Sex differences and Autism: Brain function during verbal fluency and mental rotation

PLoS ONE

Volumn 7, Issue 6, 2012, Pages

  Beacher, Felix D C C ^a,c   Radulescu, Eugenia ^a,b   Minati, Ludovico ^a,d   Baron Cohen, Simon ^e   Lombardo, Michael V ^e   Lai, Meng Chuan ^e   Walker, Anne ^f   Howard, Dawn ^f   Gray, Marcus A ^a,b,g   Harrison, Neil A ^a,b,f   Critchley, Hugo D ^a,b,f  

^a BRIGHTON AND SUSSEX MEDICAL SCHOOL   (United Kingdom)

^b UNIVERSITY OF SUSSEX   (United Kingdom)

^c St Francis Hospital The Heart Center   (United States)

^d DEPARTMENT OF NEUROSURGERY   (Italy)

^e UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^f SUSSEX PARTNERSHIP NHS FOUNDATION TRUST   (United Kingdom)

^g MONASH UNIVERSITY   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

ADULT; ARTICLE; ASPERGER SYNDROME; AUTISM; BOLD SIGNAL; BRAIN FUNCTION; CEREBELLUM; CONTROLLED STUDY; DEPTH PERCEPTION; DSM-IV-TR; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HUMAN; IMAGE ANALYSIS; MALE; MENTAL ROTATION TASK; MIDDLE FRONTAL GYRUS; MIDDLE TEMPORAL GYRUS; OCCIPITAL LOBE; PARAHIPPOCAMPAL GYRUS; PARIETAL LOBE; PRECUNEUS; REACTION TIME; RIGHT HANDEDNESS; SEX DIFFERENCE; TASK PERFORMANCE; TEMPORAL LOBE; VERBAL FLUENCY TASK; BRAIN; IMAGE PROCESSING; NEUROPSYCHOLOGICAL TEST; NUCLEAR MAGNETIC RESONANCE IMAGING; PATHOPHYSIOLOGY; PHYSIOLOGY; SEXUAL DEVELOPMENT; VERBAL BEHAVIOR;

ASPERGER SYNDROME; BRAIN; FEMALE; HUMANS; IMAGE PROCESSING, COMPUTER-ASSISTED; MAGNETIC RESONANCE IMAGING; MALE; NEUROPSYCHOLOGICAL TESTS; SEX CHARACTERISTICS; SPACE PERCEPTION; VERBAL BEHAVIOR;

EID: 84862164119     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0038355     Document Type: Article

References (75)

