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Sleep Spindle Deficit in Schizophrenia: Contextualization of Recent Findings

  • Sleep Disorders (P Gehrman, Section Editor)
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Abstract

Sleep spindles are wax and waning brain oscillations at a frequency range of 11–16 Hz, lasting 0.5–2 s, that define non-rapid eye movement sleep stage 2. Over the past few years, several independent studies pointed to a decrease of sleep spindles in schizophrenia. The aim of this review is to contextualize these findings within the growing literature on these oscillations across other neuro-psychiatric disorders. Indeed, spindles reflect the coordinated activity of thalamocortical networks, and their abnormality can be observed in a variety of conditions that disrupt local or global thalamocortical connectivity. Although the broad methodological variability across studies limits the possibility of drawing firm conclusions, impaired spindling activity has been observed in several neurodevelopmental and neurodegenerative disorders. Despite such lack of specificity, schizophrenia remains the only condition with a typical late adolescence to young adulthood onset in which impaired spindling has been consistently reported. Further research is necessary to clearly define the pathogenetic mechanisms that lead to this deficit and the validity of its widespread use as a clinical biomarker.

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References

Papers of particular interest, published recently, have been highlighted as • Of importance

  1. Keshavan MS, Reynolds 3rd CF, Miewald JM, Montrose DM. A longitudinal study of EEG sleep in schizophrenia. Psychiatry Res. 1996;59(3):203–11.

    Article  CAS  PubMed  Google Scholar 

  2. Gardner RJ, Kersante F, Jones MW, Bartsch U. Neural oscillations during non-rapid eye movement sleep as biomarkers of circuit dysfunction in schizophrenia. Eur J Neurosci. 2014;39(7):1091–106. doi:10.1111/ejn.12533.

    Article  PubMed  Google Scholar 

  3. Andrillon T, Nir Y, Staba RJ, Ferrarelli F, Cirelli C, Tononi G, et al. Sleep spindles in humans: insights from intracranial EEG and unit recordings. J Neurosci. 2011;31(49):17821–34. doi:10.1523/JNEUROSCI.2604-11.2011.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Frauscher B, Bernasconi N, Caldairou B, von Ellenrieder N, Bernasconi A, Gotman J, et al. Interictal hippocampal spiking influences the occurrence of hippocampal sleep spindles. Sleep. 2015;38(12):1927–33. doi:10.5665/sleep.5242.

    Article  PubMed  PubMed Central  Google Scholar 

  5. Frauscher B, von Ellenrieder N, Dubeau F, Gotman J. Scalp spindles are associated with widespread intracranial activity with unexpectedly low synchrony. NeuroImage. 2015;105:1–12. doi:10.1016/j.neuroimage.2014.10.048.

    Article  PubMed  PubMed Central  Google Scholar 

  6. Sarasso S, Proserpio P, Pigorini A, Moroni F, Ferrara M, De Gennaro L, et al. Hippocampal sleep spindles preceding neocortical sleep onset in humans. NeuroImage. 2014;86:425–32. doi:10.1016/j.neuroimage.2013.10.031.

    Article  CAS  PubMed  Google Scholar 

  7. Astori S, Wimmer RD, Luthi A. Manipulating sleep spindles—expanding views on sleep, memory, and disease. Trends Neurosci. 2013;36(12):738–48. doi:10.1016/j.tins.2013.10.001.

    Article  CAS  PubMed  Google Scholar 

  8. 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.

    Article  CAS  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  10. Poulin J, Daoust A-M, 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):147–53.

    Article  PubMed  Google Scholar 

  11. 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. doi:10.1176/ajp.2007.164.3.483.

    Article  PubMed  Google Scholar 

  12. 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. doi:10.1176/appi.ajp.2010.09121731.

    Article  PubMed  PubMed Central  Google Scholar 

  13. 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. doi:10.1016/j.neuroimage.2014.08.017.

    Article  PubMed  PubMed Central  Google Scholar 

  14. Manoach DS, Thakkar KN, Stroynowski E, Ely A, McKinley SK, Wamsley E, et al. Reduced overnight consolidation of procedural learning in chronic medicated schizophrenia is related to specific sleep stages. J Psychiatr Res. 2010;44(2):112–20. doi:10.1016/j.jpsychires.2009.06.011.

