Skip to main content

Advertisement

Log in

Identifying ADHD and subtypes through microstates analysis and complex networks

  • Original Article
  • Published:
Medical & Biological Engineering & Computing Aims and scope Submit manuscript

Abstract

The diagnosis of attention-deficit hyperactivity disorder (ADHD) is based on the health history and on the evaluation of questionnaires to identify symptoms. This evaluation can be subjective and lengthy, especially in children. Therefore, a biomarker would be of great value to assist mental health professionals in the process of diagnosing ADHD. Event-related potential (ERP) is one of the most informative and dynamic methods of monitoring cognitive processes. Previous works suggested that specific sets of ERP-microstates are selectively affected by ADHD. This paper proposes a new methodology for the ERP-microstate analysis and identification of ADHD patients based on complex networks to model the microstate topographic maps. The analysis of global and local features of ERP-microstate networks revealed topological differences between ADHD and healthy control. The classification using a neural network with a single hidden layer resulted in an average accuracy of 99.72% in binary classification and 99.31% in the classification of ADHD subtypes. The results were compared to the power band spectral densities and the energy of wavelet coefficients. The temporal features of ERP-microstates, such as frequency of occurrence, duration, coverage, and transition probabilities, were also evaluated for comparison proposes. Overall, the selected topological features of ERP-microstate networks derived from the proposed method performed significantly better classification results. The results suggest that topological features of ERP-microstate networks are promising to identify ADHD and its subtypes with a neural network model compared to power band spectrum density, wavelet transform, and temporal features of ERP-microstates.

Graphical abstract

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

Data availability

The datasets analyzed during the current study are available in the OSF repository (https://osf.io/6594x/).

References

  1. Thomas R, Sanders S, Doust J, Beller E, Glasziou P (2015) Prevalence of attention-deficit/hyperactivity disorder: a systematic review and meta-analysis. Pediatrics 135(4):994–1001

    Article  Google Scholar 

  2. Song P, Zha M, Yang Q, Zhang Y, Li X, Rudan I (2021) The prevalence of adult attention-deficit hyperactivity disorder: a global systematic review and meta-analysis. J Global Health 11

  3. Association AP et al (2022) Diagnostic and statistical manual of mental disorders fifth edition, text revision (DSM-5-TR). Author

  4. Ahmadi N, Mohammadi MR, Araghi SM, Zarafshan H (2014) Neurocognitive profile of children with attention deficit hyperactivity disorders (ADHD): a comparison between subtypes. Iran J Psychiatry 9(4):197

    PubMed  PubMed Central  Google Scholar 

  5. Ghanizadeh A (2011) Overlap of ADHD and oppositional defiant disorder DSM-IV derived criteria. Arch Iran Med 14(3):179

    PubMed  Google Scholar 

  6. Dubreuil-Vall L, Ruffini G, Camprodon JA (2020) Deep learning convolutional neural networks discriminate adult ADHD from healthy individuals on the basis of event-related spectral EEG. Front Neurosci 14

  7. Vahid A, Bluschke A, Roessner V, Stober S, Beste C (2019) Deep learning based on event-related EEG differentiates children with ADHD from healthy controls. J Clin Med 8(7):1055

    Article  PubMed  PubMed Central  Google Scholar 

  8. Tosun M (2021) Effects of spectral features of EEG signals recorded with different channels and recording statuses on ADHD classification with deep learning. Phys Eng Sci Med 44(3):693–702

    Article  PubMed  Google Scholar 

  9. Férat V, Arns M, Deiber M-P, Hasler R, Perroud N, Michel CM, Ros T (2022) Electroencephalographic microstates as novel functional biomarkers for adult attention-deficit/hyperactivity disorder. Biol Psychiatry Cogn Neurosci Neuroimaging 7(8):814–823

    PubMed  Google Scholar 

  10. Jahanshahloo HR, Shamsi M, Ghasemi E, Kouhi A (2017) Automated and ERP-based diagnosis of attention-deficit hyperactivity disorder in children. J Med Signals Sens 7(1):26

