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Association of inattention with slow-spindle density in sleep EEG of children with attention deficit-hyperactivity disorder

  • Yoshihiko Saito
    Affiliations
    Department of Child Neurology, National Center Hospital, NCNP of National Center of Neurology and Psychiatry, 4-1-1 Ogawahigashi-machi, Kodaira, Tokyo 187-8551, Japan
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  • Yoshimi Kaga
    Correspondence
    Corresponding author.
    Affiliations
    Department of Developmental Disorders, National Institute of Mental Health, NCNP of National Center of Neurology and Psychiatry, 4-1-1 Ogawahigashi-machi, Kodaira, Tokyo 187-8553, Japan
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  • Eiji Nakagawa
    Affiliations
    Department of Child Neurology, National Center Hospital, NCNP of National Center of Neurology and Psychiatry, 4-1-1 Ogawahigashi-machi, Kodaira, Tokyo 187-8551, Japan

    Department of Developmental Disorders, National Institute of Mental Health, NCNP of National Center of Neurology and Psychiatry, 4-1-1 Ogawahigashi-machi, Kodaira, Tokyo 187-8553, Japan
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  • Mariko Okubo
    Affiliations
    Department of Child Neurology, National Center Hospital, NCNP of National Center of Neurology and Psychiatry, 4-1-1 Ogawahigashi-machi, Kodaira, Tokyo 187-8551, Japan
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  • Kosuke Kohashi
    Affiliations
    Department of Child Neurology, National Center Hospital, NCNP of National Center of Neurology and Psychiatry, 4-1-1 Ogawahigashi-machi, Kodaira, Tokyo 187-8551, Japan
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  • Mikimasa Omori
    Affiliations
    Department of Developmental Disorders, National Institute of Mental Health, NCNP of National Center of Neurology and Psychiatry, 4-1-1 Ogawahigashi-machi, Kodaira, Tokyo 187-8553, Japan
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  • Ayako Fukuda
    Affiliations
    Department of Developmental Disorders, National Institute of Mental Health, NCNP of National Center of Neurology and Psychiatry, 4-1-1 Ogawahigashi-machi, Kodaira, Tokyo 187-8553, Japan
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  • Masumi Inagaki
    Affiliations
    Department of Developmental Disorders, National Institute of Mental Health, NCNP of National Center of Neurology and Psychiatry, 4-1-1 Ogawahigashi-machi, Kodaira, Tokyo 187-8553, Japan
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      Abstract

      Objective

      We evaluated the power of slow sleep spindles during sleep stage 2 to clarify their relationship with executive function, especially with attention, in children with attention deficit-hyperactivity disorder (ADHD).

      Methods

      Subjects were 21 children with ADHD and 18 aged-matched, typically developing children (TDC). ADHD subjects were divided into groups of only ADHD and ADHD + autism spectrum disorder (ASD). We employed the Continuous Performance Test (CPT) to measure attention. We focused on sleep spindle frequencies (12–14 Hz) in sleep stage 2 and performed a power spectral analysis using fast Fourier transform techniques and compared sleep spindles with the variability of reaction time in CPT.

      Results

      In the CPT, reaction variabilities in ADHD and ADHD + ASD significantly differed from those in TDC. Twelve-hertz spindles were mainly distributed in the frontal pole and frontal area and 14-Hz spindles in the central area. The ratio of 12-Hz frontal spindle power was higher in ADHD than in TDC, especially in ADHD + ASD. Significant correlation between the ratio of 12-Hz spindles and reaction time variability was observed.

      Conclusions

      Twelve-hertz frontal spindle EEG activity may have positive associations with sustained attention function. Slow frontal spindles may be useful as a biomarker of inattention in children with ADHD.

