery: perception or action? Neuropsychologia 33:1395–1417PubMedCrossRefGoogle Scholar
  2. Bard C, Fleury M, Teasdale N, Paillard J, Nougier V (1995) Contribution of proprioception for calibrating and updating the motor space. Can J Physiol Pharmacol 73:246–254PubMedGoogle Scholar
  3. Berlucchi G, Aglioti S (1997) The body in the brain: neural bases of corporeal awareness. Trends Neurosci 20:560–564PubMedCrossRefGoogle Scholar
  4. Berti A, Bottini G, Gandola M, Pia L, Smania N, Stracciari A, Castiglioni I, Vallar G, Paulesu E (2005) Shared cortical anatomy for motor awareness and motor control. Science 309:488–491PubMedCrossRefGoogle Scholar
  5. Binkofski F, Buccino G, Posse S, Seitz RJ, Rizzolatti G, Freund HJ (1999) A frontoparietal circuit for object manipulation in man: evidence from an fMRI study. Eur J Neurosci 11:3276–3286PubMedCrossRefGoogle Scholar
  6. Binkofski F, Kunesch E, Classen J, Seitz RJ, Freund HJ (2001) Tactile apraxia: unimodal apractic disorder of tactile object exploration associated with parietal lobe lesions. Brain 124:132–144PubMedCrossRefGoogle Scholar
  7. Bodegard A, Geyer S, Grefkes C, Zilles K, Roland PE (2001) Hierarchical processing of tactile shape in the human brain. Neuron 31:317–328PubMedCrossRefGoogle Scholar
  8. Brinkman J, Colebatch JG, Porter R, York DH (1985) Responses of precentral cells during cooling of postcentral cortex in conscious monkeys. J Physiol (Lond) 368:611–625PubMedGoogle Scholar
  9. Burchfiel JL, Duffy FH (1972) Muscle afferent input to single cells in primate somatosensory cortex. Brain Res 45:241–246PubMedCrossRefGoogle Scholar
  10. Burke D, Hagbarth K, Lofstedt L, Wallin G. (1976) The responses of human muscle spindle endings to vibration of non-contracting muscles. J Physiol (Lond) 261:673–693PubMedGoogle Scholar
  11. Burke D, Gandevia SC, Macefield G. (1988) Responses to passive movement of receptors in joint, skin and muscle of the human hand. J Physiol 402:347–361PubMedGoogle Scholar
  12. Cadoret G, Smith AM (1995) Input-output properties of hand-related cells in the ventral cingulate cortex in the monkey. J Neurophysiol 73:2584–2590PubMedGoogle Scholar
  13. Colebatch JG, Sayer RJ, Porter R, White OB (1990) Responses of monkey precentral neurones to passive movements and phasic muscle stretch: relevance to man. Electroencephalogr Clin Neurophysiol 75:44–55PubMedCrossRefGoogle Scholar
  14. Collins DF, Refshauge KM, Todd G, Gandevia SC (2005) Cutaneous receptors contribute to kinesthesia at the index finger, elbow, and knee. J Neurophysiol 94:1699–706PubMedCrossRefGoogle Scholar
  15. Duffy FH, Burchfiel JL (1971) Somatosensory system: organizational hierarchy from single units in monkey area 5. Science 172:273–275PubMedCrossRefGoogle Scholar
  16. Edin BB (2004) Quantitative analyses of dynamic strain sensitivity in human skin mechanoreceptors. J Neurophysiol 92:3233–3243PubMedCrossRefGoogle Scholar
  17. Edin BB, Abbs JH (1991) Finger movement responses of cutaneous mechanoreceptors in the dorsal skin of human hand. J Neurophysiol 65:657–670PubMedGoogle Scholar
  18. Edin BB, Johansson N (1995) Skin strain patterns provide kinaesthetic information to the human central nervous system. J Physiol 487:243–251PubMedGoogle Scholar
  19. Edin BB, Vallbo ÅB (1988) Stretch sensitization of human muscle spindles. J Physiol 400:101–111PubMedGoogle Scholar
  20. Edin BB, Vallbo ÅB (1990) Dynamic response of human muscle spindle afferents to stretch. J Neurophysiol 63:1297–1306PubMedGoogle Scholar
  21. Ehrsson HH, Fagergren E, Jonsson T, Westling G, Johansson RS, Forssberg H (2000) Cortical activity in precision-versus power-grip tasks: an fMRI study. J Neurophysiol 83:528–536PubMedGoogle Scholar
