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Atypical Mediofrontal Theta Oscillations Underlying Cognitive Control in Kindergarteners With Autism Spectrum Disorder

Published:April 14, 2021DOI:https://doi.org/10.1016/j.bpsc.2021.03.016

      Abstract

      Background

      Children with autism spectrum disorder (ASD) often exhibit deficits in cognitive control. Neuroimaging approaches have implicated disruptions to mediofrontal cortex structure and function. However, previous work is limited in testing whether young children with ASD exhibit disruptions to task-related theta oscillations thought to arise from the mediofrontal cortex.

      Methods

      Children with ASD (n = 43) and age- and sex-matched typically developing peers (n = 24) at kindergarten entry performed a child-friendly Go/NoGo task while 64-channel electroencephalography was recorded. Time-frequency approaches were employed to assess the magnitude of mediofrontal theta oscillations immediately after error (vs. correct) responses (early theta) as well as later emerging theta oscillations (late theta). We tested whether error-related mediofrontal theta oscillations differed as a function of diagnosis (ASD/typical) and timing (early/late theta). In addition, links to social and academic outcomes were tested.

      Results

      Overall, children showed increased theta power after error versus correct responses. Compared with typically developing children, children with ASD exhibited a selective reduction in error-related mediofrontal theta power during the late time window. There were no significant group differences for early theta power. Moreover, reduced error-related theta power during the late, but not early, time window significantly predicted poorer academic and social skills.

      Conclusions

      Kindergarteners with ASD demonstrated a selective reduction in error-related mediofrontal theta power during a relatively late time window, which is consistent with impairments in specific cognitive processes that recruit top-down control. Targeting these particular cognitive control processes via intervention prior to school entry may promote more successful functional outcomes for children with ASD.

