Abstract
Autism spectrum disorder (ASD) is characterized by difficulties in theory of mind (ToM) and social communication. Studying structural and functional correlates of ToM in the brain and how autistic and nonautistic groups differ in terms of these correlates can help with diagnosis and understanding the biological mechanisms of ASD. In this study, we investigated white matter volume (WMV) and gray matter volume (GMV) differences between matching autistic and nonautistic samples, and how these structural features relate to age and ToM skills, indexed by the Reading the Mind in the Eyes (RMIE) measure. The results showed widespread GMV and WMV differences between the two groups in regions crucial for social processes. The autistic group did not express the typically observed negative GMV and positive WMV correlations with age at the same level as the nonautistic group, pointing to abnormalities in developmental structural changes. In addition, we found differences between the two groups in how GMV relates to ToM, particularly in the left frontal regions, and how WMV relates to ToM, mostly in the cingulate and corpus callosum. Finally, GMV in the left insula, a region that is part of the salience network, was found to be crucial in distinguishing ToM performance between the two groups.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
Thrersholded statistical maps for all contrasts presented in the results are available at https://identifiers.org/neurovault.collection:13948. The raw data and analysis scripts that support the findings of this study are available from the corresponding author, FS, upon reasonable request.
References
Abell F, Krams M, Ashburner J, Passingham R, Friston K, Frackowiak R, Happé F, Frith C, Frith U (1999) The neuroanatomy of autism: a voxel-based whole brain analysis of structural scans. NeuroReport 10(8):1647–1651
Alexander AL, Lee JE, Lazar M, Boudos R, DuBray MB, Oakes TR, Miller JN, Lu J, Jeong E-K, McMahon WM, Bigler ED, Lainhart JE (2007) Diffusion tensor imaging of the corpus callosum in autism. Neuroimage 34(1):61–73. https://doi.org/10.1016/j.neuroimage.2006.08.032
American Psychiatric Association (2013) Diagnostic and statistical manual of mental disorders: DSM-5, vol 5. American Psychiatric Association.
Amodio DM, Frith CD (2006) Meeting of minds: the medial frontal cortex and social cognition. Nat Rev Neurosci 7(4):268–277. https://doi.org/10.1038/nrn1884
Aoki Y, Abe O, Nippashi Y, Yamasue H (2013) Comparison of white matter integrity between autism spectrum disorder subjects and typically developing individuals: a meta-analysis of diffusion tensor imaging tractography studies. Mol Autism 4(1):25. https://doi.org/10.1186/2040-2392-4-25
Ashburner J, Friston KJ (2001) Why voxel-based morphometry should be used. Neuroimage 14(6):1238–1243. https://doi.org/10.1006/nimg.2001.0961
Bakhtiari R, Zürcher NR, Rogier O, Russo B, Hippolyte L, Granziera C, Araabi BN, Ahmadabadi MN, Hadjikhani N (2012) Differences in white matter reflect atypical developmental trajectory in autism: a tract-based spatial statistics study. NeuroImage Clin 1(1):48–56. https://doi.org/10.1016/j.nicl.2012.09.001
Barnea-Goraly N, Kwon H, Menon V, Eliez S, Lotspeich L, Reiss AL (2004) White matter structure in autism: preliminary evidence from diffusion tensor imaging. Biol Psychiatry 55(3):323–326. https://doi.org/10.1016/j.biopsych.2003.10.022
Baron-Cohen S, Wheelwright S, Spong A, Scahill V, Lawson J (2001) Are intuitive physics and intuitive psychology independent? A test with children with Asperger Syndrome. J Dev Learn Disord 4(1):47–78
Billstedt E, Gillberg IC, Gillberg C (2011) Aspects of quality of life in adults diagnosed with autism in childhood: a population-based study. Autism Int J Res Pract 15(1):7–20. https://doi.org/10.1177/1362361309346066
