Brain Structure and Function

, Volume 216, Issue 2, pp 151–157 | Cite as

Different brain structures related to self- and external-agency attribution: a brief review and meta-analysis

  • Marco Sperduti
  • Pauline Delaveau
  • Philippe Fossati
  • Jaqueline Nadel
Original Article


Several neuroimaging studies have consistently shown activations of areas surrounding the temporo-parietal junction (TPJ) during tasks exploring the sense of agency. Beyond TPJ, activations in different structures, such as the dorsolateral prefrontal cortex (dLPFC), the pre-supplementary motor area (pre-SMA), the insula and the precuneus have been reported. Moreover, a possible dissociation between self- and external-agency attribution has been suggested. To test the hypothesis of distinct neural correlates for self- and external-agency attribution a quantitative meta-analysis, based on activation likelihood estimation (ALE) method, across 15 PET and fMRI studies (228 subjects) was conducted. Results show converging activations including the TPJ, pre-SMA, precuneus and dorsomedial prefrontal cortex (dMPFC) in external-agency, while insula activation was related to self-agency. We discuss these findings, highlighting the role of the insula, and calling for the use of alternative paradigms such as intentional binding and interactive imitation to study agency.


Agency Insula fMRI PET Meta-analysis 



M.S. was funded by the EU FP6 IST Contract Feelix Growing no. 045169.