    Article  PubMed  Google Scholar 

  15. Wamsley EJ, Tucker MA, Shinn AK, Ono KE, McKinley SK, Ely AV, et al. Reduced sleep spindles and spindle coherence in schizophrenia: mechanisms of impaired memory consolidation? Biol Psychiatry. 2012;71(2):154–61. doi:10.1016/j.biopsych.2011.08.008.

    Article  PubMed  Google Scholar 

  16. Seeck-Hirschner M, Baier PC, Sever S, Buschbacher A, Aldenhoff JB, Goder R. Effects of daytime naps on procedural and declarative memory in patients with schizophrenia. J Psychiatr Res. 2010;44(1):42–7. doi:10.1016/j.jpsychires.2009.05.008.

    Article  PubMed  Google Scholar 

  17. Keshavan MS, Montrose DM, Miewald JM, Jindal RD. Sleep correlates of cognition in early course psychotic disorders. Schizophr Res. 2011;131(1-3):231–4. doi:10.1016/j.schres.2011.05.027.

    Article  PubMed  PubMed Central  Google Scholar 

  18. Goder R, Graf A, Ballhausen F, Weinhold S, Baier PC, Junghanns K, et al. Impairment of sleep-related memory consolidation in schizophrenia: relevance of sleep spindles? Sleep Med. 2015;16(5):564–9. doi:10.1016/j.sleep.2014.12.022. This study showed that the memory-promoting effect of sleep was significantly lower in chronic schizophrenia patients than in controls for a visual recognition task using neutral and emotional pictures. The performance at this task correlated with sleep spindle density, which was reduced in patients compared to controls.

    Article  PubMed  Google Scholar 

  19. 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. doi:10.3389/fnhum.2014.00762. This is the first study investigating sleep spindles in antipsychotic-naïve early-course schizophrenia patients and in non-psychotic first-degree relatives. The finding of a deficit in sleep spindle density, which correlated with cognitive performance, indicates that the spindle deficit may be an endophenotype of the disorder.

    Article  PubMed  PubMed Central  Google Scholar 

  20. Tesler N, Gerstenberg M, Franscini M, Jenni OG, Walitza S, Huber R. Reduced sleep spindle density in early onset schizophrenia: a preliminary finding. Schizophr Res. 2015;166(1-3):355–7. doi:10.1016/j.schres.2015.04.042. This is the first study showing a reduction in sleep spindle density in a group of nine adolescents with early-onset schizophrenia.

    Article  PubMed  Google Scholar 

  21. Guénolé F, Chevrier É, Stip E, Godbout R. A microstructural study of sleep instability in drug-naive patients with schizophrenia and healthy controls: sleep spindles, rapid eye movements, and muscle atonia. Schizophr Res. 2014;155(1):31–8.

    Article  PubMed  Google Scholar 

  22. Genzel L, Dresler M, Cornu M, Jager E, Konrad B, Adamczyk M, et al. Medial prefrontal-hippocampal connectivity and motor memory consolidation in depression and schizophrenia. Biol Psychiatry. 2015;77(2):177–86. doi:10.1016/j.biopsych.2014.06.004.

    Article  PubMed  Google Scholar 

  23. Lustenberger C, O’Gorman RL, Pugin F, Tushaus L, Wehrle F, Achermann P, et al. Sleep spindles are related to schizotypal personality traits and thalamic glutamine/glutamate in healthy subjects. Schizophr Bull. 2015;41(2):522–31. doi:10.1093/schbul/sbu109.

    Article  PubMed  Google Scholar 

  24. Goetz RR, Goetz DM, Hanlon C, Davies M, Weitzman ED, Puig-Antich J. Spindle characteristics in prepubertal major depressives during an episode and after sustained recovery: a controlled study. Sleep. 1983;6(4):369–75.

