Abnormally Enhanced Midfrontal Theta-Band Activity During Response Monitoring in Youth with Obsessive-Compulsive Disorder

Published:November 12, 2022DOI:



      Response monitoring, as reflected in the electroencephalogram (EEG) recording after commission of errors, has been consistently shown to be abnormally enhanced in individuals with obsessive-compulsive disorder (OCD). This has been traditionally quantified as error-related negativity (ERN) and may reflect abnormal neurophysiological mechanisms underlying OCD. However, the ERN reflects the increase in phase-locked activities, particularly in the theta-band (4-8 Hz), and does not reflect non-phase-locked activities. To more broadly interrogate midfrontal theta-band activity in a brain region essential for complex cognition, this study investigated theta-band abnormalities during response monitoring in OCD participants for a better understanding of the mechanism underlying the ERN.


      EEG data were recorded from 99 participants with pediatric OCD and 99 sex- and age-matched healthy control (HC) participants while they completed the arrow flanker task. Effects of Group (OCD, HC) and Response type (Error, Correct) on post-response theta-band total power and inter-trial phase coherence (ITPC) were examined using mixed analysis of covariance and Bayesian analyses controlling for sex and accuracy.


      Theta-band total power was larger on Error than Correct trials and larger in OCD than HC participants, but there was no effect of response type between groups. Theta-band ITPC was larger on Error than Correct trials, but there were no group difference nor response type difference between groups. Correlations of theta-band total power and ITPC with clinical measures were overall small.


      Abnormally enhanced midfrontal theta-band total power, but not ITPC, may reflect ineffective heightened response monitoring or compensatory activity in pediatric OCD.


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      1. American Psychiatric Association (2013): Diagnostic and Statistical Manual of Mental Disorders (5th Ed.). Washington, D.C.: American Psychiatric Association.

