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

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Representation and Brain
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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.

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References

  • Annett J (1995) Motor imagery: perception or action? Neuropsychologia 33:1395–1417

    Article  PubMed  CAS  Google Scholar 

  • 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 73:246–254

    PubMed  CAS  Google Scholar 

  • Berlucchi G, Aglioti S (1997) The body in the brain: neural bases of corporeal awareness. Trends Neurosci 20:560–564

    Article  PubMed  CAS  Google Scholar 

  • 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 309:488–491

    Article  PubMed  CAS  Google Scholar 

  • 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 11:3276–3286

    Article  PubMed  CAS  Google Scholar 

  • 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 124:132–144

    Article  PubMed  CAS  Google Scholar 

  • Bodegard A, Geyer S, Grefkes C, Zilles K, Roland PE (2001) Hierarchical processing of tactile shape in the human brain. Neuron 31:317–328

    Article  PubMed  CAS  Google Scholar 

  • Brinkman J, Colebatch JG, Porter R, York DH (1985) Responses of precentral cells during cooling of postcentral cortex in conscious monkeys. J Physiol (Lond) 368:611–625

    PubMed  CAS  Google Scholar 

  • Burchfiel JL, Duffy FH (1972) Muscle afferent input to single cells in primate somatosensory cortex. Brain Res 45:241–246

    Article  PubMed  CAS  Google Scholar 

  • 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) 261:673–693

    PubMed  CAS  Google Scholar 

  • Burke D, Gandevia SC, Macefield G. (1988) Responses to passive movement of receptors in joint, skin and muscle of the human hand. J Physiol 402:347–361

    PubMed  CAS  Google Scholar 

  • Cadoret G, Smith AM (1995) Input-output properties of hand-related cells in the ventral cingulate cortex in the monkey. J Neurophysiol 73:2584–2590

    PubMed  CAS  Google Scholar 

  • 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 75:44–55

    Article  PubMed  CAS  Google Scholar 

  • Collins DF, Refshauge KM, Todd G, Gandevia SC (2005) Cutaneous receptors contribute to kinesthesia at the index finger, elbow, and knee. J Neurophysiol 94:1699–706

    Article  PubMed  CAS  Google Scholar 

  • Duffy FH, Burchfiel JL (1971) Somatosensory system: organizational hierarchy from single units in monkey area 5. Science 172:273–275

    Article  PubMed  CAS  Google Scholar 

  • Edin BB (2004) Quantitative analyses of dynamic strain sensitivity in human skin mechanoreceptors. J Neurophysiol 92:3233–3243

    Article  PubMed  Google Scholar 

  • Edin BB, Abbs JH (1991) Finger movement responses of cutaneous mechanoreceptors in the dorsal skin of human hand. J Neurophysiol 65:657–670

    PubMed  CAS  Google Scholar 

  • Edin BB, Johansson N (1995) Skin strain patterns provide kinaesthetic information to the human central nervous system. J Physiol 487:243–251

    PubMed  CAS  Google Scholar 

  • Edin BB, Vallbo ÅB (1988) Stretch sensitization of human muscle spindles. J Physiol 400:101–111

    PubMed  CAS  Google Scholar 

  • Edin BB, Vallbo ÅB (1990) Dynamic response of human muscle spindle afferents to stretch. J Neurophysiol 63:1297–1306

    PubMed  CAS  Google Scholar 

  • 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 83:528–536

    PubMed  CAS  Google Scholar 

  • 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 85:2613–2623

    PubMed  CAS  Google Scholar 

  • 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 90:3304–3316

    Article  PubMed  Google Scholar 

  • 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:e412

    Article  PubMed  CAS  Google Scholar 

  • Eklund G., Hagbarth KE (1966) Normal variability of tonic vibration reflexes in man. Exp Biol 16:80–92

    CAS  Google Scholar 

  • 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 43:1070–1089

    PubMed  CAS  Google Scholar 

  • Fogassi L, Ferrari PF, Gesierich B, Rozzi S, Chersi F, Rizzolatti G (2005) Parietal lobe: from action organization to intention understanding. Science 308:662–667

    Article  PubMed  CAS  Google Scholar 

  • 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 11:3656–3666

    PubMed  CAS  Google Scholar 

  • Frith C, Dolan RJ (1997) Brain mechanisms associated with top-down processes in perception. Philos Trans R Soc Lond B Biol Sci 352:1221–1230

    Article  PubMed  CAS  Google Scholar 

  • Gandevia SC (1985) Illusory movements produced by electrical stimulation of lowthreshold muscle afferents from the hand. Brain 108:965–981

    Article  PubMed  Google Scholar 

  • Gandevia SC, Smith JL, Crawford M, Proske U, Taylor JL (2006) Motor commands contribute to human position sense. J Physiol 571:703–710

    Article  PubMed  CAS  Google Scholar 

  • Ghez C, Sainburg R (1995) Proprioceptive control of interjoint coordination. Can J Physiol Pharmacol 73:273–284

    PubMed  CAS  Google Scholar 

  • 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 95:705–748

    Article  PubMed  CAS  Google Scholar 

  • Gordon J, Ghilardi MF, Ghez C (1995) Impairments of reaching movements in patients without proprioception. I. Spatial errors. J Neurophysiol 73:347–360

    PubMed  CAS  Google Scholar 

  • Graziano MS, Gross CG (1998) Spatial maps for the control of movement. Curr Opin Neurobiol 8:195–201

    Article  PubMed  CAS  Google Scholar 

  • Head H, Holmes G (1911) Sensory disturbances from cerebral lesions. Brain 34:102–254

