Neural networks for action representation: A functional magnetic-resonance imaging and dynamic causal modeling study

Frontiers in Human Neuroscience

Volumn , Issue AUGUST, 2012, Pages

  Sasaki, Akihiro T ^a,b,c   Kochiyama, Takanori ^d   Sugiura, Motoaki ^e   Tanabe, Hiroki C ^a,b   Sadato, Norihiro ^a,b,f  

^a NATIONAL INSTITUTE FOR PHYSIOLOGICAL SCIENCES   (Japan)

^b GRADUATE UNIVERSITY FOR ADVANCED STUDIES   (Japan)

^c JAPAN SOCIETY FOR THE PROMOTION OF SCIENCE   (Japan)

^d KYOTO UNIVERSITY   (Japan)

^e TOHOKU UNIVERSITY   (Japan)

^f UNIVERSITY OF FUKUI   (Japan)

Author keywords

Cross modal transformation; Mirror system; Network analysis; Posterior parietal cortex; Sensorimotor integration

Indexed keywords

ADULT; ARTICLE; BRAIN REGION; CAUSAL MODELING; CONTROLLED STUDY; ELECTROMYOGRAPHY; FEEDBACK SYSTEM; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HAND MOVEMENT; HUMAN; HUMAN EXPERIMENT; IMAGE ANALYSIS; INFERIOR PARIETAL LOBULE; MALE; MENTAL TASK; NERVE CELL NETWORK; NEUROIMAGING; NORMAL HUMAN; PARTICIPANT OBSERVATION; PREMOTOR CORTEX; SENSORIMOTOR CORTEX; SUPERIOR TEMPORAL SULCUS; TASK PERFORMANCE; VENTRAL PREMOTOR AREA;

EID: 84933673203     PISSN: 16625161     EISSN: 16625161     Source Type: Journal    
DOI: 10.3389/fnhum.2012.00236     Document Type: Article

References (102)

