On the role of object information in action observation: An fMRI study

Cerebral Cortex

Volumn 20, Issue 12, 2010, Pages 2798-2809

  Bach, Patric ^a,b   Peelen, Marius V ^c,d   Tipper, Steven P ^a  

^a BANGOR UNIVERSITY   (United Kingdom)

^b UNIVERSITY OF PLYMOUTH   (United Kingdom)

^c UNIVERSITY OF TRENTO   (Italy)

^d HARVARD UNIVERSITY   (United States)

Author keywords

intraparietal sulcus; middle frontal gyrus; mirror neurons; premotor cortex; tool use

Indexed keywords

ADULT; ARTICLE; BEHAVIOR; BRAIN FUNCTION; BRAIN MAPPING; BRAIN REGION; COGNITION; FRONTAL CORTEX; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HUMAN; HUMAN EXPERIMENT; INFORMATION; MOTOR PERFORMANCE; MOTOR SYSTEM; NORMAL HUMAN; PARIETAL LOBE; PREMOTOR CORTEX; PRIORITY JOURNAL; STIMULUS RESPONSE; SUBICULUM; TASK PERFORMANCE; VISUAL CORTEX;

ADOLESCENT; ADULT; BRAIN; BRAIN MAPPING; HUMANS; IMAGE INTERPRETATION, COMPUTER-ASSISTED; MAGNETIC RESONANCE IMAGING; MOVEMENT; SPACE PERCEPTION; TOOL USE BEHAVIOR; VISUAL PERCEPTION; YOUNG ADULT;

EID: 78349296770     PISSN: 10473211     EISSN: 14602199     Source Type: Journal    
DOI: 10.1093/cercor/bhq026     Document Type: Article

References (102)