    Article  Google Scholar 

  • 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 24:849–937

    PubMed  CAS  Google Scholar 

  • 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 39:484–500

    PubMed  CAS  Google Scholar 

  • Huerta MF, Pons TP (1990) Primary motor cortex receives input from area 3a in macaque. Brain Res 537:367–371

    Article  PubMed  CAS  Google Scholar 

  • Jackson PL, Decety J (2004) Motor cognition: a new paradigm to study self-other interaction. Curr Opin Neurobiol 14:259–263

    Article  PubMed  CAS  Google Scholar 

  • Jennings VA, Lamour Y, Solis H, Fromm C (1983) Somatosensory cortex activity related to position and force. J Neurophysiol 49:1216–1229

    PubMed  CAS  Google Scholar 

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

    Google Scholar 

  • Johansson RS, Vallbo AB (1983) Tactile sensory coding in the glabrous skin of the human hand. Trends Neurosci 6:27–32

    Article  Google Scholar 

  • Johnson-Frey SH (2004) The neural bases of complex tool use in humans. Trends Cognit Sci 8:71–78

    Article  Google Scholar 

  • Johnson-Frey SH, Newman-Norlund R, Grafton ST (2005) A distributed left hemisphere network active during planning of everyday tool use skills. Cereb Cortex 15:681–695

    Article  PubMed  Google Scholar 

  • Iriki A, Tanaka M, Iwamura Y (1996) Coding of modified body schema during tool use by macaque postcentral neurones. Neuroreport 7:2325–2330

    Article  PubMed  CAS  Google Scholar 

  • Iwamura Y (1998) Hierarchical somatosensory processing. Curr Opin Neurobiol. 8:522–528

    Article  PubMed  CAS  Google Scholar 

  • Iwamura Y, Iriki A, Tanaka M (1994) Bilateral hand representation in the postcentral somatosensory cortex. Nature (Lond) 369:554–556

    Article  PubMed  CAS  Google Scholar 

  • 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 1114:75–84

    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, Taublieb AB (1983) Reciprocal interactions between the position sense representations of the two forearms. J Neurosci 3:2280–2285

    PubMed  CAS  Google Scholar 

  • 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 36:445–462

    Article  PubMed  CAS  Google Scholar 

  • Lewis JW (2006) Cortical networks related to human use of tools. Neuroscientist 12:1–12

    Article  Google Scholar 

  • 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 91:179–193

    Article  PubMed  CAS  Google Scholar 

  • Maravita A, Iriki A (2004) Tools for the body (schema). Trends Cognit Sci 8:79–86

    Article  Google Scholar 

  • 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 

  • 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 78:2226–2230

    PubMed  CAS  Google Scholar 

  • 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 83:2580–2601

    PubMed  CAS  Google Scholar 

  • Naito E (2004) Sensing limb movements in the motor cortex: how humans sense limb movement. Neuroscientist 9:73–82

    Article  Google Scholar 

  • Naito E, Ehrsson HH (2001) Kinesthetic illusion of wrist movement activates motorrelated areas. Neuroreport 12:3805–3809

    Article  PubMed  CAS  Google Scholar 

  • Naito E, Ehrsson HH (2006) Somatic sensation of hand-object interactive movement is associated with activity in the left inferior parietal cortex. J Neurosci 26:3783–3790

    Article  PubMed  CAS  Google Scholar 

  • Naito E, Sadato N (2003) Internal simulation of expected sensory experiences before movements get started. Rev Neurosci 14:387–399

    PubMed  Google Scholar 

  • Naito E, Ehrsson HH, Geyer S, Zilles K, Roland PE (1999) Illusory arm movements activate cortical motor areas: a PET study. J Neurosci 19:6134–6144

    PubMed  CAS  Google Scholar 

  • 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 22:3683–3691

    PubMed  CAS  Google Scholar 

  • 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 

  • 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 36:979–988

    Article  PubMed  CAS  Google Scholar 

  • 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 93:1020–1034

    Article  PubMed  Google Scholar 

  • 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 210:463–472

    Article  PubMed  Google Scholar 

  • 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) 217:419–446

    PubMed  CAS  Google Scholar 

  • 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 247–272

    Google Scholar 

  • Ribot-Ciscar E, Roll JP (1998) Ago-antagonist muscle spindle inputs contribute together to joint movement coding in man. Brain Res 791:167–176

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Roland PE (1987) Somatosensory detection of microgeometry, macrogeometry and kinesthesia after localized lesions of the cerebral hemispheres in man. Brain Res 434:43–94

    PubMed  CAS  Google Scholar 

  • Roll JP, Vedel JP (1982) Kinaesthetic role of muscle afferent in man, studied by tendon vibration and microneurography. Exp Brain Res 47:177–190

    Article  PubMed  CAS  Google Scholar 

  • Roll JP, Vedel JP, Ribot E (1989) Alteration of proprioceptive messages induced by tendon vibration in man: a microneurographic study. Exp Brain Res 76:213–222

    Article  PubMed  CAS  Google Scholar 

  • Sainburg RL, Ghilardi MF, Poizner H, Ghez C (1995) Control of limb dynamics in normal participants and patients without proprioception. J Neurophysiol 73:820–835

    PubMed  CAS  Google Scholar 

  • 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 64:85–102

    Article  PubMed  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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 17:516–526

    Article  PubMed  CAS  Google Scholar 

  • 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 19:1067–1072

    Article  PubMed  CAS  Google Scholar 

  • 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 123:315–322

    Article  PubMed  CAS  Google Scholar 

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Naito, E. (2007). Neuronal Correlates of the Simulation, Execution, and Perception of Limb Movements. In: Funahashi, S. (eds) Representation and Brain. Springer, Tokyo. https://doi.org/10.1007/978-4-431-73021-7_7

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