Sleep disorder in childhood impairs declarative but not nondeclarative forms of learning

Journal of Clinical and Experimental Neuropsychology

Volumn 35, Issue 7, 2013, Pages 677-685

  Csábi, Eszter ^a   Benedek, Pálma ^b   Janacsek, Karolina ^c   Katona, Gábor ^b   Nemeth, Dezso ^c,d  

^a UNIVERSITY OF SZEGED   (Hungary)

^b HEIM PÁL CHILDREN S HOSPITAL   (Hungary)

^c EÖTVÖS LORÁND UNIVERSITY   (Hungary)

^d UNIVERSITY OF TEXAS AT AUSTIN   (United States)

Author keywords

Declarative memory; General skill learning; Nondeclarative memory; Obstructive sleep apnea; Sequence specific learning; Sleep; Sleep breathing disorder; Snoring

Indexed keywords

ARTICLE; CHILD; EXECUTIVE FUNCTION; FEMALE; FRONTAL LOBE; HUMAN; LEARNING; LEARNING DISORDER; MALE; MEMORY; NEUROPSYCHOLOGICAL TEST; PHYSIOLOGY; PSYCHOLOGICAL ASPECT; PSYCHOMOTOR PERFORMANCE; REACTION TIME; RECALL; SLEEP DISORDER; SOCIOECONOMICS; STATISTICAL ANALYSIS;

CHILD; DATA INTERPRETATION, STATISTICAL; EXECUTIVE FUNCTION; FEMALE; FRONTAL LOBE; HUMANS; LEARNING; LEARNING DISORDERS; MALE; MEMORY; MENTAL RECALL; NEUROPSYCHOLOGICAL TESTS; PSYCHOMOTOR PERFORMANCE; REACTION TIME; SERIAL LEARNING; SLEEP DISORDERS; SOCIOECONOMIC FACTORS;

EID: 84884901405     PISSN: 13803395     EISSN: 1744411X     Source Type: Journal    
DOI: 10.1080/13803395.2013.815693     Document Type: Article

References (72)

