Sleep neurophysiology in childhood onset schizophrenia
Andjela Markovic
University Hospital of Child and Adolescent Psychiatry and Psychotherapy, University of Bern, Bern, Switzerland
Graduate School for Health Sciences, University of Bern, Bern, Switzerland
Search for more papers by this authorAshura Buckley
National Institute of Mental Health, National Institutes of Health, Bethesda, Maryland
Search for more papers by this authorDavid I. Driver
Child Psychiatry Branch, National Institute of Mental Health, National Institutes of Health, Bethesda, Maryland
Search for more papers by this authorDiane Dillard-Broadnax
Child Psychiatry Branch, National Institute of Mental Health, National Institutes of Health, Bethesda, Maryland
Search for more papers by this authorPeter A. Gochman
Child Psychiatry Branch, National Institute of Mental Health, National Institutes of Health, Bethesda, Maryland
Search for more papers by this authorKerstin Hoedlmoser
Laboratory for Sleep, Cognition and Consciousness Research, Department of Psychology, Centre for Cognitive Neuroscience, University of Salzburg, Salzburg, Austria
Search for more papers by this authorJudith L. Rapoport
Child Psychiatry Branch, National Institute of Mental Health, National Institutes of Health, Bethesda, Maryland
Judith L. Rapoport and Leila Tarokh shared senior authorship.Search for more papers by this authorCorresponding Author
Leila Tarokh
University Hospital of Child and Adolescent Psychiatry and Psychotherapy, University of Bern, Bern, Switzerland
Judith L. Rapoport and Leila Tarokh shared senior authorship.Correspondence
Leila Tarokh, University Hospital of Child and Adolescent Psychiatry and Psychotherapy, University of Bern, Bolligenstrasse 111, Haus A 3000 Bern, Switzerland.
Email: [email protected]
Search for more papers by this authorAndjela Markovic
University Hospital of Child and Adolescent Psychiatry and Psychotherapy, University of Bern, Bern, Switzerland
Graduate School for Health Sciences, University of Bern, Bern, Switzerland
Search for more papers by this authorAshura Buckley
National Institute of Mental Health, National Institutes of Health, Bethesda, Maryland
Search for more papers by this authorDavid I. Driver
Child Psychiatry Branch, National Institute of Mental Health, National Institutes of Health, Bethesda, Maryland
Search for more papers by this authorDiane Dillard-Broadnax
Child Psychiatry Branch, National Institute of Mental Health, National Institutes of Health, Bethesda, Maryland
Search for more papers by this authorPeter A. Gochman
Child Psychiatry Branch, National Institute of Mental Health, National Institutes of Health, Bethesda, Maryland
Search for more papers by this authorKerstin Hoedlmoser
Laboratory for Sleep, Cognition and Consciousness Research, Department of Psychology, Centre for Cognitive Neuroscience, University of Salzburg, Salzburg, Austria
Search for more papers by this authorJudith L. Rapoport
Child Psychiatry Branch, National Institute of Mental Health, National Institutes of Health, Bethesda, Maryland
Judith L. Rapoport and Leila Tarokh shared senior authorship.Search for more papers by this authorCorresponding Author
Leila Tarokh
University Hospital of Child and Adolescent Psychiatry and Psychotherapy, University of Bern, Bern, Switzerland
Judith L. Rapoport and Leila Tarokh shared senior authorship.Correspondence
Leila Tarokh, University Hospital of Child and Adolescent Psychiatry and Psychotherapy, University of Bern, Bolligenstrasse 111, Haus A 3000 Bern, Switzerland.
Email: [email protected]
Search for more papers by this authorAbstract
Altered sleep neurophysiology has consistently been reported in adult patients with schizophrenia. Converging evidence suggests that childhood onset schizophrenia (COS), a rare but severe form of schizophrenia, is continuous with adult onset schizophrenia. The aim of the current study was to characterize sleep neurophysiology in COS. An overnight sleep electroencephalogram (EEG) was recorded in 17 children and adolescents with COS (16 years ± 6.6) and 17 age and gender-matched controls. Non-rapid eye movement (NREM) and rapid eye movement (REM) sleep EEG power and coherence for the frequency bands delta (1.6–4.8 Hz), theta (5–8.4 Hz), alpha (8.6–11 Hz), beta 1 (16.4–20.2 Hz) and beta 2 (20.4–24.2 Hz) were compared between COS patients and controls. COS patients exhibited significant and widespread deficits in beta power during NREM and REM sleep. With regard to coherence, we found increases in COS patients across brain regions, frequency bands and sleep states. This study demonstrates the utility of the sleep EEG for studying vulnerable populations and its potential to aid diagnosis.
CONFLICT OF INTEREST
The authors have no conflicts of interest to declare.
REFERENCES
- American Psychiatric Association (2013). American Psychiatric Association diagnostic and statistical manual of mental disorder. Washington, DC: American Psychiatric Association.
