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Associations between cognitive performance and sigma power during sleep in children with attention-deficit/hyperactivity disorder, healthy children, and healthy adults


Autoři: Arnika Bestmann aff001;  Annette Conzelmann aff002;  Lioba Baving aff001;  Alexander Prehn-Kristensen aff001
Působiště autorů: Department of Child and Adolescent Psychiatry and Psychotherapy, Centre for Integrative Psychiatry, University Hospital Schleswig-Holstein, Kiel, Germany aff001;  Department of Child and Adolescent Psychiatry, Psychosomatics and Psychotherapy, University of Tübingen, Tübingen, Germany aff002;  PFH—Private University of Applied Sciences, Department of Psychology (Clinical Psychology II), Göttingen, Germany aff003
Vyšlo v časopise: PLoS ONE 14(10)
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pone.0224166

Souhrn

Sigma power during sleep is associated with cognitive abilities in healthy humans. We examined the relationship between sigma power in sleep EEG and intelligence and alertness in schoolchildren with ADHD (n = 17) in comparison to mentally healthy children (n = 16) and adults (n = 23). We observed a positive correlation between sigma power in sleep stage 2 and IQ in healthy adults but a negative correlation in children with ADHD. Furthermore, children with ADHD showed slower reaction times in alertness testing than both control groups. In contrast, only healthy children displayed a positive correlation between sigma power and reaction times. These data suggest that the associations between sigma power and cognitive performance underlie distinct developmental processes. A negative association between IQ and sigma power indicates a disturbed function of sleep in cognitive functions in ADHD, whereas the function of sleep appears to be matured early in case of motor-related alertness performance.

Klíčová slova:

Children – Child health – Cognition – Electroencephalography – Sleep disorders – ADHD – Reaction time – Sleep


Zdroje

1. Killgore WD. Effects of sleep deprivation on cognition. Prog Brain Res. 2010;185:105–29. Epub 2010/11/16. doi: 10.1016/B978-0-444-53702-7.00007-5 21075236.

2. Lim J, Dinges DF. A meta-analysis of the impact of short-term sleep deprivation on cognitive variables. Psychol Bull. 2010;136(3):375–89. Epub 2010/05/05. doi: 10.1037/a0018883 20438143; PubMed Central PMCID: PMC3290659.

3. Dewald JF, Meijer AM, Oort FJ, Kerkhof GA, Bogels SM. The influence of sleep quality, sleep duration and sleepiness on school performance in children and adolescents: A meta-analytic review. Sleep Med Rev. 2010;14(3):179–89. Epub 2010/01/23. doi: 10.1016/j.smrv.2009.10.004 20093054.

4. de Bruin EJ, van Run C, Staaks J, Meijer AM. Effects of sleep manipulation on cognitive functioning of adolescents: A systematic review. Sleep Med Rev. 2017;32:45–57. Epub 2016/04/04. doi: 10.1016/j.smrv.2016.02.006 27039223.

5. Borbely AA, Achermann P. Sleep homeostasis and models of sleep regulation. J Biol Rhythms. 1999;14(6):557–68. Epub 2000/01/22. 10643753.

6. Fogel SM, Nader R, Cote KA, Smith CT. Sleep spindles and learning potential. Behav Neurosci. 2007;121(1):1–10. Epub 2007/02/28. doi: 10.1037/0735-7044.121.1.1 17324046.

7. Bodizs R, Gombos F, Ujma PP, Kovacs I. Sleep spindling and fluid intelligence across adolescent development: sex matters. Front Hum Neurosci. 2014;8:952. Epub 2014/12/17. doi: 10.3389/fnhum.2014.00952 25506322; PubMed Central PMCID: PMC4246682.

8. Lustenberger C, Maric A, Durr R, Achermann P, Huber R. Triangular relationship between sleep spindle activity, general cognitive ability and the efficiency of declarative learning. PLoS One. 2012;7(11):e49561. Epub 2012/11/28. doi: 10.1371/journal.pone.0049561 23185361; PubMed Central PMCID: PMC3504114.

