Long-lasting cortical reorganization as the result of motor imagery of throwing a ball in a virtual tennis court

Frontiers in Psychology

Volumn 6, Issue DEC, 2015, Pages

  Cebolla, Ana M ^a   Petieau, Mathieu ^a   Cevallos, Carlos ^a   Leroy, Axelle ^a   Dan, Bernard ^b   Cheron, Guy ^a,c,d  

^a UNIVERSITÉ LIBRE DE BRUXELLES   (Belgium)

^b HOP UNIV DES ENFANTS REINE FABIOLA   (Belgium)

^c Haute Ecole Condorcet   (Belgium)

^d UNIVERSITY OF MONS   (Belgium)

Author keywords

Beta; EEG; ERD; ERSP; ITC; Motor imagery; N300; Virtual reality

Indexed keywords

EID: 84954285544     PISSN: None     EISSN: 16641078     Source Type: Journal    
DOI: 10.3389/fpsyg.2015.01869     Document Type: Article

References (88)

1. Abbruzzese, G., Assini, A., Buccolieri, A., Marchese, R., and Trompetto, C. (1999). Changes of intracortical inhibition during motor imagery in human participants. Neurosci. Lett. 263, 113-116. doi: 10.1016/S0304-3940(99)00120-2
2. Basar, E., Basar-Eroglu, C., Karakas, S., and Schürmann, M. (1999). Oscillatory brain theory: a new trend in neuroscience. IEEE Eng. Med. Biol. Mag. 18, 56-66. doi: 10.1109/51.765190
3. Bastos, T. F., Muller, S. M. T., Benevides, A. B., and Sarcinelli-Filho, M. (2011). Robotic wheelchair commanded by SSVEP, motor imagery and word generation. Conf. Proc. IEEE Eng. Med. Biol. Soc. 2011, 4753-4756. doi: 10.1109/IEMBS.2011.6091177
4. Beisteiner, R., Höllinger, P., Lindinger, G., Lang, W., and Berthoz, A. (1995). Mental representations of movements. Brain potentials associated with imagination of hand movements. Electroencephalogr. Clin. Neurophysiol. 96, 183-193. doi: 10.1016/0168-5597(94)00226-5
5. Brinkman, L., Stolk, A., Dijkerman, H. C., de Lange, F. P., and Toni, I. (2014). Distinct roles for alpha- and beta-band oscillations during mental simulation of goal-directed actions. J. Neurosci. 34, 14783-14792. doi: 10.1523/JNEUROSCI.2039-14.2014
6. Butler, A. J., Cazeaux, J., Fidler, A., Jansen, J., Lefkove, N., Gregg, M., et al. (2012). The movement imagery questionnaire-revised, second edition (MIQ-RS) is a reliable and valid tool for evaluating motor imagery in stroke populations. Evid. Based Complement. Alternat. Med. 2012, 497289. doi: 10.1155/2012/497289
7. Cebolla, A. M., Palmero-Soler, E., Dan, B., and Cheron, G. (2014). Modulation of the N30 generators of the somatosensory evoked potentials by the mirror neuron system. Neuroimage 95, 48-60. doi: 10.1016/j.neuroimage.2014.03.039
8. Cebolla, A. M., Palmero-Soler, E., Dan, B., and Cheron, G. (2011). Frontal phasic and oscillatory generators of the N30 somatosensory evoked potential. Neuroimage 54, 1297-1306. doi: 10.1016/j.neuroimage.2010.08.060
9. Chen, X., Bin, G., Daly, I., and Gao, X. (2013). Event-related desynchronization (ERD) in the alpha band during a hand mental rotation task. Neurosci. Lett. 541, 238-242. doi: 10.1016/j.neulet.2013.02.036
10. Cheron, G., and Borenstein, S. (1992). Mental movement simulation affects the N30 frontal component of the somatosensory evoked potential. Electroencephalogr. Clin. Neurophysiol. 84, 288-292. doi: 10.1016/0168-5597(92)90010-9
11. Cheron, G., Cebolla, A. M., Petieau, M., Bengoetxea, A., Palmero-Soler, E., Leroy, A., et al. (2009). Adaptive changes of rhythmic EEG oscillations in space implications for brain-machine interface applications. Int. Rev. Neurobiol. 86, 171-187. doi: 10.1016/S0074-7742(09)86013-3
