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Is mild ADHD beneficial: Brain criticality is maximal with moderate ADHD symptom scores

View ORCID ProfileJonni Hirvonen, View ORCID ProfileHamed Haque, View ORCID ProfileSheng H. Wang, View ORCID ProfileJaana Simola, View ORCID ProfileIsabel Morales-Muñoz, View ORCID ProfileBenjamin U. Cowley, View ORCID ProfileJ. Matias Palva, View ORCID ProfileSatu Palva
doi: https://doi.org/10.1101/2022.12.14.519751
Jonni Hirvonen
1Neuroscience Center, Helsinki Institute of Life Science, University of Helsinki, Finland
2BioMag laboratory, HUS Medical Imaging Center, Finland
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Hamed Haque
1Neuroscience Center, Helsinki Institute of Life Science, University of Helsinki, Finland
2BioMag laboratory, HUS Medical Imaging Center, Finland
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Sheng H. Wang
1Neuroscience Center, Helsinki Institute of Life Science, University of Helsinki, Finland
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Jaana Simola
1Neuroscience Center, Helsinki Institute of Life Science, University of Helsinki, Finland
3Faculty of Educational Sciences, University of Helsinki, Finland
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Isabel Morales-Muñoz
1Neuroscience Center, Helsinki Institute of Life Science, University of Helsinki, Finland
4Public Health and Welfare, Finnish Institute for Health and Welfare, Helsinki, Finland
5Institute for Mental Health, School of Psychology, University of Birmingham, United Kingdom
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Benjamin U. Cowley
3Faculty of Educational Sciences, University of Helsinki, Finland
6Cognitive Science, Department of Digital Humanities, Faculty of Arts, University of Helsinki
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J. Matias Palva
1Neuroscience Center, Helsinki Institute of Life Science, University of Helsinki, Finland
7Department of Neuroscience and Biomedical Engineering, Aalto University, Finland
8Centre for Cognitive Neuroimaging, Institute of Neuroscience and Psychology, University of Glasgow, United Kingdom
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Satu Palva
1Neuroscience Center, Helsinki Institute of Life Science, University of Helsinki, Finland
8Centre for Cognitive Neuroimaging, Institute of Neuroscience and Psychology, University of Glasgow, United Kingdom
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  • For correspondence: satu.palva@helsinki.fi
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Abstract

Attention-deficit/hyperactivity disorder (ADHD) is characterized by involuntary fluctuations of attention in continuous performance tasks (CPTs) wherein attention must be sustained over long periods of time. The neuronal basis underlying aberrant attentional fluctuations in time scales from seconds to minutes have remained poorly understood. Neuronal alpha- and gammaband oscillations are thought to implement attentional and top-down control of sensorimotor processing. We hypothesized that aberrant behavioral fluctuations in ADHD would be caused by aberrant endogenous brain dynamics in alpha and gamma-band oscillations and specifically by their aberrant long-range temporal correlations (LRTCs). We measured brain activity with magnetoencephalography (MEG) from adult participants diagnosed with ADHD (N = 19) and from healthy control subjects (N = 20) during resting state and two CPTs; a threshold stimulus detection task and a Go/NoGo task. We then estimated LRTCs of neuronal oscillations and behavioral fluctuations with detrended fluctuation analysis (DFA). ADHD was associated with aberrant LRTCs in both behavioral performance and of neuronal oscillations. LRTCs were correlated with symptom severity with a U-shaped correlations indicating that the LRTCs were largest with moderate symptom scores. These data demonstrate the presence of aberrant temporal dynamics of neuronal oscillations in adult ADHD patients, which may underlie involuntary attentional fluctuations in ADHD. Taken that LRTCs are a hallmark of brain critical dynamics, these data show that moderate ADHD symptoms scores maximize brain criticality which is thought to be beneficial for performance.

Competing Interest Statement

The authors have declared no competing interest.

  • Abbreviations

    ADHD
    Attention Deficit and Hyperactivity Disorder
    ASRS
    Adult ADHD Self-Report Scale
    BADDS
    Brown Attention Deficit Disorder Symptom Assessment Scale
    BIS
    Barrett Impulsiveness Scale
    CPT
    Continuous Performance Task
    DAN
    Dorsal Attention Network
    DFA
    Detrended Fluctuation Analysis
    EOG
    Electro-oculography
    FA
    False Alarm
    FDR
    False Discovery Rate
    HR
    Hit Rate
    ICA
    Independent Component Analysis
    IQ
    Intelligence quotient
    lPFC
    lateral Prefrontal Cortex
    LRTC
    Long-Range Temporal Correlation
    MEG
    Magnetoencephalography
    mPFC
    media Prefrontal Cortex
    mPPC
    medial Parietal Cortex
    NE
    Norepinephrine
    PPC
    Posterior Parietal Cortex
    RS
    resting state
    RT
    Reaction Time
    RTV
    Reaction Time Variability
    SBM
    Surface-based Morphometry
    SOA
    Stimulus Onset Asynchrony
    TSDT
    Threshold of Stimulus Detection Task
    VAN
    Ventral Attention Network
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    Posted December 15, 2022.
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    Is mild ADHD beneficial: Brain criticality is maximal with moderate ADHD symptom scores
    Jonni Hirvonen, Hamed Haque, Sheng H. Wang, Jaana Simola, Isabel Morales-Muñoz, Benjamin U. Cowley, J. Matias Palva, Satu Palva
    bioRxiv 2022.12.14.519751; doi: https://doi.org/10.1101/2022.12.14.519751
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    Is mild ADHD beneficial: Brain criticality is maximal with moderate ADHD symptom scores
    Jonni Hirvonen, Hamed Haque, Sheng H. Wang, Jaana Simola, Isabel Morales-Muñoz, Benjamin U. Cowley, J. Matias Palva, Satu Palva
    bioRxiv 2022.12.14.519751; doi: https://doi.org/10.1101/2022.12.14.519751

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