Abstract
Recently multimodal neuroimaging which combines signals from different brain modalities has started to be considered as a potential to improve the accuracy of diagnosis. The current study aimed to explore a new method for discriminating attention-deficit hyperactivity disorder (ADHD) patients and control group by means of simultaneous measurement of electroencephalography (EEG) and functional near-infrared spectroscopy (fNIRS). Twenty-three pre-medicated combined type ADHD children and 21 healthy children were included in the study. Nonlinear brain dynamics of subjects were obtained from EEG signal using Higuchi fractal dimensions and Lempel–Ziv complexity, latency and amplitude values of P3 wave obtained from auditory evoked potentials and frontal cortex hemodynamic responses calculated from fNIRS. Lower complexity values, prolonged P3 latency and reduced P3 amplitude values were found in ADHD children. fNIRS indicated that the control subjects exhibited higher right prefrontal activation than ADHD children. Features are analyzed, looking for the best classification accuracy and finally machine learning techniques, namely Support Vector Machines, Naïve Bayes and Multilayer Perception Neural Network, are introduced for EEG signals alone and for combination of fNIRS and EEG signals. Naive Bayes provided the best classification with an accuracy rate of 79.54% and 93.18%, using EEG and EEG-fNIRS systems, respectively. Our findings demonstrate that utilization of information by combining features obtained from fNIRS and EEG improves the classification accuracy. As a conclusion, our method has indicated that EEG-fNIRS multimodal neuroimaging is a promising method for ADHD objective diagnosis.
Similar content being viewed by others
Change history
20 February 2022
A Correction to this paper has been published: https://doi.org/10.1007/s00521-022-07056-0
References
Biederman J, Faraone SV (2005) Attention-deficit hyperactivity disorder. Lancet 366:237–248
American Psychiatric Association (1994) Diagnostic and statistical manual of mental disorders, 4th edn. DSM-IV. APA, Philadelphia
Bruchmüller K, Margraf J, Schneider S (2012) Is ADHD diagnosed in accord with diagnostic criteria? Overdiagnosis and influence of client gender on diagnosis. J Consult Clin Psychol 80(1):128–138
Wolraich ML, Bard DE, Neas B, Doffing M, Beck L (2013) The psychometric properties of the Vanderbilt attention-deficit hyperactivity disorder diagnostic teacher rating scale in a community population. J Dev Behav Pediatr 34(2):83–93
Roscha KS, Crocettia D, Hirabayashi K, Denckla MB, Mostofskya SH, Mahonea EM (2018) Reduced subcortical volumes among preschool-age girls and boys with ADHD. Psychiatry Res Neuroimaging 271:67–74
Sridhar C, Bhat S, Acharya UR, Adeli H, Bairy GM (2017) Diagnosis of attention deficit hyperactivity disorder using imaging and signal processing techniques. Comput Biol Med 88:93–99
Monden Y, Dan H, Nagashima M, Dan I, Tsuzuki D, Kyutoku Y, Gunji Y, Yamagata T, Watanabe E, Momoi MY (2012) Right prefrontal activation as a neuro-functional biomarker for monitoring acute effects of methylphenidate in ADHD children: an fNIRS study. Neuroimage Clin 1(1):131–140
Bush G (2011) Cingulate, frontal, and parietal cortical dysfunction in attention-deficit/hyperactivity disorder. Biol Psychiatry 69:1160–1167
Bush G, Valera EM, Seidman LJ (2005) Functional neuroimaging of attention-deficit/hyperactivity disorder: a review and suggested future directions. Biol Psychiatry 57:1273–1284
Vaidya CJ, Austin G, Kirkorian G, Ridlehuber HW, Desmond JE, Glover GH, Gabrieli JD (1998) Selective effects of methylphenidate in attention deficit hyperactivity disorder: a functional magnetic resonance study. Proc Natl Acad Sci USA 95:14494–14499
Durston S, Tottenham NT, Thomas KM, Davidson MC, Eigsti IM, Yang Y, Ulug AM, Casey BJ (2003) Differential patterns of striatal activation in young children with and without ADHD. Biol Psychiatry 53:871–878
