No evidence for mirror system dysfunction in schizophrenia from a multimodal TMS/EEG study

Psychiatry Research

Volumn 228, Issue 3, 2015, Pages 431-440

  Andrews, Sophie C ^a,b   Enticott, Peter G ^b,c   Hoy, Kate E ^b   Thomson, Richard H ^b   Fitzgerald, Paul B ^b  

^a MONASH UNIVERSITY   (Australia)

^b Australia   (Australia)

^c DEAKIN UNIVERSITY   (Australia)

Author keywords

Electroencephalography; Mirror neurons; Schizoaffective disorder; Social perception; Theory of mind; Transcranial magnetic stimulation

Indexed keywords

ADULT; ARTICLE; CLINICAL ARTICLE; CONCURRENT VALIDITY; CONTROLLED STUDY; ELECTROENCEPHALOGRAPHY; EMOTIONALITY; FACIAL EXPRESSION; FEMALE; HAND MOVEMENT; HUMAN; MALE; MIDDLE AGED; MIRROR NEURON; PRIORITY JOURNAL; SCHIZOAFFECTIVE PSYCHOSIS; SCHIZOPHRENIA; SOCIAL COGNITION; TASK PERFORMANCE; THEORY OF MIND; TRANSCRANIAL MAGNETIC STIMULATION; CASE CONTROL STUDY; COGNITION DISORDERS; COMPLICATION; MULTIMODAL IMAGING; PATHOPHYSIOLOGY; PHYSIOLOGY; PSYCHOSIS; YOUNG ADULT;

ADULT; CASE-CONTROL STUDIES; COGNITION DISORDERS; ELECTROENCEPHALOGRAPHY; FEMALE; HUMANS; MALE; MIDDLE AGED; MIRROR NEURONS; MULTIMODAL IMAGING; PSYCHOTIC DISORDERS; SCHIZOPHRENIA; TRANSCRANIAL MAGNETIC STIMULATION; YOUNG ADULT;

EID: 84938742469     PISSN: 01651781     EISSN: 18727123     Source Type: Journal    
DOI: 10.1016/j.psychres.2015.05.067     Document Type: Article

References (60)

