Compensatory plasticity in the action observation network: Virtual lesions of STS enhance anticipatory simulation of seen actions

Cerebral Cortex

Volumn 23, Issue 3, 2013, Pages 570-580

  Avenanti, Alessio ^a,b,c   Annella, Laura ^a,b   Candidi, Matteo ^c,d   Urgesi, Cosimo ^e,f   Aglioti, Salvatore M ^c,d  

^a UNIVERSITY OF BOLOGNA   (Italy)

^b Centro di Studi e Ricerche in Neuroscienze Cognitive   (Italy)

^c IRCCS FONDAZIONE SANTA LUCIA   (Italy)

^d SAPIENZA UNIVERSITY OF ROME   (Italy)

^e UNIVERSITY OF UDINE   (Italy)

^f Polo Friuli Venezia Giulia   (Italy)

Author keywords

action prediction and simulation; functional connectivity; plasticity; superior temporal sulcus; transcranial magnetic stimulation

Indexed keywords

ADULT; ANTICIPATORY SIMULATION; ARTICLE; COMPENSATORY PLASTICITY; FEMALE; FRONTAL CORTEX; HUMAN; HUMAN EXPERIMENT; MALE; MOTOR PERFORMANCE; NERVE CELL EXCITABILITY; NERVE CELL PLASTICITY; NEURONAVIGATION; NEUROPHYSIOLOGY; PERCEPTION; PREDICTION; PRIORITY JOURNAL; SIMULATION; SUPERIOR TEMPORAL SULCUS; TRANSCRANIAL MAGNETIC STIMULATION; VISUAL STIMULATION;

EID: 84873689264     PISSN: 10473211     EISSN: 14602199     Source Type: Journal    
DOI: 10.1093/cercor/bhs040     Document Type: Article

References (92)

