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Voxel-based meta-analysis of regional white-matter volume differences in autism spectrum disorder versus healthy controls

Published online by Cambridge University Press:  16 November 2010

J. Radua ,
E. Via ,
M. Catani  and
D. Mataix-Cols
J. Radua*
Affiliation:
Department of Psychosis Studies, Institute of Psychiatry, King's College London, London, UK Hospital Benito Menni Complex Assistencial en Salut Mental, CIBERSAM, Sant Boi de Llobregat, Spain
E. Via
Affiliation:
Department of Psychosis Studies, Institute of Psychiatry, King's College London, London, UK Hospital Universitari de Bellvitge, IDIBELL, L'Hospitalet de Llobregat, Spain
M. Catani
Affiliation:
Natbrainlab, Department of Forensic and Neurodevelopmental Science, Institute of Psychiatry, King's College London, London, UK
D. Mataix-Cols
Affiliation:
Department of Psychosis Studies, Institute of Psychiatry, King's College London, London, UK
*
*Address for correspondence: J. Radua M.D., Department of Psychosis Studies, PO Box 69, Institute of Psychiatry, King's College London, London SE5 8AF, UK. (Email: Joaquim.Radua@iop.kcl.ac.uk)
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Abstract

Background

We conducted a meta-analysis of voxel-based morphometry (VBM) studies in autism spectrum disorder (ASD) to clarify the changes in regional white-matter volume underpinning this condition, and generated an online database to facilitate replication and further analyses by other researchers.

Method

PubMed, ScienceDirect, Web of Knowledge and Scopus databases were searched between 2002 (the date of the first white-matter VBM study in ASD) and 2010. Manual searches were also conducted. Authors were contacted to obtain additional data. Coordinates were extracted from clusters of significant white-matter difference between patients and controls. A new template for white matter was created for the signed differential mapping (SDM) meta-analytic method. A diffusion tensor imaging (DTI)-derived atlas was used to optimally localize the changes in white-matter volume.

Results

Thirteen datasets comprising 246 patients with ASD and 237 healthy controls met inclusion criteria. No between-group differences were found in global white-matter volumes. ASD patients showed increases of white-matter volume in the right arcuate fasciculus and also in the left inferior fronto-occipital and uncinate fasciculi. These findings remained unchanged in quartile and jackknife sensitivity analyses and also in subgroup analyses (pediatric versus adult samples).

Conclusions

Patients with ASD display increases of white-matter volume in tracts known to be important for language and social cognition. Whether the results apply to individuals with lower IQ or younger age and whether there are meaningful neurobiological differences between the subtypes of ASD remain to be investigated.

Keywords

Arcuate fasciculusAspergerautismmeta-analysisuncinate fasciculusvoxel-based morphometrywhite matter
Type
Original Articles
Information
Psychological Medicine , Volume 41 , Issue 7 , July 2011 , pp. 1539 - 1550
Copyright
Copyright © Cambridge University Press 2010

