Neural representations involved in observed, imagined, and imitated actions are dissociable and hierarchically organized

NeuroImage

Volumn 59, Issue 3, 2012, Pages 2798-2807

  Macuga, Kristen L ^a   Frey, Scott H ^a,b  

^a UNIVERSITY OF OREGON   (United States)

^b UNIVERSITY OF MISSOURI   (United States)

Author keywords

Action observation; Cerebellum; FMRI; Motor imagery; Sensorimotor; SMA

Indexed keywords

ADULT; ANALYTICAL PARAMETERS; ARTICLE; BEHAVIOR; BRAIN CORTEX; BRAIN FUNCTION; CENTRAL SULCUS; CEREBELLUM; CONTROLLED STUDY; FEMALE; FINGER; FRONTAL CORTEX; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HAND MOVEMENT; HUMAN; HUMAN EXPERIMENT; IMAGERY; IMITATION; MALE; MOTOR IMAGERY; NEUROTRANSMISSION; NORMAL HUMAN; OBSERVATION; PARIETAL OPERCULUM; POSTCENTRAL GYRUS; PRIMARY MOTOR CORTEX; PRIORITY JOURNAL; REGION OF INTEREST ANALYSIS; SENSORIMOTOR CORTEX; SENSORIMOTOR INTEGRATION; SUBCORTEX; SUPPLEMENTARY MOTOR AREA; TASK PERFORMANCE; VISUAL STIMULATION;

ADOLESCENT; ADULT; ATTENTION; BRAIN; BRAIN MAPPING; CEREBELLUM; CEREBRAL CORTEX; DATA INTERPRETATION, STATISTICAL; ELECTROMYOGRAPHY; EXECUTIVE FUNCTION; FEMALE; FRONTAL LOBE; FUNCTIONAL LATERALITY; HAND; HUMANS; IMAGE PROCESSING, COMPUTER-ASSISTED; IMAGINATION; IMITATIVE BEHAVIOR; MAGNETIC RESONANCE IMAGING; MALE; MOTOR CORTEX; MOVEMENT; NEURONAL PLASTICITY; PARIETAL LOBE; PSYCHOMOTOR PERFORMANCE; SOMATOSENSORY CORTEX; VISUAL PERCEPTION; YOUNG ADULT;

EID: 84855444161     PISSN: 10538119     EISSN: 10959572     Source Type: Journal    
DOI: 10.1016/j.neuroimage.2011.09.083     Document Type: Article

References (71)

