Features of EEG Reactions in Typically Developing Children and Children with Autism Spectrum Disorder When Observing Movements and Imitating Them

In normotypic children 4-7 years old and their peers with autism spectrum disorders (ASD), an electroencephalogram (EEG) was recorded in situations of observation of imaginary and real actions of the experimenter, as well as when the action was repeated by children. The relevance of the study is due to the assumption of a violation in children with ASD of the functioning of the so-called mirror neuron system (MNS). In both groups of children in these situations, desynchronization of EEG power was detected in individually defined mu-rhythm ranges in the central, frontal and parietal locus, which indicates the activation of MNS. At the same time, in children with ASD in all experimental situations, there was a greater desynchronization of the mu-rhythm in the areas of the lower frontal gyri of the left and right hemispheres (locus F7 and F8), compared with normotypic children. However, in the central locus of the right hemisphere (C4 locus), under the conditions of observation of a real action in children with ASD, there is significantly less desynchronization of the mu-rhythm compared to the norm group, which is probably due to less activation of MNS when perceiving the purposeful actions of another person. The results obtained are important for understanding social behavior disorders in children with ASD and developing methods for their correction.

1. Bozhkova E.D., Balandina O.V., Konovalov A.A. Rasstroistva autisticheskogo spektra: sovremennoe sostoyanie problemy (obzor) [Autism spectrum disorders: the current state of the problem (review)]. Sovremennye tekhnologii v meditsine [Modern technologies in medicine], 2020. Vol. 12, no. 2, pp. 111—120. DOI:10.17691/stm2020.12.2.14 (In Russ.).
2. Bronnikov V.A., Grigorieva M.I., Vaitulevichius N.G., SerebryakovaV.Yu. Early assistance in the system of comprehensive support for children with ASD and their families in the Perm region. Autism and developmental disorders, 2022. Vol. 20, no. 1, pp. 20—28. DOI:10.17759/autdd.2022200103 (In Russ.).
3. Dukhanina O.S. Application of the video modeling method in the formation of social skills in a child with ASD. Autism and developmental disorders. 2023. Vol. 21, no. 3, pp. 54—61. (In Russ.).
4. Kubasova T.S. Programs for supporting children with ASD and developmental disorders, implemented at the State Darwin Museum. Autism and Developmental Disorders, 2022. Vol. 20, no. 2, pp. 13—19. DOI:10.17759/autdd.2022200202 (In Russ.).
5. Larionova E.V. Garakh Zh.V., Zaitseva Yu.S. Myu-ritm v sovremennykh issledovaniyakh: teoreticheskie i metodologicheskie aspekty [Mu-rhythm in modern research: theoretical and methodological aspects]. vyssh. nervn. deyat [Journal of higher nervous activity], 2022. Vol. 72, no. 1, pp. 11—35. (In Russ.).
6. Lebedeva N.N., Zufman A.I., Mal'tsev V.Yu. Sistema zerkal'nykh neironov mozga: klyuch k obucheniyu, formirovaniyu lichnosti i ponimaniyu chuzhogo soznaniya [System of mirror neurons of the brain: the key to learning, personality formation and understanding of someone else's consciousness]. Uspekhi fiziologicheskikh nauk [Successes of physiological Sciences], 2017. Vol. 48, no. 4, pp. 16—28. (In Russ.).
7. Lebedeva N.N., Burkitbaev S.E., Karimova E.D. Aktivatsiya zerkal'noi sistemy mozga zavisit ot sposoba pred"yavleniya stimulov: neposredstvenno eksperimentatorom ili kak videorolik [Activation of the mirror system of the brain depends on the method of presentation of stimuli: directly by the experimenter or as a video]. vyssh. nervn. deyat. im. I.P. Pavlova [Journal. higher. nervous. act. named after I.P. Pavlov], 2020. Vol. 70, no. 4, pp. 460—472. (In Russ.).
8. Morozov S.A., Morozova S.S., Tarasova N.V., Chigrina S.G. Study of relationships within a family with a child with autism and its relationships with the social environment. Autism and Developmental Disorders, 2023. Vol. 21, no. 1, pp. 86—93. DOI:10.17759/autdd.2023210110 (In Russ.).
