Recent Insights from fMRI Studies into the Neural Basis of Reciprocal Imitation in Autism Spectrum Disorders

  • Yuko OkamotoEmail author
  • Hirotaka Kosaka
Part of the Contemporary Clinical Neuroscience book series (CCNE)


Persons with autism spectrum disorder (ASD) show atypical engagement in imitative interaction with peers and caregivers. Because imitative interaction is a precursor of a theory of mind, disturbances of the brain regions associated with imitative interaction are an important component of the pathophysiology of ASD. Recently, advanced functional magnetic resonance imaging (fMRI) studies have begun to address the neural basis of reciprocal imitation in individuals with ASD, which includes both imitating another’s action and being imitated by another person. These studies suggest that a disturbance of an internal model represented by the human mirror neuron system (MNS) leads to atypical engagement in imitative interaction. However, it is still unknown whether individuals with ASD have an abnormality in the MNS itself or altered modulation/control of the MNS. We also discuss how to resolve this question and the possibilities of a new fMRI technique, hyper-scanning, for understanding the neural underpinnings of atypical engagement in imitative interaction.


Autism spectrum disorder (ASD) Imitating Being imitated Functional magnetic resonance imaging (fMRI) The lateral occipitotemporal cortex (LOTC) The extrastriate body area (EBA) The mirror neuron system (MNS) 


