Sex differences in the neuroanatomy of human mirror-neuron system: A voxel-based morphometric investigation

Neuroscience

Volumn 158, Issue 2, 2009, Pages 713-720

  Cheng, Y ^a,d   Chou, K H ^a   Decety, J ^b   Chen, I Y ^a   Hung, D ^c   Tzeng, O J L ^a   Lin, C P ^a  

^a NATIONAL YANG MING UNIVERSITY   (Taiwan)

^b UNIVERSITY OF CHICAGO   (United States)

^c NATIONAL CENTRAL UNIVERSITY   (Taiwan)

^d TAIPEI CITY HOSPITAL   (Taiwan)

Author keywords

empathy; mirror neuron system; neuroanatomy; sex differences; voxel based morphometry

Indexed keywords

ADULT; ARTICLE; BRAIN MAPPING; BRAIN SIZE; COGNITION; CONTROLLED STUDY; CORRELATION ANALYSIS; EMOTIONALITY; EMPATHY; FEMALE; GRAY MATTER; HUMAN; HUMAN EXPERIMENT; IMAGE ANALYSIS; MALE; NEUROANATOMY; NEUROPSYCHOLOGY; NORMAL HUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; PRIORITY JOURNAL; SEX DIFFERENCE;

ADULT; ANALYSIS OF VARIANCE; BRAIN; BRAIN MAPPING; CASE-CONTROL STUDIES; COGNITION; FEMALE; HUMANS; IMAGING, THREE-DIMENSIONAL; MAGNETIC RESONANCE IMAGING; MALE; MIDDLE AGED; NEUROANATOMY; NEURONS; NEUROPSYCHOLOGICAL TESTS; SEX CHARACTERISTICS;

EID: 58149472699     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2008.10.026     Document Type: Article

References (79)