9. Mikhailova A.A., Orekhova L.S., Dyagileva Yu.O., Mukhtarimova T.I., Pavlenko V.B. Reaktivnost' myu-ritma EEG pri nablyudenii i vypolnenii deistvii u detei rannego vozrasta, imeyushchikh raznyi uroven' razvitiya retseptivnoi rechi [Reactivity of the EEG mu-rhythm during observation and performance of actions in young children with different levels of receptive speech development]. vyssh. nerv. deyat. im. I.P. Pavlova [Journal. higher. nervous. act. named after I.P. Pavlov], 2020. Vol. 70, no. 3, pp. 423—433. (In Russ.).
10. Pavlenko V.B., Orekhova L.S., Portugal'skaya A.A., Mikhailova A.A. Stanovlenie prosotsial'nogo povedeniya v rannem detstvei ego neirofiziologicheskie mekhanizmy. vyssh. nerv. deyat. im. I.P. Pavlova [Journal. higher. nervous. act. namedafterI.P. Pavlov], 2023. Vol. 73, no. 2, pp. 193—213. (In Russ.).
11. Pavlenko V.B., Kaida A.I., Klinkov V.N., Mikhailova A.A., Orekhova L.S., Portugal'skaya A.A. Osobennosti reaktivnosti μ-ritma EEG u detei s rasstroistvami autisticheskogo spektra v situatsiyakh pomogayushchego povedeniya [Features of the reactivity of the μ-rhythm of the EEG in children with autism spectrum disorders in situations of helping behavior]. Vestnik RGMU [Bulletin of RSMU], Vol. 2, pp. 26—32. (In Russ.).
12. Pakhtusova N.A., Akmaev V.A., Nekrasova O.S. An integrated approach to accompanying a child with autism spectrum disorder using the example of a clinical case. Autism and Developmental Disorders, 2023. Vol. 21, no. 2, pp. 42—49. DOI:10.17759/autdd.2023210206 (In Russ.).
13. Stroganova T.A., Orekhova E.V., Galyuta I.A. Neironnye mekhanizmy narushenii orientirovki vnimaniya u detei s rasstroistvom autisticheskogo spectra [Neural mechanisms of attention orientation disorders in children with autism spectrum disorder]. Eksperimental'naya psikhologiya [Experimental psychology], 2015. Vol. 8, no. 3, pp. 7—23. DOI:10.17759/exppsy.2015080302 (In Russ.).
14. Bonini L., Rotunno C., Arcuri E., Gallese V. Mirror neurons 30 years later: implications and applications. Trends Cogn Sci, Vol. 26, no. 9, pp. 767—781.
15. Buard I., Kronberg E., Steinmetz S., Hepburn S., Rojas D.C. Neuromagnetic Beta-Band Oscillations during Motor Imitation in Youth with Autism. Autism Research and Treatment, 2018. Vol. 2018, Article 9035793. DOI:10.1155/2018/9035793
16. Cannon E.N., Simpson E.A., Fox N.A., Vanderwert R.E., Woodward A.L., Ferrari P.F. Relations between infants' emerging reach-grasp competence and event-related desynchronization in EEG. Sci., 2016. Vol. 19, no. 1, pp. 50—62.
17. Chan M.M.Y., Han Y.M.Y. Differential mirror neuron system (MNS) activation during action observation with and without social-emotional components in autism: a meta-analysis of neuroimaging studies. Mol Autism, Vol. 11, no. 1, pp. 72. DOI:10.1186/s13229-020-00374-x
18. Essler, Becher T., Pletti C., Gniewosz B. Paulus M. Longitudinal evidence that infants develop their imitation abilities by being imitated. Current biology, 2023. Vol. 33, no. 21, pp. 4674—4678.
19. Fan Y.T., Decety J., Yang C.Y., Liu J.L., Cheng Y. Unbroken mirror neurons in autism spectrum disorders. J Child Psychol Psychiatry, Vol. 51, no. 9, pp. 981—988. DOI:10.1111/j.1469-7610.2010.02269.x
20. Filippi C., Cannon E.N., Fox N., Thorpe S., Ferrari P.F., Woodward A. Motor system activation predicts goal imitation in 7-month-old infants. Psychol Sci, Vol. 27, no. 5, pp. 675—684.
21. Fox N.A., Bakermans-Kranenburg M.J., Yoo K.H., Bowman L.C., Cannon E.N., Vanderwert R.E., Ferrari P.F., IJzendoorn M.H. Assessing human mirror activity with EEG mu rhythm: A meta-analysis. Psychol Bull, Vol. 142, no. 3, pp. 291—313.
