Inter-brain synchrony to delineate the social impairment in autism spectrum disorder: a systematic review on hyperscanning studies

Abstract

Autism spectrum disorder (ASD) is a common neurodevelopmental disorder marked by significant deficits in social interaction and restricted repetitive behaviors. Despite rigorous research efforts, the early and effective diagnosis and intervention of ASD remain challenging, due primarily to its considerable heterogeneity and complex neurobiological underpinnings. Traditional neuroimaging techniques have largely focused on individual brain responses to social stimuli, often overlooking the critical interactive dynamics that contribute to social impairments in individuals with ASD. This review explored hyperscanning, an innovative neuroimaging approach that features simultaneous recording of brain activity across multiple individuals, to enhance our understanding of the neural mechanisms underlying social difficulties in ASD. By searching published articles conducted between 2000 and 2024, we found eight empirical studies conducted between 2012 and 2024, which employed various brain imaging techniques. We analyzed and summarized participant demographics, experimental designs, and key outcomes, with a particular focus on inter-brain synchrony (IBS) as a measure of social engagement and the quality of interpersonal interactions. Our review identified specific patterns of neural synchrony that correlate with the severity of ASD symptoms. Furthermore, we critically evaluated the limitations of current studies and proposed future research directions, highlighting the need for more nuanced hyperscanning methodologies. Such advancements could significantly deepen our understanding of social impairments in ASD and inform targeted intervention strategies. This comprehensive review aimed to assess the potential of hyperscanning techniques to propel progress in ASD research and intervention, ultimately contributing to more effective clinical practices.

Keywords

autism spectrum disorder / social impairment / inter-brain synchrony / hyperscanning / brain imaging

Author contributions

Shuo Guan (Conceptualization), Dalin Yang (Conceptualization), Dongyun Li (Conceptualization), Qiong Xu (Conceptualization), Yingchun Zhang (Conceptualization), and Rihui Li (Conceptualization, Funding acquisition, Supervision, Writing - review & editing).

Conflict of interest statement

The authors declare no competing interests.

Acknowledgments

This research was funded by the National Natural Science Foundation of China (Reference: 82301743), the Science and Technology Development Fund of the Macao SAR (0010/2023/ITP1, 0016/2024/RIB1), and the University of Macau (SRG2023-00015-ICI, MYRG-GRG2024-00296-ICI, and MYRG-CRG2024-00022-ICI).

References

[1] Acquadro MAS, Congedo M, De Riddeer D. (2016) Music performance as an experimental approach to hyperscanning studies. Front Hum Neurosci. 10:242. https://doi.org/10.3389/fnhum.2016.00242.

[2] Alderson TH, Bokde ALW, Kelso JAS, et al. (2018) Metastable neural dynamics in Alzheimer's disease are disrupted by lesions to the structural connectome. Neuroimage. 183:438-55.

[3] American Psychiatric Association, & American Psychiatric Association(Eds.). (2013) Diagnostic and statistical manual of mental disorders: DSM-5DSM-5 (5th ed). Washington, DC: American Psychiatric Association.

[4] Ashwin C, Baron-Cohen S, Wheelwright S, et al. (2007) Differential activation of the amygdala and the ‘social brain’ during fearful face-processing in Asperger Syndrome. Neuropsychologia. 45(1):2-14.

[5] Babiloni F, Astolfi L. (2014) Social neuroscience and hyperscanning techniques: past, present and future. Neurosci Biobehav Rev. 44:76-93.

[6] Baker JK, Fenning RM, Howland MA, et al. (2015) Brief Report: a pilot study of parent-child biobehavioral aynchrony in autism spectrum disorder. J Autism Dev Disord. 45(12):4140-6.

[7] Bilek E, Zeidman P, Kirsch P, et al. (2022) Directed coupling in multi-brain networks underlies generalized synchrony during social exchange. Neuroimage. 252:119038.

[8] Bookheimer SY, Wang AT, Scott A, et al. (2008) Frontal contributions to face processing differences in autism: evidence from fMRI of inverted face processing. J Int Neuropsychol Soc. 14(6):922-32.

[9] Chang Y-C, Locke J. (2016) A systematic review of peer-mediated interventions for children with autism spectrum disorder. Res Autism Spectrum Disord. 27:1-10.