  1. Augustine JR (1996) Circuitry and functional aspects of the insular lobe in primates including humans. Brain Res Brain Res Rev 22:229–244PubMedCrossRefGoogle Scholar
  2. Bralslev D, Nielsen FÅ, Lund TE, Law I, Paulson OB (2006) Similar brain networks for detecting visuo-motor and visuo-proprioceptive synchrony. NeuroImage 31:308–312CrossRefGoogle Scholar
  3. Brass M, Ruby P, Spengler S (2009) Inhibition of imitative behaviour and social cognition. Philos Trans R Soc Lond B Biol Sci 364:2359–2367PubMedCrossRefGoogle Scholar
  4. Ciccarelli O, Toosy AT, Marsden JF, Wheeler-Kingshott CM, Sahyoun C, Matthews CM, Miller DH, Thompson AJ (2005) Identifying brain regions for integrative sensorimotor processing with ankle movements. Exp Brain Res 166:31–42PubMedCrossRefGoogle Scholar
  5. Corradi-Dell’Acqua C, Ueno K, Ogawa A, Cheng K, Rumiati RI, Iriki A (2008) Effects of shifting perspective of the self: an fMRI study. NeuroImage 40:1902–1911PubMedCrossRefGoogle Scholar
  6. Craig AD (2009a) Emotional moments across time: a possible neural basis for time perception in the anterior insula. Phil Trans R Soc B 364:1933–1942PubMedCrossRefGoogle Scholar
  7. Craig AD (2009b) How do you feel now? The anterior insula and human awareness. Nat Rev Neurosci 10:59–70PubMedCrossRefGoogle Scholar
  8. Craig AD (2010) The sentient self. Brain Struct Funct 214:563–577PubMedCrossRefGoogle Scholar
  9. Crespo-Facorro B, Kim J-J, Andreasen NC, O’Leary DS, Bockholt HJ, Magnotta V (2000) Insular cortex abnormalities in schizophrenia: a structural magnetic resonance imaging study of first-episode patients. Schizophr Res 46:35–43PubMedCrossRefGoogle Scholar
  10. Cunnington R, Windischberger C, Deecke L, Moser E (2002) The preparation and execution of self-initiated and externally-triggered movement: a study of event related fMRI. NeuroImage 15:373–385PubMedCrossRefGoogle Scholar
  11. Cunnington R, Windischberger C, Robinson S, Moser E (2006) The selection of intended actions and the observation of others’ actions: a time-resolved fMRI study. NeuroImage 29:1294–1302PubMedCrossRefGoogle Scholar
  12. David N, Cohen MX, Newen A, Bewernick BH, Shah NJ, Fink GR, Vogeley K (2007) The extrastriate cortex distinguishes between the consequences of one’s own and others’ behavior. NeuroImage 36:1004–1014PubMedCrossRefGoogle Scholar
  13. David N, Newen A, Vogeley K (2008) The “sense of agency” and its underlying cognitive and neural mechanisms. Conscious Cogn 17:523–534PubMedCrossRefGoogle Scholar
  14. Decety J, Lamm C (2007) The role of the right temporoparietal junction in social interaction: how low-level computational processes contribute to meta-cognition. Neuroscientist 13:580–593PubMedCrossRefGoogle Scholar
  15. Dumas G, Nadel J, Soussignan R, Martinerie J, Garnero L (2010) Inter-brain synchronization during social interaction. PLoS One 5:e12166PubMedCrossRefGoogle Scholar
  16. Eickhoff SB, Laird AR, Grefkes C, Wang LE, Zilles K, Fox PT (2009) Coordinate-based activation likelihood estimation meta-analysis of neuroimaging data: a random-effects approach based on empirical estimates of spatial uncertainty. Hum Brain Mapp 30:2907–2926PubMedCrossRefGoogle Scholar
  17. Farrer C, Frith CD (2002) Experiencing oneself vs another person as being the cause of an action: the neural correlates of the experience of agency. NeuroImage 15:596–603PubMedCrossRefGoogle Scholar
  18. Farrer C, Franck N, Georgieff N, Fith CD, Decety J, Jeannerod M (2003) Modulating the experience of agency: a positron emission tomography study. NeuroImage 18:324–333PubMedCrossRefGoogle Scholar
  19. Farrer C, Frey SH, Van Horn JD, Tunik E, Turk D, Inati S, Grafton ST (2008) The angular gyrus computes action awareness representation. Cereb Cortex 18:254–261PubMedCrossRefGoogle Scholar
  20. Fink GR, Marshall JC, Halligan PW, Frith CD, Driver J, Frackowiak RSJ, Dolan RJ (1999) The neural consequences of conflict between intention and the senses. Brain 122:497–512PubMedCrossRefGoogle Scholar
  21. Francis S, Lin X, Aboushoushah S, White TP, Phillips M, Bowtell R, Constantinescu CS (2009) fMRI analysis of active, passive and electrically stimulated ankle dorsiflexion. Neuroimage 44:469–479PubMedCrossRefGoogle Scholar
  22. Frith CD, Blakemore S, Wolpert DM (2000) Explaining the symptoms of schizophrenia: abnormalities in the awareness of action. Brain Res Brain Res Rev 31:357–363PubMedCrossRefGoogle Scholar
