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Neurobiology of Continuous Spike-Wave in Slow-Wave Sleep and Landau-Kleffner Syndromes

  • Naoum P. Issa
    Correspondence
    Communications should be addressed to: Dr. Issa; Department of Neurology; The University of Chicago Medical Center; 5841 South Maryland Avenue, MC 2030; Chicago, Illinois 60637-1470.
    Affiliations
    Department of Neurology, The University of Chicago Medical Center, Chicago, Illinois
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      Abstract

      Background

      Several pediatric seizure disorders have common electrophysiological features during slow-wave sleep that produce different syndromes based on which part of the developing brain is involved. These disorders, of which continuous spike-wave in slow-wave sleep and Landau-Kleffner are the most common, are characterized by continuous spike-wave activity during slow-wave sleep, developmentally regulated onset and termination of abnormal electrical activity, and loss of previously acquired skills. Over the last 20 years, a variety of basic science findings suggest how spike-wave activity during sleep can cause the observed clinical outcomes.

      Methods

      Literature review and analysis.

      Results

      The role of slow-wave sleep in normal cortical plasticity during developmental critical periods, how disruption of slow-wave sleep by electrographic seizures could affect cortical maps and development, and the organization and functional connectivity of the thalamic structures that when damaged are thought to produce these seizure disorders are reviewed.

      Conclusions

      Potential therapeutic directions are proposed based on the mechanisms of plasticity and anatomical structures involved in cortical plasticity during slow-wave sleep.

      Keywords

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      References

        • Deonna T.
        Epilepsies with cognitive symptomatology.
        in: Wallace S. Epilepsy in Children. Chapman Medical, London1996: 315-322
        • Hughes J.R.
        A review of the relationships between Landau-Kleffner syndrome, electrical status epilepticus during sleep, and continuous spike-waves during sleep.
        Epilepsy Behav. 2011; 20: 247-253
        • Landau W.M.
        • Kleffner F.R.
        Syndrome of acquired aphasia with convulsive disorder in children.
        Neurology. 1957; 7: 523-530
        • Nickels K.
        • Wirrell E.
        Electrical status epilepticus in sleep.
        Semin Pediatr Neurol. 2008; 15: 50-60
        • Gordon N.
        The Landau-Kleffner syndrome: increased understanding.
        Brain Dev. 1997; 19: 311-316
        • Tassinari C.A.
        • Rubboli G.
        Cognition and paroxysmal EEG activities: from a single spike to electrical status epilepticus during sleep.
        Epilepsia. 2006; 47: 40-43
        • Fernández I.S.
        • Chapman K.E.
        • Peters J.M.
        • Harini C.
        • Rotenberg A.
        • Loddenkemper T.
        Continuous spikes and waves during sleep: electroclinical presentation and suggestions for management.
        Epilepsy Res Treat. 2013; 2013: 583531
        • Loddenkemper T.
        • Fernández I.S.
        • Peters J.M.
        Continuous spike and waves during sleep and electrical status epilepticus in sleep.
        J Clin Neurophysiol. 2011; 28: 154-164
        • Fernández I.S.
