Multimodal Virtual Reality-Based Assessment of Adult ADHD: A Feasibility Study in Healthy Subjects

Neuropsychological assessments are often surprisingly inaccurate in mapping clinically-reported attention-deficit hyperactivity disorder (ADHD) symptoms, presumably due to their low ecological validity. Virtual reality (VR) might offer a potential solution for this problem, given its capability to generate standardized and yet highly realistic virtual environments. As the first adaptation of existing virtual classroom scenarios to an adult population, we developed a Virtual Seminar Room (VSR) for multimodal characterization of ADHD symptoms. To test its feasibility, N = 35 healthy participants were immersed into the VSR via a head-mounted display and carried out a VR-embedded continuous performance task (CPT) under varying levels of distractions in two experimental blocks (24 min each). CPT performance, electroencephalography (EEG) measures, and head movements (actigraphy) were simultaneously recorded and analyzed offline. Although CPT performance remained constant throughout the task, head movements increased significantly from Block 1 to Block 2. In addition, EEG theta (4–7 Hz) and beta (13–30 Hz) power was higher during Block 1 than Block 2, and during distractor-present than distractor-absent phases. Moreover, P300 amplitudes were higher during Block 1 than Block 2, and P300 latencies were prolonged in distractor-absent compared with distractor-present phases. Although the paradigm awaits further improvements, this study confirms the general feasibility of the VSR and provides a first step toward a multimodal, ecologically valid, and reliable VR-based adult ADHD assessment.

[1]  U. Ettinger,et al.  The Eyes Have It: A Meta-analysis of Oculomotor Inhibition in ADHD. , 2021, Biological psychiatry. Cognitive neuroscience and neuroimaging.

[2]  Sarah L. Jones,et al.  EEG for Diagnosis of Adult ADHD: A Systematic Review With Narrative Analysis , 2020, Frontiers in Psychiatry.

[3]  Hanneke van Dijk,et al.  Different Spectral Analysis Methods for the Theta/Beta Ratio Calculate Different Ratios But Do Not Distinguish ADHD from Controls , 2020, Applied psychophysiology and biofeedback.

[4]  P. Pauli,et al.  The Influence of Methylphenidate on Hyperactivity and Attention Deficits in Children With ADHD: A Virtual Classroom Test , 2020, Journal of attention disorders.

[5]  R. Barry,et al.  The Theta/Beta Ratio as an Index of Cognitive Processing in Adults With the Combined Type of Attention Deficit Hyperactivity Disorder , 2019, Clinical EEG and neuroscience.

[6]  Ortal Slobodin,et al.  Gender Differences in Objective and Subjective Measures of ADHD Among Clinic-Referred Children , 2019, Front. Hum. Neurosci..

[7]  C. Kelly,et al.  EEG spectral power, but not theta/beta ratio, is a neuromarker for adult ADHD , 2019, bioRxiv.

[8]  R. Barkley Neuropsychological Testing is Not Useful in the Diagnosis of ADHD: Stop It (or Prove It)! , 2019, The ADHD Report.

[9]  Marcus Magnor,et al.  Immersive EEG: Evaluating Electroencephalography in Virtual Reality , 2019, 2019 IEEE Conference on Virtual Reality and 3D User Interfaces (VR).

[10]  Robert J. Barry,et al.  Frontal EEG theta/beta ratio during mind wandering episodes , 2019, Biological Psychology.

[11]  Trish L. Varao-Sousa,et al.  In the lab and in the wild: How distraction and mind wandering affect attention and memory , 2018, Cognitive Research: Principles and Implications.

[12]  B. Franke,et al.  Live fast, die young? A review on the developmental trajectories of ADHD across the lifespan , 2018, European Neuropsychopharmacology.

[13]  Celestino Rodríguez,et al.  Efficacy of a Continuous Performance Test Based on Virtual Reality in the Diagnosis of ADHD and Its Clinical Presentations , 2018, Journal of attention disorders.

[14]  Jim Lagopoulos,et al.  Is the Theta/Beta EEG Marker for ADHD Inherently Flawed? , 2018, Journal of attention disorders.

[15]  Jaehyun Park,et al.  Virtual reality sickness questionnaire (VRSQ): Motion sickness measurement index in a virtual reality environment. , 2018, Applied ergonomics.

[16]  A. Lundervold,et al.  Event-Related-Potential (ERP) Correlates of Performance Monitoring in Adults With Attention-Deficit Hyperactivity Disorder (ADHD) , 2018, Front. Psychol..

