Massive somatic deafferentation and motor deefferentation of the lower part of the body impair its visual recognition: A psychophysical study of patients with spinal cord injury

European Journal of Neuroscience

Volumn 36, Issue 11, 2012, Pages 3509-3518

  Pernigo, S ^a   Moro, V ^a   Avesani, R ^b   Miatello, C ^a   Urgesi, C ^c   Aglioti, S M ^d,e  

^a UNIVERSITY OF VERONA   (Italy)

^b Don Calabria Hospital   (Italy)

^c UNIVERSITY OF UDINE   (Italy)

^d SAPIENZA UNIVERSITY OF ROME   (Italy)

^e IRCCS FONDAZIONE SANTA LUCIA   (Italy)

Author keywords

Body inversion effect; Body representation; Paraplegia; SCI; Sensorimotor plasticity

Indexed keywords

ADULT; ARTICLE; BODY BUILD; BRAIN CORTEX; CLINICAL ARTICLE; CONTROLLED STUDY; DEAFFERENTATION; FEMALE; HUMAN; MALE; MOTOR DEAFFERENTATION; MOTOR PERFORMANCE; PRIORITY JOURNAL; SOMATIC DEAFFERENTATION; SOMATOSENSORY SYSTEM; SPINAL CORD INJURY; TASK PERFORMANCE; VISUAL DISCRIMINATION; VISUAL MEMORY;

ADULT; AFFERENT PATHWAYS; CASE-CONTROL STUDIES; EFFERENT PATHWAYS; FEMALE; HUMANS; LEG; MALE; MIDDLE AGED; MOTION PERCEPTION; MOTOR ACTIVITY; MOTOR CORTEX; PATTERN RECOGNITION, VISUAL; PSYCHOMOTOR PERFORMANCE; SPINAL CORD INJURIES; SPORTS;

EID: 84870513760     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/j.1460-9568.2012.08266.x     Document Type: Article

References (84)