Boddaert N, Chabane N, Gervais H, Good CD, Bourgeois M, Plumet M-H, Barthélémy C, Mouren M-C, Artiges E, Samson Y, Brunelle F, Frackowiak RSJ, Zilbovicius M (2004) Superior temporal sulcus anatomical abnormalities in childhood autism: a voxel-based morphometry MRI study. Neuroimage 23(1):364–369. https://doi.org/10.1016/j.neuroimage.2004.06.016
Brain Development Cooperative Group (2012) Total and regional brain volumes in a population-based normative sample from 4 to 18 years: the NIH MRI study of normal brain development. Cereb Cortex 22(1):1–12. https://doi.org/10.1093/cercor/bhr018
Carper RA, Courchesne E (2005) Localized enlargement of the frontal cortex in early autism. Biol Psychiatry 57(2):126–133. https://doi.org/10.1016/j.biopsych.2004.11.005
Cauda F, Geda E, Sacco K, D’Agata F, Duca S, Geminiani G, Keller R (2011) Grey matter abnormality in autism spectrum disorder: an activation likelihood estimation meta-analysis study. J Neurol Neurosurg Psychiatry 82(12):1304–1313. https://doi.org/10.1136/jnnp.2010.239111
Courchesne E, Campbell K, Solso S (2011a) Brain growth across the life span in autism: age-specific changes in anatomical pathology. Brain Res 1380:138–145. https://doi.org/10.1016/j.brainres.2010.09.101
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(2):245–254. https://doi.org/10.1212/wnl.57.2.245
Courchesne E, Mouton PR, Calhoun ME, Semendeferi K, Ahrens-Barbeau C, Hallet MJ, Barnes CC, Pierce K (2011b) Neuron number and size in prefrontal cortex of children with autism. JAMA 306(18):2001–2010. https://doi.org/10.1001/jama.2011.1638
Craig M, Zaman SH, Daly EM, Cutter WJ, Robertson DMW, Hallahan B, Toal F, Reed S, Ambikapathy A, Brammer M, Murphy CM, Murphy DGM (2007) Women with autistic-spectrum disorder: magnetic resonance imaging study of brain anatomy. Br J Psychiatry 191(3):224–228. https://doi.org/10.1192/bjp.bp.106.034603
d’Albis M-A, Guevara P, Guevara M, Laidi C, Boisgontier J, Sarrazin S, Duclap D, Delorme R, Bolognani F, Czech C, Bouquet C, Moal ML-L, Holiga S, Amestoy A, Scheid I, Gaman A, Leboyer M, Poupon C, Mangin J-F, Houenou J (2018) Local structural connectivity is associated with social cognition in autism spectrum disorder. Brain J Neurol 141(12):3472–3481. https://doi.org/10.1093/brain/awy275
DeRamus TP, Kana RK (2015) Anatomical likelihood estimation meta-analysis of grey and white matter anomalies in autism spectrum disorders. NeuroImage Clin 7:525–536. https://doi.org/10.1016/j.nicl.2014.11.004
Dimond D, Schuetze M, Smith RE, Dhollander T, Cho I, Vinette S, Eycke KT, Lebel C, McCrimmon A, Dewey D, Connelly A, Bray S (2019) Reduced white matter fiber density in autism spectrum disorder. Cereb Cortex 29(4):1778–1788. https://doi.org/10.1093/cercor/bhy348
Duerden EG, Oatley HK, Mak-Fan KM, McGrath PA, Taylor MJ, Szatmari P, Roberts SW (2012) Risk factors associated with self-injurious behaviors in children and adolescents with autism spectrum disorders. J Autism Dev Disord 42(11):2460–2470. https://doi.org/10.1007/s10803-012-1497-9
Eack SM, Wojtalik JA, Keshavan MS, Minshew NJ (2017) Socio-cognitive brain function and connectivity during visual perspective-taking in autism and schizophrenia. Schizophr Res 183:102–109. https://doi.org/10.1016/j.schres.2017.03.009
Ecker C (2017) The neuroanatomy of autism spectrum disorder: an overview of structural neuroimaging findings and their translatability to the clinical setting. Autism 21(1):18–28. https://doi.org/10.1177/1362361315627136
Ecker C, Ginestet C, Feng Y, Johnston P, Lombardo MV, Lai M-C, Suckling J, Palaniyappan L, Daly E, Murphy CM, Williams SC, Bullmore ET, Baron-Cohen S, Brammer M, Murphy DGM, MRC AIMS Consortium, for the (2013) Brain surface anatomy in adults with autism: the relationship between surface area, cortical thickness, and autistic symptoms. JAMA Psychiat 70(1):59–70. https://doi.org/10.1001/jamapsychiatry.2013.265