9. Ohayon MM, Carskadon MA, Guilleminault C, Vitiello MV. Meta-Analysis of Quantitative Sleep Parameters From Childhood to Old Age in Healthy Individuals: Developing Normative Sleep Values Across the Human Lifespan. Sleep. 2004;27(7):1255–73. doi: 10.1093/sleep/27.7.1255 15586779

10. Baker FC, Willoughby AR, de Zambotti M, Franzen PL, Prouty D, Javitz H, et al. Age-Related Differences in Sleep Architecture and Electroencephalogram in Adolescents in the National Consortium on Alcohol and Neurodevelopment in Adolescence Sample. Sleep. 2016;39(7):1429–39. Epub 2016/06/03. doi: 10.5665/sleep.5978 27253763; PubMed Central PMCID: PMC4909625.

11. Scholle S, Zwacka G, Scholle HC. Sleep spindle evolution from infancy to adolescence. Clin Neurophysiol. 2007;118(7):1525–31. doi: 10.1016/j.clinph.2007.03.007 17475551.

12. Colrain IM, Baker FC. Changes in sleep as a function of adolescent development. Neuropsychol Rev. 2011;21(1):5–21. Epub 2011/01/13. doi: 10.1007/s11065-010-9155-5 21225346.

13. Kurth S, Ringli M, Geiger A, LeBourgeois M, Jenni OG, Huber R. Mapping of cortical activity in the first two decades of life: a high-density sleep electroencephalogram study. J Neurosci. 2010;30(40):13211–9. Epub 2010/10/12. 30/40/13211 [pii] doi: 10.1523/JNEUROSCI.2532-10.2010 20926647; PubMed Central PMCID: PMC3010358.

14. Hoedlmoser K, Heib DP, Roell J, Peigneux P, Sadeh A, Gruber G, et al. Slow sleep spindle activity, declarative memory, and general cognitive abilities in children. Sleep. 2014;37(9):1501–12. Epub 2014/08/22. doi: 10.5665/sleep.4000 25142558; PubMed Central PMCID: PMC4153050.

15. Tarokh L, Carskadon MA, Achermann P. Early adolescent cognitive gains are marked by increased sleep EEG coherence. PLoS One. 2014;9(9):e106847. Epub 2014/09/11. doi: 10.1371/journal.pone.0106847 25208326; PubMed Central PMCID: PMC4160237.

16. Gruber R, Wise MS. Sleep Spindle Characteristics in Children with Neurodevelopmental Disorders and Their Relation to Cognition. Neural Plast. 2016;2016:4724792. Epub 2016/08/02. doi: 10.1155/2016/4724792 27478646; PubMed Central PMCID: PMC4958463.

17. Reynolds CM, Short MA, Gradisar M. Sleep spindles and cognitive performance across adolescence: A meta-analytic review. J Adolesc. 2018;66:55–70. Epub 2018/05/22. doi: 10.1016/j.adolescence.2018.04.003 29783103.

18. Hahn M, Joechner AK, Roell J, Schabus M, Heib DP, Gruber G, et al. Developmental changes of sleep spindles and their impact on sleep-dependent memory consolidation and general cognitive abilities: A longitudinal approach. Dev Sci. 2019;22(1):e12706. Epub 2018/09/27. doi: 10.1111/desc.12706 30252185; PubMed Central PMCID: PMC6492121.

19. American Psychiatric Association. The Diagnostic and Statistical Manual of Mental Disorders, 5th ed. Washington, DC: American Psychiatric Association 2013.

20. Polanczyk GV, Salum GA, Sugaya LS, Caye A, Rohde LA. Annual research review: A meta-analysis of the worldwide prevalence of mental disorders in children and adolescents. J Child Psychol Psychiatry. 2015;56(3):345–65. Epub 2015/02/05. doi: 10.1111/jcpp.12381 25649325.