1. Abernethy, B. & Zawi, K. (2007) Pickup of essential kinematics underpins expert perception of movement patterns. J. Mot. Behav., 39, 353-367.
2. Abernethy, B., Zawi, K. & Jackson, R.C. (2008) Expertise and attunement to kinematic constraints. Perception, 37, 931-948.
3. Aglioti, S.M. & Pazzaglia, M. (2011) Sounds and scents in (social) action. Trends Cogn. Sci. (Regul. Ed.), 15, 47-55.
4. Aglioti, S.M., Cesari, P., Romani, M. & Urgesi, C. (2008) Action anticipation and motor resonance in elite basketball players. Nat. Neurosci., 11, 1109-1116.
5. Aguilar, J., Humanes-Valera, D., Alonso-Calviño, E., Yague, J.G., Moxon, K.A., Oliviero, A. & Foffani, G. (2010) Spinal cord injury immediately changes the state of the brain. J. Neurosci., 30, 7528-7537.
6. Andersen, R.A., Hwang, E.J. & Mulliken, G.H. (2010) Cognitive neural prosthetics. Annu. Rev. Psychol., 61, 169-190, C1-3.
7. Arrighi, R., Cartocci, G. & Burr, D. (2011) Reduced perceptual sensitivity for biological motion in paraplegia patients. Curr. Biol., 21, R910-R911.
8. Astafiev, S.V., Shulman, G.L., Stanley, C.M., Snyder, A.Z., Van Essen, D.C. & Corbetta, M. (2003) Functional organization of human intraparietal and frontal cortex for attending, looking, and pointing. J. Neurosci., 23, 4689-4699.
9. Avenanti, A., Bolognini, N., Maravita, A. & Aglioti, S.M. (2007) Somatic and motor components of action simulation. Curr. Biol., 17, 2129-2135.
10. Avenanti, A., Annella, L., Candidi, M., Urgesi, C. & Aglioti, S.M. (2012) Compensatory plasticity in the action observation network: virtual lesions of STS enhance anticipatory simulation of seen actions. Cereb. Cortex, DOI: 10.1093/cercor/bhs040. [Epub ahead of print].
11. Avikainen, S., Forss, N. & Hari, R. (2002) Modulated activation of the human SI and SII cortices during observation of hand actions. Neuroimage, 15, 640-646.
12. Barsalou, L.W. (2008) Grounded cognition. Annu. Rev. Psychol., 59, 617-645.
13. Berlucchi, G. & Aglioti, S.M. (2010) The body in the brain revisited. Exp. Brain Res., 200, 25-35.
14. Bosbach, S., Cole, J., Prinz, W. & Knoblich, G. (2005) Inferring another's expectation from action: the role of peripheral sensation. Nat. Neurosci., 8, 1295-1297.
15. Bosbach, S., Knoblich, G., Reed, C.L., Cole, J. & Prinz, W. (2006) Body inversion effect without body sense: insights from deafferentation. Neuropsychologia, 44, 2950-2958.
16. Brandman, T. & Yovel, G. (2010) The body inversion effect is mediated by face-selective, not body-selective, mechanisms. J. Neurosci., 30, 10534-10540.
17. Buccino, G., Binkofski, F., Fink, G.R., Fadiga, L., Fogassi, L., Gallese, V., Seitz, R.J., Zilles, K., Rizzolatti, G. & Freund, H.J. (2001) Action observation activates premotor and parietal areas in a somatotopic manner: an fMRI study. Eur. J. Neurosci., 13, 400-404.
18. Calvo-Merino, B., Grèzes, J., Glaser, D.E., Passingham, R.E. & Haggard, P. (2006) Seeing or doing? Influence of visual and motor familiarity in action observationCurr. Biol., 16, 1905-1910.
19. Candidi, M., Urgesi, C., Ionta, S. & Aglioti, S.M. (2008) Virtual lesion of ventral premotor cortex impairs visual perception of biomechanically possible but not impossible actions. Soc. Neurosci., 3, 388-400.
20. Casile, A. & Giese, M.A. (2006) Nonvisual motor training influences biological motion perception. Curr. Biol., 16, 69-74.
21. Castro, A., Díaz, F. & van Boxtel, G.J.M. (2007) How does a short history of spinal cord injury affect movement-related brain potentials?Eur. J. Neurosci., 25, 2927-2934.
22. Cermik, T.F., Tuna, H., Kaya, M., Tuna, F., Gültekin, A., Yiǧitbaşi, O.N. & Alavi, A. (2006) Assessment of regional blood flow in cerebral motor and sensory areas in patients with spinal cord injury. Brain Res., 1109, 54-59.
