NREM2 and Sleep Spindles Are Instrumental to the Consolidation of Motor Sequence Memories

PLoS Biology

Volumn 14, Issue 3, 2016, Pages

  Laventure, Samuel ^a,b   Fogel, Stuart ^a,b,c   Lungu, Ovidiu ^a,b   Albouy, Geneviève ^a,b,d   Sévigny Dupont, Pénélope ^a   Vien, Catherine ^a,b   Sayour, Chadi ^a,b   Carrier, Julie ^a,b,e   Benali, Habib ^f   Doyon, Julien ^a,b  

^a UNIVERSITÉ DE MONTRÉAL   (Canada)

^b CRIUGM   (Canada)

^c UNIVERSITY OF WESTERN ONTARIO   (Canada)

^d UNIVERSITY OF LEUVEN   (Belgium)

^e Center for Advanced Research in Sleep Medicine   (Canada)

^f SORBONNE UNIVERSITÉ   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CASE REPORT; CONTROLLED STUDY; EXPERIMENTAL MODEL; EXPOSURE; HUMAN; LEARNING; NIGHT; NONREM SLEEP; ODOR; SLEEP SPINDLE; ADULT; FEMALE; MALE; MEMORY CONSOLIDATION; MOTOR PERFORMANCE; PHYSIOLOGY; SLEEP STAGE; YOUNG ADULT;

FRAGRANCE;

ADULT; FEMALE; HUMANS; MALE; MEMORY CONSOLIDATION; MOTOR SKILLS; ODORANTS; SLEEP STAGES; SMELL; YOUNG ADULT;

EID: 84962166678     PISSN: 15449173     EISSN: 15457885     Source Type: Journal    
DOI: 10.1371/journal.pbio.1002429     Document Type: Article

References (98)

