Electroencephalographic microstate evidence of visual network hyperactivation in children with autism spectrum disorder

Abstract

Visual hypersensitivity, including extreme visual sensitivity and avoidance response, is one of the main features of autism spectrum disorder (ASD). It has been proposed to be an effect of aberrant sensory integration and impaired functional brain networks. EEG microstates reflect brain activity fluctuations and offer an innovative way to study the neurological framework of visual hypersensitivity in ASD. The study included 54 children aged 6-9 years: 27 with ASD and 27 typically developing (TD) peers matched for age and gender. 64-channel EEG data were recorded while the subjects were at rest with their eyes open. The duration, occurrence, and coverage of Microstate B were substantially higher in children with ASD than in the TD group (all p < 0.05), suggesting increased stability and activation of the visual network and impaired cross-network resource allocation. ASD participants showed increased transitions from D to B (p = 0.003) and A to B (p = 0.022), indicating more frequent switching to the visual network and excessive visual attention allocation, which maybe the potential neural mechanism of visual hypersensitivity in ASD children. These results indicate disrupted functional network dynamics and increased visual network dominance in ASD, offering insights into the neurological basis of visual hypersensitivity.

Keywords

autism spectrum disorder / EEG / microstate / resting-state EEG / visual networks

References

[1] Bai Y, Yu M, Li Y. Dynamic neural patterns of human emotions in virtual reality: insights from EEG microstate analysis. Brain Sci. 2024; 14(2):113. https://doi.org/10.3390/brainsci14020113

[2] Yao MH, Meng MZ, Yang XY, et al. POSH regulates assembly of the NMDAR/PSD-95/Shank complex and synaptic function. Cell Rep. 2022; 39(1): 21. https://doi.org/10.1016/j.celrep.2022.110642

[3] Rylaarsdam L, Guemez-Gamboa A. Genetic causes and modifiers of autism spectrum disorder. Front Cell Neurosci. 2019; 13: 15. https://doi.org/10.3389/fncel.2019.00385

[4] Marco EJ, Hinkley LB, Hill SS, Nagarajan SS. Sensory processing in autism: a review of neurophysiologic findings. Pediatr Res. 2011; 69(5 Pt 2): 48r-54r. https://doi.org/10.1203/pdr.0b013e3182130c54

[5] Jones EJH, Dawson G, Webb SJ. Sensory hypersensitivity predicts enhanced attention capture by faces in the early development of ASD. Developmental cognitive neuroscience. 2018; 29: 11-20. https://doi.org/10.1016/j.dcn.2017.04.001

[6] Lassalle A, Åsberg Johnels J, ZüRCHER NR, et al. Hypersensitivity to low intensity fearful faces in autism when fixation is constrained to the eyes. 2017, 38(12): 5943-5957.

[7] Wang S, Jiang M, Duchesne Xavier M, et al. Atypical visual saliency in autism spectrum disorder quantified through model-based eye tracking. Neuron. 2015; 88(3): 604-616. https://doi.org/10.1016/j.neuron.2015.09.042

[8] Jolliffe T, Baron-Cohen S. Are people with autism and Asperger syndrome faster than normal on the embedded figures test? J Child Psychol Psychiatry Allied Discip. 1997; 38(5): 527-534.

[9] Khanna A, Pascual-Leone A, Michel CM, Farzan F. Microstates in resting-state EEG: current status and future directions. Neurosci Biobehav Rev. 2015; 49: 105-113. https://doi.org/10.1016/j.neubiorev.2014.12.010

[10] Jia H, Yu D. Aberrant intrinsic brain activity in patients with autism spectrum disorder: insights from EEG microstates. Brain Topogr. 2019; 32(2): 295-303. https://doi.org/10.1007/s10548-018-0685-0

[11] D'Croz-Baron DF, Baker M, Michel CM, Karp T. EEG microstates analysis in young adults with autism spectrum disorder during resting-state. Frontiers in human neuroscience. 2019; 13:173. https://doi.org/10.3389/fnhum.2019.00173