23. Chambers, C.D., Stokes, M.G. & Mattingley, J.B. (2004) Modality-specific control of strategic spatial attention in parietal cortex. Neuron, 44, 925-930.
24. Chica, A.B., Bartolomeo, P. & Valero-Cabré, A. (2011) Dorsal and ventral parietal contributions to spatial orienting in the human brain. J. Neurosci., 31, 8143-8149.
25. Christensen, M.S., Lundbye-Jensen, J., Geertsen, S.S., Petersen, T.H., Paulson, O.B. & Nielsen, J.B. (2007) Premotor cortex modulates somatosensory cortex during voluntary movements without proprioceptive feedback. Nat. Neurosci., 10, 417-419.
26. Conson, M., Sacco, S., Sarà, M., Pistoia, F., Grossi, D. & Trojano, L. (2008) Selective motor imagery defect in patients with locked-in syndrome. Neuropsychologia, 46, 2622-2628.
27. Conson, M., Pistoia, F., Sarà, M., Grossi, D. & Trojano, L. (2010) Recognition and mental manipulation of body parts dissociate in locked-in syndrome. Brain Cogn., 73, 189-193.
28. Corbetta, M., Burton, H., Sinclair, R.J., Conturo, T.E., Akbudak, E. & McDonald, J.W. (2002) Functional reorganization and stability of somatosensory-motor cortical topography in a tetraplegic subject with late recovery. Proc. Natl. Acad. Sci. USA, 99, 17066-17071.
29. Costantini, M., Galati, G., Ferretti, A., Caulo, M., Tartaro, A., Romani, G.L. & Aglioti, S.M. (2005) Neural systems underlying observation of humanly impossible movements: an FMRI study. Cereb. Cortex, 15, 1761-1767.
30. Cramer, S.C., Lastra, L., Lacourse, M.G. & Cohen, M.J. (2005) Brain motor system function after chronic, complete spinal cord injury. Brain, 128, 2941-2950.
31. Cramer, S.C., Orr, E.L.R., Cohen, M.J. & Lacourse, M.G. (2007) Effects of motor imagery training after chronic, complete spinal cord injury. Exp. Brain Res., 177, 233-242.
32. Crollen, V., Dormal, G., Seron, X., Lepore, F. & Collignon, O. (2011) Embodied numbers: the role of vision in the development of number-space interactions. Cortex, DOI: 10.1016/j.cortex.2011.11.006. [Epub ahead of print].
33. Cross, E.S., Hamilton, A.F. & Grafton, S.T. (2006) Building a motor simulation de novo: observation of dance by dancers. Neuroimage, 31, 1257-1267.
34. Cross, E.S., Kraemer, D.J.M., Hamilton, A.F., Kelley, W.M. & Grafton, S.T. (2009) Sensitivity of the action observation network to physical and observational learning. Cereb. Cortex, 19, 315-326.
35. Ditunno, J.F., Young, W., Donovan, W.H. & Creasey, G. (1994) The International Standards Booklet for Neurological and Functional Classification of Spinal Cord Injury. Paraplegia, 32, 70-80.
36. Downing, P.E., Jiang, Y., Shuman, M. & Kanwisher, N. (2001) A cortical area selective for visual processing of the human body. Science, 293, 2470-2473.
37. Downing, P.E., Peelen, M.V., Wiggett, A.J. & Tew, B.D. (2006) The role of the extrastriate body area in action perception. Soc. Neurosci., 1, 52-62.
38. Enzinger, C., Ropele, S., Fazekas, F., Loitfelder, M., Gorani, F., Seifert, T., Reiter, G., Neuper, C., Pfurtscheller, G. & Müller-Putz, G. (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.
39. Fazio, P., Cantagallo, A., Craighero, L., D'Ausilio, A., Roy, A.C., Pozzo, T., Calzolari, F., Granieri, E. & Fadiga, L. (2009) Encoding of human action in Broca's area. Brain, 132, 1980-1988.
40. Ferri, F., Salone, A., Ebisch, S.J., De Berardis, D., Romani, G.L., Ferro, F.M. & Gallese, V. (2012) Action verb understanding in first-episode schizophrenia: is there evidence for a simulation deficit?Neuropsychologia, 50, 988-996.
41. Filippi, R., Richardson, F.M., Dick, F., Leech, R., Green, D.W., Thomas, M.S.C. & Price, C.J. (2011) The right posterior paravermis and the control of language interference. J. Neurosci., 31, 10732-10740.
42. Fiorio, M., Tinazzi, M. & Aglioti, S.M. (2006) Selective impairment of hand mental rotation in patients with focal hand dystonia. Brain, 129, 47-54.