Ehlis AC, Schneidera S, Dreslera T, Fallgatter AJ (2014) Application of functional near-infrared spectroscopy in psychiatry. Neuroimage 85(1):478–488
Moser SJ, Cutini S, Weber P, Schroeter ML (2009) Right prefrontal brain activation due to Stroop interference is altered in attention-deficit hyperactivity disorder—a functional near-infrared spectroscopy study. Psychiatry Res Neuroimaging 173:190–195
Schecklmann M, Schaldecker M, Aucktor S, Brast J, Kirchgäßner K, Mühlberger A, Warnke A, Gerlach M, Fallgatter AJ, Romanos M (2011) Effects of methylphenidate on olfaction and frontal and temporal brain oxygenation in children with ADHD. J Psychiatr Res 45:1463–1470
Ichikawa H, Nakato E, Kanazawa S, Shimamura K, Sakuta Y, Sakuta R, Yamaguchi MK, Kakigi R (2014) Hemodynamic response of children with attention-deficit and hyperactive disorder (ADHD) to emotional facial expressions. Neuropsychologia 63:51–58
Schecklmann M, Ehlis AC, Plichta MM, Romanos J, Heine M, Boreatti-Hümmer A, Jacob C, Fallgatter AJ (2008) Diminished prefrontal oxygenation with normal and above-average verbal fluency performance in adult ADHD. J Psychiatr Res 43:98–106
Rubia K, Halari R, Cubillo A, Mohammad AM, Brammer M, Taylor E (2009) Meth-ylphenidate normalises activation and functional connectivity deficits in attention and motivation networks in medication-naive children with ADHD during a rewarded continuous performance task. Neuropharmacology 57:640–652
Yasumura A, Kokubo N, Yamamoto H, Yasumura Y, Nakagawa E, Kaga M, Hiraki K, Inagaki M (2014) Neurobehavioral and hemodynamic evaluation of Stroop and reverse Stroop interference in children with attention-deficit/hyperactivity disorder. Brain Dev 36(2):97–106
Monden Y, Dan I, Nagashima M, Dan H, Uga M, Ikeda T, Tsuzuki D, Kyutoku Y, Gunji Y, Hirano D, Taniguchi T, Shimoizumi H, Watanabe E, Yamagataa T (2015) Individual classification of ADHD children by right prefrontal hemodynamic responses during a go/no-go task as assessed by fNIRS. Neuroimage Clin 9:1–12
Gu Y, Miao S, Han J, Zeng K, Ouyang G, Yang J, Li X (2017) Complexity analysis of fNIRS signals in ADHD children during working memory task. Sci Rep 7(1):829
Barry RJ, Clarke AR, Johnstone SJ (2003) A review of electrophysiology in attention-deficit/hyperactivity disorder: I. Qualitative and quantitative electroencephalography. Clin Neurophysiol 114(2):171–183
Loo SK, Makeig S (2012) Clinical utility of EEG in attention-deficit/hyperactivity disorder: a research update. Neurotherapeutics 9:569–587
Zhang Y, Ji X, Liu B, Huang D, Xie F, Zhang Y (2017) Combined feature extraction method for classification of EEG signals. Neural Comput Appl 28:3153–3161
Cerquera A, Arns M, Gutiérrez RM, Freund J (2012) Dynamical measures for characterization of EEG registers in patients with attention deficit hyperactivity disorder treated with neurofeedback. In: XVII symposium of image, signal processing, and artificial vision (STSIVA)
Fernández A, Quintero J, Hornero R, Zuluaga P, Navas M, Gómez C, Escudero J, García-Campos N, Biederman J, Ortiz T (2009) Complexity analysis of spontaneous brain activity in attention-deficit/hyperactivity disorder: diagnostic implications. Biol Psychiatry 65:571–577
Chenxi L, Chen Y, Li Y, Wang J, Liu T (2016) Complexity analysis of brain activity in attention-deficit/hyperactivity disorder: a multiscale entropy analysis. Brain Res Bull 124:12–20
Esteban FJ, Beltrán LD, Di Ieva A (2016) The fractal geometry of the brain. Springer, New York
Oztoprak H, Toycan M, Alp YK, Arıkan O, Doğtepe E, Karakas S (2017) Machine-based classification of ADHD and nonADHD participants using time/frequency features of event-related neuroelectric activity. Clin Neurophysiol 128:2400–2410
Johnstone SJ, Barry RJ, Clarke AR (2013) Ten years on: a follow-up review of ERP research in attention-deficit/hyperactivity disorder. Clin Neurophysiol 124:644–657
Polich J (2007) Updating P300: an integrative theory of P3a and P3b. Clin Neurophysiol 118:2128–2148
Senderecka M, Grabowska A, Szewczyk J, Gerc K, Chmylak R (2012) Response inhibition of children with ADHD in the stop-signal task: an event-related potential study. Int J Psychophysiol 85(1):93–105