12. Cheron, G., Leroy, A., Palmero-Soler, E., De Saedeleer, C., Bengoetxea, A., Cebolla, A.-M., et al. (2014). Gravity influences top-down signals in visual processing. PLoS ONE 9:e82371. doi: 10.1371/journal.pone.0082371
13. Cramer, S. C., Orr, E. L. R., Cohen, M. J., and Lacourse, M. G. (2007). Effects of motor imagery training after chronic, complete spinal cord injury. Exp. Brain Res. 177, 233-242. doi: 10.1007/s00221-006-0662-9
14. Cunnington, R., Iansek, R., Bradshaw, J. L., and Phillips, J. G. (1996). Movement-related potentials associated with movement preparation and motor imagery. Exp. Brain Res. 111, 429-436. doi: 10.1007/BF00228732
15. Debruille, J. B., Brodeur, M. B., and Franco Porras, C. (2012). N300 and social affordances: a study with a real person and a dummy as stimuli. PLoS ONE 7:e47922. doi: 10.1371/journal.pone.0047922
16. Decety, J. (1996). Neural representations for action. Rev. Neurosci. 7, 285-297. doi: 10.1515/REVNEURO.1996.7.4.285
17. Dechent, P., Merboldt, K.-D., and Frahm, J. (2004). Is the human primary motor cortex involved in motor imagery? Brain Res. Cogn. Brain Res. 19, 138-144. doi: 10.1016/j.cogbrainres.2003.11.012
18. Deiber, M. P., Ibañez, V., Honda, M., Sadato, N., Raman, R., and Hallett, M. (1998). Cerebral processes related to visuomotor imagery and generation of simple finger movements studied with positron emission tomography. Neuroimage 7, 73-85. doi: 10.1006/nimg.1997.0314
19. de Lange, F. P., Jensen, O., Bauer, M., and Toni, I. (2008). Interactions between posterior gamma and frontal alpha/beta oscillations during imagined actions. Front. Hum. Neurosci. 2:7. doi: 10.3389/neuro.09.007.2008
20. Delorme, A., and Makeig, S. (2004). EEGLAB: an open source toolbox for analysis of single-trial EEG dynamics including independent component analysis. J. Neurosci. Methods 134, 9-21. doi: 10.1016/j.jneumeth.2003.10.009
21. Dijkerman, H. C., Ietswaart, M., Johnston, M., and MacWalter, R. S. (2004). Does motor imagery training improve hand function in chronic stroke patients? A pilot study. Clin. Rehabil. 18, 538-549. doi: 10.1191/0269215504cr769oa
22. Di Rienzo, F., Blache, Y., Kanthack, T. F. D., Monteil, K., Collet, C., and Guillot, A. (2015). Short-term effects of integrated motor imagery practice on muscle activation and force performance. Neuroscience 305, 146-156. doi: 10.1016/j.neuroscience.2015.07.080
23. Dyck, M., and Brodeur, M. B. (2015). ERP evidence for the influence of scene context on the recognition of ambiguous and unambiguous objects. Neuropsychologia 72, 43-51. doi: 10.1016/j.neuropsychologia.2015.04.023
24. Eimer, M. (1993). Effects of attention and stimulus probability on ERPs in a Go/Nogo task. Biol. Psychol. 35, 123-138. doi: 10.1016/0301-0511(93)90009-W
25. Falkenstein, M., Hoormann, J., and Hohnsbein, J. (1999). ERP components in Go/Nogo tasks and their relation to inhibition. Acta Psychol. (Amst.) 101, 267-291. doi: 10.1016/S0001-6918(99)00008-6
26. Filippi, M. M., Oliveri, M., Pasqualetti, P., Cicinelli, P., Traversa, R., Vernieri, F., et al. (2001). Effects of motor imagery on motor cortical output topography in Parkinson's disease. Neurology 57, 55-61. doi: 10.1212/WNL.57.1.55
27. Friedrich, E. V. C., Scherer, R., and Neuper, C. (2013). Stability of event-related (de-) synchronization during brain-computer interface-relevant mental tasks. Clin. Neurophysiol. 124, 61-69. doi: 10.1016/j.clinph.2012.05.020