1. Robertson EM, Pascual-Leone A, Miall RC, Current concepts in procedural consolidation. Nat Rev Neurosci. 2004;5(7):576–82. 15208699
2. Maquet P, The role of sleep in learning and memory. Science. 2001;294(5544):1048–52. 11691982
3. Stickgold R, Walker MP, Sleep-dependent memory triage: evolving generalization through selective processing. Nat Neurosci. Nature Publishing Group. 2013Feb;16(2):139–45.
4. Doyon J, Bellec P, Amsel R, Penhune V, Monchi O, Carrier J, et al. Contributions of the basal ganglia and functionally related brain structures to motor learning. Behav Brain Res. 2009Apr12;199(1):61–75. doi: 10.1016/j.bbr.2008.11.01219061920
5. Doyon J, Motor sequence learning and movement disorders. Curr Opin Neurol. 2008Aug;21(4):478–83. doi: 10.1097/WCO.0b013e328304b6a318607210
6. Doyon J, Korman M, Morin A, Dostie V, Hadj Tahar A, Benali H, et al. Contribution of night and day sleep vs. simple passage of time to the consolidation of motor sequence and visuomotor adaptation learning. Exp Brain Res. 2009May;195(1):15–26. doi: 10.1007/s00221-009-1748-y19277618
7. Korman M, Doyon J, Doljansky J, Carrier J, Dagan Y, Karni A, Daytime sleep condenses the time course of motor memory consolidation. Nat Neurosci. Nature Publishing Group. 2007Sep;10(9):1206–13.
8. Walker MP, A refined model of sleep and the time course of memory formation. Behav Brain Sci. 2005Feb;28(1):51–104. 16047457
9. Cajochen C, Knoblauch V, Wirz-Justice A, Kräuchi K, Graw P, Wallach D, Circadian modulation of sequence learning under high and low sleep pressure conditions. Behav Brain Res. 2004May5;151(1–2):167–76. 15084432
10. Robertson EM, Pascual-Leone A, Press DZ, Awareness modifies the skill-learning benefits of sleep. Curr Biol. 2004Feb3;14(3):208–12. 14761652
11. Fischer S, Hallschmid M, Elsner AL, Born J, Sleep forms memory for finger skills. Proc Natl Acad Sci U S A. 2002Sep3;99(18):11987–91. 12193650
12. Doyon J, Orban P, Barakat M, Debas K, Lungu O, Albouy G, et al. Functional brain plasticity associated with motor learning. Med Sci MS. 2011;27(4):413–20.
13. Walker MP, Brakefield T, Morgan A, Hobson JA, Stickgold R, Practice with Sleep Makes Perfect: Sleep-Dependant Motor Skill Learning. Neuron. 2002;35(1):205–11. 12123620
14. Genzel L, Kroes MCW, Dresler M, Battaglia FP, Light sleep versus slow wave sleep in memory consolidation: a question of global versus local processes?Trends Neurosci. 2014Jan;37(1):10–9. doi: 10.1016/j.tins.2013.10.00224210928
15. Rasch B, Pommer J, Diekelmann S, Born J, Pharmacological REM sleep suppression paradoxically improves rather than impairs skill memory. Nat Neurosci. Nature Publishing Group; 2009Apr;12(4):396–7.
16. Fogel S, Smith CT, The function of the sleep spindle: a physiological index of intelligence and a mechanism for sleep-dependent memory consolidation. Neurosci Biobehav Rev. Elsevier Ltd; 2011Apr;35(5):1154–65.
17. Barakat M, Carrier J, Debas K, Lungu O, Fogel S, Vandewalle G, et al. Sleep spindles predict neural and behavioral changes in motor sequence consolidation. Hum Brain Mapp. 2013Jun5;34(May 2011):2918–28.
18. Barakat M, Doyon J, Debas K, Vandewalle G, Morin A, Poirier G, et al. Fast and slow spindle involvement in the consolidation of a new motor sequence. Behav Brain Res. Elsevier B.V.; 2011Feb2;217(1):117–21.
19. Morin A, Doyon J, Dostie V, Barakat M, Hadj Tahar A, Korman M, et al. Motor sequence learning increases sleep spindles and fast frequencies in post-training sleep. Sleep. 2008Aug;31(8):1149–56. 18714787
20. Nishida M, Walker MP, Daytime naps, motor memory consolidation and regionally specific sleep spindles. PLoS ONE. Public Library of Science; 2007Jan4;2(4):e341.