[17]  R. Silberstein,et al.  Continuous performance task in ADHD: Is reaction time variability a key measure? , 2018, Neuropsychiatric disease and treatment.

[18]  R. Alarcón,et al.  Non‐normal data: Is ANOVA still a valid option? , 2017, Psicothema.

[19]  Joel M. Cooper,et al.  Assessing Cognitive Distraction Using Event Related Potentials , 2017 .

[20]  R. Barry,et al.  Atypical interference control in children with AD/HD with elevated theta/beta ratio , 2017, Biological Psychology.

[21]  D. David,et al.  . Virtual-reality-based attention assessment of , 2018 .

[22]  W. Does,et al.  Frontal EEG theta/beta ratio as an electrophysiological marker for attentional control and its test-retest reliability , 2016, Biological Psychology.

[23]  T. Kishimoto,et al.  Event-related potentials reflect the efficacy of pharmaceutical treatments in children and adolescents with attention deficit/hyperactivity disorder , 2016, Psychiatry Research.

[24]  Venke Arntsberg Grane,et al.  ERP Correlates of Proactive and Reactive Cognitive Control in Treatment-Naïve Adult ADHD , 2016, PloS one.

[25]  H. B. Meziane,et al.  Attention-related EEG markers in adult ADHD , 2016, Neuropsychologia.

[26]  M. Groom,et al.  The clinical utility of the continuous performance test and objective measures of activity for diagnosing and monitoring ADHD in children: a systematic review , 2016, European Child & Adolescent Psychiatry.

[27]  U. Díaz-Orueta,et al.  AULA—Advanced Virtual Reality Tool for the Assessment of Attention , 2016, Journal of attention disorders.

[28]  Frederic M. Stoll,et al.  The Effects of Cognitive Control and Time on Frontal Beta Oscillations. , 2016, Cerebral cortex.

[29]  T. Parsons Virtual Reality for Enhanced Ecological Validity and Experimental Control in the Clinical, Affective and Social Neurosciences , 2015, Front. Hum. Neurosci..

[30]  B. Franke,et al.  White matter microstructure and developmental improvement of hyperactive/impulsive symptoms in attention-deficit/hyperactivity disorder. , 2015, Journal of child psychology and psychiatry, and allied disciplines.

[31]  B. Franke,et al.  Cognitive heterogeneity in adult attention deficit/hyperactivity disorder: A systematic analysis of neuropsychological measurements , 2015, European Neuropsychopharmacology.

[32]  Riccardo Barbieri,et al.  EEG-based index for engagement level monitoring during sustained attention , 2015, 2015 37th Annual International Conference of the IEEE Engineering in Medicine and Biology Society (EMBC).

[33]  J. Sergeant,et al.  When self-report diverges from performance: The usage of BIS-11 along with neuropsychological tests , 2014, Psychiatry Research.

[34]  K. Lange,et al.  Utility of cognitive neuropsychological assessment in attention-deficit/hyperactivity disorder , 2014, ADHD Attention Deficit and Hyperactivity Disorders.

[35]  Bart Verkuil,et al.  EEG theta/beta ratio as a potential biomarker for attentional control and resilience against deleterious effects of stress on attention , 2013, Cognitive, Affective, & Behavioral Neuroscience.

[36]  R. Tannock,et al.  Neurophysiological differences in inhibitory control between adults with ADHD and their peers , 2013, Neuropsychologia.

[37]  Joseph S. Raiker,et al.  Reaction time variability in ADHD: a meta-analytic review of 319 studies. , 2013, Clinical psychology review.

[38]  H. Kraemer,et al.  A Decade of EEG Theta/Beta Ratio Research in ADHD , 2013, Journal of attention disorders.

[39]  D. Rojas,et al.  Neuronal effects of auditory distraction on visual attention , 2013, Brain and Cognition.

[40]  F. Rist,et al.  Electrophysiological indices of error monitoring in juvenile and adult attention deficit hyperactivity disorder (ADHD)--a meta-analytic appraisal. , 2013, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[41]  H. Möller,et al.  Associations between trait impulsivity and prepotent response inhibition , 2012, Journal of clinical and experimental neuropsychology.

[42]  C. Fabrigoule,et al.  Impact of time on task on ADHD patient's performances in a virtual classroom. , 2012, European journal of paediatric neurology : EJPN : official journal of the European Paediatric Neurology Society.

[43]  S. Loo,et al.  Clinical Utility of EEG in Attention Deficit Hyperactivity Disorder , 2005, Applied neuropsychology.