1. Andersson J.L.R., Jenkinson M., Smith S.M. Non-linear Optimisation 2007.
2. Battaglia F., Quartarone A., Ghilardi M.F., Dattola R., Bagnato S., Rizzo V., Morgante L., Girlanda P. Unilateral cerebellar stroke disrupts movement preparation and motor imagery. Clin Neurophysiol 2006, 117:1009-1016.
3. Buccino G., Binkofski F., Fink G.R., Fadiga L., Fogassi L., Gallese V., Seitz R.J., Zilles K., Rizzolatti G., Freund H.J. Action observation activates premotor and parietal areas in a somatotopic manner: an fMRI study. Eur. J. Neurosci. 2001, 13:400-404.
4. Butler A.J., Page S.J. Mental practice with motor imagery: evidence for motor recovery and cortical reorganization after stroke. Arch. Phys. Med. Rehabil. 2006, 87:S2-S11.
5. Caggiano V., Fogassi L., Rizzolatti G., Pomper J.K., Thier P., Giese M.A., Casile A. View-based encoding of actions in mirror neurons of area f5 in macaque premotor cortex. Curr. Biol. 2011, 21:144-148.
6. Caspers S., Zilles K., Laird A., Eickhoff S. ALE meta-analysis of action observation and imitation in the human brain. NeuroImage 2010, 50:1148-1167.
7. Clark S., Tremblay F., Ste-Marie D. Differential modulation of corticospinal excitability during observation, mental imagery and imitation of hand actions. Neuropsychologia 2004, 42:105-112.
8. Cunnington R., Windischberger C., Moser E. Premovement activity of the pre-supplementary motor area and the readiness for action: studies of time-resolved event-related functional MRI. Hum. Mov. Sci. 2005, 24:644-656.
9. Decety J., Jeannerod M. Mentally simulated movements in virtual reality: does Fitts's law hold in motor imagery?. Behav. Brain Res. 1996, 72:127-134.
10. Dechent P., Merboldt K.D., Frahm J. Is the human primary motor cortex involved in motor imagery?. Brain Res. Cogn. Brain Res. 2004, 19:138-144.
11. Dinomais M., Minassian A.T., Tuilier T., Delion M., Wilke M., N'Guyen S., Richard I., Aubé C., Menei P. Functional MRI comparison of passive and active movement: possible inhibitory role of supplementary motor area. Neuroreport 2009, 20:1351-1355.
12. Dinstein I., Hasson U., Rubin N., Heeger D.J. Brain areas selective for both observed and executed movements. J. Neurophysiol. 2007, 98:1415-1427.
13. Duvernoy H.M. The Human Brain: Surface, Blood Supply, and Three-dimensional Sectional Anatomy 1991, Springer Wien, New York. 2nd ed.
14. Ehrsson H.H., Geyer S., Naito E. Imagery of voluntary movement of fingers, toes, and tongue activates corresponding body-part-specific motor representations. J. Neurophysiol. 2003, 90:3304-3316.
15. Ertelt D., Small S., Solodkin A., Dettmers C., McNamara A., Binkofski F., Buccino G. Action observation has a positive impact on rehabilitation of motor deficits after stroke. NeuroImage 2007, 36:T164-T173.
16. Fadiga L., Fogassi L., Pavesi G., Rizzolatti G. Motor facilitation during action observation: a magnetic stimulation study. J. Neurophysiol. 1995, 73:2608-2611.
17. Fadiga L., Buccino G., Craighero L., Fogassi L., Gallese V., Pavesi G. Corticospinal excitability is specifically modulated by motor imagery: a magnetic stimulation study. Neuropsychologia 1999, 37:147-158.
18. Filimon F., Nelson J., Hagler D., Sereno M. Human cortical representations for reaching: mirror neurons for execution, observation, and imagery. NeuroImage 2007, 37:1315-1328.
19. Frey S.H. Forecasting the long-range consequences of manual and tool use actions: neurophysiological, behavioral and computational considerations. Motor Control: Theories, Experiments and Applications 2010, 295-313. New York, Oxford. F.M.L.E. Danion (Ed.).
20. Frey S.H., Gerry V.E. Modulation of neural activity during observational learning of actions and their sequential orders. J. Neurosci. 2006, 26:13194-13201.
21. Gerardin E., Sirigu A., Lehericy S., Poline J.B., Gaymard B., Marsault C., Agid Y., Le Bihan D. Partially overlapping neural networks for real and imagined hand movements. Cereb. Cortex 2000, 10:1093-1104.
22. Gonzalez B., Rodriguez M., Ramirez C., Sabate M. Disturbance of motor imagery after cerebellar stroke. Behav Neurosci 2005, 119:622-626.