21. Yang G, Lai CSW, Cichon J, Ma L, Li W, Gan W-B, Sleep promotes branch-specific formation of dendritic spines after learning. Science. 2014;344:1173–8. doi: 10.1126/science.124909824904169
22. Ramanathan DS, Gulati T, Ganguly K, Sleep-Dependent Reactivation of Ensembles in Motor Cortex Promotes Skill Consolidation. PLoS Biol. Public Library of Science; 2015Sep18;13(9):e1002263.
23. Ackermann S, Rasch B, Differential effects of non-REM and REM sleep on memory consolidation?Curr Neurol Neurosci Rep. 2014;14.
24. Marshall L, Helgadóttir H, Mölle M, Born J, Boosting slow oscillations during sleep potentiates memory. Nature. 2006Nov30;444(7119):610–3. 17086200
25. Diekelmann S, Sleep for cognitive enhancement. Front Syst Neurosci. 2014Jan;8(April):46.
26. Rasch B, Born J, About sleep’s role in memory. Physiol Rev. 2013Apr1;93(2):681–766. doi: 10.1152/physrev.00032.201223589831
27. Oudiette D, Paller KA, Upgrading the sleeping brain with targeted memory reactivation. Trends Cogn Sci. 2013Mar;17(3):142–9. doi: 10.1016/j.tics.2013.01.00623433937
28. Rudoy JD, Voss JL, Westerberg CE, Paller K a, Strengthening individual memories by reactivating them during sleep. Science. 2009Nov20;326(November):1079.
29. Rasch B, Büchel C, Gais S, Born J, Odor cues during slow-wave sleep prompt declarative memory consolidation. Science. 2007Mar9;315(5817):1426–9. 17347444
30. Rihm JS, Diekelmann S, Born J, Rasch B, Reactivating memories during sleep by odors: odor specificity and associated changes in sleep oscillations. J Cogn Neurosci. 2014Aug26;26(8):1806–18. doi: 10.1162/jocn_a_0057924456392
31. Guerrien A, Dujardin K, Mandal O, Sockeel P, Leconte P, Enhancement of memory by auditory stimulation during postlearning REM sleep in humans. Physiol Behav. 1989May;45(5):947–50. 2780879
32. Smith CT, Weeden K, Post training REMs coincident auditory stimulation enhances memory in humans. Psychiatr J Univ Ottawa. 1990Jun;15(2):85–90.
33. Schönauer M, Geisler T, Gais S, Strengthening procedural memories by reactivation in sleep. J Cogn Neurosci. 2014Jan;26(1):143–53. doi: 10.1162/jocn_a_0047123984946
34. Cousins JN, El-Deredy W, Parkes LM, Hennies N, Lewis PA, Cued Memory Reactivation during Slow-Wave Sleep Promotes Explicit Knowledge of a Motor Sequence. J Neurosci. 2014Nov26;34(48):15870–6. doi: 10.1523/JNEUROSCI.1011-14.201425429129
35. Antony JW, Gobel EW, O’Hare JK, Reber PJ, Paller K a, Cued memory reactivation during sleep influences skill learning. Nat Neurosci. 2012/07/04 ed. Nature Publishing Group; 2012Aug;15(8):1114–6.
36. Arzi A, Shedlesky L, Ben-Shaul M, Nasser K, Oksenberg A, Hairston IS, et al. Humans can learn new information during sleep. Nat Neurosci. Nature Publishing Group; 2012Oct;15(10):1460–5.
37. Guazzelli M, Feinberg I, Aminoff M, Fein G, Floyd TC, Maggini C, Sleep spindles in normal elderly: comparison with young adult patterns and relation to nocturnal awakening, cognitive function and brain atrophy. Electroencephalogr Clin Neurophysiol. 1986Jun;63(6):526–39. 2422002
38. Himanen S-L, Virkkala J, Huhtala H, Hasan J, Spindle frequencies in sleep EEG show U-shape within first four NREM sleep episodes. J Sleep Res. 2002Mar;11(1):35–42. 11869425
39. De Gennaro L, Ferrara M, Bertini M, Effect of slow-wave sleep deprivation on topographical distribution of spindles. Behav Brain Res. 2000Nov15;116(1):55–9. 11090885
40. Laventure S. Data from: NREM2 and Sleep Spindles are Instrumental to the Consolidation of Motor Sequence Memories [Internet]. 2016. 10.5061/dryad.b4t60