10.1176/appi.books.9780890425596 Google Scholar
- Baglioni, C., Nanovska, S., Regen, W., Spiegelhalder, K., Feige, B., Nissen, C., … Riemann, D. (2016). Sleep and mental disorders: A meta-analysis of polysomnographic research. Psychological Bulletin, 142, 969–990.
- Castelnovo, A., Graziano, B., Ferrarelli, F., & D’Agostino, A. (2017). Sleep spindles and slow waves in schizophrenia and related disorders: Main findings, challenges, and future perspectives. European Journal of Neuroscience, 48, 2738–2758.
- Christian, E. P., Snyder, D. H., Song, W., Gurley, D. A., Smolka, J., Maier, D. L., … Doherty, J. J. (2015). EEG-β/γ spectral power elevation in rat: A translatable biomarker elicited by GABA(Aα2/3)-positive allosteric modulators at nonsedating anxiolytic doses. Journal of Neurophysiology, 113, 116–131.
- Cohen, J. (1992). A power primer. Psychological Bulletin, 112, 155–159.
- de Jonge, J. C., Vinkers, C. H., Hulshoff Pol, H. E., & Marsman, A. (2017). GABAergic mechanisms in schizophrenia: Linking postmortem and in vivo studies. Frontiers in Psychiatry, 8, 118.
- Driver, D. I., Gogtay, N., & Rapoport, J. L. (2013). Childhood onset schizophrenia and early onset schizophrenia spectrum disorders. Child and Adolescent Psychiatric Clinics of North America, 22, 539–555.
- Feinberg, I. (1982). Schizophrenia: Caused by a fault in programmed synaptic elimination during adolescence? Journal of Psychiatric Research, 17, 319–334.
- Ferrarelli, F., Huber, R., Peterson, M. J., Massimini, M., Murphy, M., Riedner, B. A., … Tononi, G. (2007). Reduced sleep spindle activity in schizophrenia patients. American Journal of Psychiatry, 164, 483–492.
- Ferrarelli, F., Peterson, M. J., Sarasso, S., Riedner, B. A., Murphy, M. J., Benca, R. M., … Tononi, G. (2010). Thalamic dysfunction in schizophrenia suggested by whole-night deficits in slow and fast spindles. American Journal of Psychiatry, 167, 1339–1348.
- Ford, M. R., Goethe, J. W., & Dekker, D. K. (1986). EEG coherence and power in the discrimination of psychiatric disorders and medication effects. Biological Psychiatry, 21, 1175–1188.
- Fuentealba, P., & Steriade, M. (2005). The reticular nucleus revisited: Intrinsic and network properties of a thalamic pacemaker. Progress in Neurobiology, 75, 125–141.
- Ganguli, R., Reynolds, C. F., & Kupfer, D. J. (1987). Electroencephalographic sleep in young, never-medicated schizophrenics. A comparison with delusional and nondelusional depressives and with healthy controls. Archives of General Psychiatry, 44, 36–44.
- Göder, R., Aldenhoff, J. B., Boigs, M., Braun, S., Koch, J., & Fritzer, G. (2006). Delta power in sleep in relation to neuropsychological performance in healthy subjects and schizophrenia patients. Journal of Neuropsychiatry and Clinical Neurosciences, 18, 529–535.
- Göder, R., Graf, A., Ballhausen, F., Weinhold, S., Baier, P. C., Junghanns, K., & Prehn-Kristensen, A. (2015). Impairment of sleep-related memory consolidation in schizophrenia: Relevance of sleep spindles? Sleep Medicine, 16, 564–569.
- Gordon, C. T., Frazier, J. A., McKenna, K., Giedd, J., Zametkin, A., Kaysen, D., … Hommer, D. (1994). Childhood-onset schizophrenia: An NIMH study in progress. Schizophrenia Bulletin, 20, 697–712.
- Gur, R. E., Cowell, P., Turetsky, B. I., Gallacher, F., Cannon, T., Bilker, W., & Gur, R. C. (1998). A follow-up magnetic resonance imaging study of schizophrenia. Relationship of neuroanatomical changes to clinical and neurobehavioral measures. Archives of General Psychiatry, 55, 145–152.
- Hiatt, J. F., Floyd, T. C., Katz, P. H., & Feinberg, I. (1985). Further evidence of abnormal non-rapid-eye-movement sleep in schizophrenia. Archives of General Psychiatry, 42, 797–802.
- Kaskie, R. E., Graziano, B., & Ferrarelli, F. (2017). Schizophrenia and sleep disorders: Links, risks, and management challenges. Nature and Science Sleep, 9, 227–239.
- Keshavan, M. S., Reynolds, C. F., Miewald, J. M., Montrose, D. M., Sweeney, J. A., Vasko, R. C., & Kupfer, D. J. (1998). Delta sleep deficits in schizophrenia: Evidence from automated analyses of sleep data. Archives of General Psychiatry, 55, 443–448.