    Article  PubMed  PubMed Central  Google Scholar 

  11. Mueller A, Candrian G, Kropotov JD, Ponomarev VA, Baschera G-M (2010) Classification of ADHD patients on the basis of independent ERP components using a machine learning system. In: Nonlinear Biomedical Physics, vol 4, pp 1–12. Springer

  12. Lehmann D, Ozaki H, Pal I (1987) EEG alpha map series: brain micro-states by space-oriented adaptive segmentation. Electroencephalogr Clin Neurophysiol 67(3):271–288

    Article  CAS  PubMed  Google Scholar 

  13. Pascual-Marqui RD (2002) Standardized low resolution brain electromagnetic tomography (sLORETA): Technical details 24 Suppl D:5–12

  14. Lehmann D (2010) Multimodal analysis of resting state cortical activity: what does FMRI add to our knowledge of microstates in resting state EEG activity?: Commentary to the papers by britz et al. and musso et al. in the current issue of neuroimage. NeuroImage 52(4):1173–1174

  15. Pascual-Marqui RD, Michel CM, Lehmann D (1995) Segmentation of brain electrical activity into microstates: model estimation and validation. IEEE Trans Biomed Eng 42(7):658–665

    Article  CAS  PubMed  Google Scholar 

  16. Albrecht B, Uebel-von Sandersleben H, Wiedmann K, Rothenberger A (2015) ADHD history of the concept: the case of the continuous performance test. Curr Dev Disord Rep 2(1):10–22

    Article  Google Scholar 

  17. Brandeis D, van Leeuwen TH, Steger J, Imhof K, Steinhausen H-C (2002) Mapping brain functions of ADHD children. In: International Congress Series, vol 1232, pp 649–654. Elsevier

  18. Meier NM, Perrig W, Koenig T (2012) Neurophysiological correlates of delinquent behaviour in adult subjects with ADHD. Int J Psychophysiol 84(1):1–16

    Article  PubMed  Google Scholar 

  19. Michel CM, Koenig T, Brandeis D, Gianotti LR, Wackermann J (2009) Electrical neuroimaging, 1st edn. Cambridge University Press, ???

  20. Khanna A, Pascual-Leone A, Farzan F (2014) Reliability of resting-state microstate features in electroencephalography.(research article). PLoS ONE 9(12)

  21. Karalunas SL (2022) Electroencephalographic biomarkers in psychiatry-how do we make good on promises? Biological Psychiatry: Cognitive Neuroscience and Neuroimaging 7(8):752–753

    PubMed  Google Scholar 

  22. Koenig T, Kottlow M, Stein M, Melie-Garcia L (2011) Ragu: a free tool for the analysis of EEG and MEG event-related scalp field data using global randomization statistics 2011:938925

  23. Poulsen AT, Pedroni A, Langer N, Hansen LK (2018) Microstate EEGlab toolbox: an introductory guide. bioRxiv

  24. Hu L, Zhang Z (2019) EEG signal processing and feature extraction. Springer, Singapore

    Book  Google Scholar 

  25. de Vico Fallani F, Richiardi J, Chavez M, Achard S (2014) Graph analysis of functional brain networks: practical issues in translational neuroscience. Phil Trans R Soc B Biol Sci 369(1653):20130521

    Article  Google Scholar 

  26. Telesford QK, Simpson SL, Burdette JH, Hayasaka S, Laurienti PJ (2011) The brain as a complex system: using network science as a tool for understanding the brain. Brain connectivity 1(4):295–308

    Article  PubMed  PubMed Central  Google Scholar 

  27. Rubinov M, Sporns O (2010) Complex network measures of brain connectivity: uses and interpretations. Neuroimage 52(3):1059–1069

    Article  PubMed  Google Scholar 

  28. Perrin F, Pernier J, Bertrand O, Echallier J (1989) Spherical splines for scalp potential and current density mapping. Electroencephalogr Clin Neurophysiol 72(2):184–187

    Article  CAS  PubMed  Google Scholar 

  29. Cohen MX (2014) Analyzing neural time series data: theory and practice. MIT press, USA

    Book  Google Scholar 

  30. Nunez PL, Srinivasan R et al (2006) Electric fields of the brain: the neurophysics of EEG, 2nd edn. Oxford University Press, USA, ???