41. Ray L, Sockeel S, Bore A, Carrier J, Doyon J, Fogel S, A novel sleep spindle detection method to account for intra- and inter-individual differences in spindle characteristics [Abstract]. J Sleep Res. 2014;23(S1):106.
42. Pan SC, Rickard TC, Sleep and Motor Learning: Is There Room for Consolidation?Psychol Bull. 2015Mar30;
43. Plihal W, Born J, Effects of early and late nocturnal sleep on declarative and procedural memory. J Cogn Neurosci. 1997Jul;9(4):534–47. doi: 10.1162/jocn.1997.9.4.53423968216
44. Smith CT, Sleep states and memory processes in humans: procedural versus declarative memory systems. Sleep Med Rev. 2001Dec;5(6):491–506. 12531156
45. Fogel S, Smith CT, Learning-dependent changes in sleep spindles and Stage 2 sleep. J Sleep Res. 2006Sep;15(April 2005):250–5.
46. Fogel S, Smith CT, Cote KA, Dissociable learning-dependent changes in REM and non-REM sleep in declarative and procedural memory systems. Behav Brain Res. 2007Jun4;180(1):48–61. 17400305
47. 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. 2009Mar;32(3):302–10. 19294950
48. Genzel L, Kiefer T, Renner L, Wehrle R, Kluge M, Grözinger M, et al. Sex and modulatory menstrual cycle effects on sleep related memory consolidation. Psychoneuroendocrinology. 2012Jul;37(7):987–98. doi: 10.1016/j.psyneuen.2011.11.00622153362
49. Debas K, Carrier J, Barakat M, Marrelec G, Bellec P, Hadj Tahar A, et al. Off-line consolidation of motor sequence learning results in greater integration within a cortico-striatal functional network. Neuroimage. 2014Oct1;99:50–8. doi: 10.1016/j.neuroimage.2014.05.02224844748
50. Lansink CS, Goltstein PM, Lankelma J V, McNaughton BL, Pennartz CMA, Stevens CF, Hippocampus leads ventral striatum in replay of place-reward information. PLoS Biol. 2009Aug;7(8):e1000173. doi: 10.1371/journal.pbio.100017319688032
51. Schabus M, Hoedlmoser K, Pecherstorfer T, Anderer P, Gruber G, Parapatics S, et al. Interindividual sleep spindle differences and their relation to learning-related enhancements. Brain Res. 2008Jan29;1191:127–35. doi: 10.1016/j.brainres.2007.10.10618164280
52. Schabus M, Hödlmoser K, Gruber G, Sauter C, Anderer P, Klösch G, et al. Sleep spindle-related activity in the human EEG and its relation to general cognitive and learning abilities. Eur J Neurosci. 2006Apr;23(7):1738–46. 16623830
53. Schabus M, Gruber G, Parapatics S, Sauter C, Klösch G, Anderer P, et al. Sleep spindles and their significance for declarative memory consolidation. Sleep. 2004Dec15;27(8):1479–85. 15683137
54. O’Reilly C, Nielsen T, Assessing EEG sleep spindle propagation. Part 2: Experimental characterization. J Neurosci Methods. Elsevier B.V.; 2014;221:215–27.
55. Contreras D, Destexhe A, Steriade M, Intracellular and computational characterization of the intracortical inhibitory control of synchronized thalamic inputs in vivo. J Neurophysiol. 1997;78(1):335–50. 9242284
56. Rosanova M, Ulrich D, Pattern-specific associative long-term potentiation induced by a sleep spindle-related spike train. J Neurosci. 2005Oct12;25(41):9398–405. 16221848
57. Sejnowski TJ, Destexhe A, Why do we sleep?Brain Res. 2000Dec;886(1–2):208–23. 11119697
58. Astori S, Wimmer RD, Lüthi A, Manipulating sleep spindles—expanding views on sleep, memory, and disease. Trends Neurosci. 2013;36(12):738–48. doi: 10.1016/j.tins.2013.10.00124210901
59. Werth E, Achermann P, Dijk D-J, Borbély AA, Spindle frequency activity in the sleep EEG: individual differences and topographical distribution. Electroencephalogr Clin Neurophysiol. 1997Nov;103(5):535–42. 9402884