28. Friston, K. J. (1997). Another neural code? Neuroimage 5, 213-220. doi: 10.1006/nimg.1997.0260
29. Friston, K. J., Stephan, K. M., and Frackowiak, R. S. (1997). Transient phase-locking and dynamic correlations: Are they the same thing? Hum. Brain Mapp. 5, 48-57. doi: 10.1002/(SICI)1097-0193(1997)5:1<48::AID-HBM5>;3.0.CO;2-N
30. Gama, R. L., Bruin, V. M. S., Távora, D. G. F., Duran, F. L. S., Bittencourt, L., and Tufik, S. (2014). Structural brain abnormalities in patients with Parkinson's disease with visual hallucinations: a comparative voxel-based analysis. Brain Cogn. 87, 97-103. doi: 10.1016/j.bandc.2014.03.011
31. Gerardin, E., Sirigu, A., Lehéricy, S., Poline, J. B., Gaymard, B., Marsault, C., et al. (2000). Partially overlapping neural networks for real and imagined hand movements. Cereb. Cortex 10, 1093-1104. doi: 10.1093/cercor/10.11.1093
32. Geronimo, A., Schiff, S. J., and Kamrunnahar, M. (2012). Visual evoked potentials for attentional gating in a brain-computer interface. Conf. Proc. IEEE Eng. Med. Biol. Soc. 2012, 1745-1748. doi: 10.1109/EMBC.2012.6346286
33. Grafton, S. T., Arbib, M. A., Fadiga, L., and Rizzolatti, G. (1996). Localization of grasp representations in humans by positron emission tomography. 2. Observation compared with imagination. Exp. Brain Res. 112, 103-111. doi: 10.1007/BF00227183
34. Grangeon, M., Revol, P., Guillot, A., Rode, G., and Collet, C. (2012). Could motor imagery be effective in upper limb rehabilitation of individuals with spinal cord injury? A case study. Spinal Cord 50, 766-771. doi: 10.1038/sc.2012.41
35. Guillot, A., Collet, C., Nguyen, V. A., Malouin, F., Richards, C., and Doyon, J. (2008). Functional neuroanatomical networks associated with expertise in motor imagery. Neuroimage 41, 1471-1483. doi: 10.1016/j.neuroimage.2008.03.042
36. Gusnard, D. A., Raichle, M. E., and Raichle, M. E. (2001). Searching for a baseline: functional imaging and the resting human brain. Nat. Rev. Neurosci. 2, 685-694. doi: 10.1038/35094500
37. Hall, C. R., and Martin, K. A. (1997). Measuring movement imagery abilities: a revision of the Movement Imagery Questionnaire. J. Ment. Image. 21, 143-154.
38. Hamm, J. P., Johnson, B. W., and Kirk, I. J. (2002). Comparison of the N300 and N400 ERPs to picture stimuli in congruent and in congruent contexts. Clin. Neurophysiol. 113, 1339-1350. doi: 10.1016/S1388-2457(02)00161-X
39. Hanakawa, T., Immisch, I., Toma, K., Dimyan, M. A., Van Gelderen, P., and Hallett, M. (2003). Functional properties of brain areas associated with motor execution and imagery. J. Neurophysiol. 89, 989-1002. doi: 10.1152/jn.00132.2002
40. Hashimoto, Y., and Ushiba, J. (2013). EEG-based classification of imaginary left and right foot movements using beta rebound. Clin. Neurophysiol. 124, 2153-2160. doi: 10.1016/j.clinph.2013.05.006
41. Hasson, U., and Malach, R. (2006). Human brain activation during viewing of dynamic natural scenes. Novartis Found. Symp. 270, 203-212; discussion 212-216, 232-237. doi: 10.1002/9780470034989.ch16
42. Holm, S. (1979). A simple sequentially rejective multiple test procedure. Scand. J. Stat. 6, 65-70.
43. Jeannerod, M. (1994). The representing brain: neural correlates of motor intention and imagery. Behav. Brain Sci. 17, 187-202. doi: 10.1017/S0140525X00034026