Emery NJ, Perrett DI (2000) How can studies of the monkey brain help us to understand “theory of mind” and autism in humans? In: Baron-Cohen S, Tager-Flusberg H, Cohen DJ (eds) Understanding other minds: perspectives from developmental cognitive neuroscience. Oxford University Press, pp 274–305
Forbes CE, Grafman J (2010) The role of the human prefrontal cortex in social cognition and moral judgment. Annu Rev Neurosci 33:299–324. https://doi.org/10.1146/annurev-neuro-060909-153230
Frith CD (2008) Social cognition. Philos Trans R Soc B Biol Sci 363(1499):2033–2039. https://doi.org/10.1098/rstb.2008.0005
Frith CD, Frith U (2007) Social cognition in humans. Curr Biol 17(16):724–732. https://doi.org/10.1016/j.cub.2007.05.068
Gauthier I, Skudlarski P, Gore JC, Anderson AW (2000) Expertise for cars and birds recruits brain areas involved in face recognition. Nat Neurosci 3:191–197
Gibbard CR, Ren J, Seunarine KK, Clayden JD, Skuse DH, Clark CA (2013) White matter microstructure correlates with autism trait severity in a combined clinical–control sample of high-functioning adults. NeuroImage Clin 3:106–114. https://doi.org/10.1016/j.nicl.2013.07.007
Gibbard CR, Ren J, Skuse DH, Clayden JD, Clark CA (2018) Structural connectivity of the amygdala in young adults with autism spectrum disorder. Hum Brain Mapp 39(3):1270–1282. https://doi.org/10.1002/hbm.23915
Gogtay N, Giedd JN, Lusk L, Hayashi KM, Greenstein D, Vaituzis AC, Nugent TF, Herman DH, Clasen LS, Toga AW, Rapoport JL, Thompson PM (2004) Dynamic mapping of human cortical development during childhood through early adulthood. Proc Natl Acad Sci U S A 101(21):8174–8179. https://doi.org/10.1073/pnas.0402680101
Goodkind M, Eickhoff SB, Oathes DJ, Jiang Y, Chang A, Jones-Hagata LB, Ortega BN, Zaiko YV, Roach EL, Korgaonkar MS, Grieve SM, Galatzer-Levy I, Fox PT, Etkin A (2015) Identification of a common neurobiological substrate for mental illness. JAMA Psychiat 72(4):305. https://doi.org/10.1001/jamapsychiatry.2014.2206
Green SA, Hernandez L, Bookheimer SY, Dapretto M (2016) Salience network connectivity in autism is related to brain and behavioral markers of sensory overresponsivity. J Am Acad Child Adolesc Psychiatry 55(7):618–626. https://doi.org/10.1016/j.jaac.2016.04.013
Greimel E, Nehrkorn B, Schulte-Rüther M, Fink G, Nickl-Jockschat T, Herpertz-Dahlmann B, Konrad K, Eickhoff S (2013) Changes in grey matter development in autism spectrum disorder. Brain Struct Funct 218(4):929–942. https://doi.org/10.1007/s00429-012-0439-9
Hadjikhani N, Joseph RM, Snyder J, Tager-Flusberg H (2006) Anatomical differences in the mirror neuron system and social cognition network in autism. Cereb Cortex 16(9):1276–1282
Hagmann P, Sporns O, Madan N, Cammoun L, Pienaar R, Wedeen VJ, Meuli R, Thiran J-P, Grant PE (2010) White matter maturation reshapes structural connectivity in the late developing human brain. Proc Natl Acad Sci USA 107(44):19067–19072. https://doi.org/10.1073/pnas.1009073107
Han M, Jiang G, Luo H, Shao Y (2021) Neurobiological bases of social networks. Front Psychol. https://doi.org/10.3389/fpsyg.2021.626337
Happé F, Frith U (2006) The weak coherence account: detail-focused cognitive style in autism spectrum disorders. J Autism Dev Disord 36(1):5–25. https://doi.org/10.1007/s10803-005-0039-0
Hotier S, Leroy F, Boisgontier J, Laidi C, Mangin J-F, Delorme R, Bolognani F, Czech C, Bouquet C, Toledano E, Bouvard M, Petit J, Mishchenko M, d’Albis M-A, Gras D, Gaman A, Scheid I, Leboyer M, Zalla T, Houenou J (2017) Social cognition in autism is associated with the neurodevelopment of the posterior superior temporal sulcus. Acta Psychiatr Scand 136(5):517–525. https://doi.org/10.1111/acps.12814
