1932

Abstract

According to embodied cognition theories, higher cognitive abilities depend on the reenactment of sensory and motor representations. In the first part of this review, we critically analyze the central claims of embodied theories and argue that the existing behavioral and neuroimaging data do not allow investigators to discriminate between embodied cognition and classical cognitive accounts, which assume that conceptual representations are amodal and symbolic. In the second part, we review the main claims and the core electrophysiological findings typically cited in support of the mirror neuron theory of action understanding, one of the most influential examples of embodied cognition theories. In the final part, we analyze the claim that mirror neurons subserve action understanding by mapping visual representations of observed actions on motor representations, trying to clarify in what sense the representations carried by these neurons can be claimed motor.

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2014-07-08
2024-06-17
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Literature Cited

  1. Aziz-Zadeh L, Wilson SM, Rizzolatti G, Iacoboni M. 2006. Congruent embodied representations for visually presented actions and linguistic phrases describing actions. Curr. Biol. 16:1818–23 [Google Scholar]
  2. Barsalou LW. 2008. Grounded cognition. Annu. Rev. Psychol. 59:617–45 [Google Scholar]
  3. Bedny M, Caramazza A. 2011. Perception, action, and word meanings in the human brain: the case from action verbs. Ann. N. Y. Acad. Sci. 1224:81–95 [Google Scholar]
  4. Borghi AM, Glenberg AM, Kaschak MP. 2004. Putting words in perspective. Mem. Cogn. 32:863–73 [Google Scholar]
  5. Bosbach S, Prinz W, Kerzel D. 2005. Is direction position? Position- and direction-based correspondence effects in tasks with moving stimuli. Q. J. Exp. Psychol. A 58:467–506 [Google Scholar]
  6. Boulenger V, Hauk O, Pulvermüller F. 2009. Grasping ideas with the motor system: semantic somatotopy in idiom comprehension. Cereb. Cortex 19:1905–14 [Google Scholar]
  7. Bouvier SE, Engel SA. 2006. Behavioral deficits and cortical damage loci in cerebral achromatopsia. Cereb. Cortex 16:183–91 [Google Scholar]
  8. Buccino G, Riggio L, Melli G, Binkofski F, Gallese V, Rizzolatti G. 2005. Listening to action-related sentences modulates the activity of the motor system: a combined TMS and behavioral study. Brain Res. Cogn. Brain Res. 24:355–63 [Google Scholar]
  9. Buccino G, Vogt S, Ritzl A, Fink GR, Zilles K. et al. 2004. Neural circuits underlying imitation learning of hand actions: an event-related fMRI study. Neuron 42:323–34 [Google Scholar]
  10. Caggiano V, Fogassi L, Rizzolatti G, Casile A, Giese MA, Thier P. 2012. Mirror neurons encode the subjective value of an observed action. Proc. Natl. Acad. Sci. USA 109:11848–53 [Google Scholar]
  11. Caggiano V, Fogassi L, Rizzolatti G, Pomper JK, Thier P. et al. 2011. View-based encoding of actions in mirror neurons of area F5 in macaque premotor cortex. Curr. Biol. 21:144–48 [Google Scholar]
  12. Caramazza A, Hillis AE, Rapp BC, Romani C. 1990. The Multiple Semantics Hypothesis: multiple confusions?. Cogn. Neuropsychol. 7:161–89 [Google Scholar]
  13. Caspers S, Zilles K, Laird AR, Eickhoff SB. 2010. ALE meta-analysis of action observation and imitation in the human brain. NeuroImage 50:1148–67 [Google Scholar]