        • Loddenkemper T.
        • Peters J.M.
        • Kothare S.V.
        Electrical status epilepticus in sleep: clinical presentation and pathophysiology.
        Pediatr Neurol. 2012; 47: 390-410
        • Tassinari C.A.
        • Cantalupo G.
        • Dalla Bernardina B.
        • et al.
        Encephalopathy related to status epilepticus during slow sleep (ESES) including Landau-Kleffner syndrome.
        in: Bureau M. Genton P. Dravet C. Epileptic Syndromes in Infancy, Childhood and Adolescence. 5th ed. John Libbey EUROTEXT, 2012: 255-275
        • Wiesel T.N.
        • Hubel D.H.
        Effects of visual deprivation on morphology and physiology of cells in the cats lateral geniculate body.
        J Neurophysiol. 1963; 26: 978-993
        • Wiesel T.N.
        • Hubel D.H.
        Single-cell responses in striate cortex of kittens deprived of vision in one eye.
        J Neurophysiol. 1963; 26: 1003-1017
        • Hubel D.H.
        • Wiesel T.N.
        Binocular interaction in striate cortex of kittens reared with artificial squint.
        J Neurophysiol. 1965; 28: 1041-1059
        • Hubel D.H.
        • Wiesel T.N.
        The period of susceptibility to the physiological effects of unilateral eye closure in kittens.
        J Physiol. 1970; 206: 419-436
        • Crowley J.C.
        • Katz L.C.
        Development of ocular dominance columns in the absence of retinal input.
        Nat Neurosci. 1999; 2: 1125-1130
        • Crowley J.C.
        • Katz L.C.
        Early development of ocular dominance columns.
        Science. 2000; 290: 1321-1324
        • Crair M.C.
        • Horton J.C.
        • Antonini A.
        • Stryker M.P.
        Emergence of ocular dominance columns in cat visual cortex by 2 weeks of age.
        J Comp Neurol. 2001; 430: 235-249
        • Shatz C.J.
        • Stryker M.P.
        Ocular dominance in layer IV of the cat's visual cortex and the effects of monocular deprivation.
        J Physiol. 1978; 281: 267-283
        • Hubel D.H.
        • Wiesel T.N.
        • LeVay S.
        Plasticity of ocular dominance columns in monkey striate cortex.
        Philos Trans R Soc Lond B Biol Sci. 1977; 278: 377-409
        • Issa N.P.
        • Trachtenberg J.T.
        • Chapman B.
        • Zahs K.R.
        • Stryker M.P.
        The critical period for ocular dominance plasticity in the Ferret's visual cortex.
        J Neurosci. 1999; 19: 6965-6978
        • Vaegan
        • Taylor D.
        Critical period for deprivation amblyopia in children.
        Trans Ophthalmol Soc U K. 1979; 99: 432-439
        • Fawcett S.L.
        • Wang Y.-Z.
        • Birch E.E.
        The critical period for susceptibility of human stereopsis.
        Invest Ophthalmol Vis Sci. 2005; 46: 521-525
        • Johnson J.S.
        • Newport E.L.
        Critical period effects in second language learning: the influence of maturational state on the acquisition of English as a second language.
        Cogn Psychol. 1989; 21: 60-99
        • Birdsong D.
        • Molis M.
        On the evidence for maturational constraints in second-language acquisition.
        J Mem Lang. 2001; 44: 235-249
      1. Nicholas J, Geers A. Effect of age of cochlear implantation on receptive and expressive spoken language in 3-year-old deaf children. In: Proceedings of the VIII International Cochlear Implant Conference; International Congress.; 2004:340–343.