43. Freund, P., Rothwell, J., Craggs, M., Thompson, A.J. & Bestmann, S. (2011a) Corticomotor representation to a human forearm muscle changes following cervical spinal cord injury. Eur. J. Neurosci., 34, 1839-1846.
44. Freund, P., Weiskopf, N., Ward, N.S., Hutton, C., Gall, A., Ciccarelli, O., Craggs, M., Friston, K. & Thompson, A.J. (2011b) Disability, atrophy and cortical reorganization following spinal cord injury. Brain, 134, 1610-1622.
45. Gandevia, S.C. & Phegan, C.M. (1999) Perceptual distortions of the human body image produced by local anaesthesia, pain and cutaneous stimulation. J. Physiol. (Lond.), 514(Pt 2), 609-616.
46. Green, A.M. & Kalaska, J.F. (2011) Learning to move machines with the mind. Trends Neurosci., 34, 61-75.
47. Grossman, E.D. & Blake, R. (2002) Brain areas active during visual perception of biological motion. Neuron, 35, 1167-1175.
48. Hari, R. & Kujala, M.V. (2009) Brain basis of human social interaction: from concepts to brain imaging. Physiol. Rev., 89, 453-479.
49. Heed, T., Habets, B., Sebanz, N. & Knoblich, G. (2010) Others' actions reduce crossmodal integration in peripersonal space. Curr. Biol., 20, 1345-1349.
50. Henderson, L.A., Gustin, S.M., Macey, P.M., Wrigley, P.J. & Siddall, P.J. (2011) Functional reorganization of the brain in humans following spinal cord injury: evidence for underlying changes in cortical anatomy. J. Neurosci., 31, 2630-2637.
51. Hotz-Boendermaker, S., Funk, M., Summers, P., Brugger, P., Hepp-Reymond, M.-C., Curt, A. & Kollias, S.S. (2008) Preservation of motor programs in paraplegics as demonstrated by attempted and imagined foot movements. Neuroimage, 39, 383-394.
52. Hotz-Boendermaker, S., Hepp-Reymond, M.-C., Curt, A. & Kollias, S. (2011) Movement observation activates lower limb motor networks in chronic complete paraplegia. Neurorehabil. Neural Repair, 25, 469-476.
53. Iacoboni, M., Molnar-Szakacs, I., Gallese, V., Buccino, G., Mazziotta, J.C. & Rizzolatti, G. (2005) Grasping the intentions of others with one's own mirror neuron system. PLoS Biol., 3, e79.
54. Invernizzi, M., Carda, S., Milani, P., Mattana, F., Fletzer, D., Iolascon, G., Gimigliano, F. & Cisari, C. (2010) Development and validation of the Italian version of the Spinal Cord Independence Measure III. Disabil. Rehabil., 32, 1194-1203.
55. Kirshblum, S.C., Burns, S.P., Biering-Sorensen, F., Donovan, W., Graves, D.E., Jha, A., Johansen, M., Jones, L., Krassioukov, A., Mulcahey, M.J., Schmidt-Read, M. & Waring, W. (2011) International standards for neurological classification of spinal cord injury (Revised 2011). J. Spinal Cord Med., 34, 535-546.
56. Kokotilo, K.J., Eng, J.J. & Curt, A. (2009) Reorganization and preservation of motor control of the brain in spinal cord injury: a systematic review. J. Neurotrauma, 26, 2113-2126.
57. Moro, V., Urgesi, C., Pernigo, S., Lanteri, P., Pazzaglia, M. & Aglioti, S.M. (2008) The neural basis of body form and body action agnosia. Neuron, 60, 235-246.
58. Nishimura, Y. & Isa, T. (2009) Compensatory changes at the cerebral cortical level after spinal cord injury. Neuroscientist, 15, 436-444.
59. Paqueron, X., Leguen, M., Rosenthal, D., Coriat, P., Willer, J.C. & Danziger, N. (2003) The phenomenology of body image distortions induced by regional anaesthesia. Brain, 126, 702-712.
60. Pavlova, M. & Sokolov, A. (2000) Orientation specificity in biological motion perception. Percept. Psychophys., 62, 889-899.
61. Pazzaglia, M., Pizzamiglio, L., Pes, E. & Aglioti, S.M. (2008) The sound of actions in apraxia. Curr. Biol., 18, 1766-1772.
62. Peelen, M.V. & Downing, P.E. (2007) The neural basis of visual body perception. Nat. Rev. Neurosci., 8, 636-648.
63. Peelen, M.V., Wiggett, A.J. & Downing, P.E. (2006) Patterns of fMRI activity dissociate overlapping functional brain areas that respond to biological motion. Neuron, 49, 815-822.