1. Adolphs, R. (2009). The social brain: neural basis of social knowledge. Annu. Rev. Psychol. 60, 693-716.
2. Aertsen, A., and Presl, H. (1991). "Dynamics of activity and connectivity in physiological neuronal networks," in Nonlinear Dynamics and Neuronal Networks, ed H. G. Schuster (New York, NY: VCH Publishers Inc.), 281-302.
3. Barsalou, L. W., Niedenthal, P. M., Barbey, A. K., and Ruppert, J. A. (2003). Social embodiment. Psychol. Learn. Motiv. 43, 43-92.
4. Beauchamp, M. S., Lee, K. E., Haxby, J. V., and Martin, A. (2003). FMRI responses to video and point-light displays of moving humans and manipulable objects. J. Cogn. Neurosci. 15, 991-1001.
5. Benjamini, Y., and Hochberg, Y. (1995). Controlling the false discovery rate: a practical and powerful approach to multiple testing. J. R. Stat. Soc. er. B 57 289-300.
6. Blake, R., and Shiffrar, M. (2007). Perception of human motion. Annu. Rev. Psychol. 58, 47-73.
7. Blakemore, S. J., and Decety, J. (2001). From the perception of action to the understanding of intention. Nat. Rev. Neurosci. 2, 561-567.
8. Bonda, E., Petrides, M., and Evans, A. (1996). Neural systems for tactual memories. J. Neurophysiol. 75, 1730-1737.
9. Brass, M., and Heyes, C. (2005). Imitation: is cognitive neuroscience solving the correspondence problem? Trends Cogn.Sci. 9, 489-495.
10. Buccino, G., Lui, F., Canessa, N., Patteri, I., Lagravinese, G., Benuzzi, F., Porro, C. A., and Rizzolatti, G. (2004). Neural circuits involved in the recognition of actions performed by non conspecifics: an FMRI study. J. Cogn. Neurosci. 16, 114-126.
11. Buxton, R. B., Wong, E. C., and Frank, L. R. (1998). Dynamics of blood flow and oxygenation changes during brain activation: the balloon model. Magn. Reson. Med. 855-864.
12. Caminiti, R., Ferraina, S., and Johnson, P. B. (1996). The sources of visual information to the primate frontal lobe: a novel role for the superior parietal lobule. Cereb. Cortex 6, 319-328.
13. Campbell, R., Macsweeney, M., Surguladze, S., Calvert, G., McGuire, P., Suckling, J., Brammer, M. J., and David, A. S. (2001). Cortical substrates for the perception of face actions: an fMRI study of the specificity of activation for seen speech and for meaningless lower-face acts (gurning). Brain Res. Cogn. Brain Res. 12, 233-243.
14. Caspers, S., Eickhoff, S. B., Geyer, S., Scheperjans, F., Mohlberg, H., Zilles, K., and Amunts, K. (2008). The human inferior parietal lobule in stereotaxic space. Brain Struct. Funct. 212, 481-495.
15. Caspers, S., Eickhoff, S. B., Rick, T., Von Kapri, A., Kuhlen, T., Huang, R., Shah, N. J., and Zilles, K. (2011). Probabilistic fibre tract analysis of cytoarchitectonically defined human inferior parietal lobule areas reveals similarities to macaques. Neuroimage 58, 362-380.
16. Caspers, S., Geyer, S., Schleicher, A., Mohlberg, H., Amunts, K., and Zilles, K. (2006). The human inferior parietal cortex: cytoarchitec-tonic parcellation and interindi-vidual variability. Neuroimage 33, 430-448.
17. Caspers, S., Zilles, K., Laird, A. R., and Eickhoff, S. B. (2010). ALE meta-analysis of action observation and imitation in the human brain. Neuroimage 50, 1148-1167.
18. Catani, M., Jones, D. K., and Ffytche, D. H. (2005). Perisylvian language networks of the human brain. Ann. Neurol. 57, 8-16.
19. Chartrand, T. L., and Bargh, J. A. (1999). The chameleon effect: the perception-behavior link and social interaction. J. Pers. Soc. Psychol. 76, 893-910.
20. Craighero, L., Bello, A., Fadiga, L., and Rizzolatti, G. (2002). Hand action preparation influences the responses to hand pictures. Neuropsychologia 40, 492-502.
21. Csibra, G., and Gergely, G. (2007). Obsessed with goals': functions and mechanisms of teleological interpretation of actions in humans. Acta Psychol (Amst.) 124, 60-78.
22. Deiber, M. P., Wise, S. P., Honda, M., Catalan, M. J., Grafman, J., and Hallett, M. (1997). Frontal and parietal networks for conditional motor learning: a positron emission tomography study. J. Neurophysiol 78, 977-991.
23. Del Giudice, M., Manera, V., and Keysers, C. (2009). Programmed to learn? The ontogeny of mirror neurons. Dev. Sci. 12, 350-363.
24. di Pellegrino, G., Fadiga, L., Fogassi, L., Gallese, V., and Rizzolatti, G. (1992). Understanding motor events: a neurophysiological study. Exp. Brain Res. 91, 176-180.
25. Dinstein, I., Hasson, U., Rubin, N., and Heeger, D. J. (2007). Brain areas selective for both observed and executed movements. J. Neurophysiol 98, 1415-1427.