[12] Anderson AJ, Perone S. Developmental change in the resting state electroencephalogram: insights into cognition and the brain. Brain Cognit. 2018; 126: 40-52. https://doi.org/10.1016/j.bandc.2018.08.001

[13] Sadik EŞ, Saraoğlu HM, Kabay SC, et al. Comparison of different data augmentation methods with an experimental EEG dataset. In: proceedings of the 2021 13th International Conference on Electrical and Electronics Engineering (ELECO); 2021. F 25-27 Nov. 2021.

[14] Lehmann D, Pascual-Marqui RD, Michel C. EEG microstates. Scholarpedia. 2009; 4(3):7632. https://doi.org/10.4249/scholarpedia.7632

[15] Britz J, Van De Ville D, Michel CM. BOLD correlates of EEG topography reveal rapid resting-state network dynamics. Neuroimage. 2010; 52(4): 1162-1170. https://doi.org/10.1016/j.neuroimage.2010.02.052

[16] Bagdasarov A, Roberts K, BréCHET L, Brunet D, Michel CM, Gaffrey MS. Spatiotemporal dynamics of EEG microstates in four-to eight-year-old children: age- and sex-related effects. Developmental cognitive neuroscience. 2022; 57:101134. https://doi.org/10.1016/j.dcn.2022.101134

[17] Mottron L, Dawson M, SoulièRES I, Hubert B, Burack J. Enhanced perceptual functioning in autism: an update, and eight principles of autistic perception. J Autism Dev Disord. 2006; 36(1): 27-43. https://doi.org/10.1007/s10803-005-0040-7

[18] Zanesco AP, King BG, Skwara AC, Saron CD. Within and between-person correlates of the temporal dynamics of resting EEG microstates. Neuroimage. 2020; 211:116631. https://doi.org/10.1016/j.neuroimage.2020.116631

[19] Portnova G, Martynova O. Macro- and microstates of resting-state EEG in children with low-functioning autism. Advances in Neurodevelopmental Disorders. 2024; 8(4): 559-573. https://doi.org/10.1007/s41252-023-00374-x

[20] Takarae Y, Zanesco A, Keehn B, Chukoskie L, Müller R, Townsend J. EEG microstates suggest atypical resting-state network activity in high-functioning children and adolescents with autism spectrum development. Dev Sci. 2022; 25(4):e13231. https://doi.org/10.1111/desc.13231

[21] Zhang K, Yuan Y, Chen J, Wang G, Chen Q, Luo M. Eye tracking research on the influence of spatial frequency and inversion effect on facial expression processing in children with autism spectrum disorder. Brain Sci. 2022; 12(2):283. https://doi.org/10.3390/brainsci12020283

[22] Kale S, Williams ME, Deans MR. Getting connected: pathfinding and synaptogenesis in neural development, evolution, and disease. Dev Dyn. 2023; 252(1): 7-9. https://doi.org/10.1002/dvdy.558

[23] Ameis SH, Lerch JP, Taylor MJ, et al. A diffusion tensor imaging study in children with ADHD, autism spectrum disorder, OCD, and matched controls: distinct and non-distinct white matter disruption and dimensional brain-behavior relationships. Am J Psychiatr. 2016; 173(12): 1213-1222. https://doi.org/10.1176/appi.ajp.2016.15111435

[24] Shi Q, Li Y, Wang J, et al. Correlation between brain networks functional connectivity in resting state and executive function in patients with different degrees of cognitive impairment associated with white matter lesions. Chinese Journal of Behavioral Medicine and Brain Science. 2022; 31(3): 220-228. https://doi.org/10.3760/cma.j.cn371468-20211001-00568

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2025 The Author(s). Journal of Intelligent Medicine published by John Wiley & Sons Australia, Ltd on behalf of Tianjin University.