21. Beaussart ML, Barbarot S, Mauger C, Roy A. Systematic Review and Meta-analysis of Executive Functions in Preschool and School-Age Children With Neurofibromatosis Type 1. J Int Neuropsychol Soc. 2018;24(9):977–94. Epub 2018/10/31. doi: 10.1017/S1355617718000383 30375317

22. Lecendreux M, Konofal E, Bouvard M, Falissard B, Mouren-Simeoni MC. Sleep and alertness in children with ADHD. J Child Psychol Psychiatry. 2000;41(6):803–12. 11039692.

23. Tucha L, Tucha O, Walitza S, Sontag TA, Laufkotter R, Linder M, et al. Vigilance and sustained attention in children and adults with ADHD. J Atten Disord. 2009;12(5):410–21. Epub 2008/04/11. doi: 10.1177/1087054708315065 18400983.

24. Frazier TW, Demaree HA, Youngstrom EA. Meta-analysis of intellectual and neuropsychological test performance in attention-deficit/hyperactivity disorder. Neuropsychology. 2004;18(3):543–55. Epub 2004/08/05. doi: 10.1037/0894-4105.18.3.543 15291732.

25. Corkum P, Tannock R, Moldofsky H. Sleep disturbances in children with attention-deficit/hyperactivity disorder. J Am Acad Child Adolesc Psychiatry. 1998;37(6):637–46. Epub 1998/06/17. doi: 10.1097/00004583-199806000-00014 9628084.

26. Owens JA. A clinical overview of sleep and attention-deficit/hyperactivity disorder in children and adolescents. J Can Acad Child Adolesc Psychiatry. 2009;18(2):92–102. 19495429.

27. Cortese S, Faraone SV, Konofal E, Lecendreux M. Sleep in children with attention-deficit/hyperactivity disorder: meta-analysis of subjective and objective studies. J Am Acad Child Adolesc Psychiatry. 2009;48(9):894–908. Epub 2009/07/25. doi: 10.1097/CHI.0b013e3181ac09c9 19625983.

28. Cortese S, Kelly C, Chabernaud C, Proal E, Di Martino A, Milham MP, et al. Toward systems neuroscience of ADHD: a meta-analysis of 55 fMRI studies. AJ Psychiatry. 2012;169(10):1038–55. Epub 2012/09/18. doi: 10.1176/appi.ajp.2012.11101521 22983386; PubMed Central PMCID: PMC3879048.

29. Diaz-Roman A, Hita-Yanez E, Buela-Casal G. Sleep Characteristics in Children with Attention Deficit Hyperactivity Disorder: Systematic Review and Meta-Analyses. Journal of clinical sleep medicine: JCSM: official publication of the American Academy of Sleep Medicine. 2016;12(5):747–56. Epub 2016/03/10. doi: 10.5664/jcsm.5810 26951416; PubMed Central PMCID: PMC4865562.

30. Kirov R, Brand S. Sleep problems and their effect in ADHD. Expert Rev Neurother. 2014;14(3):287–99. Epub 2014/02/05. doi: 10.1586/14737175.2014.885382 24491141.

31. Saletin JM, Coon WG, Carskadon MA. Stage 2 Sleep EEG Sigma Activity and Motor Learning in Childhood ADHD: A Pilot Study. J Clin Child Adolesc Psychol. 2017;46(2):188–97. Epub 2016/06/09. doi: 10.1080/15374416.2016.1157756 27267670; PubMed Central PMCID: PMC5802965.

32. De Dea F, Zanus C, Carrozzi M, Stecca M, Accardo A. Characteristics of EEG power spectrum during sleep spindle events in ADHD children. Conference proceedings: Annual International Conference of the IEEE Engineering in Medicine and Biology Society IEEE Engineering in Medicine and Biology Society Annual Conference. 2018;2018:1456–9. Epub 2018/11/18. doi: 10.1109/embc.2018.8512486 30440667.