1. Volkmar FR, Klin A, (2000) Pervasive Developmental Disorders. In: Kaplan and Sadock's Comprehensive Textbook of Psychiatry CD-ROM 7th edition. Publisher: Lippincott Williams and Wilkins, Philadelphia, PA.
2. Cosgrove KP, Mazure CM, Staley JK, (2007) Evolving knowledge of sex differences in brain structure, function, and chemistry. Biological psychiatry. Oct 15 62(8): 847 55.
3. Cahill L, (2006) Why sex matters for neuroscience. Nature reviews. Neuroscience, Jun 7(6): 477 84.
4. Baron-Cohen S, (2009) Autism: the empathizing-systemizing (E-S) theory. Annals of the New York Academy of Sciences. Mar 1156: 68 80.
5. Baron-Cohen S, Richler J, Bisarya D, Gurunathan N, Wheelwright S, (2003) The systemizing quotient: an investigation of adults with Asperger syndrome or high-functioning autism, and normal sex differences. Philosophical transactions of the Royal Society of London. Feb 28 358(1430): 361 74.
6. Baron-Cohen S, Wheelwright S, (2004) The empathy quotient: an investigation of adults with Asperger syndrome or high functioning autism, and normal sex differences. Journal of autism and developmental disorders. Apr 34(2): 163 75.
7. Baron-Cohen S, Knickmeyer RC, Belmonte MK, (2005) Sex differences in the brain: implications for explaining autism. Science (New York, NY. Nov 4 310(5749): 819 23.
8. Beacher FD, Minati L, Baron-Cohen S, Lombardo MV, Lai MC, et al. (2011) Autism attenuates sex differences in brain structure: a combined voxel-based morphometry and diffusion tensor imaging study. AJNR. Jan 33(1): 83 9.
9. Radulescu E, Ganeshan B, Minati L, Beacher FD, Gray MA, et al. (2012) Gray matter textural heterogeneity as a potential in-vivo biomarker of fine structural abnormalities in Asperger syndrome. The Pharmacogenomics Journal. Feb 14.
10. Lai MC, (2011) PhD Dissertation: "How is Sex Related to Autism?" University of Cambridge.
11. Schwarz E, Guest PC, Rahmoune H, Wang L, Levin Y, et al. (2011) Sex-specific serum biomarker patterns in adults with Asperger's syndrome. Molecular Psychiatry. Dec 16(12): 1213 20.
12. Bejerot S, Eriksson JM, Bonde S, Carlstrom K, Humble MB, Eriksson E, (2012) The extreme male brain revisited: gender coherence in adults with autism spectrum disorder. British Journal of Psychiatry. Doi:10.1192/bjp.bp.111.097899.
13. Herlitz A, Nilsson LG, Backman L, (1997) Gender differences in episodic memory. Memory & cognition. Nov 25(6): 801 11.
14. Kozaki T, Yasukouchi A, (2009) Sex differences on components of mental rotation at different menstrual phases. The International journal of neuroscience 119(1): 59 67.
15. Astur RS, Tropp J, Sava S, Constable RT, Markus EJ, (2004) Sex differences and correlations in a virtual Morris water task, a virtual radial arm maze, and mental rotation. Behavioural brain research. May 5 151(1-2): 103 15.
16. Crucian GP, Berenbaum SA, (1998) Sex differences in right hemisphere tasks. Brain and cognition. Apr 36(3): 377 89.
17. Parsons TD, Larson P, Kratz K, Thiebaux M, Bluestein B, et al. (2004) Sex differences in mental rotation and spatial rotation in a virtual environment. Neuropsychologia. 42(4): 555 62.
18. Silk TJ, Rinehart N, Bradshaw JL, Tonge B, Egan G, et al. (2006) Visuospatial processing and the function of prefrontal-parietal networks in autism spectrum disorders: a functional MRI study. The American journal of psychiatry. Aug 163(8): 1440 3.
19. Kleinhans NM, Richards T, Sterling L, Stegbauer KC, Mahurin R, et al. (2008) Abnormal functional connectivity in autism spectrum disorders during face processing. Brain. Apr;131(Pt 4): 1000 12.
20. Decety J, (2011) The neuroevolution of empathy. Annals of the New York Academy of Sciences. Aug 1231: 35 45.
21. Brosnan M, Daggar R, Collomosse J, (2010) The relationship between systemising and mental rotation and the implications for the extreme male brain theory of autism. Journal of autism and developmental disorders. Jan 40(1): 1 7.
22. Kaiser A, Haller S, Schmitz S, Nitsch C, (2009) On sex/gender related similarities and differences in fMRI language research. Brain research reviews. Oct 61(2): 49 59.
23. Halari R, Sharma T, Hines M, Andrew C, Simmons A, Kumari V, (2006) Comparable fMRI activity with differential behavioural performance on mental rotation and overt verbal fluency tasks in healthy men and women. Experimental brain research Experimentelle Hirnforschung. Feb 169(1): 1 14.
24. Weiss EM, Siedentopf C, Hofer A, Deisenhammer EA, Hoptman MJ, et al. (2003) Brain activation pattern during a verbal fluency test in healthy male and female volunteers: a functional magnetic resonance imaging study. Neuroscience letters. Dec 11 352(3): 191 4.
25. Gauthier CT, Duyme M, Zanca M, Capron C, (2009) Sex and performance level effects on brain activation during a verbal fluency task: a functional magnetic resonance imaging study. Cortex; a journal devoted to the study of the nervous system and behavior. Feb 45(2): 164 76.
