Sleep spindles as neurophysiological biomarkers of schizophrenia.

EEG GABA glutamate sleep thalamocortical networks

Journal

The European journal of neuroscience

ISSN: 1460-9568

Titre abrégé: Eur J Neurosci

Pays: France

ID NLM: 8918110

Informations de publication

Date de publication:
26 Oct 2023

Historique:

revised: 17 09 2023

received: 11 06 2023

accepted: 11 10 2023

medline: 27 10 2023

pubmed: 27 10 2023

entrez: 27 10 2023

Statut: aheadofprint

Résumé

Schizophrenia (SCZ) is a complex psychiatric disorder characterized by a wide range of clinical symptoms, including disrupted sleep. In recent years, there has been growing interest in assessing alterations in sleep parameters in patients with SCZ. Sleep spindles are brief (0.5-2 s) bursts of 12- to 16-Hz rhythmic electroencephalogram (EEG) oscillatory activity occurring during non-rapid eye movement (NREM) sleep. Spindles have been implicated in several critical brain functions, including learning, memory and plasticity, and are thought to reflect the integrity of underlying thalamocortical circuits. This review aims to provide an overview of the current research investigating sleep spindles in SCZ. After briefly describing the neurophysiological features of sleep spindles, I will discuss alterations in spindle characteristics observed in SCZ, their associations with the clinical symptomatology of these patients and their putative underlying neuronal and molecular mechanisms. I will then discuss the utility of sleep spindle measures as predictors of treatment response and disease progression. Finally, I will highlight future directions for research in this emerging field, including the prospect of utilizing sleep spindles as neurophysiological biomarkers of SCZ.

Identifiants

DOI: 10.1111/ejn.16178 PMID: 37885306

pubmed: 37885306

doi: 10.1111/ejn.16178

doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

Subventions

Organisme : NIMH NIH HHS

ID : R01MH125816

Pays : United States

Organisme : NIMH NIH HHS

ID : R01MH130376

Pays : United States

Informations de copyright

Références

Ackermann, S., & Rasch, B. (2014). Differential effects of non-REM and REM sleep on memory consolidation? Current Neurology and Neuroscience Reports, 14, 430. https://doi.org/10.1007/s11910-013-0430-8

Adamantidis, A. R., Gutierrez Herrera, C., & Gent, T. C. (2019). Oscillating circuitries in the sleeping brain. Nature Reviews. Neuroscience, 20, 746-762. https://doi.org/10.1038/s41583-019-0223-4

Aguilar, D. D., Strecker, R. E., Basheer, R., & McNally, J. M. (2020). Alterations in sleep, sleep spindle, and EEG power in mGluR5 knockout mice. Journal of Neurophysiology, 123, 22-33. https://doi.org/10.1152/jn.00532.2019

Andrade, A., Hope, J., Allen, A., Yorgan, V., Lipscombe, D., & Pan, J. Q. (2016). A rare schizophrenia risk variant of CACNA1I disrupts Ca(V)3.3 channel activity. Scientific Reports, 6, 34233. https://doi.org/10.1038/srep34233

Andrillon, T., Poulsen, A. T., Hansen, L. K., Leger, D., & Kouider, S. (2016). Neural markers of responsiveness to the environment in human sleep. The Journal of Neuroscience, 36, 6583-6596. https://doi.org/10.1523/JNEUROSCI.0902-16.2016

Astori, S., Wimmer, R. D., Prosser, H. M., Corti, C., Corsi, M., Liaudet, N., Volterra, A., Franken, P., Adelman, J. P., & Luthi, A. (2011). The Ca(V)3.3 calcium channel is the major sleep spindle pacemaker in thalamus. Proceedings of the National Academy of Sciences of the United States of America, 108, 13823-13828. https://doi.org/10.1073/pnas.1105115108

Baandrup, L., Christensen, J. A. E., Fagerlund, B., & Jennum, P. (2019). Investigation of sleep spindle activity and morphology as predictors of neurocognitive functioning in medicated patients with schizophrenia. Journal of Sleep Research, 28, e12672. https://doi.org/10.1111/jsr.12672