      Keywords

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      References

        • Botvinick M.M.
        • Braver T.S.
        • Barch D.M.
        • Carter C.S.
        • Cohen J.D.
        Conflict monitoring and cognitive control.
        Psychol Rev. 2001; 108: 624-652
        • Zelazo P.D.
        • Müller U.
        Executive function in typical and atypical development.
        in: Goswami U. The Wiley-Blackwell Handbook of Childhood Cognitive Development. 2nd ed. Wiley-Blackwell, 2011: 574-603
        • American Psychiatric Association, DSM-5 Task Force
        Diagnostic and Statistical Manual of Mental Disorders: DSM-5®.
        (Available at:) (American Psychiatric Publishing, Inc. Accessed December 1, 2021)
        • Demetriou E.A.
        • Lampit A.
        • Quintana D.S.
        • Naismith S.L.
        • Song Y.J.C.
        • Pye J.E.
        • et al.
        Autism spectrum disorders: A meta-analysis of executive function.
        Mol Psychiatry. 2018; 23: 1198-1204
        • Gilotty L.
        • Kenworthy L.
        • Sirian L.
        • Black D.O.
        • Wagner A.E.
        Adaptive skills and executive function in autism spectrum disorders.
        Child Neuropsychol. 2002; 8: 241-248
        • Griffith E.M.
        • Pennington B.F.
        • Wehner E.A.
        • Rogers S.J.
        Executive functions in young children with autism.
        Child Dev. 1999; 70: 817-832
        • Happé F.
        • Booth R.
        • Charlton R.
        • Hughes C.
        Executive function deficits in autism spectrum disorders and attention-deficit/hyperactivity disorder: Examining profiles across domains and ages.
        Brain Cogn. 2006; 61: 25-39
        • Hill E.L.
        Executive dysfunction in autism.
        Trends Cogn Sci. 2004; 8: 26-32
        • Jeste S.S.
        • Nelson 3rd, C.A.
        Event related potentials in the understanding of autism spectrum disorders: An analytical review.
        J Autism Dev Disord. 2009; 39: 495-510
        • DuPuis D.
        • Ram N.
        • Willner C.J.
        • Karalunas S.
        • Segalowitz S.J.
        • Gatzke-Kopp L.M.
        Implications of ongoing neural development for the measurement of the error-related negativity in childhood.
        Dev Sci. 2015; 18: 452-468
        • Buzzell G.A.
        • Barker T.V.
        • Troller-Renfree S.V.
        • Bernat E.M.
        • Bowers M.E.
        • Morales S.
        • et al.
        Adolescent cognitive control, theta oscillations, and social observation.
        Neuroimage. 2019; 198: 13-30
        • Cavanagh J.F.
        • Frank M.J.
        Frontal theta as a mechanism for cognitive control.
        Trends Cogn Sci. 2014; 18: 414-421
        • Herrmann C.S.
        • Strüber D.
        • Helfrich R.F.
        • Engel A.K.
        EEG oscillations: From correlation to causality.
        Int J Psychophysiol. 2016; 103: 12-21
        • Narayanan N.S.
        • Cavanagh J.F.
        • Frank M.J.
        • Laubach M.
        Common medial frontal mechanisms of adaptive control in humans and rodents.
        Nat Neurosci. 2013; 16: 1888-1895
        • Allan N.P.
        • Hume L.E.
        • Allan D.M.
        • Farrington A.L.
        • Lonigan C.J.
        Relations between inhibitory control and the development of academic skills in preschool and kindergarten: A meta-analysis.
        Dev Psychol. 2014; 50: 2368-2379
        • McClelland M.M.
        • Acock A.C.
        • Morrison F.J.
        The impact of kindergarten learning-related skills on academic trajectories at the end of elementary school.
        Early Child Res Q. 2006; 21: 471-490
        • Morrison F.J.
        • Ponitz C.C.
        • McClelland M.M.
        Self-regulation and academic achievement in the transition to school.
        in: Calkins S.D. Bell M.A. Human Brain Development. Child Development at the Intersection of Emotion and Cognition. American Psychological Association, Washington, DC2010: 203-224
        • Passolunghi M.C.
        • Costa H.M.
        Working memory and early numeracy training in preschool children.
        Child Neuropsychol. 2016; 22: 81-98
        • Willoughby M.T.
        • Blair C.B.
        • Wirth R.J.
        • Greenberg M.
        The measurement of executive function at age 5: Psychometric properties and relationship to academic achievement.
        Psychol Assess. 2012; 24: 226-239
        • Konstantareas M.M.
        • Stewart K.
        Affect regulation and temperament in children with autism spectrum disorder.
        J Autism Dev Disord. 2006; 36: 143-154