1. Aglioti SM, Cesari P, Romani M, Urgesi C. 2008. Action anticipation and motor resonance in elite basketball players. Nat Neurosci. 11:1109-1116.
2. Aglioti SM, Pazzaglia M. 2011. Sounds and scents in social action. Trends Cogn Sci. 15:47-55.
3. Avenanti A, Bolognini N, Maravita A, Aglioti SM. 2007. Somatic and motor components of action simulation. Curr Biol. 17:2129-2135.
4. Avenanti A, Coccia M, Ladavas E, Provinciali L, Ceravolo MG. 2012. Lowfrequency rTMS promotes use-dependent motor plasticity in chronic stroke: a randomized trial. Neurology. 78:256-264.
5. Avenanti A, Minio-Paluello I, Bufalari I, Aglioti SM. 2009. The pain of amodel in thepersonality ofanonlooker: influenceof state- reactivityandpersonality traits on embodied empathy for pain. Neuroimage. 44:275-283.
6. Avenanti A, Minio-Paluello I, Sforza A, Aglioti SM. 2009. Freezing or escaping? Opposite modulations of empathic reactivity to the pain of others. Cortex. 45:1072-1077.
7. Avenanti A, Urgesi C. 2011. Understanding 'what' others do: mirror mechanisms play a crucial role in action perception. Soc Cogn Affect Neurosci. 6:257-259.
8. Aziz-Zadeh L, Maeda F, Zaidel E, Mazziotta J, Iacoboni M. 2002. Lateralization in motor facilitation during action observation: a TMS study. Exp Brain Res. 144:127-131.
9. Bertini C, Leo F, Avenanti A, Ladavas E. 2010. Independent mechanisms for ventriloquism and multisensory integration as revealed by thetaburst stimulation. Eur J Neurosci. 31:1791-1799.
10. Borroni P, Montagna M, Cerri G, Baldissera F. 2005. Cyclic time course of motor excitability modulation during the observation of a cyclic hand movement. Brain Res. 1065:115-124.
11. Brasil-Neto JP, Cohen LG, Panizza M, Nilsson J, Roth BJ, Hallett M. 1992. Optimal focal transcranial magnetic activation of the human motor cortex: effects of coil orientation, shape of the induced current pulse, and stimulus intensity. J Clin Neurophysiol. 9:132-136.
12. Candidi M, Stienen BM, Aglioti SM, de Gelder B. 2011. Event-related repetitive transcranial magnetic stimulation of posterior superior temporal sulcus improves the detection of threatening postural changes in human bodies. J Neurosci. 31:17547-17554.
13. Candidi M, Vicario CM, Abreu AM, Aglioti SM. 2010. Competing mechanisms for mapping action-related categorical knowledge and observed actions. Cereb Cortex. 20:1018-1022.
14. Caspers S, Zilles K, Laird AR, Eickhoff SB. 2010. ALE meta-analysis of action observation and imitation in the human brain. Neuroimage. 50:1148-1167.
15. Catmur C, Mars RB, Rushworth MF, Heyes C. 2011. Making mirrors: premotor cortex stimulation enhances mirror and counter-mirror motor facilitation. J Cogn Neurosci. 23:2352-2362.
16. Cattaneo L, Barchiesi G, Tabarelli D, Arfeller C, Sato M, Glenberg AM. 2011. One's motor performance predictably modulates the understanding of others' actions through adaptation of premotor visuo-motor neurons. Soc Cogn Affect Neurosci. 6:301-310.
17. Cattaneo L, Sandrini M, Schwarzbach J. 2010. State-dependent TMS reveals a hierarchical representation of observed acts in the temporal, parietal, and premotor cortices. Cereb Cortex. 20:2252-2258.
18. Cattaneo L, Voss M, Brochier T, Prabhu G, Wolpert DM, Lemon RN. 2005. A cortico-cortical mechanism mediating object-driven grasp in humans. Proc Natl Acad Sci U S A. 102:898-903.
19. Chao LL, Martin A. 2000. Representation of manipulable man-made objects in the dorsal stream. Neuroimage. 12:478-484.
20. Chong TT, Cunnington R, Williams MA, Kanwisher N, Mattingley JB. 2008. fMRI adaptation reveals mirror neurons in human inferior parietal cortex. Curr Biol. 18:1576-1580.
21. Davare M, Montague K, Olivier E, Rothwell JC, Lemon RN. 2009. Ventral premotor to primary motor cortical interactions during objectdriven grasp in humans. Cortex. 45:1050-1057.
22. D'Ausilio A, Bufalari I, Salmas P, Fadiga L. 2011. The role of the motor system in discriminating normal and degraded speech sounds. Cortex. doi: 10.1016/j.cortex.2011.05.017.