        • Kessler R.C.
        • Chiu W.T.
        • Demler O.
        • Walters E.E.
        Prevalence, severity, and comorbidity of 12-month dsm-iv disorders in the national comorbidity survey replication.
        Arch Gen Psychiatry. 2005; 62: 617-627
        • Ruscio A.M.
        • Stein D.J.
        • Chiu W.T.
        • Kessler R.C.
        The epidemiology of obsessive-compulsive disorder in the National Comorbidity Survey Replication.
        Mol Psychiatry. 2010; 15: 53-63
        • The Pediatric OCD Treatment Study (POTS) Team
        Cognitive-behavior therapy, sertraline, and their combination for children and adolescents with obsessive-compulsive disorder: The pediatric OCD treatment study (POTS) randomized controlled trial.
        JAMA. 2004; 292: 1969-1976
        • Krebs G.
        • Heyman I.
        Obsessive-compulsive disorder in children and adolescents.
        Arch Dis Child. 2015; 100: 495-499
        • Riesel A.
        The erring brain: Error-related negativity as an endophenotype for OCD—A review and meta-analysis.
        Psychophysiology. 2019; 56e13348
        • Gehring W.J.
        • Goss B.
        • Coles M.G.H.
        • Meyer D.E.
        • Donchin E.
        A neural system for error detection and compensation.
        Psychol Sci. 1993; 4: 385-390
        • Falkenstein M.
        • Hohnsbein J.
        • Hoormann J.
        • Blanke L.
        Effects of crossmodal divided attention on late ERP components. II. Error processing in choice reaction tasks.
        Electroencephalogr Clin Neurophysiol. 1991; 78: 447-455
        • Riesel A.
        • Weinberg A.
        • Endrass T.
        • Meyer A.
        • Hajcak G.
        The ERN is the ERN is the ERN? Convergent validity of error-related brain activity across different tasks.
        Biol Psychol. 2013; 93: 377-385
        • Dehaene S.
        • Posner M.I.
        • Tucker D.M.
        Localization of a neural system for error detection and compensation.
        Psychol Sci. 1994; 5: 303-305
        • Holroyd C.B.
        • Coles M.G.H.
        The neural basis of human error processing: Reinforcement learning, dopamine, and the error-related negativity.
        Psychol Rev. 2002; 109: 679-709
        • Iannaccone R.
        • Hauser T.U.
        • Staempfli P.
        • Walitza S.
        • Brandeis D.
        • Brem S.
        Conflict monitoring and error processing: New insights from simultaneous EEG–fMRI.
        NeuroImage. 2015; 105: 395-407
        • Suzuki T.
        • Ait Oumeziane B.
        • Novak K.
        • Samuel D.B.
        • Foti D.
        Error-monitoring across social and affective processing contexts.
        Int J Psychophysiol. 2020; 150: 37-49
        • Olvet D.M.
        • Hajcak G.
        The error-related negativity relates to sadness following mood induction among individuals with high neuroticism.
        Soc Cogn Affect Neurosci nsr007. 2011;
        • Olvet D.M.
        • Hajcak G.
        The error-related negativity (ERN) and psychopathology: Toward an endophenotype.
        Clin Psychol Rev. 2008; 28: 1343-1354
        • Coles M.G.H.
        • Scheffers M.K.
        • Holroyd C.B.
        Why is there an ERN/Ne on correct trials? Response representations, stimulus-related components, and the theory of error-processing.
        Biol Psychol. 2001; 56: 173-189
        • Yeung N.
        • Botvinick M.M.
        • Cohen J.D.
        The neural basis of error detection: Conflict monitoring and the error-related negativity.
        Psychol Rev. 2004; 111: 931-959
        • Weinberg A.
        • Hajcak G.
        Longer term test–retest reliability of error-related brain activity.
        Psychophysiology. 2011; 48: 1420-1425
        • Riesel A.
        • Endrass T.
        • Auerbach L.A.
        • Kathmann N.
        Overactive performance monitoring as an endophenotype for obsessive-compulsive disorder: Evidence from a treatment study.
        Am J Psychiatry. 2015; 172: 665-673
        • Anokhin A.P.
        • Golosheykin S.
        • Heath A.C.
        Heritability of frontal brain function related to action monitoring.
        Psychophysiology. 2008; 45: 524-534
        • Davies P.L.
        • Segalowitz S.J.
        • Gavin W.J.
        Development of Response-Monitoring ERPs in 7- to 25-Year-Olds.
        Dev Neuropsychol. 2004; 25: 355-376
        • Grammer J.K.
        • Carrasco M.
        • Gehring W.J.
        • Morrison F.J.
        Age-related changes in error processing in young children: A school-based investigation.
        Dev Cogn Neurosci. 2014; 9: 93-105
      2. Luck SJ (2014): An Introduction to the Event-Related Potential Technique. MIT Press.

        • Phillips J.M.
        • Everling S.
        Event-related potentials associated with performance monitoring in non-human primates.
        NeuroImage. 2014; 97: 308-320
        • Sajad A.
        • Godlove D.C.
        • Schall J.D.
        Cortical microcircuitry of performance monitoring [no. 2].
        Nat Neurosci. 2019; 22: 265-274
        • Robble M.A.
        • Schroder H.S.
        • Kangas B.D.
        • Nickels S.
        • Breiger M.
        • Iturra-Mena A.M.
        • et al.
        Concordant neurophysiological signatures of cognitive control in humans and rats [no. 7].
        Neuropsychopharmacol. 2021; 46: 1252-1262
        • Narayanan V.
        • Heiming R.S.
        • Jansen F.
        • Lesting J.
        • Sachser N.
        • Pape H.-C.
        • Seidenbecher T.
        Social Defeat: Impact on Fear Extinction and Amygdala-Prefrontal Cortical Theta Synchrony in 5-HTT Deficient Mice.
        PLOS ONE. 2011; 6e22600
      3. Cohen MX (2017): Neurophysiological oscillations and action monitoring. The Wiley Handbook of Cognitive Control. John Wiley & Sons, Ltd, pp 242–258.