60. Albouy G, King BR, Maquet P, Doyon J, Hippocampus and striatum: dynamics and interaction during acquisition and sleep-related motor sequence memory consolidation. Hippocampus. 2013Nov;23(11):985–1004. doi: 10.1002/hipo.2218323929594
61. Genzel L, Dresler M, Cornu M, Jäger E, Konrad B, Adamczyk M, et al. Medial prefrontal-hippocampal connectivity and motor memory consolidation in depression and schizophrenia. Biol Psychiatry. 2015Jan15;77(2):177–86. doi: 10.1016/j.biopsych.2014.06.00425037555
62. Dayan E, Cohen LG, Neuroplasticity subserving motor skill learning. Neuron. 2011Nov3;72(3):443–54. doi: 10.1016/j.neuron.2011.10.00822078504
63. Hikosaka O, Nakamura K, Sakai K, Nakahara H, Central mechanisms of motor skill learning. Curr Opin Neurobiol. 2002Apr;12(2):217–22. 12015240
64. Albouy G, Fogel S, King BR, Laventure S, Benali H, Karni A, et al. Maintaining vs. Enhancing Motor Sequence Memories: Respective Roles of Striatal and Hippocampal Systems. Neuroimage. 2015Dec23;108:423–34. doi: 10.1016/j.neuroimage.2014.12.04925542533
65. Albouy G, Fogel S, Pottiez H, Nguyen VA, Ray L, Lungu O, et al. Daytime sleep enhances consolidation of the spatial but not motoric representation of motor sequence memory. PLoS ONE. 2013/01/10 ed. 2013Jan;8(1):e52805. doi: 10.1371/journal.pone.005280523300993
66. Cox R, Hofman WF, de Boer M, Talamini LM, Local sleep spindle modulations in relation to specific memory cues. Neuroimage. Elsevier Inc.; 2014Oct1;99:103–10.
67. 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. 2011Dec7;31(49):17821–34. doi: 10.1523/JNEUROSCI.2604-11.201122159098
68. Anderer P, Klösch G, Gruber G, Trenker E, Pascual-Marqui R, Zeitlhofer J, et al. Low-resolution brain electromagnetic tomography revealed simultaneously active frontal and parietal sleep spindle sources in the human cortex. Neuroscience. 2001Mar;103(3):581–92. 11274780
69. Tyvaert L, Levan P, Grova C, Dubeau F, Gotman J, Effects of fluctuating physiological rhythms during prolonged EEG-fMRI studies. Clin Neurophysiol. 2008Dec;119(12):2762–74. doi: 10.1016/j.clinph.2008.07.28418977169
70. Schabus M, Dang-Vu TT, Albouy G, Balteau E, Boly M, Carrier J, et al. Hemodynamic cerebral correlates of sleep spindles during human non-rapid eye movement sleep. Proc Natl Acad Sci U S A. 2007Aug7;104(32):13164–9. 17670944
71. Andrade KC, Spoormaker VI, Dresler M, Wehrle R, Holsboer F, Sämann PG, et al. Sleep spindles and hippocampal functional connectivity in human NREM sleep. J Neurosci. 2011Jul13;31(28):10331–9. doi: 10.1523/JNEUROSCI.5660-10.201121753010
72. Beck AT, Epstein N, Brown G, Steer RA, An inventory for measuring clinical anxiety: psychometric properties. J Consult Clin Psychol. 1988Dec;56(6):893–7. 3204199
73. Beck AT, Rial WY, Rickels K, Short form of depression inventory: cross-validation. Psychol Rep. 1974Jun;34(3):1184–6. 4424377
74. Buysse DJ, Reynolds CF, Monk TH, Berman SR, Kupfer DJ, The Pittsburgh sleep quality index: A new instrument for psychiatric practice and research. Psychiatry Res. 1989May;28(2):193–213. 2748771
75. Iber C, Ancoli-Israel S, Chesson AL, Jr.Quan SF, The AASM manual for the scoring of sleep and associated events: Rules, terminology and technical specifications. Westchester, IL: American Academy of Sleep Medicine; 2007. 59 p.
76. Maclean AW, Fekken GC, Saskin P, Knowles JB, Psychometric evaluation of the Stanford Sleepiness Scale. J Sleep Res. 1992Mar;1(1):35–9. 10607023
77. Karni A, Meyer G, Jezzard P, Adams MM, Turner R, Ungerleider LG, Functional MRI evidence for adult motor cortex plasticity during motor skill learning. Nature. 1995Sep14;377(6545):155–8. 7675082
