Abstract
This research investigates an efficient strategy for early detection and intervention of attention-deficit hyperactivity disorder (ADHD) in children. ADHD is a neurodevelopmental condition characterized by inattention and hyperactivity/impulsivity symptoms, which can significantly impact a child’s daily life. This study employed two distinct brain functional connectivity measurements to assess our approach across various local graph features. Six common classifiers are employed to distinguish between children with ADHD and healthy control. Based on the phase-based analysis, the study proposes two biomarkers that differentiate children with ADHD from healthy control, with a remarkable accuracy of 99.174%. Our findings suggest that subgraph centrality of phase-lag index brain connectivity within the beta and delta frequency bands could be a promising biomarker for ADHD diagnosis. Additionally, we identify node betweenness centrality of inter-site phase clustering connectivity within the delta and theta bands as another potential biomarker that warrants further exploration. These biomarkers were validated using a t-statistical test and yielded a p-value of under 0.05, which approved their significant difference in these two groups. Suggested biomarkers have the potential to improve the accuracy of ADHD diagnosis and could help identify effective intervention strategies for children with the condition.
Similar content being viewed by others
Data availability
The utilized dataset can be accessed from the IEEE DataPort repository at the following address: https://doi.org/10.21227/rzfh-zn36.
References
Leffa DT, Caye A, Rohde LA (2022) ADHD in children and adults: diagnosis and prognosis. In: Stanford SC, Sciberras E (eds) New discoveries in the behavioral neuroscience of attention-deficit hyperactivity disorder. Current topics in behavioral neurosciences, vol 57. Springer, Cham, pp 1–18. https://doi.org/10.1007/7854_2022_329
Tsakou V, Drigas A (2022) Early detection of preschool children with ADHD and the role of mobile apps and AI. Tech Soc Sci J 30:127–137. https://doi.org/10.47577/tssj.v30i1.6266
Peasgood T, Bhardwaj A, Biggs K, Brazier JE, Coghill D, Cooper CL, Daley D, De Silva C, Harpin V, Hodgkins P, Nadkarni A, Setyawan J, Sonuga-Barke EJS (2016) The impact of ADHD on the health and well-being of ADHD children and their siblings. Eur Child Adolesc Psychiatry 25(11):1217–1231. https://doi.org/10.1007/s00787-016-0841-6
Feil EG, Small JW, Seeley JR, Walker HM, Golly A, Frey A, Forness SR (2016) Early intervention for preschoolers at risk for attention-deficit/hyperactivity disorder: preschool first step to success. Behav Disord 41(2):95–106. https://doi.org/10.17988/0198-7429-41.2.95
Fraga González G, Smit DJA, van der Molen MJW, Tijms J, Jan Stam C, de Geus EJC, van der Molen MW (2018) EEG resting state functional connectivity in adult dyslexics using phase lag index and graph analysis. Front Hum Neurosci. https://doi.org/10.3389/fnhum.2018.00341
Ismail LE, Karwowski W (2020) A graph theory-based modeling of functional brain connectivity based on EEG: a systematic review in the context of neuroergonomics. IEEE Access 8:155103–155135. https://doi.org/10.1109/ACCESS.2020.3018995
Ekhlasi A, Nasrabadi AM, Mohammadi M (2022) Analysis of EEG brain connectivity of children with ADHD using graph theory and directional information transfer. Biomed Eng/Biomed Tech. https://doi.org/10.1515/bmt-2022-0100
Ahmadlou M, Adeli H (2011) Fuzzy synchronization likelihood with application to attention-deficit/hyperactivity disorder. Clin EEG Neurosci 42(1):6–13. https://doi.org/10.1177/155005941104200105
Ahmadlou M, Adeli H (2011) Functional community analysis of brain: a new approach for EEG-based investigation of the brain pathology. Neuroimage 58(2):401–408. https://doi.org/10.1016/j.neuroimage.2011.04.070
Alim A, Imtiaz MH (2023) Automatic identification of children with ADHD from EEG brain waves. Signals 4(1):193–205. https://doi.org/10.3390/signals4010010
Rezaei M, Zare H, Hakimdavoodi H, Nasseri S, Hebrani P (2022) Classification of drug-naive children with attention-deficit/hyperactivity disorder from typical development controls using resting-state fMRI and graph theoretical approach. Front Hum Neurosci 16:948706. https://doi.org/10.3389/fnhum.2022.948706
TaghiBeyglou B, Shahbazi A, Bagheri F, Akbarian S, Jahed M (2022) Detection of ADHD cases using CNN and classical classifiers of raw EEG. Comput Methods Progr Biomed Update 2:100080. https://doi.org/10.1016/j.cmpbup.2022.100080
Kiiski H, Rueda-Delgado LM, Bennett M, Knight R, Rai L, Roddy D, Grogan K, Bramham J, Kelly C, Whelan R (2020) Functional EEG connectivity is a neuromarker for adult attention deficit hyperactivity disorder symptoms. Clin Neurophysiol 131(1):330–342. https://doi.org/10.1016/j.clinph.2019.08.010
Furlong S, Cohen JR, Hopfinger J, Snyder J, Robertson MM, Sheridan MA (2021) Resting-state EEG connectivity in young children with ADHD. J Clin Child Adolesc Psychol 50(6):746–762. https://doi.org/10.1080/15374416.2020.1796680
Ekhlasi A, Motie Nasrabadi A, Mohammadi MR (2021) Analysis of effective connectivity strength in children with attention deficit hyperactivity disorder using phase transfer entropy. Iran J Psychiatry. https://doi.org/10.18502/ijps.v16i4.7224