        • Stefanatos G.
        Changing perspectives on Landau-Kleffner syndrome.
        Clin Neuropsychol. 2011; 25: 963-988
        • Bishop D.V.
        Age of onset and outcome in “acquired aphasia with convulsive disorder” (Landau-Kleffner syndrome).
        Dev Med Child Neurol. 1985; 27: 705-712
        • Villarejo-Ortega F.
        • García-Fernández M.
        • Fournier-Del Castillo C.
        • et al.
        Seizure and developmental outcomes after hemispherectomy in children and adolescents with intractable epilepsy.
        Childs Nerv Syst. 2013; 29: 475-488
        • Gallagher A.
        • Tanaka N.
        • Suzuki N.
        • Liu H.
        • Thiele E.A.
        • Stufflebeam S.M.
        Decreased language laterality in tuberous sclerosis complex: a relationship between language dominance and tuber location as well as history of epilepsy.
        Epilepsy Behav. 2012; 25: 36-41
        • Gallagher A.
        • Tanaka N.
        • Suzuki N.
        • Liu H.
        • Thiele E.A.
        • Stufflebeam S.M.
        Diffuse cerebral language representation in tuberous sclerosis complex.
        Epilepsy Res. 2013; 104: 125-133
        • Diekelmann S.
        • Born J.
        The memory function of sleep.
        Nat Rev Neurosci. 2010; 11: 114-126
        • Urbain C.
        • Di Vincenzo T.
        • Peigneux P.
        • Van Bogaert P.
        Is sleep-related consolidation impaired in focal idiopathic epilepsies of childhood? A pilot study.
        Epilepsy Behav. 2011; 22: 380-384
        • Korkman M.
        • Granström M.L.
        • Appelqvist K.
        • Liukkonen E.
        Neuropsychological characteristics of five children with the Landau-Kleffner syndrome: dissociation of auditory and phonological discrimination.
        J Int Neuropsychol Soc. 1998; 4: 566-575
        • Frank M.G.
        • Issa N.P.
        • Stryker M.P.
        Sleep enhances plasticity in the developing visual cortex.
        Neuron. 2001; 30: 275-287
        • Huber R.
        • Ghilardi M.F.
        • Massimini M.
        • Tononi G.
        Local sleep and learning.
        Nature. 2004; 430: 78-81
        • Jha S.K.
        • Jones B.E.
        • Coleman T.
        • et al.
        Sleep-dependent plasticity requires cortical activity.
        J Neurosci. 2005; 25: 9266-9274
        • Bölsterli B.K.
        • Schmitt B.
        • Bast T.
        • et al.
        Impaired slow wave sleep downscaling in encephalopathy with status epilepticus during sleep (ESES).
        Clin Neurophysiol. 2011; 122: 1779-1787
        • Vyazovskiy V.V.
        • Olcese U.
        • Lazimy Y.M.
        • et al.
        Cortical firing and sleep homeostasis.
        Neuron. 2009; 63: 865-878
        • Eriksson K.
        • Kylliäinen A.
        • Hirvonen K.
        • Nieminen P.
        • Koivikko M.
        Visual agnosia in a child with non-lesional occipito-temporal CSWS.
        Brain Dev. 2003; 25: 262-267
        • Crair M.C.
        • Gillespie D.C.
        • Stryker M.P.
        The role of visual experience in the development of columns in cat visual cortex.
        Science. 1998; 279: 566-570
        • Issa N.P.
        • Rosenberg A.
        • Husson T.R.
        Models and measurements of functional maps in V1.
        J Neurophysiol. 2008; 99: 2745-2754
        • Caraballo R.H.
        • Veggiotti P.
        • Kaltenmeier M.C.
        • et al.
        Encephalopathy with status epilepticus during sleep or continuous spikes and waves during slow sleep syndrome: a multicenter, long-term follow-up study of 117 patients.
        Epilepsy Res. 2013; 105: 164-173
        • Monteiro J.P.
        • Roulet-Perez E.
        • Davidoff V.
        • Deonna T.
        Primary neonatal thalamic haemorrhage and epilepsy with continuous spike-wave during sleep: a longitudinal follow-up of a possible significant relation.
        Eur J Paediatr Neurol. 2001; 5: 41-47
        • Guzzetta F.
        • Battaglia D.
        • Veredice C.
        • et al.
        Early thalamic injury associated with epilepsy and continuous spike-wave during slow sleep.
        Epilepsia. 2005; 46: 889-900
        • Steriade M.
        • Contreras D.
        Spike-wave complexes and fast components of cortically generated seizures. I. Role of neocortex and thalamus.
        J Neurophysiol. 1998; 80: 1439-1455
        • Kersbergen K.J.
        • de Vries L.S.
        • Leijten F.S.S.
        • et al.
        Neonatal thalamic hemorrhage is strongly associated with electrical status epilepticus in slow wave sleep.
        Epilepsia. 2013; 54: 733-740
        • Fernández I.S.
        • Takeoka M.
        • Tas E.
        • et al.
        Early thalamic lesions in patients with sleep-potentiated epileptiform activity.
        Neurology. 2012; 78: 1721-1727
        • Battaglia D.
        • Veggiotti P.
        • Lettori D.
        • et al.
        Functional hemispherectomy in children with epilepsy and CSWS due to unilateral early brain injury including thalamus: sudden recovery of CSWS.