26. Thomsen T, Hugdahl K, Ersland L, Barndon R, Lundervold A, et al. (2000) Functional magnetic resonance imaging (fMRI) study of sex differences in a mental rotation task. Med Sci Monit. Nov-Dec 6(6): 1186 96.
27. Weiss E, Siedentopf CM, Hofer A, Deisenhammer EA, Hoptman MJ, et al. (2003) Sex differences in brain activation pattern during a visuospatial cognitive task: a functional magnetic resonance imaging study in healthy volunteers. Neuroscience letters. Jul 3 344(3): 169 72.
28. Hugdahl K, Thomsen T, Ersland L, (2006) Sex differences in visuo-spatial processing: an fMRI study of mental rotation. Neuropsychologia. 44(9): 1575 83.
29. Jordan K, Wustenberg T, Heinze HJ, Peters M, Jancke L, (2002) Women and men exhibit different cortical activation patterns during mental rotation tasks. Neuropsychologia. 40(13): 2397 408.
30. Leekam SR, Libby SJ, Wing L, Gould J, Taylor C, (2002) The Diagnostic Interview for Social and Communication Disorders: algorithms for ICD-10 childhood autism and Wing and Gould autistic spectrum disorder. Journal of child psychology and psychiatry, and allied disciplines. Mar 43(3): 327 42.
31. Baron-Cohen S, Wheelwright S, Skinner R, Martin J, Clubley E, (2001) The autism-spectrum quotient (AQ): evidence from Asperger syndrome/high-functioning autism, males and females, scientists and mathematicians. Journal of autism and developmental disorders. Feb 31(1): 5 17.
32. Wakabayashi A, Baron-Cohen S, Wheelwright S, Tojo Y, (2006) The Autism-Spectrum Quotient (AQ) in Japan: A cross-cultural comparison. Journal of autism and developmental disorders. Feb 36(2): 263 70.
33. Lawrence EJ, Shaw P, Baker D, Baron-Cohen S, David AS, (2004) Measuring empathy: reliability and validity of the Empathy Quotient. Psychological medicine. Jul 34(5): 911 9.
34. Nelson HE, O'Connell A, (1978) Dementia: the estimation of premorbid intelligence levels using the New Adult Reading Test. Cortex; a journal devoted to the study of the nervous system and behavior. Jun 14(2): 234 44.
35. Deichmann R, Josephs O, Hutton C, Corfield DR, Turner R, (2002) Compensation of susceptibility-induced BOLD sensitivity losses in echo-planar fMRI imaging. NeuroImage. Jan 15(1): 120 35.
36. Ashburner J, Friston KJ, (2005) Unified segmentation. NeuroImage. Jul 1 26(3): 839 51.
37. Friston KJ, Josephs O, Zarahn E, Holmes AP, Rouquette S, et al. (2000) To smooth or not to smooth? Bias and efficiency in fMRI time-series analysis. NeuroImage. Aug 12(2): 196 208.
38. Josephs O, Henson RN, (1999) Event-related functional magnetic resonance imaging: modelling, inference and optimization. Philosophical transactions of the Royal Society of London. Jul 29 354(1387): 1215 28.
39. Murty VP, Sambataro F, Radulescu E, Altamura M, Iudicello J, et al. (2011) Selective updating of working memory content modulates meso-cortico-striatal activity. NeuroImage. Aug 1 57(3): 1264 72.
40. Deary IJ, Penke L, Johnson W, (2010) The neuroscience of human intelligence differences. Nature reviews. Mar 11(3): 201 11.
41. Slotnick SD, Moo LR, Segal JB, Hart J, (2003) Distinct prefrontal cortex activity associated with item memory and source memory for visual shapes. Brain research. Jun 17(1): 75 82.
42. Zacks JM, (2008) Neuroimaging studies of mental rotation: a meta-analysis and review. Journal of cognitive neuroscience. Jan 20(1): 1 19.
43. Filipek PA, Accardo PJ, Baranek GT, Cook EH, Dawson G, et al. (1999) The screening and diagnosis of autistic spectrum disorders. Journal of autism and developmental disorders. Dec 29(6): 439 84.
44. Lai MC, Lombardo MV, Pasco G, Ruigrok AN, Wheelwright SJ, et al. (2011) A behavioral comparison of male and female adults with high functioning autism spectrum conditions. PloS one. 6(6): e20835.
45. Wing L, Gould J, Gillberg C, (2011) Autism spectrum disorders in the DSM-V: Better or worse than the DSM-IV? Research in developmental disabilities;Jan 3.
46. Baron-Cohen S, Lombardo MV, Auyeung B, Ashwin E, Chakrabarti B, et al. (2011) Why are autism spectrum conditions more prevalent in males? PLoS biology. Jun 9(6): e1001081.
47. Dehaene S, Le Clec HG, Poline JB, Le Bihan D, Cohen L, (2002) The visual word form area: a prelexical representation of visual words in the fusiform gyrus. Neuroreport. Mar 4 13(3): 321 5.
48. Amaral DG, Schumann CM, Nordahl CW, (2008) Neuroanatomy of autism. Trends in neurosciences. Mar 31(3): 137 45.
49. Wallace GL, Dankner N, Kenworthy L, Giedd JN, Martin A, (2010) Age-related temporal and parietal cortical thinning in autism spectrum disorders. Brain. Dec;133(Pt 12): 3745 54.
50. Minshew NJ, Williams DL, (2007) The new neurobiology of autism: cortex, connectivity, and neuronal organization. Archives of neurology. Jul 64(7): 945 50.