23. Grafton S.T., Arbib M.A., Fadiga L., Rizzolatti G. Localization of grasp representations in humans by positron emission tomography. 2. Observation compared with imagination. Exp. Brain Res. 1996, 112:103-111.
24. Grealy M.A., Lee D.N. An automatic-voluntary dissociation and mental imagery disturbance following a cerebellar lesion. Neuropsychologia 2011, 49:271-275.
25. Grezes J., Decety J. Functional anatomy of execution, mental simulation, observation, and verb generation of actions: a meta-analysis. Hum. Brain Mapp. 2001, 12:1-19.
26. Grush R. The emulation theory of representation: motor control, imagery, and perception. Behav. Brain Sci. 2004, 27:377-396. discussion 396-442.
27. Guillot A., Collet C., Nguyen V.A., Malouin F., Richards C., Doyon J. Brain activity during visual versus kinesthetic imagery: an fMRI study. Hum. Brain Mapp. 2009, 30:2157-2172.
28. Haggard P., Whitford B. Supplementary motor area provides an efferent signal for sensory suppression. Brain Res. Cogn. Brain Res. 2004, 19:52-58.
29. Hanakawa T., Immisch I., Toma K., Dimyan M., Van Gelderen P., Hallett M. Functional properties of brain areas associated with motor execution and imagery. J. Neurophysiol. 2003, 89:989-1002.
30. Hanakawa T., Dimyan M., Hallett M. Motor planning, imagery, and execution in the distributed motor network: a time-course study with functional MRI. Cereb. Cortex 2008, 18:2775-2788.
31. Jackson P., Meltzoff A., Decety J. Neural circuits involved in imitation and perspective-taking. NeuroImage 2006, 31:429-439.
32. Jeannerod M. The representing brain: neural correlates of motor intention and imagery. Brain Behav. Sci. 1994, 17:187-245.
33. Jeannerod M. Mental imagery in the motor context. Neuropsychologia 1995, 33:1419-1432.
34. Jeannerod M. Neural simulation of action: a unifying mechanism for motor cognition. NeuroImage 2001, 14:S103-S109.
35. Johnson S.H. Cerebral organization of motor imagery: contralateral control of grip selection in mentally represented prehension. Psychol. Sci. 1998, 9:219-222.
36. Johnson S.H. Imagining the impossible: intact motor representations in hemiplegics. Neuroreport 2000, 11:729-732.
37. Johnson S.H., Corballis P.M., Gazzaniga M.S. Within grasp but out of reach: evidence for a double dissociation between imagined hand and arm movements in the left cerebral hemisphere. Neuropsychologia 2001, 39:36-50.
38. Johnson S.H., Rotte M., Grafton S.T., Hinrichs H., Gazzaniga M.S., Heinze H.J. Selective activation of a parietofrontal circuit during implicitly imagined prehension. NeuroImage 2002, 17:1693-1704.
39. Kamousi B., Liu Z., He B. Classification of motor imagery tasks for brain-computer interface applications by means of two equivalent dipoles analysis. IEEE Trans. Neural Syst. Rehabil. Eng. 2005, 13:166-171.
40. Kasess C.H., Windischberger C., Cunnington R., Lanzenberger R., Pezawas L., Moser E. The suppressive influence of SMA on M1 in motor imagery revealed by fMRI and dynamic causal modeling. NeuroImage 2008, 40:828-837.
41. Kilner J.M., Paulignan Y., Blakemore S.J. An interference effect of observed biological movement on action. Curr. Biol. 2003, 13:522-525.
42. Lingnau A., Gesierich B., Caramazza A. Asymmetric fMRI adaptation reveals no evidence for mirror neurons in humans. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:9925-9930.
43. Lotze M., Montoya P., Erb M., Hulsmann E., Flor H., Klose U., Birbaumer N., Grodd W. Activation of cortical and cerebellar motor areas during executed and imagined hand movements: an fMRI study. J. Cogn. Neurosci. 1999, 11:491-501.
44. Macuga K.L., Frey S.H. Selective responses in right inferior frontal and supramarginal gyri differentiate between observed movements of oneself vs. another. Neuropsychologia 2011, 49:1202-1207.
45. Maeda F., Chang V., Mazziotta J., Iacoboni M. Experience-dependent modulation of motor corticospinal excitability during action observation. Exp. Brain Res. 2001, 140:241-244.
46. Mattar A., Gribble P. Motor learning by observing. Neuron 2005, 46:153-160.
47. Miall R.C., King D. State estimation in the cerebellum. Cerebellum 2008, 7:572-576.