23. di Pellegrino G, Fadiga L, Fogassi L, Gallese V, Rizzolatti G. 1992. Understanding motor events: a neurophysiological study. Exp Brain Res. 91:176-180.
24. Dum RP, Strick PL. 1991. The origin of corticospinal projections from the premotor areas in the frontal lobe. J Neurosci. 11:667-689.
25. Etzel JA, Gazzola V, Keysers C. 2008. Testing simulation theory with cross-modal multivariate classification of fMRI data. PLoS One. 311:e3690.
26. Fadiga L, Craighero L, Olivier E. 2005. Human motor cortex excitability during the perception of others' action. Curr Opin Neurobiol. 15:213-218.
27. Fazio P, Cantagallo A, Craighero L, D'Ausilio A, Roy AC, Pozzo T, Calzolari F, Granieri E, Fadiga L. 2009. Encoding of human action in Broca's area. Brain. 132:1980-1988.
28. 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.
29. Fourkas AD, Bonavolonta V, Avenanti A, Aglioti SM. 2008. Kinesthetic imagery and tool-specific modulation of corticospinal representations in expert tennis players. Cereb Cortex. 18:2382-2390.
30. Friston K, Mattout J, Kilner J. 2011. Action understanding and active inference. Biol Cybern. 104:137-160.
31. Gallese V, Fadiga L, Fogassi L, Rizzolatti G. 1996. Action recognition in the premotor cortex. Brain. 119:593-609.
32. Gangitano M, Mottaghy FM, Pascual-Leone A. 2004. Modulation of premotor mirror neuron activity during observation of unpredictable grasping movements. Eur J Neurosci. 20:2193-2202.
33. Gazzola V, Keysers C. 2009. The observation and execution of actions share motor and somatosensory voxels in all tested subjects: single-subject analyses of unsmoothed fMRI data. Cereb Cortex. 19:1239-1255.
34. Gazzola V, van der Worp H, Mulder T, Wicker B, Rizzolatti G, Keysers C. 2007. Aplasics born without hands mirror the goal of hand actions with their feet. Curr Biol. 17:1235-1240.
35. Gerschlager W, Siebner HR, Rothwell JC. 2001. Decreased corticospinal excitability after subthreshold 1 Hz rTMS over lateral premotor cortex. Neurology. 57:449-455.
36. Giese MA, Poggio T. 2003. Neural mechanisms for the recognition of biological movements. Nat Rev Neurosci. 4:179-192.
37. Grafton ST. 2009. Embodied cognition and the simulation of action to understand others. Ann N Y Acad Sci. 1156:97-117.
38. Grossman E, Donnelly M, Price R, Pickens D, Morgan V, Neighbor G, Blake R. 2000. Brain areas involved in perception of biological motion. J Cogn Neurosci. 12:711-720.
39. Grossman ED, Battelli L, Pascual-Leone A. 2005. Repetitive TMS over posterior STS disrupts perception of biological motion. Vision Res. 45:2847-2853.
40. Heiser M, Iacoboni M, Maeda F, Marcus J, Mazziotta JC. 2003. The essential role of Broca's area in imitation. Eur J Neurosci. 17:1123-1128.
41. Hickok G. 2009. Eight problems for the mirror neuron theory of action understanding in monkeys and humans. J Cogn Neurosci. 21:1229-1243.
42. Hupe JM, James AC, Payne BR, Lomber SG, Girard P, Bullier J. 1998. Cortical feedback improves discrimination between figure and background by V1, V2 and V3 neurons. Nature. 394:784-787.
43. Jellema T, Perrett DI. 2003. Cells in monkey STS responsive to articulated body motions and consequent static posture: a case of implied motion? Neuropsychologia. 41:1728-1737.
44. Johnson-Frey SH, Maloof FR, Newman-Norlund R, Farrer C, Inati S, Grafton ST. 2003. Actions or hand-object interactions? Human inferior frontal cortex and action observation. Neuron. 39:1053-1058.
45. Keysers C, Perrett DI. 2004. Demystifying social cognition: a Hebbian perspective. Trends Cogn Sci. 8:501-507.
46. Kilner JM, Friston KJ, Frith CD. 2007. Predictive coding: an account of the mirror neuron system. Cogn Process. 8:159-166.
47. Kilner JM, Neal A, Weiskopf N, Friston KJ, Frith CD. 2009. Evidence of mirror neurons in human inferior frontal gyrus. J Neurosci. 29:10153-10159.