1. Bach P, Gunter TC, Knoblich G, Prinz W, Friederici AD. 2008. N400-like negativities in action perception reflect two components of an action representation. Soc Neurosci. 4(3):212-232.
2. Bach P, Knoblich G, Gunter TC, Friederici AD, Prinz W. 2005. Action comprehension: deriving spatial and functional relations. J Exp Psychol Hum Percept Perform. 31(3):465-479.
3. Baumgaertner A, Buccino G, Lange R, McNamara A, Binkofski F. 2007. Polymodal conceptual processing of human biological actions in the left inferior frontal lobe. Eur J Neurosci. 25(3):881-889.
4. Begliomini C, Caria A, Grodd W, Castiello U. 2007. Comparing natural and constrained movements: new insights into the visuomotor control of grasping. PLoS One. 2(10):e1108.
5. Binkofski F, Buccino G. 2006. The role of ventral premotor cortex in action execution and action understanding. J Physiol. 99:396-405.
6. Binkofski F, Dohle C, Posse S, Stephan KM, Hefter H, Seitz RJ, Freund HJ. 1998. Human anterior intraparietal area subserves prehension: a combined lesion and functional MRI activation study. Neurology. 50:1253-1259.
7. Boria S, Fabbri-Destro M, Cattaneo L, Sparaci L, Sinigaglia C, Santelli E, Cossu G, Rizzolatti G. 2009. Intention understanding in autism. PLoS One. 4(5):e5596doi: 10.1371/journal.pone.0005596.
8. Boronat C, Buxbaum LJ, Coslett H, Tang K, Saffran E, Kimberg D, Detre J. 2005. Distinctions between manipulation and function knowledge of objects: evidence from functional magnetic resonance imaging. Brain Res Cogn Brain Res. 23:361-373.
9. Botvinick MM, Buxbaum LJ, Bylsma LM, Jax SA. 2009. Toward an integrated account of object and action selection: a computational analysis and empirical findings from reaching-to-grasp and tool-use. Neuropsychologia. 47(3):671-683.
10. Brass M, Schmitt R, Spengler S, Gergely G. 2007. Investigating action understanding: inferential processes versus motor simulation. Curr Biol. 17(24):2117-2121.
11. Buccino G, Binkofski F, Fink GR, Fadiga L, Fogassi L, Gallese V, Seitz RJ, Zilles K, Rizzolatti G, Freund HJ. 2001. Action observation activates premotor and parietal areas in a somatotopic manner: an fMRI study. Eur J Neurosci. 13:400-404.
12. Buxbaum LJ. 2001. Ideomotor apraxia: a call to action. Neurocase. 7:445-458.
13. Buxbaum LJ, Kyle KM, Grossman M, Coslett HB. 2007. Left inferior parietal representations for skilled hand-object interactions: evidence from stroke and corticobasal degeneration. Cortex. 43(3):411-423.
14. Buxbaum LJ, Kyle KM, Menon R. 2005. On beyond mirror neurons: internal representations subserving imitation and recognition of skilled object-related actions in humans. Brain Res Cogn Brain Res. 25(1):226-239.
15. Buxbaum LJ, Saffran EM. 1998. Knowing 'how' vs "what for": a new dissociation. Brain Lang. 65:73-86.
16. Buxbaum LJ, Sirigu A, Schwartz M, Klatzky R. 2003. Cognitive representations of hand posture in ideomotor apraxia. Neuropsycho-logia. 41(8):1091-1113.
17. Buxbaum LJ, Tyle KM, Tang K, Detre JA. 2006. Neural substrates of knowledge of hand postures for object grasping and functional object use: evidence from fMRI. Brain Res. 1117(1):175-185.
18. Calvo-Merino B, Glaser DE, Grezes J, Passingham RE, Haggard P. 2005. Action observation and acquired motor skills: an fMRI study with expert dancers. Cereb Cortex. 15:1243-1249.
19. Canessa N, Borgo F, Cappa SF, Perani D, Falini A, Buccino G, Tettamanti M, Shallice T. 2008. The different neural correlates of action and functional knowledge in semantic memory: an FMRI study. Cereb Cortex. 18(4):740-751.
20. Castiello U. 2005. The neuroscience of grasping. Nat Rev Neurosci. 6:726-736.
21. Chao LL, Haxby JV, Martin A. 1999. Attribute-based neural substrates in temporal cortex for perceiving and knowing about objects. Nat Neurosci. 2:913-919.
22. Chao LL, Martin A. 2000. Representation of manipulable man-made objects in the dorsal stream. Neuro Image. 12:478-484.
23. Chao LL, Weisberg J, Martin A. 2002. Experience-dependent modulation of category-related brain activity. Cereb Cortex. 12(5):545-551.