Bagautdinova, J., Mayeli, A., Wilson, J. D., Donati, F. L., Colacot, R. M., Meyer, N., Fusar-Poli, P., & Ferrarelli, F. (2023). Sleep abnormalities in different clinical stages of psychosis: A systematic review and meta-analysis. JAMA Psychiatry, 80, 202-210. https://doi.org/10.1001/jamapsychiatry.2022.4599

Baran, B., Correll, D., Vuper, T. C., Morgan, A., Durrant, S. J., Manoach, D. S., & Stickgold, R. (2018). Spared and impaired sleep-dependent memory consolidation in schizophrenia. Schizophrenia Research, 199, 83-89. https://doi.org/10.1016/j.schres.2018.04.019

Baran, B., Karahanoglu, F. I., Mylonas, D., Demanuele, C., Vangel, M., Stickgold, R., Anticevic, A., & Manoach, D. S. (2019). Increased thalamocortical connectivity in schizophrenia correlates with sleep spindle deficits: Evidence for a common pathophysiology. Biological Psychiatry: Cognitive Neuroscience and Neuroimaging, 4(8), 706-714.

Berry, R. B., Brooks, R., Gamaldo, C., Harding, S. M., Lloyd, R. M., Quan, S. F., Troester, M. T., & Vaughn, B. V. (2017). AASM scoring manual updates for 2017 (version 2.4). Journal of Clinical Sleep Medicine, 13, 665-666. https://doi.org/10.5664/jcsm.6576

Buchmann, A., Dentico, D., Peterson, M. J., Riedner, B. A., Sarasso, S., Massimini, M., Tononi, G., & Ferrarelli, F. (2014). Reduced mediodorsal thalamic volume and prefrontal cortical spindle activity in schizophrenia. NeuroImage, 102(Pt 2), 540-547. https://doi.org/10.1016/j.neuroimage.2014.08.017

Califf, R. M. (2018). Biomarker definitions and their applications. Experimental Biology and Medicine (Maywood, N.J.), 243, 213-221. https://doi.org/10.1177/1535370217750088

Castelnovo, A., Graziano, B., Ferrarelli, F., & D'Agostino, A. (2018). Sleep spindles and slow waves in schizophrenia and related disorders: Main findings, challenges and future perspectives. The European Journal of Neuroscience, 48, 2738-2758. https://doi.org/10.1111/ejn.13815

Cohen, B. M., Ongur, D., & Babb, S. M. (2021). Alternative diagnostic models of the psychotic disorders: Evidence-based choices. Psychotherapy and Psychosomatics, 90, 373-385. https://doi.org/10.1159/000517027

Collaborators, G. B. D. M. D. (2022). Global, regional, and national burden of 12 mental disorders in 204 countries and territories, 1990-2019: A systematic analysis for the global burden of disease study 2019. Lancet Psychiatry, 9, 137-150. https://doi.org/10.1016/S2215-0366(21)00395-3

Daskalakis, Z. J., Farzan, F., Barr, M. S., Maller, J. J., Chen, R., & Fitzgerald, P. B. (2008). Long-interval cortical inhibition from the dorsolateral prefrontal cortex: A TMS-EEG study. Neuropsychopharmacology, 33, 2860-2869. https://doi.org/10.1038/npp.2008.22

De Gennaro, L., & Ferrara, M. (2003). Sleep spindles: An overview. Sleep Medicine Reviews, 7, 423-440. https://doi.org/10.1053/smrv.2002.0252

Diekelmann, S., & Born, J. (2010). The memory function of sleep. Nature Reviews. Neuroscience, 11, 114-126. https://doi.org/10.1038/nrn2762

Fernandez, L. M. J., & Luthi, A. (2020). Sleep spindles: Mechanisms and functions. Physiological Reviews, 100, 805-868. https://doi.org/10.1152/physrev.00042.2018

Ferrarelli, F. (2013). Endophenotypes and biological markers of schizophrenia: From biological signs of illness to novel treatment targets. Current Pharmaceutical Design, 19, 6462-6479. https://doi.org/10.2174/13816128113199990554