1. Addington J., Addington D. Facial affect recognition and information processing in schizophrenia and bipolar disorder. Schizophr. Res. 1998, 32:171-181.
2. Alaerts K., Swinnen S.P., Wenderoth N. Is the human primary motor cortex activated by muscular or direction-dependent features of observed movements?. Cortex 2009, 45:1148-1155.
3. Borroni P., Baldissera F. Activation of motor pathways during observation and execution of hand movements. Soc. Neurosci. 2008, 3:276-288.
4. Brune M. Emotion recognition, "theory of mind", and social behavior in schizophrenia. Psychiatry Res. 2005, 133:135-147.
5. Dapretto M., Davies M.S., Pfeifer J.H., Scott A.A., Sigman M., Bookheimer S.Y., Iacoboni M. Understanding emotions in others: mirror neuron dysfunction in children with autism spectrum disorders. Nat. Neurosci. 2006, 9:28-30.
6. Daskalakis Z.J., Christensen B.K., Fitzgerald P.B., Moller B., Fountain S.I., Chen R. Increased cortical inhibition in persons with schizophrenia treated with clozapine. J. Psychopharmacol. 2008, 22:203-209.
7. Di Pellegrino G., Fadiga L., Fogassi L., Gallese V., Rizzolatti G. Understanding motor events: a neurophysiological study. Exp. Brain Res. 1992, 91:176-180.
8. Dinstein I., Thomas C., Humphreys K., Minshew N., Behrmann M., Heeger D.J. Normal movement selectivity in autism. Neuron 2010, 66:461-469.
9. Donne C.M., Enticott P.G., Rinehart N.J., Fitzgerald P.B. A transcranial magnetic stimulation study of corticospinal excitability during the observation of meaningless, goal-directed, and social behaviour. Neurosci. Lett. 2011, 489:57-61.
10. Enticott P.G., Hoy K.E., Herring S.E., Johnston P.J., Daskalakis Z.J., Fitzgerald P.B. Reduced motor facilitation during action observation in schizophrenia: a mirror neuron deficit?. Schizophr. Res. 2008, 102:116-121.
11. Enticott P.G., Johnston P.J., Herring S.E., Hoy K.E., Fitzgerald P.B. Mirror neuron activation is associated with facial emotion processing. Neuropsychologia 2008, 46:2851-2854.
12. Enticott P.G., Kennedy H.A., Bradshaw J.L., Rinehart N.J., Fitzgerald P.B. Understanding mirror neurons: evidence for enhanced corticospinal excitability during the observation of transitive but not intransitive hand gestures. Neuropsychologia 2010, 48:2675-2680.
13. Enticott P.G., Kennedy H.A., Bradshaw J.L., Rinehart N.J., Fitzgerald P.B. Motor corticospinal excitability during the observation of interactive hand gestures. Brain Res. Bull. 2011, 85:89-95.
14. Enticott P.G., Kennedy H.A., Rinehart N.J., Bradshaw J.L., Tonge B.J., Daskalakis Z.J., Fitzgerald P.B. Interpersonal motor resonance in autism spectrum disorder: evidence against a global "mirror system" deficit. Front. Hum. Neurosci. 2013, 7:218.
15. Enticott P.G., Kennedy H.A., Rinehart N.J., Tonge B.J., Bradshaw J.L., Taffe J.R., Daskalakis Z.J., Fitzgerald P.B. Mirror neuron activity associated with social impairments but not age in autism spectrum disorder. Biol. Psychiatry 2012, 71:427-433.
16. Fadiga L., Craighero L., Olivier E. Human motor cortex excitability during the perception of others' action. Curr. Opin. Neurobiol. 2005, 15:213-218.
17. Fadiga L., Fogassi L., Pavesi G., Rizzolatti G. Motor facilitation during action observation: a magnetic stimulation study. J. Neurophysiol. 1995, 73:2608-2611.
18. Fan Y.T., Decety J., Yang C.Y., Liu J.L., Cheng Y. Unbroken mirror neurons in autism spectrum disorders. J. Child Psychol. Psychiatry 2010, 51:981-988.
19. Fitzgerald P.B., Brown T.L., Marston N.A., Oxley T., de Castella A., Daskalakis Z., Kulkarni J. Reduced plastic brain responses in schizophrenia: a transcranial magnetic stimulation study. Schizophr. Res. 2004, 71:17-26.
20. Gallese V., Goldman A. Mirror neurons and the simulation theory of mindreading. Trends Cogn. Sci. 1998, 2:493-501.
21. Gallese V., Keysers C., Rizzolatti G. A unifying view of the basis of social cognition. Trends Cogn. Sci. 2004, 8:396-403.