24. Chong T, Cunnington R, Williams M, Kanwisher N, Mattingley J. 2008. fMRI adaptation reveals mirror neurons in human inferior parietal cortex. Curr Biol. 18(20):1576-1580.
25. Creem SH, Proffitt DR. 2001. Grasping objects by their handles: a necessary interaction between cognition and action. J Exp Psychol Hum Percept Perform. 1:218-228.
26. Creem-Regehr SH, Dilda V, Vicchrilli AE, Federer FL, James N. 2007. The influence of complex action knowledge on representations of novel graspable objects: evidence from functional magnetic resonance imaging. J Int Neuropsychol Soc. 13(6):1009-1020.
27. Cross ES, Hamilton AF, Grafton ST. 2006. Building a motor simulation de novo: observation of dance by dancers. Neuro Image. 31(3):1257-1267.
28. Culham JC, Danckert SL, DeSouza JF, Gati JS, Menon RS, Goodale MA. 2003. Visually guided grasping produces fMRI activation in dorsal but not ventral stream brain areas. Exp Brain Res. 153:180-189.
29. Daprati E, Sirigu A. 2006. How we interact with objects: learning from brain lesions. Trends Cogn Sci. 10:265-270.
30. de Lange FP, Spronk M, Willems RM, Toni I, Bekkering H. 2008. Complementary systems for understanding action intentions. Curr Biol. 18:454-457.
31. di Pellegrino G, Fadiga L, Fogassi L, Gallese L, Rizzolatti G. 1992. Understanding motor events: a neurophysiological study. Exp Brain Res. 91:176-189.
32. Downing PE, Jiang Y, Shuman M, Kanwisher N. 2001. A cortical area selective for visual processing of the human body. Science. 293:2470-2473.
33. Ebisch SJ, Babiloni C, Del Gratta C, Ferretti A, Perrucci MG, Caulo M, Sitskoorn MM, Romani GL. 2007. Human neural systems for conceptual knowledge of proper object use: a functional magnetic resonance imaging study. Cereb Cortex. 17(11):2744-2751.
34. Frey SH. 2007. What puts the how in where: semantic and sensori-motor bases of everyday tool use. Cortex. 43:368-375.
35. Frey SH, Vinton D, Norlund R, Grafton ST. 2005. Cortical topography of human anterior intraparietal cortex active during visually guided grasping. Brain Res Cogn Brain Res. 23(2-3):397-405.
36. Gallese L, Fadiga L, Fogassi L, Rizzolatti G. 1996. Action recognition in the premotor cortex. Brain. 119:593-609.
37. Genovese CR, Lazar NA, Nichols T. 2002. Thresholding of statistical maps in functional neuroimaging using the false discovery rate. Neuro Image. 15:870-878.
38. Glover S. 2004. Separate visual representations in the planning and control of action. Behav Brain Sci. 27:3-78.
39. Goldenberg G. 2009. Apraxia and the parietal lobes. Neuropsychologia. 47(6):1449-1459.
40. Goldenberg G, Spatt J. 2009. The neural basis of tool use. Brain. 132: 1645-1655.
41. Goodale MA, Humphrey GK. 1998. The objects of action and perception. Cognition. 67(1-2):181-207.
42. Grabowski TJ, Damasio H, Damasio AR. 1998. Premotor and prefrontal correlates of category-related lexical retrieval. Neuro Image. 7(3): 232-243.
43. Grafton ST, Hamilton AF. 2007. Evidence for a distributed hierarchy of action representation in the brain. Hum Mov Sci. 26(4):590-616.
44. Green CB, Hummel JE. 2006. Familiar interacting object pairs are perceptually grouped. J Exp Psychol Hum Percept Perform. 32(5): 1107-1119.
45. Greenlee MW. 2000. Human cortical areas underlying the perception of optic flow: brain imaging studies. Int Rev Neurobiol. 44:269-292.
46. Grezes J, Armony L, Rowe J, Passingham RE. 2003. Activations related to "mirror" and "canonical" neurones in the human brain: an fMRI study. Neuro Image. 18:928-937.
47. Haaland KY, Harrington DL, Knight RT. 2000. Neural representations of skilled movement. Brain. 123:2306-2313.
48. Hamilton AF, Grafton ST. 2006. Goal representation in human anterior intraparietal sulcus. J Neurosci. 26:1133-1137.
49. Hauk O, Johnsrude I, Pulvermueller F. 2004. Somatotopic representation of action words in human motor and premotor cortex. Neuron. 41:301-307.
50. Hodges JR, Bozeat S, Lambon Ralph MA, Patterson K, Spatt J. 2000. The role of conceptual knowledge in object use evidence from semantic dementia. Brain. 123:1913-1925.