33. Prehn-Kristensen A, Goder R, Fischer J, Wilhelm I, Seeck-Hirschner M, Aldenhoff J, et al. Reduced sleep-associated consolidation of declarative memory in attention-deficit/hyperactivity disorder. Sleep Med. 2011;12(7):672–9. Epub 2011/06/24. doi: 10.1016/j.sleep.2010.10.010 21697007.

34. Prehn-Kristensen A, Munz M, Molzow I, Wilhelm I, Wiesner CD, Baving L. Sleep promotes consolidation of emotional memory in healthy children but not in children with attention-deficit hyperactivity disorder. PLoS One. 2013;8(5):e65098. Epub 2013/06/05. doi: 10.1371/journal.pone.0065098 23734235; PubMed Central PMCID: PMC3667133.

35. American Psychiatric Association. Diagnostic and Statistical Manual of Mental disorders, 4th ed. (Text revision): DSM IV-TR. Washington, DC: American Psychiatric Association; 2000.

36. Kaufman J, Birmaher B, Brent D, Rao U, Flynn C, Moreci P, et al. Schedule for affective disorders and schizophrenia for school-age children—Present and lifetime version (K-SADS-PL): Initial reliability and validity data. J Am Acad Child Adolesc Psychiatry. 1997;36:980–8. doi: 10.1097/00004583-199707000-00021 9204677

37. Delmo C, Weiffenbach O, Gabriel M, Bölte S, Marchio E, Poustka F. Kiddie-SADS-present and lifetime version (K-SADS-PL), 3rd edn. 3rd ed. Frankfurt, Germany: Clinic of Child and Adolescent Psychiatry; 2000.

38. Wittchen H-U, Zaudig M, Fydrich T. SKID Strukturiertes Klinisches Interview für DSM-IV. Achse I und II. Göttingen: Hogrefe; 1997.

39. Hardt J, Egle UT, Kappis B, Hessel A, Brahler E. [Symptom Checklist SCL-27]. Psychother Psychosom Med Psychol. 2004;54(5):214–23. Epub 2004/04/24. doi: 10.1055/s-2003-814786 15106055.

40. Rösler M, Retz-Junginger P, Retz W, Stieglitz RD. Homburger ADHS-Skalen für Erwachsene—HASE. Göttingen: Hogrefe; 2008.

41. Retz-Junginger P, Retz W, Blocher D, Weijers HG, Trott GE, Wender PH, et al. [Wender Utah rating scale. The short-version for the assessment of the attention-deficit hyperactivity disorder in adults]. Nervenarzt. 2002;73(9):830–8. Epub 2002/09/07. doi: 10.1007/s00115-001-1215-x 12215873.

42. Buysse DJ, Reynolds CF 3rd, Monk TH, Berman SR, Kupfer DJ. The Pittsburgh Sleep Quality Index: a new instrument for psychiatric practice and research. Psychiatry Res. 1989;28(2):193–213. Epub 1989/05/01. 0165-1781(89)90047-4 [pii]. doi: 10.1016/0165-1781(89)90047-4 2748771.

43. Prehn-Kristensen A, Göder R, Chirobeja S, Bressmann I, Ferstl R, Baving L. Sleep in children enhances preferentially emotional declarative but not procedural memories. J Exp Child Psychol. 2009;104(1):132–9. doi: 10.1016/j.jecp.2009.01.005 19251274.

44. Prehn-Kristensen A, Molzow I, Munz M, Wilhelm I, Müller K, Freytag D, et al. Sleep restores daytime deficits in procedural memory in children with attention-deficit/hyperactivity disorder. Res Dev Disabil. 2011;32(6):2480–8. Epub 2011/08/09. S0891-4222(11)00268-X [pii] doi: 10.1016/j.ridd.2011.06.021 21820271.

45. Weiß RH. Grundintelligenztest Skala 2, CFT 20-R [Basic Intelligence Test, Scale 2, CFT 20 (revised)]. Göttingen, Germany: Hogrefe; 2006.

46. Hooks K, Milich R, Pugzles Lorch E. Sustained and selective attention in boys with attention deficit hyperactivity disorder. Journal of Clinical child psychology. 1994;23(1):69–77.