1. Albouy, G., Sterpenich, V., Balteau, E., Vandewalle, G., Desseilles, M., Dang-Vu, T., . . . Maquet, P. (2008). Both the hippocampus and striatum are involved in consolidation of motor sequence memory. Neuron, 58, 261-272. (Pubitemid 351538999)
2. Andreano, J. M., & Cahill, L. (2006). Glucocorticoid release and memory consolidation in men and woman. Psychological Science, 17, 466-470. (Pubitemid 43855788)
3. Andreano, J. M., & Cahill, L. (2008). Menstrual cycle modulation of the relationship between cortisol and long-term memory. Psychoneuroendocrinology, 33, 874-882.
4. Archbold, K. H. (2006). Sleep disorders and attentiondeficit hyperactivity disorder in children: A missing differential diagnosis. Journal of the American Psychiatric Nurses Association, 12, 216-224. (Pubitemid 44530533)
5. Archbold, K. H., Giordani, B., Ruzicka, D. L., & Chervin, R. D. (2004). Cognitive executive dysfunction in children with mild sleep-disordered breathing. Biological Research for Nursing, 5, 168-176.
6. Arens, R., McDonough, J. M., Costarino, A. T., Mahboubi, S., Tayag-Kier, C. E., Maislin, G., . . . Pack, A. J. (2001). Magnetic resonance imaging of the upper airway structure of children with obstructive sleep apnea syndrome. American Journal of Respiratory and Critical Care Medicine, 164, 698-703. (Pubitemid 32801679)
7. Backhaus, J., Hoeckesfeld, R., Hohagen, J. B., & Junghanns, K. (2008). Immediate as well as delayed post learning sleep but not wakefulness enhances declarative memory consolidation in children. Neurobiology of Learning and Memory, 89, 76-80. (Pubitemid 350102249)
8. Bartlett, D. J., Rae, C., Thompson, C. H., Byth, K., Joffe, D. A., Enright, T., & Grunstein, R. R. (2004). Hippocampal area metabolites relate to severity and cognitive function in obstructive sleep apnea. Sleep Medicine, 5, 593-596. (Pubitemid 39420039)
9. Bartlett, F. C. (1932). Remembering: An experimental and social study. Cambridge: Cambridge University.
10. Beebe, D. W. (2006). Neurobehavioral morbidity associated with disordered breathing during sleep in children: A comprehensive review. Sleep, 29, 1115-1134. (Pubitemid 44484806)
11. Beebe, D. W., & Gozal, D. (2002). Obstructive sleep apnea and the prefrontal cortex: Towards a comprehensive model linking nocturnal upper airway obstruction to daytime cognitive and behavioral deficits. Journal of Sleep Research, 11, 1-16. (Pubitemid 34227209)
12. Beebe, D. W., Wells, C. T., Jeffries, J., Chini, B., Kalra, M., & Amin, R. (2004). Neuropsychological effects of pediatric obstructive sleep apnea. Journal of the International Neuropsychological Society, 10, 962-975.
13. Bergman, E. T., & Roediger, H. L. (1999). Can Bartlett's repeated reproduction experiments be replicated? Memory & Cognition, 27, 937-947.
14. Blunden, S., Lushington, K., Kennedy, D., Martin, J., & Dawson, D. (2000). Behavior and neurocognitive performance in children aged 5-10 years who snore compared to controls. Journal of Clinical and Experimental Neuropsychology, 22, 554-568.
15. Cohen, D. A., Pascual-Leone, A., Press, D. Z., & Robertson, E. M. (2005). Off-line learning of motor skill memory: A double dissociation of goal and movement. Proceedings of the National Academy of Sciences of the United States of America, 102, 18237-18241. (Pubitemid 41798531)
16. Coleman, J. (2003). Pathophysiology of snoring and obstructive sleep apnea: Airway dynamics. In D. N. F. Fairbanks, S. A. Mickelson, & B. T. Woodson (Eds.), Snoring and obstructive sleep apnea (pp. 19-24). Philadelphia, PA: Williams & Wilkins Co.
17. Cosentino, F. I., Bosco.P., Drago, V., Prestianni, G., Lanuzza, B., Iero, I., . . . Ferri, R. (2008). The APOE epsilon4 allele increases the risk of impaired spatial working memory in obstructive sleep apnea. Sleep Medicine, 9, 831-839.