  22. Ehrsson HH, Fagergren E, Forssberg H (2001) Differential fronto-parietal activation depending on force used in a precision grip task: an fMRI study. J Neurophysiol 85:2613–2623PubMedGoogle Scholar
  23. Ehrsson HH, Geyer S, Naito E (2003) Imagery of voluntary movement of fingers, toes, and tongue activates corresponding body-part-specific motor representations. J Neurophysiol 90:3304–3316PubMedCrossRefGoogle Scholar
  24. Ehrsson HH, Kito T, Sadato N, Passingham RE, Naito E (2005) Neural substrate of body size: illusory feeling of shrinking of the waist. PLoS Biol 3:e412PubMedCrossRefGoogle Scholar
  25. Eklund G., Hagbarth KE (1966) Normal variability of tonic vibration reflexes in man. Exp Biol 16:80–92Google Scholar
  26. Fetz EE, Finocchio DV, Baker MA, Soso MJ (1980) Sensory and motor responses of precentral cortex cells during comparable passive and active joint movements. J Neurophysiol 43:1070–1089PubMedGoogle Scholar
  27. Fogassi L, Ferrari PF, Gesierich B, Rozzi S, Chersi F, Rizzolatti G (2005) Parietal lobe: from action organization to intention understanding. Science 308:662–667PubMedCrossRefGoogle Scholar
  28. Fried I, Katz A, McCarthy G, Sass KJ, Williamson P, Spencer SS, Spencer DD (1991) Functional organization of human supplementary motor cortex studied by electrical stimulation. J Neurosci 11:3656–3666PubMedGoogle Scholar
  29. Frith C, Dolan RJ (1997) Brain mechanisms associated with top-down processes in perception. Philos Trans R Soc Lond B Biol Sci 352:1221–1230PubMedCrossRefGoogle Scholar
  30. Gandevia SC (1985) Illusory movements produced by electrical stimulation of lowthreshold muscle afferents from the hand. Brain 108:965–981PubMedCrossRefGoogle Scholar
  31. Gandevia SC, Smith JL, Crawford M, Proske U, Taylor JL (2006) Motor commands contribute to human position sense. J Physiol 571:703–710PubMedCrossRefGoogle Scholar
  32. Ghez C, Sainburg R (1995) Proprioceptive control of interjoint coordination. Can J Physiol Pharmacol 73:273–284PubMedGoogle Scholar
  33. Goodwin GM, McCloskey DI, Matthews PBC (1972) The contribution of muscle afferents to kinesthesia shown by vibration induced illusions of movement and by the effects of paralysing joint afferents. Brain 95:705–748PubMedCrossRefGoogle Scholar
  34. Gordon J, Ghilardi MF, Ghez C (1995) Impairments of reaching movements in patients without proprioception. I. Spatial errors. J Neurophysiol 73:347–360PubMedGoogle Scholar
  35. Graziano MS, Gross CG (1998) Spatial maps for the control of movement. Curr Opin Neurobiol 8:195–201PubMedCrossRefGoogle Scholar
  36. Head H, Holmes G (1911) Sensory disturbances from cerebral lesions. Brain 34:102–254CrossRefGoogle Scholar
  37. Hommel B, Musseler J, Aschersleben G, Prinz W (2001) The theory of event coding (TEC): a framework for perception and action planning. Behav Brain Sci 24:849–937PubMedGoogle Scholar
  38. Hore J, Preston JB, Durkovic RG, Cheney PD (1976) Responses of cortical neurons (area 3a and 4) to ramp stretch of hindlimb muscles in the baboon. J Neurophysiol 39:484–500PubMedGoogle Scholar
  39. Huerta MF, Pons TP (1990) Primary motor cortex receives input from area 3a in macaque. Brain Res 537:367–371PubMedCrossRefGoogle Scholar
  40. Jackson PL, Decety J (2004) Motor cognition: a new paradigm to study self-other interaction. Curr Opin Neurobiol 14:259–263PubMedCrossRefGoogle Scholar
  41. Jennings VA, Lamour Y, Solis H, Fromm C (1983) Somatosensory cortex activity related to position and force. J Neurophysiol 49:1216–1229PubMedGoogle Scholar
  42. Jeannerod M (1994) The representing brain: neural correlates of motor intention and imagery. Behav Brain Sci 17:187–245Google Scholar
  43. Johansson RS, Vallbo AB (1983) Tactile sensory coding in the glabrous skin of the human hand. Trends Neurosci 6:27–32CrossRefGoogle Scholar