  1. 1.
    American Psychiatric Association (2013) Diagnostic and statistical manual of mental disorders, 5th edn. American Psychiatric Association, Washington, DCCrossRefGoogle Scholar
  2. 2.
    Asperger H (1944) Die“Autistischen Psychopathen”im Kindesalter. Archiv fur Psychiatrie und Nervenkrankheiten 117:76–136CrossRefGoogle Scholar
  3. 3.
    Kanner L (1943) Autistic disturbances of affective contact. Nervous Child 2:217–250Google Scholar
  4. 4.
    Nadel J (2002) Imitation and imitation recognition: functional use in preverbal infants and nonverbal children with autism. In: Meltzoff AN, Prinz W (eds) The imitative mind: development evolution and brain basis. Cambridge Univer-sity Press, Cambridge, pp 42–62CrossRefGoogle Scholar
  5. 5.
    Williams JH, Whiten A, Singh T (2004) A systematic review of action imitation in autistic spectrum disorder. J Autism Dev Disord 34(3):285–299CrossRefPubMedGoogle Scholar
  6. 6.
    Meltzoff AN (2005) Imitation and other minds: the “like me” hypothesis. In: Hurley S, Chater N (eds) Perspectives on imitation: from neuroscience to social science, vol 2. MIT Press, Cambridge, pp 55–77Google Scholar
  7. 7.
    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(1):28–30CrossRefPubMedGoogle Scholar
  8. 8.
    Jack A, Morris JP (2014) Neocerebellar contributions to social perception in adolescents with autism spectrum disorder. Dev Cogn Neurosci 10:77–92CrossRefPubMedGoogle Scholar
  9. 9.
    Poulin-Lord MP, Barbeau EB, Soulieres I, Monchi O, Doyon J, Benali H, Mottron L (2014) Increased topographical variability of task-related activation in perceptive and motor associative regions in adult autistics. Neuroimage Clin 4:444–453CrossRefPubMedPubMedCentralGoogle Scholar
  10. 10.
    Williams JH, Waiter GD, Gilchrist A, Perrett DI, Murray AD, Whiten A (2006) Neural mechanisms of imitation and ‘mirror neuron’ functioning in autistic spectrum disorder. Neuropsychologia 44(4):610–621CrossRefPubMedGoogle Scholar
  11. 11.
    Delaveau P, Arzounian D, Rotge JY, Nadel J, Fossati P (2015) Does imitation act as an oxytocin nebulizer in autism spectrum disorder? Brain 138:e360CrossRefPubMedGoogle Scholar
  12. 12.
    Okamoto Y, Kitada R, Tanabe HC, Hayashi MJ, Kochiyama T, Munesue T, Ishitobi M, Saito DN, Yanaka HT, Omori M, Wada Y, Okazawa H, Sasaki AT, Morita T, Itakura S, Kosaka H, Sadato N (2014) Attenuation of the contingency detection effect in the extrastriate body area in autism spectrum disorder. Neurosci Res 87:66–76CrossRefPubMedGoogle Scholar
  13. 13.
    Cook JL, Bird G (2012) Atypical social modulation of imitation in autism spectrum conditions. J Autism Dev Disord 42(6):1045–1051CrossRefPubMedGoogle Scholar
  14. 14.
    Cook J, Barbalat G, Blakemore SJ (2012) Top-down modulation of the perception of other people in schizophrenia and autism. Front Hum Neurosci 6:175CrossRefPubMedPubMedCentralGoogle Scholar
  15. 15.
    Chartrand TL, van Baaren R (2009) Chapter 5 human mimicry. Adv Exp Soc Psychol 41:219–274CrossRefGoogle Scholar
  16. 16.
    Smith IM, Bryson SE (1994) Imitation and action in autism: a critical review. Psychol Bull 116(2):259–273CrossRefPubMedGoogle Scholar
  17. 17.
    di Pellegrino G, Fadiga L, Fogassi L, Gallese V, Rizzolatti G (1992) Understanding motor events: a neurophysiological study. Exp Brain Res 91(1):176–180CrossRefPubMedGoogle Scholar
  18. 18.
    Gallese V, Fadiga L, Fogassi L, Rizzolatti G (1996) Action recognition in the premotor cortex. Brain 119:593–609CrossRefPubMedGoogle Scholar
  19. 19.
    Rizzolatti G, Fadiga L, Gallese V, Fogassi L (1996) Premotor cortex and the recognition of motor actions. Brain Res Cogn Brain Res 3(2):131–141CrossRefPubMedGoogle Scholar
  20. 20.
    Fogassi L, Ferrari PF, Gesierich B, Rozzi S, Chersi F, Rizzolatti G (2005) Parietal lobe: from action organization to intention understanding. Science 308(5722):662–667CrossRefPubMedGoogle Scholar
  21. 21.
    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):1569–1588CrossRefPubMedGoogle Scholar
  22. 22.
    Chong TT, Cunnington R, Williams MA, Kanwisher N, Mattingley JB (2008) fMRI adaptation reveals mirror neurons in human inferior parietal cortex. Curr Biol 18(20):1576–1580CrossRefPubMedPubMedCentralGoogle Scholar
  23. 23.
    de la Rosa S, Schillinger FL, Bulthoff HH, Schultz J, Uludag K (2016) fMRI adaptation between action observation and action execution reveals cortical areas with mirror neuron properties in human BA 44/45. Front Hum Neurosci 10:78PubMedPubMedCentralGoogle Scholar
  24. 24.
    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(6):1239–1255CrossRefPubMedGoogle Scholar
  25. 25.
    Molenberghs P, Cunnington R, Mattingley JB (2009) Is the mirror neuron system involved in imitation? A short review and meta-analysis. Neurosci Biobehav Rev 33(7):975–980CrossRefPubMedGoogle Scholar
  26. 26.
    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(2):1077–1089CrossRefPubMedPubMedCentralGoogle Scholar
  27. 27.
    Brass M, Heyes C (2005) Imitation: is cognitive neuroscience solving the correspondence problem? Trends Cogn Sci 9(10):489–495CrossRefPubMedGoogle Scholar
  28. 28.
