Enhanced Activation of Motor Execution Networks Using Action Observation Combined with Imagination of Lower Limb Movements

PLoS ONE

Volumn 8, Issue 8, 2013, Pages

  Villiger, Michael ^a,b,c   Estévez, Natalia ^b   Hepp Reymond, Marie Claude ^c   Kiper, Daniel ^c   Kollias, Spyros S ^b   Eng, Kynan ^c   Hotz Boendermaker, Sabina ^a  

^a BALGRIST UNIVERSITY HOSPITAL   (Switzerland)

^b UNIVERSITY HOSPITAL ZURICH   (Switzerland)

^c UNIVERSITY OF ZURICH   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

ADULT; ARTICLE; AWARENESS; BRAIN FUNCTION; BRAIN REGION; EXECUTIVE FUNCTION; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; GOAL ATTAINMENT; HUMAN; HUMAN EXPERIMENT; IMAGINATION; IMITATION; INFERIOR PARIETAL LOBULE; INSULA; INTERMETHOD COMPARISON; LEFT HEMISPHERE; LIMB MOVEMENT; MALE; NORMAL HUMAN; OBSERVATION; ONLINE SYSTEM; PREMOTOR CORTEX; PSYCHOMOTOR ACTIVITY; VIDEORECORDING;

ADOLESCENT; ADULT; BRAIN MAPPING; EXECUTIVE FUNCTION; FEMALE; FOOT; HUMANS; IMAGERY (PSYCHOTHERAPY); IMAGINATION; LEG; MAGNETIC RESONANCE IMAGING; MALE; MOTOR CORTEX; MOVEMENT; PARIETAL LOBE; PHOTIC STIMULATION; PSYCHOMOTOR PERFORMANCE; YOUNG ADULT;

EID: 84883170299     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0072403     Document Type: Article

References (78)