    CAS  PubMed  Google Scholar 

  25. Reynolds 3rd CF, Kupfer DJ, Taska LS, Hoch CC, Spiker DG, Sewitch DE, et al. EEG sleep in elderly depressed, demented, and healthy subjects. Biol Psychiatry. 1985;20(4):431–42.

    Article  PubMed  Google Scholar 

  26. de Maertelaer V, Hoffman G, Lemaire M, Mendlewicz J. Sleep spindle activity changes in patients with affective disorders. Sleep. 1987;10(5):443–51.

    PubMed  Google Scholar 

  27. Lopez J, Hoffmann R, Armitage R. Reduced sleep spindle activity in early-onset and elevated risk for depression. J Am Acad Child Adolesc Psychiatry. 2010;49(9):934–43.

    Article  PubMed  PubMed Central  Google Scholar 

  28. Plante DT, Goldstein MR, Landsness EC, Peterson MJ, Riedner BA, Ferrarelli F, et al. Topographic and sex-related differences in sleep spindles in major depressive disorder: a high-density EEG investigation. J Affect Disord. 2013;146(1):120–5. doi:10.1016/j.jad.2012.06.016.

    Article  CAS  PubMed  Google Scholar 

  29. Roth C, Jeanmonod D, Magnin M, Morel A, Achermann P. Effects of medial thalamotomy and pallido-thalamic tractotomy on sleep and waking EEG in pain and Parkinsonian patients. Clin Neurophysiol. 2000;111(7):1266–75.

    Article  CAS  PubMed  Google Scholar 

  30. Henriksen GF, Grossman C, Merlis JK. EEG observations in a case with thalamic syndrome. Electroencephalogr Clin Neurophysiol. 1949;1(4):505–7.

    Article  CAS  PubMed  Google Scholar 

  31. Jurko M, Andy O. Serial EEG study following thalamotomy. Electroencephalogr Clin Neurophysiol. 1965;18(5):500–3.

    Article  CAS  PubMed  Google Scholar 

  32. Jurko M, Andy O. Diencephalic lesion effects on EEG sleep patterns. Electroencephalogr Clin Neurophysiol. 1969;27(5):551.

    CAS  PubMed  Google Scholar 

  33. Webster C, Jurko M, Andy O. Spindling alterations following diencephalotomy. Stereotact Funct Neurosurg. 1965;26(3-5):269–71.

    Google Scholar 

  34. Guilleminault C, Quera-Salva MA, Goldberg MP. Pseudo-hypersomnia and pre-sleep behaviour with bilateral paramedian thalamic lesions. Brain J Neurol. 1993;116(Pt 6):1549–63.

    Article  Google Scholar 

  35. Hermann DM, Siccoli M, Brugger P, Wachter K, Mathis J, Achermann P, et al. Evolution of neurological, neuropsychological and sleep-wake disturbances after paramedian thalamic stroke. Stroke J Cereb Circ. 2008;39(1):62–8. doi:10.1161/STROKEAHA.107.494955.

    Article  Google Scholar 

  36. Bassetti C, Mathis J, Gugger M, Lovblad KO, Hess CW. Hypersomnia following paramedian thalamic stroke: a report of 12 patients. Ann Neurol. 1996;39(4):471–80. doi:10.1002/ana.410390409.

    Article  CAS  PubMed  Google Scholar 

  37. Jurko M, Andy O, Webster C. Disordered sleep patterns following thalamotomy. Clin Electroencephalogr. 1971;2:213–7.

    Google Scholar 

  38. Rossetti AO, Maeder-Ingvar M, Reichhart MD, Despland PA, Bogousslavsky J. Transitory sleep spindles impairment in deep cerebral venous thrombosis. Neurophysiol Clin = Clin Neurophysiol. 2005;35(1):19–23. doi:10.1016/j.neucli.2004.12.003.

    Article  Google Scholar 

  39. Santamaria J, Pujol M, Orteu N, Solanas A, Cardenal C, Santacruz P, et al. Unilateral thalamic stroke does not decrease ipsilateral sleep spindles. Sleep. 2000;23(3):333–9.

