Experimental Brain Research

, Volume 206, Issue 2, pp 141–151 | Cite as

Representing actions through their sound

  • Salvatore M. Aglioti
  • Mariella Pazzaglia


Since the discovery of ‘mirror neurons’ in the monkey premotor and parietal cortex, an increasing body of evidence in animals and humans alike has supported the notion of the inextricable link between action execution and action perception. Although research originally focused on the relationship between performed and viewed actions, more recent studies highlight the importance of representing the actions of others through audition. In the first part of this article, we discuss animal studies, which provide direct evidence that action is inherently linked to multi-sensory cues, as well as the studies carried out on healthy subjects by using state-of-the-art cognitive neuroscience techniques such as functional magnetic resonance imaging (fMRI), event-related potentials (ERP), magnetoencephalography (MEG), and transcranial magnetic stimulation (TMS). In the second section, we review the lesion analysis studies in brain-damaged patients demonstrating the link between ‘resonant’ fronto-parieto-temporal networks and the ability to represent an action by hearing its sound. Moreover, we examine the evidence in favour of somatotopy as a possible representational rule underlying the auditory mapping of actions and consider the links between language and audio-motor action mapping. We conclude with a discussion of some outstanding questions for future research on the link between actions and the sounds they produce.


Fronto-parietal Mirror circuits Sound action fMRI TMS Language 


  1. Aglioti SM, Cesari P, Romani M, Urgesi C (2008) Action anticipation and motor resonance in elite basketball players. Nat Neurosci 11:1109–1116CrossRefPubMedGoogle Scholar
  2. Alaerts K, Swinnen SP, Wenderoth N (2009) Interaction of sound and sight during action perception: evidence for shared modality-dependent action representations. Neuropsychologia 47:2593–2599CrossRefPubMedGoogle Scholar
  3. Amedi A, von Kriegstein K, van Atteveldt NM, Beauchamp MS, Naumer MJ (2005) Functional imaging of human crossmodal identification and object recognition. Exp Brain Res 166:559–571CrossRefPubMedGoogle Scholar
  4. Arbib MA (2005) From monkey-like action recognition to human language: an evolutionary framework for neurolinguistics. Behav Brain Sci 28:105–124PubMedGoogle Scholar
  5. Avenanti A, Bolognini N, Maravita A, Aglioti SM (2007) Somatic and motor components of action simulation. Curr Biol 17:2129–2135CrossRefPubMedGoogle Scholar
  6. Aziz-Zadeh L, Iacoboni M, Zaidel E, Wilson S, Mazziotta J (2004) Left hemisphere motor facilitation in response to manual action sounds. Eur J Neurosci 19:2609–2612CrossRefPubMedGoogle Scholar
  7. Aziz-Zadeh L, Wilson SM, Rizzolatti G, Iacoboni M (2006) Congruent embodied representations for visually presented actions and linguistic phrases describing actions. Curr Biol 16:1818–1823CrossRefPubMedGoogle Scholar
  8. Barsalou LW (2008) Grounded cognition. Annu Rev Psychol 59:617–645CrossRefPubMedGoogle Scholar
  9. Belin P (2006) Voice processing in human and non-human primates. Philos Trans R Soc Lond B Biol Sci 361:2091–2107CrossRefPubMedGoogle Scholar
  10. Bidet-Caulet A, Voisin J, Bertrand O, Fonlupt P (2005) Listening to a walking human activates the temporal biological motion area. Neuroimage 28:132–139CrossRefPubMedGoogle Scholar
  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 13:400–404PubMedGoogle Scholar
