Sleep spindle deficits in antipsychotic-naïve early course schizophrenia and in non-psychotic first-degree relatives

Frontiers in Human Neuroscience

Volumn 8, Issue OCT, 2014, Pages

  Manoach, Dara S ^a,b   Demanuele, Charmaine ^a,b   Wamsley, Erin J ^b,c,e   Montrose, Debra M ^d   Miewald, Jean ^d   Kupfer, David ^d   Buysse, Daniel ^d   Stickgold, Robert ^b,c   Keshavan, Matcheri S ^b,c,d  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c BETH ISRAEL DEACONESS MEDICAL CENTER   (United States)

^d UNIVERSITY OF PITTSBURGH   (United States)

^e FURMAN UNIVERSITY   (United States)

Author keywords

Cognition; Endophenotype; IQ; Polysomnography; Relatives; Schizophrenia; Sleep; Sleep spindles

Indexed keywords

ADULT; ARTICLE; CLINICAL ARTICLE; COGNITION; CONTROLLED STUDY; EXECUTIVE FUNCTION; FEMALE; FIRST DEGREE RELATIVE; HUMAN; INTELLIGENCE QUOTIENT; MALE; POSITIVE SYNDROME; PSYCHOSIS; SCHIZOPHRENIA; SLEEP DISORDER; SLEEP QUALITY; SLEEP SPINDLE; SLEEP STAGE;

EID: 84933677797     PISSN: None     EISSN: 16625161     Source Type: Journal    
DOI: 10.3389/fnhum.2014.00762     Document Type: Article

References (82)