18. Dennis, N., & Cabeza, R. (2011). Age-related dedifferentiation of learning systems: An fMRI study of implicit and explicit learning. Neurobiology of Aging, 32, 2318-2330.
19. Diekelmann, S., & Born, J. (2010). The memory function of sleep. Nature Reviews Neuroscience, 11, 114-126.
20. Diekelmann, S.,Wilhelm, I., & Born, J. (2009). The whats and whens of sleep-dependent memory consolidation. Sleep Medicine Reviews, 13, 309-321.
21. Donelly, L. F., Shott, S. R., LaRose, C. L., Chini, B. A., & Amin, R. S. (2004). Causes of persistent obstructive sleep apnoea despite previous tonsillectomy and adenoidectomy in children with Down syndrome as depicted on static and dynamic cine MRI. American Journal of Roentgenology, 183, 175-181. (Pubitemid 38789033)
22. Doyon, J., Bellec, P., Amsel, R., Penhune, V., Monchi, O., Carrier, J., . . . Benali, H. (2009). Contributions of the basal ganglia and functionally related brain structures to motor learning. Behavioral Brain Research, 199, 61-75.
23. Fischer, S.,Wilhelm, I., & Born, J. (2007). Developmental differences in sleep's role for implicit off-line learning: Comparing children with adults. Journal of Cognitive Neuroscience, 19, 214-227. (Pubitemid 46220704)
24. Fletcher, P. C., Zafiris, O., Frith, C. D., Honey, R. A. E., Corlett, P. R., Zilles, K., & Fink, G. R. (2005). On the benefits of not trying: Brain activity and connectivity reflecting the interactions of explicit and implicit sequence learning. Cerebral Cortex, 15, 1002-1015. (Pubitemid 40848069)
25. Gais, S., & Born, J. (2004). Declarative memory consolidation: Mechanisms acting during human sleep. Learning & Memory, 11, 679-685. (Pubitemid 39602505)
26. Gauld, A., & Stephenson, G. M. (1967). Some experiments relating to Bartlett's theory of remembering. British Journal of Psychology, 58, 39-49.
27. Genzel, L., Dresler, M., Wehrle, R., Grözinger, M., & Steiger, A. (2009). Slow wave sleep and REM sleep awakenings do not affect sleep dependent memory consolidation. Sleep, 32, 302.
28. Goldbart, A. D., & Tal, A. (2008). Inflammation and sleep disordered breathing in children: A state-of-theart review. Pediatric Pulmonology, 43, 1151-1160.
29. Gottlieb, D. J., Chase, C., Vezina, R. M., Heeren, T. C., Corwin, M. J., Auerbach, S. H., . . . Lesko, S. M. (2004). Sleep-disordered breathing symptoms are associated with poorer cognitive function in 5-yearold children. Journal of Pediatrics, 145, 458-464. (Pubitemid 39345980)
30. Gozal, D., & O'Brien, L. M. (2004). Snoring and obstructive sleep apnoea in children: Why should we treat? Pediatric Respiratory Reviews, 5, S371-S376.
31. Guimaraes, C. V. A., Kalra, M., Donelly, L. F., Shott, S. R., Fitz, K., Singla, A., & Amin, R. S. (2008). The frequency of lingual tonsil enlargement in obese children. American Journal of Roentgenology, 190, 973-975. (Pubitemid 351571518)
32. Halbower, A. C., Degaonkar, M., Barker, P. B., Earley, C. J., Marcus, C. L., Smith, P. L., . . . Mahone, E. M. (2006). Childhood obstructive sleep apnea associates with neuropsychological deficits and neuronal brain injury. PLoS Medicine, 3, e301.
33. Hamasaki Uema, S. F., Nagata Pignatari, S. S., Fujita, R. R., Moreira, G. A., Pradella-Hallinan, M., & Weckx, L. (2007). Assessment of cognitive learning function in children with obstructive sleep breathing disorders. Brazilian Journal of Otorhinolaryngology, 73, 315-320.
34. Hardt, O., Einarsson, E. Ö., & Nader, K. (2010). A bridge over troubled water: Reconsolidation as a link between cognitive and neuroscientific memory research traditions. Annual Review of Psychology, 61, 141-167.
35. Howard, D. V., Howard, J. H., Jr., Japikse, K., DiYanni, C., Thompson, A., & Somberg, R. (2004). Implicit sequence learning: Effects of level of structure, adult age, and extended practice. Psychology and Aging, 19, 79-92. (Pubitemid 38338267)