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References

Abell, F, Krams, M, Ashburner, J, Passingham, R, Friston, K, Frackowiak, R, Happe, F, Frith, C, Frith, U (1999). The neuroanatomy of autism: a voxel-based whole brain analysis of structural scans. Neuroreport 10, 1647–1651.CrossRefGoogle ScholarPubMed
Abrahams, BS, Geschwind, DH (2008). Advances in autism genetics: on the threshold of a new neurobiology. Nature Reviews Genetics 9, 341–355.CrossRefGoogle ScholarPubMed
Alexander, AL, Lee, JE, Lazar, M, Boudos, R, DuBray, MB, Oakes, TR, Miller, JN, Lu, J, Jeong, EK, McMahon, WM, Bigler, ED, Lainhart, JE (2007). Diffusion tensor imaging of the corpus callosum in autism. NeuroImage 34, 61–73.CrossRefGoogle ScholarPubMed
APA (2000). Diagnostic and Statistical Manual of Mental Disorders: DSM-IV-TR. American Psychiatric Association: Washington, DC.Google Scholar
Ashburner, J, Friston, KJ (2000). Voxel-based morphometry – the methods. NeuroImage 11, 805–821.CrossRefGoogle ScholarPubMed
Ashburner, J, Friston, KJ (2001). Why voxel-based morphometry should be used. NeuroImage 14, 1238–1243.CrossRefGoogle ScholarPubMed
Ashwin, C, Baron-Cohen, S, Wheelwright, S, O'Riordan, M, Bullmore, ET (2007). Differential activation of the amygdala and the ‘social brain’ during fearful face-processing in Asperger syndrome. Neuropsychologia 45, 2–14.CrossRefGoogle ScholarPubMed
Autism and Developmental Disabilities Monitoring Network Surveillance Year 2006 Principal Investigators; Centers for Disease Control and Prevention (CDC) (2009). Prevalence of autism spectrum disorders – Autism and Developmental Disabilities Monitoring Network, United States, 2006. MMWR. Surveillance Summaries 58, 1–20.Google Scholar
Aylward, EH, Minshew, NJ, Field, K, Sparks, BF, Singh, N (2002). Effects of age on brain volume and head circumference in autism. Neurology 59, 175–183.CrossRefGoogle ScholarPubMed
Baron-Cohen, S, Ring, HA, Bullmore, ET, Wheelwright, S, Ashwin, C, Williams, SC (2000). The amygdala theory of autism. Neuroscience & Biobehavioral Reviews 24, 355–364.CrossRefGoogle ScholarPubMed
Baron-Cohen, S, Ring, HA, Wheelwright, S, Bullmore, ET, Brammer, MJ, Simmons, A, Williams, SC (1999). Social intelligence in the normal and autistic brain: an fMRI study. European Journal of Neuroscience 11, 1891–1898.CrossRefGoogle Scholar
Bigler, ED, Abildskov, TJ, Petrie, JA, Johnson, M, Lange, N, Chipman, J, Lu, J, McMahon, W, Lainhart, JE (2010). Volumetric and voxel-based morphometry findings in autism subjects with and without macrocephaly. Developmental Neuropsychology 35, 278–295.Google Scholar
Boddaert, N, Chabane, N, Gervais, H, Good, CD, Bourgeois, M, Plumet, MH, Barthelemy, C, Mouren, MC, Artiges, E, Samson, Y, Brunelle, F, Frackowiak, RS, Zilbovicius, M (2004). Superior temporal sulcus anatomical abnormalities in childhood autism: a voxel-based morphometry MRI study. NeuroImage 23, 364–369.CrossRefGoogle ScholarPubMed
Bonilha, L, Cendes, F, Rorden, C, Eckert, M, Dalgalarrondo, P, Li, LM, Steiner, CE (2008). Gray and white matter imbalance – typical structural abnormality underlying classic autism? Brain & Development 30, 396–401.CrossRefGoogle ScholarPubMed
Bora, E, Fornito, A, Yucel, M, Pantelis, C (2010). Voxelwise meta-analysis of gray matter abnormalities in bipolar disorder. Biological Psychiatry 67, 1097–1105.CrossRefGoogle ScholarPubMed
Bowers, D, Coslett, HB, Bauer, RM, Speedie, LJ, Heilman, KM (1987). Comprehension of emotional prosody following unilateral hemispheric lesions: processing defect versus distraction defect. Neuropsychologia 25, 317–328.CrossRefGoogle ScholarPubMed