  12. Buccino G, Vogt S, Ritzl A, Fink GR, Zilles K, Freund HJ, Rizzolatti G (2004) Neural circuits underlying imitation learning of hand actions: an event-related fMRI study. Neuron 42:323–334CrossRefPubMedGoogle Scholar
  13. Caetano G, Jousmäki V, Hari R (2007) Actor’s and observer’s primary motor cortices stabilize similarly after seen or heard motor actions. Proc Natl Acad Sci USA 104:9058–9062CrossRefPubMedGoogle Scholar
  14. Calvo-Merino B, Grèzes J, Glaser DE, Passingham RE, Haggard P (2006) Seeing or doing? Influence of visual and motor familiarity in action observation. Curr Biol 16:1905–1910CrossRefPubMedGoogle Scholar
  15. Campanella S, Belin P (2007) Integrating face and voice in person perception. Trends Cogn Sci 11:535–543CrossRefPubMedGoogle Scholar
  16. Candidi M, Vicario CM, Abreu AM, Aglioti SM (2010) Competing mechanisms for mapping action-related categorical knowledge and observed actions. Cereb Cortex [Epub ahead of print]Google Scholar
  17. Casile A, Giese MA (2006) Nonvisual motor training influences biological motion perception. Curr Biol 16:69–74CrossRefPubMedGoogle Scholar
  18. Celnik P, Webster B, Glasser DM, Cohen LG (2008) Effects of action observation on physical training after stroke. Stroke 39:1814–1820. Epub 2008 Apr 10Google Scholar
  19. Chen YC, Spence C (2009) When hearing the bark helps to identify the dog: semantically-congruent sounds modulate the identification of masked pictures. CognitionGoogle Scholar
  20. Corballis MC (2002) From hand to mouth: the origins of language Princeton University Press, PrincetonGoogle Scholar
  21. Corballis MC (2009) The evolution of language. Ann NY Acad Sci 1156:19–43CrossRefPubMedGoogle Scholar
  22. Costantini M, Galati G, Ferretti A, Caulo M, Tartaro A, Romani GL, Aglioti SM (2005) Neural systems underlying observation of humanly impossible movements: an fMRI study. Cereb Cortex 15:1761–1767CrossRefPubMedGoogle Scholar
  23. D’Ausilio A, Pulvermüller F, Salmas P, Bufalari I, Begliomini C, Fadiga L (2009) The motor somatotopy of speech perception. Curr Biol 19:381–385 (Epub 2009 Feb 12)Google Scholar
  24. Dapretto M, Davies MS, Pfeifer JH, Scott AA, Sigman M, Bookheimer SY, Iacoboni M (2006) Understanding emotions in others: mirror neuron dysfunction in children with autism spectrum disorders. Nat Neurosci 9:28–30CrossRefPubMedGoogle Scholar
  25. De Lucia M, Camen C, Clarke S, Murray MM (2009) The role of actions in auditoryobject discrimination. Neuroimage 48:475–485 (Epub 2009 Jun 24)Google Scholar
  26. de Zubicaray G, Postle N, McMahon K, Meredith M, Ashton R (2010) Mirror neurons, the representation of word meaning, and the foot of the third left frontal convolution. Brain Lang 112:77–84 (Epub 2008 Nov 1)Google Scholar
  27. Decety J, Grèzes J, Costes N, Perani D, Jeannerod M, Procyk E, Grassi F, Fazio F (1997) Brain activity during observation of actions. Influence of action content and subject’s strategy. Brain 120:1763–1777CrossRefPubMedGoogle Scholar
  28. di Pellegrino G, Fadiga L, Fogassi L, Gallese V, Rizzolatti G (1992) Understanding motor events: a neurophysiological study. Exp Brain Res 91:176–180PubMedGoogle Scholar
  29. Dick F, Saygin AP, Galati G, Pitzalis S, Bentrovato S et al (2007) What is involved and what is necessary for complex linguistic and nonlinguistic auditory processing: evidence from functional magnetic resonance imaging and lesion data. J Cogn Neurosci 19:799–816CrossRefPubMedGoogle Scholar
  30. Driver J, Spence C (2000) Multisensory perception: beyond modularity and convergence. Curr Biol 10:R731–R735CrossRefPubMedGoogle Scholar