Ferrarelli, F. (2021). Sleep abnormalities in schizophrenia: State of the art and next steps. The American Journal of Psychiatry, appiajp202020070968, 903-913. https://doi.org/10.1176/appi.ajp.2020.20070968

Ferrarelli, F., Huber, R., Peterson, M. J., Massimini, M., Murphy, M., Riedner, B. A., Watson, A., Bria, P., & Tononi, G. (2007). Reduced sleep spindle activity in schizophrenia patients. The American Journal of Psychiatry, 164, 483-492. https://doi.org/10.1176/ajp.2007.164.3.483

Ferrarelli, F., Peterson, M. J., Sarasso, S., Riedner, B. A., Murphy, M. J., Benca, R. M., Bria, P., Kalin, N. H., & Tononi, G. (2010). Thalamic dysfunction in schizophrenia suggested by whole-night deficits in slow and fast spindles. The American Journal of Psychiatry, 167, 1339-1348. https://doi.org/10.1176/appi.ajp.2010.09121731

Ferrarelli, F., & Tononi, G. (2011). The thalamic reticular nucleus and schizophrenia. Schizophrenia Bulletin, 37, 306-315. https://doi.org/10.1093/schbul/sbq142

Ferrarelli, F., & Tononi, G. (2017). Reduced sleep spindle activity point to a TRN-MD thalamus-PFC circuit dysfunction in schizophrenia. Schizophrenia Research, 180, 36-43. https://doi.org/10.1016/j.schres.2016.05.023

Frohlich, F., & Lustenberger, C. (2020). Neuromodulation of sleep rhythms in schizophrenia: Towards the rational design of non-invasive brain stimulation. Schizophrenia Research, 221, 71-80. https://doi.org/10.1016/j.schres.2020.04.003

Genzel, L., Dresler, M., Cornu, M., Jager, E., Konrad, B., Adamczyk, M., Friess, E., Steiger, A., Czisch, M., & Goya-Maldonado, R. (2015). Medial prefrontal-hippocampal connectivity and motor memory consolidation in depression and schizophrenia. Biological Psychiatry, 77, 177-186. https://doi.org/10.1016/j.biopsych.2014.06.004

Gerstenberg, M., Furrer, M., Tesler, N., Franscini, M., Walitza, S., & Huber, R. (2020). Reduced sleep spindle density in adolescent patients with early-onset schizophrenia compared to major depressive disorder and healthy controls. Schizophrenia Research, 221, 20-28. https://doi.org/10.1016/j.schres.2019.11.060

Gimenez, S., Clos, S., Romero, S., Grasa, E., Morte, A., & Barbanoj, M. J. (2007). Effects of olanzapine, risperidone and haloperidol on sleep after a single oral morning dose in healthy volunteers. Psychopharmacology, 190, 507-516. https://doi.org/10.1007/s00213-006-0633-7

Giordano, G. M., Brando, F., Pezzella, P., de Angelis, M., Mucci, A., & Galderisi, S. (2022). Factors influencing the outcome of integrated therapy approach in schizophrenia: A narrative review of the literature. Frontiers in Psychiatry, 13, 970210. https://doi.org/10.3389/fpsyt.2022.970210

Goder, R., Fritzer, G., Gottwald, B., Lippmann, B., Seeck-Hirschner, M., Serafin, I., & Aldenhoff, J. B. (2008). Effects of olanzapine on slow wave sleep, sleep spindles and sleep-related memory consolidation in schizophrenia. Pharmacopsychiatry, 41, 92-99. https://doi.org/10.1055/s-2007-1004592

Halassa, M. M., Siegle, J. H., Ritt, J. T., Ting, J. T., Feng, G., & Moore, C. I. (2011). Selective optical drive of thalamic reticular nucleus generates thalamic bursts and cortical spindles. Nature Neuroscience, 14, 1118-1120. https://doi.org/10.1038/nn.2880