Brieber, S, Neufang, S, Bruning, N, Kamp-Becker, I, Remschmidt, H, Herpertz-Dahlmann, B, Fink, GR, Konrad, K (2007). Structural brain abnormalities in adolescents with autism spectrum disorder and patients with attention deficit/hyperactivity disorder. Journal of Child Psychology and Psychiatry, and Allied Disciplines 48, 1251–1258.CrossRefGoogle ScholarPubMed
Brugha, T, McManus, S, Meltzer, H, Smith, J, Scott, FJ, Purdon, S, Harris, J, Bankart, J (2009). Autism spectrum disorders in adults living in households throughout England. Report from the Adult Psychiatric Morbidity Survey 2007 (www.ic.nhs.uk/webfiles/publications/mental%20health/mental%20health%20surveys/APMS_Autism_report_standard_20_OCT_09.pdf).Google Scholar
Carper, RA, Moses, P, Tigue, ZD, Courchesne, E (2002). Cerebral lobes in autism: early hyperplasia and abnormal age effects. NeuroImage 16, 1038–1051.CrossRefGoogle ScholarPubMed
Catani, M, Howard, RJ, Pajevic, S, Jones, DK (2002). Virtual in vivo interactive dissection of white matter fasciculi in the human brain. NeuroImage 17, 77–94.Google Scholar
Catani, M, Jones, DK, Daly, E, Embiricos, N, Deeley, Q, Pugliese, L, Curran, S, Robertson, D, Murphy, DG (2008). Altered cerebellar feedback projections in Asperger syndrome. NeuroImage 41, 1184–1191.Google Scholar
Catani, M, Jones, DK, ffytche, DH (2005). Perisylvian language networks of the human brain. Annals of Neurology 57, 8–16.CrossRefGoogle ScholarPubMed
Catani, M, Thiebaut de Schotten, M (2008). A diffusion tensor imaging tractography atlas for virtual in vivo dissections. Cortex 44, 1105–1132.CrossRefGoogle ScholarPubMed
Catani, M, Thiebaut de Schotten, M (2011). Atlas of Human Brain Connections. Oxford University Press: Oxford.Google Scholar
Cody, H, Pelphrey, K, Piven, J (2002). Structural and functional magnetic resonance imaging of autism. International Journal of Developmental Neuroscience 20, 421–438.CrossRefGoogle ScholarPubMed
Courchesne, E, Karns, CM, Davis, HR, Ziccardi, R, Carper, RA, Tigue, ZD, Chisum, HJ, Moses, P, Pierce, K, Lord, C, Lincoln, AJ, Pizzo, S, Schreibman, L, Haas, RH, Akshoomoff, NA, Courchesne, RY (2001). Unusual brain growth patterns in early life in patients with autistic disorder: an MRI study. Neurology 57, 245–254.CrossRefGoogle ScholarPubMed
Courchesne, E, Pierce, K (2005). Why the frontal cortex in autism might be talking only to itself: local over-connectivity but long-distance disconnection. Current Opinion in Neurobiology 15, 225–230.CrossRefGoogle ScholarPubMed
Craig, MC, Catani, M, Deeley, Q, Latham, R, Daly, E, Kanaan, R, Picchioni, M, McGuire, P, Fahy, T, Murphy, D (2009). Altered connections on the road to psychopathy. Molecular Psychiatry 14, 946–953.CrossRefGoogle ScholarPubMed
Craig, MC, Zaman, SH, Daly, EM, Cutter, WJ, Robertson, DM, Hallahan, B, Toal, F, Reed, S, Ambikapathy, A, Brammer, M, Murphy, CM, Murphy, DG (2007). Women with autistic-spectrum disorder: magnetic resonance imaging study of brain anatomy. British Journal of Psychiatry 191, 224–228.CrossRefGoogle ScholarPubMed
Damasio, AR, Maurer, RG (1978). A neurological model for childhood autism. Archives of Neurology 35, 777–786.CrossRefGoogle ScholarPubMed
Davatzikos, C (2004). Why voxel-based morphometric analysis should be used with great caution when characterizing group differences. NeuroImage 23, 17–20.Google Scholar
Di Martino, A, Ross, K, Uddin, LQ, Sklar, AB, Castellanos, FX, Milham, MP (2009). Functional brain correlates of social and nonsocial processes in autism spectrum disorders: an activation likelihood estimation meta-analysis. Biological Psychiatry 65, 63–74.CrossRefGoogle ScholarPubMed