1. Ambrosius, U., Lietzenmaier, S., Wehrle, R., Wichniak, A., Kalus, S., Winkelmann, J., et al. (2008). Heritability of sleep electroencephalogram. Biol. Psychiatry 64, 344-348. doi: 10.1016/j.biopsych.2008.03.002
2. American Psychiatric Association. (2000). Diagnostic and Statistical Manual of Mental Disorders, (4th Edn., text revision). Washington, DC: Author.
3. Andersen, R. (2008). Modern Methods for Robust Regression. Series on Quantitative Applications in the Social Sciences. Thousand Oaks, CA: SAGE Publications, 7-152.
4. Andreasen, N. C. (1983). Scale for the Assessment of Negative Symptoms (SANS). Iowa City, IA: University of Iowa.
5. Andreasen, N. C. (1990). Methods for assessing positive and negative symptoms. Mod. Probl. Pharmacopsychiatry24, 73-88.
6. Benca, R. M. (1996). Sleep in psychiatric disorders. Neurol. Clin. 14, 739-764. doi: 10.1016/S0733-8619(05)70283-8
7. Benson, K. L. (2006). Sleep in schizophrenia: impairments, correlates, and treatment. Psychiatr. Clin. North Am. 29, 1033-1045; abstract: ix-x. doi: 10.1016/j.psc.2006.08.002
8. Berg, E. A. (1948). A simple objective technique for measuring flexibility in thinking. J. Gen. Psychol. 39, 15-22. doi: 10.1080/00221309.1948.9918159
9. Breslau, N., Roth, T., Rosenthal, L., and Andreski, P. (1996). Sleep disturbance and psychiatric disorders: a longitudinal epidemiological study of young adults. Biol. Psychiatry 39, 411-418. doi: 10.1016/0006-3223(95)00188-3
10. Buzsaki, G. (1998). Memory consolidation during sleep: a neurophysiological perspective. J. Sleep Res. 7(Suppl. 1), 17-23. doi: 10.1046/j.1365-2869.7.s1.3.x
11. Cannon-Spoor, H. E., Potkin, S. G., and Wyatt, R. J. (1982). Measurement of premorbid adjustment in chronic schizophrenia. Schizophr. Bull. 8, 470-484. doi: 10.1093/schbul/8.3.470
12. Chapman, L. J., Chapman, J. P., and Raulin, M. L. (1978). Body-image aberration in Schizophrenia. J. Abnorm. Psychol. 87, 399-407. doi: 10.1037/0021-843X.87.4.399
13. Chouinard, S., Poulin, J., Stip, E., and Godbout, R. (2004). Sleep in untreated patients with schizophrenia: a meta-analysis. Schizophr. Bull. 30, 957-967. doi: 10.1093/oxfordjournals.schbul.a007145
14. Clemens, Z., Fabo, D., and Halasz, P. (2005). Overnight verbal memory retention correlates with the number of sleep spindles. Neuroscience 132, 529-535. doi: 10.1016/j.neuroscience.2005.01.011
15. Clemens, Z., Fabo, D., and Halasz, P. (2006). Twenty-four hours retention of visuospatial memory correlates with the number of parietal sleep spindles. Neurosci. Lett. 403, 52-56. doi: 10.1016/j.neulet.2006.04.035
16. Cornblatt, B. A., Risch, N. J., Faris, G., Friedman, D., and Erlenmeyer-Kimling, L. (1988). The Continuous Performance Test, identical pairs version (CPT-IP): I. New findings about sustained attention in normal families. Psychiatry Res. 26, 223-238. doi: 10.1016/0165-1781(88)90076-5
17. De Gennaro, L., Marzano, C., Fratello, F., Moroni, F., Pellicciari, M. C., Ferlazzo, F., et al. (2008). The electroencephalographic fingerprint of sleep is genetically determined: a twin study. Ann. Neurol. 64, 455-460. doi: 10.1002/ana.21434
18. Delis, D. C., Freeland, J., Kramer, J. H., and Kaplan, E. (1988). Integrating clinical assessment with cognitive neuroscience: construct validation of the California Verbal Learning Test. J. Consult. Clin. Psychol. 56, 123-130. doi: 10.1037/0022-006X.56.1.123
19. Demjaha, A., Egerton, A., Murray, R. M., Kapur, S., Howes, O. D., Stone, J. M., et al. (2014). Antipsychotic treatment resistance in schizophrenia associated with elevated glutamate levels but normal dopamine function. Biol. Psychiatry 75, e11-e13. doi: 10.1016/j.biopsych.2013.06.011
20. Dencker, S. J., Malm, U., and Lepp, M. (1986). Schizophrenic relapse after drug withdrawal is predictable. Acta Psychiatr. Scand. 73, 181-185. doi: 10.1111/j.1600-0447.1986.tb10584.x
21. Eckblad, M., and Chapman, L. J. (1983). Magical ideation as an indicator of schizotypy. J. Consult. Clin. Psychol. 51, 215-225. doi: 10.1037/0022-006X.51.2.215
22. Ferrarelli, F., Huber, R., Peterson, M. J., Massimini, M., Murphy, M., Riedner, B. A., et al. (2007). Reduced sleep spindle activity in schizophrenia patients. Am. J. Psychiatry 164, 483-492. doi: 10.1176/appi.ajp.164.3.483