48. Mostofsky S.H., Schafer J.G., Abrams M.T., Goldberg M.C., Flower A.A., Boyce A., Courtney S.M., Calhoun V.D., Kraut M.A., Denckla M.B., Pekar J.J. fMRI evidence that the neural basis of response inhibition is task-dependent. Brain Res. Cogn. Brain Res. 2003, 17:419-430.
49. Mulder T. Motor imagery and action observation: cognitive tools for rehabilitation. J. Neural Transm. 2007, 114:1265-1278.
50. Nair D.G., Purcott K.L., Fuchs A., Steinberg F., Kelso J.A. Cortical and cerebellar activity of the human brain during imagined and executed unimanual and bimanual action sequences: a functional MRI study. Brain Res. Cogn. Brain Res. 2003, 15:250-260.
51. Nichols T., Brett M., Andersson J., Wager T., Poline J.B. Valid conjunction inference with the minimum statistic. NeuroImage 2005, 25:653-660.
52. Page S.J., Levine P., Leonard A. Mental practice in chronic stroke: results of a randomized, placebo-controlled trial. Stroke 2007, 38:1293-1297.
53. Picard N., Strick P.L. Motor areas of the medial wall: a review of their location and functional activation. Cereb. Cortex 1996, 6:342-353.
54. Prinz W. Perception and action planning. Eur. J. Cogn. Psychol. 1997, 9:129-154.
55. Rizzolatti G., Craighero L. The mirror-neuron system. Annu. Rev. Neurosci. 2004, 27:169-192.
56. Rizzolatti G., Fadiga L., Matelli M., Bettinardi V., Paulesu E., Perani D., Fazio F. Localization of grasp representations in humans by PET: 1. Observation versus execution. Exp. Brain Res. 1996, 111:246-252.
57. Ruby P., Decety J. Effect of subjective perspective taking during simulation of action: a PET investigation of agency. Nat. Neurosci. 2001, 4:546-550.
58. Sabate M. Brain lateralization of motor imagery: motor planning asymmetry as a cause of movement lateralization. Neuropsychologia 2004, 42:1041-1049.
59. Sharma N., Pomeroy V.M., Baron J.C. Motor imagery: a backdoor to the motor system after stroke?. Stroke 2006, 37:1941-1952.
60. Sharma N., Jones P., Carpenter T., Baron J. Mapping the involvement of BA 4a and 4p during motor imagery. NeuroImage 2008, 41:92-99.
61. Sharp D.J., Bonnelle V., De Boissezon X., Beckmann C.F., James S.G., Patel M.C., Mehta M.A. Distinct frontal systems for response inhibition, attentional capture, and error processing. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:6106-6111.
62. Shmuelof L., Zohary E. Mirror-image representation of action in the anterior parietal cortex. Nat. Neurosci. 2008, 11:1267-1269.
63. Sirigu A., Cohen L., Duhamel J.R., Pillon B., Dubois B., Agid Y., Pierrot-Deseilligny C. Congruent unilateral impairments for real and imagined hand movements. Neuroreport 1995, 6:997-1001.
64. Sirigu A., Duhamel J.R., Cohen L., Pillon B., Dubois B., Agid Y. The mental representation of hand movements after parietal cortex damage. Science 1996, 273:1564-1568.
65. Smith S.M., Jenkinson M., Woolrich M.W., Beckmann C.F., Behrens T.E., Johansen-Berg H., Bannister P.R., De Luca M., Drobnjak I., Flitney D.E., Niazy R.K., Saunders J., Vickers J., Zhang Y., De Stefano N., Brady J.M., Matthews P.M. Advances in functional and structural MR image analysis and implementation as FSL. NeuroImage 2004, 23(Suppl. 1):S208-S219.
66. Stephan K.M., Fink G.R., Passingham R.E., Silbersweig D., Ceballos-Baumann A.O., Frith C.D., Frackowiak R.S. Functional anatomy of the mental representation of upper extremity movements in healthy subjects. J. Neurophysiol. 1995, 73:373-386.
67. Strafella A.P., Paus T. Modulation of cortical excitability during action observation: a transcranial magnetic stimulation study. Neuroreport 2000, 11:2289-2292.
68. Van Essen D.C. A population-average, landmark- and surface-based (PALS) atlas of human cerebral cortex. NeuroImage 2005, 28:635-662.
69. Van Essen D.C., Drury H.A., Dickson J., Harwell J., Hanlon D., Anderson C.H. An integrated software suite for surface-based analyses of cerebral cortex. J. Am. Med. Inform. Assoc. 2001, 8:443-459.
70. Vogt S., Thomaschke R. From visuo-motor interactions to imitation learning: behavioural and brain imaging studies. J. Sports Sci. 2007, 25:497-517.
71. Wolpert D.M., Miall R.C., Kawato M. Internal models in the cerebellum. Trends Cogn. Sci. 1998, 2:338-347.