Howlin P, Moss P, Savage S, Rutter M (2013) Social outcomes in mid- to later adulthood among individuals diagnosed with autism and average nonverbal IQ as children. J Am Acad Child Adolesc Psychiatry 52(6):572–658. https://doi.org/10.1016/j.jaac.2013.02.017
Hyde KL, Samson F, Evans AC, Mottron L (2010) Neuroanatomical differences in brain areas implicated in perceptual and other core features of autism revealed by cortical thickness analysis and voxel-based morphometry. Hum Brain Mapp 31(4):556–566. https://doi.org/10.1002/hbm.20887
Im WY, Ha JH, Kim EJ, Cheon K-A, Cho J, Song D-H (2018) Impaired white matter integrity and social cognition in high-function autism: diffusion tensor imaging study. Psychiatry Investig 15(3):292–299. https://doi.org/10.30773/pi.2017.08.15
Isaksson J, Westeinde AV, Cauvet É, Kuja-Halkola R, Lundin K, Neufeld J, Willfors C, Bölte S (2019) Social cognition in autism and other neurodevelopmental disorders: a co-twin control study. J Autism Dev Disord 49(7):2838–2848. https://doi.org/10.1007/s10803-019-04001-4
Johansen-Berg H (2010) Behavioural relevance of variation in white matter microstructure. Curr Opin Neurol 23(4):351–358. https://doi.org/10.1097/WCO.0b013e32833b7631
Johnson MH, Griffin R, Csibra G, Halit H, Farroni T, de Haan M, Tucker LA, Baron-Cohen S, Richards J (2005) The emergence of the social brain network: evidence from typical and atypical development. Dev Psychopathol 17(3):599–619. https://doi.org/10.1017/S0954579405050297
Jones CRG, Simonoff E, Baird G, Pickles A, Marsden AJS, Tregay J, Happé F, Charman T (2018) The association between theory of mind, executive function, and the symptoms of autism spectrum disorder. Autism Res 11(1):95–109. https://doi.org/10.1002/aur.1873
Just MA, Cherkassky VL, Keller TA, Kana RK, Minshew NJ (2007) Functional and anatomical cortical underconnectivity in autism: evidence from an fMRI study of an executive function task and corpus callosum morphometry. Cereb Cortex 17:951–961. https://doi.org/10.1093/cercor/bhl006
Kana RK, Keller TA, Cherkassky VL, Minshew NJ, Just MA (2009) Atypical frontal-posterior synchronization of theory of mind regions in autism during mental state attribution. Soc Neurosci 4(2):135–152. https://doi.org/10.1080/17470910802198510
Kana RK, Keller TA, Minshew NJ, Just MA (2007) Inhibitory control in high-functioning autism: decreased activation and underconnectivity in inhibition networks. Biol Psychiatry 62(3):198–206. https://doi.org/10.1016/j.biopsych.2006.08.004
Kana RK, Patriquin MA, Black BS, Channell MM, Wicker B (2016) Altered medial frontal and superior temporal response to implicit processing of emotions in autism: implicit processing of emotions in autism. Autism Res 9(1):55–66. https://doi.org/10.1002/aur.1496
Kanske P, Böckler A, Trautwein F-M, Singer T (2015) Dissecting the social brain: introducing the EmpaToM to reveal distinct neural networks and brain-behavior relations for empathy and theory of mind. Neuroimage 122:6–19. https://doi.org/10.1016/j.neuroimage.2015.07.082
Kodama M, Ono T, Yamashita F, Ebata H, Liu M, Kasuga S, Ushiba J (2018) Structural gray matter changes in the hippocampus and the primary motor cortex on an-hour-to-one- day scale can predict arm-reaching performance improvement. Front Hum Neurosci. https://doi.org/10.3389/fnhum.2018.00209
Kolb B, Mychasiuk R, Muhammad A, Li Y, Frost DO, Gibb R (2012) Experience and the developing prefrontal cortex. Proc Natl Acad Sci USA 109:17186–17193. https://doi.org/10.1073/pnas.1121251109
Lai M-C, Baron-Cohen S, Buxbaum JD (2015) Understanding autism in the light of sex/gender. Mol Autism 6:24. https://doi.org/10.1186/s13229-015-0021-4
Lefebvre A, Beggiato A, Bourgeron T, Toro R (2015) Neuroanatomical diversity of corpus callosum and brain volume in autism: meta-analysis, analysis of the autism brain imaging data exchange project, and simulation. Biol Psychiatry 78(2):126–134. https://doi.org/10.1016/j.biopsych.2015.02.010