26. Dumoulin, S. O., Bittar, R. G., Kabani, N. J., Baker, C. L. Jr., Le Goualher, G., Bruce Pike, G., and Evans, A. C. (2000). A new anatomical landmark for reliable identification of human area V5/MT: a quantitative analysis of sulcal patterning. Cereb. Cortex 10, 454-463.
27. Eickhoff, S. B., Klaas, S. E., Mohlberg, H., Grefkes, C., Fink, G. R., Amunts, K., andZilles, K. (2005). Anew SPM toolbox for combining probabilistic cytoarchitectonic maps and functional imaging data. Neuroimage 25, 1325-1335.
28. Fadiga, L., Craighero, L., and Olivier, E. (2005). Human motor cortex excitability during the perception of others' action. Curr. Opin. Neurobiol 15,213-218.
29. Fadiga, L., Fogassi, L., Pavesi, G., and Rizzolatti, G. (1995). Motor facilitation during action observation: a magnetic stimulation study. J. Neurophysiol 73, 2608-2611.
30. Fazio, P., Cantagallo, A., Craighero, L., D'Ausilio, A., Roy, A. C, Pozzo, T., Calzolari, F., Granieri, E., and Fadiga, L. (2009). Encoding of human action in Broca's area. Brain 132, 1980-1988.
31. Flanagan, J. R., Vetter, P., Johansson, R. S., and Wolpert, D. M. (2003). Prediction precedes control in motor learning. Curr. Biol 13, 146-150.
32. Friston, K. J. (2007). Statistical Parametric Mapping. London: Academic Press.
33. Friston, K. J., Harrison, L., and Penny, W. D. (2003). Dynamic causal modelling. Neuroimage 19 1273-1302.
34. Friston, K. J., Tononi, G., Reeke, G. N J., Sporns, O., and Edelman, G. M (1994). Value-dependent selection in the brain: simulation in a synthetic neural model. Neuroscience 59, 229-243.
35. Gallese, V., Fadiga, L., Fogassi, L., and Rizzolatti, G. (1996). Action recog nition in the premotor cortex. Brain 119(Pt 2), 593-609.
36. Gazzola, V., and Keysers, C. (2009) The observation and execution o actions share motor and somatosensory voxels in all tested participants: single-participant analysis of unsmoothed fMRI data. Cereb Cortex 19, 1239-1255.
37. Giese, M. A., and Poggio, T. (2003) Neural mechanisms for the recogni tion of biological movements. Nat Rev. Neurosci. 4, 179-192.
38. Gobbini, M. I., Koralek, A. C., Bryan, R E., Montgomery, K. J., and Haxby J. V. (2007). Two takes on the socia brain: a comparison of theory o mind tasks. J. Cogn. Neurosci. 19 1803-1814.
39. Grefkes, C., Geyer, S., Schormann, T., Roland, P., and Zilles, K. (2001) Human somatosensory area 2 observer-independent cytoarchi tectonic mapping, interindividua variability, and population map Neuroimage 14, 617-631.
40. Grezes, J., Costes, N., and Decety, J (1998). Top-down effect of strategy on the perception of human bio logical motion: a PET investigation Cogn. Neuropsychol. 15, 553-582.
41. Grol, M. J., Majdandzic, J., Stephan K. E., Verhagen, L., Dijkerman, H C., Bekkering, H., Verstraten, F A., and Toni, I. (2007). Parieto frontal connectivity during visuall guided grasping. J. Neurosci. 27 11877-11887.
42. Grossman, E. D., and Blake, R. (2002) Brain areas active during visua perception of biological motion Neuron 35, 1167-1175.
43. Grossman, E. D., Jardine, N. L., and Pyles, J. A. (2010). MRI-adaptation reveals invariant coding of biolog ical motion on the human STS Front. Hum. Neurosci. 4:15. doi 10.3389/neuro.09.015.2010
44. Hamilton, A. F. (2008). Emulation and mimicry for social interaction: theoretical approach to imitation in autism. Q. J. Exp. Psychol. (Hove) 61 101-115.
45. Hamilton, A. F., and Grafton, S. T (2006). Goal representation in human anteiror intraparietal sulcus J. Neurosci. 26, 1133-1137.
46. Hattori, N., Shibasaki, H., Wheaton L. A., Wu, T., Matsuhashi, M., and Hallett, M. (2009). Discrete parieto-frontal functional connectivity related to grasping. J. Neurophysiol. 101, 1267-1282.
47. Haxby, J. V., Hoffman, E. A., and Gobbini, M. I. (2000). The distributed human neural system for face perception. Trends Cogn. Sci. 4, 223-233.
48. Hickok, G., and Poeppel, D. (2000). Towards a functional neuroanatomy of speech perception. Trends Cogn. Sci. 4, 131-138.
49. Jeannerod, M. (2006). Motor Cognition. What Actions Tell the Self. Oxford: Oxford University Press.
50. Jeannerod, M., Arbib, M. A., Rizzolatti, G., and Sakata, H. (1995). Grasping objects: the cortical mechanisms of visuomotor transformation. Trends Neurosci. 18, 314-320.
51. Keysers, C., and Perrett, D. I. (2004). Demystifying social cognition: a Hebbian perspective. Trends Cogn. Sci. 8, 501-507.