  31. Drost UC, Rieger M, Brass M, Gunter TC, Prinz W (2005) When hearing turns into playing: movement induction by auditory stimuli in pianists. Q J Exp Psychol A 58:1376–1389CrossRefPubMedGoogle Scholar
  32. Ekimov A, Sabatier JM (2006) Vibration and sound signatures of human footsteps in buildings. J Acoust Soc Am 120:762–768CrossRefPubMedGoogle Scholar
  33. Engel LR, Frum C, Puce A, Walker NA, Lewis JW (2009) Different categories of living and non-living sound-sources activate distinct cortical networks. Neuroimage 47:1778–1791 (Epub 2009 May 22)Google Scholar
  34. Fadiga L, Fogassi L, Pavesi G, Rizzolatti G (1995) Motor facilitation during action observation: a magnetic stimulation study. J Neurophysiol 73:2608–2611PubMedGoogle Scholar
  35. Fadiga L, Craighero L, Buccino G, Rizzolatti G (2002) Speech listening specifically modulates the excitability of tongue muscles: a TMS study. Eur J Neurosci 15:399–402CrossRefPubMedGoogle Scholar
  36. Fernandino L, Iacoboni M (2010) Are cortical motor maps based on body parts or coordinated actions? Implications for embodied semantics. Brain Lang 112:44–53 (Epub 2009 Apr 3)Google Scholar
  37. Fogassi L, Ferrari PF, Gesierich B, Rozzi S, Chersi F, Rizzolatti G et al (2005) Parietal lobe: from action organization to intention understanding. Science 308:662–667CrossRefPubMedGoogle Scholar
  38. Galati G, Committeri G, Spitoni G, Aprile T, Pitzalis S et al (2008) A selective representation of the meaning of actions in the auditory mirror system. Neuroimage 40:1274–1286CrossRefPubMedGoogle Scholar
  39. Gallese V (2007) Before and below ‘theory of mind’: embodied simulation and the neural correlates of social cognition. Philos Trans R Soc Lond B Biol Sci 362:659–669CrossRefPubMedGoogle Scholar
  40. Gallese V, Fadiga L, Fogassi L, Rizzolatti G (1996) Action recognition in the premotor cortex. Brain 119:593–609CrossRefPubMedGoogle Scholar
  41. Gallese V, Rochat M, Cossu G, Sinigaglia C (2009) Motor cognition and its role in the phylogeny and ontogeny of action understanding. Dev Psychol 45:103–113CrossRefPubMedGoogle Scholar
  42. Gangitano M, Mottaghy FM, Pascual-Leone A (2001) Phase-specific modulation of cortical motor output during movement observation. Neuroreport 12:1489–1492CrossRefPubMedGoogle Scholar
  43. 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 19:1239–1255CrossRefPubMedGoogle Scholar
  44. Gazzola V, Aziz-Zadeh L, Keysers C (2006) Empathy and the somatotopic auditory mirror system in humans. Curr Biol 16:1824–1829CrossRefPubMedGoogle Scholar
  45. Gentilucci M, Dalla Volta R (2008) Spoken language and arm gestures are controlled by the same motor control system. Q J Exp Psychol (Colchester) 61:944–957CrossRefGoogle Scholar
  46. Gori M, Del Viva M, Sandini G, Burr DC (2008) Young children do not integrate visual and haptic form information. Curr Biol 18:694–698CrossRefPubMedGoogle Scholar
  47. Hari R, Kujala MV (2009) Brain basis of human social interaction: from concepts to brain imaging. Physiol Rev 89:453–479CrossRefPubMedGoogle Scholar
  48. Haslinger B, Erhard P, Altenmüller E, Schroeder U, Boecker H, Ceballos-Baumann AO (2005) Transmodal sensorimotor networks during action observation in professional pianists. J Cogn Neurosci 17:282–293CrossRefPubMedGoogle Scholar
  49. Hauk O, Johnsrude I, Pulvermüller F (2004) Somatotopic representation of action words in human motor and premotor cortex. Neuron 41:301–307CrossRefPubMedGoogle Scholar