1. Abell F., Krams M., Ashburner J., Passingham R., Friston K., Frackowiak R., Happe F., Frith C., and Frith U. The neuroanatomy of autism: a voxel-based whole brain analysis of structural scans. Neuroreport 10 (1999) 1647-1651
2. Alexander G.M., and Hines M. Sex differences in response to children's toys in nonhuman primates (Cercopithecus aethiops sabaeus). Evol Hum Behav 23 (2002) 467-479
3. Ashburner J., and Friston K.J. Multimodal image coregistration and partitioning: a unified framework. Neuroimage 6 (1997) 209-217
4. Ashburner J., and Friston K.J. Voxel-based morphometry: the methods. Neuroimage 11 (2000) 805-821
5. Baron-Cohen S., O'Riordan M., Joines R., Stone V., and Plaisted K. Recognition of faux pas by normally developing children with Asperger syndrome or high-functioning autism. J Autism Dev Disord 29 (1999) 407-418
6. Baron-Cohen S., and Wheelwright S. The Empathy Quotient: an investigation of adults with Asperger syndrome or high functioning autism, and normal sex differences. J Autism Dev Disord 34 (2004) 163-175
7. Baron-Cohen S., Knickmeyer R., and Belmonte M.K. Sex differences in the brain: implications for explaining autism. Science 310 (2005) 819-823
8. Buccino G., Binkofski F., Fink G.R., Fadiga L., Fogassi L., Gallese V., Seitz R.J., Zilles K., Rizzolatti G., and Freund H.J. Action observation activates premotor and parietal areas in a somatotopic manner: an fMRI study. Eur J Neurosci 13 (2001) 400-404
9. Cahill L., Haier R.J., White N.S., Fallon J., Kilpatrick J., Lawrence C., Potkin S.G., and Alkire M.T. Sex-related differences in amygdale activity during emotionally influenced memory storage. Neurobiol Learn Mem 75 (2001) 1-9
10. Carr L., Iacoboni M., Dubeau M.C., Mazziotta J.C., and Lenzi G.L. Neural mechanisms of empathy in humans: a relay from neural systems for imitation to limbic areas. Proc Natl Acad Sci U S A 100 (2003) 5497-5502
11. Chao L.L., and Martin A. Representation of manipulable man-made objects in the dorsal stream. Neuroimage 12 (2000) 478-484
12. Cheng Y., Tzeng O.J.L., Decety J., Imada T., and Hsieh J.C. Gender differences in the human mirror system: a magnetoencephalography study. Neuroreport 17 (2006) 1115-1119
13. Cheng Y., Decety J., Lin C.P., Hsieh J.C., Hung D., and Tzeng O.J.L. Sex differences in spinal excitability during observation of bipedal locomotion. Neuroreport 18 (2007) 887-890
14. Cheng Y., Melzoff A., and Decety J. Motivation modulates the activity of the human mirror-neuron system. Cereb Cortex 17 (2007) 1979-1986
15. Cheng Y., Lin C.P., Liu H.L., Hsu Y., Lim K., Hung D., and Decety J. Expertise modulates the perception of pain in others. Curr Biol 17 (2007) 1708-1713
16. Cheng Y., Yang C.Y., Lin C.P., Lee P.L., and Decety J. The perception of pain in others suppresses somatosensory oscillations. Neuroimage 40 (2008) 1833-1840
17. Cheng Y., Lee P.L., Yang C.Y., Lin C.P., Hung D., and Decety J. Gender differences in the mu rhythm of the human mirror-neuron system. PLoS ONE 3 (2008) e2113
18. Cialdini R.B., Schaller M., Houlihan D., Arps K., Fultz J., and Beaman A.L. Empathy-based helping: Is it selflessly or selfishly motivated?. J Pers Soc Psychol 52 (1987) 749-758
19. Connellan J., Baron-Cohen S., Wheelwright S., Batki A., and Ahluwalia J. Sex differences in human neonatal social perception. Infant Behav Dev 23 (2001) 113-118
20. Dapretto M., Davies M.S., Pfeifer J.H., Scott A.A., Sigman M., Bookeimer S.Y., and Iacoboni M. Understanding emotions in others: mirror neuron dysfunction in children with autism spectrum disorders. Nat Neurosci 9 (2006) 28-30
21. Davis M.H. Empathy: A social psychological approach (1996), Westview Press, Madison, WI
22. Decety J., and Jackson P.L. The functional architecture of human empathy. Behav Cogn Neurosci Rev 3 (2004) 71-100
23. Decety J., and Lamm C. Human empathy through the lens of social neuroscience. Sci World J 6 (2006) 1146-1163
24. Decety J., and Batson C.D. Social neuroscience approaches to interpersonal sensitivity. Soc Neurosci 2 (2007) 151-157
25. di Pellegrino G., Fadiga L., Fogassi L., Gallese V., and Rizzolatti G. Understanding motor events: a neurophysiological study. Exp Brain Res 91 (1992) 176-180
26. Doherty R.W. The emotional contagion scale: A measure of individual differences. J Nonverbal Behav 21 (1997) 131-154
27. Eisenberg N., and Fabes R.A. Empathy: conceptualization, measurement, and relation to prosocial behavior. Motiv Emotion 14 (1990) 131-149