22. Heyes C., Catmur C. What Happened to Mirror Neurons? Perspect Psychol Sci, 2022. Vol. 17, no. 1, pp. 153—168. DOI:1177/1745691621990638
23. Hofsten C., Uhlig H., Adell M., Kochukhova O. How children with autism look at events. Research in Autism Spectrum Disorders, Vol. 3, no. 2009, pp. 556—569.
24. Kemmerer D. What modulates the Mirror Neuron System during action observation?: Multiple factors involving the action, the actor, the observer, the relationship between actor and observer, and the context. Progr Neurobiol, Vol. 205, Article 102128. DOI:10.1016/j.pneurobio.2021.102128
25. Khalil R., Richard T., Thomas B., Ahmed A.M., Ahmed A.K. Social decision making in autism: On the impact of mirror neurons, motor control, and imitative behaviors CNS. Neurosci Ther, Vol. 24, pp. 669—676. DOI:10.1111/cns.13001
26. Kilroy E., Ring P., Hossain A., Nalbach A., Butera C., Harrison L., Jayashankar A., Vigen C., Aziz-Zadeh L., Cermak S.A. Motor performance, praxis, and social skills in autism spectrum disorder and developmental coordination disorder. Autism Res, Vol. 15, no. 9, pp. 1649—1664. DOI:10.1002/aur.2774
27. Koessler L., Maillard L., Benhadid A., Vignal J.P., Felblinger J., Vespignani H., Braun M. Automated cortical projection of EEG sensors: anatomical correlation via the international 10-10 system. Neuroimage, Vol. 46, no. 1, pp. 64—72. DOI:10.1016/j.neuroimage.2009.02.006
28. Köster M., Meyer M. Down and up! Does the mu rhythm index a gating mechanism in the developing motor system? Dev Cogn Neurosci, Vol. 60, Article 101239. DOI:10.1016/j.dcn.2023.101239
29. Marshall P.J., Meltzoff A.N. Neural mirroring systems: Exploring the EEG mu rhythm in human infancy. Developmental Cognitive Neuroscience, Vol. 1, pp. 110—123.
30. Nyström P., Ljunghammar T., Rosander K., Hofsten C. Using mu rhythm desynchronization to measure mirror neuron activity in infants. Developmental Science, Vol. 14, pp. 327—335.
31. Oberman L.M., Hubbard E.M., McCleery J.P., Altschuler E.L., Ramachandran V.S., Pineda J.A. EEG evidence for mirror neuron dysfunction in autism spectrum disorders. Cognitive Brain Research, Vol. 24, no. 2, pp. 190—198.
32. Saby J.N., Meltzoff A.N., Marshall P.J. Infants’ somatotopic neural responses to seeing human actions: I’ve got you under my skin. PLoS One, Vol. 8, no. 10, pp. e77905. DOI:10.1371/journal.pone.0077905
33. Sotoodeh M.S., Taheri-Torbati H., Sohrabi M., Ghoshuni M. Perception of biological motions is preserved in people with autism spectrum disorder: electrophysiological and behavioural evidences. J Intellect Disabil Res, Vol. 63, no. 1, pp. 72—84. DOI:10.1111/jir.12565
34. Thorpe S.G., Cannon E.N., Fox N.A. Spectral and source structural development of mu and alpha rhythms from infancy through adulthood. Neurophysiol., 2016. Vol. 127, no. 1, pp. 254—269.
35. Wadsworth H.M., Maximo J.O., Donnelly R.J., Kana R.K. Action simulation and mirroring in children with autism spectrum disorders. Behav Brain Res, Vol. 2, no. 341, pp. 1—8. DOI:10.1016/j.bbr.2017.12.012
36. Warreyn P., Ruysschaert L., Wiersema R., Handl A., Pattyn G., Roeyers H. Infants’ mu suppression during the observation of real and mimicked goal-directed actions. Developmental Science, Vol. 16, no. 2, pp. 173—185.
37. Williams J.H.G., Whiten A., Suddendorf T., Perrett D.I. Imitation, mirror neurons and autism. Biobehav. Rev., 2001. Vol. 25, pp. 287—295.
38. Yates L., Hobson H. Continuing to look in the mirror: A review of neuroscientific evidence for the broken mirror hypothesis, EP-M model and STORM model of autism spectrum conditions. Autism, Vol. 24, no. 8, pp. 1945—1959. DOI:10.1177/1362361320936945