Libero LE, DeRamus TP, Deshpande HD, Kana RK (2014) Surface-based morphometry of the cortical architecture of autism spectrum disorders: volume, thickness, area, and gyrification. Neuropsychologia 62(1):1–10. https://doi.org/10.1016/j.neuropsychologia.2014.07.001
Libero LE, Nordahl CW, Li DD, Ferrer E, Rogers SJ, Amaral DG (2016) Persistence of megalencephaly in a subgroup of young boys with autism spectrum disorder. Autism Res 9(11):1169–1182. https://doi.org/10.1002/aur.1643
Lim L, Chantiluke K, Cubillo AI, Smith AB, Simmons A, Mehta MA, Rubia K (2015) Disorder-specific grey matter deficits in attention deficit hyperactivity disorder relative to autism spectrum disorder. Psychol Med 45(5):965–976. https://doi.org/10.1017/S0033291714001974
Lo Y-C, Chen Y-J, Hsu Y-C, Tseng W-YI, Gau SS-F (2017) Reduced tract integrity of the model for social communication is a neural substrate of social communication deficits in autism spectrum disorder. J Child Psychol Psychiatry 58(5):576–585. https://doi.org/10.1111/jcpp.12641
Long JA (2019) Interactions: comprehensive, user-friendly toolkit for probing interactions. https://cran.r-project.org/package=interactions
Loomba N, Beckerson ME, Ammons CJ, Maximo JO, Kana RK (2021) Corpus callosum size and homotopic connectivity in autism spectrum disorder. Psychiatry Res Neuroimaging 313:111301. https://doi.org/10.1016/j.pscychresns.2021.111301
Luna B, Minshew NJ, Garver KE, Lazar NA, Thulborn KR, Eddy WF, Sweeney JA (2002) Neocortical system abnormalities in autism: an fMRI study of spatial working memory. Neurology 59(6):834–840. https://doi.org/10.1212/wnl.59.6.834
Maguire EA, Spiers HJ, Good CD, Hartley T, Frackowiak RSJ, Burgess N (2003) Navigation expertise and the human hippocampus: a structural brain imaging analysis. Hippocampus 13(2):250–259. https://doi.org/10.1002/hipo.10087
Martino AD, 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. Biol Psychiatry 65(1):63–74. https://doi.org/10.1016/j.biopsych.2008.09.022
May KE, Kana RK (2020) Frontoparietal network in executive functioning in autism spectrum disorder. Autism Res 13(10):1762–1777. https://doi.org/10.1002/aur.2403
Mazurek MO (2014) Loneliness, friendship, and well-being in adults with autism spectrum disorders. Autism Int J Res Pract 18(3):223–232. https://doi.org/10.1177/1362361312474121
Mcalonan GM, Cheung V, Cheung C, Suckling J, Lam GY, Tai KS, Yip L, Murphy DGM, Chua SE (2005) Mapping the brain in autism. A voxel-based MRI study of volumetric differences and intercorrelations in autism. Brain J Neurol 128(2):268–276. https://doi.org/10.1093/brain/awh332
Menon V, Uddin LQ (2010) Saliency, switching, attention and control: a network model of insula function NIH Public Access Author Manuscript Introduction and overview. Brain Struct Funct 214(5–6):655–667. https://doi.org/10.1007/s00429-010-0262-0
Morgan JT, Chana G, Abramson I, Semendeferi K, Courchesne E, Everall IP (2012) Abnormal microglial–neuronal spatial organization in the dorsolateral prefrontal cortex in autism. Brain Res 1456:72–81. https://doi.org/10.1016/j.brainres.2012.03.036
Mueller S, Wang D, Fox MD, Yeo BTT, Sepulcre J, Sabuncu MR, Shafee R, Lu J, Liu H (2013) Individual variability in functional connectivity architecture of the human brain. Neuron 77(3):586–595. https://doi.org/10.1016/j.neuron.2012.12.028
Murdaugh DL, Shinkareva SV, Deshpande HR, Wang J, Pennick MR, Kana RK (2012) Differential deactivation during mentalizing and classification of autism based on default mode network connectivity. PLoS ONE 7(11):e50064. https://doi.org/10.1371/journal.pone.0050064