47. Bioulac S, Lallemand S, Rizzo A, Philip P, Fabrigoule C, Bouvard MP. Impact of time on task on ADHD patient's performances in a virtual classroom. Eur J Paediatr Neurol. 2012;16(5):514–21. Epub 2012/01/25. doi: 10.1016/j.ejpn.2012.01.006 22269913.

48. Zimmermann P, Gondan M, Fimm B. Testbatterie zur Aufmerksamkeitsprüfung für Kinder (KITAP): Würselen: Psychtest; 2005.

49. Renner G, Lessing T, Krampen G, Irblich D. Reliabilität und Retest-Stabilität der „Testbatterie zur Aufmerksamkeitsprüfung fuer Kinder”(KITAP) bei 6- bis 7-jaehrigen Kindern. Zeitschrift fuer Neuropsychologie. 2012;23(1):27–36.

50. Kales A, Rechtschaffen A. A manual of standardized terminology, techniques and scoring system for sleep stages of human subjects: US Department of Health, Education and Welfare, Public Health Service, National Institutes of Health, National Institute of Neurological Diseases and Blindness, Neurological Information Network; 1968.

51. Wechsler D. Wechsler Intelligence Scale for Children–Fourth Edition (WISC-IV). San Antonio, TX: The Psychological Corporation; 2003.

52. Campbell IG, Feinberg I. Maturational Patterns of Sigma Frequency Power Across Childhood and Adolescence: A Longitudinal Study. Sleep. 2016;39(1):193–201. Epub 2015/08/19. doi: 10.5665/sleep.5346 26285004; PubMed Central PMCID: PMC4678354.

53. Purcell SM, Manoach DS, Demanuele C, Cade BE, Mariani S, Cox R, et al. Characterizing sleep spindles in 11,630 individuals from the National Sleep Research Resource. Nature communications. 2017;8:15930. Epub 2017/06/27. doi: 10.1038/ncomms15930 28649997; PubMed Central PMCID: PMC5490197.

54. Shinomiya S, Nagata K, Takahashi K, Masumura T. Development of sleep spindles in young children and adolescents. Clin Electroencephalogr. 1999;30(2):39–43. Epub 1999/06/08. 10358781.

55. Nunez PL. Toward a quantitative description of large-scale neocortical dynamic function and EEG. Behav Brain Sci. 2000;23(3):371–98; discussion 99–437. Epub 2001/04/17. 11301576.

56. Jenni OG, Carskadon MA. Spectral analysis of the sleep electroencephalogram during adolescence. Sleep. 2004;27(4):774–83. Epub 2004/07/31. 15283014.

57. Philipsen A, Feige B, Hesslinger B, Ebert D, Carl C, Hornyak M, et al. Sleep in adults with attention-deficit/hyperactivity disorder: a controlled polysomnographic study including spectral analysis of the sleep EEG. Sleep. 2005;28(7):877–84. Epub 2005/08/30. doi: 10.1093/sleep/28.7.877 16124669.

58. Geiger A, Huber R, Kurth S, Ringli M, Jenni OG, Achermann P. The sleep EEG as a marker of intellectual ability in school age children. Sleep. 2011;34(2):181–9. Epub 2011/02/03. doi: 10.1093/sleep/34.2.181 21286251; PubMed Central PMCID: PMC3022938.

59. Giedd JN, Blumenthal J, Jeffries NO, Castellanos FX, Liu H, Zijdenbos A, et al. Brain development during childhood and adolescence: a longitudinal MRI study. Nat Neurosci. 1999;2(10):861–3. Epub 1999/09/24. doi: 10.1038/13158 10491603.

60. Konrad K, Firk C, Uhlhaas PJ. Brain development during adolescence: neuroscientific insights into this developmental period. Dtsch Arztebl Int. 2013;110(25):425–31. Epub 2013/07/11. doi: 10.3238/arztebl.2013.0425 23840287; PubMed Central PMCID: PMC3705203.