23. Ferrarelli, F., Peterson, M. J., Sarasso, S., Riedner, B. A., Murphy, M. J., Benca, R. M., et al. (2010). Thalamic dysfunction in schizophrenia suggested by whole-night deficits in slow and fast spindles. Am. J. Psychiatry 167, 1339-1348. doi: 10.1176/appi.ajp.2010.09121731
24. First, M. B., Spitzer, R. L., Gibbon, M., and Williams, J. B. W. (1997). Structured Clinical Interview for DSM-IV Axis I Disorders, Research Version, Patient Edition with Psychotic Screen (SCID-I/P W/PSY SCREEN). New York, NY: Biometrics Research, New York State Psychiatric Institute.
25. First, M. B., Spitzer, R. L., Gibbon, M., and Williams, J. B. W. (2002). Structured Clinical Interview for DSM-IV-TR Axis I Disorders, Research Version, Nonpatient Edition. New York, NY: Biometrics Research, New York State Psychiatric Institute.
26. Fogel, S. M., and Smith, C. T. (2006). Learning-dependent changes in sleep spindles and Stage 2 sleep. J. Sleep Res. 15, 250-255. doi: 10.1111/j.1365-2869.2006.00522.x
27. Fogel, S. M., and Smith, C. T. (2011). The function of the sleep spindle: a physiological index of intelligence and a mechanism for sleep-dependent memory consolidation. Neurosci. Biobehav. Rev. 35, 1154-1165. doi: 10.1016/j.neubiorev.2010.12.003
28. Ford, D. E., and Kamerow, D. B. (1989). Epidemiologic study of sleep disturbances and psychiatric disorders. An opportunity for prevention? JAMA 262, 1479-1484. doi: 10.1001/jama.1989.03430110069030
29. Forest, G., Poulin, J., Daoust, A. M., Lussier, I., Stip, E., and Godbout, R. (2007). Attention and non-REM sleep in neuroleptic-naive persons with schizophrenia and control participants. Psychiatry Res. 149, 33-40. doi: 10.1016/j.psychres.2005.11.005
30. Germain, A., Buysse, D. J., and Nofzinger, E. (2008). Sleep-specific mechanisms underlying posttraumatic stress disorder: integrative review and neurobiological hypotheses. Sleep Med. Rev. 12, 185-195. doi: 10.1016/j.smrv.2007.09.003
31. Gilbert, A. R., Rosenberg, D. R., Harenski, K., Spencer, S., Sweeney, J. A., and Keshavan, M. S. (2001). Thalamic volumes in patients with first-episode schizophrenia. Am. J. Psychiatry 158, 618-624. doi: 10.1176/appi.ajp.158.4.618
32. Goder, R., Fritzer, G., Gottwald, B., Lippmann, B., Seeck-Hirschner, M., Serafin, I., et al. (2008). Effects of olanzapine on slow wave sleep, sleep spindles and sleep-related memory consolidation in schizophrenia. Pharmacopsychiatry 41, 92-99. doi: 10.1055/s-2007-1004592
33. Gottesman, I. I., and Gould, T. D. (2003). The endophenotype concept in psychiatry: etymology and strategic intentions. Am. J. Psychiatry 160, 636-645. doi: 10.1176/appi.ajp.160.4.636
34. Guillery, R. W., and Harting, J. K. (2003). Structure and connections of the thalamic reticular nucleus: advancing views over half a century. J. Comp. Neurol. 463, 360-371. doi: 10.1002/cne.10738
35. Hiatt, J. F., Floyd, T. C., Katz, P. H., and Feinberg, I. (1985). Further evidence of abnormal non-rapid-eye-movement sleep in schizophrenia. Arch. Gen. Psychiatry 42, 797-802. doi: 10.1001/archpsyc.1985.01790310059007
36. Hollingshead, A. B. (1965). Two Factor Index of Social Position. New Haven, CT: Yale University Press.
37. Houser, C. R., Vaughn, J. E., Barber, R. P., and Roberts, E. (1980). GABA neurons are the major cell type of the nucleus reticularis thalami. Brain Res. 200, 341-354. doi: 10.1016/0006-8993(80)90925-7
38. Huang, Y. S., Guilleminault, C., Li, H. Y., Yang, C. M., Wu, Y. Y., and Chen, N. H. (2007). Attention-deficit/hyperactivity disorder with obstructive sleep apnea: a treatment outcome study. Sleep Med. 8, 18-30. doi: 10.1016/j.sleep.2006.05.016
39. Ibrahim, H. M., Hogg, A. J. Jr., Healy, D. J., Haroutunian, V., Davis, K. L., and Meador-Woodruff, J. H. (2000). Ionotropic glutamate receptor binding and subunit mRNA expression in thalamic nuclei in schizophrenia. Am. J. Psychiatry 157, 1811-1823. doi: 10.1176/appi.ajp.157.11.1811
40. Jacobsen, R. B., Ulrich, D., and Huguenard, J. R. (2001). GABA(B) and NMDA receptors contribute to spindle-like oscillations in rat thalamus in vitro. J. Neurophysiol. 86, 1365-1375.
41. Jastak, S., and Wilkinson, G. (1984). The Wide Range Acheivement Test-Revised: Administration Manual. Wilmington, DE: Jastak Associates.
