Illusory arm movements activate cortical motor areas: A positron emission tomography study

Journal of Neuroscience

Volumn 19, Issue 14, 1999, Pages 6134-6144

  Naito, Eiichi ^a,b,e   Ehrsson, H Henrik ^a   Geyer, Stefan ^c,d   Zilles, Karl ^c,d   Roland, Per E ^a  

^a KAROLINSKA INSTITUTE   (Sweden)

^b GIFU UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^c HEINRICH HEINE UNIVERSITY   (Germany)

^d Juelich Research Center   (Germany)

^e KYOTO UNIVERSITY   (Japan)

Author keywords

Caudal part of cingulate motor cortex (CMAc); Cytoarchitectural areas 4a, 4p, 3a, 3b, and 1; Dorsal premotor cortex (PMd); Human; Kinesthetic illusion; Positron emission tomography (PET); Supplementary motor area (SMA)

Indexed keywords

BUTANOL;

ADULT; ARM MOVEMENT; ARTICLE; BRAIN BLOOD FLOW; BRAIN REGION; CINGULATE GYRUS; CONTROLLED STUDY; ELECTROMYOGRAPHY; HUMAN; HUMAN EXPERIMENT; IMAGE ANALYSIS; KINESTHESIA; MALE; MOTOR CORTEX; NORMAL HUMAN; POSITRON EMISSION TOMOGRAPHY; PREMOTOR CORTEX; PRIORITY JOURNAL; PSYCHOPHYSICS; SOMATOSENSORY CORTEX; VIBRATION;

EID: 0033565579     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.19-14-06134.1999     Document Type: Article

References (95)