  14. Cattaneo L, Caruana F, Jezzini A, Rizzolatti G. 2009. Representation of goal and movements without overt motor behavior in the human motor cortex: a transcranial magnetic stimulation study. J. Neurosci. 29:11134–38 [Google Scholar]
  15. 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 20:2252–58 [Google Scholar]
  16. Chatterjee A. 2010. Disembodying cognition. Lang. Cogn. 2:79–116 [Google Scholar]
  17. Chong TT, Cunnington R, Williams MA, Kanwisher N, Mattingley JB. 2008. fMRI adaptation reveals mirror neurons in human inferior parietal cortex. Curr. Biol. 18:1576–80 [Google Scholar]
  18. Cook R, Bird G, Catmur C, Press C, Heyes C. 2014. Mirror neurons: from origin to function. Behav. Brain Sci. In press [Google Scholar]
  19. Csibra G. 2008. Action mirroring and action understanding: an alternative account. Sensorimotor Foundations of Higher Cognition: Attention and Performance XXII P Haggard, Y Rossetti, M Kawato 435–59 New York: Oxford Univ. Press [Google Scholar]
  20. D'Ausilio A, Pulvermüller F, Salmas P, Bufalari I, Begliomini C, Fadiga L. 2009. The motor somatotopy of speech perception. Curr. Biol. 19:381–85 [Google Scholar]
  21. de Zubicaray G, Arciuli J, McMahon K. 2013. Putting an “end” to the motor cortex representations of action words. J. Cogn. Neurosci. 25:1957–74 [Google Scholar]
  22. di Pellegrino G, Fadiga L, Fogassi L, Gallese V, Rizzolatti G. 1992. Understanding motor events: a neurophysiological study. Exp. Brain Res. 91:176–80 [Google Scholar]
  23. Dinstein I, Hasson U, Rubin N, Heeger DJ. 2007. Brain areas selective for both observed and executed movements. J. Neurophysiol. 98:1415–27 [Google Scholar]
  24. Dinstein I, Thomas C, Behrmann M, Heeger DJ. 2008. A mirror up to nature. Curr. Biol. 18:R13–18 [Google Scholar]
  25. Fadiga L, Fogassi L, Pavesi G, Rizzolatti G. 1995. Motor facilitation during action observation: a magnetic stimulation study. J. Neurophysiol. 73:2608–11 [Google Scholar]
  26. Ferrari PF, Rozzi S, Fogassi L. 2005. Mirror neurons responding to observation of actions made with tools in monkey ventral premotor cortex. J. Cogn. Neurosci. 17:212–26 [Google Scholar]
  27. Fischer MH, Zwaan RA. 2008. Embodied language: a review of the role of the motor system in language comprehension. Q. J. Exp. Psychol. 61:825–50 [Google Scholar]
  28. Fogassi L, Ferrari PF, Gesierich B, Rozzi S, Chersi F, Rizzolatti G. 2005. Parietal lobe: from action organization to intention understanding. Science 308:662–67 [Google Scholar]
  29. Freedman DJ, Assad JA. 2011. A proposed common neural mechanism for categorization and perceptual decisions. Nat. Neurosci. 14:143–46 [Google Scholar]
  30. Gallese V, Fadiga L, Fogassi L, Rizzolatti G. 1996. Action recognition in the premotor cortex. Brain 119:Pt. 2593–609 [Google Scholar]
  31. Gallese V, Fadiga L, Fogassi L, Rizzolatti G. 2002. Action representation and the inferior parietal lobule. Common Mechanisms in Perception and Action: Attention and Performance W Prinz, B Hommel 334–55 Oxford, UK: Oxford Univ. Press [Google Scholar]
  32. Gallese V, Lakoff G. 2005. The Brain's concepts: the role of the sensory-motor system in conceptual knowledge. Cogn. Neuropsychol. 22:455–79 [Google Scholar]
  33. Gentilucci M, Gangitano M. 1998. Influence of automatic word reading on motor control. Eur. J. Neurosci. 10:752–56 [Google Scholar]