      4. Cohen MX (2014): Analyzing Neural Time Series Data: Theory and Practice. MIT Press.

        • Wang X.-J.
        Neurophysiological and computational principles of cortical rhythms in cognition.
        Physiol Rev. 2010; 90: 1195-1268
        • Trujillo L.T.
        • Allen J.J.B.
        Theta EEG dynamics of the error-related negativity.
        Clin Neurophysiol. 2007; 118: 645-668
        • Cavanagh J.F.
        • Cohen M.X.
        • Allen J.J.B.
        Prelude to and resolution of an error: EEG phase synchrony reveals cognitive control dynamics during action monitoring.
        J Neurosci. 2009; 29: 98-105
        • Cavanagh J.F.
        • Shackman A.J.
        Frontal midline theta reflects anxiety and cognitive control: Meta-analytic evidence.
        J Physiol-Paris. 2015; 109: 3-15
      5. Grove TB, Lasagna CA, Martinez-Cancino R, Pamidighantam P, Deldin PJ, Tso IF (2020): Neural oscillatory abnormalities duringgaze processing in schizophrenia: Evidence of reduced theta phase consistency and inter-areal theta-gamma coupling. Biol Psychiatry Cogn Neurosci Neuroimaging.

        • Sandre A.
        • Weinberg A.
        Neither wrong nor right: Theta and delta power increase during performance monitoring under conditions of uncertainty.
        Int J Psychophysiol. 2019; 146: 225-239
        • Peris T.S.
        • Salgari G.
        • Perez J.
        • Jurgiel J.
        • Vreeland A.
        • O’Neill J.
        • et al.
        Shared and unique neural mechanisms underlying pediatric trichotillomania and obsessive compulsive disorder.
        Psychiatry Res. 2021; 298113653
        • Carmi L.
        • Alyagon U.
        • Barnea-Ygael N.
        • Zohar J.
        • Zangen A.
        • Dar R.
        From self-induced to perceived errors – A generalized over-monitoring activity in obsessive–compulsive disorder.
        Eur Neuropsychopharmacol. 2019; 29: 1083-1091
        • Riesel A.
        • Kathmann N.
        • Endrass T.
        Overactive performance monitoring in obsessive–compulsive disorder is independent of symptom expression.
        Eur Arch Psychiatry Clin Neurosci. 2014; 264: 707-717
        • Scahill L.
        • Riddle M.A.
        • McSwiggin-Hardin M.
        • Ort S.I.
        • King R.A.
        • Goodman W.K.
        • et al.
        Children’s Yale-Brown Obsessive Compulsive Scale: Reliability and Validity.
        J Am Acad Child Adolesc Psychiatry. 1997; 36: 844-852
        • Kaufman J.
        • Birmaher B.
        • Brent D.
        • Rao U.
        • Flynn C.
        • Moreci P.
        • et al.
        Schedule for Affective Disorders and Schizophrenia for School-Age Children-Present and Lifetime Version (K-SADS-PL): initial reliability and validity data.
        J Am Acad Child Adolesc Psychiatry. 1997; 36: 980-988
      6. Hanna GL (2013): Schedule for Obsessive-Compulsive and Other Behavioral Syndromes (SOCOBS). Ann Arbor, MI: University of Michigan.

      7. Culbertson WC, Zillmer EA (n.d.): Tower of London-Drexel University (TOL DX), 2001. Multi-Health Syst Chic IL.

      8. Achenbach TM, Rescorla LA (2001): Manual for the ASEBA school-age forms & profiles: an integrated system of multi-informant assessment Burlington, VT: University of Vermont. Res Cent Child Youth Fam 1617.

        • Hudziak J.J.
        • Althoff R.R.
        • Stanger C.
        • van Beijsterveldt C.e. m.
        • Nelson E.C.
        • Hanna G.L.
        • et al.
        The Obsessive Compulsive Scale of the Child Behavior Checklist predicts obsessive-compulsive disorder: a receiver operating characteristic curve analysis.
        J Child Psychol Psychiatry. 2006; 47: 160-166
        • Eriksen B.A.
        • Eriksen C.W.
        Effects of noise letters upon the identification of a target letter in a nonsearch task.
        Percept Psychophys. 1974; 16: 143-149
      9. The Mathworks, Inc. (2019): MATLAB, version 2019a. Natick, MA.