        • Christ S.E.
        • Holt D.D.
        • White D.A.
        • Green L.
        Inhibitory control in children with autism spectrum disorder.
        J Autism Dev Disord. 2007; 37: 1155-1165
        • Ridderinkhof K.R.
        • Ullsperger M.
        • Crone E.A.
        • Nieuwenhuis S.
        The role of the medial frontal cortex in cognitive control.
        Science. 2004; 306: 443-447
        • Agam Y.
        • Joseph R.M.
        • Barton J.J.S.
        • Manoach D.S.
        Reduced cognitive control of response inhibition by the anterior cingulate cortex in autism spectrum disorders.
        Neuroimage. 2010; 52: 336-347
        • Kana R.K.
        • Keller T.A.
        • Minshew N.J.
        • Just M.A.
        Inhibitory control in high-functioning autism: Decreased activation and underconnectivity in inhibition networks.
        Biol Psychiatry. 2007; 62: 198-206
        • Carter C.S.
        • Braver T.S.
        • Barch D.M.
        • Botvinick M.M.
        • Noll D.
        • Cohen J.D.
        Anterior cingulate cortex, error detection, and the online monitoring of performance.
        Science. 1998; 280: 747-749
        • Thakkar K.N.
        • Polli F.E.
        • Joseph R.M.
        • Tuch D.S.
        • Hadjikhani N.
        • Barton J.J.S.
        • Manoach D.S.
        Response monitoring, repetitive behaviour and anterior cingulate abnormalities in autism spectrum disorders (ASD).
        Brain. 2008; 131: 2464-2478
        • Haznedar M.M.
        • Buchsbaum M.S.
        • Wei T.C.
        • Hof P.R.
        • Cartwright C.
        • Bienstock C.A.
        • Hollander E.
        Limbic circuitry in patients with autism spectrum disorders studied with positron emission tomography and magnetic resonance imaging.
        Am J Psychiatry. 2000; 157: 1994-2001
        • Cavanagh J.F.
        • Cohen M.X.
        • Allen J.J.
        Prelude to and resolution of an error: EEG phase synchrony reveals cognitive control dynamics during action monitoring.
        J Neurosci. 2009; 29: 98-105
        • Cohen M.X.
        Error-related medial frontal theta activity predicts cingulate-related structural connectivity.
        Neuroimage. 2011; 55: 1373-1383
        • Verguts T.
        Binding by random bursts: A computational model of cognitive control.
        J Cogn Neurosci. 2017; 29: 1103-1118
        • Larrain-Valenzuela J.
        • Zamorano F.
        • Soto-Icaza P.
        • Carrasco X.
        • Herrera C.
        • Daiber F.
        • et al.
        Theta and alpha oscillation impairments in autistic spectrum disorder reflect working memory deficit.
        Sci Rep. 2017; 7: 14328
        • Chan A.S.
        • Han Y.M.Y.
        • Leung W.W.
        • Leung C.
        • Wong V.C.N.
        • Cheung M.
        Abnormalities in the anterior cingulate cortex associated with attentional and inhibitory control deficits: A neurophysiological study on children with autism spectrum disorders.
        Res Autism Spectr Disord. 2011; 5: 254-266
        • van Noordt S.
        • Wu J.
        • Venkataraman A.
        • Larson M.J.
        • South M.
        • Crowley M.J.
        Inter-trial coherence of medial frontal theta oscillations linked to differential feedback processing in youth and young adults with autism.
        Res Autism Spectr Disord. 2017; 37: 1-10
        • Yeung M.K.
        • Han Y.M.Y.
        • Sze S.L.
        • Chan A.S.
        Abnormal frontal theta oscillations underlie the cognitive flexibility deficits in children with high-functioning autism spectrum disorders.
        Neuropsychology. 2016; 30: 281-295
        • Lushchekina E.A.
        • Podreznaya E.D.
        • Lushchekin V.S.
        • Novototskii-Vlasov V.Y.
        • Strelets V.B.
        Comparative studies of EEG theta and gamma rhythms in normal children and children with early childhood autism.
        Neurosci Behav Physiol. 2014; 44: 902-908
        • Kim S.H.
        • Buzzell G.
        • Faja S.
        • Choi Y.B.
        • Thomas H.R.
        • Brito N.H.
        • et al.
        Neural dynamics of executive function in cognitively able kindergarteners with autism spectrum disorders as predictors of concurrent academic achievement.
        Autism. 2020; 24: 780-794
        • 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
        • Kim M.H.
        • Marulis L.M.
        • Grammer J.K.
        • Morrison F.J.
        • Gehring W.J.
        Motivational processes from expectancy-value theory are associated with variability in the error positivity in young children.
        J Exp Child Psychol. 2017; 155: 32-47