  34. Gerfo EL, Oliveri M, Torriero S, Salerno S, Koch G, Caltagirone C. 2008. The influence of rTMS over prefrontal and motor areas in a morphological task: grammatical vs. semantic effects. Neuropsychologia 46:764–70 [Google Scholar]
  35. Glenberg AM, Kaschak MP. 2002. Grounding language in action. Psychon. Bull. Rev. 9:558–65 [Google Scholar]
  36. Goldberg RF, Perfetti CA, Schneider W. 2006. Perceptual knowledge retrieval activates sensory brain regions. J. Neurosci. 26:4917–21 [Google Scholar]
  37. Grèzes J, Armony JL, Rowe J, Passingham RE. 2003. Activations related to “mirror” and “canonical” neurones in the human brain: an fMRI study. NeuroImage 18:928–37 [Google Scholar]
  38. Hansen T, Olkkonen M, Walter S, Gegenfurtner KR. 2006. Memory modulates color appearance. Nat. Neurosci. 9:1367–68 [Google Scholar]
  39. Hauk O, Johnsrude I, Pulvermüller F. 2004. Somatotopic representation of action words in human motor and premotor cortex. Neuron 41:301–7 [Google Scholar]
  40. Hauk O, Pulvermüller F. 2004. Neurophysiological distinction of action words in the fronto-central cortex. Hum. Brain Mapp. 21:191–201 [Google Scholar]
  41. Hickok G. 2009. Eight problems for the mirror neuron theory of action understanding in monkeys and humans. J. Cogn. Neurosci. 21:1229–43 [Google Scholar]
  42. Iacoboni M, Woods RP, Brass M, Bekkering H, Mazziotta JC, Rizzolatti G. 1999. Cortical mechanisms of human imitation. Science 286:2526–28 [Google Scholar]
  43. Jacob P, Jeannerod M. 2005. The motor theory of social cognition: a critique. Trends Cogn. Sci. 9:21–25 [Google Scholar]
  44. Jeannerod M. 2001. Neural simulation of action: a unifying mechanism for motor cognition. NeuroImage 14:S103–9 [Google Scholar]
  45. Kemmerer D, Castillo JG, Talavage T, Patterson S, Wiley C. 2008. Neuroanatomical distribution of five semantic components of verbs: evidence from fMRI. Brain Lang. 107:16–43 [Google Scholar]
  46. Kemmerer D, Gonzalez-Castillo J. 2010. The Two-Level Theory of verb meaning: an approach to integrating the semantics of action with the mirror neuron system. Brain Lang. 112:54–76 [Google Scholar]
  47. Kiefer M, Pulvermüller F. 2012. Conceptual representations in mind and brain: theoretical developments, current evidence and future directions. Cortex 48:805–25 [Google Scholar]
  48. Kilner JM, Neal A, Weiskopf N, Friston KJ, Frith CD. 2009. Evidence of mirror neurons in human inferior frontal gyrus. J. Neurosci. 29:10153–59 [Google Scholar]
  49. Kohler E, Keysers C, Umiltà MA, Fogassi L, Gallese V, Rizzolatti G. 2002. Hearing sounds, understanding actions: action representation in mirror neurons. Science 297:846–48 [Google Scholar]
  50. 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 64:922–30 [Google Scholar]
  51. Kreiman G, Koch C, Fried I. 2000. Category-specific visual responses of single neurons in the human medial temporal lobe. Nat. Neurosci. 3:946–53 [Google Scholar]
  52. Kurata K, Tanji J. 1986. Premotor cortex neurons in macaques: activity before distal and proximal forelimb movements. J. Neurosci. 6:403–11 [Google Scholar]
  53. Lorey B, Naumann T, Pilgramm S, Petermann C, Bischoff M. et al. 2013. How equivalent are the action execution, imagery, and observation of intransitive movements? Revisiting the concept of somatotopy during action simulation. Brain Cogn. 81:139–50 [Google Scholar]