52. Kilner, J. M., Friston, K. J., and Frith, C. D. (2007a). The mirror-neuron system: a Bayesian perspective. Neuroreport 18, 619-623.
53. Kilner, J. M., Friston, K. J., and Frith, C. D. (2007b). Predictive coding: an account of the mirror neuron system. Cogn. Process. 8, 159-166.
54. Kilner, J. M., and Frith, C. D. (2007). A possible role for primary motor cortex during action observation. Proc. Natl. Acad. Sci. U.S.A. 104, 8683-8684.
55. Lakin, J. L., and Chartrand, T. L. (2003). Using nonconscious behavioral mimicry to create affiliation and rapport. Psychol. Sci. 14, 334-339.
56. Lamm, C., Fischer, M. H., and Decety, J. (2007). Predicting the actions of others taps into one's own somatosensory representations a functional MRI study. Neuropsychologia 45, 2480-2491.
57. Maeda, F., Chang, V. Y., Mazziotta, J., and Iacoboni, M. (2001). Experience-dependent modulation of motor corticospinal excitability during action observation. Exp. Brain Res. 140, 241-244.
58. Maeda, F., Kleiner-Fisman, G., and Pascual-Leone, A. (2002). Motor facilitation while observing hand actions: specificity of the effect and role of observer's orientation. J. Neurophysiol. 87, 1329-1335.
59. Makuuchi, M., Someya, Y., Ogawa, S., and Takayama, Y. (2012). Hand shape selection in pantomimed grasping: interaction between the dorsal and the ventral visual streams and convergence on the ventral premotor area. Hum. Brain Mapp. 33, 1821-1833.
60. Martin, A., and Weisberg, J. (2003) Neural foundations for under standing social and mechanica concepts. Cogn. Neuropsychol. 20 575-587.
61. Materna, S., Dicke, P. W., and Thei P. (2008). Dissociable roles of the superior temporal sulcus and the intraparietal sulcus in joint attention: a functional magnetic resonance imaging study. J. Cogn Neurosci. 20, 1-11.
62. Matsumura, M., Sadato, N. Kochiyama, T., Nakamura, S., Naito E., Matsunami, K., Kawashima, R, Fukuda, H., and Yonekura, Y (2004). Role of the cerebellum i implicit motor skill learning: a PE study. Brain Res. Bull. 63, 471-483.
63. McIntosh, D. N., Reichmann-Decke A., Winkielman, P., and Wilbarger J. L. (2006). When the social mirror breaks: deficits in automatic but not voluntary, mimicry of emotional facial expressions in autism Dev. Sci. 9, 295-302.
64. Miall, R. C. (2003). Connecting mirror neurons and forward models. Neuroreport 14, 2135-2137.
65. Michels, L., Lappe, M., and Vaina, L M. (2005). Visual areas involve in the perception of human movement from dynamic form analysis Neuro report 16, 1037-1041.
66. Mitchell, J. P. (2008). Activity in righ temporo-parietal junction is no selective for theory-of-mind. Cereb Cortex 18, 262-271.
67. Molenberghs, P., Brander, C., Mattingley, J. B., and Cunnington R. (2010). The role of the superio temporal sulcus and the mirro neuron system in imitation. Hum Brain Mapp. 31, 1316-1326.
68. Molenberghs, P., Cunnington, R and Mattingley, J. B. (2012). Brai regions with mirror properties: meta-analysis of 125 human fMR studies. Neurosci. Biobehav. Rev. 36 341-349.
69. Morin, O., and Grezes, J. (2008). Wha is "mirror" in the premotor cor tex? A review. Neurophysiol. Clin. 38 189-195.
70. Nadel, J. (2002). "Imitation an imitation recognition: functiona use in preverbal infants and non verbal children with autism," in The Imitative Mind: Development Evolution and Brain Bases, eds A Meltzoff and W. Prinz (Cambridge MA: Cambridge University Press) 42-62.
71. Oldfield, R. (1971). The assessmen and analysis of handedness the Edinburgh inventory Neuropsychologia 9, 97-113.
72. Puce, A., and Perrett, D. (2003) Electrophysiology and brain imag ing of biological motion. Philos Trans. R. Soc. Lond. B Biol. Sci. 358 435-445.
73. Rilling, J. K., Glasser, M. F., Preuss T. M., Ma, X., Zhao, T., Hu, X. and Behrens, T. E. (2008). The evolution of the arcuate fasciculu revealed with comparative DTI. Nat Neurosci. 11, 426-428.
74. Rizzolatti, G., Camarda, R., Fogassi, L. Gentilucci, M., Luppino, G., and Matelli, M. (1988). Functional organization of inferior area 6 in the macaque monkey. II. Area F5 an the control of distal movements Exp. Brain Res. 71, 491-507.
75. Rizzolatti, G., and Craighero, L. (2004) The mirror-neuron system. Annu Rev. Neurosci. 27, 169-192.
76. Rizzolatti, G., Fadiga, L., Gallese, V and Fogassi, L. (1996). Premoto cortex and the recognition of moto actions. Cogn. BrainRes. 3, 131-141