    CAS  PubMed  Google Scholar 

  40. Bassetti CL, Aldrich MS. Sleep electroencephalogram changes in acute hemispheric stroke. Sleep Med. 2001;2(3):185–94.

    Article  PubMed  Google Scholar 

  41. Gottselig JM, Bassetti CL, Achermann P. Power and coherence of sleep spindle frequency activity following hemispheric stroke. Brain J Neurol. 2002;125(Pt 2):373–83.

    Article  CAS  Google Scholar 

  42. Poryazova R, Huber R, Khatami R, Werth E, Brugger P, Barath K, et al. Topographic sleep EEG changes in the acute and chronic stage of hemispheric stroke. J Sleep Res. 2015;24(1):54–65. doi:10.1111/jsr.12208.

    Article  PubMed  Google Scholar 

  43. Crowley K, Trinder J, Kim Y, Carrington M, Colrain IM. The effects of normal aging on sleep spindle and K-complex production. Clin Neurophysiol. 2002;113(10):1615–22.

    Article  PubMed  Google Scholar 

  44. Wauquier A. Aging and changes in phasic events during sleep. Physiol Behav. 1993;54(4):803���6.

    Article  CAS  PubMed  Google Scholar 

  45. Stratmann K, Heinsen H, Korf HW, Del Turco D, Ghebremedhin E, Seidel K, et al. Precortical phase of Alzheimer’s disease (AD)-related tau cytoskeletal pathology. Brain Pathol. 2015. doi:10.1111/bpa.12289.

    PubMed  Google Scholar 

  46. Prinz PN, Peskind ER, Vitaliano PP, Raskind MA, Eisdorfer C, Zemcuznikov N, et al. Changes in the sleep and waking EEGs of nondemented and demented elderly subjects. J Am Geriatr Soc. 1982;30(2):86–93.

    Article  CAS  PubMed  Google Scholar 

  47. Rauchs G, Schabus M, Parapatics S, Bertran F, Clochon P, Hot P, et al. Is there a link between sleep changes and memory in Alzheimer’s disease? Neuroreport. 2008;19(11):1159–62. doi:10.1097/WNR.0b013e32830867c4.

    Article  PubMed  PubMed Central  Google Scholar 

  48. Westerberg CE, Mander BA, Florczak SM, Weintraub S, Mesulam MM, Zee PC, et al. Concurrent impairments in sleep and memory in amnestic mild cognitive impairment. J Int Neuropsychol Soc. 2012;18(3):490–500. doi:10.1017/S135561771200001X.

    Article  PubMed  PubMed Central  Google Scholar 

  49. Gorgoni M, Lauri G, Truglia I, Cordone S, Sarasso S, Scarpelli S, et al. Parietal fast sleep spindle density decrease in Alzheimer’s disease and amnesic mild cognitive impairment. Neural Plast. 2016;2016:8376108. doi:10.1155/2016/8376108.

    PubMed  PubMed Central  Google Scholar 

  50. Aarsland D, Kurz MW. The epidemiology of dementia associated with Parkinson disease. J Neurol Sci. 2010;289(1-2):18–22. doi:10.1016/j.jns.2009.08.034.

    Article  PubMed  Google Scholar 

  51. Hely MA, Reid WG, Adena MA, Halliday GM, Morris JG. The Sydney multicenter study of Parkinson’s disease: the inevitability of dementia at 20 years. Mov Disord. 2008;23(6):837–44.

    Article  PubMed  Google Scholar 

  52. Emser W, Brenner M, Stober T, Schimrigk K. Changes in nocturnal sleep in Huntington’s and Parkinson’s disease. J Neurol. 1988;235(3):177–9.

    Article  CAS  PubMed  Google Scholar 

  53. Comella CL, Tanner CM, Ristanovic RK. Polysomnographic sleep measures in Parkinson’s disease patients with treatment-induced hallucinations. Ann Neurol. 1993;34(5):710–4. doi:10.1002/ana.410340514.

    Article  CAS  PubMed  Google Scholar 

  54. Myslobodsky M, Mintz M, Ben-Mayor V, Radwan H. Unilateral dopamine deficit and lateral EEG asymmetry: sleep abnormalities in hemi-Parkinson’s patients. Electroencephalogr Clin Neurophysiol. 1982;54(2):227–31.