44. Jeannerod, M., and Decety, J. (1995). Mental motor imagery: a window into the representational stages of action. Curr. Opin. Neurobiol. 5, 727-732. doi: 10.1016/0959-4388(95)80099-9
45. Jiang, D., Edwards, M. G., Mullins, P., and Callow, N. (2015). The neural substrates for the different modalities of movement imagery. Brain Cogn. 97, 22-31. doi: 10.1016/j.bandc.2015.04.005
46. Jodo, E., and Kayama, Y. (1992). Relation of a negative ERP component to response inhibition in a Go/No-go task. Electroencephalogr. Clin. Neurophysiol. 82, 477-482. doi: 10.1016/0013-4694(92)90054-L
47. Jonas, J., Frismand, S., Vignal, J.-P., Colnat-Coulbois, S., Koessler, L., Vespignani, H., et al. (2014). Right hemispheric dominance of visual phenomena evoked by intracerebral stimulation of the human visual cortex. Hum. Brain Mapp. 35, 3360-3371. doi: 10.1002/hbm.22407
48. Kopp, B., Mattler, U., Goertz, R., and Rist, F. (1996). N2, P3 and the lateralized readiness potential in a nogo task involving selective response priming. Electroencephalogr. Clin. Neurophysiol. 99, 19-27. doi: 10.1016/0921-884X(96)95617-9
49. Krippl, M., Karim A. A., and Brechmann, A. (2015). Neuronal correlates of voluntary facial movements. Front. Hum. Neurosci. 9:598. doi: 10.3389/fnhum.2015.00598
50. Lachaux, J. P., Rodriguez, E., Martinerie, J., and Varela, F. J. (1999). Measuring phase synchrony in brain signals. Hum. Brain Mapp. 8, 194-208.
51. Llanos, C., Rodriguez, M., Rodriguez-Sabate, C., Morales, I., and Sabate, M. (2013). Mu-rhythm changes during the planning of motor and motor imagery actions. Neuropsychologia 51, 1019-1026. doi: 10.1016/j.neuropsychologia.2013.02.008
52. Lotze, M., Montoya, P., Erb, M., Hülsmann, E., Flor, H., Klose, U., et al. (1999). Activation of cortical and cerebellar motor areas during executed and imagined hand movements: an fMRI study. J. Cogn. Neurosci. 11, 491-501. doi: 10.1162/089892999563553
53. Machado, S., Arias-Carrión, O., Paes, F., Ribeiro, P., Cagy, M., Piedade, R., et al. (2013). Changes in cortical activity during real and imagined movements: an ERP study. Clin. Pract. Epidemiol. Ment. Health 9, 196-201. doi: 10.2174/1745017901309010196
54. Makeig, S. (1993). Auditory event-related dynamics of the EEG spectrum and effects of exposure to tones. Electroencephalogr. Clin. Neurophysiol. 86, 283-293. doi: 10.1016/0013-4694(93)90110-H
55. McFarland, D. J., Miner, L. A., Vaughan, T. M., and Wolpaw, J. R. (2000). Mu and beta rhythm topographies during motor imagery and actual movements. Brain Topogr. 12, 177-186. doi: 10.1023/A:1023437823106
56. Meister, I. G., Krings, T., Foltys, H., Boroojerdi, B., Müller, M., Töpper, R., et al. (2004). Playing piano in the mind-an fMRI study on music imagery and performance in pianists. Brain Res. Cogn. Brain Res. 19, 219-228. doi: 10.1016/j.cogbrainres.2003.12.005
57. Missonnier, P., Deiber, M.-P., Gold, G., Millet, P., Gex-Fabry Pun, M., Fazio-Costa, L., et al. (2006). Frontal theta event-related synchronization: comparison of directed attention and working memory load effects. J. Neural Transm. (Vienna) 113, 1477-1486. doi: 10.1007/s00702-005-0443-9
58. Naito, E., Kochiyama, T., Kitada, R., Nakamura, S., Matsumura, M., Yonekura, Y., et al. (2002). Internally simulated movement sensations during motor imagery activate cortical motor areas and the cerebellum. J. Neurosci. 22, 3683-3691.