  44. Johnson-Frey SH (2004) The neural bases of complex tool use in humans. Trends Cognit Sci 8:71–78CrossRefGoogle Scholar
  45. Johnson-Frey SH, Newman-Norlund R, Grafton ST (2005) A distributed left hemisphere network active during planning of everyday tool use skills. Cereb Cortex 15:681–695PubMedCrossRefGoogle Scholar
  46. Iriki A, Tanaka M, Iwamura Y (1996) Coding of modified body schema during tool use by macaque postcentral neurones. Neuroreport 7:2325–2330PubMedCrossRefGoogle Scholar
  47. Iwamura Y (1998) Hierarchical somatosensory processing. Curr Opin Neurobiol. 8:522–528PubMedCrossRefGoogle Scholar
  48. Iwamura Y, Iriki A, Tanaka M (1994) Bilateral hand representation in the postcentral somatosensory cortex. Nature (Lond) 369:554–556PubMedCrossRefGoogle Scholar
  49. Kito T, Hashimoto T, Yoneda T, Katamoto S, Naito E (2006) Sensory processing during kinesthetic aftereffect following illusory hand movement elicited by tendon vibration. Brain Res 1114:75–84PubMedCrossRefGoogle Scholar
  50. Lackner JR (1988) Some proprioceptive influences on the perceptual representation of body shape and orientation. Brain 111:281–297PubMedCrossRefGoogle Scholar
  51. Lackner JR, Taublieb AB (1983) Reciprocal interactions between the position sense representations of the two forearms. J Neurosci 3:2280–2285PubMedGoogle Scholar
  52. Lemon RN, Van Der Burg J (1979) Short-latency peripheral inputs to thalamic neurons projecting to the motor cortex in the monkey. Exp Brain Res 36:445–462PubMedCrossRefGoogle Scholar
  53. Lewis JW (2006) Cortical networks related to human use of tools. Neuroscientist 12:1–12CrossRefGoogle Scholar
  54. Lim SH, Dinner DS, Pillay PK, Luder H, Morris HH, Klem G, Wyllie E, Awad IA (1994) Functional anatomy of the human supplementary sensorimotor area: results of extraoperative electrical stimulation. Electroencephalogr Clin Neurophysiol 91:179–193PubMedCrossRefGoogle Scholar
  55. Maravita A, Iriki A (2004) Tools for the body (schema). Trends Cognit Sci 8:79–86CrossRefGoogle Scholar
  56. Mercier C, Reilly KT, Vargas CD, Aballea A, Sirigu A (2006) Mapping phantom movement representation in the motor cortex of amputees. Brain (in press)Google Scholar
  57. Murata A, Fadiga L, Fogassi L, Gallese V, Raos V, Rizzolatti G (1997) Object representation in the ventral premotor cortex (area F5) of the monkey. J Neurophysiol 78:2226–2230PubMedGoogle Scholar
  58. Murata A, Gallese V, Luppino G, Kaseda M, Sakata H (2000) Selectivity for the shape, size, and orientation of objects for grasping in neurons of monkey parietal area AIP. J Neurophysiol 83:2580–2601PubMedGoogle Scholar
  59. Naito E (2004) Sensing limb movements in the motor cortex: how humans sense limb movement. Neuroscientist 9:73–82CrossRefGoogle Scholar
  60. Naito E, Ehrsson HH (2001) Kinesthetic illusion of wrist movement activates motorrelated areas. Neuroreport 12:3805–3809PubMedCrossRefGoogle Scholar
  61. Naito E, Ehrsson HH (2006) Somatic sensation of hand-object interactive movement is associated with activity in the left inferior parietal cortex. J Neurosci 26:3783–3790PubMedCrossRefGoogle Scholar
  62. Naito E, Sadato N (2003) Internal simulation of expected sensory experiences before movements get started. Rev Neurosci 14:387–399PubMedGoogle Scholar
  63. Naito E, Ehrsson HH, Geyer S, Zilles K, Roland PE (1999) Illusory arm movements activate cortical motor areas: a PET study. J Neurosci 19:6134–6144PubMedGoogle Scholar
  64. Naito E, Kochiyama T, Kitada R, Nakamura S, Matsumura M, Yonekura Y, Sadato N (2002a) Internally simulated movement sensations during motor imagery activate the cortical motor areas and the cerebellum. J Neurosci 22:3683–3691PubMedGoogle Scholar
