Sleep in Patients With Schizophrenia

Whiteford HA, Degenhardt L, Rehm J, Baxter AJ, Ferrari AJ, Erskine HE, et al. Global burden of disease attributable to mental and substance use disorders: findings from the Global Burden of Disease Study 2010. Lancet. 2013;382(9904):1575–86.

Fusar-Poli P, Politi P. Paul Eugen Bleuler and the birth of schizophrenia (1908). Am J Psychiatry. 2008;165(11):1407.

Barch DM, Bustillo J, Gaebel W, Gur R, Heckers S, Malaspina D, et al. Logic and justification for dimensional assessment of symptoms and related clinical phenomena in psychosis: relevance to DSM-5. Schizophr Res. 2013;150(1):15–20.

Gur RE, Calkins ME, Gur RC, Horan WP, Nuechterlein KH, Seidman LJ, et al. The Consortium on the Genetics of Schizophrenia: neurocognitive endophenotypes. Schizophr Bull. 2007;33(1):49–68.

Onitsuka T, Oribe N, Nakamura I, Kanba S. Review of neurophysiological findings in patients with schizophrenia. Psychiatry Clin Neurosci. 2013;67(7):461–70.

Schaefer J, Giangrande E, Weinberger DR, Dickinson D. The global cognitive impairment in schizophrenia: consistent over decades and around the world. Schizophr Res. 2013;150(1):42–50.

Riedner BA, Hulse BK, Murphy MJ, Ferrarelli F, Tononi G. Temporal dynamics of cortical sources underlying spontaneous and peripherally evoked slow waves. Prog Brain Res. 2011;193:201–18.

Luthi A. Sleep spindles: where they come from, what they do. Neurosci Rev J Bring Neurobiol Neurol Psychiatry. 2013;20(3):243–56. doi: 10.1177/1073858413500854 .

Diekelmann S, Born J. The memory function of sleep. Nat Rev Neurosci. 2010;11(2):114–26.

Tononi G. Slow wave homeostasis and synaptic plasticity. J Clin Sleep Med JCSM Off Publ Am Acad Sleep Med. 2009;5(2 Suppl):S16–9.

Manoach DS, Stickgold R. Does abnormal sleep impair memory consolidation in schizophrenia? Front Hum Neurosci. 2009;3:21.

Wamsley EJ, Shinn AK, Tucker MA, Ono KE, McKinley SK, Ely AV, et al. The effects of eszopiclone on sleep spindles and memory consolidation in schizophrenia: a randomized placebo-controlled trial. Sleep. 2013;36(9):1369–76. This is the first study showing a pharmacologically mediated improvement in sleep spindle incidence in patients with schizophrenia.

Monti JM, Monti D. Sleep disturbance in schizophrenia. Int Rev Psychiatry. 2005;17(4):247–53.

Kahn-Greene ET, Killgore DB, Kamimori GH, Balkin TJ, Killgore WD. The effects of sleep deprivation on symptoms of psychopathology in healthy adults. Sleep Med. 2007;8(3):215–21.

Miller TJ, Zipursky RB, Perkins D, Addington J, Woods SW, Hawkins KA, et al. The PRIME North America randomized double-blind clinical trial of olanzapine versus placebo in patients at risk of being prodromally symptomatic for psychosis. II. Baseline characteristics of the "prodromal" sample. Schizophr Res. 2003;61(1):19–30.

Gordon JA, Moore H. Charting a course toward an understanding of schizophrenia. Neuron. 2012;76(3):465–7.

Keefe RS. The longitudinal course of cognitive impairment in schizophrenia: an examination of data from premorbid through posttreatment phases of illness. J Clin Psychiatry. 2014;75 Suppl 2:8–13.

Yang C, Winkelman JW. Clinical significance of sleep EEG abnormalities in chronic schizophrenia. Schizophr Res. 2006;82(2–3):251–60.

Poulin J, Daoust AM, Forest G, Stip E, Godbout R. Sleep architecture and its clinical correlates in first episode and neuroleptic-naive patients with schizophrenia. Schizophr Res. 2003;62(1–2):147–53.

Keshavan MS, Reynolds 3rd CF, Miewald MJ, Montrose DM, Sweeney JA, Vasko Jr RC, et al. Delta sleep deficits in schizophrenia: evidence from automated analyses of sleep data. Arch Gen Psychiatry. 1998;55(5):443–8.

Chouinard S, Poulin J, Stip E, Godbout R. Sleep in untreated patients with schizophrenia: a meta-analysis. Schizophr Bull. 2004;30(4):957–67.

Hiatt JF, Floyd TC, Katz PH, Feinberg I. Further evidence of abnormal non-rapid-eye-movement sleep in schizophrenia. Arch Gen Psychiatry. 1985;42(8):797–802.

Goder R, Aldenhoff JB, Boigs M, Braun S, Koch J, Fritzer G. Delta power in sleep in relation to neuropsychological performance in healthy subjects and schizophrenia patients. J Neuropsychiatry Clin Neurosci. 2006;18(4):529–35.