[10] Chen B, Jiang L, Lu G, et al. (2023) Altered dynamic network interactions in children with ASD during face recognition revealed by time-varying EEG networks. In Cereb Cortex. 33:11170-80.

[11] Chen GK, Kono N, Geschwind DH, et al. (2006) Quantitative trait locus analysis of nonverbal communication in autism spectrum disorder. Mol Psychiatry. 11(2):214-20.

[12] Chiang C-H, Soong W-T, Lin T-L, et al. (2008) Nonverbal communication skills in young children with autism. J Autism Dev Disord. 38(10):1898-906.

[13] Clauser P, Ding Y, Chen EC, et al. (2021) Parenting styles, parenting stress, and behavioral outcomes in children with autism. School Psychol Int. 42(1):33-56.

[14] Collins AGE, Frank MJ. (2018) Within- and across-trial dynamics of human EEG reveal cooperative interplay between reinforcement learning and working memory. Proc Natl Acad Sci USA. 115(10):2502-7.

[15] Corbett BA, Carmean V, Ravizza S, et al. (2009) A functional and structural study of emotion and face processing in children with autism. Psychiatry Res Neuroimaging. 173(3):196-205.

[16] Crowell JA, Keluskar J, Gorecki A. (2019) Parenting behavior and the development of children with autism spectrum disorder. Compr Psychiatry. 90:21-9.

[17] Cui X, Bryant DM, Reiss AL. (2012) NIRS-based hyperscanning reveals increased interpersonal coherence in superior frontal cortex during cooperation. Neuroimage. 59(3):2430-7.

[18] de Leeuw A, Happé F, Hoekstra RA. (2020) A conceptual framework for understanding the cultural and contextual factors on autism across the Globe. Autism Res. 13(7):1029-50.

[19] Du B, Zhang W, Chen L, et al. (2024) Higher or lower? Interpersonal behavioral and neural synchronization of movement imitation in autistic children. Autism Res. 17(9):1876-901.

[20] Duan X, Chen H. (2022) Mapping brain functional and structural abnormities in autism spectrum disorder: moving toward precision treatment. Psychoradiology. 2(3):78-85.

[21] Dunsmore JC, Ashley RA, Zhou Y, et al. (2019) Marching to the beat of your own drum?: a proof-of-concept study assessing physiological linkage in Autism Spectrum Disorder. Biol Psychol. 144:37-45.

[22] Eggebrecht AT, White BR, Ferradal SL, et al. (2012) A quantitative spatial comparison of high-density diffuse optical tomography and fMRI cortical mapping. Neuroimage. 61(4):1120-8.

[23] Filmer HL, Fox A, Dux PE. (2019) Causal evidence of right temporal parietal junction involvement in implicit Theory of Mind processing. Neuroimage. 196:329-36.

[24] Freeman S, Kasari C. (2013) Parent-child interactions in autism: characteristics of play. Autism. 17(2):147-61.

[25] Grinsted A, Moore JC, Jevrejeva S. (2004) Application of the cross wavelet transform and wavelet coherence to geophysical time series. Nonlin Processes Geophys. 11(5/6):561-6.

[26] Guo X, Zhai G, Liu J, et al. (2022) Inter-individual heterogeneity of functional brain networks in children with autism spectrum disorder. Molecular Autism. 13(1):52.

[27] Hakim U, De Felice S, Pinti P, et al. (2023) Quantification of inter-brain coupling: a review of current methods used in haemodynamic and electrophysiological hyperscanning studies. Neuroimage. 280:120354.

[28] Hernandez LM, Rudie JD, Green SA, et al. (2015) Neural signatures of autism spectrum disorders: insights into brain network dynamics. Neuropsychopharmacol. 40(1): 171-89.

[29] Hirsch J, Zhang X, Noah JA, et al. (2022) Neural correlates of eye contact and social function in autism spectrum disorder. PLoS One. 17(11):e0265798.

[30] Hu Y, Hu Y, Li X, et al. (2017) Brain-to-brain synchronization across two persons predicts mutual prosociality. Soc Cognit Affect Neurosci. 12(12):1835-44.