77. Rizzolatti, G., Fogassi, L., and Gallese V. (1997). Parietal cortex: from sigh to action. Curr. Opin. Neurobiol. 7 562-567.
78. Rizzolatti, G., Fogassi, L., and Gallese V. (2001). Neurophysiologica mechanisms underlying the under standing and imitation of action. Nat Rev. Neurosci. 2, 661-670.
79. Rizzolatti, G., Fogassi, L., and Gallese V. (2002). Motor and cognitiv functions of the ventral premoto cortex. Curr. Opin. Neurobiol. 12 149-154.
80. Rizzolatti, G., and Luppino, G. (2001) The cortical motor system. Neuron 31, 889-901.
81. Rizzolatti, G., and Matelli, M. (2003) Two different streams form the dorsal visual system: anatomy and functions. Exp. BrainRes. 153, 146-157.
82. Roebroeck, A., Fromisano, E., Goebel, R. (2005). Mappin directed influence over the brai using Granger causality and fMRI Neuroimage 25, 230-242.
83. Saxe, R., Xiao, D. K., Kovacs, G., Perrett, D. I., and Kanwisher, N (2004). A region of right pos terior superior temporal sulcu responds to observed intentiona actions. Neuropsychologia 42
84. Saygin, A. P. (2007). Superior tempora and premotor brain areas necessar for biological motion perception Brain 130, 2452-2461.
85. Schippers, M. B., and Keysers, C (2011). Mapping the flow of infor mation within the putative mir ror neuron system during ges ture observation. Neuroimage 57 37-44.
86. Schubotz, R. I., and von Cramon, D. Y (2004). Sequences of abstract non biological stimuli share ventral pre motor cortex with action observation and imagery. J. Neurosci. 24 5467-5474.
87. Seltzer, B., and Pandya, D. N. (1994) Parietal, temporal, and occipita projections to cortex of the superior temporal sulcus in the rhesu monkey: a retrograde tracer study J. Comp. Neurol. 343, 445-463.
88. Shmuelof, L., and Zohary, E. (2005) Dissociation between ventral and dorsal fMRI activation during object and action recognition Neuron 47, 457-470.
89. Shmuelof, L., and Zohary, E. (2006) A mirror representation of other' actions in the human anterio parietal cortex. J. Neurosci. 26 9736-9742.
90. Sirigu, A., Duhamel, J. R., Cohen, L., Pillon, B., Dubois, B., and Agid Y. (1996). The mental representation of hand movements after parietal cortex damage. Science 273 1564-1568.
91. Stephan, K. E., Harrison, L. M., Kiebel S. J., David, O., Penny, W. D. and Friston, K. J. (2007). Dynami causal models of neural system dynamics: current state and futur extensions. J. Biosci. 32, 129-144.
92. Stephan, K. E., Penny, W. D., Daunizeau, J., Moran, R. J. and Friston, K. J. (2009). Bayesian model selection for group studies Neuroimage 46, 1004-1017.
93. Stephan, K. E., Penny, W. D., Moran R. J., Den Ouden, H. E., Daunizeau J., and Friston, K. J. (2010) Ten simple rules for dynami causal modeling. Neuroimage 49 3099-3109.
94. Strafella, A. P., and Paus, T. (2000) Modulation of cortical excitabilit during action observation: a tran scranial magnetic stimulation study Neuro report 11, 2289-2292.
95. Tanabe, H. C., Sakai, T., Morito Y., Kochiyama, T., and Sadato, N (2011). Neural correlates and effec tive connectivity of participantiv colors during the Behnam's top illu sion: a functional MRI study. Cereb Cortex 21, 123-133.
96. Thompson, J. C., Clarke, M., Stewart, T., and Puce, A. (2005). Configural processing of biological motion in human superior temporal sulcus. J. Neurosci. 25, 9059-9066.
97. van Kemenade, B. M., Muggleton, N., Walsh, V., and Saygin, A. P. (2012). Effects of TMS over premotor and superior temporal cortices on biological motion perception. J. Cogn. Neurosci. 24, 896-904.
98. Vogt, S., Buccino, G., Wohlschläger, A. M., Canessa, N., Shah, N. J., Zilles, K., Eickhoff, S. B., Freund, H. J., Rizzolatti, G., and Fink, G. R. (2007). Prefrontal involvement in imitation learning of hand actions: effects of practice and expertise. Neuroimage 37, 1371-1383.
99. Vogt, S., Taylor, P., and Hopkins, B. (2003). Visuomotor priming by pictures of hand postures: perspective matters. Neuropsychologia 41, 941-951.
100. Wheaton, L. A., and Hallett, M. (2007). Ideomotor apraxia: a review. J. Neurol. Sci. 260, 1-10.
101. Wise, S. P., Boussaoud, D., Johnson, P. B., and Caminiti, R. (1997). Premotor and parietal cortex: cor-ticocortical connectivity and combinatorial computations. Annu. Rev. Neurosci. 20, 25-42.
102. Wolpert, D. M., Doya, K., and Kawato, M. (2003). A unifying computational framework for motor control and social interaction. Philos. Trans. R. Soc. Lond. B Biol. Sci. 358, 593-602.