64. Pfurtscheller, G., Linortner, P., Winkler, R., Korisek, G. & Müller-Putz, G. (2009) Discrimination of motor imagery-induced EEG patterns in patients with complete spinal cord injury. Comput. Intell. Neurosci., 2009, 104-180.
65. Pobric, G. & Hamilton, A.F.C. (2006) Action understanding requires the left inferior frontal cortex. Curr. Biol., 16, 524-529.
66. Putzar, L., Goerendt, I., Lange, K., Rösler, F. & Röder, B. (2007) Early visual deprivation impairs multisensory interactions in humans. Nat. Neurosci., 10, 1243-1245.
67. Raos, V., Evangeliou, M.N. & Savaki, H.E. (2004) Observation of action: grasping with the mind's hand. Neuroimage, 23, 193-201.
68. Reed, C.L., Stone, V.E., Bozova, S. & Tanaka, J. (2003) The body-inversion effect. Psychol. Sci., 14, 302-308.
69. Reed, C.L., Stone, V.E., Grubb, J.D. & McGoldrick, J.E. (2006) Turning configural processing upside down: part and whole body postures. J. Exp. Psychol. Hum. Percept. Perform., 32, 73-87.
70. Rossi, S., Tecchio, F., Pasqualetti, P., Ulivelli, M., Pizzella, V., Romani, G.L., Passero, S., Battistini, N. & Rossini, P.M. (2002) Somatosensory processing during movement observation in humans. Clin. Neurophysiol., 113, 16-24.
71. Sakamoto, M., Muraoka, T., Mizuguchi, N. & Kanosue, K. (2009) Combining observation and imagery of an action enhances human corticospinal excitability. Neurosci. Res., 65, 23-27.
72. Serino, A., De Filippo, L., Casavecchia, C., Coccia, M., Shiffrar, M. & Làdavas, E. (2010) Lesions to the motor system affect action perception. J. Cogn. Neurosci., 22, 413-426.
73. Thompson, J.C., Clarke, M., Stewart, T. & Puce, A. (2005) Configural processing of biological motion in human superior temporal sulcus. J. Neurosci., 25, 9059-9066.
74. Townsend, J.T. & Ashby, F.G. (1983) The Stochastic Modeling of Elementary Psychological Processes. Cambridge University Press, Cambridge.
75. Truccolo, W., Friehs, G.M., Donoghue, J.P. & Hochberg, L.R. (2008) Primary motor cortex tuning to intended movement kinematics in humans with tetraplegia. J. Neurosci., 28, 1163-1178.
76. Urgesi, C., Berlucchi, G. & Aglioti, S.M. (2004) Magnetic stimulation of extrastriate body area impairs visual processing of nonfacial body parts. Curr. Biol., 14, 2130-2134.
77. Urgesi, C., Calvo-Merino, B., Haggard, P. & Aglioti, S.M. (2007a) Transcranial magnetic stimulation reveals two cortical pathways for visual body processing. J. Neurosci., 27, 8023-8030.
78. Urgesi, C., Candidi, M., Ionta, S. & Aglioti, S.M. (2007b) Representation of body identity and body actions in extrastriate body area and ventral premotor cortex. Nat. Neurosci., 10, 30-31.
79. Urgesi, C., Savonitto, M.M., Fabbro, F. & Aglioti, S.M. (2012) Long- and short-term plastic modeling of action prediction abilities in volleyball. Psychol. Res., 76, 542-560.
80. Waters, R.L., Adkins, R.H. & Yakura, J.S. (1991) Definition of complete spinal cord injury. Paraplegia, 29, 573-581.
81. Wei, T., Liang, X., He, Y., Zang, Y., Han, Z., Caramazza, A. & Bi, Y. (2012) Predicting conceptual processing capacity from spontaneous neuronal activity of the left middle temporal gyrus. J. Neurosci., 32, 481-489.
82. Wilson, M. & Knoblich, G. (2005) The case for motor involvement in perceiving conspecifics. Psychol. Bull., 131, 460-473.
83. Wrigley, P.J., Gustin, S.M., Macey, P.M., Nash, P.G., Gandevia, S.C., Macefield, V.G., Siddall, P.J. & Henderson, L.A. (2009) Anatomical changes in human motor cortex and motor pathways following complete thoracic spinal cord injury. Cereb. Cortex, 19, 224-232.
84. Yovel, G., Pelc, T. & Lubetzky, I. (2010) It's all in your head: why is the body inversion effect abolished for headless bodies?J. Exp. Psychol. Hum. Percept. Perform., 36, 759-767.