        • Kim M.H.
        • Grammer J.K.
        • Marulis L.M.
        • Carrasco M.
        • Morrison F.J.
        • Gehring W.J.
        Early math and reading achievement are associated with the error positivity.
        Dev Cogn Neurosci. 2016; 22: 18-26
        • Lord C.
        • Rutter M.
        • DiLavore P.
        • Risi S.
        • Gotham K.
        • Bishop S.
        Autism Diagnostic Observation Schedule (ADOS-2).
        Western Psychological Services, Los Angeles, CA2012
        • Gotham K.
        • Risi S.
        • Pickles A.
        • Lord C.
        The Autism Diagnostic Observation Schedule: Revised algorithms for improved diagnostic validity.
        J Autism Dev Disord. 2007; 37: 613-627
        • Achenbach T.M.
        Manual for the Child Behavior Checklist/4-18 and 1991 Profile.
        Department of Psychiatry, University of Vermont, Burlington, VT1991
        • Elliot C.
        Differential Ability Scales.
        2nd ed. Hartcourt Assessment, San Antonio, TX2007
        • Bishop S.L.
        • Farmer C.
        • Thurm A.
        Measurement of nonverbal IQ in autism spectrum disorder: Scores in young adulthood compared to early childhood.
        J Autism Dev Disord. 2015; 45: 966-974
        • Fantuzzo J.W.
        • Hampton V.R.
        Penn Interactive Peer Play Scale: A parent and teacher rating system for young children.
        in: Gitlin-Weiner K. Sandgrund A. Schaefer C. Play Diagnosis and Assessment. John Wiley and Sons, Inc., Hoboken, NJ2000: 599-620
        • Woodcock R.W.
        • McGrew K.S.
        • Mather N.
        • Schrank F.
        Woodcock-Johnson III: Tests of Achievement.
        Riverside Publishing, Itasca, IL2001
        • 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
        • Lamm C.
        • Walker O.L.
        • Degnan K.A.
        • Henderson H.A.
        • Pine D.S.
        • McDermott J.M.
        • Fox N.A.
        Cognitive control moderates early childhood temperament in predicting social behavior in 7-year-old children: An ERP study.
        Dev Sci. 2014; 17: 667-681
        • 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
        • Nolan H.
        • Whelan R.
        • Reilly R.B.
        FASTER: Fully automated statistical thresholding for EEG artifact rejection.
        J Neurosci Methods. 2010; 192: 152-162
        • Mognon A.
        • Jovicich J.
        • Bruzzone L.
        • Buiatti M.
        ADJUST: An automatic EEG artifact detector based on the joint use of spatial and temporal features.
        Psychophysiology. 2011; 48: 229-240
        • Bernat E.M.
        • Williams W.J.
        • Gehring W.J.
        Decomposing ERP time-frequency energy using PCA.
        Clin Neurophysiol. 2005; 116: 1314-1334
        • Debnath R.
        • Buzzell G.A.
        • Morales S.
        • Bowers M.E.
        • Leach S.C.
        • Fox N.A.
        The Maryland analysis of developmental EEG (MADE) pipeline.
        Psychophysiology. 2020; 57e13580
        • Winkler I.
        • Debener S.
        • Müller K.R.
        • Tangermann M.
        On the influence of high-pass filtering on ICA-based artifact reduction in EEG-ERP.
        Annu Int Conf IEEE Eng Med Biol Soc. 2015; 2015: 4101-4105
        • Viola F.C.
        • Debener S.
        • Thorne J.
        • Schneider T.
        Using ICA for the analysis of multi-channel EEG data.
        in: Simultaneous EEG and fMRI: Recording, Analysis, and Application. 2010: 121-133
        • Trujillo L.T.
        • Allen J.J.B.
        Theta EEG dynamics of the error-related negativity.
        Clin Neurophysiol. 2007; 118: 645-668
        • Steele V.R.
        • Anderson N.E.
        • Claus E.D.
        • Bernat E.M.
        • Rao V.
        • Assaf M.
        • et al.
        Neuroimaging measures of error-processing: Extracting reliable signals from event-related potentials and functional magnetic resonance imaging.
        Neuroimage. 2016; 132: 247-260
        • Luce R.D.
        Response Times: Their Role in Inferring Elementary Mental Organization.
        Oxford University Press, New York1986
        • Langen M.
        • Leemans A.
        • Johnston P.
        • Ecker C.
        • Daly E.
        • Murphy C.M.
        • et al.
        Fronto-striatal circuitry and inhibitory control in autism: Findings from diffusion tensor imaging tractography.
        Cortex. 2012; 48: 183-193
        • Howlin P.
        • Goode S.
        • Hutton J.
        • Rutter M.
        Adult outcome for children with autism.
        J Child Psychol Psychiatry. 2004; 45: 212-229