[44]  A. Brzezicka,et al.  β band oscillations engagement in human alertness process. , 2012, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[45]  B. Pennington,et al.  Validity of DSM-IV attention deficit/hyperactivity disorder symptom dimensions and subtypes. , 2012, Journal of abnormal psychology.

[46]  M. Tsai,et al.  Auditory event-related potentials in children with attention deficit hyperactivity disorder. , 2012, Pediatrics and neonatology.

[47]  Chongxun Zheng,et al.  Electroencephalogram and electrocardiograph assessment of mental fatigue in a driving simulator. , 2012, Accident; analysis and prevention.

[48]  E. Walker,et al.  Diagnostic and Statistical Manual of Mental Disorders , 2013 .

[49]  Melissa A. Cyders,et al.  Measurement of constructs using self-report and behavioral lab tasks: is there overlap in nomothetic span and construct representation for impulsivity? , 2011, Clinical psychology review.

[50]  P. Czobor,et al.  P300 deficits in adults with attention deficit hyperactivity disorder: a meta-analysis , 2010, Psychological Medicine.

[51]  Emanuel Schmider,et al.  Is It Really Robust , 2010 .

[52]  A. Asbjørnsen,et al.  An Examination of Shared Variance in Self-Report and Objective Measures of Attention in the Incarcerated Adult Population , 2010, Journal of attention disorders.

[53]  C. C. Duncan,et al.  Event-related potentials in clinical research: Guidelines for eliciting, recording, and quantifying mismatch negativity, P300, and N400 , 2009, Clinical Neurophysiology.

[54]  Todd Bowerly,et al.  A Virtual Reality Scenario for All Seasons: The Virtual Classroom , 2009, CNS Spectrums.

[55]  Albert A. Rizzo,et al.  Distractibility in Attention/Deficit/ Hyperactivity Disorder (ADHD): The Virtual Reality Classroom , 2009, Child neuropsychology : a journal on normal and abnormal development in childhood and adolescence.

[56]  J. Polich Updating P300: An integrative theory of P3a and P3b , 2007, Clinical Neurophysiology.

[57]  J. Galen Buckwalter,et al.  A Controlled Clinical Comparison of Attention Performance in Children with ADHD in a Virtual Reality Classroom Compared to Standard Neuropsychological Methods , 2007, Child neuropsychology : a journal on normal and abnormal development in childhood and adolescence.

[58]  Yuanyuan Zhang,et al.  Attentional processing in adults with ADHD as reflected by event-related potentials , 2007, Neuroscience Letters.

[59]  H. Roeyers,et al.  State Regulation in Adult ADHD: An Event-related Potential Study , 2006, Journal of clinical and experimental neuropsychology.

[60]  J. Hall,et al.  A Meta-analysis of Quantitative EEG Power Associated With Attention-Deficit Hyperactivity Disorder , 2006, Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society.

[61]  T. Demiralp,et al.  Comparative analysis of event-related potentials during Go/NoGo and CPT: Decomposition of electrophysiological markers of response inhibition and sustained attention , 2006, Brain Research.

[62]  W. Klimesch,et al.  Relevance of EEG alpha and theta oscillations during task switching , 2006, Experimental Brain Research.

[63]  Maarten A. S. Boksem,et al.  Effects of mental fatigue on attention: an ERP study. , 2005, Brain research. Cognitive brain research.

[64]  Joel T. Nigg,et al.  Causal Heterogeneity in Attention-Deficit/Hyperactivity Disorder: Do We Need Neuropsychologically Impaired Subtypes? , 2005, Biological Psychiatry.

[65]  B. Pennington,et al.  Validity of the Executive Function Theory of Attention-Deficit/Hyperactivity Disorder: A Meta-Analytic Review , 2005, Biological Psychiatry.

[66]  S. Nieuwenhuis,et al.  The Beneficial Effect of Concurrent Task-Irrelevant Mental Activity on Temporal Attention , 2005, Psychological science.

[67]  D. Marks,et al.  The Utility of Self-Report Measures and the Continuous Performance Test in the Diagnosis of ADHD in Adults , 2004, CNS Spectrums.

[68]  J. Epstein,et al.  Neuropsychology of adults with attention-deficit/hyperactivity disorder: a meta-analytic review. , 2004, Neuropsychology.

[69]  J. Barrett Side Effects of Virtual Environments: A Review of the Literature , 2004 .

[70]  Arnaud Delorme,et al.  EEGLAB: an open source toolbox for analysis of single-trial EEG dynamics including independent component analysis , 2004, Journal of Neuroscience Methods.