  23. Gallagher S (2007) The natural philosophy of agency. Philos Compass 2:347–357CrossRefGoogle Scholar
  24. Garavan H, Ross TJ, Kaufman J, Stein EA (2003) A midline dissociation between error-processing and response-conflict monitoring. NeuroImage 20:1132–1139PubMedCrossRefGoogle Scholar
  25. Genovese CR, Lazar NA, Nichols T (2002) Thresholding of statistical maps in functional neuroimaging using the false discovery rate. NeuroImage 15:870–878PubMedCrossRefGoogle Scholar
  26. Haggard P, Clark S, Kalogeras J (2002) Voluntary action and conscious awareness. Nat Neurosci 5:382–385PubMedCrossRefGoogle Scholar
  27. Iacoboni M, Lieberman MD, Knowlton BJ, Molnar-Szakacs I, Moritz M, Throop CJ, Fiske AP (2004) Watching social interactions produces dorsomedial prefrontal and medial parietal BOLD fMRI signal increases compared to a resting baseline. NeuroImage 21:1167–1173PubMedCrossRefGoogle Scholar
  28. Karnath H-O, Baier B (2010) Right insula for our sense of limb ownership and self-awareness of action. Brain Struct Funct 214:411–417PubMedCrossRefGoogle Scholar
  29. Kontaris I, Wiggett AJ, Downing PE (2009) Dissociation of extrastriate body and biological-motion selective areas by manipulation of visual-motor congruency. Neuropsychologia 47:3118–3124PubMedCrossRefGoogle Scholar
  30. Kurth F, Zilles K, Fox PT, Laird AR, Eickhoff SB (2010) A link between the systems: functional differentiation and integration within the human insula revealed by meta-analysis. Brain Struct Funct 214:519–534PubMedCrossRefGoogle Scholar
  31. Laird AR, Fox M, Price CJ, Glahn DC, Uecker AM, Lancaster JL, Turkeltaub PE, Kochunov P, Fox PT (2005) ALE meta-analysis: controlling the false discovery rate and performing statistical contrasts. Hum Brain Mapp 25:155–164PubMedCrossRefGoogle Scholar
  32. Lancaster JL, Tordesillas-Gutiérrez D, Martinez M, Salinas F, Evans A, Zilles K, Mazziotta JC, Fox PT (2007) Bias between MNI and Talairach coordinates analyzed using the ICBM-152 brain template. Hum Brain Mapp 28:1194–1205PubMedCrossRefGoogle Scholar
  33. Lau HC, Rogers RD, Haggard P, Passingham RE (2004) Attention to Intention. Science 303:1208–1210PubMedCrossRefGoogle Scholar
  34. Leube DT, Knoblich G, Erb M, Grodd W, Bartels M, Kircher TTJ (2003a) The neural correlates of perceiving one’s own movements. NeuroImage 20:2084–2090PubMedCrossRefGoogle Scholar
  35. Leube DT, Knoblich G, Erb M, Kircher TTJ (2003b) Observing ones hand become anarchic: an fMRI study of action identification. Conscious Cogn 12:597–608PubMedCrossRefGoogle Scholar
  36. Matsuzawa M, Matsuo K, Sugio T, Kato C, Nakai T (2005) Temporal relationship between action and visual outcome modulates brain activation: and fMRI study. Magn Reson Med Sci 4:115–121PubMedCrossRefGoogle Scholar
  37. Moore JW, Ruge D, Wenke D, Rothwell J, Haggard P (2010) Disrupting the experience of control in the human brain: pre-supplementary motor area contributes to the sense of agency. Proc Biol Sci. doi: 10.1098/rspb.2010.0404
  38. Nachev P, Rees G, Parton A, Kennard C, Husain M (2005) Volition and conflict in human medial frontal cortex. Curr Biol 15:122–128PubMedCrossRefGoogle Scholar
  39. Nachev P, Wydell H, O’Neill K, Husain M, Kennard C (2007) The role of pre-supplementary motor area in the control of action. NeuroImage 36:T155–T163PubMedCrossRefGoogle Scholar
  40. Nahab FB, Kundu P, Gallea C, Kakareka J, Pursley R, Pohida T, Miletta N, Friedman J, Hallett M (2010). The neural processes underlying self-agency. Cereb Cortex. doi: 10.1093/cercor/bhq059
  41. Picard N, Strick PL (1996) Motor areas of the medial wall: a review of their location and functional activation. Cereb Cortex 6:342–353PubMedCrossRefGoogle Scholar
  42. Ruby P, Decety J (2001) Effect of subjective perspective taking during simulation of action: a PET investigation of agency. Nat Neurosci 4:546–550PubMedGoogle Scholar
  43. Ruby P, Decety J (2003) What you believe versus what you think they believe: a neuroimaging study of conceptual perspective-taking. Eur J Neurosci 17:2475–2480PubMedCrossRefGoogle Scholar