Hennevin, E., Huetz, C., & Edeline, J. M. (2007). Neural representations during sleep: From sensory processing to memory traces. Neurobiology of Learning and Memory, 87, 416-440. https://doi.org/10.1016/j.nlm.2006.10.006

Hjorthoj, C., Sturup, A. E., McGrath, J. J., & Nordentoft, M. (2017). Years of potential life lost and life expectancy in schizophrenia: A systematic review and meta-analysis. Lancet Psychiatry, 4, 295-301. https://doi.org/10.1016/S2215-0366(17)30078-0

Hoftman, G. D., Dienel, S. J., Bazmi, H. H., Zhang, Y., Chen, K., & Lewis, D. A. (2017). Altered gradients of glutamate and gamma-aminobutyric acid transcripts in the cortical visuospatial working memory network in schizophrenia. Biological Psychiatry, 83(8), 670-679.

Howes, O. D., & Shatalina, E. (2022). Integrating the neurodevelopmental and dopamine hypotheses of schizophrenia and the role of cortical excitation-inhibition balance. Biological Psychiatry, 92, 501-513. https://doi.org/10.1016/j.biopsych.2022.06.017

Javitt, D. C., & Freedman, R. (2015). Sensory processing dysfunction in the personal experience and neuronal machinery of schizophrenia. The American Journal of Psychiatry, 172, 17-31. https://doi.org/10.1176/appi.ajp.2014.13121691

Kahn, R. S., & Keefe, R. S. (2013). Schizophrenia is a cognitive illness: Time for a change in focus. JAMA Psychiatry, 70, 1107-1112. https://doi.org/10.1001/jamapsychiatry.2013.155

Kaskie, R. E., Graziano, B., & Ferrarelli, F. (2019). Topographic deficits in sleep spindle density and duration point to frontal thalamo-cortical dysfunctions in first-episode psychosis. Journal of Psychiatric Research, 113, 39-44. https://doi.org/10.1016/j.jpsychires.2019.03.009

Krause, M., Hoffmann, W. E., & Hajos, M. (2003). Auditory sensory gating in hippocampus and reticular thalamic neurons in anesthetized rats. Biological Psychiatry, 53, 244-253. https://doi.org/10.1016/S0006-3223(02)01463-4

Lacourse, K., Delfrate, J., Beaudry, J., Peppard, P., & Warby, S. C. (2019). A sleep spindle detection algorithm that emulates human expert spindle scoring. Journal of Neuroscience Methods, 316, 3-11. https://doi.org/10.1016/j.jneumeth.2018.08.014

Lai, M., Hegde, R., Kelly, S., Bannai, D., Lizano, P., Stickgold, R., Manoach, D. S., & Keshavan, M. (2022). Investigating sleep spindle density and schizophrenia: A meta-analysis. Psychiatry Research, 307, 114265. https://doi.org/10.1016/j.psychres.2021.114265

LaRocco, J., Franaszczuk, P. J., Kerick, S., & Robbins, K. (2018). Spindler: A framework for parametric analysis and detection of spindles in EEG with application to sleep spindles. Journal of Neural Engineering, 15, 066015. https://doi.org/10.1088/1741-2552/aadc1c

Lee, E. E., Adamowicz, D. H., Frangou, S., & Members of the, N.W.o.N.-A.P.i.M. & Beyond. (2023). An NIMH workshop on non-affective psychosis in midlife and beyond: Research agenda on phenomenology, clinical trajectories, underlying mechanisms, and intervention targets. The American Journal of Geriatric Psychiatry, 31, 353-365. https://doi.org/10.1016/j.jagp.2023.01.019

Leong, C. W. Y., Leow, J. W. S., Grunstein, R. R., Naismith, S. L., Teh, J. Z., D'Rozario, A. L., & Saini, B. (2022). A systematic scoping review of the effects of central nervous system active drugs on sleep spindles and sleep-dependent memory consolidation. Sleep Medicine Reviews, 62, 101605. https://doi.org/10.1016/j.smrv.2022.101605