Romero AC, Capellini SA, Frizzo AC (2013) Cognitive potential of children with attention deficit and hyperactivity disorder. Braz J Otorhinolaryngol 79(5):609–615
Lawrence C, Barry R, Clarke A, Johnstone S, McCarthy R, Selikowitz M, Broyd S (2005) Methylphenidate effects in attention deficit/hyperactivity disorder: electrodermal and ERP measures during a continuous performance task. Psychopharmacology 183:81–91
Liu S, Cai W, Liu S, Zhang F, Fulham M, Feng D, Pujol S, Kikinis R (2015) Multimodal neuroimaging computing: a review of the applications in neuropsychiatric disorders. Brain Inform 2:167–180
Liu Y, Ayaz H, Shewokis PA (2017) Mental workload classification with concurrent electroencephalography and functional near-infrared spectroscopy. Brain Comput Interfaces 4(3):175–185
Pelletier I, Sauerwein HC, Lepore F, Saint-Amour D, Lassonde M (2007) Non-invasive alternatives to the Wada test in the presurgical evaluation of language and memory functions in epilepsy patients. Epileptic Disord 9(2):111–126
Shibasaki H (2008) Human brain mapping: hemodynamic response and electrophysiology. Clin Neurophysiol 119:731–743
Izzetoglu M, Bunce SC, Izzetoglu K, Onaral B, Pourrezaei K (2007) Functional brain imaging using near-infrared technology for cognitive activity assessment. IEEE Eng Med Biol Mag Spec Issue Role Opt Imaging Augment Cognit 26:38–46
Fazli S, Mehnert J, Steinbrink J, Curio G, Villringer A, Müller KR, Blankertz B (2012) Enhanced performance by hybrid NIRS–EEG brain computer interface. Neuroimage 59(1):519–529
Wallois F, Patil A, Héberlé C, Grebe R (2010) EEG-NIRS in epilepsy in children and neonates. Neurophysiol Clin 40(5–6):281–292
Wallois F, Mahmoudzadeh M, Patil A, Grebe R (2012) Usefulness of simultaneous EEG-NIRS recording in language studies. Brain Lang 121(2):110–123
Gratton G, Goodman-Wood MR, Fabiani M (2001) Comparison of neuronal and hemodynamic measure of the brain response to visual stimulation: an optical imaging study. Hum Brain Mapp 13:13–25
Dolu N, Altınkaynak M, Güven A, Özmen S, Demirci E, İzzetoğlu M, Pektaş F (2018) Effects of methylphenidate treatment in children with ADHD: a multimodal EEG/fNIRS approach. Psychiatry Clin Psychopharmacol. https://doi.org/10.1080/24750573.2018.1542779
Wechsler D (1974) WISC-R manual for the wechsler intelligence scale for children revised (WISC-R). United Kingdom
Izzetoglu M, Izzetoglu K, Bunce S, Ayaz H, Devaraj A, Onaral B, Pourrezaei K (2005) Functional near-infrared neuroimaging. IEEE Trans Neural Syst Rehabil Eng 13(2):153–159
Strangman G, Boas DA, Sutton JP (2002) Non-invasive neuroimaging using near-infrared light. Biol Psychiatry 52(7):679–693
Cope M, Delpy DT (1988) System for long-term measurement of cerebral blood flow and tissue oxygenation on newborn infants by infrared transillumination. Med Biol Eng Comput 26:289–294
Ayaz H, Shewokis PA, Bunce S, Izzetoglu K, Willems B, Onaral B (2012) Optical brain monitoring for operator training and mental workload assessment. Neuroimage 59(2012):36–47
Fisch BJ (1999) EEG PRIMER: basic principles of digital and analog EEG, 3rd edn. Elsevier Academic Press, Amsterdam
Hoshi Y (2003) Functional near-infrared optical imaging: utility and limitations in human brain mapping. Psychophysiology 40(4):511–520
Ehlis AC, Bahne CG, Jacob CP, Herrmann MJ, Fallgatter AJ (2008) Reduced lateral prefrontal activation in adult patients with attention-deficit/hyperactivity disorder (ADHD) during a working memory task: a functional near-infrared spectroscopy (fNIRS) study. J Psychiatr Res 42:1060–1067
Schecklmann M, Romanos M, Bretscher F, Plichta MM, Warnke A, Fallgatter AJ (2010) Prefrontal oxygenation during working memory in ADHD. J Psychiatr Res 44:621–628
Plichta MM, Herrmann MJ, Baehte CG, Ehlis AC, Richter MM, Pauli P et al (2006) Event related functional near-infrared spectroscopy (fNIRS): are the measurements reliable? Neuroimage 31:116–124