42. Jia, F., Goldstein, P. A., and Harrison, N. L. (2009). The modulation of synaptic GABA(A) receptors in the thalamus by eszopiclone and zolpidem. J. Pharmacol. Exp. Ther. 328, 1000-1006. doi: 10.1124/jpet.108.146084
43. Kahn-Greene, E. T., Killgore, D. B., Kamimori, G. H., Balkin, T. J., and Killgore, W. D. (2007). The effects of sleep deprivation on symptoms of psychopathology in healthy adults. Sleep Med. 8, 215-221. doi: 10.1016/j.sleep.2006.08.007
44. Keshavan, M. S. (1999). Development, disease and degeneration in schizophrenia: a unitary pathophysiological model. J. Psychiatr. Res. 33, 513-521. doi: 10.1016/S0022-3956(99)00033-3
45. Keshavan, M. S., Diwadkar, V. A., Montrose, D. M., Stanley, J. A., and Pettegrew, J. W. (2004). Premorbid characterization in schizophrenia: the Pittsburgh High Risk Study. World Psychiatry 3, 163-168.
46. Keshavan, M. S., Montrose, D. M., Miewald, J. M., and Jindal, R. D. (2011). Sleep correlates of cognition in early course psychotic disorders. Schizophr. Res. 131, 231-234. doi: 10.1016/j.schres.2011.05.027
47. Kraepelin, E. (1919). Dementia Praecox and Paraphrenia. Edinburgh: E.S. Livingston.
48. Lieberman, J. A., Stroup, T. S., McEvoy, J. P., Swartz, M. S., Rosenheck, R. A., Perkins, D. O., et al. (2005). Effectiveness of antipsychotic drugs in patients with chronic schizophrenia. N. Engl. J. Med. 353, 1209-1223. doi: 10.1056/NEJMoa051688
49. Lunsford-Avery, J. R., Orr, J. M., Gupta, T., Pelletier-Baldelli, A., Dean, D. J., Smith Watts, A. K., et al. (2013). Sleep dysfunction and thalamic abnormalities in adolescents at ultra high-risk for psychosis. Schizophr. Res. 151, 148-153. doi: 10.1016/j.schres.2013.09.015
50. Manoach, D. S., Thakkar, K. N., Stroynowski, E., Ely, A., McKinley, S. K., Wamsley, E., et al. (2010). Reduced overnight consolidation of procedural learning in chronic medicated schizophrenia is related to specific sleep stages. J. Psychiatr. Res. 44, 112-120. doi: 10.1016/j.jpsychires.2009.06.011
51. Miller, T. J., Zipursky, R. B., Perkins, D., Addington, J., Woods, S. W., Hawkins, K. A., et al. (2003). 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. 61, 19-30. doi: 10.1016/S0920-9964(02)00440-1
52. Mishlove, M., and Chapman, L. J. (1985). Social anhedonia in the prediction of psychosis proneness. J. Abnorm. Psychol. 94, 384-396. doi: 10.1037/0021-843X.94.3.384
53. Molle, M., and Born, J. (2011). Slow oscillations orchestrating fast oscillations and memory consolidation. Prog. Brain Res. 193, 93-110. doi: 10.1016/B978-0-444-53839-0.00007-7
54. Nishida, M., and Walker, M. P. (2007). Daytime naps, motor memory consolidation and regionally specific sleep spindles. PLoS ONE 2:e341. doi: 10.1371/journal.pone.0000341
55. O'Neill, J., Pleydell-Bouverie, B., Dupret, D., and Csicsvari, J. (2010). Play it again: reactivation of waking experience and memory. Trends Neurosci. 33, 220-229. doi: 10.1016/j.tins.2010.01.006
56. Orvaschel, H., and Puig-Antich, J. (1987). Schedule for Affective Disorders and Schizophrenia for School-Age Children: Epidemiologic 4th version. Ft. Lauderdale, FL: Nova University, Center for Psychological Study.
57. Otto, W., and McMenemy, R. A. (1965). An appraisal of the ammons quick test in a remedial reading program. J. Educ. Meas. 2, 193-198. doi: 10.1111/j.1745-3984.1965.tb00415.x
58. Peters, K. R., Ray, L., Smith, V., and Smith, C. (2008). Changes in the density of stage 2 sleep spindles following motor learning in young and older adults. J. Sleep Res. 17, 23-33. doi: 10.1111/j.1365-2869.2008.00634.x
59. Poulin, J., Daoust, A. M., Forest, G., Stip, E., and Godbout, R. (2003). Sleep architecture and its clinical correlates in first episode and neuroleptic-naive patients with schizophrenia. Schizophr. Res. 62, 147-153. doi: 10.1016/S0920-9964(02)00346-8
60. Rasch, B., Pommer, J., Diekelmann, S., and Born, J. (2008). Pharmacological REM sleep suppression paradoxically improves rather than impairs skill memory. Nat. Neurosci. 12, 396-397.
61. Rechtschaffen, A., and Kales, A. (1968). A Manual Standardized Terminology, Techniques and Scoring System for Sleep Stages of Human Subjects. Bethesda, MD: National Institute of Neurological Diseases and Blindness, Neurological Information Network.