1. Aizawa H, Tanji J (1994) Corticocortical and thalamocortical responses of neurons in the monkey primary motor cortex and their reaction to a trained motor task. J Neurophysiol 71:550-560.
2. Asanuma H, Larsen K, Yumiya H (1980) Peripheral input pathways to the monkey motor cortex. Exp Brain Res 38:349-355.
3. Bergström M, Boethius J, Eriksson L, Greitz T, Ribbe T, Widen L (1981) Head fixation device for reproducible position alignment in transmission CT and positron emission tomography. J Comput Assist Tomogr 5:136-141.
4. 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.
5. Burke D, Gandevia SC, Macefield G (1988) Responses to passive movement of receptors in joint, skin, and muscle of the human hand. J Physiol (Lond) 401:347-361.
6. Brinkman C, Porter R (1979) Supplementary motor area in the monkey: Activity of neurons during performance of a learned motor task. J Neurophysiol 42:681-709.
7. 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.
8. Burton H, Videen TO, Raichle ME (1993) Tactile-vibration-activated foci in insula and parietal-opercular cortex studied with positron emission tomography: mapping the second somatosensory area in humans. Somatosens Mot Res 10:297-308.
9. Buser P, Bancaud J (1967) Bases techniques et méthodologiques de l'éxploration fonctionelle stéréotaxique de télencephale. In: Atlas stéréotaxique du télencéphale (Talairach F, Szikta G, eds), pp 251-318. Paris: Masson et Cie.
10. 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.
11. Capaday C, Cooke JD (1981) The effects of muscle vibration on the attainment of intended final position during voluntary human arm movement. Exp Brain Res 42:228-230.
12. Capaday C, Cooke JD (1983) Vibration-induced changes in movement-related EMG activity in humans. Exp Brain Res 52:139-146.
13. Coghill RC, Talbot JD, Evans AC, Meyer E, Gjedde A, Bushnell MC, Duncan GH (1994) Distributed processing of pain and vibration by the human brain. J Neurosci 14:4095-4108.
14. Colebatch JG, Sayer RJ, Porter R, White OB (1990) Responses of monkey precentral neurones to passive movements and phasic muscle stretch: relevance to man. Electroencepharogr Clin Neurophysiol 75:44-55.
15. Cordo P, Gurfinkel VS, Bevan L, Kerr GK (1995) Proprioceptive consequences of tendon vibration during movement. J Neurophysiol 74:1675-1688.
16. Craske B (1977) Perception of impossible limb positions induced by tendon vibration. Science 196:71-73.
17. Crutcher MD, Alexander GE (1990) Movement-related neuronal activity selectively coding either direction or muscle pattern in three motor areas of the monkey. J Neurophysiol 64:151-163.
18. Darian-Smith C, Darian-Smith I (1993) Thalamic projections to area 3a, 3b, and 4 in the sensorimotor cortex of the mature and infant macaque monkey. J Comp Neurol 335:173-199.
19. Darian-Smith C, Darian-Smith I, Burman K, Ratcliffe N (1993) Ipsilateral cortical projections to areas 3a, 3b, and 4 in the macaque monkey. J Comp Neurol 335:200-213.
20. Dykes RW (1983) Parallel processing of somatosensory information: a theory. Brain Res Rev 6:47-115.
21. Edin BB (1990) Finger joint movement sensitivity of non-cutaneous mechanoreceptor afferents in the human radial nerve. Exp Brain Res 82:417-422.
22. Edin BB (1992) Quantitative analysis of static strain sensitivity in human mechanoreceptors from hairy skin. J Neurophysiol 67:1105-1113.
23. Edin BB, Abbs JH (1991) Finger movement responses of cutaneous mechanoreceptors in the dorsal skin of human hand. J Neurophysiol 65:657-670.
24. Edin BB, Johansson N (1995) Skin strain patterns provide kinaesthetic information to the human central nervous system. J Physiol (Lond) 487:243-251.
25. Edin BB, Vallbo ÅB (1988) Strech sensitization of human muscle spindles. J Physiol (Lond) 400:101-111.
26. Edin BB, Vallbo ÅB (1990) Dynamic response of human muscle spindle afferents to strech. J Neurophysiol 63:1297-1306.
27. Eklund G (1972) Position sense and state of contraction: the effects of vibration. J Neurol Neurosurg Psychiatry 35:606-611.
28. Eklund G, Hagbarth KE (1966) Normal variability of tonic vibration reflexes in man. Exp Neurol 16:80-92.
29. 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.
30. Fox PT, Burton H, Raichle ME (1987) Mapping human somatosensory cortex with positron emission tomography. J Neurosurg 67:34-43.
31. Frederick WJC, Schwartz MP, Smit GP (1990) Proprioceptive guidance of human voluntary wrist movements studied using muscle vibration. J Physiol (Lond) 427:455-470.
32. 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.
33. Garraghty PE, Florence SL, Kaas JH (1990) Ablations of areas 3a and 3b of monkey somatosensory cortex abolish cutaneous responsivity in area 1. Brain Res 528:165-169.
34. Geyer S, Ledberg A, Schleicher A, Kinomura S, Schomann T, Bürgel U, Klingberg T, Larsson J, Zilles K, Roland PE (1996) Two different areas within the primary motor cortex of man. Nature 382:805-807.