48. Kilner JM, Vargas C, Duval S, Blakemore SJ, Sirigu A. 2004. Motor activation prior to observation of a predicted movement. Nat Neurosci. 7:1299-1301.
49. Koch G, Versace V, Bonn? S, Lupo F, Lo Gerfo E, Oliveri M, Caltagirone C. 2010. Resonance of cortico-cortical connections of the motor system with the observation of goal directed grasping movements. Neuropsychologia. 48:3513-3520.
50. Kourtzi Z, Kanwisher N. 2000. Activation in human MT/MST by static images with implied motion. J Cogn Neurosci. 12:48-55.
51. Kraskov A, Dancause N, Quallo MM, Shepherd S, Lemon RN. 2009. Corticospinal neurons in macaque ventral premotor cortex with mirror properties: a potential mechanism for action suppression?. Neuron. 64:922-930.
52. Mayka MA, Corcos DM, Leurgans SE, Vaillancourt DE. 2006. Threedimensional locations and boundaries of motor and premotor cortices as defined by functional brain imaging: a meta-analysis. Neuroimage. 31:1453-1474.
53. Moro V, Urgesi C, Pernigo S, Lanteri P, Pazzaglia M, Aglioti SM. 2008. The neural basis of body form and body action agnosia. Neuron. 60:235-246.
54. Nelissen K, Borra E, Gerbella M, Rozzi S, Luppino G, Vanduffel W, Rizzolatti G, Orban GA. 2011. Action observation circuits in the macaque monkey cortex. J Neurosci. 31:3743-3756.
55. Nelissen K, Luppino G, Vanduffel W, Rizzolatti G, Orban GA. 2005. Observing others: multiple action representation in the frontal lobe. Science. 310:332-336.
56. Nishitani N, Avikainen S, Hari R. 2004. Abnormal imitation-related cortical activation sequences in Asperger's syndrome. Ann Neurol. 55:558-562.
57. Nishitani N, Hari R. 2002. Viewing lip forms: cortical dynamics. Neuron. 36:1211-1220.
58. Oldfield RC. 1971. The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia. 9:97-113.
59. Oosterhof NN, Wiggett AJ, Diedrichsen J, Tipper SP, Downing PE. 2010. Surface-based information mapping reveals crossmodal vision-action representations in human parietal and occipitotemporal cortex. J Neurophysiol. 104:1077-1089.
60. O'Shea J, Johansen-Berg H, Trief D, Gobel S, Rushworth MFS. 2007. Functionally specific reorganization in human premotor cortex. Neuron. 54:479-490.
61. Paus T. 2005. Inferring causality in brain images: a perturbation approach. Philos Trans R Soc Lond B Biol Sci. 360:1109-1114.
62. Pazzaglia M, Smania N, Corato E, Aglioti SM. 2008. Neural underpinnings of gesture discrimination in patients with limb apraxia. J Neurosci. 28:3030-3041.
63. Peelen MV, Wiggett AJ, Downing PE. 2006. Patterns of fMRI activity dissociate. overlapping functional brain areas that respond to biological motion. Neuron. 49:815-822.
64. Peigneux P, Salmon E, van der Linden M, Garraux G, Aerts J, Delfiore G, Degueldre C, Luxen A, Orban G, Franck G. 2000. The role of lateral occipitotemporal junction and area MT/V5 in the visual analysis of upper-limb postures. Neuroimage. 11:644-655.
65. Perrett DI, Xiao D, Barraclough NE, Keysers C, Oram MW. 2009. Seeing the future: natural image sequences produce ''anticipatory'' neuronal activity and bias perceptual report. Q J Exp Psychol (Colchester). 62:2081-2104.
66. Pobric G, Hamilton AF. 2006. Action understanding requires the left inferior frontal cortex. Curr Biol. 16:524-529.
67. Press C, Heyes C, Kilner JM. 2011. Learning to understand others' actions. Biol Lett. 7:457-460.
68. Proverbio AM, Riva F, Zani A. 2009. Observation of static pictures of dynamic actions enhances the activity of movement-related brain areas. PLoS One. 4:e5389.
69. Rizzolatti G, Craighero L. 2004. The mirror-neuron system. Annu Rev Neurosci. 27:169-192.
70. Rizzolatti G, Luppino G. 2001. The cortical motor system. Neuron. 31:889-890.
71. Rossi S, Hallett M, Rossini PM, Pascual-Leone A. The Safety of TMS Consensus Group 2009. Safety, ethical considerations, and application guidelines for the use of transcranial magnetic stimulation in clinical practice and research. Clin Neurophysiol. 120:2008-2039.