        • Delorme A.
        • Makeig S.
        EEGLAB: an open source toolbox for analysis of single-trial EEG dynamics including independent component analysis.
        J Neurosci Methods. 2004; 134: 9-21
        • Foti D.
        • Kotov R.
        • Hajcak G.
        Psychometric considerations in using error-related brain activity as a biomarker in psychotic disorders.
        J Abnorm Psychol. 2013; 122: 520-531
        • Keil A.
        • Bernat E.M.
        • Cohen M.X.
        • Ding M.
        • Fabiani M.
        • Gratton G.
        • et al.
        Recommendations and publication guidelines for studies using frequency domain and time-frequency domain analyses of neural time series.
        Psychophysiology. 2022; 59e14052
        • Hanna G.L.
        • Liu Y.
        • Isaacs Y.E.
        • Ayoub A.M.
        • Brosius A.
        • Salander Z.
        • et al.
        Error-related brain activity in adolescents with obsessive-compulsive disorder and major depressive disorder.
        Depress Anxiety. 2018; 35: 752-760
        • Hanna G.L.
        • Liu Y.
        • Isaacs Y.E.
        • Ayoub A.M.
        • Torres J.J.
        • O’Hara N.B.
        • Gehring W.J.
        Withdrawn/depressed behaviors and error-related brain activity in youth with obsessive-compulsive disorder.
        J Am Acad Child Adolesc Psychiatry. 2016; 55: 906-913.e2
      10. R Core Team (2019): R: A Language and environment for statistical computing. Retrieved May 30, 2017, from

      11. Revelle W (2019, January 12): psych: Procedures for psychological, psychometric, and personality research, version 1.8.12. Retrieved September 11, 2019, from

      12. Kuznetsova A, Brockhoff PB, Christensen RHB, Jensen SP (2020, October 23): lmerTest: Tests in Linear Mixed Effects Models, version 3.1-3. Retrieved August 30, 2021, from

      13. Su Y-S, Yajima M (2020, April 27): R2jags: Using R to Run “JAGS,” version 0.6-1. Retrieved November 1, 2021, from

      14. Plummer M (2003): JAGS: A Program for Analysis of Bayesian Graphical Models Using Gibbs Sampling. 10.

      15. Sarkar D, Andrews F, Wright (documentation) K, Klepeis N, title) JL (colorkey, Murrell P (2021, May 2): lattice: Trellis Graphics for R, version 0.20-44. Retrieved November 1, 2021, from

      16. Wickham H (2011): ggplot2. Wiley Interdiscip Rev Comput Stat 3: 180–185.

        • Cohen J.
        A power primer.
        Psychol Bull. 1992; 112: 155-159
        • Groom M.J.
        • Cahill J.D.
        • Bates A.T.
        • Jackson G.M.
        • Calton T.G.
        • Liddle P.F.
        • Hollis C.
        Electrophysiological indices of abnormal error-processing in adolescents with attention deficit hyperactivity disorder (ADHD).
        J Child Psychol Psychiatry. 2010; 51: 66-76
        • Morris S.E.
        • Yee C.M.
        • Nuechterlein K.H.
        Electrophysiological analysis of error monitoring in schizophrenia.
        J Abnorm Psychol. 2006; 115: 239-250
      17. National Institute of Mental Health (2018, May 30): NIMH » RDoC Matrix. Retrieved May 30, 2018, from