35. Ghosh S, Brinkman C, Porter RA (1987) A quantitative study of the distribution of neurons projecting to the precentral motor cortex in the monkey (M. fascicularis). J Comp Neurol 259:424-444.
36. Goodwin GM, McCloskey DI, Matthews PBC (1972a) 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.
37. Goodwin GM, McCloskey DI, Matthews PBC (1972b) Proprioceptive illusions induced by muscle vibration: Contribution by muscle spindles to perception? Science 175:1382-1384.
38. Greenan TJ, Strick PL (1986) Do thalamic regions which project to rostral primate motor cortex receive spinothalamic input? Brain Res 362:384-388.
39. Hadjikhani N, Roland PE (1998) Cross-modal transfer of information between the tactile and the visual representations in the human brain: a positron emission tomographic study. J Neurosci 18:1072-1084.
40. Holsapple JW, Preston JB, Strick PL (1991) The origin of thalamic inputs to the "hand" representation in the primary motor cortex. J Neurosci 11:2644-2654.
41. 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.
42. Home MK, Tracey DJ (1979) The afferents and projections of the ventroposterolateral thalamus in the monkey. Exp Brain Res 36:129-141.
43. Huerta MF, Pons TP (1990) Primary motor cortex receives input from area 3a in macaque. Brain Res 537:367-371.
44. Hummelsheim H, Bianchetti M, Wiesendanger M, Wiesendanger R (1988) Sensory inputs to agranular motor fields: a comparison between precentral, supplementary-motor and premotor areas in the monkey. Exp Brain Res 69:289-298.
45. Iwamura Y, Tanaka M, Sakamoto M, Hikosaka O (1983) Functional subdivisions representing different finger regions in area 3 of the first somatosensory cortex of the conscious monkey. Exp Brain Res 51:315-326.
46. Iwamura Y, Tanaka M, Sakamoto M, Hikosaka O (1993) Rostrocaudal gradients in the neuronal receptive field complexity in the finger region of the alert monkey's postcentral gyrus. Exp Brain Res 92:360-368.
47. Johansson RS, Landström U, Lundström R (1982) Responses of mechanoreceptive afferent units in the glabrous skin of the human hand to sinusoidal skin displacement. Brain Res 244:17-25.
48. Jones EG, Friedman DP (1982) Projection pattern of functional components of thalamic ventrobasal complex on monkey somatosensory cortex. J Neurophysiol 48:521-544.
49. Jones EG, Porter R (1980) What is area 3a? Brain Res Rev 2:1-43.
50. Landgren S, Silfvenius H (1969) Projection to cerebral cortex of group I muscle afferents from the cat's hind limb. J Physiol (Lond) 200:353-372.
51. Landgren S, Silfvenius H (1971) Nucleus Z, the medullary relay in the projection path to the cerebral cortex of group I muscle afferents from the cat's hind limb. J Physiol (Lond) 218:551-571.
52. Landgren S, Silfvenius H, Wolsk D (1967) Somato-sensory paths to the second cortical projection area of the group I muscle afferents. J Physiol (Lond) 191:543-559.
53. Lebedev MA, Nelson RJ (1996) High-frequency vibratory sensitive neurons in monkey primary somatosensory cortex: entrained and nonentrained responses to vibration during the performance of vibratorycued hand movement. Exp Brain Res 111:313-325.
54. Ledberg A, Åkerman S, Roland PE (1998) Estimation of the probabilities of 3D clusters in functional brain images. NeuroImage 8:113-128.
55. Lemon RN (1981a) Functional properties of monkey motor cortex neurones receiving afferent input from the hand and fingers. J Physiol (Lond) 311:497-519.
56. Lemon RN (1981b) Variety of functional organization within the monkey motor cortex. J Physiol (Lond) 311:521-540.
57. Lemon RN, Porter R (1976) Afferent input to movement-related precentral neurones in conscious monkeys. Proc R Soc Lond B Biol Sci 194:313-339.
58. Lemon RN, Van Der Burg J (1979) Short-latency peripheral inputs to thalamic neurons projecting the motor cortex in the monkey. Exp Brain Res 36:445-462.
59. Lemon RN, Hanby JA, Porter R (1976) Relationship between the activity of precentral neurones during active and passive movements in conscious monkeys. Proc R Soc Lond B Biol Sci 194:341-373.
60. Lim SH, Dinner DS, Pillay PK, Lüders H, Morris HH, Klem G, Wyllie E, Awad IA (1994) Functional anatomy of the human supplementary sensorimotor area: results of extraoperative electrical stimulation. Electroencepharogr Clin Neurophysiol 91:179-193.
61. Macefield G, Gandevia SC, Burke D (1990) Perceptual responses to microstimulation of single afferents innervating joints, muscles and skin of the human hand. J Physiol (Lond) 429:113-129.
62. Maendly R, Ruegg DG, Wiesendanger M, Wiesendanger R, Lagowska J, Hess B (1981) Thalamic relay for group I muscle afferents of forelimb nerves in the monkey. J Neurophysiol 46:901-917.
63. 15O autoradiographic method and dynamic PET. J Nucl Med 30:1069-1078.
64. 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.
65. Picard N, Smith AM (1992) Primary motor cortical responses to perturbations of prehension in the monkey. J Neurophysiol 68:1882-1894.
66. Pons TP, Garraghty PE, Mishkin M (1992) Serial and parallel processing of tactual information in somatosensory cortex of rhesus monkey. J Neurophysiol 68:518-527.