22. Green M.F. Cognitive impairment and functional outcome in schizophrenia and bipolar disorder. J. Clin. Psychiatry 2006, 67(Suppl 9):S3-S8.
23. Harrington L., Siegert R.J., McClure J. Theory of mind in schizophrenia: a critical review. Cogn. Neuropsychiatry 2005, 10:249-286.
24. Heyes C. Where do mirror neurons come from?. Neurosci. Biobehav. Rev. 2010, 34:575-583.
25. Hooker C.I., Park S. Emotion processing and its relationship to social functioning in schizophrenia patients. Psychiatry Res. 2002, 112:41-50.
26. Horan W.P., Iacoboni M., Cross K.A., Korb A., Lee J., Nori P., Quintana J., Wynn J.K., Green M.F. Self-reported empathy and neural activity during action imitation and observation in schizophrenia. Neuroimage Clin. 2014, 5:100-108.
27. Horan W.P., Pineda J.A., Wynn J.K., Iacoboni M., Green M.F. Some markers of mirroring appear intact in schizophrenia: evidence from mu suppression. Cogn. Affect. Behav. Neurosci. 2014, 14:1-12.
28. Huang C.L., Hsiao S., Hwu H.-G., Howng S.-L. Are there differential deficits in facial emotion recognition between paranoid and non-paranoid schizophrenia? A signal detection analysis. Psychiatry Res. 2013, 209:424-430.
29. Iacoboni M., Molnar-Szakacs I., Gallese V., Buccino G., Mazziotta J.C., Rizzolatti G. Grasping the intentions of others with one's own mirror neuron system. PLoS Biol. 2005, 3:e79.
30. Lepage J.-F., Saint-Amour D., Theoret H. EEG and neuronavigated single-pulse TMS in the study of the observation/execution matching system: are both techniques measuring the same process?. J. Neurosci. Methods 2008, 175:17-24.
31. Lepage J.F., Tremblay S., Théoret H. Early non-specific modulation of corticospinal excitability during action observation. Eur. J. Neurosci. 2010, 31:931-937.
32. Lieberman J.A., Stroup T.S., Perkins D.O. The American Psychiatric Publishing Textbook of Schizophrenia 2006, American Psychiatric Publishing, Inc., Washington, DC.
33. Martino D.J., Strejilevich S.A., Fassi G., Marengo E., Igoa A. Theory of mind and facial emotion recognition in euthymic bipolar I and bipolar II disorders. Psychiatry Res. 2011, 189:379-384.
34. McCormick L.M., Brumm M.C., Beadle J.N., Paradiso S., Yamada T., Andreasen N. Mirror neuron function, psychosis, and empathy in schizophrenia. Psychiatry Res.: Neuroimaging 2012, 201:233-239.
35. Mehta U.M., Basavaraju R., Thirthalli J., Gangadhar B.N. Mirror neuron dysfunction - a neuro-marker for social cognition deficits in drug naive schizophrenia. Schizophr. Res. 2012, 141:281-283.
36. Mehta U.M., Thirthalli J., Aneelraj D., Jadhav P., Gangadhar B.N., Keshavan M.S. Mirror neuron dysfunction in schizophrenia and its functional implications: a systematic review. Schizophr. Res. 2014, 160:9-19.
37. Molenberghs P., Cunnington R., Mattingley J.B. Brain regions with mirror properties: a meta-analysis of 125 human fMRI studies. Neurosci. Biobehav. Rev. 2012, 36:341-349.
38. Montag C., Dziobek I., Richter I.S., Neuhaus K., Lehmann A., Sylla R., Heekeren H.R., Heinz A., Gallinat J. Different aspects of theory of mind in paranoid schizophrenia: evidence from a video-based assessment. Psychiatry Res. 2011, 186:203-209.
39. Oberman L.M., Hubbard E.M., McCleery J.P., Altschuler E.L., Ramachandran V.S., Pineda J.A. EEG evidence of mirror neuron dysfunction in autism spectrum disorders. Cogn. Brain Res. 2005, 24:190-198.
40. Oberman L.M., Pineda J.A., Ramachandran V.S. The human mirror system: a link between action observation and social skills. Scan 2007, 2:62-66.
41. Oberman L.M., Ramachandran V.S., Pineda J.A. Modulation of mu suppression in children with autism spectrum disorders in response to familiar or unfamiliar stimuli: the mirror neuron hypothesis. Neuropsychologia 2008, 46:1558-1565.
42. Oztop E., Kawato M., Arbib M.A. Mirror neurons: functions, mechanisms and models. Neurosci. Lett. 2013, 540:43-55.