72. Rossini PM, Barker AT, Berardelli A, Caramia MD, Caruso G, Cracco RQ, Dimitrijevic MR, Hallett M, Katayama Y, Lu cking CH, et al. 1994. Non-invasive electrical and magnetic stimulation of the brain, spinal cord and roots: basic principles and procedures for routine clinical application. Report of an IFCN committee. Electroencephalogr Clin Neurophysiol. 91:79-92.
73. Sartori L, Cavallo A, Bucchioni G, Castiello U. 2011. Corticospinal excitability is specifically modulated by the social dimension of observed actions. Exp Brain Res. 211:557-568.
74. Saygin AP. 2007. Superior temporal and premotor brain areas necessary for biological motion perception. Brain. 130:2452-2461.
75. Schippers MB, Keysers C. 2011. Mapping the flow of information within the putative mirror neuron system during gesture observation. Neuroimage. 57:37-44.
76. Schubotz RI. 2007. Prediction of external events with our motor system: towards a new framework. Trends Cogn Sci. 11:211-218.
77. Schu tz-Bosbach S, Avenanti A, Aglioti SM, Haggard P. 2009. Don't do it! Cortical inhibition and self-attribution during action observation. J Cogn Neurosci. 21:1215-1227.
78. Schu tz-Bosbach S, Prinz W. 2007. Prospective coding in event representation. Cogn Process. 8:93-102.
79. Senior C, Barnes J, Giampietro V, Simmons A, Bullmore ET, Brammer M, David AS. 2000. The functional neuroanatomy of implicit-motion perception or representational momentum. Curr Biol. 10:16-22.
80. Serino A, Canzoneri E, Avenanti A. 2011. Fronto-parietal areas necessary for a multisensory representation of peripersonal space in humans: an rTMS study. J Cogn Neurosci. 23:2956-2967.
81. Shimazu H, Maier MA, Cerri G, Kirkwood PA, Lemon RN. 2004. Macaque ventral premotor cortex exerts powerful facilitation of motor cortex outputs to upper limb motoneurons. J Neurosci. 24:1200-1211.
82. Tidoni E, Borgomaneri S, di Pellegrino G, Avenanti A. 2012. Action simulation plays a critical role in deceptive action recognition. In revision. Tootell RB, Reppas JB, Kwong KK, Malach R, Born RT, Brady TJ, Rosen BR, Belliveau JW. 1995. Functional analysis of human MT and related visual cortical areas using magnetic resonance imaging. J Neurosci. 15:3215-3230.
83. Touge T, Gerschlager W, Brown P, Rothwell JC. 2001. Are the aftereffects of low-frequency rTMS on motor cortex excitability due to changes in the efficacy of cortical synapses? Clin Neurophysiol. 112:2138-2145.
84. Umilta MA, Kohler E, Gallese V, Fogassi L, Fadiga L, Keysers C, Rizzolatti G. 2001. I know what you are doing. a neurophysiological study. Neuron. 31:155-165.
85. Uozumi T, Tamagawa A, Hashimoto T, Tsuji S. 2004. Motor hand representation in cortical area 44. Neurology. 62:757-761.
86. Urgesi C, Candidi M, Ionta S, Aglioti SM. 2007. Representation of body identity and body actions in extrastriate body area and ventral premotor cortex. Nat Neurosci. 10:30-31.
87. Urgesi C, Maieron M, Avenanti A, Tidoni E, Fabbro F, Aglioti SM. 2010. Simulating the future of actions in the human corticospinal system. Cereb Cortex. 20:2511-2521.
88. Urgesi C, Moro V, Candidi M, Aglioti SM. 2006. Mapping implied body actions in the human motor system. J Neurosci. 26: 7942-7949.
89. Vaina LM, Solomon J, Chowdhury S, Sinha P, Belliveau JW. 2001. Functional neuroanatomy of biological motion perception in humans. Proc Natl Acad Sci U S A. 98:11656-11661.
90. Van Overwalle F, Baetens K. 2009. Understanding others' actions and goals by mirror and mentalizing systems: a meta-analysis. Neuroimage. 48:564-584.
91. Walsh V, Pascual-Leone A. 2003. Transcranial magnetic stimulation. A neurochronometrics of mind. Cambridge (MA): MIT Press. Wilson M, Knoblich G. 2005. The case of motor involvement in perceiving conspecifics. Psychol Bull. 131:460-473.
92. Wolpert DM, Doya K, Kawato M. 2003. A unifying computational framework for motor control and social interaction. Philos Trans R Soc Lond B Biol Sci. 2358:593-602.