62. Reitan, R. M. (1958). Validity of the Trail Making Test as an indication of organic brain damage. Percept. Mot. Skills8, 251-276. doi: 10.2466/pms.1958.8.3.271
63. Rosanova, M., and Ulrich, D. (2005). Pattern-specific associative long-term potentiation induced by a sleep spindle-related spike train. J. Neurosci. 25, 9398-9405. doi: 10.1523/JNEUROSCI.2149-05.2005
64. Sateia, M. J. (2009). Update on sleep and psychiatric disorders. Chest 135, 1370-1379. doi: 10.1378/chest.08-1834
65. Schabus, M., Hoedlmoser, K., Pecherstorfer, T., Anderer, P., Gruber, G., Parapatics, S., et al. (2008). Interindividual sleep spindle differences and their relation to learning-related enhancements. Brain Res. 1191, 127-135. doi: 10.1016/j.brainres.2007.10.106
66. Seeck-Hirschner, M., Baier, P. C., Sever, S., Buschbacher, A., Aldenhoff, J. B., and Goder, R. (2011). Effects of daytime naps on procedural and declarative memory in patients with schizophrenia. J. Psychiatr. Res. 44, 42-47. doi: 10.1016/j.jpsychires.2009.05.008
67. Smith, R. E., Haroutunian, V., Davis, K. L., and Meador-Woodruff, J. H. (2001). Expression of excitatory amino acid transporter transcripts in the thalamus of subjects with schizophrenia. Am. J. Psychiatry 158, 1393-1399. doi: 10.1176/appi.ajp.158.9.1393
68. Tamaki, M., Matsuoka, T., Nittono, H., and Hori, T. (2008). Fast sleep spindle (13-15 hz) activity correlates with sleep-dependent improvement in visuomotor performance. Sleep 31, 204-211.
69. Thompson, M., Weickert, C. S., Wyatt, E., and Webster, M. J. (2009). Decreased glutamic acid decarboxylase(67) mRNA expression in multiple brain areas of patients with schizophrenia and mood disorders. J. Psychiatr. Res. 43, 970-977. doi: 10.1016/j.jpsychires.2009.02.005
70. Turek, F. W. (2005). Insomnia and depression: if it looks and walks like a duck. Sleep 28, 1362-1363.
71. Turkheimer, E., Haley, A., Waldron, M., D'Onofrio, B., and Gottesman, I. I. (2003). Socioeconomic status modifies heritability of IQ in young children. Psychol. Sci. 14, 623-628. doi: 10.1046/j.0956-7976.2003.psci_1475.x
72. Tyler, D. B. (1955). Psychological changes during experimental sleep deprivation. Dis. Nerv. Syst. 16, 293-299.
73. Van Cauter, E., Linkowski, P., Kerkhofs, M., Hubain, P., L'Hermite-Baleriaux, M., Leclercq, R., et al. (1991). Circadian and sleep-related endocrine rhythms in schizophrenia. Arch. Gen. Psychiatry 48, 348-356.
74. Van Dongen, H. P., Maislin, G., Mullington, J. M., and Dinges, D. F. (2003). The cumulative cost of additional wakefulness: dose-response effects on neurobehavioral functions and sleep physiology from chronic sleep restriction and total sleep deprivation. Sleep 26, 117-126.
75. Walker, M. P., Brakefield, T., Morgan, A., Hobson, J. A., and Stickgold, R. (2002). Practice with sleep makes perfect: sleep-dependent motor skill learning. Neuron 35, 205-211. doi: 10.1016/S0896-6273(02)00746-8
76. Wamsley, E. J., Shinn, A. K., Tucker, M. A., Ono, K. E., McKinley, S. K., Ely, A. V., et al. (2013). The effects of eszopiclone on sleep spindles and memory consolidation in schizophrenia: a randomized placebo-controlled trial. Sleep 36, 1369-1376. doi: 10.5665/sleep.2968
77. Wamsley, E., Tucker, M. A., Shinn, A. K., Ono, K. E., McKinley, S., Ely, A. V., et al. (2012). Reduced sleep spindles and spindle coherence in schizophrenia: mechanisms of impaired memory consolidation? Biol. Psychiatry 71, 154-161. doi: 10.1016/j.biopsych.2011.08.008
78. Warby, S. C., Wendt, S. L., Welinder, P., Munk, E. G., Carrillo, O., Sorensen, H. B., et al. (2014). Sleep-spindle detection: crowdsourcing and evaluating performance of experts, non-experts and automated methods. Nat. Methods 11, 385-392. doi: 10.1038/nmeth.2855
79. Wechsler, D. (1981). The Wechsler Adult Intelligence Scale-Revised. New York, NY: Psychological Corporation.
80. Wehr, T. A., Sack, D. A., and Rosenthal, N. E. (1987). Sleep reduction as a final common pathway in the genesis of mania. Am. J. Psychiatry 144, 201-204.
81. Werk, C. M., Harbour, V. L., and Chapman, C. A. (2005). Induction of long-term potentiation leads to increased reliability of evoked neocortical spindles in vivo. Neuroscience 131, 793-800. doi: 10.1016/j.neuroscience.2004.12.020
82. Wright, J. B. (1993). Mania following sleep deprivation. Br. J. Psychiatry 163, 679-680. doi: 10.1192/bjp.163.5.679