Duffau, H, Gatignol, P, Mandonnet, E, Peruzzi, P, Tzourio-Mazoyer, N, Capelle, L (2005). New insights into the anatomo-functional connectivity of the semantic system: a study using cortico-subcortical electrostimulations. Brain 128, 797–810.Google Scholar
Ebeling, U, von Cramon, D (1992). Topography of the uncinate fascicle and adjacent temporal fiber tracts. Acta Neurochirurgica 115, 143–148.CrossRefGoogle ScholarPubMed
Ecker, C, Rocha-Rego, V, Johnston, P, Mourao-Miranda, J, Marquand, A, Daly, EM, Brammer, MJ, Murphy, C, Murphy, DG (2010). Investigating the predictive value of whole-brain structural MR scans in autism: a pattern classification approach. NeuroImage 49, 44–56.Google Scholar
Fletcher, PT, Whitaker, RT, Tao, R, DuBray, MB, Froehlich, A, Ravichandran, C, Alexander, AL, Bigler, ED, Lange, N, Lainhart, JE (2010). Microstructural connectivity of the arcuate fasciculus in adolescents with high-functioning autism. NeuroImage 51, 1117–1125.CrossRefGoogle ScholarPubMed
Gadow, KD, Devincent, CJ, Pomeroy, J, Azizian, A (2005). Comparison of DSM-IV symptoms in elementary school-age children with PDD versus clinic and community samples. Autism 9, 392–415.CrossRefGoogle ScholarPubMed
Ghaziuddin, M, Greden, J (1998). Depression in children with autism/pervasive developmental disorders: a case-control family history study. Journal of Autism and Developmental Disorders 28, 111–115.Google Scholar
Ghaziuddin, M, Leininger, L, Tsai, L (1995). Brief report: thought disorder in Asperger syndrome: comparison with high-functioning autism. Journal of Autism and Developmental Disorders 25, 311–317.CrossRefGoogle ScholarPubMed
Ghaziuddin, M, Mountain-Kimchi, K (2004). Defining the intellectual profile of Asperger syndrome: comparison with high-functioning autism. Journal of Autism and Developmental Disorders 34, 279–284.CrossRefGoogle ScholarPubMed
Ghaziuddin, M, Weidmer-Mikhail, E, Ghaziuddin, N (1998). Comorbidity of Asperger syndrome: a preliminary report. Journal of Applied Research in Intellectual Disabilities 42, 279–283.CrossRefGoogle ScholarPubMed
Hadland, KA, Rushworth, MF, Gaffan, D, Passingham, RE (2003). The effect of cingulate lesions on social behaviour and emotion. Neuropsychologia 41, 919–931.CrossRefGoogle ScholarPubMed
Hardan, AY, Minshew, NJ, Keshavan, MS (2000). Corpus callosum size in autism. Neurology 55, 1033–1036.Google Scholar
Hasan, KM, Iftikhar, A, Kamali, A, Kramer, LA, Ashtari, M, Cirino, PT, Papanicolaou, AC, Fletcher, JM, Ewing-Cobbs, L (2009). Development and aging of the healthy human brain uncinate fasciculus across the lifespan using diffusion tensor tractography. Brain Research 1276, 67–76.CrossRefGoogle ScholarPubMed
Hazlett, HC, Poe, M, Gerig, G, Smith, RG, Provenzale, J, Ross, A, Gilmore, J, Piven, J (2005). Magnetic resonance imaging and head circumference study of brain size in autism: birth through age 2 years. Archives of General Psychiatry 62, 1366–1376.Google Scholar
Haznedar, MM, Buchsbaum, MS, Metzger, M, Solimando, A, Spiegel-Cohen, J, Hollander, E (1997). Anterior cingulate gyrus volume and glucose metabolism in autistic disorder. American Journal of Psychiatry 154, 1047–1050.Google ScholarPubMed
Hedges, LV, Olkin, I (1985). Statistical Methods for Meta-Analysis. Academic Press: Orlando.Google Scholar
Heilman, KM, Scholes, R, Watson, RT (1975). Auditory affective agnosia. Disturbed comprehension of affective speech. Journal of Neurology, Neurosurgery, and Psychiatry 38, 69–72.Google Scholar