59. Neuper, C., Scherer, R., Reiner, M., and Pfurtscheller, G. (2005). Imagery of motor actions: differential effects of kinesthetic and visual-motor mode of imagery in single-trial EEG. Brain Res. Cogn. Brain Res. 25, 668-677. doi: 10.1016/j.cogbrainres.2005.08.014
60. Nolte, G., Bai, O., Wheaton, L., Mari, Z., Vorbach, S., and Hallett, M. (2004). Identifying true brain interaction from EEG data using the imaginary part of coherency. Clin. Neurophysiol. 115, 2292-2307. doi: 10.1016/j.clinph.2004.04.029
61. Ocklenburg, S., Güntürkün, O., and Beste, C. (2011). Lateralized neural mechanisms underlying the modulation of response inhibition processes. Neuroimage 55, 1771-1778. doi: 10.1016/j.neuroimage.2011.01.035
62. Oldfield, R. C. (1971). The assessment, and analysis of handedness: the Edinburgh inventory. Neuropsychologia 9, 97-113. doi: 10.1016/0028-3932(71)90067-4
63. Osuagwu, B. A., and Vuckovic, A. (2014). Similarities between explicit and implicit motor imagery in mental rotation of hands: an EEG study. Neuropsychologia 65, 197-210. doi: 10.1016/j.neuropsychologia.2014.10.029
64. Pfefferbaum, A., Ford, J. M., Weller, B. J., and Kopell, B. S. (1985). ERPs to response production and inhibition. Electroencephalogr. Clin. Neurophysiol. 60, 423-434. doi: 10.1016/0013-4694(85)91017-X
65. Pfurtscheller, G., Allison, B. Z., Brunner, C., Bauernfeind, G., Solis-Escalante, T., Scherer, R., et al. (2010). The hybrid BCI. Front. Neurosci. 4:30. doi: 10.3389/fnpro.2010.00003
66. Pfurtscheller, G., and Neuper, C. (1994). Event-related synchronization of mu rhythm in the EEG over the cortical hand area in man. Neurosci. Lett. 174, 93-96. doi: 10.1016/0304-3940(94)90127-9
67. Pfurtscheller, G., Solis-Escalante, T., Barry, R. J., Klobassa, D. S., Neuper, C., and Müller-Putz, G. R. (2013). Brisk heart rate and EEG changes during execution and withholding of cue-paced foot motor imagery. Front. Hum. Neurosci. 7:379. doi: 10.3389/fnhum.2013.00379
68. Porro, C. A., Francescato, M. P., Cettolo, V., Diamond, M. E., Baraldi, P., Zuiani, C., et al. (1996). Primary motor and sensory cortex activation during motor performance and motor imagery: a functional magnetic resonance imaging study. J. Neurosci. 16, 7688-7698.
69. Ridderinkhof, K. R., and Brass, M. (2015). How Kinesthetic Motor Imagery works: a predictive-processing theory of visualization in sports and motor expertise. J. Physiol. Paris 109, 53-63. doi: 10.1016/j.jphysparis.2015.02.003
70. Romero, D. H., Lacourse, M. G., Lawrence, K. E., Schandler, S., and Cohen, M. J. (2000). Event-related potentials as a function of movement parameter variations during motor imagery and isometric action. Behav. Brain Res. 117, 83-96. doi: 10.1016/S0166-4328(00)00297-7
71. Rossini, P. M., Rossi, S., Pasqualetti, P., and Tecchio, F. (1999). Corticospinal excitability modulation to hand muscles during movement imagery. Cereb. Cortex 9, 161-167. doi: 10.1093/cercor/9.2.161
72. Schendan, H. E., and Kutas, M. (2007). Neurophysiological evidence for the time course of activation of global shape, part, and local contour representations during visual object categorization and memory. J. Cogn. Neurosci. 19, 734-749. doi: 10.1162/jocn.2007.19.5.734
73. Singer, W. (1999). Neuronal synchrony: a versatile code for the definition of relations? Neuron 24, 49-65, 111-125. doi: 10.1016/S0896-6273(00)80821-1