  50. Hauk O, Shtyrov Y, Pulvermuller F (2006) The sound of actions as reflected by mismatch negativity: rapid activation of cortical sensory-motor networks by sounds associated with finger and tongue movements. Eur J Neurosci 23:811–821CrossRefPubMedGoogle Scholar
  51. Hauk O, Shtyrov Y, Pulvermüller F (2008) The time course of action and action-word comprehension in the human brain as revealed by neurophysiology. J Physiol Paris 102:50–58 (Epub Apr 1)Google Scholar
  52. Kaplan JT, Iacoboni M (2007) Multimodal action representation in human left ventral premotor cortex. Cogn Process 8:103–113CrossRefPubMedGoogle Scholar
  53. Kemmerer D, Castillo JG, Talavage T, Patterson S, Wiley C (2008) Neuroanatomical distribution of five semantic components of verbs: evidence from fMRI. Brain Lang 107:16–43CrossRefPubMedGoogle Scholar
  54. Keysers C, Kohler E, Umilta MA, Nanetti L, Fogassi L et al (2003) Audiovisual mirror neurons and action recognition. Exp Brain Res 153:628–636CrossRefPubMedGoogle Scholar
  55. Knoblich G, Repp BH (2009) Inferring agency from sound. Cognition 111:248–262CrossRefPubMedGoogle Scholar
  56. Kohler E, Keysers C, Umiltà MA, Fogassi L, Gallese V et al (2002) Hearing sounds, understanding actions: action representation in mirror neurons. Science 297:846–848CrossRefPubMedGoogle Scholar
  57. Lahav A, Saltzman E, Schlaug G (2007) Action representation of sound: audiomotor recognition network while listening to newly acquired actions. J Neurosci 27:308–314CrossRefPubMedGoogle Scholar
  58. Le Bel RM, Pineda JA, Sharma A (2009) Motor-auditory-visual integration: the role of the human mirror neuron system in communication and communication disorders. J Commun Disord 42:299–304CrossRefPubMedGoogle Scholar
  59. Lepage JF, Théoret H (2006) EEG evidence for the presence of an action observation-execution matching system in children. Eur J Neurosci 23:2505–2510CrossRefPubMedGoogle Scholar
  60. Lepage JF, Théoret H (2007) The mirror neuron system: grasping others’ actions from birth. Dev Sci 10:513–523CrossRefPubMedGoogle Scholar
  61. Lepage JF, Tremblay S, Nguyen DK, Champoux F, Lassonde M, Théoret H (2010) Action related sounds induce early and late modulations of motor cortex activity. Neuroreport 21:250–253CrossRefPubMedGoogle Scholar
  62. Leroi-Gourhan Le Geste et la Parole I (1964) Technique et Langage, Parigi, Albin Michel (coll. Sciences d’aujourd’hui), p 323Google Scholar
  63. Leroi-Gourhan Le Geste et la Parole II (1965) La Mémoire et les rythmes, Parigi, Albin Michel (coll. Sciences d’aujourd’hui), p 285Google Scholar
  64. Leslie KR, Johnson-Frey S, Grafton ST (2004) Functional imaging of face and hand imitation: towards a motor theory of empathy. NeuroImage 21:601–607CrossRefPubMedGoogle Scholar
  65. Lewis JW, Brefczynski JA, Phinney RE, Janik JJ, DeYoe EA (2005) Distinct cortical pathways for processing tool versus animal sounds. J Neurosci 25:5148–5158CrossRefPubMedGoogle Scholar
  66. Lewis JW, Phinney RE, Brefczynski-Lewis JA, DeYoe EA (2006) Lefties get it “right” when hearing tool sounds. J Cogn Neurosci 18:1313–1314Google Scholar
  67. Liberman AM, Mattingly IG (1985) The motor theory of speech perception revised. Cognition 21:1–36CrossRefPubMedGoogle Scholar
  68. Meltzoff AN, Moore MK (1977) Imitation of facial and manual gestures by human neonates. Science 198:74–78CrossRefPubMedGoogle Scholar
  69. Möttönen R, Watkins KE (2009) Motor representations of articulators contribute to categorical perception of speech sounds. J Neurosci 29:9819–9825CrossRefPubMedGoogle Scholar