Tekell JL, Hoffmann R, Hendrickse W, Greene RW, Rush AJ, Armitage R. High frequency EEG activity during sleep: characteristics in schizophrenia and depression. Clin EEG Neurosci. 2005;36(1):25–35.

Ferrarelli F, Huber R, Peterson MJ, Massimini M, Murphy M, Riedner BA, et al. Reduced sleep spindle activity in schizophrenia patients. Am J Psychiatry. 2007;164(3):483–92. This is the first study showing spindle activity deficits in patients with schizophrenia employing hd-EEG.

Ferrarelli F, Peterson MJ, Sarasso S, Riedner BA, Murphy MJ, Benca RM, et al. Thalamic dysfunction in schizophrenia suggested by whole-night deficits in slow and fast spindles. Am J Psychiatry. 2010;167(11):1339–48. In this follow-up study it was shown that spindle deficits were unrelated to antipsychotic medications and they were likely specific for schizophrenia patients.

Boutros NN, Mucci A, Vignapiano A, Galderisi S. Electrophysiological aberrations associated with negative symptoms in schizophrenia. Curr Top Behav Neurosci. 2014. doi: 10.1007/7854_2014_303 .

Van Cauter E, Linkowski P, Kerkhofs M, Hubain P, L'Hermite-Baleriaux M, Leclercq R, et al. Circadian and sleep-related endocrine rhythms in schizophrenia. Arch Gen Psychiatry. 1991;48(4):348–56.

Ferrarelli F, Tononi G. The thalamic reticular nucleus and schizophrenia. Schizophr Bull. 2011;37(2):306–15.

Manoach DS, Demanuele C, Wamsley EJ, Vangel M, Montrose DM, Miewald J, et al. Sleep spindle deficits in antipsychotic-naive early course schizophrenia and in non-psychotic first-degree relatives. Front Hum Neurosci. 2014;8:762. This study established reduced spindle activity in first-break schizophrenia patients and their relatives compared to healthy controls and to early course patients with other psychotic disorders.

Pinault D. The thalamic reticular nucleus: structure, function and concept. Brain Res Brain Res Rev. 2004;46(1):1–31.

Fuentealba P, Steriade M. The reticular nucleus revisited: intrinsic and network properties of a thalamic pacemaker. Prog Neurobiol. 2005;75(2):125–41.

McAlonan K, Cavanaugh J, Wurtz RH. Guarding the gateway to cortex with attention in visual thalamus. Nature. 2008;456(7220):391–4.

Krause M, Hoffmann WE, Hajos M. Auditory sensory gating in hippocampus and reticular thalamic neurons in anesthetized rats. Biol Psychiatry. 2003;53(3):244–53.

Freedman R, Ross R, Leonard S, Myles-Worsley M, Adams CE, Waldo M, et al. Early biomarkers of psychosis. Dialogues Clin Neurosci. 2005;7(1):17–29.

Sherman SM, Guillery RW. The role of the thalamus in the flow of information to the cortex. Philos Trans R Soc Lond B Biol Sci. 2002;357(1428):1695–708.

Buchmann A, Dentico D, Peterson MJ, Riedner BA, Sarasso S, Massimini M, et al. Reduced mediodorsal thalamic volume and prefrontal cortical spindle activity in schizophrenia. Neuroimage. 2014;102(Pt 2):540–7. This study's findings point to a TRN-MD thalamus-prefrontal cortex circuit defect, which may underie spindle deficits and cognitive impairment in schizophrenia.

Nakamura M, Uchida S, Maehara T, Kawai K, Hirai N, Nakabayashi T, et al. Sleep spindles in human prefrontal cortex: an electrocorticographic study. Neurosci Res. 2003;45(4):419–27.

Camchong J, Dyckman KA, Chapman CE, Yanasak NE, McDowell JE. Basal ganglia-thalamocortical circuitry disruptions in schizophrenia during delayed response tasks. Biol Psychiatry. 2006;60(3):235–41.

Ferrarelli F, Massimini M, Peterson MJ, Riedner BA, Lazar M, Murphy MJ, et al. Reduced evoked gamma oscillations in the frontal cortex in schizophrenia patients: a TMS/EEG study. Am J Psychiatry. 2008;165(8):996–1005.

Akbarian S, Kim JJ, Potkin SG, Hetrick WP, Bunney Jr WE, Jones EG. Maldistribution of interstitial neurons in prefrontal white matter of the brains of schizophrenic patients. Arch Gen Psychiatry. 1996;53(5):425–36.

Gardner RJ, Hughes SW, Jones MW. Differential spike timing and phase dynamics of reticular thalamic and prefrontal cortical neuronal populations during sleep spindles. J Neurosci. 2013;33(47):18469–80.

Ramcharan EJ, Gnadt JW, Sherman SM. Higher-order thalamic relays burst more than first-order relays. Proc Natl Acad Sci U S A. 2005;102(34):12236–41.