[31] Hyde DC, Simon CE, Ting F, et al. (2018) Functional organization of the temporal-parietal junction for theory of mind in preverbal infants: a near-infrared spectroscopy study. J Neurosci. 38(18):4264-74.

[32] Jellema T, Lorteije J, van Rijn S, et al. (2009) Involuntary interpretation of social cues is compromised in autism spectrum disorders. Autism Res. 2(4):192-204.

[33] Jurek L, Leadbitter K, Falissard B, et al. (2023) Parental experience of parent-mediated intervention for children with ASD: a systematic review and qualitative evidence synthesis. Autism. 27(3):647-66.

[34] Kelly AB, Garnett MS, Attwood T, et al. (2008) Autism spectrum symptomatology in children: the impact of family and peer relationships. J Abnorm Child Psychol. 36(7):1069-81.

[35] Kelsen BA, Sumich A, Kasabov N, et al. (2022) What has social neuroscience learned from hyperscanning studies of spoken communication? A systematic review. Neurosci Biobehav Rev. 132:1249-62.

[36] Key AP, Yan Y, Metelko M, et al. (2022a) Greater social competence is associated with higher interpersonal neural synchrony in adolescents with autism. Front Human Neurosci. 15.

[37] Key AP, Yan Y, Metelko M, et al. (2022b) Greater social competence is associated with higher interpersonal neural synchrony in adolescents with autism. Front Hum Neurosci. 15:15.

[38] Kleinhans NM, Richards T, Johnson LC, et al. (2011) fMRI evidence of neural abnormalities in the subcortical face processing system in ASD. Neuroimage. 54(1):697-704.

[39] Koike T, Sumiya M, Nakagawa E, et al. (2019) What makes eye contact special? Neural substrates of on-line mutual eye-gaze: a hyperscanning fMRI study. Eneuro. 6(1): ENEURO.0284-0218.2019.

[40] Konrad K, Gerloff C, Kohl SH, et al. (2024) Interpersonal neural synchrony and mental disorders: unlocking potential pathways for clinical interventions. Front Neurosci. 18:1286130. https://doi.org/10.3389/fnins.2024.1286130.

[41] Kruppa JA, Reindl V, Gerloff C, et al. (2021) Brain and motor synchrony in children and adolescents with ASD-a fNIRS hyperscanning study. Soc Cognit Affect Neurosci. 16(1-2):103-16. https://doi.org/10.1093/scan/nsaa092.

[42] Lamb ME, Lewis C. (2011) The role of parent-child relationships in child development. In Social and Personality Development. Psychology Press. 259-308.

[43] Lau WKW, Leung M-K, Poon K, et al. (2024) Early diagnosis of autism spectrum disorder using structural connectivity biomarker. Psychoradiology. 4:kkae004.

[44] Léné P, Karran AJ, Labonté-Lemoyne E, et al., (2020) Wavelet transform coherence:an innovative method to investigate social interaction in NeuroIS. In Davis F. D., Riedl R., vom Brocke J., Léger P.-M., Randolph A., Fischer T.(Eds.), Information Systems and Neuroscience. Berlin: Springer International Publishing, 147-54.

[45] Li R, Hosseini H, Saggar M, et al. (2023) Current opinions on the present and future use of functional near-infrared spectroscopy in psychiatry. Neurophoton. 10(1):013505. https://doi.org/10.1117/1.NPh.10.1.013505.

[46] Li R, Mayseless N, Balters S, et al. (2021) Dynamic inter-brain synchrony in real-life inter-personal cooperation: a functional near-infrared spectroscopy hyperscanning study. Neuroimage. 238:118263.

[47] Lord C, Brugha TS, Charman T, et al. (2020) Autism spectrum disorder. Nat Rev Dis Primers. 6(1):1-23.

[48] Neuhaus E, Lowry SJ, Santhosh M, et al. (2021) Resting state EEG in youth with ASD: age, sex, and relation to phenotype. J Neurodevelop Disord. 13(1):33.

[49] Page MJ, McKenzie JE, Bossuyt PM, et al. (2021) The PRISMA 2020 statement: an updated guideline for reporting systematic reviews. Int J Surg. 88:105906.

[50] Pan Y, Cheng X, Zhang Z, et al. (2017) Cooperation in lovers: an fNIRS-based hyperscanning study. Hum Brain Mapp. 38(2):831-41.