- Linkenkaer-Hansen, K., Smit, D. J. A., Barkil, A., van Beijsterveldt, T. E. M., Brussaard, A. B., Boomsma, D. I., … de Geus, E. J. C. (2007). Genetic contributions to long-range temporal correlations in ongoing oscillations. Journal of Neuroscience, 27, 13882–13889.
- Maccrimmon, D., Brunet, D., Criollo, M., Galin, H., & Lawson, J. S. (2012). Clozapine augments delta, theta, and right frontal EEG alpha power in schizophrenic patients. ISRN Psychiatry, 2012, 596486.
- Manoach, D. S., Demanuele, C., Wamsley, E. J., Vangel, M., Montrose, D. M., Miewald, J., … Keshavan, M. S. (2014). Sleep spindle deficits in antipsychotic-naïve early course schizophrenia and in non-psychotic first-degree relatives. Frontiers in Human Neuroscience, 8, 762.
- Manoach, D. S., Thakkar, K. N., Stroynowski, E., Ely, A., McKinley, S. K., Wamsley, E., … Stickgold, R. (2010). Reduced overnight consolidation of procedural learning in chronic medicated schizophrenia is related to specific sleep stages. Journal of Psychiatric Research, 44, 112.
- Maris, E., & Oostenveld, R. (2007). Nonparametric statistical testing of EEG- and MEG-data. Journal of Neuroscience Methods, 164, 177–190.
- Markovic, A., Achermann, P., Rusterholz, T., & Tarokh, L. (2018). Heritability of sleep EEG topography in adolescence: Results from a Longitudinal Twin Study. Scientific Reports, 8, 7334.
- Medkour, T., Walden, A. T., Burgess, A. P., & Strelets, V. B. (2010). Brain connectivity in positive and negative syndrome schizophrenia. Neuroscience, 169, 1779–1788.
- Merrin, E. L., Floyd, T. C., & Fein, G. (1989). EEG coherence in unmedicated schizophrenic patients. Biological Psychiatry, 25, 60–66.
- Mientus, S., Gallinat, J., Wuebben, Y., Pascual-Marqui, R. D., Mulert, C., Frick, K., … Winterer, G. (2002). Cortical hypoactivation during resting EEG in schizophrenics but not in depressives and schizotypal subjects as revealed by low resolution electromagnetic tomography (LORETA). Psychiatry Research, 116, 95–111.
- Nagase, Y., Okubo, Y., Matsuura, M., Kojima, T., & Toru, M. (1992). EEG coherence in unmedicated schizophrenic patients: Topographical study of predominantly never medicated cases. Biological Psychiatry, 32, 1028–1034.
- Nicolson, R., & Rapoport, J. L. (1999). Childhood-onset schizophrenia: Rare but worth studying. Biological Psychiatry, 46, 1418–1428.
- Poulin, J., Stip, E., & Godbout, R. (2008). REM sleep EEG spectral analysis in patients with first-episode schizophrenia. Journal of Psychiatric Research, 42, 1086–1093.
- Ranlund, S., Nottage, J., Shaikh, M., Dutt, A., Constante, M., Walshe, M., … Bramon, E. (2014). Resting EEG in psychosis and at-risk populations–a possible endophenotype? Schizophrenia Research, 153, 96–102.
- Rusterholz, T., Hamann, C., Markovic, A., Schmidt, S. J., Achermann, P., & Tarokh, L. (2018). Nature and Nurture: Brain region specific inheritance of sleep neurophysiology in adolescence. The Journal of Neuroscience, 38, 9275–9285.
- Sekimoto, M., Kato, M., Watanabe, T., Kajimura, N., & Takahashi, K. (2011). Cortical regional differences of delta waves during all-night sleep in schizophrenia. Schizophrenia Research, 126, 284–290.
- Sponheim, S. R., Clementz, B. A., Iacono, W. G., & Beiser, M. (1994). Resting EEG in first-episode and chronic schizophrenia. Psychophysiology, 31, 37–43.
- Tarokh, L., & Carskadon, M. A. (2010). Developmental changes in the human sleep EEG during early adolescence. Sleep, 33, 801–809.
- Wamsley, E. J., Tucker, M. A., Shinn, A. K., Ono, K. E., McKinley, S. K., Ely, A. V., … Manoach, D. S. (2012). Reduced sleep spindles and spindle coherence in schizophrenia: Mechanisms of impaired memory consolidation? Biological Psychiatry, 71, 154–161.
- Whittington, M. A., Traub, R. D., Kopell, N., Ermentrout, B., & Buhl, E. H. (2000). Inhibition-based rhythms: Experimental and mathematical observations on network dynamics. International Journal of Psychophysiology, 38, 315–336.
- Winsky-Sommerer, R., de Oliveira, P., Loomis, S., Wafford, K., Dijk, D.-J., & Gilmour, G. (2018). Disturbances of sleep quality, timing and structure and their relationship with other neuropsychiatric symptoms in Alzheimer’s disease and schizophrenia: Insights from studies in patient populations and animal models. Neuroscience and Biobehavioral Reviews, 97, 112–137.
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