  65. Naito E, Nakashima T, Kito T, Aramaki Y, Okada T, Sadato N (2007) Human limbspecific and non limb-specific brain representations during kinesthetic illusory movements of the upper and lower extremities. Eur J Neurosci (in press)Google Scholar
  66. Naito E, Roland PE, Ehrsson HH (2002b) I feel my hand moving: a new role of the primary motor cortex in somatic perception of limb movement. Neuron 36:979–988PubMedCrossRefGoogle Scholar
  67. Naito E, Roland PE, Grefkes C, Choi HJ, Eickhoff S, Geyer S, Zilles K, Ehrsson HH (2005) Dominance of the right hemisphere and role of area 2 in human kinesthesia. J Neurophysiol 93:1020–1034PubMedCrossRefGoogle Scholar
  68. Nickel J, Seitz RJ (2005) Functional clusters in the human parietal cortex as revealed by an observer-independent meta-analysis of functional activation studies. Anat Embryol 210:463–472PubMedCrossRefGoogle Scholar
  69. Phillips CG, Powell TPS, Wiesendanger M (1971) Projection from low-threshold muscle afferents of hand and forearm to area 3a of baboon’s cortex. J Physiol (Lond) 217:419–446PubMedGoogle Scholar
  70. Porter R, Lemon RN (1993) Inputs from the peripheral receptors to motor cortex neurones. In: Corticospinal function and voluntary movement. Oxford University Press, New York, pp 247–272Google Scholar
  71. Ribot-Ciscar E, Roll JP (1998) Ago-antagonist muscle spindle inputs contribute together to joint movement coding in man. Brain Res 791:167–176PubMedCrossRefGoogle Scholar
  72. Rizzolatti G, Luppino G (2001) The cortical motor system. Neuron 31:889–901PubMedCrossRefGoogle Scholar
  73. Roland PE (1987) Somatosensory detection of microgeometry, macrogeometry and kinesthesia after localized lesions of the cerebral hemispheres in man. Brain Res 434:43–94PubMedGoogle Scholar
  74. Roll JP, Vedel JP (1982) Kinaesthetic role of muscle afferent in man, studied by tendon vibration and microneurography. Exp Brain Res 47:177–190PubMedCrossRefGoogle Scholar
  75. Roll JP, Vedel JP, Ribot E (1989) Alteration of proprioceptive messages induced by tendon vibration in man: a microneurographic study. Exp Brain Res 76:213–222PubMedCrossRefGoogle Scholar
  76. Sainburg RL, Ghilardi MF, Poizner H, Ghez C (1995) Control of limb dynamics in normal participants and patients without proprioception. J Neurophysiol 73:820–835PubMedGoogle Scholar
  77. Sakata H, Takaoka Y, Kawarasaki A, Shibutani H (1973) Somatosensory properties of neurons in the superior parietal cortex (area 5) of the rhesus monkey. Brain Res 64:85–102PubMedCrossRefGoogle Scholar
  78. Sellal F, Renaseau-Leclerc C, Labrecque R (1996) The man with six arms. An analysis of supernumerary phantom limbs after right hemisphere stroke. Rev Neurol (Paris) 152:190–195.PubMedGoogle Scholar
  79. Schwarz DWF, Deecke L, Fredrickson JM (1973) Cortical projection of group I muscle afferents to area 2, 3a and the vestibular field in the rhesus monkey. Exp Brain Res 17:516–526PubMedCrossRefGoogle Scholar
  80. Stoeckel MC, Weder B, Binkofski F, Choi HJ, Amunts K, Pieperhoff P, Shah NJ, Seitz RJ (2004) Left and right superior parietal lobule in tactile object discrimination. Eur J Neurosci 19:1067–1072PubMedCrossRefGoogle Scholar
  81. Taoka M, Toda T, Iwamura Y (1998) Representation of the midline trunk, bilateral arms, and shoulders in the monkey postcentral somatosensory cortex. Exp Brain Res 123:315–322PubMedCrossRefGoogle Scholar

Copyright information

© Springer 2007

Authors and Affiliations

  • Eiichi Naito
    • 1
    • 2
  1. 1.Natinal Institute of Information and Communication TechnologyKobe Advanced ICT Research Center & ATR Computational Neuroscience LaboratoriesKyotoJapan
  2. 2.Graduate School of Human and Environmental StudiesKyoto UniversityKyotoJapan

Personalised recommendations