    Article  CAS  PubMed  Google Scholar 

  55. Happe S, Anderer P, Pirker W, Klosch G, Gruber G, Saletu B, et al. Sleep microstructure and neurodegeneration as measured by [123I]beta-CIT SPECT in treated patients with Parkinson’s disease. J Neurol. 2004;251(12):1465–71. doi:10.1007/s00415-004-0564-3.

    Article  PubMed  Google Scholar 

  56. Puca FM, Bricolo A, Turella G. Effect of L-dopa or amantadine therapy on sleep spindles in Parkinsonism. Electroencephalogr Clin Neurophysiol. 1973;35(3):327–30.

    Article  CAS  PubMed  Google Scholar 

  57. Christensen JA, Kempfner J, Zoetmulder M, Leonthin HL, Arvastson L, Christensen SR, et al. Decreased sleep spindle density in patients with idiopathic REM sleep behavior disorder and patients with Parkinson’s disease. Clin Neurophysiol. 2014;125(3):512–9. doi:10.1016/j.clinph.2013.08.013.

    Article  PubMed  Google Scholar 

  58. Christensen JA, Nikolic M, Warby SC, Koch H, Zoetmulder M, Frandsen R, et al. Sleep spindle alterations in patients with Parkinson’s disease. Front Hum Neurosci. 2015;9:233. doi:10.3389/fnhum.2015.00233. This study found that Parkinson’s disease patients have a lower sleep spindle density and a longer sleep spindle duration, a higher maximum peak-to-peak amplitude, and a slower oscillation frequency. This study was based on a group consensus of five individual experts’ identification of sleep spindles in N2 sleep. Inter-expert reliability in sleep spindle scoring was lower in scoring definite sleep spindles in patients when compared to controls. This suggested caution in interpretation of results from sleep spindle density analyses, highlighting the need to consider not only the number but also the morphology of sleep spindles when comparing patients and controls. Moreover, authors correctly pointed to the fact that a biomarker does not have to be specific to a disease to have clinical utility, as different information have to be considered in the diagnostic process.

    Article  PubMed  PubMed Central  Google Scholar 

  59. Latreille V, Carrier J, Lafortune M, Postuma RB, Bertrand JA, Panisset M, et al. Sleep spindles in Parkinson’s disease may predict the development of dementia. Neurobiol Aging. 2015;36(2):1083–90. doi:10.1016/j.neurobiolaging.2014.09.009.

    Article  PubMed  Google Scholar 

  60. Aldrich MS, Foster NL, White RF, Bluemlein L, Prokopowicz G. Sleep abnormalities in progressive supranuclear palsy. Ann Neurol. 1989;25(6):577–81. doi:10.1002/ana.410250609.

    Article  CAS  PubMed  Google Scholar 

  61. Gross RA, Spehlmann R, Daniels JC. Sleep disturbances in progressive supranuclear palsy. Electroencephalogr Clin Neurophysiol. 1978;45(1):16–25.

    Article  CAS  PubMed  Google Scholar 

  62. Arnulf I, Merino-Andreu M, Bloch F, Konofal E, Vidailhet M, Cochen V, et al. REM sleep behavior disorder and REM sleep without atonia in patients with progressive supranuclear palsy. Sleep. 2005;28(3):349–54.

    PubMed  Google Scholar 

  63. Autret A, Laffont F, de Toffol B, Cathala HP. A syndrome of REM and non-REM sleep reduction and lateral gaze paresis after medial tegmental pontine stroke. Computed tomographic scans and anatomical correlations in four patients. Arch Neurol. 1988;45(11):1236–42.

    Article  CAS  PubMed  Google Scholar 

  64. Valldeoriola F, Santamaria J, Graus F, Tolosa E. Absence of REM sleep, altered NREM sleep and supranuclear horizontal gaze palsy caused by a lesion of the pontine tegmentum. Sleep. 1993;16(2):184–8.