  44. Schnell K, Heekeren K, Schnitker R, Daumann J, Weber J, Hesselmann V, Möller-Hartmann W, Thron A, Gouzoulis-Mayfrank E (2007) An fMRI approach to particularize the frontoparietal network for visuomotor action monitoring: detection of incongruence between test subjects’ actions and resulting perceptions. NeuroImage 34:332–341PubMedCrossRefGoogle Scholar
  45. Seidel EM, Eickhoff SB, Kellermann T, Schneider F, Gur RC, Habel U, Derntl B (2010) Who is to blame? Neural correlates of causal attribution in social situations. Soc Neurosci 15:1–16Google Scholar
  46. Spengler S, von Cramon DY, Brass M (2009) Was it me or was it you? How the sense of agency originates from ideomotor learning revealed by fMRI. NeuroImage 46:290–298PubMedCrossRefGoogle Scholar
  47. Spreng RN, Mar RA, Kim AS (2009) The common neural basis of autobiographical memory, prospection, navigation, theory of mind, and the default mode: a quantitative meta-analysis. J Cogn Neurosci 21:489–510PubMedCrossRefGoogle Scholar
  48. Tatsuya M, Sadato N, Yazawa S, Hanakawa T, Fukuyama H, Yonekura Y, Shibasaki H (1999) Brain structures related to active and passive finger movements in man. Brain 122:1989–1997CrossRefGoogle Scholar
  49. Tsakiris M, Haggard P (2005) Experimenting with the acting self. Cogn Neuropsychol 22:387–407PubMedCrossRefGoogle Scholar
  50. Tsakiris M, Costantini M, Haggard P (2008) The role of the right temporo-parietal junction in maintaining a coherent sense of one’s body. Neuropsychologia 46:3014–3018PubMedCrossRefGoogle Scholar
  51. Tsakiris M, Longo MR, Haggard P (2010) Having a body versus moving your body: neural signature of agency and body-ownership. Neuropsychologia. doi: 10.1016/j.neuropsychologia.2010.05.021
  52. Turkeltaub PE, Eden GF, Jones KM, Zeffiro TA (2002) Meta-analysis of the functional neuroanatomy of single-word reading: method and validation. NeuroImage 16:765–780PubMedCrossRefGoogle Scholar
  53. Ullsperger M, von Cramon DY (2001) Subprocesses of performance monitoring: a dissociation of error processing and response competition revealed by event-related fMRI and ERPs. NeuroImage 14:1387–1401PubMedCrossRefGoogle Scholar
  54. van der Meer L, Costafreda S, Aleman A, David AS (2010) Self-reflection and the brain: a theoretical review and meta-analysis of neuroimaging studies with implications for schizophrenia. Neurosci Biobehav Rev 34:935–946PubMedCrossRefGoogle Scholar
  55. Volz KG, Schubotz RI, von Cramon DY (2003) Predicting events of varying probability: uncertainty investigated by fMRI. NeuroImage 19:271–280PubMedCrossRefGoogle Scholar
  56. Volz KG, Schubotz RI, von Cramon DY (2004) Why am I unsure? Internal and external attribution of uncertainty dissociated by fMRI. NeuroImage 21:848–857PubMedCrossRefGoogle Scholar
  57. Volz KG, Schubotz RI, von Cramon DY (2005) Variants of uncertainty in decision-making and their neural correlates. Brain Res Bull 67:403–412PubMedCrossRefGoogle Scholar
  58. Voss M, Moore J, Hauser M, Gallinat J, Heinz A, Haggard P (2010) Altered awareness of action in schizophrenia: a specific deficit in predicting action consequences. Brain 133:3104–3112PubMedCrossRefGoogle Scholar
  59. Wiener M, Turkeltaub P, Coslett HB (2010) The image of time: a voxel-wise meta-analysis. NeuroImage 49:1728–1740PubMedCrossRefGoogle Scholar
  60. Wittmann M, Simmons AN, Aron JL, Paulus MP (2010) Accumulation of neural activity in the posterior insula encodes the passage of time. Neuropsychologia 48:3110–3120PubMedCrossRefGoogle Scholar
  61. Wolpert DM, Miall RC (1996) Forward models for physiological motor control. Neural Netw 9:1265–1279PubMedCrossRefGoogle Scholar
  62. Wolpert DM, Ghahramani Z, Jordan MI (1995) An internal model for sensorimotor integration. Science 269:1880–1882PubMedCrossRefGoogle Scholar
  63. Wylie KP, Tregellas JR (2010) The role of insula in schizophrenia. Schizophr Res. doi: 10.1016/j.schres.2010.08.027
  64. Yomogida Y, Sugiura M, Sassa Y, Wakusawa K, Sekiguchi A, Fukushima A, Takeuchi H, Horie K, Sato S, Kawashima R (2010) The neural basis of agency: an fMRI study. NeuroImage 50:198–207PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2011

Authors and Affiliations

  1. 1.Centre Emotion, CNRS 3246, Pavillon ClérambaultHôpital de la SalpêtrièreParisFrance
  2. 2.Pierre et Marie Curie UniversityParisFrance
  3. 3.Assistance Publique-Hôpitaux de Paris, Department of PsychiatryPitié-Salpêtrière HospitalParisFrance

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