Wei H, Bonjean M, Petry HM, Sejnowski TJ, Bickford ME. Thalamic burst firing propensity: a comparison of the dorsal lateral geniculate and pulvinar nuclei in the tree shrew. J Neurosci. 2011;31(47):17287–99.

Astori S, Wimmer RD, Luthi A. Manipulating sleep spindles–expanding views on sleep, memory, and disease. Trends Neurosci. 2013;36(12):738–48. This is an elegant review on the current understanding of spindles in sleep, memory, and mental illness.

Huguenard JR. Low-threshold calcium currents in central nervous system neurons. Annu Rev Physiol. 1996;58:329–48. doi: 10.1146/annurev.ph.58.030196.001553 .

Talley EM, Cribbs LL, Lee JH, Daud A, Perez-Reyes E, Bayliss DA. Differential distribution of three members of a gene family encoding low voltage-activated (T-type) calcium channels. J Neurosci Off J Soc Neurosci. 1999;19(6):1895–911.

Astori S, Wimmer RD, Prosser HM, Corti C, Corsi M, Liaudet N, et al. The Ca(V)3.3 calcium channel is the major sleep spindle pacemaker in thalamus. Proc Natl Acad Sci U S A. 2011;108(33):13823–8. This study shows that the Ca(V)3.3 calcium channel, which is expressed abundantly in the TRN, is the major sleep spindle pacemaker in thalamus.

Irish Schizophrenia Genomics C, the Wellcome Trust Case Control C. Genome-wide association study implicates HLA-C*01:02 as a risk factor at the major histocompatibility complex locus in schizophrenia. Biol Psychiatry. 2012;72(8):620–8.

Schizophrenia Working Group of the Psychiatric Genomics C. Biological insights from 108 schizophrenia-associated genetic loci. Nature. 2014;511(7510):421–7. This large multi-stage schizophrenia genome-wide association studypresents 108 loci, including genes regulating calcium channels, significantly associated to schizophrenia.

Pangratz-Fuehrer S, Rudolph U, Huguenard JR. Giant spontaneous depolarizing potentials in the developing thalamic reticular nucleus. J Neurophysiol. 2007;97(3):2364–72.

Cadenhead KS, Light GA, Shafer KM, Braff DL. P50 suppression in individuals at risk for schizophrenia: the convergence of clinical, familial, and vulnerability marker risk assessment. Biol Psychiatry. 2005;57(12):1504–9.

Lewis DA, Hashimoto T, Volk DW. Cortical inhibitory neurons and schizophrenia. Nat Rev Neurosci. 2005;6(4):312–24.

Daskalakis ZJ, Christensen BK, Fitzgerald PB, Moller B, Fountain SI, Chen R. Increased cortical inhibition in persons with schizophrenia treated with clozapine. J Psychopharmacol. 2008;22(2):203–9.

Pakkenberg B, Scheel-Kruger J, Kristiansen LV. Schizophrenia; from structure to function with special focus on the mediodorsal thalamic prefrontal loop. Acta Psychiatr Scand. 2009;120(5):345–54.

Santana N, Troyano-Rodriguez E, Mengod G, Celada P, Artigas F. Activation of thalamocortical networks by the N-methyl-D-aspartate receptor antagonist phencyclidine: reversal by clozapine. Biol Psychiatry. 2011;69(10):918–27.

Jardemark K, Marcus MM, Shahid M, Svensson TH. Effects of asenapine on prefrontal N-methyl-D-aspartate receptor-mediated transmission: involvement of dopamine D1 receptors. Synapse. 2010;64(11):870–4.

Zhang Y, Llinas RR, Lisman JE. Inhibition of NMDARs in the nucleus reticularis of the thalamus produces delta frequency bursting. Front Neural Circ. 2009;3:20.

Dawson N, Morris BJ, Pratt JA. Subanaesthetic ketamine treatment alters prefrontal cortex connectivity with thalamus and ascending subcortical systems. Schizophr Bull. 2013;39(2):366–77.

Wilson S, Argyropoulos S. Sleep in schizophrenia: time for closer attention. Br J Psychiatry. 2012;200(4):273–4.

Pisarenco I, Caporro M, Prosperetti C, Manconi M. High-density electroencephalography as an innovative tool to explore sleep physiology and sleep related disorders. Int J Psychophysiol. 2014.

Born J, Wilhelm I. System consolidation of memory during sleep. Psychol Res. 2012;76(2):192–203.

Massimini M, Tononi G, Huber R. Slow waves, synaptic plasticity and information processing: insights from transcranial magnetic stimulation and high-density EEG experiments. Eur J Neurosci. 2009;29(9):1761–70.

Massimini M, Ferrarelli F, Esser SK, Riedner BA, Huber R, Murphy M, et al. Triggering sleep slow waves by transcranial magnetic stimulation. Proc Natl Acad Sci U S A. 2007;104(20):8496–501.

Buzsaki G, Watson BO. Brain rhythms and neural syntax: implications for efficient coding of cognitive content and neuropsychiatric disease. Dialogues Clin Neurosci. 2012;14(4):345–67.