Luptak, M., Michalickova, D., Fisar, Z., Kitzlerova, E., & Hroudova, J. (2021). Novel approaches in schizophrenia-from risk factors and hypotheses to novel drug targets. World Journal of Psychiatry, 11, 277-296. https://doi.org/10.5498/wjp.v11.i7.277

de Maertelaer, V., Hoffman, G., Lemaire, M., & Mendlewicz, J. (1987). Sleep spindle activity changes in patients with affective disorders. Sleep, 10, 443-451. https://doi.org/10.1093/sleep/10.5.443

Manoach, D. S., Demanuele, C., Wamsley, E. J., Vangel, M., Montrose, D. M., Miewald, J., Kupfer, D., Buysse, D., Stickgold, R., & Keshavan, M. S. (2014). Sleep spindle deficits in antipsychotic-naive early course schizophrenia and in non-psychotic first-degree relatives. Frontiers in Human Neuroscience, 8, 762. https://doi.org/10.3389/fnhum.2014.00762

Manoach, D. S., & Stickgold, R. (2019). Abnormal sleep spindles, memory consolidation, and schizophrenia. Annual Review of Clinical Psychology, 15, 451-479. https://doi.org/10.1146/annurev-clinpsy-050718-095754

Manoach, D. S., Thakkar, K. N., Stroynowski, E., Ely, A., McKinley, S. K., Wamsley, E., Djonlagic, I., Vangel, M. G., Goff, D. C., & Stickgold, R. (2010). Reduced overnight consolidation of procedural learning in chronic medicated schizophrenia is related to specific sleep stages. Journal of Psychiatric Research, 44, 112-120. https://doi.org/10.1016/j.jpsychires.2009.06.011

Massimini, M., Tononi, G., & Huber, R. (2009). Slow waves, synaptic plasticity and information processing: Insights from transcranial magnetic stimulation and high-density EEG experiments. The European Journal of Neuroscience, 29, 1761-1770. https://doi.org/10.1111/j.1460-9568.2009.06720.x

Mayeli, A., LaGoy, A. D., Smagula, S. F., Wilson, J. D., Zarbo, C., Rocchetti, M., Starace, F., Zamparini, M., Casiraghi, L., Calza, S., Rota, M., D'Agostino, A., de Girolamo, G., Di, A. C., & Ferrarelli, F. (2023). Shared and distinct abnormalities in sleep-wake patterns and their relationship with the negative symptoms of schizophrenia spectrum disorder patients. Molecular Psychiatry, 28, 2049-2057. https://doi.org/10.1038/s41380-023-02050-x

Mayeli, A., Wilson, J. D., Donati, F. L., LaGoy, A. D., & Ferrarelli, F. (2022). Sleep spindle alterations relate to working memory deficits in individuals at clinical high-risk for psychosis. Sleep, 45(11). https://doi.org/10.1093/sleep/zsac193

McCutcheon, R. A., Reis Marques, T., & Howes, O. D. (2020). Schizophrenia-An overview. JAMA Psychiatry, 77, 201-210. https://doi.org/10.1001/jamapsychiatry.2019.3360

Pellegrini, C., Lecci, S., Luthi, A., & Astori, S. (2016). Suppression of sleep spindle rhythmogenesis in mice with deletion of CaV3.2 and CaV3.3 T-type ca(2+) channels. Sleep, 39, 875-885. https://doi.org/10.5665/sleep.5646

Peltola, M. E., Leitinger, M., Halford, J. J., Vinayan, K. P., Kobayashi, K., Pressler, R. M., Mindruta, I., Mayor, L. C., Lauronen, L., & Beniczky, S. (2023). Routine and sleep EEG: Minimum recording standards of the International Federation of Clinical Neurophysiology and the international league against epilepsy. Clinical Neurophysiology, 147, 108-120. https://doi.org/10.1016/j.clinph.2023.01.002

Perrottelli, A., Giordano, G. M., Brando, F., Giuliani, L., Pezzella, P., Mucci, A., & Galderisi, S. (2022). Unveiling the associations between EEG indices and cognitive deficits in schizophrenia-spectrum disorders: A systematic review. Diagnostics (Basel), 12, 2193. https://doi.org/10.3390/diagnostics12092193