Hong, SS, Ke, XY, Tang, TY, Huang, HQ, Zou, B, Li, HG, Hang, YY, Lu, ZH (2008). Corpus callosum morphometry in high functioning autism. In Asia-Pacific Conference on Mind Brain and Education, pp. 404–407. Research Center for Learning Science. Key Laboratory of Child Development and Learning Science, Ministry of Education, Southeast University, People's Republic of China: Washington, DC.Google Scholar
Howlin, P (2003). Outcome in high-functioning adults with autism with and without early language delays: implications for the differentiation between autism and Asperger syndrome. Journal of Autism and Developmental Disorders 33, 3–13.CrossRefGoogle ScholarPubMed
Hyde, KL, Samson, F, Evans, AC, Mottron, L (2009). Neuroanatomical differences in brain areas implicated in perceptual and other core features of autism revealed by cortical thickness analysis and voxel-based morphometry. Human Brain Mapping 31, 556–566.CrossRefGoogle Scholar
Ke, X, Hong, S, Tang, T, Zou, B, Li, H, Hang, Y, Zhou, Z, Ruan, Z, Lu, Z, Tao, G, Liu, Y (2008). Voxel-based morphometry study on brain structure in children with high-functioning autism. Neuroreport 19, 921–925.Google Scholar
Ke, X, Tang, T, Hong, S, Hang, Y, Zou, B, Li, H, Zhou, Z, Ruan, Z, Lu, Z, Tao, G, Liu, Y (2009). White matter impairments in autism, evidence from voxel-based morphometry and diffusion tensor imaging. Brain Research 1265, 171–177.CrossRefGoogle ScholarPubMed
Klin, A, Pauls, D, Schultz, R, Volkmar, F (2005). Three diagnostic approaches to Asperger syndrome: implications for research. Journal of Autism and Developmental Disorders 35, 221–234.CrossRefGoogle ScholarPubMed
Knaus, TA, Silver, AM, Kennedy, M, Lindgren, KA, Dominick, KC, Siegel, J, Tager-Flusberg, H (2010). Language laterality in autism spectrum disorder and typical controls: a functional, volumetric, and diffusion tensor MRI study. Brain and Language 112, 113–120.Google Scholar
Koning, C, Magill-Evans, J (2001). Social and language skills in adolescent boys with Asperger syndrome. Autism 5, 23–36.Google Scholar
Kumar, A, Sundaram, SK, Sivaswamy, L, Behen, ME, Makki, MI, Ager, J, Janisse, J, Chugani, HT, Chugani, DC (2009). Alterations in frontal lobe tracts and corpus callosum in young children with autism spectrum disorder. Cerebral Cortex 20, 2103–2113.Google Scholar
Kwon, H, Ow, AW, Pedatella, KE, Lotspeich, LJ, Reiss, AL (2004). Voxel-based morphometry elucidates structural neuroanatomy of high-functioning autism and Asperger syndrome. Developmental Medicine and Child Neurology 46, 760–764.CrossRefGoogle ScholarPubMed
Langen, M, Schnack, HG, Nederveen, H, Bos, D, Lahuis, BE, de Jonge, MV, van Engeland, H, Durston, S (2009). Changes in the developmental trajectories of striatum in autism. Biological Psychiatry 66, 327–333.CrossRefGoogle ScholarPubMed
Makris, N, Kennedy, DN, McInerney, S, Sorensen, AG, Ruopeng, W, Caviness, Jr. VS, Pandya, DN (2005). Segmentation of subcomponents within the superior longitudinal fascicle in humans: a quantitative, in vivo, DT-MRI study. Cerebral Cortex 15, 854–869.Google Scholar
McAlonan, GM, Cheung, C, Cheung, V, Wong, N, Suckling, J, Chua, SE (2009). Differential effects on white-matter systems in high-functioning autism and Asperger's syndrome. Psychological Medicine 39, 1885–1893.CrossRefGoogle ScholarPubMed
McAlonan, GM, Cheung, V, Cheung, C, Suckling, J, Lam, GY, Tai, KS, Yip, L, Murphy, DG, Chua, SE (2005). Mapping the brain in autism. A voxel-based MRI study of volumetric differences and intercorrelations in autism. Brain 128, 268–276.CrossRefGoogle ScholarPubMed