Collette F, Hogge M, Salmon E, Van der Linden M (2006) Exploration of the neural substrates of executive functioning by functional neuroimaging. Neuroscience 139:209–221
Lempel A, Ziv J (1976) On the complexity of finite sequences. IEEE Trans Inf Theory 22:75–81
Kesić S, Spasić SZ (2016) Application of Higuchi’s fractal dimension from basic to clinical neurophysiology: a review. Comput Methods Programs Biomed 133:55–70
Higuchi T (1988) Approach to an irregular time series on the basis of the fractal theory. Physica D 31:277–283
Accardo A, Affinito M, Carrozzi M, Bouquet F (1997) Use of the fractal dimension for the analysis of electroencephalographic time series. Biol Cybern 77:339–350
Davila CE, Srebro R (2000) Subspace averaging of steady-state visual evoked potentials. IEEE Trans Biomed Eng 47(6):720–728
Cawley GC, Talbot NLC (2004) Fast exact leave-one-out cross-validation of sparse least-squares support vector machines. Neural Netw 17:1467–1475
Jayalakshmi T, Santhakumaran A (2011) Statistical normalization and back propagation for classification. Int J Comput Theory Eng 3(1):1793–8201
Thomas CG, Lynda GJ (2005) ADHD: is objective diagnosis possible? Psychiatry (Edgmont) 2(11):44–53
Spinella M, Yang B, Lester D (2004) Prefrontal system dysfunction and credit card debt. Int J Neurosci 114:1323–1332
Miller EK, Cohen JD (2001) An integrative theory of prefrontal cortex function. Annu Rev Neurosci 24:167–202
Bush G (2010) Attention-deficit/hyperactivity disorder and attention networks. Neuropsychopharmacology 35(1):278–300
Weber P, Lutschg J, Fahnenstich H (2005) Cerebral hemodynamic changes in response to an executive function task in children with attention deficit hyperactivity disorder measured by near-infrared spectroscopy. J Dev Behav Pediatr 26:105–111
Inoue Y, Sakihara K, Gunji A, Ozawa H, Kimiya S, Shinoda H, Kaga M, Inagaki M (2012) Reduced prefrontal hemodynamic response in children with ADHD during the Go/NoGo task: a NIRS study. Neuroreport 23:55–60
Rubia K, Smith AB, Brammer MJ, Toone B, Taylor E (2005) Abnormal brain activation during inhibition and error detection in medication-naïve adolescents with ADHD. Am J Psychiatry 162:1067–1075
Booth JR, Burman DD, Meyer JR, Lei Z, Trommer BL, Davenport ND, Li W, Parrish TB, Gitelman DR, Mesulam MM (2005) Larger deficits in brain networks for response inhibition than for visual selective attention in attention deficit hyperactivity disorder (ADHD). J Child Psychol Psychiatry 46(1):94–111
Smith AB, Taylor E, Brammer M, Halari R, Rubia K (2008) Reduced activation in right lateral prefrontal cortex and anterior cingulate gyrus in medication-naïve adolescents with attention deficit hyperactivity disorder during time discrimination. J Child Psychol Psychiatry 49(9):977–985
Depuea BE, Burgess GC, Willcutt EG, Ruzic L, Banich M (2010) Inhibitory control of memory retrieval and motor processing associated with the right lateral prefrontal cortex: evidence from deficits in individuals with ADHD. Neuropsychologia 48(13):3909–3917
Naseer N, Hong MJ, Hong KS (2014) Online binary decision decoding using functional near-infrared spectroscopy for the development of brain–computer interface. Exp Brain Res 232:555–564
Mihara M, Miyai I, Hattori N, Hatakenaka M, Yagura H, Kawano T, Yagura H, Kawano T, Okibayashi M, Danjo N, Ishikawa A, Inoue Y, Kubota K (2012) Neurofeedback using real-time near-infrared spectroscopy enhances motor imagery related cortical activation. PLoS ONE 7(3):e32234
Tylová L, Kukala J, Hubata-Vacek VH, Vyšatabc O (2018) Unbiased estimation of permutation entropy in EEG analysis for Alzheimer’s disease classification. Biomed Signal Process Control 39:424–430
Li M, Chen W, Zhang T (2017) Automatic epileptic EEG detection using DT-CWT-based non-linear features. Biomed Signal Process Control 34:114–125
Birjandtalab J, Pouyan MB, Cogan D, Nourani M, Harvey J (2017) Automated seizure detection using limited-channel EEG and non-linear dimension reduction. Comput Biol Med 82:49–58
Goldberger AL, Peng CK, Lipsitz LA (2002) What is physiologic complexity and how does it change with aging and disease? Neurobiol Aging 23:23–26