74. Sirigu, A., Duhamel, J. R., Cohen, L., Pillon, B., Dubois, B., and Agid, Y. (1996). The mental representation of hand movements after parietal cortex damage. Science 273, 1564-1568. doi: 10.1126/science.273.5281.1564
75. Sitnikova, T., Holcomb, P. J., Kiyonaga, K. A., and Kuperberg, G. R. (2008). Two neurocognitive mechanisms of semantic integration during the comprehension of visual real-world events. J. Cogn. Neurosci. 20, 2037-2057. doi: 10.1162/jocn.2008.20143
76. Stinear, C. M., Fleming, M. K., and Byblow, W. D. (2006). Lateralization of unimanual and bimanual motor imagery. Brain Res. 1095, 139-147. doi: 10.1016/j.brainres.2006.04.008
77. Tabrizi, Y. M., Mazhari, S., Nazari, M. A., Zangiabadi, N., Sheibani, V., and Azarang, S. (2013). Compromised motor imagery ability in individuals with multiple sclerosis and mild physical disability: an ERP study. Clin. Neurol. Neurosurg. 115, 1738-1744. doi: 10.1016/j.clineuro.2013.04.002
78. Tallon-Baudry, C., Bertrand, O., Delpuech, C., and Pernier, J. (1996). Stimulus specificity of phase-locked and non-phase-locked 40 Hz visual responses in human. J. Neurosci. 16, 4240-4249.
79. Thomas, E., Fruitet, J., and Clerc, M. (2012). Investigating brief motor imagery for an ERD/ERS based BCI. Conf. Proc. IEEE Eng. Med. Biol. Soc. 2012, 2929-2932. doi: 10.1109/EMBC.2012.6346577
80. Tononi, G., and Edelman, G. M. (1998). Consciousness and the integration of information in the brain. Adv. Neurol. 77, 245-279; discussion 279-280.
81. Volz, M. S., Suarez-Contreras, V., Portilla, A. L. S., and Fregni, F. (2015). Mental imagery-induced attention modulates pain perception and cortical excitability. BMC Neurosci. 16:15. doi: 10.1186/s12868-015-0146-6
82. Vucinovic, M., Kardum, G., Bonkovic, M., Resic, B., Ursic, A., and Vukovics, J. (2014). Sleep EEG composition in the first three months of life in monozygotic and dizygotic twins. Clin. EEG Neurosci. 45, 193-200. doi: 10.1177/1550059413497000
83. Wang, Z., Wang, S., Shi, F.-Y., Guan, Y., Wu, Y., Zhang, L.-L., et al. (2014). The effect of motor imagery with specific implement in expert badminton player. Neuroscience 275, 102-112. doi: 10.1016/j.neuroscience.2014.06.004
84. Yahagi, S., and Kasai, T. (1999). Motor evoked potentials induced by motor imagery reveal a functional asymmetry of cortical motor control in left- and right-handed human participants. Neurosci. Lett. 276, 185-188. doi: 10.1016/S0304-3940(99)00823-X
85. Yi, W., Qiu, S., Qi, H., Zhang, L., Wan, B., and Ming, D. (2013). EEG feature comparison and classification of simple and compound limb motor imagery. J. Neuroeng. Rehabil. 10, 106. doi: 10.1186/1743-0003-10-106
86. Zhang, R., Li, Y., Yan, Y., Zhang, H., Wu, S., and Yu, T. (2015). Control of a wheelchair in an indoor environment based on a brain-computer interface and automated navigation. IEEE Trans. Neural Syst. Rehabil. Eng. doi: 10.1109/tnsre.2015.2439298 [Epub ahead of print].
87. Zhou, Z., and Wan, B. (2012). Wavelet packet-based independent component analysis for feature extraction from motor imagery EEG of complex movements. Clin. Neurophysiol. 123, 1779-1788. doi: 10.1016/j.clinph.2012.02.071
88. Zich, C., Debener, S., De Vos, M., Frerichs, S., Maurer, S., and Kranczioch, C. (2015). Lateralization patterns of covert but not overt movements change with age: an EEG neurofeedback study. Neuroimage 116, 80-91. doi: 10.1016/j.neuroimage.2015.05.009