        Epilepsy Res. 2009; 87: 290-298
        • Siniatchkin M.
        • Groening K.
        • Moehring J.
        • et al.
        Neuronal networks in children with continuous spikes and waves during slow sleep.
        Brain. 2010; 133: 2798-2813
        • Guido W.
        • Weyand T.
        Burst responses in thalamic relay cells of the awake behaving cat.
        J Neurophysiol. 1995; 74: 1782-1786
        • Guido W.
        • Lu S.M.
        • Vaughan J.W.
        • Godwin D.W.
        • Sherman S.M.
        Receiver operating characteristic (ROC) analysis of neurons in the cat's lateral geniculate nucleus during tonic and burst response mode.
        Vis Neurosci. 1995; 12: 723-741
        • Sherman S.M.
        Dual response modes in lateral geniculate neurons: mechanisms and functions.
        Vis Neurosci. 1996; 13: 205-213
        • Ji D.
        • Wilson M.A.
        Coordinated memory replay in the visual cortex and hippocampus during sleep.
        Nat Neurosci. 2007; 10: 100-107
        • Meeren H.
        • van Luijtelaar G.
        • Lopes da Silva F.
        • Coenen A.
        Evolving concepts on the pathophysiology of absence seizures: the cortical focus theory.
        Arch Neurol. 2005; 62: 371-376
        • Buzsáki G.
        The thalamic clock: emergent network properties.
        Neuroscience. 1991; 41: 351-364
        • Avanzini G.
        • de Curtis M.
        • Marescaux C.
        • Panzica F.
        • Spreafico R.
        • Vergnes M.
        Role of the thalamic reticular nucleus in the generation of rhythmic thalamo-cortical activities subserving spike and waves.
        J Neural Transm Suppl. 1992; 35: 85-95
        • Llano D.A.
        • Theyel B.B.
        • Mallik A.K.
        • Sherman S.M.
        • Issa N.P.
        Rapid and sensitive mapping of long-range connections in vitro using flavoprotein autofluorescence imaging combined with laser photostimulation.
        J Neurophysiol. 2009; 101: 3325-3340
        • Rakhade S.N.
        • Jensen F.E.
        Epileptogenesis in the immature brain: emerging mechanisms.
        Nat Rev Neurol. 2009; 5: 380-391
        • Silverstein F.S.
        • Jensen F.E.
        Neonatal seizures.
        Ann Neurol. 2007; 62: 112-120
        • Toyoizumi T.
        • Miyamoto H.
        • Yazaki-Sugiyama Y.
        • Atapour N.
        • Hensch T.K.
        • Miller K.D.
        A theory of the transition to critical period plasticity: inhibition selectively suppresses spontaneous activity.
        Neuron. 2013; 80: 51-63
        • Aton S.J.
        • Seibt J.
        • Dumoulin M.
        • et al.
        Mechanisms of sleep-dependent consolidation of cortical plasticity.
        Neuron. 2009; 61: 454-466
        • Wang W.Z.
        • Hoerder-Suabedissen A.
        • Oeschger F.M.
        • et al.
        Subplate in the developing cortex of mouse and human.
        J Anat. 2010; 217: 368-380
        • McQuillen P.S.
        • Sheldon R.A.
        • Shatz C.J.
        • Ferriero D.M.
        Selective vulnerability of subplate neurons after early neonatal hypoxia-ischemia.
        J Neurosci. 2003; 23: 3308-3315
        • Sretavan D.W.
        • Shatz C.J.
        • Stryker M.P.
        Modification of retinal ganglion cell axon morphology by prenatal infusion of tetrodotoxin.
        Nature. 1988; 336: 468-471
        • Penn A.A.
        • Riquelme P.A.
        • Feller M.B.
        • Shatz C.J.
        Competition in retinogeniculate patterning driven by spontaneous activity.
        Science. 1998; 279: 2108-2112
        • Gervain J.
        • Vines B.W.
        • Chen L.M.
        • et al.
        Valproate reopens critical-period learning of absolute pitch.
        Front Syst Neurosci. 2013; 7: 102
        • Putignano E.
        • Lonetti G.
        • Cancedda L.
        • et al.
        Developmental downregulation of histone posttranslational modifications regulates visual cortical plasticity.
        Neuron. 2007; 53: 747-759
        • Aton S.J.
        • Seibt J.
        • Dumoulin M.C.
        • Coleman T.
        • Shiraishi M.
        • Frank M.G.
        The sedating antidepressant trazodone impairs sleep-dependent cortical plasticity.
        PLoS One. 2009; 4: e6078
        • Tringham E.
        • Powell K.L.
        • Cain S.M.
        • et al.
        T-type calcium channel blockers that attenuate thalamic burst firing and suppress absence seizures.
        Sci Transl Med. 2012; 4: 121ra19
        • Margoliash D.
        • van Drongelen W.
        • Kohrman M.
        Introducing songbirds as a model system for epilepsy research.
        J Clin Neurophysiol. 2010; 27: 433-437
        • Theyel B.B.
        • Llano D.A.
        • Issa N.P.
        • Mallik A.K.
        • Sherman S.M.
        In vitro imaging using laser photostimulation with flavoprotein autofluorescence.
        Nat Protoc. 2011; 6: 502-508