1. Jeannerod M, (2001) Neural simulation of action: a unifying mechanism for motor cognition. Neuroimage 14: 103-109.
2. Nedelko V, Hassa T, Hamzei F, Schoenfeld MA, Dettmers C, (2012) Action imagery combined with action observation activates more corticomotor regions than action observation alone. J Neurol Phys Ther 36: 182-188.
3. Munzert J, Lorey B, Zentgraf K, (2009) Cognitive motor processes: the role of motor imagery in the study of motor representations. Brain Res Rev 60: 306-326.
4. Adamovich SV, Fluet GG, Tunik E, Merians AS, (2009) Sensorimotor training in virtual reality: a review. NeuroRehabilitation 25: 29-44.
5. Bohil CJ, Alicea B, Biocca FA, (2011) Virtual reality in neuroscience research and therapy. Nat Rev Neurosci 12: 752-762.
6. Villiger M, Hepp-Reymond MC, Pyk P, Kiper D, Spillman J, et al. (2011) Virtual reality rehabilitation system for neuropathic pain and motor dysfunction in spinal cord injury patients. Proc Int Conf on Virtual Rehab: doi: 10.1109/ICVR.2011.5971865.
7. Villiger M, Bohli D, Kiper D, Pyk P, Spillmann J, et al. (2013) Virtual Reality-Augmented Neurorehabilitation Improves Motor Function and Reduces Neuropathic Pain in Patients With Incomplete Spinal Cord Injury. Neurorehabil Neural Repair: doi: 10.1177/1545968313490999.
8. Cross ES, Hamilton AF, Grafton ST, (2006) Building a motor simulation de novo: observation of dance by dancers. Neuroimage 31: 1257-1267.
9. Simmons L, Sharma N, Baron JC, Pomeroy VM, (2008) Motor imagery to enhance recovery after subcortical stroke: who might benefit, daily dose, and potential effects. Neurorehabil Neural Repair 22: 458-467.
10. Macuga KL, Frey SH, (2012) Neural representations involved in observed, imagined, and imitated actions are dissociable and hierarchically organized. Neuroimage 59: 2798-2807.
11. Wang C, Wai Y, Weng Y, Yu J, Wang J, (2008) The cortical modulation from the external cues during gait observation and imagination. Neurosci Lett 443: 232-235.
12. Alkadhi H, Brugger P, Boendermaker SH, Crelier G, Curt A, et al. (2005) What disconnection tells about motor imagery: evidence from paraplegic patients. Cereb Cortex 15: 131-140.
13. Aziz-Zadeh L, Wilson SM, Rizzolatti G, Iacoboni M, (2006) Congruent embodied representations for visually presented actions and linguistic phrases describing actions. Curr Biol 16: 1818-1823.
14. Buccino G, Binkofski F, Fink GR, Fadiga L, Fogassi L, et al. (2001) Action observation activates premotor and parietal areas in a somatotopic manner: an fMRI study. Eur J Neurosci 13: 400-404.
15. Catmur C, Gillmeister H, Bird G, Liepelt R, Brass M, et al. (2008) Through the looking glass: counter-mirror activation following incompatible sensorimotor learning. Eur J Neurosci 28: 1208-1215.
16. Chaminade T, Meltzoff AN, Decety J, (2005) An fMRI study of imitation: action representation and body schema. Neuropsychologia 43: 115-127.
17. Cramer SC, Lastra L, Lacourse MG, Cohen MJ, (2005) Brain motor system function after chronic, complete spinal cord injury. Brain 128: 2941-2950.
18. Cramer SC, Orr EL, Cohen MJ, Lacourse MG, (2007) Effects of motor imagery training after chronic, complete spinal cord injury. Exp Brain Res 177: 233-242.
19. 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.
20. Enzinger C, Ropele S, Fazekas F, Loitfelder M, Gorani F, et al. (2008) Brain motor system function in a patient with complete spinal cord injury following extensive brain-computer interface training. Exp Brain Res 190: 215-223.
21. Gustin SM, Wrigley PJ, Henderson LA, Siddall PJ, (2010) Brain circuitry underlying pain in response to imagined movement in people with spinal cord injury. Pain 148: 438-445.
22. Hotz-Boendermaker S, Funk M, Summers P, Brugger P, Hepp-Reymond MC, et al. (2008) Preservation of motor programs in paraplegics as demonstrated by attempted and imagined foot movements. Neuroimage 39: 383-394.
23. Hotz-Boendermaker S, Hepp-Reymond MC, Curt A, Kollias SS, (2011) Movement observation activates lower limb motor networks in chronic complete paraplegia. Neurorehabil Neural Repair 25: 469-476.
24. Jackson PL, Meltzoff AN, Decety J, (2006) Neural circuits involved in imitation and perspective-taking. Neuroimage 31: 429-439.
25. Jastorff J, Begliomini C, Fabbri-Destro M, Rizzolatti G, Orban GA, (2010) Coding observed motor acts: different organizational principles in the parietal and premotor cortex of humans. J Neurophysiol 104: 128-140.
26. Jastorff J, Abdollahi RO, Orban GA (2012) Acting Alters Visual Processing: Flexible Recruitment of Visual Areas by One's Own Actions. Cereb Cortex: doi: 10.1093/cercor/bhr1382.