Peters, K. R., Ray, L. B., Fogel, S., Smith, V., & Smith, C. T. (2014). Age differences in the variability and distribution of sleep spindle and rapid eye movement densities. PLoS ONE, 9, e91047. https://doi.org/10.1371/journal.pone.0091047

Petit, J. M., Strippoli, M. F., Stephan, A., Ranjbar, S., Haba-Rubio, J., Solelhac, G., Heinzer, R., Preisig, M., Siclari, F., & Do, K. Q. (2022). Sleep spindles in people with schizophrenia, schizoaffective disorders or bipolar disorders: A pilot study in a general population-based cohort. BMC Psychiatry, 22, 758. https://doi.org/10.1186/s12888-022-04423-y

Purcell, S. M., Manoach, D. S., Demanuele, C., Cade, B. E., Mariani, S., Cox, R., Panagiotaropoulou, G., Saxena, R., Pan, J. Q., Smoller, J. W., Redline, S., & Stickgold, R. (2017). Characterizing sleep spindles in 11,630 individuals from the National Sleep Research Resource. Nature Communications, 8, 15930. https://doi.org/10.1038/ncomms15930

Ritter, P. S., Schwabedal, J., Brandt, M., Schrempf, W., Brezan, F., Krupka, A., Sauer, C., Pfennig, A., Bauer, M., Soltmann, B., & Nikitin, E. (2018). Sleep spindles in bipolar disorder - a comparison to healthy control subjects. Acta Psychiatrica Scandinavica, 138, 163-172. https://doi.org/10.1111/acps.12924

Schilling, C., Schlipf, M., Spietzack, S., Rausch, F., Eisenacher, S., Englisch, S., Reinhard, I., Haller, L., Grimm, O., Deuschle, M., Tost, H., Zink, M., Meyer-Lindenberg, A., & Schredl, M. (2017). Fast sleep spindle reduction in schizophrenia and healthy first-degree relatives: Association with impaired cognitive function and potential intermediate phenotype. European Archives of Psychiatry and Clinical Neuroscience, 267, 213-224. https://doi.org/10.1007/s00406-016-0725-2

Schizophrenia Working Group of the Psychiatric Genomics, C. (2014). Biological insights from 108 schizophrenia-associated genetic loci. Nature, 511, 421-427. https://doi.org/10.1038/nature13595

Silber, M. H., Ancoli-Israel, S., Bonnet, M. H., Chokroverty, S., Grigg-Damberger, M. M., Hirshkowitz, M., Kapen, S., Keenan, S. A., Kryger, M. H., Penzel, T., Pressman, M. R., & Iber, C. (2007). The visual scoring of sleep in adults. Journal of Clinical Sleep Medicine, 3, 121-131. https://doi.org/10.5664/jcsm.26814

Steriade, M., Domich, L., Oakson, G., & Deschenes, M. (1987). The deafferented reticular thalamic nucleus generates spindle rhythmicity. Journal of Neurophysiology, 57, 260-273. https://doi.org/10.1152/jn.1987.57.1.260

Steriade, M., McCormick, D. A., & Sejnowski, T. J. (1993). Thalamocortical oscillations in the sleeping and aroused brain. Science, 262, 679-685. https://doi.org/10.1126/science.8235588

Sun, Y. G., Wu, C. S., Renger, J. J., Uebele, V. N., Lu, H. C., & Beierlein, M. (2012). GABAergic synaptic transmission triggers action potentials in thalamic reticular nucleus neurons. The Journal of Neuroscience, 32, 7782-7790. https://doi.org/10.1523/JNEUROSCI.0839-12.2012

Talley, E. M., Cribbs, L. L., Lee, J. H., Daud, A., Perez-Reyes, E., & Bayliss, D. A. (1999). Differential distribution of three members of a gene family encoding low voltage-activated (T-type) calcium channels. The Journal of Neuroscience, 19, 1895-1911. https://doi.org/10.1523/JNEUROSCI.19-06-01895.1999