[51] Pan Y, Wen Y, Wang Y, et al. (2023) Interpersonal coordination in schizophrenia: a concise update on paradigms, computations, and neuroimaging findings. Psychoradiology. 3:kkad002.

[52] Pan Y., Novembre G., Song B, et al. (2018) Interpersonal synchronization of inferior frontal cortices tracks social interactive learning of a song. NeuroImage. 183:280-90.

[53] Perepa P. (2014) Cultural basis of social ‘deficits’ in autism spectrum disorders. Eur J Special Needs Edu. 29(3):313-26.

[54] Quiñones‐Camacho LE, Fishburn FA, Belardi K, et al. (2021) Dysfunction in interpersonal neural synchronization as a mechanism for social impairment in autism spectrum disorder. Autism Res. 14(8):1585-96.

[55] Quiñones‐Camacho LE, Fishburn FA, Camacho MC, et al. (2020) Parent-child neural synchrony: a novel approach to elucidating dyadic correlates of preschool irritability. Child Psychology Psychiatry. 61(11):1213-23.

[56] Reindl V, Gerloff C, Scharke W, et al. (2018) Brain-to-brain synchrony in parent-child dyads and the relationship with emotion regulation revealed by fNIRS-based hyperscanning. Neuroimage. 178:493-502.

[57] Reindl V, Wass S, Leong V, et al. (2022) Multimodal hyperscanning reveals that synchrony of body and mind are distinct in mother-child dyads. Neuroimage. 251:118982.

[58] Rogge N, Janssen J. (2019) The economic costs of autism spectrum disorder: a literature review. J Autism Dev Disord. 49(7):2873-900.

[59] Rommelse N, Buitelaar JK, Hartman CA. (2017) Structural brain imaging correlates of ASD and ADHD across the lifespan: a hypothesis-generating review on developmental ASD-ADHD subtypes. J Neural Transm. 124(2):259-71.

[60] Senju A, Johnson MH. (2009) Atypical eye contact in autism: models, mechanisms and development. Neurosci Biobehav Rev. 33(8):1204-14.

[61] Tanabe HC, Kosaka H, Saito DN, et al. (2012) Hard to”tune in”: neural mechanisms of live face-to-face interaction with high-functioning autistic spectrum disorder. Front. Hum. Neurosci. 6:268. https://doi.org/10.3389/fnhum.2012.00268.

[62] Tang Y., Wang C., Liu X, et al. (2023) Children with autism spectrum disorder perform comparably to their peers in a parent-child cooperation task. Experimental Brain Research. 241(7):1905-17.

[63] Wan L, Li Y, Zhu G, et al. (2024) Multimodal investigation of dynamic brain network alterations in autism spectrum disorder: linking connectivity dynamics to symptoms and developmental trajectories. Neuroimage. 302:120895.

[64] Wang Q, Han Z, Hu X, et al. (2020) Autism symptoms modulate interpersonal neural synchronization in children with autism spectrum disorder in cooperative interactions. Brain Topogr. 33(1):112-22.

[65] Yang M-T, Fan H-C, Lee H-J, et al. (2024) Inter-subject gamma oscillation synchronization as a biomarker of abnormal processing of social interaction in ADHD. Sci Rep. 14(1):17924. https://doi.org/10.1038/s41598-024-68905-7.

[66] Zeidan J, Fombonne E, Scorah J, et al. (2022) Global prevalence of autism: a systematic review update. Autism Res. 15(5):778-90.

[67] Zhao Q, Zhao W, Lu C, et al. (2024) Interpersonal neural synchronization during social interactions in close relationships: a systematic review and meta-analysis of fNIRS hyperscanning studies. Neurosci Biobehav Rev. 158:105565.

[68] Zhou H, Xu X, Yan W, et al. (2020) Prevalence of autism spectrum disorder in China: a nationwide multi-center population-based study among children aged 6 to 12 years. Neurosci Bull. 36(9):961-71.

[69] Zhu G, Li Y, Wan L, et al. (2024) Divergent electroencephalogram resting-state functional network alterations in subgroups of autism spectrum disorder: a symptom-based clustering analysis. Cereb Cortex. 34(1):bhad413.