  31. Michel CM, Koenig T (2017) EEG microstates as a tool for studying the temporal dynamics of whole-brain neuronal networks: a review

  32. Zhang M, Zhou H, Liu L, Feng L, Yang J, Wang G, Zhong N (2018) Randomized EEG functional brain networks in major depressive disorders with greater resilience and lower rich-club coefficient. Clin Neurophys 129(4):743–758

    Article  Google Scholar 

  33. Mann HB, Whitney DR (1947) On a test of whether one of two random variables is stochastically larger than the other. Ann Math Stat 18(1):50–60

    Article  MathSciNet  Google Scholar 

  34. Snoek J, Larochelle H, Adams RP (2012) Practical Bayesian optimization of machine learning algorithms. arXiv preprint. arXiv:1206.2944

  35. Baratloo A, Hosseini M, Negida A, El Ashal G (2015) Part 1: simple definition and calculation of accuracy, sensitivity and specificity. Emergency 3(2):48–49

    PubMed  PubMed Central  Google Scholar 

  36. Welch P (1967) The use of fast Fourier transform for the estimation of power spectra: a method based on time averaging over short, modified periodograms. IEEE Trans Audio Electroacoust 15(2):70–73

    Article  ADS  Google Scholar 

  37. Heinrich H, Moll G, Dickhaus H, Kolev V, Yordanova J, Rothenberger A (2001) Time-on-task analysis using wavelet networks in an event-related potential study on attention-deficit hyperactivity disorder. Clin Neurophys 112(7):1280–1287

    Article  CAS  Google Scholar 

  38. Jain A, Zongker D (1997) Feature selection: evaluation, application, and small sample performance. IEEE Transactions Patt Anal Mach Intell 19(2):153–158

    Article  Google Scholar 

  39. Rieger K, Diaz Hernandez L, Baenninger A, Koenig T (2016) 15 years of microstate research in schizophrenia - where are we? A meta-analysis. Front Psychiatry 7:22

    Article  PubMed  PubMed Central  Google Scholar 

  40. Chennu S, Finoia P, Kamau E, Allanson J, Williams GB, Monti MM, Noreika V, Arnatkeviciute A, Canales-Johnson A, Olivares F et al (2014) Spectral signatures of reorganised brain networks in disorders of consciousness. PLoS Comput Biol 10(10):1003887

    Article  Google Scholar 

  41. Zillessen K, Scheuerpflug P, Fallgatter A, Strik W, Warnke A (2001) Changes of the brain electrical fields during the continuous performance test in attention-deficit hyperactivity disorder-boys depending on methylphenidate medication. Clin Neurophys 112(7):1166–1173

    Article  CAS  Google Scholar 

  42. Moghaddari M, Lighvan MZ, Danishvar S (2020) Diagnose ADHD disorder in children using convolutional neural network based on continuous mental task EEG. Comput Methods Prog Biomed 197

  43. He L, Hu D, Wan M, Wen Y, Von Deneen KM, Zhou M (2015) Common Bayesian network for classification of EEG-based multiclass motor imagery BCI. IEEE Trans Syst Man Cybern Sys 46(6):843–854

    Article  Google Scholar 

  44. Hesse W, Möller E, Arnold M, Schack B (2003) The use of time-variant EEG granger causality for inspecting directed interdependencies of neural assemblies. J Neurosci Methods 124(1):27–44

    Article  PubMed  Google Scholar 

Download references

Funding

The authors thank the Programa de Pós-Graduação em Engenharia Elétrica (PPGEE - UFES) and the financial support for the research from the project of the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) and Fundação de Amparo à Pesquisa do Espírito Santo (FAPES), number 598/2018.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Lorraine Marques Alves.

Ethics declarations

Conflict of interest

The authors declare no competing interests.

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.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Alves, L.M., Côco, K.F., De Souza, M.L. et al. Identifying ADHD and subtypes through microstates analysis and complex networks. Med Biol Eng Comput 62, 687–700 (2024). https://doi.org/10.1007/s11517-023-02948-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11517-023-02948-2

Keywords

Navigation