51. Hodges JR, Spatt J, Patterson K. 1999. "What" and "how": evidence for the dissociation of object knowledge and mechanical problem-solving skills in the human brain. Proc Natl Acad Sci USA. 96:9444-9448.
52. Iacoboni M, Woods RP, Brass M, Bekkering H, Mazziotta JC, Rizzolatti G. 1999. Cortical mechanisms of human imitation. Science. 286: 2526-2528.
53. Johnson-Frey SH. 2003. What's so special about human tool use. Neuron. 39:201-204.
54. Johnson-Frey SH. 2004. The neural bases of complex tool use in humans. Trends Cogn Sci. 8(2):71-78.
55. Johnson-Frey SH, Grafton ST. 2003. From "acting on" to "acting with": the functional anatomy of action representation. In: Prablanc C, Pelisson D, Rossetti Y, editors. Space coding and action production. New York: Elsevier. p. 127-139.
56. Johnson-Frey SH, Maloof FR, Newman-Norlund R, Farrer C, Inati S, Grafton ST. 2003. Actions or hand-object-interactions: human inferior frontal cortex in action observation. Neuron. 39:1053-1058.
57. Johnson-Frey SH, Newman-Norlund R, Grafton ST. 2005. A distributed left hemisphere network active during planning of everyday tool use skills. Cereb Cortex. 15(6):681-695.
58. Kellenbach ML, Brett M, Patterson K. 2003. Actions speak louder than functions: the importance of manipulability and action in tool representation. J Cogn Neurosci. 15(1):30-46.
59. Knoblich G, Flach R. 2001. Predicting the effects of actions: interactions of perception and action. Psychol Sci. 12:467-472.
60. Koski L, Iacoboni M, Mazziotta JC. 2002. Deconstructing apraxia: understanding disorders of intentional movement after stroke. Curr Opin Neurol. 15(1):71-77.
61. Kourtzi Z, Kanwisher N. 2000. Activation in human MT/MST by static images with implied motion. J Cogn Neurosci. 12(1):48-55.
62. Lestou V, Pollick F, Kourtzi Z. 2008. Neural substrates for action understanding at different description levels in the human brain. J Cogn Neurosci. 20:324-341.
63. Lewis JW. 2006. Cortical networks related to human use of tools. Neuroscientist. 12:211-231.
64. Liepmann H. 1920. Apraxie: Brugschs Ergebnisse der Gesamten Medizin. Berlin (Germany): Urban & Schwarzenberg.
65. Lindemann O, Stenneken P, van Schie HT, Bekkering H. 2006. Semantic activation in action planning. J Exp Psychol Hum Percept Perform. 32:633-643.
66. Mahon BZ, Milleville SC, Negri GAL, Rumiati RI, Caramazza A, Martin A. 2007. Action-related properties shape object representations in the ventral stream. Neuron. 55(3):507-520.
67. Malach R, Levy I, Hasson U. 2002. The topography of high-order human object areas. Trends Cogn Sci. 6(4):176-184.
68. Manthey S, Schubotz RI, von Cramon DY. 2003. Premotor cortex in observing erroneous action: an fMRI study. Brain Res Cogn Brain Res. 15:296-307.
69. Milner AD, Goodale MA. 1995. The visual brain in action. Oxford: Oxford University Press.
70. Nelissen K, Luppino G, Vanduffel W, Rizzolatti G, Orban GA. 2005. Observing others: multiple action representation in the frontal lobe. Science. 310:332-336.
71. Noppeney U. 2008. The neural systems of tool and action semantics: a perspective from functional imaging. J Physiol Paris. 102(1-3):40-49.
72. Nowak MA, Plotkin JB, Jansen VAA. 2000. The evolution of syntactic communication. Nature. 404:495-498.
73. Ochipa C, Rothi LJG, Heilman KM. 1989. Ideational apraxia: a deficit in tool selection and use. Ann Neurol. 25:190-193.
74. Oztop E, Arbib MA. 2002. Schema design and implementation of the grasp-related mirror neuron system. Biol Cybern. 87:116-140.
75. Peelen MV, Downing PE. 2005. Within-subject reproducibility of category-specific visual activation with functional MRI. Hum Brain Mapp. 25:402-408.
76. 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(5):e5389. doi: 10.1371/journal.pone.0005389.
77. Riddoch JM, Humphreys GW, Edwards S, Baker T, Wilson K. 2003. Seeing the action: neurophysiological evidence for action-based effects on object selection. Nat Neurosci. 6(1):82-89.