    CAS  PubMed  Google Scholar 

  65. Gironell A, de la Calzada MD, Sagales T, Barraquer-Bordas L. Absence of REM sleep and altered non-REM sleep caused by a haematoma in the pontine tegmentum. J Neurol Neurosurg Psychiatry. 1995;59(2):195–6.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. Wiegand M, Möller A, Lauer C, Stolz S, Schreiber W, Dose M, et al. Nocturnal sleep in Huntington’s disease. J Neurol. 1991;238(4):203–8.

    Article  CAS  PubMed  Google Scholar 

  67. Cooke PM. Clinical electroencephalography in epilepsy and related conditions in children. JAMA. 1964;187(6):464–5.

    Article  Google Scholar 

  68. Drake Jr ME, Pakalnis A, Padamadan H, Weate SM, Cannon PA. Sleep spindles in epilepsy. Clin Electroencephalogr. 1991;22(3):144–9.

    Article  PubMed  Google Scholar 

  69. Myatchin I, Lagae L. Sleep spindle abnormalities in children with generalized spike-wave discharges. Pediatr Neurol. 2007;36(2):106–11. doi:10.1016/j.pediatrneurol.2006.09.014.

    Article  PubMed  Google Scholar 

  70. Tezer FI, Remi J, Erbil N, Noachtar S, Saygi S. A reduction of sleep spindles heralds seizures in focal epilepsy. Clin Neurophysiol. 2014;125(11):2207–11. doi:10.1016/j.clinph.2014.03.001.

    Article  PubMed  Google Scholar 

  71. Latka M, Kozik A, Jernajczyk J, West BJ, Jernajczyk W. Wavelet mapping of sleep spindles in young patients with epilepsy. J Physiol Pharmacol. 2005;56 Suppl 4:15–20.

    PubMed  Google Scholar 

  72. Bersagliere A, Achermann P, Lo Russo G, Proserpio P, Nobili L. Spindle frequency activity may provide lateralizing information in drug-resistant nocturnal mesial frontal lobe epilepsy: a pilot study on the contribution of sleep recordings. Seizure. 2013;22(9):719–25. doi:10.1016/j.seizure.2013.05.011.

    Article  PubMed  Google Scholar 

  73. Mahowald MW, Schenck CH. REM sleep behaviour disorder: a marker of synucleinopathy. Lancet Neurol. 2013;12(5):417–9. doi:10.1016/S1474-4422(13)70078-4.

    Article  PubMed  Google Scholar 

  74. Braak H, Del Tredici K, Rüb U, de Vos RA, Steur ENJ, Braak E. Staging of brain pathology related to sporadic Parkinson’s disease. Neurobiol Aging. 2003;24(2):197–211.

    Article  PubMed  Google Scholar 

  75. O’Reilly C, Godin I, Montplaisir J, Nielsen T. REM sleep behaviour disorder is associated with lower fast and higher slow sleep spindle densities. J Sleep Res. 2015;24(6):593–601.

    Article  PubMed  Google Scholar 

  76. Espa F, Ondze B, Deglise P, Billiard M, Besset A. Sleep architecture, slow wave activity, and sleep spindles in adult patients with sleepwalking and sleep terrors. Clin Neurophysiol. 2000;111(5):929–39.

    Article  CAS  PubMed  Google Scholar 

  77. Lugaresi E, Medori R, Montagna P, Baruzzi A, Cortelli P, Lugaresi A, et al. Fatal familial insomnia and dysautonomia with selective degeneration of thalamic nuclei. N Engl J Med. 1986;315(16):997–1003. doi:10.1056/NEJM198610163151605.

    Article  CAS  PubMed  Google Scholar 

  78. Sforza E, Montagna P, Tinuper P, Cortelli P, Avoni P, Ferrillo F, et al. Sleep-wake cycle abnormalities in fatal familial insomnia. Evidence of the role of the thalamus in sleep regulation. Electroencephalogr Clin Neurophysiol. 1995;94(6):398–405.