  70. Nelissen N, Pazzaglia M, Vandenbulcke M, Sunaert S, Fannes K, Dupont P, Aglioti SM, Vandenberghe R (2010) Gesture discrimination in primary progressive aphasia: the intersection between gesture and language processing pathways. J Neurosci (in press)Google Scholar
  71. Pazzaglia M, Pizzamiglio L, Pes E, Aglioti SM (2008a) The sound of actions in apraxia. Curr Biol 18:1766–1772 (Epub 2008 Nov 13)Google Scholar
  72. Pazzaglia M, Smania N, Corato E, Aglioti SM (2008b) Neural underpinnings of gesture discrimination in patients with limb apraxia. J Neurosci 28:3030–3041CrossRefPubMedGoogle Scholar
  73. Penfield W, Rasmussen T (1950) The cerebral cortex of man. MacMillan, New YorkGoogle Scholar
  74. Pietrini P, Furey ML, Ricciardi E, Gobbini MI, Wu WH, Cohen L, Guazzelli M, Haxby JV (2004) Beyond sensory images: object-based representation in the human ventral pathway. Proc Natl Acad Sci USA 101:5658–5663CrossRefPubMedGoogle Scholar
  75. Pizzamiglio L, Aprile T, Spitoni G, Pitzalis S, Bates E, D’Amico S, Di Russo F (2005) Separate neural systems for processing action- or non-action-related sounds. Neuroimage 24:852–861CrossRefPubMedGoogle Scholar
  76. Postle N, McMahon K, Ashton R, Meredith M, de Zubicaray G (2008) Action word meaning representations in cytoarchitectonically defined primary and premotor cortices. NeuroImage 43:634–644CrossRefPubMedGoogle Scholar
  77. Prather JF, Peters S, Nowicki S, Mooney R (2008) Precise auditory-vocal mirroring in neurons for learned vocal communication. Nature 451:305–310CrossRefPubMedGoogle Scholar
  78. Pulvermüller F (2001) Brain reflections of words and their meaning. Trends Cogn Sci 5:517–524CrossRefPubMedGoogle Scholar
  79. Pulvermüller F (2005) Brain mechanisms linking language and action. Nat Rev Neurosci 6:576–682CrossRefPubMedGoogle Scholar
  80. Ricciardi E, Bonino D, Sani L, Vecchi T, Guazzelli M, Haxby JV, Fadiga L, Pietrini P (2009) Do we really need vision? How blind people “see” the actions of others. J Neurosci 29:9719–9724CrossRefPubMedGoogle Scholar
  81. Rizzolatti G, Arbib MA (1998) Language within our grasp. Trends Neurosci 21:188–194CrossRefPubMedGoogle Scholar
  82. Rizzolatti G, Craighero L (2004) The mirror-neuron system. Annu Rev Neurosci 27:169–192CrossRefPubMedGoogle Scholar
  83. Rizzolatti G, Sinigaglia C (2008) Further reflections on how we interpret the actions of others. Nature 455:589CrossRefPubMedGoogle Scholar
  84. Rizzolatti G, Fadiga L, Matelli M, Bettinardi V, Paulesu E, Perani D, Fazio F (1996) Localization of grasp representations in humans by PET: 1. Observation versus execution. Exp Brain Res 111:246–252CrossRefPubMedGoogle Scholar
  85. Romani M, Cesari P, Urgesi C, Facchini S, Aglioti SM (2005) Motor facilitation of the human cortico-spinal system during observation of bio-mechanically impossible movements. Neuroimage 26:755–763CrossRefPubMedGoogle Scholar
  86. Rossi S, De Capua A, Pasqualetti P, Ulivelli M, Fadiga L, Falzarano V, Bartalini S, Passero S, Nuti D, Rossini PM (2008) Distinct olfactory cross-modal effects on the human motor system. PLoS One 27(3):e1702Google Scholar
  87. Saarela MV, Hari R (2008) Listening to humans walking together activates the social brain circuitry. Soc Neurosci 3:401–409CrossRefPubMedGoogle Scholar
  88. Sauter DA, Eimer M (2010) Rapid detection of emotion from human vocalizations. J Cogn Neurosci 22:474–481CrossRefPubMedGoogle Scholar
  89. Saygin AP, Dick F, Wilson SM, Dronkers NF, Bates E (2003) Neural resources for processing language and environmental sounds: evidence from aphasia. Brain 126:928–945CrossRefPubMedGoogle Scholar