  54. Maeda F, Kleiner-Fisman G, Pascual-Leone A. 2002. Motor facilitation while observing hand actions: specificity of the effect and role of observer's orientation. J. Neurophysiol. 87:1329–35 [Google Scholar]
  55. Mahon BZ, Caramazza A. 2008. A critical look at the embodied cognition hypothesis and a new proposal for grounding conceptual content. J. Physiol. Paris 102:59–70 [Google Scholar]
  56. Meteyard L, Zokaei N, Bahrami B, Vigliocco G. 2008. Visual motion interferes with lexical decision on motion words. Curr. Biol. 18:R732–33 [Google Scholar]
  57. Miceli G, Fouch E, Capasso R, Shelton JR, Tomaiuolo F, Caramazza A. 2001. The dissociation of color from form and function knowledge. Nat. Neurosci. 4:662–67 [Google Scholar]
  58. Möttönen R, Watkins KE. 2009. Motor representations of articulators contribute to categorical perception of speech sounds. J. Neurosci. 29:9819–25 [Google Scholar]
  59. Mukamel R, Ekstrom AD, Kaplan J, Iacoboni M, Fried I. 2010. Single-neuron responses in humans during execution and observation of actions. Curr. Biol. 20:750–56 [Google Scholar]
  60. Myung JY, Blumstein SE, Sedivy JC. 2006. Playing on the typewriter, typing on the piano: manipulation knowledge of objects. Cognition 98:223–43 [Google Scholar]
  61. Oosterhof NN, Tipper SP, Downing PE. 2012. Viewpoint (in)dependence of action representations: an MVPA study. J. Cogn. Neurosci. 24:975–89 [Google Scholar]
  62. Oosterhof NN, Tipper SP, Downing PE. 2013. Crossmodal and action-specific: neuroimaging the human mirror neuron system. Trends Cogn. Sci. 17:311–18 [Google Scholar]
  63. 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. 104:1077–89 [Google Scholar]
  64. Papeo L, Lingnau A, Agosta S, Pascual-Leone A, Battelli L, Caramazza A. 2014. The origin of word-related motor activity. Cereb. Cortex. In press. doi: 10.1093/cercor/bht423 [Google Scholar]
  65. Papeo L, Pascual-Leone A, Caramazza A. 2013. Disrupting the brain to validate hypotheses on the neurobiology of language. Front. Hum. Neurosci. 7:148 [Google Scholar]
  66. Papeo L, Vallesi A, Isaja A, Rumiati RI. 2009. Effects of TMS on different stages of motor and non-motor verb processing in the primary motor cortex. PLoS ONE 4:e4508 [Google Scholar]
  67. Peelen M, Romagno D, Caramazza A. 2012. Independent representations of verbs and actions in left temporal cortex. J. Cogn. Neurosci. 24:2096–107 [Google Scholar]
  68. Postle N, Ashton R, McFarland K, de Zubicaray GI. 2013. No specific role for the manual motor system in processing the meanings of words related to the hand. Front. Hum. Neurosci. 7:11 [Google Scholar]
  69. Postle N, McMahon KL, Ashton R, Meredith M, de Zubicaray GI. 2008. Action word meaning representations in cytoarchitectonically defined primary and premotor cortices. NeuroImage 43:634–44 [Google Scholar]
  70. Press C, Weiskopf N, Kilner JM. 2012. Dissociable roles of human inferior frontal gyrus during action execution and observation. NeuroImage 60:1671–77 [Google Scholar]
  71. Pulvermüller F. 2005. Brain mechanisms linking language and action. Nat. Rev. Neurosci. 6:576–82 [Google Scholar]
  72. Pulvermüller F, Härle M, Hummel F. 2000. Neurophysiological distinction of verb categories. NeuroReport 11:2789–93 [Google Scholar]
  73. Pulvermüller F, Huss M, Kherif F, Moscoso del Prado Martin F, Hauk O, Shtyrov Y. 2006. Motor cortex maps articulatory features of speech sounds. Proc. Natl. Acad. Sci. USA 103:7865–70 [Google Scholar]