Naito M (2003) The relationship between theory of mind and episodic memory: evidence for the development of autonoetic consciousness. J Exp Child Psychol 85(4):312–336. https://doi.org/10.1016/s0022-0965(03)00075-4
Nickl-Jockschat T, Habel U, Maria Michel T, Manning J, Laird AR, Fox PT, Schneider F, Eickhoff SB (2012a) Brain structure anomalies in autism spectrum disorder-a meta-analysis of VBM studies using anatomic likelihood estimation. Hum Brain Mapp 33(6):1470–1489. https://doi.org/10.1002/hbm.21299
Nickl-Jockschat T, Habel U, Michel TM, Manning J, Laird AR, Fox PT, Schneider F, Eickhoff SB (2012b) Brain structure anomalies in autism spectrum disorder–a meta-analysis of VBM studies using anatomic likelihood estimation. Hum Brain Mapp 33(6):1470–1489. https://doi.org/10.1002/hbm.21299
Nomi JS, Molnar-Szakacs I, Uddin LQ (2019) Insular function in autism: update and future directions in neuroimaging and interventions. Prog Neuropsychopharmacol Biol Psychiatry 89:412–426. https://doi.org/10.1016/j.pnpbp.2018.10.015
Noriuchi M, Kikuchi Y, Yoshiura T, Kira R, Shigeto H, Hara T, Tobimatsu S, Kamio Y (2010) Altered white matter fractional anisotropy and social impairment in children with autism spectrum disorder. Brain Res 1362:141–149. https://doi.org/10.1016/j.brainres.2010.09.051
Orsmond GI, Shattuck PT, Cooper BP, Sterzing PR, Anderson KA (2013) Social participation among young adults with an autism spectrum disorder. J Autism Dev Disord 43(11):2710–2719. https://doi.org/10.1007/s10803-013-1833-8
Park MTM, Raznahan A, Shaw P, Gogtay N, Lerch JP, Chakravarty MM (2018) Neuroanatomical phenotypes in mental illness: identifying convergent and divergent cortical phenotypes across autism, ADHD and schizophrenia. J Psychiatry Neurosci JPN 43(3):201–212. https://doi.org/10.1503/jpn.170094
Patriquin MA, DeRamus T, Libero LE, Laird A, Kana RK (2016) Neuroanatomical and neurofunctional markers of social cognition in autism spectrum disorder. Hum Brain Mapp 37(11):3957–3978. https://doi.org/10.1002/hbm.23288
R Core Team (2022) R: a language and environment for statistical computing. R Foundation for Statistical Computing. https://www.R-project.org/
Radeloff D, Ciaramidaro A, Siniatchkin M, Hainz D, Schlitt S, Weber B, Poustka F, Bölte S, Walter H, Freitag CM (2014) Structural alterations of the social brain: a comparison between schizophrenia and autism. PLoS ONE 9(9):1–9. https://doi.org/10.1371/journal.pone.0106539
Retico A, Giuliano A, Tancredi R, Cosenza A, Apicella F, Narzisi A, Biagi L, Tosetti M, Muratori F, Calderoni S (2016) The effect of gender on the neuroanatomy of children with autism spectrum disorders: a support vector machine case-control study. Mol Autism 7(5):1–20. https://doi.org/10.1186/s13229-015-0067-3
Rosenblau G, O’Connell G, Heekeren HR, Dziobek I (2020) Neurobiological mechanisms of social cognition treatment in high-functioning adults with autism spectrum disorder. Psychol Med 50(14):2374–2384. https://doi.org/10.1017/S0033291719002472
Sacco R, Gabriele S, Persico AM (2015) Head circumference and brain size in autism spectrum disorder: a systematic review and meta-analysis. Psychiatry Res 234(2):239–251. https://doi.org/10.1016/j.pscychresns.2015.08.016
Sasson NJ, Faso DJ, Nugent J, Lovell S, Kennedy DP, Grossman RB (2017) Neurotypical peers are less willing to interact with those with autism based on thin slice judgments. Sci Rep 7(1):1–10. https://doi.org/10.1038/srep40700
Sato W, Kochiyama T, Uono S, Yoshimura S, Kubota Y, Sawada R, Sakihama M, Toichi M (2017) Reduced gray matter volume in the social brain network in adults with autism spectrum disorder. Front Hum Neurosci 11(395):1–12. https://doi.org/10.3389/fnhum.2017.00395
Sato W, Toichi M, Uono S, Kochiyama T (2012) Impaired social brain network for processing dynamic facial expressions in autism spectrum disorders. BMC Neurosci. https://doi.org/10.1186/1471-2202-13-99