78. Debas K, Carrier J, Orban P, Barakat M, Lungu O, Vandewalle G, et al. Brain plasticity related to the consolidation of motor sequence learning and motor adaptation. Proc Natl Acad Sci U S A. 2010Oct12;107(41):17839–44. doi: 10.1073/pnas.101317610720876115
79. Reis J, Schambra HM, Cohen LG, Buch ER, Fritsch B, Zarahn E, et al. Noninvasive cortical stimulation enhances motor skill acquisition over multiple days through an effect on consolidation. Proc Natl Acad Sci U S A. 2009Feb3;106(5):1590–5. doi: 10.1073/pnas.080541310619164589
80. Dan X, King BR, Doyon J, Chan P, Motor Sequence Learning and Consolidation in Unilateral De Novo Patients with Parkinson’s Disease. PLoS ONE. 2015Jan;10(7):e0134291. doi: 10.1371/journal.pone.013429126222151
81. Rosner B, Percentage Points for a Generalized ESD Many-Outlier Procedure. Technometrics. Taylor & Francis; 1983May;25(2):165–72.
82. NIST/SEMATECH e-Handbook of Statistical Methods [Internet]. 2012 [cited 2014 Jan 1]. http://www.itl.nist.gov/div898/handbook/
83. Laska M, Distel H, Hudson R, Trigeminal perception of odorant quality in congenitally anosmic subjects. Chem Senses. 1997Aug1;22(4):447–56. 9279467
84. Badia P, Wesensten N, Lammers W, Culpepper J, Harsh J, Responsiveness to olfactory stimuli presented in sleep. Physiol Behav. 1990;48(1):87–90. 2236283
85. Arzi A, Sela L, Green A, Givaty G, Dagan Y, Sobel N, The influence of odorants on respiratory patterns in sleep. Chem Senses. 2010Jan1;35(1):31–40. doi: 10.1093/chemse/bjp07919917590
86. Gesser HD, Applied Chemistry: A Textbook for Engineers and Technologists. Springer; 2002. 38 p.
87. Rickard TC, Cai DJ, Rieth CA, Jones J, Ard MC, Sleep does not enhance motor sequence learning. J Exp Psychol Learn Mem Cogn. 2008;34(4):834–42. doi: 10.1037/0278-7393.34.4.83418605872
88. Verwey WB, Evidence for the development of concurrent processing in a sequential keypressing task. Acta Psychol (Amst). 1994May;85(3):245–62.
89. Rechtschaffen A, Kales A, A Manual of Standardized Terminology, Techniques, and Scoring System for Sleep Stage Scoring of Human Subjects. Bethesda, MD; 1968.
90. Walter DO, The method of complex demodulation. Electroencephalogr Clin Neurophysiol. 1968Jan;Suppl 27:53–7. 4184012
91. Mölle M, Marshall L, Gais S, Born J, Grouping of spindle activity during slow oscillations in human non-rapid eye movement sleep. J Neurosci. 2002Dec15;22(24):10941–7. 12486189
92. Suihko V, Malmivuo J, Eskola H, Sensitivity Distribution of Electric Leads in an Inhomogeneous Spherical Head Model. 1993.
93. Nir Y, Staba RJ, Andrillon T, Vyazovskiy V V, Cirelli C, Fried I, et al. Regional slow waves and spindles in human sleep. Neuron. 2011Apr14;70(1):153–69. doi: 10.1016/j.neuron.2011.02.04321482364
94. O’Reilly C, Nielsen T, Assessing EEG sleep spindle propagation. Part 1: Theory and proposed methodology. J Neurosci Methods. Elsevier B.V.; 2014;221:202–14.
95. Ujma PP, Gombos F, Genzel L, Konrad BN, Simor P, Steiger A, et al. A comparison of two sleep spindle detection methods based on all night averages: individually adjusted vs. fixed frequencies. Front Hum Neurosci. 2015Feb17;9:52. doi: 10.3389/fnhum.2015.0005225741264
96. Lunneborg CE, Random assignment of available cases: Bootstrap standard errors and confidence intervals. Psychol Methods. 2001;6(4):402–12. 11778680
97. Hayes AF, Introduction to Mediation, Moderation, and Conditional Process Analysis: A Regression-Based Approach. New York: Guilford Press; 2013. 507 p.
98. Efron B, Better Bootstrap Confidence Intervals. J Am Stat Assoc. Taylor & Francis; 1987Mar;82(397):171–85.