27. Lafleur MF, Jackson PL, Malouin F, Richards CL, Evans AC, et al. (2002) Motor learning produces parallel dynamic functional changes during the execution and imagination of sequential foot movements. Neuroimage 16: 142-157.
28. Lee JH, Marzelli M, Jolesz FA, Yoo SS, (2009) Automated classification of fMRI data employing trial-based imagery tasks. Med Image Anal 13: 392-404.
29. Orr EL, Lacourse MG, Cohen MJ, Cramer SC, (2008) Cortical activation during executed, imagined, and observed foot movements. Neuroreport 19: 625-630.
30. Rocca MA, Filippi M, (2010) FMRI correlates of execution and observation of foot movements in left-handers. J Neurol Sci 288: 34-41.
31. Roux FE, Lotterie JA, Cassol E, Lazorthes Y, Sol JC, et al. (2003) Cortical areas involved in virtual movement of phantom limbs: comparison with normal subjects. Neurosurgery 53: 1342-1352.
32. Sahyoun C, Floyer-Lea A, Johansen-Berg H, Matthews PM, (2004) Towards an understanding of gait control: brain activation during the anticipation, preparation and execution of foot movements. Neuroimage 21: 568-575.
33. Sakreida K, Schubotz RI, Wolfensteller U, von Cramon DY, (2005) Motion class dependency in observers' motor areas revealed by functional magnetic resonance imaging. J Neurosci 25: 1335-1342.
34. Stippich C, Ochmann H, Sartor K, (2002) Somatotopic mapping of the human primary sensorimotor cortex during motor imagery and motor execution by functional magnetic resonance imaging. Neurosci Lett 331: 50-54.
35. Wheaton KJ, Thompson JC, Syngeniotis A, Abbott DF, Puce A, (2004) Viewing the motion of human body parts activates different regions of premotor, temporal, and parietal cortex. Neuroimage 22: 277-288.
36. Yuan H, Liu T, Szarkowski R, Rios C, Ashe J, et al. (2010) Negative covariation between task-related responses in alpha/beta-band activity and BOLD in human sensorimotor cortex: an EEG and fMRI study of motor imagery and movements. Neuroimage 49: 2596-2606.
37. Solodkin A, Hlustik P, Chen EE, Small SL, (2004) Fine modulation in network activation during motor execution and motor imagery. Cereb Cortex 14: 1246-1255.
38. Iseki K, Hanakawa T, Shinozaki J, Nankaku M, Fukuyama H, (2008) Neural mechanisms involved in mental imagery and observation of gait. Neuroimage 41: 1021-1031.
39. Yu N, Estevez N, Hepp-Reymond MC, Kollias SS, Riener R, (2011) fMRI assessment of upper extremity related brain activation with an MRI-compatible manipulandum. Int J Comput Assist Radiol Surg 6: 447-455.
40. Isaac A, Marks D, Russell D, (1986) An instrument for assessing imagery of movement: the vividness of movement imagery questionnaire (VMIQ). J Ment Image 10: 23-30.
41. Friston KJ, Holmes AP, Worsley KJ, (1999) How many subjects constitute a study? Neuroimage 10: 1-5.
42. Grootoonk S, Hutton C, Ashburner J, Howseman AM, Josephs O, et al. (2000) Characterization and correction of interpolation effects in the realignment of fMRI time series. Neuroimage 11: 49-57.
43. Forman SD, Cohen JD, Fitzgerald M, Eddy WF, Mintun MA, et al. (1995) Improved assessment of significant activation in functional magnetic resonance imaging (fMRI): use of a cluster-size threshold. Magnetic resonance in medicine: official journal of the Society of Magnetic Resonance in Medicine/Society of Magnetic Resonance in Medicine 33: 636-647.
44. Slotnick SD, Moo LR, Segal JB, Hart J Jr, (2003) Distinct prefrontal cortex activity associated with item memory and source memory for visual shapes. Brain research Cognitive brain research 17: 75-82.
45. Thompson WL, Slotnick SD, Burrage MS, Kosslyn SM, (2009) Two forms of spatial imagery: neuroimaging evidence. Psychological science 20: 1245-1253.
46. Nichols T, Brett M, Andersson J, Wager T, Poline JB, (2005) Valid conjunction inference with the minimum statistic. Neuroimage 25: 653-660.
47. Maldjian JA, Laurienti PJ, Kraft RA, Burdette JH, (2003) An automated method for neuroanatomic and cytoarchitectonic atlas-based interrogation of fMRI data sets. Neuroimage 19: 1233-1239.
48. Tzourio-Mazoyer N, Landeau B, Papathanassiou D, Crivello F, Etard O, et al. (2002) Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain. Neuroimage 15: 273-289.
49. Schmahmann JD, Doyon J, McDonald D, Holmes C, Lavoie K, et al. (1999) Three-dimensional MRI atlas of the human cerebellum in proportional stereotaxic space. Neuroimage 10: 233-260.
50. Cross ES, Kraemer DJ, Hamilton AF, Kelley WM, Grafton ST, (2009) Sensitivity of the action observation network to physical and observational learning. Cereb Cortex 19: 315-326.
