Sleep stage II contributes to the consolidation of declarative memories

Neuropsychologia

Volumn 50, Issue 10, 2012, Pages 2389-2396

  Ruch, Simon ^a   Markes, Oliver ^a   Duss, Simone B ^a   Oppliger, Daniel ^a   Reber, Thomas P ^a   Koenig, Thomas ^a,b   Mathis, Johannes ^b   Roth, Corinne ^b   Henke, Katharina ^a  

^a UNIVERSITY OF BERN   (Switzerland)

^b UNIVERSITY OF BERN   (Switzerland)

Author keywords

Delta waves; Explicit; Implicit; Nap; Recall; Slow oscillations; Spindles

Indexed keywords

ADULT; ARTICLE; CONTROLLED STUDY; DECLARATIVE MEMORY; DELTA RHYTHM; HUMAN; HUMAN EXPERIMENT; MALE; MEMORY CONSOLIDATION; MENTAL PERFORMANCE; NONREM SLEEP; POLYSOMNOGRAPHY; RECALL; SLEEP QUALITY; SLEEP SPINDLE; SLEEP STAGE; STATE DEPENDENT LEARNING; TASK PERFORMANCE;

ADULT; ASSOCIATION; DELTA RHYTHM; HUMANS; LEARNING; MALE; MEMORY; MENTAL RECALL; NEUROPSYCHOLOGICAL TESTS; POLYSOMNOGRAPHY; SLEEP STAGES; TIME FACTORS; YOUNG ADULT;

EID: 84864393109     PISSN: 00283932     EISSN: 18733514     Source Type: Journal    
DOI: 10.1016/j.neuropsychologia.2012.06.008     Document Type: Article

References (60)