    Sasaki AT, Kochiyama T, Sugiura M, Tanabe HC, Sadato N (2012) Neural networks for action representation: a functional magnetic-resonance imaging and dynamic causal modeling study. Front Hum Neurosci 6:236CrossRefPubMedPubMedCentralGoogle Scholar
  29. 29.
    Peelen MV, Downing PE (2007) The neural basis of visual body perception. Nat Rev Neurosci 8(8):636–648CrossRefPubMedGoogle Scholar
  30. 30.
    Puce A, Perrett D (2003) Electrophysiology and brain imaging of biological motion. Philos Trans R Soc Lond Ser B Biol Sci 358(1431):435–445CrossRefGoogle Scholar
  31. 31.
    Caspers S, Zilles K, Laird AR, Eickhoff SB (2010) ALE meta-analysis of action observation and imitation in the human brain. NeuroImage 50(3):1148–1167CrossRefPubMedPubMedCentralGoogle Scholar
  32. 32.
    Kilner JM, Friston KJ, Frith CD (2007) Predictive coding: an account of the mirror neuron system. Cogn Process 8(3):159–166CrossRefPubMedPubMedCentralGoogle Scholar
  33. 33.
    Iacoboni M, Woods RP, Brass M, Bekkering H, Mazziotta JC, Rizzolatti G (1999) Cortical mechanisms of human imitation. Science 286(5449):2526–2528CrossRefPubMedGoogle Scholar
  34. 34.
    Fishman I, Datko M, Cabrera Y, Carper RA, Muller RA (2015) Reduced integration and differentiation of the imitation network in autism: a combined functional connectivity magnetic resonance imaging and diffusion-weighted imaging study. Ann Neurol 78(6):958–969CrossRefPubMedPubMedCentralGoogle Scholar
  35. 35.
    Nebel MB, Eloyan A, Nettles CA, Sweeney KL, Ament K, Ward RE, Choe AS, Barber AD, Pekar JJ, Mostofsky SH (2016) Intrinsic visual-motor synchrony correlates with social deficits in autism. Biol Psychiatry 79(8):633–641CrossRefPubMedGoogle Scholar
  36. 36.
    Hamilton AF (2013) Reflecting on the mirror neuron system in autism: a systematic review of current theories. Dev Cogn Neurosci 3:91–105CrossRefPubMedGoogle Scholar
  37. 37.
    Yang J, Hofmann J (2016) Action observation and imitation in autism spectrum disorders: an ALE meta-analysis of fMRI studies. Brain Imaging Behav 10(4):960–969CrossRefGoogle Scholar
  38. 38.
    Ubaldi S, Barchiesi G, Cattaneo L (2015) Bottom-up and top-down visuomotor responses to action observation. Cereb Cortex 25(4):1032–1041CrossRefPubMedGoogle Scholar
  39. 39.
    Berger NI, Ingersoll B (2015) An evaluation of imitation recognition abilities in typically developing children and young children with autism Spectrum disorder. Autism Res 8(4):442–453CrossRefPubMedGoogle Scholar
  40. 40.
    Gergely G (2001) The obscure object of desire: ‘nearly, but clearly not, like me’: contingency preference in normal children versus children with autism. Bull Menn Clin 65(3):411–426CrossRefGoogle Scholar
  41. 41.
    Gergely G, Watson JS (1999) Early socio-emotional development: contingency perception and the social-biofeedback model. In: Mahwah NJ (ed) Social cognition: understanding others in the first months of life. Lawrence Erlbaum Associates, p 101–36 NJ, United States.Google Scholar
  42. 42.
    Bahrick LE, Watson JS (1985) Detection of intermodal proprioceptive-visual contingency as a potential basis of self-perception in infancy. Dev Psychol 21(6):963–973CrossRefGoogle Scholar
  43. 43.
    Downing PE, Jiang Y, Shuman M, Kanwisher N (2001) A cortical area selective for visual processing of the human body. Science 293(5539):2470–2473CrossRefPubMedGoogle Scholar
  44. 44.
    Astafiev SV, Stanley CM, Shulman GL, Corbetta M (2004) Extrastriate body area in human occipital cortex responds to the performance of motor actions. Nat Neurosci 7(5):542–548CrossRefPubMedGoogle Scholar
  45. 45.
    Jeannerod M (2004) Visual and action cues contribute to the self-other distinction. Nat Neurosci 7(5):422–423CrossRefPubMedGoogle Scholar
  46. 46.
    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(3):1004–1014CrossRefPubMedGoogle Scholar
  47. 47.
    David N, Jansen M, Cohen MX, Osswald K, Molnar-Szakacs I, Newen A, Vogeley K, Paus T (2009) Disturbances of self-other distinction after stimulation of the extrastriate body area in the human brain. Soc Neurosci 4(1):40–48CrossRefPubMedGoogle Scholar
  48. 48.
    Escalona A, Field T, Nadel J, Lundy B (2002) Brief report: imitation effects on children with autism. J Autism Dev Disord 32(2):141–144CrossRefPubMedGoogle Scholar
  49. 49.
    Field T, Field T, Sanders C, Nadel J (2001) Children with autism display more social behaviors after repeated imitation sessions. Autism 5(3):317–323CrossRefPubMedGoogle Scholar
  50. 50.
    Contaldo A, Colombi C, Narzisi A, Muratori F (2016) The social effect of “being imitated” in children with autism Spectrum disorder. Front Psychol 7:726CrossRefPubMedPubMedCentralGoogle Scholar
  51. 51.
    Tanabe HC, Kosaka H, Saito DN, Koike T, Hayashi MJ, Izuma K, Komeda H, Ishitobi M, Omori M, Munesue T, Okazawa H, Wada Y, Sadato N (2012) Hard to “tune in”: neural mechanisms of live face-to-face interaction with high-functioning autistic spectrum disorder. Front Hum Neurosci 6:268CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Research Center for Child Mental DevelopmentUniversity of FukuiFukuiJapan

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