      Keywords

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      References

        • Weiss M.D.
        • Gadow K.
        • Wasdell M.B.
        Effectiveness outcomes in attention-deficit/hyperactivity disorder.
        J Clin Psychiatry. 2006; 67: 38-45
        • Corkum P.
        • Tannock R.
        • Moldofsky H.
        Sleep disturbances in children with attention-deficit/hyperactivity disorder.
        J Am Acad Child Adolesc Psychiatry. 1998; 37: 637-646
        • Day H.D.
        • Abmayr S.B.
        Parent reports of sleep disturbances in stimulant-medicated children with attention-deficit hyperactivity disorder.
        J Clin Psychol. 1998; 54: 701-716
        • Sobanski E.
        • Schredl M.
        • Kettler N.
        • Alm B.
        Sleep in adults with attention deficit hyperactivity disorder (ADHD) before and during treatment with methylphenidate: a controlled polysomnographic study.
        Sleep. 2008; 31: 375-381
        • O'Brien L.M.
        • Ivanenko A.
        • Crabtree V.M.
        • Holbrook C.R.
        • Bruner J.L.
        • Klaus C.J.
        • et al.
        Sleep disturbances in children with attention deficit hyperactivity disorder.
        Pediatr Res. 2003; 54: 237-243
        • Lecendreux M.
        • Konofal E.
        • Bouvard M.
        • Falissard B.
        • Mouren-Simeoni M.C.
        Sleep and alertness in children with ADHD.
        J Child Psychol Psychiatry. 2000; 41: 803-812
        • Van der Heijden K.B.
        • Smits M.G.
        • Van Someren E.J.
        • Gunning W.B.
        Idiopathic chronic sleep onset insomnia in attention-deficit/hyperactivity disorder: a circadian rhythm sleep disorder.
        Chronobiol Int. 2005; 22: 559-570
        • Sonuga-Barke E.
        • Bitsakou P.
        • Thompson M.
        Beyond the dual pathway model: evidence for the dissociation of timing, inhibitory, and delay-related impairments in attention-deficit/hyperactivity disorder.
        J Am Acad Child Adolesc Psychiatry. 2010; 49: 345-355
        • Lee E.H.
        • Choi Y.S.
        • Yoon H.S.
        • Bahn G.H.
        Clinical impact of epileptiform discharge in children with attention-deficit/hyperactivity disorder (ADHD).
        J Child Neurol. 2016; 31: 584-588
        • Kanemura H.
        • Sano F.
        • Tando T.
        • Hosaka H.
        • Sugita K.
        • Aihara M.
        EEG improvements with antiepileptic drug treatment can show a high correlation with behavioral recovery in children with ADHD.
        Epilepsy Behav. 2013; 27: 443-448
        • Ishii S.
        • Kaga Y.
        • Tando T.
        • Aoyagi K.
        • Sano F.
        • Kanemura H.
        • et al.
        Disinhibition in children with attention-deficit/hyperactivity disorder: Changes in [oxy-Hb] on near-infrared spectroscopy during “rock, paper, scissors” task.
        Brain Dev. 2017; 39: 395-402
        • Yasumura A.
        • Kokubo N.
        • Yamamoto H.
        • Yasumura Y.
        • Nakagawa E.
        • Kaga M.
        • et al.
        Neurobehavioral and hemodynamic evaluation of Stroop and reverse Stroop interference in children with attention-deficit/hyperactivity disorder.
        Brain Dev. 2014; 36: 97-106
        • Seidman L.J.
        • Valera E.M.
        • Makris N.
        • Monuteaux M.C.
        • Boriel D.L.
        • Kelkar K.
        • et al.
        Dorsolateral prefrontal and anterior cingulate cortex volumetric abnormalities in adults with attention-deficit/hyperactivity disorder identified by magnetic resonance imaging.
        Biol Psychiatry. 2006; 60: 1071-1080
        • Chatburn A.
        • Coussens S.
        • Lushington K.
        • Kennedy D.
        • Baumert M.
        • Kohler M.
        Sleep spindle activity and cognitive performance in healthy children.
        Sleep. 2013; 36: 237-243
        • Jobert M.
        • Poiseau E.
        • Jahnig P.
        • Schulz H.
        • Kubicki S.
        Topographical analysis of sleep spindle activity.
        Neuropsychobiology. 1992; 26: 210-217
        • Del Felice A.
        • Arcaro C.
        • Storti S.F.
        • Fiaschi A.
        • Manganotti P.
        Electrical source imaging of sleep spindles.
        Clin EEG Neurosci. 2014; 45: 184-192
        • Shinomiya S.
        • Nagata K.