Scarpazza C, Simone MD (2016) Voxel-based morphometry: current perspectives. Neurosci Neuroecon 5:19–35. https://doi.org/10.2147/NAN.S66439
Scherf KS, Elbich D, Minshew N, Behrmann M (2015) Individual differences in symptom severity and behavior predict neural activation during face processing in adolescents with autism. NeuroImage Clin 7:53–67. https://doi.org/10.1016/j.nicl.2014.11.003
Schulte-Rüther M, Greimel E, Markowitsch HJ, Kamp-Becker I, Remschmidt H, Fink GR, Piefke M (2011) Dysfunctions in brain networks supporting empathy: an fMRI study in adults with autism spectrum disorders. Soc Neurosci 6(1):1–21. https://doi.org/10.1080/17470911003708032
Schumann CM, Bloss CS, Barnes CC, Wideman GM, Carper RA, Akshoomoff N, Pierce K, Hagler D, Schork N, Lord C, Courchesne E (2010) Longitudinal magnetic resonance imaging study of cortical development through early childhood in autism. J Neurosci 30(12):4419–4427. https://doi.org/10.1523/JNEUROSCI.5714-09.2010
Schurz M, Maliske L, Kanske P (2020) Cross-network interactions in social cognition: a review of findings on task related brain activation and connectivity. Cortex J Study Nervous Syst Behav 130:142–157. https://doi.org/10.1016/j.cortex.2020.05.006
Seeley WW, Menon V, Schatzberg AF, Keller J, Glover GH, Kenna H, Reiss AL, Greicius MD (2007) Dissociable intrinsic connectivity networks for salience processing and executive control. J Neurosci 27(9):2349–2356. https://doi.org/10.1523/JNEUROSCI.5587-06.2007
Shine JM, Poldrack RA (2018) Principles of dynamic network reconfiguration across diverse brain states. Neuroimage 180:396–405. https://doi.org/10.1016/j.neuroimage.2017.08.010
Spreng RN (2013) Examining the role of memory in social cognition. Front Psychol. https://doi.org/10.3389/fpsyg.2013.00437
Stoner R, Chow ML, Boyle MP, Sunkin SM, Mouton PR, Roy S, Wynshaw-Boris A, Colamarino SA, Lein ES, Courchesne E (2014) Patches of disorganization in the neocortex of children with autism. N Engl J Med 370(13):1209–1219. https://doi.org/10.1056/NEJMoa1307491
Tang R, Friston KJ, Tang Y-Y (2020) Brief mindfulness meditation induces gray matter changes in a brain hub. Neural Plast. https://doi.org/10.1155/2020/8830005
Thomas C, Moya L, Avidan G, Humphreys K, Jung KJ, Peterson MA, Behrmann M (2008) Reduction in white matter connectivity, revealed by diffusion tensor imaging, May account for age-related changes in face perception. J Cogn Neurosci 20(2):268–284. https://doi.org/10.1162/jocn.2008.20025
Thompson A, Shahidiani A, Fritz A, O’Muircheartaigh J, Walker L, D’Almeida V, Murphy C, Daly E, Murphy D, Williams S, Deoni S, Ecker C (2020) Age-related differences in white matter diffusion measures in autism spectrum condition. Mol Autism 11(1):1–36. https://doi.org/10.1186/s13229-020-00325-6
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 DGM (2010) Clinical and anatomical heterogeneity in autistic spectrum disorder: a structural MRI study. Psychol Med 40(7):1171–1181. https://doi.org/10.1017/S0033291709991541
Travers BG, Adluru N, Ennis C, Tromp DPM, Destiche D, Doran S, Bigler ED, Lange N, Lainhart JE, Alexander AL (2012) Diffusion tensor imaging in autism spectrum disorder: a review. Autism Res 5(5):289–313. https://doi.org/10.1002/aur.1243
Trontel HG, Duffield TC, Bigler ED, Froehlich A, Prigge MBD, Nielsen JA, Cooperrider JR, Cariello AN, Travers BG, Anderson JS, Zielinski BA, Alexander A, Lange N, Lainhart JE (2013) Fusiform correlates of facial memory in autism. Behav Sci. https://doi.org/10.3390/bs3030348
Uddin LQ (2015) Salience processing and insular cortical function and dysfunction. Nat Rev Neurosci 16(1):55–61. https://doi.org/10.1038/nrn3857
Uddin LQ, Menon V (2009) The anterior insula in autism: under-connected and under-examined. Neurosci Biobehav Rev 33(8):1198–1203. https://doi.org/10.1016/j.neubiorev.2009.06.002