51. Margulies DS, Vincent JL, Kelly C, Lohmann G, Uddin LQ, et al. (2009) Precuneus shares intrinsic functional architecture in humans and monkeys. Proc Natl Acad Sci U S A 106: 20069-20074.
52. Jastorff J, Orban GA, (2009) Human functional magnetic resonance imaging reveals separation and integration of shape and motion cues in biological motion processing. J Neurosci 29: 7315-7329.
53. Van Overwalle F, Baetens K, (2009) Understanding others' actions and goals by mirror and mentalizing systems: a meta-analysis. Neuroimage 48: 564-584.
54. Remaud A, Boyas S, Caron GA, Bilodeau M, (2012) Attentional demands associated with postural control depend on task difficulty and visual condition. J Mot Behav 44: 329-340.
55. Dechent P, Merboldt KD, Frahm J, (2004) Is the human primary motor cortex involved in motor imagery? Brain Res Cogn Brain Res 19: 138-144.
56. Jackson PL, Lafleur MF, Malouin F, Richards C, Doyon J, (2001) Potential role of mental practice using motor imagery in neurologic rehabilitation. Arch Phys Med Rehabil 82: 1133-1141.
57. Sharma N, Pomeroy VM, Baron JC, (2006) Motor imagery: a backdoor to the motor system after stroke? Stroke 37: 1941-1952.
58. Sharma N, Jones PS, Carpenter TA, Baron JC, (2008) Mapping the involvement of BA 4a and 4p during Motor Imagery. Neuroimage 41: 92-99.
59. Szameitat AJ, Shen S, Conforto A, Sterr A, (2012) Cortical activation during executed, imagined, observed, and passive wrist movements in healthy volunteers and stroke patients. Neuroimage 62: 266-280.
60. Lehericy S, Gerardin E, Poline JB, Meunier S, Van de Moortele PF, et al. (2004) Motor execution and imagination networks in post-stroke dystonia. Neuroreport 15: 1887-1890.
61. Kimberley TJ, Khandekar G, Skraba LL, Spencer JA, Van Gorp EA, et al. (2006) Neural substrates for motor imagery in severe hemiparesis. Neurorehabil Neural Repair 20: 268-277.
62. Sharma N, Simmons LH, Jones PS, Day DJ, Carpenter TA, et al. (2009) Motor imagery after subcortical stroke: a functional magnetic resonance imaging study. Stroke 40: 1315-1324.
63. Sharma N, Baron JC, Rowe JB, (2009) Motor imagery after stroke: relating outcome to motor network connectivity. Ann Neurol 66: 604-616.
64. Villiger M, Chandrasekharan S, Welsh TN, (2011) Activity of human motor system during action observation is modulated by object presence. Exp Brain Res 209: 85-93.
65. Hardwick RM, McAllister CJ, Holmes PS, Edwards MG, (2012) Transcranial magnetic stimulation reveals modulation of corticospinal excitability when observing actions with the intention to imitate. Eur J Neurosci 35: 1475-1480.
66. Cavanna AE, Trimble MR, (2006) The precuneus: a review of its functional anatomy and behavioural correlates. Brain 129: 564-583.
67. Northoff G, Heinzel A, de Greck M, Bermpohl F, Dobrowolny H, et al. (2006) Self-referential processing in our brain-a meta-analysis of imaging studies on the self. Neuroimage 31: 440-457.
68. Dosenbach NU, Fair DA, Cohen AL, Schlaggar BL, Petersen SE, (2008) A dual-networks architecture of top-down control. Trends Cogn Sci 12: 99-105.
69. Nelson SM, Dosenbach NU, Cohen AL, Wheeler ME, Schlaggar BL, et al. (2010) Role of the anterior insula in task-level control and focal attention. Brain Struct Funct 214: 669-680.
70. Farrer C, Frith CD, (2002) Experiencing oneself vs another person as being the cause of an action: the neural correlates of the experience of agency. Neuroimage 15: 596-603.
71. Dobkin BH, Firestine A, West M, Saremi K, Woods R, (2004) Ankle dorsiflexion as an fMRI paradigm to assay motor control for walking during rehabilitation. Neuroimage 23: 370-381.
72. Caggiano V, Fogassi L, Rizzolatti G, Pomper JK, Thier P, et al. (2011) View-based encoding of actions in mirror neurons of area f5 in macaque premotor cortex. Curr Biol 21: 144-148.
73. Arzy S, Thut G, Mohr C, Michel CM, Blanke O, (2006) Neural basis of embodiment: distinct contributions of temporoparietal junction and extrastriate body area. J Neurosci 26: 8074-8081.
74. Blanke O, Ortigue S, Landis T, Seeck M, (2002) Stimulating illusory own-body perceptions. Nature 419: 269-270.
75. Blanke O, Landis T, Spinelli L, Seeck M, (2004) Out-of-body experience and autoscopy of neurological origin. Brain 127: 243-258.
76. Ionta S, Heydrich L, Lenggenhager B, Mouthon M, Fornari E, et al. (2011) Multisensory mechanisms in temporo-parietal cortex support self-location and first-person perspective. Neuron 70: 363-374.
77. Lewis JW, (2006) Cortical networks related to human use of tools. Neuroscientist 12: 211-231.
78. Tanaka S, Inui T, Iwaki S, Konishi J, Nakai T, (2001) Neural substrates involved in imitating finger configurations: an fMRI study. Neuroreport 12: 1171-1174.