36. Howard, J. H., & Howard, D. V. (1997). Age differences in implicit learning of higher-order dependencies in serial patterns. Psychology & Aging, 19, 79-92.
37. Janacsek, K., Fiser, J., & Nemeth, D. (2012). The best time to acquire new skills: Age-related differences in implicit sequence learning across the human lifespan. Developmental Science, 15, 496-505.
38. Jones, K., & Harrison, Y. (2001). Frontal lobe function, sleep loss and fragmented sleep. Sleep Medicine Reviews, 5, 463-475. (Pubitemid 34066251)
39. Kaemingk, K. L., Pasvogel, A. E., Goodwin, J. L., Mulvaney, S. A., Martinez, F., Enright, P. L., . . . Quan, S. F. (2003). Learning in children and sleep disordered breathing: Findings of the Tucson Children's Assessment of Sleep Apnea (tuCASA) prospective cohort study. Journal of the International Neuropsychological Society, 9, 1016-1026. (Pubitemid 37428445)
40. Katz, E. S., & D'Ambrosio, C. M. (2008). Pathophysiology of pediatric obstructive sleep apnoea. Proceedings of the American Thoracic Society, 5, 253-262. (Pubitemid 351237885)
41. Kennedy, J. D., Blunden, S., Hirte, C., Parsons, D. W., Martin, A. J., Crowe, E. Lushington, K. (2004). Reduced neurocognition in children who snore. Pediatric Pulmonology, 37, 330-337. (Pubitemid 38523946)
42. Kheirandish-Gozal, L., de Jong, M. R., Spruyt, K., Chamuleau, S. A. J., & Gozal, D. (2010). Obstructive sleep apnoea is associated with impaired pictorial memory task acquisition and retention in children. European Respiratory Journal, 36, 164-169.
43. Li, H.-Y., & Lee, L.-A. (2009). Sleep-disorders breathing in children. Chang Gung Medical Journal, 32, 247-257.
44. Macey, P. M., Henderson, L. A., Macey, K. E., Alger, J. R., Frysinger, R. C.,Woo, M. A., . . . Harper, R. M. (2002). Brain morphology associated with obstructive sleep apnea. American Journal of Respiratory and Critical Care Medicine, 166, 1382-1387. (Pubitemid 35292706)
45. Marsh, E. J. (2007). Retelling is not the same as recalling: Implications for memory. Current Directions in Psychological Science, 16, 16-20.
46. Mitchell, R. B. (2008). Sleep-disordered breathing in children. Missouri Medicine, 105, 267-269.
47. Montgomery-Downs, H. M., O'Brien, L. M., Cheryl, R., Holbrook, M. A. T., & Gozal, D. (2004). Snoring and sleep-disordered breathing in young children: Subjective and objective correlates. Sleep, 27, 87-94. (Pubitemid 43906317)
48. Morrell, M. J., McRobbie, D.W., Quest, R. A., Cummin, A. R., Ghiassi, R., & Corfield, D. R. (2003). Changes in brain morphology associated with obstructive sleep apnea. Sleep Medicine, 4, 451-454. (Pubitemid 37193029)
49. Muzur, A., Pace-Schott, E. F., & Hobson, J. A. (2002). The prefrontal cortex in sleep. Trends in Cognitive Sciences, 6, 475-481. (Pubitemid 35341851)
50. Nemeth, D., Csábi, E., Janacsek, K., Varszegi, M., & Mari, Z. (2012). Intact implicit probabilistic sequence learning in obstructive sleep apnea. Journal of Sleep Research, 21, 396-401.
51. Nemeth, D., Janacsek, K., Londe, Z., Ullman, M. T., Howard, D., & Howard, J. (2010). Sleep has no critical role in implicit motor sequence learning in young and old adults. Experimental Brain Research, 201, 351-358.
52. O'Brien, L. M., Lucas, N. H., Felt, B. T., Hoban, T. F., Ruzicka, D. L., Jordan, R., . . . Chervin, E. D. (2011). Aggressive behavior, bullying, snoring, and sleepiness in schoolchildren. Sleep Medicine, 12, 652-658.
53. O'Brien, L. M., Mervis, C. B., Holbrook, C. R., Bruner, J. L., Klaus, C. J., Rutherford, J., . . . Gozal, D. (2004). Neurobehavioral implications of habitual snoring in children. Pediatrics, 114, 44-49. (Pubitemid 38857564)