[71]  Adrian Angold,et al.  Relations Between Continuous Performance Test Performance Measures and ADHD Behaviors , 2003, Journal of abnormal child psychology.

[72]  James L. Szalma,et al.  The Vigilance Decrement Reflects Limitations in Effortful Attention, Not Mindlessness , 2003, Hum. Factors.

[73]  R. Barry,et al.  A review of electrophysiology in attention-deficit/hyperactivity disorder: I. Qualitative and quantitative electroencephalography , 2003, Clinical Neurophysiology.

[74]  Shana Nichols,et al.  A Review of the Validity of Laboratory Cognitive Tasks Used to Assess Symptoms of ADHD , 2003, Child psychiatry and human development.

[75]  Robert J Barry,et al.  Specificity of quantitative EEG analysis in adults with attention deficit hyperactivity disorder , 2002, Psychiatry Research.

[76]  J. Sangorrín,et al.  [Cognitive evoked potentials in the hyperactivity attention deficit disorder]. , 2002, Revista de neurologia.

[77]  J. D. Ball,et al.  Neuropsychological Characteristics of Adults with ADHD: A Comprehensive Review of Initial Studies , 2002, The Clinical neuropsychologist.

[78]  L. Eyde,et al.  Psychological testing and psychological assessment. A review of evidence and issues. , 2001, The American psychologist.

[79]  E Gordon,et al.  The Modulation of Late Component Event Related Potentials by Pre-Stimulus EEG Theta Activity in ADHD , 2001, The International journal of neuroscience.

[80]  H Stanislaw,et al.  Calculation of signal detection theory measures , 1999, Behavior research methods, instruments, & computers : a journal of the Psychonomic Society, Inc.

[81]  J. C. Ballard Computerized assessment of sustained attention: a review of factors affecting vigilance performance. , 1996, Journal of clinical and experimental neuropsychology.

[82]  J. C. Ballard Computerized assessment of sustained attention: interactive effects of task demand, noise, and anxiety. , 1996, Journal of clinical and experimental neuropsychology.

[83]  M. Hautus Corrections for extreme proportions and their biasing effects on estimated values ofd′ , 1995 .

[84]  R. Barkley The ecological validity of laboratory and analogue assessment methods of ADHD symptoms , 1991, Journal of abnormal child psychology.

[85]  P. Lachenbruch Statistical Power Analysis for the Behavioral Sciences (2nd ed.) , 1989 .

[86]  F. Perrin,et al.  Spherical splines for scalp potential and current density mapping. , 1989, Electroencephalography and clinical neurophysiology.

[87]  T R Zentall,et al.  Optimal stimulation: a model of disordered activity and performance in normal and deviant children. , 1983, Psychological bulletin.

[88]  T. Ishihara,et al.  Multivariate analytic study of EEG and mental activity in juvenile delinquents. , 1972, Electroencephalography and clinical neurophysiology.

[89]  Jacob Cohen Statistical Power Analysis for the Behavioral Sciences , 1969, The SAGE Encyclopedia of Research Design.

[90]  E. John,et al.  Evoked-Potential Correlates of Stimulus Uncertainty , 1965, Science.

[91]  H E ROSVOLD,et al.  A continuous performance test of brain damage. , 1956, Journal of consulting psychology.

[92]  A. Rizzo,et al.  A Review of Virtual Classroom Environments for Neuropsychological Assessment , 2019, Virtual Reality for Psychological and Neurocognitive Interventions.

[93]  A. Kovaleva,et al.  Eine Kurzskala zur Messung von Impulsivität nach dem UPPS-Ansatz: Die Skala Impulsives-Verhalten-8 (I-8) , 2012 .

[94]  M. Herrmann,et al.  Increased EEG power density in alpha and theta bands in adult ADHD patients , 2008, Journal of Neural Transmission.

[95]  H. Niemann,et al.  Skala zur Erfassung von Aufmerksamkeitsdefiziten (SEA) Erste psychometrische Evaluation mit einer Rasch-Analyse , 2007 .

[96]  Martin J. Herrmann,et al.  Stability of Late Event-Related Potentials: Topographical Descriptors of Motor Control Compared with the P300 Amplitude , 2004, Brain Topography.

[97]  M. Alecha,et al.  Potenciales evocados cognitivos en el trastorno por déficit de atención con hiperactividad , 2002 .

[98]  J. Lubar,et al.  The development of a quantitative electroencephalographic scanning process for attention deficit-hyperactivity disorder: reliability and validity studies. , 2001, Neuropsychology.