43. Penn D.L., Keefe R.S.E., Davis S.M., Meyer P.S., Perkins D.O., Losardo D., Lieberman J.A. The effects of antipsychotic medications on emotion perception in patients with chronic schizophrenia in the CATIE trial. Schizophr. Res. 2009, 115:17-23.
44. Penn D.L., Sanna L.J., Roberts D.L. Social cognition in schizophrenia: an overview. Schizophr. Bull. 2008, 34:408-411.
45. Pickup G.J. Relationship between theory of mind and executive function in schizophrenia: a systematic review. Psychopathology 2008, 41:206-213.
46. Pineda J.A. The functional significance of mu rhythms: translating "seeing" and "hearing" into "doing". Brain Res. Rev. 2005, 50:57-68.
47. Rossi S., Hallett M., Rossini P.M., Pascual-Leone A. Safety, ethical considerations, and application guidelines for the use of transcranial magnetic stimulation in clinical practice and research. Clin. Neurophysiol. 2009, 120:2008-2039.
48. Schmidt S., Cichy R.M., Kraft A., Brocke J., Irlbacher K., Brandt S.A. An initial transient-state and reliable measures of corticospinal excitability in TMS studies. Clin. Neurophysiol. 2009, 120:987-993.
49. Schurmann M., Jarvelainen J., Avikainen S., Cannon T.D., Lonnqvist J., Huttunen M., Hari R. Manifest disease and motor cortex reactivity in twins discordant for schizophrenia. Br. J. Psychiatry 2007, 198:178-179.
50. Shamay-Tsoory S.G., Aharon-Peretz J., Levkovitz Y. The neuroanatomical basis of affective mentalizing in schizophrenia: comparison of patients with schizophrenia and patients with localized prefrontal lesions. Schizophr. Res. 2007, 90:274-283.
51. Shamay-Tsoory S.G., Shur S., Barcai-Goodman L., Medlovich S., Harari H., Levkovitz Y. Dissociation of cognitive from affective components of theory of mind in schizophrenia. Psychiatry Res. 2007, 149:11-23.
52. Sheehan D.V., Lecrubier Y., Harnett Sheehan K., Amorim P., Janavs J., Weiller E., Hergueta T., Baker R., Dunbar G.C. The Mini-International Neuropsychiatric Interview (M.I.N.I.): the development and validation of a structured diagnostic psychiatric interview for DSM-IV and ICD-10. J. Clin. Psychiatry 1998, 59(20):22-23.
53. Singh F., Pineda J.A., Cadenhead K.S. Association of impaired EEG mu wave suppression, negative symptoms and social functioning in biological motion processing in first episode of psychosis. Schizophr. Res. 2011, 130:182-186.
54. Sparks A., McDonald S., Lino B., O'Donnell M., Green M.J. Social cognition, empathy and functional outcome in schizophrenia. Schizophr. Res. 2010, 122:172-178.
55. Sumiyoshi T., Higuchi Y., Itoh T., Matsui M., Arai H., Suzuki M., Kurachi M., Sumiyoshi C., Kawasaki Y. Effect of perospirone on P300 electrophysiological activity and social cognition in schizophrenia: a three-dimensional analysis with sLORETA. Psychiatry Res.: Neuroimaging 2009, 172:180-183.
56. Thakkar K.N., Peterman J.S., Park S. Altered brain activation during action imitation and observation in schizophrenia: a translational approach to investigating social dysfunction in schizophrenia. Am. J. Psychiatry 2014, 171:539-548.
57. Theoret H., Halligan E., Kobayashi M., Fregni F., Tager-Flusberg H., Pascual-Leone A. Impaired motor facilitation during action observation in individuals with autism spectrum disorder. Curr. Biol. 2005, 15:R84-R85.
58. Tottenham N., Tanaka J.W., Leon A.C., McCarry T., Nurse M., Hare T.A., Marcus D.J., Westerlund A., Casey B.J., Nelson C. The NimStim set of facial expressions: judgments from untrained research participants. Psychiatry Res. 2009, 168:242-249.
59. Ulloa E.R., Pineda J.A. Recognition of point-light biological motion: mu rhythms and mirror neuron activity. Behav. Brain Res. 2007, 183:188-194.
60. Virtanen J., Ruohonen J., Naatanen R., Ilmoniemi R.J. Instrumentation for the measurement of electric brain responses to transcranial magnetic stimulation. Med. Biol. Eng. Comput. 1999, 37:322-326.