Uddin LQ, Supekar K, Lynch CJ, Khouzam A, Phillips J, Feinstein C, Ryali S, Menon V (2013a) Salience network-based classification and prediction of symptom severity in children with autism. JAMA Psychiat 70(8):869. https://doi.org/10.1001/jamapsychiatry.2013.104
Uddin LQ, Supekar K, Menon V (2013b) Reconceptualizing functional brain connectivity in autism from a developmental perspective. Front Hum Neurosci. https://doi.org/10.3389/fnhum.2013.00458
van Heijst B, Geurts HM (2015) Quality of life in autism across the lifespan: a meta-analysis. Autism Int J Res Pract 19(2):158–167. https://doi.org/10.1177/1362361313517053
Velikonja T, Fett A-K, Velthorst E (2019) Patterns of nonsocial and social cognitive functioning in adults with autism spectrum disorder: a systematic review and meta-analysis. JAMA Psychiat 76(2):135–151. https://doi.org/10.1001/jamapsychiatry.2018.3645
Waiter GD, Williams JHG, 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(2):619–625. https://doi.org/10.1016/j.neuroimage.2004.02.029
Wang Y, Olson IR (2018) The original social network: White matter and social cognition. Trends Cogn Sci 22(6):504–516. https://doi.org/10.1016/j.tics.2018.03.005
Wilke M, Holland SK, Altaye M, Gaser C (2008) Template-O-Matic: a toolbox for creating customized pediatric templates. Neuroimage 41(3):903–913. https://doi.org/10.1016/j.neuroimage.2008.02.056
Williams JHG, Whiten A, Suddendorf T, Perrett DI (2001) Imitation, mirror neurons and autism. Neurosci Biobehav Rev 25(4):287–295
Xiao Z, Qiu T, Ke X, Xiao X, Xiao T, Liang F, Zou B, Huang H, Fang H, Chu K, Zhang J, Liu Y (2014) Autism spectrum disorder as early neurodevelopmental disorder: evidence from the brain imaging abnormalities in 2–3 years old toddlers. J Autism Dev Disord 44(7):1633–1640. https://doi.org/10.1007/s10803-014-2033-x
Yang DY-J, Beam D, Pelphrey KA, Abdullahi S, Jou RJ (2016) Cortical morphological markers in children with autism: a structural magnetic resonance imaging study of thickness, area, volume, and gyrification. Mol Autism 7(11):1–14. https://doi.org/10.1186/s13229-016-0076-x
Yaxu Y, Ren Z, Ward J, Jiang Q (2020) Atypical brain structures as a function of gray matter volume (GMV) and gray matter density (GMD) in young adults relating to autism spectrum traits. Front Psychol. https://doi.org/10.3389/fpsyg.2020.00523
Zielinski BA, Prigge MBD, Nielsen JA, Froehlich AL, Abildskov TJ, Anderson JS, Fletcher PT, Zygmunt KM, Travers BG, Lange N, Alexander AL, Bigler ED, Lainhart JE (2014) Longitudinal changes in cortical thickness in autism and typical development. Brain J Neurol 137(6):1799–1812. https://doi.org/10.1093/brain/awu083
Funding
The authors declare that no funds, grants, or other support were received during the preparation of this manuscript.
Author information
Authors and Affiliations
Contributions
FS: Conceptualization, methodology, analysis, software, writing, and editing. KM: Writing and editing. RK: Data collection, conceptualization, methodology, writing, and editing.
Corresponding author
Ethics declarations
Conflict of interest
The authors have no relevant financial or non-financial interests to disclose.
Ethics approval
This study was performed in line with the principles of the Declaration of Helsinki. Approval was granted by the Ethics Committee of the University of Alabama.
Consent to participate
Informed consent was obtained from all individual participants included in the study.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Soylu, F., May, K. & Kana, R. White and gray matter correlates of theory of mind in autism: a voxel-based morphometry study. Brain Struct Funct 228, 1671–1689 (2023). https://doi.org/10.1007/s00429-023-02680-5
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00429-023-02680-5