67. Rasmusson DD, Dykes RW, Hoeltzell PB (1979) Segregation of modality and submodality information in SI cortex of cat. Brain Res 166:409-412.
68. Recanzone GH, Merzenich MM, Jenkins WM, Grajski KA, Dinse HR (1992) Topographic reorganization of the hand representation in cortical area 3b of owl monkeys trained in a frequency-discrimination task. J Neurophysiol 67:1031-1056.
69. Ribot-Ciscar E, Roll JP (1998) Ago-antagonist muscle spindle inputs contribute together to joint movement coding in man. Brain Res 791:167-176.
70. Rogers DK, Bendrups AP, Lewis MM (1985) Disturbed proprioception following a period of muscle vibration in humans. Neurosci Lett 57:147-152.
71. Roland PE, Zilles K (1996) Functions and structures of the motor cortices in humans. Curr Opin Neurobiol 6:773-781.
72. Roland PE, Zilles K (1998) Structural divisions and functional fields in the human cerebral cortex. Brain Res Rev 26:87-105.
73. Roland PE, Graufeld CJ, Wåhlin J, Ingelman L, Andersson M, Ledberg A, Pedersen J, Åkerman S, Dabringhaus A, Zilles K (1994) Human Brain Atlas: for high-resolution functional and anatomical mapping. Hum Brain Mapp 1:173-184.
74. Roland PE, Geyer S, Amunts K, Schormann T, Schleicher A, Malikovic A, Zilles K (1997) Cytoarchitectural maps of the human brain in standard anatomical space. Hum Brain Mapp 5:222-227.
75. Roll JP, Vedel JP (1982) Kinaesthetic role of muscle afferent in man, Studied by tendon vibration and microneurography. Exp Brain Res 47:177-190.
76. Romo R, Hernandez A, Zainos A, Salinas E (1998) Somatosensory discrimination based on cortical microstimulation. Nature 392:387-390.
77. Rosén I, Asanuma H (1972) Peripheral afferent inputs to the forelimb area of the monkey motor cortex: Input-output relations. Exp Brain Res 14:257-273.
78. Schell GR, Strick PL (1984) The origin of thalamic inputs to the arcuate premotor and supplementary motor areas. J Neurosci 4:539-560.
79. Schleicher A, Amunts K, Geyer S, Morosan P, Zilles K (1999) Observerindependent method for microstructure parcellation of cerebral cortex: a quantitative approach to cytoarchitectonics. NeuroImage 9:165-177.
80. Seitz RJ, Roland PE (1992) Vibratory stimulation increases and decreases the regional cerebral blood flow and oxidative metabolism: a positron emission tomography (PET) study. Acta Neurol Scand 86:60-67.
81. Stepniewska I, Preuss TM, Kaas JH (1993) Architectonics, somatotopic organization, and ipsilateral cortical connections of the primary motor area (M1) of owl monkeys. J Comp Neurol 330:238-271.
82. Strick PL, Preston JB (1982) Two representations of the hand in area 4 of a primate. II. Somatosensory input organisation. J Neurophysiol 48:150-159.
83. Tanji J, Wise SP (1981) Submodality distribution in sensori-motor cortex of the unanesthetized monkey. J Neurophysiol 45:467-481.
84. Tardy-gervet MF, Gilhodes JC, Roll JP (1986) Interaction between visual and muscular information in illusions of limb movement. Behav Brain Res 20:161-174.
85. Tootell RBH, Reppas JB, Dale AM, Look RB, Sereno MI, Malach R, Brady TJ, Rosen BR (1995) Visual motion aftereffect in human cortical area MT revealed by functional magnetic resonance imaging. Nature 375:139-141.
86. Vallbo ÅB (1974) Afferent discharge from human muscle spindles in non-contracting muscle. Steady state impulse frequency as function of joint angle. Acta Physiol Scand 90:303-318.
87. Vallbo ÅB, Olausson H, Wessberg J, Kakuda N (1995) Receptive field characteristics of tactile units with myelinated afferents in hairy skin of human subjects. J Physiol (Lond) 483:783-795.
88. Weiller C, Juptner M, Fellows S, Rijntjes M, Leonhardt G, Kiebel S, Muller S, Diener HC, Thilmann AF (1996) Brain representation of active and passive movements. NeuroImage 4:105-110.
89. Wiesendanger M (1986) Recent developments in studies of the supplementary motor area of primates. Rev Physiol Biochem Pharmacol 103:1-59.
90. Wiesendanger M, Hummlesheim H, Bianchetti M (1985) Sensory input to the motor fields of the agranular frontal cortex: a comparison of the precentral, supplementary motor and premotor cortex. Behav Brain Res 18:89-94.
91. Widener GL, Cheney PD (1997) Effects on muscle activity from microstimuli applied to somatosensory and motor cortex during voluntary movement in the monkey. J Neurophysiol 77:2446-2465.
92. Wise SP, Tanji J (1981) Supplementary and precentral motor cortex: Contrast in responsiveness to peripheral input in the hindlimb area of the unanesthetized monkey. J Comp Neurol 195:433-451.
93. Wong YC, Kwan HC, MacKay WA, Murphy JT (1978) Spatial organization of precentral cortex in awake primates. I. Somatosensory inputs. J Neurophysiol 41:1107-1119.
94. Woods RP, Cherry SR, Mazziotta JC (1992) Rapid automated algorithm for aligning and reslicing PET images. J Comput Assist Tomogr 16:620-633.
95. Zeki S, Watson JD, Frackowiak RS (1993) Going beyond the information given: the relation of illusory visual motion to brain activity. Proc R Soc Lond B Biol Sci 252:215-222.