    Article  CAS  PubMed  Google Scholar 

  79. Tinuper P, Montagna P, Medori R, Cortelli P, Zucconi M, Baruzzi A, et al. The thalamus participates in the regulation of the sleep-waking cycle. A clinico-pathological study in fatal familial thalamic degeneration. Electroencephalogr Clin Neurophysiol. 1989;73(2):117–23.

    Article  CAS  PubMed  Google Scholar 

  80. Perani D, Cortelli P, Lucignani G, Montagna P, Tinuper P, Gallassi R, et al. [18F]FDG PET in fatal familial insomnia: the functional effects of thalamic lesions. Neurology. 1993;43(12):2565–9.

    Article  CAS  PubMed  Google Scholar 

  81. Godbout RBC, Stip E, Mottron L. A laboratory study of sleep and dreaming in a case of Asperger’s syndrome. Dreaming. 1998;8:75–88.

    Article  Google Scholar 

  82. Godbout R, Bergeron C, Limoges E, Stip E, Mottron L. A laboratory study of sleep in Asperger’s syndrome. Neurolreport. 2000;11(1):127–30.

    Article  CAS  Google Scholar 

  83. Limoges E, Mottron L, Bolduc C, Berthiaume C, Godbout R. Atypical sleep architecture and the autism phenotype. Brain J Neurol. 2005;128(Pt 5):1049–61. doi:10.1093/brain/awh425.

    Article  Google Scholar 

  84. Tessier S, Lambert A, Chicoine M, Scherzer P, Soulieres I, Godbout R. Intelligence measures and stage 2 sleep in typically-developing and autistic children. Int J Psychophysiol. 2015;97(1):58–65. doi:10.1016/j.ijpsycho.2015.05.003.

    Article  PubMed  Google Scholar 

  85. Tani P, Lindberg N, Nieminen-von Wendt T, von Wendt L, Virkkala J, Appelberg B, et al. Sleep in young adults with Asperger syndrome. Neuropsychobiology. 2004;50(2):147–52. doi:10.1159/000079106.

    Article  PubMed  Google Scholar 

  86. Shibagaki M, Kiyono S, Watanabe K. Spindle evolution in normal and mentally retarded children: a review. Sleep. 1981;5(1):47–57.

    Google Scholar 

  87. Monod N, Ducas P. The prognostic value of the electroencephalogram in the first two years of life. Clinical electroencephalography of children. New York: Grune and Stratton; 1968. p. 61–76.

    Google Scholar 

  88. Shibagaki M, Kiyono S, Watanabe K. Nocturnal sleep in severely mentally retarded children: abnormal EEG patterns in sleep cycle. Electroencephalogr Clin Neurophysiol. 1980;49(3-4):337–44.

    Article  CAS  PubMed  Google Scholar 

  89. Shibagaki M, Kiyono S, Watanabe K, Hakamada S. Concurrent occurrence of rapid eye movement with spindle burst during nocturnal sleep in mentally retarded children. Electroencephalogr Clin Neurophysiol. 1982;53(1):27–35.

    Article  CAS  PubMed  Google Scholar 

  90. Gibbs EL, Rich CL, Fois A, Gibbs F. Electroencephalographic study of mentally retarded persons. Am J Ment Defic. 1960;65:236–47.

    Google Scholar 

  91. Gibbs EL, Gibbs FA. Extreme spindles: correlation of electroencephalographic sleep pattern with mental retardation. Science. 1962;138(3545):1106–7.

    Article  CAS  PubMed  Google Scholar 

  92. Bixler E, Rhodes J, Rhodes J. Spindle activity during sleep in cultural-familial mild retardates. Psychophysiology. 1968;5:212.

    Google Scholar 

  93. Schulte FJ, Kaiser HJ, Engelbart S, Bell EF, Castell R, Lenard HG. Sleep patterns in hyperphenylalaninemia: a lesson on serotonin to be learned from phenylketonuria. Pediatr Res. 1973;7(6):588–99. doi:10.1203/00006450-197306000-00007.

    Article  CAS  PubMed  Google Scholar 

  94. De Giorgis GF, Nonnis E, Crocioni F, Gregori P, Rosini MP, Leuzzi V, et al. Evolution of daytime quiet sleep components in early treated phenylketonuric infants. Brain Dev. 1996;18(3):201–6.