  74. Pulvermüller F, Shtyrov Y, Ilmoniemi R. 2005. Brain signatures of meaning access in action word recognition. J. Cogn. Neurosci. 17:884–92 [Google Scholar]
  75. Quiroga RQ, Reddy L, Kreiman G, Koch C, Fried I. 2005. Invariant visual representation by single neurons in the human brain. Nature 435:1102–7 [Google Scholar]
  76. Rizzolatti G, Fadiga L, Gallese V, Fogassi L. 1996. Premotor cortex and the recognition of motor actions. Brain Res. Cogn. Brain Res. 3:131–41 [Google Scholar]
  77. Rizzolatti G, Fogassi L, Gallese V. 2001. Neurophysiological mechanisms underlying the understanding and imitation of action. Nat. Rev. Neurosci. 2:661–70 [Google Scholar]
  78. Rizzolatti G, Scandolara C, Matelli M, Gentilucci M. 1981. Afferent properties of periarcuate neurons in macaque monkeys. I. Somatosensory responses. Behav. Brain Res. 2:125–46 [Google Scholar]
  79. Rizzolatti G, Sinigaglia C. 2010. The functional role of the parieto-frontal mirror circuit: interpretations and misinterpretations. Nat. Rev. Neurosci. 11:264–74 [Google Scholar]
  80. Rueschemeyer SA, Lindemann O, van Rooij D, van Dam W, Bekkering H. 2010. Effects of intentional motor actions on embodied language processing. Exp. Psychol. 57:260–66 [Google Scholar]
  81. Simmons WK, Martin A, Barsalou LW. 2005. Pictures of appetizing foods activate gustatory cortices for taste and reward. Cereb. Cortex 15:1602–8 [Google Scholar]
  82. Simmons WK, Ramjee V, Beauchamp MS, McRae K, Martin A, Barsalou LW. 2007. A common neural substrate for perceiving and knowing about color. Neuropsychologia 45:2802–10 [Google Scholar]
  83. Solomon KO, Barsalou LW. 2004. Perceptual simulation in property verification. Mem. Cogn. 32:244–59 [Google Scholar]
  84. Stanfield RA, Zwaan RA. 2001. The effect of implied orientation derived from verbal context on picture recognition. Psychol. Sci. 12:153–56 [Google Scholar]
  85. Tettamanti M, Buccino G, Saccuman MC, Gallese V, Danna M. et al. 2005. Listening to action-related sentences activates fronto-parietal motor circuits. J. Cogn. Neurosci. 17:273–81 [Google Scholar]
  86. Umiltà MA, Escola L, Intskirveli I, Grammont F, Rochat M. et al. 2008. When pliers become fingers in the monkey motor system. Proc. Natl. Acad. Sci. USA 105:2209–13 [Google Scholar]
  87. Umiltà MA, Kohler E, Gallese V, Fogassi L, Fadiga L. et al. 2001. I know what you are doing: a neurophysiological study. Neuron 31:155–65 [Google Scholar]
  88. 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 20:2511–21 [Google Scholar]
  89. Watson CE, Cardillo ER, Ianni GR, Chatterjee A. 2013. Action concepts in the brain: an activation likelihood estimation meta-analysis. J. Cogn. Neurosci. 25:1191–205 [Google Scholar]
  90. Willems RM, Labruna L, D'Esposito M, Ivry R, Casasanto D. 2011. A functional role for the motor system in language understanding: evidence from theta-burst transcranial magnetic stimulation. Psychol. Sci. 22:849–54 [Google Scholar]
  91. Zwaan RA, Stanfield RA, Yaxley RH. 2002. Language comprehenders mentally represent the shapes of objects. Psychol. Sci. 13:168–71 [Google Scholar]
  92. Zwaan RA, Taylor LJ. 2006. Seeing, acting, understanding: motor resonance in language comprehension. J. Exp. Psychol. Gen. 135:1–11 [Google Scholar]
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