54. O'Brien, L. M., Mervis, C. B., Holbrook, C. R., Bruner, J. L., Smith, N. H., McNally, N., . . . Gozal, D. (2004). Neurobehavioral correlates of sleepdisordered breathing in children. Journal of Sleep Research, 13, 165-172. (Pubitemid 38829898)
55. Poldrack, R. A., Clark, J., Pare-Blagoev, E. J., Shohamy, D., Creso Moyano, J., Myers, C., & Gluck, M. A. (2001). Interactive memory systems in the human brain. Nature, 414, 546-550. (Pubitemid 33131537)
56. Poldrack, R. A., & Packard, M. G. (2003). Competition among multiple memory systems: Converging evidence from animal and human brain studies. Neuropsychologia, 41, 245-251. (Pubitemid 35365954)
57. Prehn-Kristensen, A., Göder, R., Chirobeja, S., Breßmann, I., Ferstl, R., & Baving, L. (2009). Sleep in children enhances preferentially emotional declarative but not procedural memories. Journal of Experimental Child Psychology, 104, 132-139.
58. Remillard, G. (2008). Implicit learning of second-, third-, and fourth-order adjacent and nonadjacent sequential dependencies. The Quarterly Journal of Experimental Psychology, 61, 400-424.
59. Salorio, C. F., White, D. A., Piccirillo, J., Duntley, S. P., & Uhles, M. L. (2002). Learning, memory, and executive control in individuals with obstructive sleep apnea syndrome. Journal of Clinical and Experimental Neuropsychology, 24, 93-100. (Pubitemid 34412141)
60. Schendan, H., Searl, M., Melrose, R., & Stern, C. (2003). An fMRI study of the role of the medial temporal lobe in implicit and explicit sequence learning. Neuron, 37, 1013-1025. (Pubitemid 36398305)
61. Schwabe, L., &Wolf, O. T. (2009). New episodic learning interferes with the reconsolidation of autobiographical memories. PloS One, 4, e7519.
62. Sinha, D., & Guilleminault, C. (2010). Sleep disordered breathing in children. Indian Journal of Medical Research, 131, 311-320.
63. Song, S., Howard, J. H., Jr., & Howard, D. V. (2007). Sleep does not benefit probabilistic motor sequence learning. Journal of Neuroscience, 27, 12475-12483. (Pubitemid 350127818)
64. Squire, L. R., & Zola, S. M. (1996). Structure and function of declarative and nondeclarative memory systems. Proceedings of the National Academy of Sciences of the United States of America, 93, 13515-13522. (Pubitemid 26424150)
65. Stickgold, R., & Walker, M. P. (2007). Sleep-dependent memory consolidation and reconsolidation. Sleep Medicine, 8, 331-343. (Pubitemid 46706355)
66. Sullivan, S., Li, K., & Guilleminault, C. (2008). Nasal obstruction in children with sleep-disordered breathing. Annals Academy of Medicine Singapore, 37, 645-648.
67. Thomas, R. J., Rosen, B. R., Stern, C. E., Weiss, J. W., & Kwong, K. K. (2005). Functional imaging of working memory in obstructive sleep-disordered breathing. Journal of Applied Physiology, 98, 2226-2234. (Pubitemid 40726919)
68. Van Der Werf, Y., Altena, E., Vis, J., Koene, T., & Van Someren, E. (2011). Reduction of nocturnal slowwave activity affects daytime vigilance lapses and memory encoding but not reaction time or implicit learning. Progress in Brain Research, 193, 245.
69. Walker, M. P., Brakefield, T., Morgan, A., Hobson, J. A., & Stickgold, R. (2002). Practice with sleep makes perfect: Sleep-dependent motor skill learning. Neuron, 35, 205-211. (Pubitemid 34804334)
70. Wilhelm, I., Diekelmann, S., & Born, J. (2008). Sleep in children improves memory performance on declarative but not procedural tasks. Learning & Memory, 15, 373-377. (Pubitemid 351629602)
71. Wilhelm, I., Metzkow-Mészáros, M., Knapp, S., & Born, J. (2012). Sleep-dependent consolidation of procedural motor memories in children and adults: The pre-sleep level of performance matters. Developmental Science, 15, 506-515.
72. Wilson, J. K., Baran, B., Pace-Schott, E. F., Ivry, R. B., & Spencer, R. (2012). Sleep modulates word-pair learning but not motor sequence learning in healthy older adults. Neurobiology of Aging, 33, 991-1000.