28. Fadiga L., and Craighero L. Electrophysiology of action representation. J Clin Neurophysiol 21 (2004) 157-169
29. Folstein S.E., and Rosen-Sheidley B. Genetics of autism: complex aetiology for a heterogeneous disorder. Nat Rev Genet 2 (2001) 943-955
30. Frederikse M.E., Lu A., Aylward E., Barta P., and Peralson G. Sex differences in the inferior parietal lobule. Cereb Cortex 9 (1999) 896-901
31. Friston K.J., Frith C.D., Frackowiak R.S., and Turner R. Characterizing dynamic brain responses with fMRI: a multivariate approach. Neuroimage 2 (1995) 166-172
32. Friston K.J., Frith C.D., Turner R., and Frackowiak R.S. Characterizing evoked hemodynamics with fMRI. Neuroimage 2 (1995) 157-165
33. Gallese V., Fadiga L., Fogassi L., and Rizzolatti G. Action recognition in the premotor cortex. Brain 119 (1996) 593-609
34. Gallese V., and Goldman A. Mirror neurons and the simulation theory of mind-reading. Trends Cogn Sci 2 (1998) 493-501
35. Gazzola V., Aziz-Zadeh L., and Keysers C. Empathy and the somatotopic auditory mirror system in humans. Curr Biol 16 (2006) 1824-1829
36. Geary D.C. Male, female: the evolution of human sex differences (1998), American Psychological Association, Washington, DC
37. Good C.D., Johnsrude I., Ashburner J., Henson R.N.A., Friston K.J., and Frackowiak R.S.J. Cerebral asymmetry and the effects of sex and handedness on brain structure: a voxel-based morphometric analysis of 465 normal adult human brains. Neuroimage 14 (2001) 685-700
38. Gu X., and Han S. Attention and reality constraints on the neural processes of empathy for pain. Neuroimage 36 (2007) 256-267
39. Gur R.C., Turetsky B.I., Matsui M., Yan M., Bilker W., Hughett P., and Gur R.E. Sex differences in brain gray and white matter in healthy young adults: correlations with cognitive performance. J Neurosci 19 (1999) 4065-4072
40. Hadjikhani N., Joseph R.M., Snyder J., and Tager-Flusberg H. Anatomical differences in the mirror neuron system and social cognition. Cereb Cortex 16 (2006) 1276-1282
41. Haier R.J., Jung R.E., Yeo R.A., Head K., and Alkire M.T. The neuroanatomy of general intelligence: sex matters. Neuroimage 25 (2005) 320-327
42. Hall J.A. Nonverbal sex differences (1984), Johns Hopkins University Press, Baltimore
43. Han S., Fan Y., and Mao L. Gender difference in empathy for pain: an electrophysiological investigation. Brain Res 1196 (2008) 85-93
44. Hyde J., and Linn M. Gender differences in verbal ability: a meta-analysis. Psychol Bull 104 (1988) 53-69
45. Iacoboni M., Molnar-Szakacs I., Gallese V., Buccino G., Mazziotta J.C., and Rizzolatti G. Grasping the intentions of others with one's own mirror neuron system. PLoS Biol 3 (2005) e79
46. Jabbi M., Swart M., and Keysers C. Empathy for positive and negative emotions in the gustatory cortex. Neuroimage 34 (2007) 1744-1753
47. Kaplan J.T., and Iacoboni M. Getting a grip on other minds: mirror neurons, intention understanding, and cognitive empathy. Soc Neurosci 1 (2006) 175-183
48. Kimura D. Sex and cognition (1999), Massachusetts Institute of Technology Press, Cambridge, MA
49. Krams M., Quinton R., Ashburner J., Friston K.J., Frackowiak R.S., Bouloux P.M., and Passingham R.E. Kallmann's syndrome: mirror movements associated with bilateral corticospinal track hypertrophy. Neurology 52 (1999) 816-822
50. Lamm C., Batson C.D., and Decety J. The neural substrate of human empathy: effects of perspective taking and cognitive appraisal. J Cogn Neurosci 19 (2007) 42-58
51. Maguire E.A., Gadian D.G., Johnsrude I.S., Good C.D., Ashburner J., Frackowiak R.S.J., and Frith C.D. Navigation-related structural change in the hippocampi of taxi drivers. Proc Natl Acad Sci U S A 97 (2000) 4398-4403
52. McClure E.B. A meta-analytic review of sex differences in facial expression processing and their development in infants, children, and adolescents. Psychol Bull 126 (2000) 424-453
53. Mehrabian A., and Epstein N. A measure of emotional empathy. J Pers 40 (1972) 525-543
54. Mummery C.J., Patterson K., Price C.J., Ashburner J., Frackowiak R.S., and Hodges J.R. A voxel-based morphometry study of semantic dementia: relationship between temporal lobe atrophy and semantic memory. Ann Neurol 47 (2000) 36-45
55. Neubauer A.C., Fink A., and Schrausser D.G. Intelligence and neural efficiency: the influence of task content and sex on the brain-IQ relationship. Intelligence 30 (2002) 515-536