  90. Schubotz RI, von Cramon DY, Lohmann G (2003) Auditory what, where, and when: a sensory somatotopy in lateral premotor cortex. Neuroimage 20:173–185CrossRefPubMedGoogle Scholar
  91. Shams L, Kamitani Y, Shimojo S (2000) Illusions. What you see is what you hear. Nature 408:788Google Scholar
  92. Smania N, Aglioti SM, Girardi F, Tinazzi M, Fiaschi A, Cosentino A, Corato E (2006) Rehabilitation of limb apraxia improves daily life activities in patients with stroke. Neurology 67:2050–2052CrossRefPubMedGoogle Scholar
  93. Stefan K, Cohen LG, Duque J, Mazzocchio R, Celnik P, Sawaki L, Ungerleider L, Classen J (2005) Formation of a motor memory by action observation. J Neurosci 25:9339–9346CrossRefPubMedGoogle Scholar
  94. Strafella AP, Paus T (2000) Modulation of cortical excitability during action observation: a transcranial magnetic stimulation study. Neuroreport 11:2289–2292CrossRefPubMedGoogle Scholar
  95. Takada M, Tokuno H, Nambu A, Inase M (1998) Corticostriatal projections from the somatic motor areas of the frontal cortex in the macaque monkey: segregation versus overlap of input zones from the primary motor cortex, the supplementary motor area, and the premotor cortex. Exp Brain Res 120:114–128CrossRefPubMedGoogle Scholar
  96. Talairach J, Tournoux P (1988) Co-planar stereotaxic atlas of the human brain. Thieme, New YorkGoogle Scholar
  97. 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 17:273–281CrossRefPubMedGoogle Scholar
  98. Theoret H, Pascual-Leone A (2002) Language acquisition: do as you hear. Curr Biol 12:R736–R737CrossRefPubMedGoogle Scholar
  99. Tokuno H, Takada M, Nambu A, Inase M (1997) Reevaluation of ipsilateral corticocortical inputs to the orofacial region of the primary motor cortex in the macaque monkey. J Comp Neurol 389:34–48CrossRefPubMedGoogle Scholar
  100. Urgesi C, Candidi M, Fabbro F, Romani M, Aglioti SM (2006) Motor facilitation during action observation: topographic mapping of the target muscle and influence of the onlooker’s posture. Eur J Neurosci 23:2522–2530CrossRefPubMedGoogle Scholar
  101. 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 [Epub ahead of print]Google Scholar
  102. Van den Stock J, Grèzes J, de Gelder B (2008) Human and animal sounds influence recognition of body language. Brain Res 1242:185–190CrossRefPubMedGoogle Scholar
  103. Vogt S, Buccino G, Wohlschläger AM, Canessa N, Shah NJ, Zilles K, Eickhoff SB, Freund HJ, Rizzolatti G, Fink GR (2007) Prefrontal involvement in imitation learning of hand actions: effects of practice and expertise. Neuroimage 37:1371–1383CrossRefPubMedGoogle Scholar
  104. Warren JE, Sauter DA, Eisner F, Wiland J, Dresner MA et al (2006) Positive emotions preferentially engage an auditory-motor “mirror” system. J Neurosci 26:13067–13075CrossRefPubMedGoogle Scholar
  105. Watkins KE, Strafella AP, Paus T (2003) Seeing and hearing speech excites the motor system involved in speech production. Neuropsychologia 41:989–994CrossRefPubMedGoogle Scholar
  106. Wheaton KJ, Thompson JC, Syngeniotis A, Abbott DF, Puce A (2004) Viewing the motion of human body parts activates different regions of premotor, temporal, and parietal cortex. NeuroImage 22:277–288CrossRefPubMedGoogle Scholar

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© Springer-Verlag 2010

Authors and Affiliations

  1. 1.Dipartimento di PsicologiaUniversità di Roma ‘La Sapienza’RomeItaly
  2. 2.IRCCS Fondazione Santa LuciaRomeItaly

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