1. Achermann P., Borbély A. Low-frequency (<1Hz) oscillations in the human sleep electroencephalogram. Neuroscience 1997, 81:213-222.
2. Andrade K.C., Spoormaker V.I., Dresler M., Wehrle R., Holsboer F., Sämann P.G., et al. Sleep spindles and hippocampal functional connectivity in human NREM sleep. The Journal of Neuroscience 2011, 31:10331-10339.
3. Backhaus J., Junghanns K. Daytime naps improve procedural motor memory. Sleep Medicine 2006, 7:508-512.
4. Baron R.M., Kenny D.A. The moderator-mediator variable distinction in social psychological research: conceptual, strategic, and statistical considerations. Journal of personality and social psychology 1986, 51:1173-1182.
5. Bódizs R., Körmendi J., Rigó P., Lázár A.S. The individual adjustment method of sleep spindle analysis: Methodological improvements and roots in the fingerprint paradigm. Journal of Neuroscience Methods 2009, 178:205-213.
6. Buzsáki G. Rhythms of the Brain 2006, Oxford University Press.
7. Clemens Z., Fabó D., Halász P. Overnight verbal memory retention correlates with the number of sleep spindles. Neuroscience 2005, 132:529-535.
8. Clemens Z., Fabó D., Halász P. Twenty-four hours retention of visuospatial memory correlates with the number of parietal sleep spindles. Neuroscience Letters 2006, 403:52-56.
9. De Gennaro L., Ferrara M., Vecchio F., Curcio G., Bertini M. An electroencephalographic fingerprint of human sleep. NeuroImage 2005, 26:114-122.
10. Diekelmann S., Born J. The memory function of sleep. Nature Reviews Neuroscience 2010, 11:114-126.
11. Duss S.B., Oggier S., Reber T.P., Henke K. Formation of semantic associations between subliminally presented face-word pairs. Consciousness and Cognition 2011, 20:928-935.
12. Eckstein D., Perrig W.J. The influence of intention on masked priming: A study with semantic classification of words. Cognition 2007, 104:345-376.
13. Fogel S.M., Smith C.T. Learning-dependent changes in sleep spindles and stage 2 sleep. Journal of Sleep Research 2006, 15:250-255.
14. Fogel S.M., Smith C.T. The function of the sleep spindle: A physiological index of intelligence and a mechanism for sleep-dependent memory consolidation. Neuroscience & Biobehavioral Reviews 2011, 35:1154-1165.
15. Fogel S.M., Smith C.T., Cote K.A. Dissociable learning-dependent changes in REM and non-REM sleep in declarative and procedural memory systems. Behavioural Brain Research 2007, 180:48-61.
16. Gais S., Mölle M., Helms K., Born J. Learning-dependent increases in sleep spindle density. The Journal of Neuroscience 2002, 22:6830-6834.
17. Genzel L., Dresler M., Wehrle R., Grözinger M., Steiger A. Slow wave sleep and REM sleep awakenings do not affect sleep dependent memory consolidation. Sleep 2009, 32:302-310.
18. Hayashi M., Motoyoshi N., Hori T. Recuperative power of a short daytime nap with or without stage 2 sleep. Sleep 2005, 28:829-836.
19. Henke K., Mondadori C.R.A., Treyer V., Nitsch R.M., Buck A., Hock C. Nonconscious formation and reactivation of semantic associations by way of the medial temporal lobe. Neuropsychologia 2003, 41:863-876.
20. Huber R., Ghilardi M.F., Massimini M., Tononi G. Local sleep and learning. Nature 2004, 430:78-81.
21. Kiefer M., Martens U. Attentional sensitization of unconscious cognition: task sets modulate subsequent masked semantic priming. Journal of Experimental Psychology. General 2010, 139:464-489.
22. Klem G.H., Lüders H.O., Jasper H.H., Elger C. The ten-twenty electrode system of the International Federation. The International Federation of Clinical Neurophysiology. Electroencephalography and Clinical Neurophysiology 1999, 52:3-6. Supplement.
23. Lahl O., Wispel C., Willigens B., Pietrowsky R. An ultra short episode of sleep is sufficient to promote declarative memory performance. Journal of Sleep Research 2008, 17:3-10.
24. Mander B.A., Santhanam S., Saletin J.M., Walker M.P. Wake deterioration and sleep restoration of human learning. Current Biology 2011, 21:183-184.
25. Marshall L., Born J. The contribution of sleep to hippocampus-dependent memory consolidation. Trends in Cognitive Sciences 2007, 11:442-450.
26. Marshall L., Helgadóttir H., Mölle M., Born J. Boosting slow oscillations during sleep potentiates memory. Nature 2006, 444:610-613.
27. Marshall L., Mölle M., Hallschmid M., Born J. Transcranial direct current stimulation during sleep improves declarative memory. The Journal of Neuroscience 2004, 24:9985-9992.
28. Masa J.F., Rubio M., Pérez P., Mota M., de Cos J.S., Montserrat J.M. Association between habitual naps and sleep apnea. Sleep 2006, 29:1463-1468.
29. Meier-Koll A., Bussmann B., Schmidt C., Neuschwander D. Walking through a maze alters the architecture of sleep. Perceptual and Motor Skills 1999, 88:1141-1159.
30. Mölle M., Eschenko O., Gais S., Sara S.J., Born J. The influence of learning on sleep slow oscillations and associated spindles and ripples in humans and rats. European Journal of Neuroscience 2009, 29:1071-1081.
31. Mölle M., Marshall L., Gais S., Born J. Grouping of spindle activity during slow oscillations in human non-rapid eye movement sleep. The Journal of Neuroscience 2002, 22:10941-10947.