51. Liederman J, Fisher JM, Coty A, Matthews G, Frye RE, et al. (2012) Sex Differences in the Use of Delayed Semantic Context When Listening to Disrupted Speech. Archives of sexual behavior. Mar 21.
52. Mayes SD, Calhoun SL, (2001) Non-significance of early speech delay in children with autism and normal intelligence and implications for DSM-IV Asperger's disorder. Autism. Mar 5(1): 81 94.
53. Turner MA, (1999) Generating novel ideas: fluency performance in high-functioning and learning disabled individuals with autism. Journal of child psychology and psychiatry, and allied disciplines. Feb 40(2): 189 201.
54. Price CJ, (2010) The anatomy of language: a review of 100 fMRI studies published in 2009. Annals of the New York Academy of Sciences. Mar 1191: 62 88.
55. Badre D, Poldrack RA, Pare-Blagoev EJ, Insler RZ, Wagner AD, (2005) Dissociable controlled retrieval and generalized selection mechanisms in ventrolateral prefrontal cortex. Neuron. Sep 15 47(6): 907 18.
56. Tesink CM, Buitelaar JK, Petersson KM, van der Gaag RJ, Teunisse JP, et al. (2011) Neural correlates of language comprehension in autism spectrum disorders: when language conflicts with world knowledge. Neuropsychologia. Apr 49(5): 1095 104.
57. Harris GJ, Chabris CF, Clark J, Urban T, Aharon I, et al. (2006) Brain activation during semantic processing in autism spectrum disorders via functional magnetic resonance imaging. Brain and cognition. Jun 61(1): 54 68.
58. Mechelli A, Josephs O, Lambon RMA, McClelland JL, Price CJ, (2007) Dissociating stimulus-driven semantic and phonological effect during reading and naming. Human brain mapping. Mar 28(3): 205 17.
59. Steinmetz KR, Muscatell KA, Kensinger EA, (2010) The effect of valence on young and older adults' attention in a rapid serial visual presentation task. Psychology and aging. Mar 25(1): 239 45.
60. Simon SR, Meunier M, Piettre L, Berardi AM, Segebarth CM, et al. (2002) Spatial attention and memory versus motor preparation: premotor cortex involvement as revealed by fMRI. Journal of neurophysiology. Oct 88(4): 2047 57.
61. Scott-Van Zeeland AA, McNealy K, Wang AT, Sigman M, et al. (2010) No neural evidence of statistical learning during exposure to artificial languages in children with autism spectrum disorders. Biological psychiatry. Aug 15 68(4): 345 51.
62. Lai G, Pantazatos SP, Schneider H, Hirsch J, (2012) Neural systems for speech and song in autism. Brain 135: 961 75.
63. Baker SC, Frith CD, Dolan RJ, (1997) The interaction between mood and cognitive function studied with PET. Psychological medicine. May 27(3): 565 78.
64. Tang J, Critchley HD, Glaser DE, Dolan RJ, Butterworth B, (2006) Imaging informational conflict: a functional magnetic resonance imaging study of numerical stroop. Journal of cognitive neuroscience. Dec 18(12): 2049 62.
65. Golestani N, Alario FX, Meriaux S, Le Bihan D, Dehaene S, et al. (2006) Syntax production in bilinguals. Neuropsychologia 44(7): 1029 40.
66. Lissek S, Peters S, Fuchs N, Witthaus H, Nicolas V, et al. (2008) Cooperation and deception recruit different subsets of the theory-of-mind network. PloS one. 2008 3(4): e2023.
67. Clements-Stephens AM, Rimrodt SL, Cutting LE, (2009) Developmental sex differences in basic visuospatial processing: differences in strategy use? Neuroscience letters. Jan 16 449(3): 155 60.
68. Parsons LM, (2003) Superior parietal cortices and varieties of mental rotation. Trends in cognitive sciences. Dec 7(12): 515 7.
69. Manjaly ZM, Bruning N, Neufang S, Stephan KE, Brieber S, et al. (2007) Neurophysiological correlates of relatively enhanced local visual search in autistic adolescents. NeuroImage. Mar 35(1): 283 91.
70. Soulieres I, Dawson M, Samson F, Barbeau EB, Sahyoun CP, et al. (2009) Enhanced visual processing contributes to matrix reasoning in autism. Human brain mapping. Dec 30(12): 4082 107.
71. Keehn B, Brenner L, Palmer E, Lincoln AJ, Muller RA, (2008) Functional brain organization for visual search in ASD. J Int Neuropsychol Soc. Nov 14(6): 990 1003.
72. Perani D, Fazio F, Borghese NA, Tettamanti M, Ferrari S, et al. (2001) Different brain correlates for watching real and virtual hand actions. NeuroImage. Sep 14(3): 749 58.
73. Critchley HD, Rotshtein P, Nagai Y, O'Doherty J, Mathias CJ, et al. (2005) Activity in the human brain predicting differential heart rate responses to emotional facial expressions. NeuroImage. Feb 1 24(3): 751 62.
74. Materna S, Dicke PW, Thier P, (2008) The posterior superior temporal sulcus is involved in social communication not specific for the eyes. Neuropsychologia. Sep 46(11): 2759 65.
75. Vollm BA, Taylor AN, Richardson P, Corcoran R, Stirling J, et al. (2006) Neuronal correlates of theory of mind and empathy: a functional magnetic resonance imaging study in a nonverbal task. NeuroImage. Jan 1 29(1): 90 8.