61. Valera EM, Faraone SV, Murray KE, Seidman LJ. Meta-analysis of structural imaging findings in attention-deficit/hyperactivity disorder. Biol Psychiatry. 2007;61(12):1361–9. Epub 2006/09/05. doi: 10.1016/j.biopsych.2006.06.011 16950217.

62. Nakao T, Radua J, Rubia K, Mataix-Cols D. Gray matter volume abnormalities in ADHD: voxel-based meta-analysis exploring the effects of age and stimulant medication. AJ Psychiatry. 2011;168(11):1154–63. Epub 2011/08/26. doi: 10.1176/appi.ajp.2011.11020281 21865529.

63. Mohamed SM, Borger NA, Geuze RH, van der Meere JJ. Brain lateralization and self-reported symptoms of ADHD in a population sample of adults: a dimensional approach. Front Psychol. 2015;6:1418. Epub 2015/10/07. doi: 10.3389/fpsyg.2015.01418 26441789; PubMed Central PMCID: PMC4585266.

64. Marcos-Vidal L, Martinez-Garcia M, Pretus C, Garcia-Garcia D, Martinez K, Janssen J, et al. Local functional connectivity suggests functional immaturity in children with attention-deficit/hyperactivity disorder. Hum Brain Mapp. 2018;39(6):2442–54. Epub 2018/02/24. doi: 10.1002/hbm.24013 29473262.

65. Doucette MR, Kurth S, Chevalier N, Munakata Y, LeBourgeois MK. Topography of Slow Sigma Power during Sleep is Associated with Processing Speed in Preschool Children. Brain sciences. 2015;5(4):494–508. Epub 2015/11/12. doi: 10.3390/brainsci5040494 26556377; PubMed Central PMCID: PMC4701024.

66. Mima T, Steger J, Schulman AE, Gerloff C, Hallett M. Electroencephalographic measurement of motor cortex control of muscle activity in humans. Clin Neurophysiol. 2000;111(2):326–37. Epub 2000/02/19. doi: 10.1016/s1388-2457(99)00229-1 10680569.

67. Shaw P, Eckstrand K, Sharp W, Blumenthal J, Lerch JP, Greenstein D, et al. Attention-deficit/hyperactivity disorder is characterized by a delay in cortical maturation. Proc Natl Acad Sci U S A. 2007;104(49):19649–54. Epub 2007/11/21. doi: 10.1073/pnas.0707741104 18024590; PubMed Central PMCID: PMC2148343.

68. Shaw P, Lerch J, Greenstein D, Sharp W, Clasen L, Evans A, et al. Longitudinal mapping of cortical thickness and clinical outcome in children and adolescents with attention-deficit/hyperactivity disorder. Arch Gen Psychiatry. 2006;63(5):540–9. Epub 2006/05/03. doi: 10.1001/archpsyc.63.5.540 16651511.

69. Shaw P, Eckstrand K, Sharp W, Blumenthal J, Lerch JP, Greenstein D, et al. Attention-deficit/hyperactivity disorder is characterized by a delay in cortical maturation. Proc Natl Acad Sci U S A. 2007;104(49):19649–54. Epub 2007/11/21. doi: 10.1073/pnas.0707741104 18024590; PubMed Central PMCID: PMC2148343.

70. De Crescenzo F, Armando M, Mazzone L, Ciliberto M, Sciannamea M, Figueroa C, et al. The use of actigraphy in the monitoring of methylphenidate versus placebo in ADHD: a meta-analysis. Atten Defic Hyperact Disord. 2014;6(1):49–58. Epub 2013/11/30. doi: 10.1007/s12402-013-0122-x 24287735.

71. Morash-Conway J, Gendron M, Corkum PThe role of sleep quality and quantity in moderating the effectiveness of medication in the treatment of children with ADHD. Atten Defic Hyperact Disord. 2017;9(1):31–8. Epub 2016/08/16. doi: 10.1007/s12402-016-0204-7 27515452.


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