Tamminga, C. A., Pearlson, G. D., Stan, A. D., Gibbons, R. D., Padmanabhan, J., Keshavan, M., & Clementz, B. A. (2017). Strategies for advancing disease definition using biomarkers and genetics: The bipolar and schizophrenia network for intermediate phenotypes. Biological Psychiatry: Cognitive Neuroscience and Neuroimaging, 2, 20-27. https://doi.org/10.1016/j.bpsc.2016.07.005

Thibaut, F., Boutros, N. N., Jarema, M., Oranje, B., Hasan, A., Daskalakis, Z. J., Wichniak, A., Schmitt, A., Riederer, P., Falkai, P., & Markers, W.T.F.o.B. (2015). Consensus paper of the WFSBP task force on biological markers: Criteria for biomarkers and endophenotypes of schizophrenia part I: Neurophysiology. The World Journal of Biological Psychiatry, 16, 280-290. https://doi.org/10.3109/15622975.2015.1050061

Thompson, M., Weickert, C. S., Wyatt, E., & Webster, M. J. (2009). Decreased glutamic acid decarboxylase(67) mRNA expression in multiple brain areas of patients with schizophrenia and mood disorders. Journal of Psychiatric Research, 43, 970-977. https://doi.org/10.1016/j.jpsychires.2009.02.005

Tsekou, H., Angelopoulos, E., Paparrigopoulos, T., Golemati, S., Soldatos, C. R., Papadimitriou, G. N., & Ktonas, P. Y. (2015). Sleep EEG and spindle characteristics after combination treatment with clozapine in drug-resistant schizophrenia: A pilot study. Journal of Clinical Neurophysiology, 32, 159-163. https://doi.org/10.1097/WNP.0000000000000145

Ulrich, D., Lalanne, T., Gassmann, M., & Bettler, B. (2018). GABA(B) receptor subtypes differentially regulate thalamic spindle oscillations. Neuropharmacology, 136, 106-116. https://doi.org/10.1016/j.neuropharm.2017.10.033

Vukadinovic, Z. (2011). Sleep abnormalities in schizophrenia may suggest impaired trans-thalamic cortico-cortical communication: Towards a dynamic model of the illness. The European Journal of Neuroscience, 34, 1031-1039. https://doi.org/10.1111/j.1460-9568.2011.07822.x

Wamsley, E. J., Tucker, M. A., Shinn, A. K., Ono, K. E., McKinley, S. K., Ely, A. V., Goff, D. C., Stickgold, R., & Manoach, D. S. (2012). Reduced sleep spindles and spindle coherence in schizophrenia: Mechanisms of impaired memory consolidation? Biological Psychiatry, 71, 154-161. https://doi.org/10.1016/j.biopsych.2011.08.008

Wang, H., & Zhuo, M. (2012). Group I metabotropic glutamate receptor-mediated gene transcription and implications for synaptic plasticity and diseases. Frontiers in Pharmacology, 3, 189. https://doi.org/10.3389/fphar.2012.00189

Warby, S. C., Wendt, S. L., Welinder, P., Munk, E. G., Carrillo, O., Sorensen, H. B., Jennum, P., Peppard, P. E., Perona, P., & Mignot, E. (2014). Sleep-spindle detection: Crowdsourcing and evaluating performance of experts, non-experts and automated methods. Nature Methods, 11, 385-392. https://doi.org/10.1038/nmeth.2855

Wei, P. P., Hunter, S. K., & Ross, R. G. (2017). Sleep spindles and auditory sensory gating: Two measures of cerebral inhibition in preschool-aged children are strongly correlated. Colo Journal of Child Psychology and Psychiatry, 2, 75-83.

Woodward, N. D., & Heckers, S. (2015). Mapping thalamocortical functional connectivity in chronic and early stages of psychotic disorders. Biological Psychiatry, 79(12), 1016-1025.

Woodward, N. D., Karbasforoushan, H., & Heckers, S. (2012). Thalamocortical dysconnectivity in schizophrenia. The American Journal of Psychiatry, 169, 1092-1099. https://doi.org/10.1176/appi.ajp.2012.12010056