Sex Differences in Spatiotemporal Consistency and Effective Connectivity of the Precuneus in Autism Spectrum Disorder

Overview

Journal J Autism Dev Disord

Publisher Springer

Date 2024 Dec 28

PMID 39731683

Authors

Le Gao

Tengda Zhang

Yigeng Zhang

Junfeng Liu

Xiaonan Guo

Affiliations

Soon will be listed here.

Abstract

Autism spectrum disorder (ASD) has been reported to exhibit altered local functional consistency. However, previous studies mainly focused on male samples and explored the temporal consistency in the ASD brain ignoring the spatial consistency. In this study, FOur-dimensional Consistency of local neural Activities (FOCA) analysis was used to investigate the sex differences of local spatiotemporal consistency of spontaneous brain activity in ASD. This study used resting-state functional magnetic resonance imaging data from the Autism Brain Imaging Data Exchange database, including 64 males/64 females with ASD and 64 male/64 female neurotypical controls (NCs). Two-way analysis of variance was performed to ascertain diagnosis-by-sex interaction effects on whole brain FOCA maps. Moreover, granger causal analysis was used to investigate effective connectivity between the brain regions with interaction effects and the whole-brain in ASD. Significant diagnosis-by-sex interaction effects on FOCA were observed in the bilateral precuneus (PCUN), bilateral medial prefrontal cortex and right dorsolateral superior frontal gyrus. Specifically, FOCA was significantly increased in males with ASD but decreased in females with ASD in the PCUN compared with the sex-matched NC group. In addition, the lack of sex differences in the causal influences from the bilateral anterior cingulate cortex/medial prefrontal cortex to the PCUN was observed in ASD. Our results reveal altered sex differences in the spatiotemporal consistency of spontaneous brain activity and functional interaction of the anterior and posterior default mode network (DMN) in ASD, highlighting the critical role of the DMN in the sex heterogeneity of ASD.

References

Alaerts K, Swinnen S, Wenderoth N . Sex differences in autism: a resting-state fMRI investigation of functional brain connectivity in males and females. Soc Cogn Affect Neurosci. 2016; 11(6):1002-16. PMC: 4884321. DOI: 10.1093/scan/nsw027. View

Assaf M, Jagannathan K, Calhoun V, Miller L, Stevens M, Sahl R . Abnormal functional connectivity of default mode sub-networks in autism spectrum disorder patients. Neuroimage. 2010; 53(1):247-56. PMC: 3058935. DOI: 10.1016/j.neuroimage.2010.05.067. View

Beacher F, Minati L, Baron-Cohen S, Lombardo M, Lai M, Gray M . Autism attenuates sex differences in brain structure: a combined voxel-based morphometry and diffusion tensor imaging study. AJNR Am J Neuroradiol. 2011; 33(1):83-9. PMC: 6345364. DOI: 10.3174/ajnr.A2880. View

Bejerot S, Eriksson J, Bonde S, Carlstrom K, Humble M, Eriksson E . The extreme male brain revisited: gender coherence in adults with autism spectrum disorder. Br J Psychiatry. 2012; 201:116-23. DOI: 10.1192/bjp.bp.111.097899. View

Carlisi C, Norman L, Lukito S, Radua J, Mataix-Cols D, Rubia K . Comparative Multimodal Meta-analysis of Structural and Functional Brain Abnormalities in Autism Spectrum Disorder and Obsessive-Compulsive Disorder. Biol Psychiatry. 2016; 82(2):83-102. DOI: 10.1016/j.biopsych.2016.10.006. View

Cavanna A . The precuneus and consciousness. CNS Spectr. 2007; 12(7):545-52. DOI: 10.1017/s1092852900021295. View

Cavanna A, Trimble M . The precuneus: a review of its functional anatomy and behavioural correlates. Brain. 2006; 129(Pt 3):564-83. DOI: 10.1093/brain/awl004. View

Chen X, Jiang Y, Chen L, He H, Dong L, Hou C . Altered Hippocampo-Cerebello-Cortical Circuit in Schizophrenia by a Spatiotemporal Consistency and Causal Connectivity Analysis. Front Neurosci. 2017; 11:25. PMC: 5277003. DOI: 10.3389/fnins.2017.00025. View

Courchesne E, Pierce K . Brain overgrowth in autism during a critical time in development: implications for frontal pyramidal neuron and interneuron development and connectivity. Int J Dev Neurosci. 2005; 23(2-3):153-70. DOI: 10.1016/j.ijdevneu.2005.01.003. View

10.

Dajani D, Uddin L . Local brain connectivity across development in autism spectrum disorder: A cross-sectional investigation. Autism Res. 2015; 9(1):43-54. PMC: 4673031. DOI: 10.1002/aur.1494. View

11.

Das S, Zomorrodi R, Enticott P, Kirkovski M, Blumberger D, Rajji T . Resting state electroencephalography microstates in autism spectrum disorder: A mini-review. Front Psychiatry. 2022; 13:988939. PMC: 9752812. DOI: 10.3389/fpsyt.2022.988939. View

12.

Di Martino A, Yan C, Li Q, Denio E, Castellanos F, Alaerts K . The autism brain imaging data exchange: towards a large-scale evaluation of the intrinsic brain architecture in autism. Mol Psychiatry. 2013; 19(6):659-67. PMC: 4162310. DOI: 10.1038/mp.2013.78. View

13.

Dong L, Luo C, Cao W, Zhang R, Gong J, Gong D . Spatiotemporal consistency of local neural activities: A new imaging measure for functional MRI data. J Magn Reson Imaging. 2014; 42(3):729-36. DOI: 10.1002/jmri.24831. View

14.

Guo X, Zhang X, Liu J, Zhai G, Zhang T, Zhou R . Resolving heterogeneity in dynamics of synchronization stability within the salience network in autism spectrum disorder. Prog Neuropsychopharmacol Biol Psychiatry. 2024; 131:110956. DOI: 10.1016/j.pnpbp.2024.110956. View

15.

Harrop C, Jones D, Zheng S, Nowell S, Boyd B, Sasson N . Circumscribed Interests and Attention in Autism: The Role of Biological Sex. J Autism Dev Disord. 2018; 48(10):3449-3459. PMC: 6267775. DOI: 10.1007/s10803-018-3612-z. View

16.

Hull L, Mandy W, Petrides K . Behavioural and cognitive sex/gender differences in autism spectrum condition and typically developing males and females. Autism. 2017; 21(6):706-727. DOI: 10.1177/1362361316669087. View

17.

Hull L, Lai M, Baron-Cohen S, Allison C, Smith P, Petrides K . Gender differences in self-reported camouflaging in autistic and non-autistic adults. Autism. 2019; 24(2):352-363. DOI: 10.1177/1362361319864804. View

18.

Igelstrom K, Graziano M . The inferior parietal lobule and temporoparietal junction: A network perspective. Neuropsychologia. 2017; 105:70-83. DOI: 10.1016/j.neuropsychologia.2017.01.001. View

19.

Jiao Q, Lu G, Zhang Z, Zhong Y, Wang Z, Guo Y . Granger causal influence predicts BOLD activity levels in the default mode network. Hum Brain Mapp. 2010; 32(1):154-61. PMC: 6870036. DOI: 10.1002/hbm.21065. View

20.

Jung M, Mody M, Saito D, Tomoda A, Okazawa H, Wada Y . Sex Differences in the Default Mode Network with Regard to Autism Spectrum Traits: A Resting State fMRI Study. PLoS One. 2015; 10(11):e0143126. PMC: 4658035. DOI: 10.1371/journal.pone.0143126. View