Kratz O, Studer P, Malcherek S, Erbe K, Moll GH, Heinrich H (2011) Attentional processes in children with ADHD: an event-related potential study using the attention network test. Int J Psychophysiol 81:82–90
Jonkman LM, Kemner C, Verbaten MN, Koelega HS, Camfferman G, vd Gaag RJ, Buitelaar JK, van Engeland H (1997) Event-related potentials and performance of attention-deficit hyperactivity disorder: children and normal controls in auditory and visual selective attention tasks. Biol Psychiatry 41:595–611
Alba-Sanchez F, Yanez-Suarez O, Brust-Carmona H (2010) Assisted diagnosis of attention-deficit hyperactivity disorder through EEG bandpower clustering with self-organizing maps. Conf Proc IEEE Eng Med Biol Soc 2010:2447–2450
Mann CA, Lubar JF, Zimmerman AW, Miller CA, Muenchen RA (1992) Quantitative-analysis of EEG in boys with attention-deficit hyperactivity disorder: controlled study with clinical implications. Pediatr Neurol 8:30–36
Smith JL, Johnstone SJ, Barry RJ (2003) Aiding diagnosis of attention-deficit/hyperactivity disorder and its subtypes: discriminant function analysis of event-related potential data. J Child Psychol Psychiatry 44:1067–1075
Sangal RB, Sangal JM (2015) Use of EEG beta-1 power and theta/beta ratio over Broca’s area to confirm diagnosis of attention deficit/hyperactivity disorder in children. Clin EEG Neurosci 46:177–182
Lenartowicz A, Delorme A, Walshaw PD, Cho AL, Bilder RM, McGough JJ et al (2014) Electroencephalography correlates of spatial working memory deficits in attention-deficit/hyperactivity disorder: vigilance, encoding, and maintenance. J Neurosci 34:1171–1182
Allahverdi A, Nasrabadi AM, Mohammad M (2011) Detecting ADHD children using symbolic dynamic of nonlinear features of EEG. Presented at the 19th Iranian conference on electrical engineering, May 17–19, Tehran, Iran
Robaey P, Breton F, Dugas M, Renault B (1992) An event-related potential study of controlled and automatic processes in 6–8-year old boys with attention deficit hyperactivity disorder. Electroencephalogr Clin Neurophysiol 82:330–340
Helgadottir H, Gudmundsson OO, Baldursson G, Magnusson P, Blin N, Brynjolfsdottir B et al (2015) Electroencephalography as a clinical tool for diagnosing and monitoring attention deficit hyperactivity disorder: a cross-sectional study. BMJ Open 5:e005500
Poil SS, Bollmann S, Ghisleni C, O’Gorman RL, Klaver P, Ball J et al (2014) Age dependent electroencephalographic changes in attention-deficit/hyperactivity disorder (ADHD). Clin Neurophysiol 125:1626–1638
Tcheslavski GV, Beex AA (2006) Phase synchrony and coherence analyses of EEG as tools to discriminate between children with and without attention deficit disorder. Biomed Signal Process Control 1:151–161
Sen B, Borle NC, Greiner R, Brown MRG (2018) A general prediction model for the detection of ADHD and autism using structural and functional MRI. PLoS ONE 13(4):e0194856
Dai D, Wang J, Hua J, He H (2012) Classification of ADHD children through multimodal magnetic resonance imaging. Front Syst Neurosci 6:63
Sato H, Yahata N, Funane T, Takizawa R, Katura T, Atsumori H, Nishimura Y, Kinoshita A, Kiguchi M, Koizumi H, Fukuda M, Kasai K (2013) A NIRS-fMRI investigation of prefrontal cortex activity during a working memory task. Neuroimage 83:158–173
Naseer N, Hong SK (2015) fNIRS-based brain–computer interfaces: a review. Front Hum Neurosci 9:3
Acknowledgements
This study was supported by the TUBITAK under Project Number 114S47.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that there is no conflict of interest regarding the publication of this article.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Güven, A., Altınkaynak, M., Dolu, N. et al. Combining functional near-infrared spectroscopy and EEG measurements for the diagnosis of attention-deficit hyperactivity disorder. Neural Comput & Applic 32, 8367–8380 (2020). https://doi.org/10.1007/s00521-019-04294-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00521-019-04294-7