        • McLoughlin G.
        • Gyurkovics M.
        • Palmer J.
        • Makeig S.
        Midfrontal theta activity in psychiatric illness: An index of cognitive vulnerabilities across disorders.
        Biol Psychiatry. 2021; 0
        • Moser J.
        • Moran T.
        • Schroder H.
        • Donnellan B.
        • Yeung N.
        On the relationship between anxiety and error monitoring: a meta-analysis and conceptual framework.
        Front Hum Neurosci. 2013; 7
        • do Rosario-Campos M.C.
        • Leckman J.F.
        • Curi M.
        • Quatrano S.
        • Katsovitch L.
        • Miguel E.C.
        • Pauls D.L.
        A family study of early-onset obsessive-compulsive disorder.
        Am J Med Genet B Neuropsychiatr Genet. 2005; 136B: 92-97
        • Davis L.K.
        • Yu D.
        • Keenan C.L.
        • Gamazon E.R.
        • Konkashbaev A.I.
        • Derks E.M.
        • et al.
        Partitioning the heritability of tourette syndrome and obsessive compulsive disorder reveals differences in genetic architecture.
        PLOS Genet. 2013; 9e1003864
        • Cavanagh J.F.
        • Zambrano‐Vazquez L.
        • Allen J.J.B.
        Theta lingua franca: A common mid-frontal substrate for action monitoring processes.
        Psychophysiology. 2012; 49: 220-238
        • Cohen M.X.
        Error-related medial frontal theta activity predicts cingulate-related structural connectivity.
        NeuroImage. 2011; 55: 1373-1383
        • Suzuki T.
        • Hill K.E.
        • Ait Oumeziane B.
        • Foti D.
        • Samuel D.B.
        Bringing the brain into personality assessment: Is there a place for event-related potentials?.
        Psychol Assess. 2018; 31: 488-501
        • Lauriola M.
        • Panno A.
        • Levin I.P.
        • Lejuez C.W.
        Individual differences in risky decision making: A meta‐analysis of sensation seeking and impulsivity with the balloon analogue risk task.
        J Behav Decis Mak. 2014; 27: 20-36
        • Owens M.M.
        • Potter A.
        • Hyatt C.S.
        • Albaugh M.
        • Thompson W.K.
        • Jernigan T.
        • et al.
        Recalibrating expectations about effect size: A multi-method survey of effect sizes in the ABCD study.
        PloS One. 2021; 16e0257535
        • Meyer A.
        • Weinberg A.
        • Klein D.N.
        • Hajcak G.
        The development of the error-related negativity (ERN) and its relationship with anxiety: Evidence from 8 to 13 year-olds.
        Dev Cogn Neurosci. 2012; 2: 152-161
        • Hill K.E.
        • Samuel D.B.
        • Foti D.
        Contextualizing individual differences in error monitoring: Links with impulsivity, negative affect, and conscientiousness.
        Psychophysiology. 2016; 53: 1143-1153
        • Carmi L.
        • Alyagon U.
        • Barnea-Ygael N.
        • Zohar J.
        • Dar R.
        • Zangen A.
        Clinical and electrophysiological outcomes of deep TMS over the medial prefrontal and anterior cingulate cortices in OCD patients.
        Brain Stimulat. 2018; 11: 158-165
        • Solomon E.A.
        • Sperling M.R.
        • Sharan A.D.
        • Wanda P.A.
        • Levy D.F.
        • Lyalenko A.
        • et al.
        Theta-burst stimulation entrains frequency-specific oscillatory responses.
        Brain Stimulat. 2021; 14: 1271-1284
        • Carrasco M.
        • Harbin S.M.
        • Nienhuis J.K.
        • Fitzgerald K.D.
        • Gehring W.J.
        • Hanna G.L.
        Increased Error-Related Brain Activity in Youth with Obsessive-Compulsive Disorder and Unaffected Siblings.
        Depress Anxiety. 2013; 30: 39-46
        • Gorka S.M.
        • Burkhouse K.L.
        • Klumpp H.
        • Kennedy A.E.
        • Afshar K.
        • Francis J.
        • et al.
        Error-related brain activity as a treatment moderator and index of symptom change during cognitive-behavioral therapy or selective serotonin reuptake inhibitors.
        Neuropsychopharmacology. 2018; 43: 1355-1363
        • Barnes J.J.M.
        • O’Connell R.G.
        • Nandam L.S.
        • Dean A.J.
        • Bellgrove M.A.
        Monoaminergic modulation of behavioural and electrophysiological indices of error processing.
        Psychopharmacology (Berl). 2014; 231: 379-392
        • Kujawa A.
        • MacNamara A.
        • Fitzgerald K.D.
        • Monk C.S.
        • Phan K.L.
        Enhanced neural reactivity to threatening faces in anxious youth: Evidence from event-related potentials.
        J Abnorm Child Psychol. 2015; 43: 1493-1501
        • Cohen M.X.
        • Donner T.H.
        Midfrontal conflict-related theta-band power reflects neural oscillations that predict behavior.
        J Neurophysiol. 2013; 110: 2752-2763