Ekhlasi A, Motie Nasrabadi A, Mohammadi MR (2021) Classification of the children with ADHD and healthy children based on the directed phase transfer entropy of EEG signals. Front Biomed Technol. https://doi.org/10.18502/fbt.v8i2.6515
Chen H, Song Y, Li X (2019) A deep learning framework for identifying children with ADHD using an EEG-based brain network. Neurocomputing 356:83–96. https://doi.org/10.1016/j.neucom.2019.04.058
Ahmadlou M, Adeli H, Adeli A (2012) Graph theoretical analysis of organization of functional brain networks in ADHD. Clin EEG Neurosci 43(1):5–13. https://doi.org/10.1177/1550059411428555
Talebi N, Motie Nasrabadi A (2022) Investigating the discrimination of linear and nonlinear effective connectivity patterns of EEG signals in children with attention-deficit/hyperactivity disorder and typically develo** children. Comput Biol Med 148:105791. https://doi.org/10.1016/j.compbiomed.2022.105791
Michelini G, Jurgiel J, Bakolis I, Cheung CHM, Asherson P, Loo SK, Kuntsi J, Mohammad-Rezazadeh I (2019) Atypical functional connectivity in adolescents and adults with persistent and remitted ADHD during a cognitive control task. Transl Psychiatry 9(1):137. https://doi.org/10.1038/s41398-019-0469-7
Motie Nasrabadi A, Allahverdy A, Samavati M, Mohammadi MR (2020) EEG data for ADHD/control children|IEEE DataPort. https://doi.org/10.21227/rzfh-zn36. https://ieee-dataport.org/open-access/eeg-data-adhd-control-children. Accessed 30 Mar 2023
Delorme A, Makeig S (2004) EEGLAB: an open source toolbox for analysis of single-trial EEG dynamics including independent component analysis. J Neurosci Methods 134(1):9–21. https://doi.org/10.1016/j.jneumeth.2003.10.009
Delorme A. Clean raw data plugin. https://github.com/sccn/clean_rawdata. Accessed 30 Mar 2023
Pion-Tonachini L, Kreutz-Delgado K, Makeig S (2019) ICLabel: an automated electroencephalographic independent component classifier, dataset, and website. Neuroimage 198:181–197. https://doi.org/10.1016/j.neuroimage.2019.05.026
Cohen MX (2014) Analyzing neural time series data. The MIT Press, Cambridge. https://doi.org/10.7551/mitpress/9609.001.0001
Stam CJ, Nolte G, Daffertshofer A (2007) Phase lag index: assessment of functional connectivity from multi channel EEG and MEG with diminished bias from common sources. Hum Brain Mapp 28(11):1178–1193. https://doi.org/10.1002/hbm.20346
Rubinov M, Sporns O (2010) Complex network measures of brain connectivity: uses and interpretations. Neuroimage 52(3):1059–1069. https://doi.org/10.1016/j.neuroimage.2009.10.003
Watts DJ, Strogatz SH (1998) Collective dynamics of ‘small-world’ networks. Nature 393(6684):440–442. https://doi.org/10.1038/30918
Latora V, Marchiori M (2001) Efficient behavior of small-world networks. Phys Rev Lett 87(19):198701–198704. https://doi.org/10.1103/PhysRevLett.87.198701
Blondel VD, Guillaume JL, Lambiotte R, Lefebvre E (2008) Fast unfolding of communities in large networks. J Stat Mech: Theory Exp 2008(10):P10008. https://doi.org/10.1088/1742-5468/2008/10/P10008
Freeman LC (1978) Centrality in social networks conceptual clarification. Soc Netw 1(3):215–239. https://doi.org/10.1016/0378-8733(78)90021-7
Estrada E, Rodríguez-Velázquez JA (2005) Subgraph centrality in complex networks. Phys Rev E 71(5):056103. https://doi.org/10.1103/PhysRevE.71.056103
Acknowledgements
The EEG data employed in this research were obtained and archived under Prof. Ali Motie Nasrabadi and his colleagues. The authors hereby express their sincere appreciation to him and his esteemed research team for generously sharing their valuable dataset.
Funding
The authors declare that no funds, grants, or other forms of support were received during the preparation of this manuscript.
Author information
Authors and Affiliations
Contributions
The idea presented in this research was conceived and developed by FAT and SAH. Additionally, FAT carried out the computations, material preparation, data collection, and analysis. He also drafted the initial version of the manuscript, which was subsequently reviewed and commented on by YM and SAH. All authors contributed to sha** the research and manuscript, providing constructive feedback. Furthermore, all authors actively participated in other aspects of the investigation, including visualization and manuscript review. Finally, all authors have read and approved the final manuscript. SAH supervised the project.
Corresponding author
Ethics declarations
Conflict of interest
The authors have no relevant financial or non-financial interests to disclose.
Consent to participate
According to the data description, informed consent was obtained from all individual participants included in the study.
Ethical approval
According to the data description, all ethical standards and guidelines were meticulously followed to ensure the protection of human subjects and the integrity of the research. The EEG recording procedure has been conducted in accordance with the ethical principles set forth by the Declaration of Helsinki and its subsequent amendments.
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
Abedinzadeh Torghabeh, F., Hosseini, S.A. & Modaresnia, Y. Potential biomarker for early detection of ADHD using phase-based brain connectivity and graph theory. Phys Eng Sci Med 46, 1447–1465 (2023). https://doi.org/10.1007/s13246-023-01310-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s13246-023-01310-y