56. Nishitabi N., Schurmann M., Amunts K., and Hari R. Broca's region: from action to language. Physiology 20 (2005) 60-69
57. Nishitani N., Avikainen S., and Hari R. Abnormal imitation-related cortical activation sequence in Asperger's syndrome. Ann Neurol 55 (2004) 558-562
58. Oberman L.M., Hubbard E.M., McCleery J.P., Altschuler E.L., Ramachandran V.S., and Pineda J.A. EEG evidence for mirror neuron dysfunction in autism spectrum disorders. Brain Res Cogn Brain Res 24 (2005) 190-198
59. Oberman L.M., Ramachandran V.S., and 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 46 (2008) 1558-1565
60. Oldfield R.C. The assessment and analysis of handedness: the Edinburgh Inventory. Neuropsychologia 9 (1971) 97-113
61. Peters M. Sex differences in the human brain size and the general meaning of differences in brain size. Can J Psychol 45 (1991) 507-522
62. Pfeifer J.H., Iacoboni M., Mazziotta J.C., and Dapretto M. Mirroring others' emotions relates to empathy and interpersonal competence in children. Neuroimage 39 (2008) 2076-2085
63. Pineda J.A. The functional significance of mu rhythms: translating "seeing" and "hearing" into "doing.". Brain Res Brain Res Rev 50 (2005) 57-68
64. Preston S.D., and de Waal F.B.M. Empathy: its ultimate and proximate bases. Behav Brain Sci 25 (2002) 1-71
65. Richardson M.P., Friston K.J., Sisodiya S.M., Koepp M.J., Ashburner J., Free S.L., Brooks D.J., and Duncan J.S. Cortical grey matter and benzodiazepine receptors in malformations of cortical development. A voxel-based comparison of structural and functional imaging data. Brain 120 (1997) 1961-1973
66. Rizzolatti G., Fogassi L., and Gallese V. Neurophysiological mechanisms underlying the understanding and imitation of action. Nat Rev Neurosci 2 (2001) 661-670
67. Rizzolatti G., and Craighero L. The mirror-neuron system. Annu Rev Neurosci 27 (2004) 169-192
68. Schulte-Rüther M., Markowitsch H.J., Fink G.R., and Piefke M. Mirror neuron and theory of mind mechanisms involved n face-to-face interactions: a functional magnetic resonance imaging approach to empathy. J Cogn Neurosci 19 (2007) 1354-1372
69. Schulte-Rüther M., Markowitsch H.J., Shah N.J., Fink F.R., and Piefke M. Gender differences in brain networks supporting empathy. Neuroimage 42 1 (2008) 393-403
70. Siu A.M.H., and Shek D.T.L. Validation of the Interpersonal Reactivity Index in a Chinese context. Res Social Work Prac 15 (2005) 118
71. Smith S.M., Zhang Y., Jenkinson M., Chen J., Matthew P.M., Federico A., and De Stefano N. Accurate, robust, and automated longitudinal and cross-sectional brain change analysis. Neuroimage 17 (2002) 479-489
72. Sowell E.R., Thompson P.M., Holmes C.J., Batth R., Jernigan T.L., and Toga A.W. Localizing age-related changes in brain structure between childhood and adolescence using statistical parametric mapping. Neuroimage 9 (1999) 587-597
73. Sowell E.R., Levitt J., Thompson P.M., Holmes C.J., Blanton R.E., Kornsand D.S., Caplan R., McCracken J., Asarnow R., and Toga A.W. Brain abnormalities in early-onset schizophrenia spectrum disorder observed with statistical parametric mapping of structural magnetic resonance images. Am J Psychiatry 157 (2000) 1475-1484
74. Talairach J., and Tournoux P. Co-planar stereotaxic atlas of the human brain (1988), Thieme, New York
75. Théoret H., Hallogan E., Kobayashi M., Fregni F., Tager-Flusberg H., and Pascual-Leone A. Impaired motor facilitation during action observation in individuals with autism spectrum disorder. Curr Biol 15 (2005) R84-R85
76. Villabos M.E., Mizuno A., Dahl B.C., Kemmotsu N., and Mu{combining double acute accent}ller R.A. Reduced functional connectivity between V1 and inferior frontal cortex associated with visuomotor performance in autism. Neuroimage 25 (2005) 916-925
77. Williams J.H.G., Whiten A., Suddendorf T., and Perrett D.I. Imitation, mirror neurons and autism. Neurosci Biobehav Rev 25 (2001) 287-295
78. Yamasue H., Abe O., Suga M., Yamada H., Rogers M.A., Aoki S., Kato N., and Kasai K. Sex-linked neuroanatomical basis of human altruistic cooperativeness. Cereb Cortex 18 (2008) 2331-2340
79. Zilles K., Kawashima R., DabringHaus A., Fukuda H., and Schormann T. Hemispheric shape of European and Japanese brains: 3-D MRI analysis of intersubject variability, ethnical, and gender differences. Neuroimage 13 (2001) 262-271