32. Nader R., Smith C.T. A role for stage 2 sleep in memory processing. Sleep and Brain Plasticity 2003, 87-98. Oxford University Press, Oxford. P. Maquet, C.T. Smith, R. Stickgold (Eds.).
33. Nishida M., Walker M.P. Daytime naps, motor memory consolidation and regionally specific sleep spindles. PLoS ONE 2007, 2:e341.
34. Peters K.R., Ray L., Smith V., Smith C. Changes in the density of stage 2 sleep spindles following motor learning in young and older adults. Journal of Sleep Research 2008, 17:23-33.
35. Peters K.R., Smith V., Smith C.T. Changes in sleep architecture following motor learning depend on initial skill level. Journal of cognitive neuroscience 2007, 19:817-829.
36. Phillips P.J., Moon H., Rizvi S.A., Rauss P.J. The FERET evaluation methodology for face recognition algorithms. Pattern Analysis and Machine Intelligence 2000, 22:1090-1104.
37. Phillips P.J., Wechsler H., Huang J., Rauss P.J. The FERET database and evaluation procedure for face recognition algorithms. Image and Vision Computing 1998, 16:295-306.
38. Plihal W., Born J. Effects of early and late nocturnal sleep on declarative and procedural memory. Journal of Cognitive Neuroscience 1997, 9:534-547.
39. Plihal W., Born J. Effects of early and late nocturnal sleep on priming and spatial memory. Psychophysiology 1999, 36:571-582.
40. Rasch B., Büchel C., Gais S., Born J. Odor cues during slow-wave sleep prompt declarative memory consolidation. Science 2007, 315:1426-1429.
41. Reber T.P., Henke K. Rapid formation and flexible expression of memories of subliminal word pairs. Frontiers in Psychology 2011, 2:343.
42. Rechtschaffen A., Kales A. A manual of standardized terminology, techniques and scoring system for sleep stages of human subjects 1968, Public Health Service, US Government Printing Office, Washington, DC.
43. Rudoy J.D., Voss J.L., Westerberg C.E., Paller K.A. Strengthening individual memories by reactivating them during sleep. Science 2009, 326:1079.
44. Sämann P.G., Wehrle R., Hoehn D., Spoormaker V.I., Peters H., Tully C., et al. Development of the brain's default mode network from wakefulness to slow wave sleep. Cerebral Cortex 2011, 21:2082-2093.
45. Schabus M., Gruber G., Parapatics S., Sauter C., Klösch G., Anderer P., et al. Sleep spindles and their significance for declarative memory consolidation. Sleep 2004, 27:1479-1485.
46. Schabus M., Hödlmoser K., Pecherstorfer T., Klösch G. Influence of midday naps on declarative memory performance and motivation. Somnologie - Schlafforschung und Schlafmedizin 2005, 9:148-153.
47. Sirota A., Csicsvari J., Buhl D., Buzsáki G. Communication between neocortex and hippocampus during sleep in rodents. Proceedings of the National Academy of Sciences of the United States of America 2003, 100:2065-2069.
48. Smith C., Macneill C. Impaired motor memory for a pursuit rotor task following Stage 2 sleep loss in college students. Journal of Sleep Research 1994, 3:206-213.
49. Squire L.R. Memory and brain 1987, Oxford University Press, New York.
50. Squire L.R., Cohen N.J., Nadel L. The medial temporal region and memory consolidation: a new hyptothesis. Memory consolidation 1984, 185-210. Lawrence Erlbaum, Hillsdale, NJ. H.J. Weingartner, E.S. Parker (Eds.).
51. Steriade M. Grouping of brain rhythms in corticothalamic systems. Neuroscience 2006, 137:1087-1106.
52. Steriade M., Nunez A., Amzica F. Intracellular analysis of relations between the slow (<1Hz) neocortical oscillation and other sleep rhythms of the electroencephalogram. TheJournal of Neuroscience 1993, 13:3266-3283.
53. Steriade M., Nunez A., Amzica F. A novel slow (<1Hz) oscillation of neocortical neurons in vivo: depolarizing and hyperpolarizing components. The Journal of Neuroscience 1993, 13:3252-3265.
54. Tucker M.A., Hirota Y., Wamsley E.J., Lau H., Chaklader A., Fishbein W. A daytime nap containing solely non-REM sleep enhances declarative but not procedural memory. Neurobiology of Learning and Memory 2006, 86:241-247.
55. van der Helm E., Gujar N., Nishida M., Walker M.P. Sleep-dependent facilitation of episodic memory details. PLoS ONE 2011, 6:e27421.
56. Vaughn B.V., Giallanza P. Technical review of polysomnography. Chest 2008, 134:1310-1319.
57. Vela-Bueno A., Fernandez-Mendoza J., Olavarrieta-Bernardino S., Vgontzas A.N., Bixler E.O., de la Cruz-Troca J.J., et al. Sleep and behavioral correlates of napping among young adults: a survey of first-year university students in Madrid, Spain. Journal of American college health 2008, 57:150-158.
58. Walker M.P., Brakefield T., Morgan A., Hobson J.A., Stickgold R. Practice with sleep makes perfect: sleep-dependent motor skill learning. Neuron 2002, 35:205-211.
59. Wamsley E.J., Tucker M.A., Payne J.D., Stickgold R. A brief nap is beneficial for human route-learning: The role of navigation experience and EEG spectral power. Learning & Memory 2010, 17:332-336.
60. Werth E., Achermann P., Dijk D.-J., Borbély A.A. Spindle frequency activity in the sleep EEG: individual differences and topographical distribution. Electroencephalography and Clinical Neurophysiology 1997, 103:535-542.