McAlonan, GM, Daly, E, Kumari, V, Critchley, HD, van Amelsvoort, T, Suckling, J, Simmons, A, Sigmundsson, T, Greenwood, K, Russell, A, Schmitz, N, Happe, F, Howlin, P, Murphy, DG (2002). Brain anatomy and sensorimotor gating in Asperger's syndrome. Brain 125, 1594–1606.CrossRefGoogle ScholarPubMed
McAlonan, GM, Suckling, J, Wong, N, Cheung, V, Lienenkaemper, N, Cheung, C, Chua, SE (2008). Distinct patterns of grey matter abnormality in high-functioning autism and Asperger's syndrome. Journal of Child Psychology and Psychiatry, and Allied Disciplines 49, 1287–1295.Google Scholar
Mechelli, A, Price, CJ, Friston, KJ, Ashburner, J (2005). Voxel-based morphometry of the human brain: methods and applications. Current Medical Imaging Reviews 1, 105–113.Google Scholar
Monk, CS, Weng, SJ, Wiggins, JL, Kurapati, N, Louro, HM, Carrasco, M, Maslowsky, J, Risi, S, Lord, C (2010). Neural circuitry of emotional face processing in autism spectrum disorders. Journal of Psychiatry & Neuroscience 35, 105–114.CrossRefGoogle ScholarPubMed
Pierce, K, Muller, RA, Ambrose, J, Allen, G, Courchesne, E (2001). Face processing occurs outside the fusiform ‘face area’ in autism: evidence from functional MRI. Brain 124, 2059–2073.CrossRefGoogle ScholarPubMed
Piven, J, Bailey, J, Ranson, BJ, Arndt, S (1997). An MRI study of the corpus callosum in autism. American Journal of Psychiatry 154, 1051–1056.Google Scholar
Pugliese, L, Catani, M, Ameis, S, Dell'Acqua, F, Thiebaut, de SM, Murphy, C, Robertson, D, Deeley, Q, Daly, E, Murphy, DG (2009). The anatomy of extended limbic pathways in Asperger syndrome: a preliminary diffusion tensor imaging tractography study. NeuroImage 47, 427–434.CrossRefGoogle ScholarPubMed
Radua, J, Mataix-Cols, D (2009). Voxel-wise meta-analysis of grey matter changes in obsessive-compulsive disorder. British Journal of Psychiatry 195, 391–400.Google Scholar
Radua, J, Mataix-Cols, D (2010). Heterogeneity of coordinate-based meta-analyses of neuroimaging data: an example from studies in OCD – authors' reply. British Journal of Psychiatry 197, 77.Google Scholar
Radua, J, van den Heuvel, OA, Surguladze, S, Mataix-Cols, D (2010). Meta-analytical comparison of voxel-based morphometry studies in obsessive-compulsive disorder vs other anxiety disorders. Archives of General Psychiatry 67, 701–711.CrossRefGoogle ScholarPubMed
Ross, ED (2010). Cerebral localization of functions and the neurology of language: fact versus fiction or is it something else? The Neuroscientist 16, 222–243.CrossRefGoogle ScholarPubMed
Ross, ED, Monnot, M (2008). Neurology of affective prosody and its functional-anatomic organization in right hemisphere. Brain and Language 104, 51–74.Google Scholar
Salimi-Khorshidi, G, Smith, SM, Keltner, JR, Wager, TD, Nichols, TE (2009). Meta-analysis of neuroimaging data: a comparison of image-based and coordinate-based pooling of studies. NeuroImage 45, 810–823.CrossRefGoogle Scholar
Schmahmann, JD, Pandya, DN, Wang, R, Dai, G, D'Arceuil, HE, de Crespigny, AJ, Wedeen, VJ (2007). Association fibre pathways of the brain: parallel observations from diffusion spectrum imaging and autoradiography. Brain 130, 630–653.Google Scholar
Schmitz, N, Daly, E, Murphy, D (2007). Frontal anatomy and reaction time in autism. Neuroscience Letters 412, 12–17.CrossRefGoogle ScholarPubMed
Schultz, RT (2005). Developmental deficits in social perception in autism: the role of the amygdala and fusiform face area. International Journal of Developmental Neuroscience 23, 125–141.CrossRefGoogle ScholarPubMed