        • Takahashi K.
        • Masumura T.
        Development of sleep spindles in young children and adolescents.
        Clin Electroencephalogr. 1999; 30: 39-43
        • Inoue Y.
        • Ito K.
        • Kita Y.
        • Inagaki M.
        • Kaga M.
        • Swanson J.M.
        Psychometric properties of Japanese version of the Swanson, Nolan, and Pelham, version-IV Scale-Teacher Form: a study of school children in community samples.
        Brain Dev. 2014; 36: 700-706
        • Inoue Y.
        • Inagaki M.
        • Gunji A.
        • Furushima W.
        • Kaga M.
        Response switching process in children with attention-deficit-hyperactivity disorder on the novel continuous performance test.
        Dev Med Child Neurol. 2008; 50: 462-466
        • Uno A.
        • Haruhara N.
        • Kaneko M.
        Raven’s coloured progressive matrices in Japanese children: as a screening intelligence test for children with learning disorder and acquired childhood aphasia. (in Japanese).
        Onsei Gengo Igaku (Tokyo). 2005; 46: 185-189
        • Ayoub A.
        • Aumann D.
        • Hörschelmann A.
        • Kouchekmanesch A.
        • Paul P.
        • Born J.
        • et al.
        Differential effects on fast and slow spindle activity, and the sleep slow oscillation in humans with carbamazepine and flunarizine to antagonize voltage-dependent Na+ and Ca2+ channel activity.
        Sleep. 2013; 36: 905-911
        • Timofeev I.
        • Chauvette S.
        The spindles: are they still thalamic?.
        Sleep. 2013; 36: 825-826
        • Claes L.
        • Del-Favero J.
        • Ceulemans B.
        • Lagae L.
        • Van Broeckhoven C.
        • De Jonghe P.
        De novo mutations in the sodium-channel gene SCN1A cause severe myoclonic epilepsy of infancy.
        Am J Hum Genet. 2001; 68: 1327-1332
        • Wolff M.
        • Cassé-Perrot C.
        • Dravet C.
        Severe myoclonic epilepsy of infants (Dravet syndrome): natural history and neuropsychological findings.
        Epilepsia. 2006; 47: 45-48
        • Damyanovich E.V.
        • Baziyan B.
        • Sagalov M.V.
        • Kumskova G.A.
        Saccadic movements of the eyes in children with attention deficit and hyperactivity syndrome.
        Bull Exp Biol Med. 2013; 156: 25-28
        • Spronk M.
        • Jonkman L.M.
        • Kemner C.
        Response inhibition and attention processing in 5- to 7-year-old children with and without symptoms of ADHD: an ERP study.
        Clin Neurophysiol. 2008; 119: 2738-2752
        • Tamaki M.
        • Matsuoka T.
        • Nittono H.
        • Hori T.
        Activation of fast sleep spindles at the premotor cortex and parietal areas contributes to motor learning: a study using sLORETA.
        Clin Neurophysiol. 2009; 120: 878-886
        • Doucette M.R.
        • Kurth S.
        • Chevalier N.
        • Munakata Y.
        • LeBourgeois M.K.
        Topography of slow sigma power during sleep is associated with processing speed in preschool children.
        Brain Sci. 2015; 5: 494-508
        • Hoedlmoser K.
        • Heib D.P.
        • Roell J.
        • Peigneux P.
        • Sadeh A.
        • Gruber G.
        • et al.
        Slow sleep spindle activity, declarative memory, and general cognitive abilities in children.
        Sleep. 2014; 37: 1501-1512
        • Lundervold A.J.
        • Stickert M.
        • Hysing M.
        • Sorensen L.
        • Gillberg C.
        • Posserud M.B.
        Attention deficits in children with combined autism and ADHD: a CPT study.
        J Atten Disord. 2016; 20: 599-609
        • Tye C.
        • Asherson P.
        • Ashwood K.L.
        • Azadi B.
        • Bolton P.
        • McLoughlin G.
        Attention and inhibition in children with ASD, ADHD and co-morbid ASD + ADHD: an event-related potential study.
        Psychol Med. 2014; 44: 1101-1116
        • Limoges E.
        • Mottron L.
        • Bolduc C.
        • Berthiaume C.
        • Godbout R.
        Atypical sleep architecture and the autism phenotype.
        Brain. 2005; 128: 1049-1061
        • Godbout R.
        • Bergeron C.
        • Limoges E.
        • Stip E.
        • Mottron L.
        A laboratory study of sleep in Asperger’s syndrome.
        NeuroReport. 2000; 11: 127-130