78. Rizzolatti G, Craighero L. 2004. The mirror neuron system. Annu Rev Neurosci. 27:169-192.
79. Rizzolatti G, Luppino G. 2001. The cortical motor system. Neuron. 31:889-901.
80. Roebroeck A, Formisano E, Goebel R. 2005. Mapping directed influence over the brain using Granger causality and fMRI. Neuro Image. 25:230-242.
81. Rozzi S, Ferrari PF, Bonini L, Rizzolatti G, Fogassi L. 2008. Functional organization of inferior parietal lobule convexity in the macaque monkey: electrophysiological characterization of motor, sensory and mirror responses and their correlation with cytoarchitectonic areas. Eur J Neurosci. 28(8):1569-1588.
82. Rumiati RI, Weiss PH, Shallice T, Ottoboni G, Noth J, Zilles K, Fink GR. 2004. The neural basis of pantomiming the use of visually presented objects. Neuro Image. 21:1224-1231.
83. Shikata E, Hamzei F, Glauche V, Knab R, Dettmers C, Weiller C, Buchel C. 2001. Surface orientation discrimination activates caudal and anterior intraparietal sulcus in humans: an event-related fMRI study. J Neurophysiol. 85:1309-1314.
84. Shikata E, Hamzei F, Glauche V, Koch M, Weiller C, Binkofski F, Buchel C. 2003. Functional properties and interaction of the anterior and posterior intraparietal areas in humans. Eur J Neurosci. 17:1105-1110.
85. Shmuelof L, Zohary E. 2006. A mirror representation of others' actions in the human anterior parietal cortex. J Neurosci. 26(38): 9736-9742.
86. Sirigu A, Duhamel J-R, Poncet M. 1991. The role of sensorimotor experience in object recognition. A case of multimodal agnosia. Brain. 114:2555-2573.
87. Sitnikova T, Kuperberg G, Holcomb PJ. 2003. Semantic integration in videos of real-world events: an electrophysiological investigation. Psychophysiology. 40(1):160-164.
88. Sturmer B, Aschersleben G, Prinz W. 2000. Correspondence effects with manual gestures and postures: a study of imitation. J Exp Psychol Hum Percept Perform. 26(6):1746-1759.
89. Talairach J, Tournoux P. 1988. Co-planar stereotaxic atlas of the human brain. New York: Thieme.
90. Tunik E, Frey SH, Grafton ST. 2005. Virtual lesions of the anterior intraparietal area disrupt goal-dependent on-line adjustments of grasp. Nat Neurosci. 8:505-511.
91. Tunik E, Lo O-Y, Adamovich SV. 2008. Transcranial magnetic stimulation to the frontal operculum and supramarginal gyrus disrupts planning of outcome-based hand-object interactions. J Neurosci. 28(53):14422-14427.
92. Tyler LK, Stamatakis EA, Dick E, Bright P, Fletcher P, Moss H. 2003. Objects and their actions: evidence for a neurally distributed semantic system. Neuro Image. 18(2):542-557.
93. Urgesi C, Moro V, Candidi M, Aglioti SM. 2006. Mapping implied body actions in the human motor system. J Neurosci. 26:7942-7949.
94. Valyear KF, Cavina-Pratesi C, Stiglick AJ, Culham JC. 2007. Does tool-related fMRI activity within the intraparietal sulcus reflect the plan to grasp? Neuro Image. 36:94-100.
95. van Elk M, van Schie HT, Bekkering. 2008. Conceptual knowledge for understanding other's actions is organized primarily around action goals. Exp Brain Res. 189(1):99-107.
96. Villarreal M, Fridman EA, Amengual A, Falasco G, Gerscovich ER, Ulloa ER, Leiguarda RC. 2008. The neural substrate of gesture recognition. Neuropsychologia. 46(9):2371-2382.
97. Vingerhoets G. 2008. Knowing about tools: neural correlates of tool familiarity and experience. Neuro Image. 40(3):1380-1391.
98. Vingerhoets G, de Lange FP, Vandemaele P, Deblaere K, Achten E. 2002. Motor imagery in mental rotation: an fMRI study. Neuro Image. 17(3):1623-1633.
99. Weisberg J, van Turennout M, Martin A. 2007. A neural system for learning about object function. Cereb Cortex. 17(3):513-521.
100. Wilson M, Knoblich G. 2005. The case for motor involvement in perceiving conspecifics. Psychol Bull. 131:460-473.
101. Wohlschlager A, Wohlschlager A. 1998. Mental and manual rotation. J Exp Psychol Hum Percept Perform. 24(2):397-412.
102. Zacks JM. 2008. Neuroimaging studies of mental rotation: a meta-analysis and review. J Cogn Neurosci. 20:1-19.