Shinozaki, J, Hanakawa, T, Fukuyama, H (2007). Heterospecific and conspecific social cognition in the anterior cingulate cortex. Neuroreport 18, 993–997.Google Scholar
Shriberg, LD, Paul, R, McSweeny, JL, Klin, AM, Cohen, DJ, Volkmar, FR (2001). Speech and prosody characteristics of adolescents and adults with high-functioning autism and Asperger syndrome. Journal of Speech, Language, and Hearing Research 44, 1097–1115.Google Scholar
Stanfield, AC, McIntosh, AM, Spencer, MD, Philip, R, Gaur, S, Lawrie, SM (2008). Towards a neuroanatomy of autism: a systematic review and meta-analysis of structural magnetic resonance imaging studies. European Archives of Psychiatry and Clinical Neuroscience 23, 289–299.Google ScholarPubMed
Stroup, DF, Berlin, JA, Morton, SC, Olkin, I, Williamson, GD, Rennie, D, Moher, D, Becker, BJ, Sipe, TA, Thacker, SB (2000). Meta-analysis of observational studies in epidemiology: a proposal for reporting. Meta-analysis Of Observational Studies in Epidemiology (MOOSE) group. Journal of the American Medical Association 283, 2008–2012.CrossRefGoogle ScholarPubMed
Toal, F, Daly, EM, Page, L, Deeley, Q, Hallahan, B, Bloemen, O, Cutter, WJ, Brammer, MJ, Curran, S, Robertson, D, Murphy, C, Murphy, KC, Murphy, DG (2009). Clinical and anatomical heterogeneity in autistic spectrum disorder: a structural MRI study. Psychological Medicine 40, 1171–1181.CrossRefGoogle ScholarPubMed
Tucker, DM, Watson, RT, Heilman, KM (1977). Discrimination and evocation of affectively intoned speech in patients with right parietal disease. Neurology 27, 947–950.CrossRefGoogle ScholarPubMed
Turkeltaub, PE, Eden, GF, Jones, KM, Zeffiro, TA (2002). Meta-analysis of the functional neuroanatomy of single-word reading: method and validation. NeuroImage 16, 765–780.CrossRefGoogle ScholarPubMed
Viechtbauer, W (2005). Bias and efficiency of meta-analytic variance estimators in the random-effects model. Journal of Educational and Behavioral Statistics 30, 261–293.CrossRefGoogle Scholar
Volkmar, FR, Klin, A, Pauls, D (1998). Nosological and genetic aspects of Asperger syndrome. Journal of Autism and Developmental Disorders 28, 457–463.CrossRefGoogle ScholarPubMed
Volkmar, FR, State, M, Klin, A (2009). Autism and autism spectrum disorders: diagnostic issues for the coming decade. Journal of Child Psychology and Psychiatry, and Allied Disciplines 50, 108–115.Google Scholar
Wager, TD, Lindquist, M, Kaplan, L (2007). Meta-analysis of functional neuroimaging data: current and future directions. Social Cognitive and Affective Neuroscience 2, 150–158.Google Scholar
Waiter, GD, Williams, JH, Murray, AD, Gilchrist, A, Perrett, DI, Whiten, A (2004). A voxel-based investigation of brain structure in male adolescents with autistic spectrum disorder. NeuroImage 22, 619–625.CrossRefGoogle ScholarPubMed
Waiter, GD, Williams, JH, Murray, AD, Gilchrist, A, Perrett, DI, Whiten, A (2005). Structural white matter deficits in high-functioning individuals with autistic spectrum disorder: a voxel-based investigation. NeuroImage 24, 455–461.CrossRefGoogle ScholarPubMed
Wickelgren, I (2005). Neurology. Autistic brains out of synch? Science 308, 1856–1858.Google Scholar
Wing, L (1996). Autistic spectrum disorders. British Medical Journal 312, 327–328.Google Scholar
Yamasue, H, Ishijima, M, Abe, O, Sasaki, T, Yamada, H, Suga, M, Rogers, M, Minowa, I, Someya, R, Kurita, H, Aoki, S, Kato, N, Kasai, K (2005). Neuroanatomy in monozygotic twins with Asperger disorder discordant for comorbid depression. Neurology 65, 491–492.CrossRefGoogle ScholarPubMed