    Article  PubMed  Google Scholar 

  95. Schultz MA, Schulte FJ, Akiyama Y, Parmelee AH. Development of electroencephalographic sleep phenomena in hypothyroid infants. Electroencephalogr Clin Neurophysiol. 1968;25(4):351–8.

    Article  CAS  PubMed  Google Scholar 

  96. Ellingson RJ, Peters JF. Development of EEG and daytime sleep patterns in trisomy-21 infants during the first year of life: longitudinal observations. Electroencephalogr Clin Neurophysiol. 1980;50(5-6):457–66.

    Article  CAS  PubMed  Google Scholar 

  97. Peirano P, Algarin C, Garrido M, Algarin D, Lozoff B. Iron-deficiency anemia is associated with altered characteristics of sleep spindles in NREM sleep in infancy. Neurochem Res. 2007;32(10):1665–72. doi:10.1007/s11064-007-9396-8.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  98. Gurses D, Kilic I, Sahiner T. The effects of hyperbilirubinemia on sleep-spindle characteristics in infants. Sleep. 2005;28(5):644–8.

    PubMed  Google Scholar 

  99. Clinton SM, Meador-Woodruff JH. Thalamic dysfunction in schizophrenia: neurochemical, neuropathological, and in vivo imaging abnormalities. Schizophr Res. 2004;69(2-3):237–53.

    Article  PubMed  Google Scholar 

  100. Janssen J, Aleman-Gomez Y, Reig S, Schnack HG, Parellada M, Graell M, et al. Regional specificity of thalamic volume deficits in male adolescents with early-onset psychosis. Br J Psychiatry J Mental Sci. 2012;200(1):30–6. doi:10.1192/bjp.bp.111.093732.

    Article  Google Scholar 

  101. 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. doi:10.1111/j.1600-0447.2009.01447.x.

    Article  CAS  PubMed  Google Scholar 

  102. Anticevic A, Haut K, Murray JD, Repovs G, Yang GJ, Diehl C, et al. Association of thalamic dysconnectivity and conversion to psychosis in youth and young adults at elevated clinical risk. JAMA Psychiatry. 2015;72(9):882–91. doi:10.1001/jamapsychiatry.2015.0566.

    Article  PubMed  PubMed Central  Google Scholar 

  103. Warby SC, Wendt SL, Welinder P, Munk EG, Carrillo O, Sorensen HB, et al. Sleep-spindle detection: crowdsourcing and evaluating performance of experts, non-experts and automated methods. Nat Methods. 2014;11(4):385–92. This is a very interesting work that evaluated the performance of spindle identification by trained experts, non-experts, and six automated spindle-detection algorithms using a gold standard dataset. Overall, spindle detection performance was highest in individual experts and the non-expert group consensus, followed by all automated detection methods we tested.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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    Authors and Affiliations

    1. Dipartimento di Salute Mentale, Università degli Studi di Milano, Via Antonio di Rudinì 8, 20142, Milan, Italy

      Anna Castelnovo, Armando D’Agostino & Cecilia Casetta

    2. Dipartimento di Scienze Biomediche e Cliniche “L. Sacco”, Università degli Studi di Milano, Via Giovanni Battista Grassi 74, 20157, Milan, Italy

      Simone Sarasso

    3. Department of Psychiatry, University of Pittsburg, 3811 O’Hara St, Pittsburgh, PA, 15213, USA

      Fabio Ferrarelli

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    1. Anna Castelnovo
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    2. Armando D’Agostino
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    3. Cecilia Casetta
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    Correspondence to Anna Castelnovo.

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    This article is part of the Topical Collection on Sleep Disorders

    Anna Castelnovo and Armando D’Agostino contributed equally to this work.

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    Castelnovo, A., D’Agostino, A., Casetta, C. et al. Sleep Spindle Deficit in Schizophrenia: Contextualization of Recent Findings. Curr Psychiatry Rep 18, 72 (2016). https://doi.org/10.1007/s11920-016-0713-2

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