Memory stabilization with targeted reactivation during human slow-wave sleep

Proceedings of the National Academy of Sciences of the United States of America

Volumn 109, Issue 26, 2012, Pages 10575-10580

  Van Dongen, Eelco V ^a,c   Takashima, Atsuko ^b   Barth, Markus ^a   Zapp, Jascha ^d   Schad, Lothar R ^d   Paller, Ken A ^e   Fernández, Guillén ^a,c  

^a RADBOUD UNIVERSITY   (Netherlands)

^b RADBOUD UNIVERSITY NIJMEGEN   (Netherlands)

^c RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

^d UNIVERSITY OF HEIDELBERG   (Germany)

^e NORTHWESTERN UNIVERSITY   (United States)

Author keywords

Consolidation; EEG functional MRI; Neuroimaging; Replay

Indexed keywords

ADULT; ALERTNESS; ARTICLE; ASSOCIATIVE MEMORY; ATTENTION; BRAIN REGION; CEREBELLUM; CONTROLLED STUDY; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HIPPOCAMPUS; HUMAN; HUMAN EXPERIMENT; LEARNING; MALE; MEMORY; NORMAL HUMAN; OBJECT RELATION; PREFRONTAL CORTEX; PRIORITY JOURNAL; SLOW WAVE SLEEP; SOUND; TEMPORAL LOBE; THALAMUS;

CASE-CONTROL STUDIES; HUMANS; MAGNETIC RESONANCE IMAGING; MEMORY; SLEEP;

EID: 84862976445     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1201072109     Document Type: Article

References (45)

1. McClelland JL, McNaughton BL, O'Reilly RC (1995) Why there are complementary learning systems in the hippocampus and neocortex: Insights from the successes and failures of connectionist models of learning and memory. Psychol Rev 102:419-457.
2. Squire LR, Stark CE, Clark RE (2004) The medial temporal lobe. Annu Rev Neurosci 27:279-306. (Pubitemid 39050405)
3. Frankland PW, Bontempi B (2005) The organization of recent and remote memories. Nat Rev Neurosci 6:119-130. (Pubitemid 40188946)
4. Winocur G, Moscovitch M (2011) Memory transformation and systems consolidation. J Int Neuropsychol Soc 17:766-780.
5. Wilson MA, McNaughton BL (1994) Reactivation of hippocampal ensemble memories during sleep. Science 265:676-679. (Pubitemid 24268281)
6. Diekelmann S, Born J (2010) The memory function of sleep. Nat Rev Neurosci 11:114-126.
7. Ji D, Wilson MA (2007) Coordinated memory replay in the visual cortex and hippocampus during sleep. Nat Neurosci 10:100-107. (Pubitemid 46026533)
8. Euston DR, Tatsuno M, McNaughton BL (2007) Fast-forward playback of recent memory sequences in prefrontal cortex during sleep. Science 318:1147-1150. (Pubitemid 350134899)
9. Maquet P, et al. (2000) Experience-dependent changes in cerebral activation during human REM sleep. Nat Neurosci 3:831-836. (Pubitemid 30485710)
10. Peigneux P, et al. (2004) Are spatial memories strengthened in the human hippo-campus during slow wave sleep? Neuron 44:535-545. (Pubitemid 39423353)
11. Rasch B, Büchel C, Gais S, Born J (2007) Odor cues during slow-wave sleep prompt declarative memory consolidation. Science 315:1426-1429. (Pubitemid 46399554)
12. Rudoy JD, Voss JL, Westerberg CE, Paller KA (2009) Strengthening individual memories by reactivating them during sleep. Science 326:1079.
13. Diekelmann S, Büchel C, Born J, Rasch B (2011) Labile or stable: Opposing consequences for memory when reactivated during waking and sleep. Nat Neurosci 14:381-386.
14. Stickgold R (2007) Of sleep, memories and trauma. Nat Neurosci 10:540-542.
15. Hasson U, Nusbaum HC, Small SL (2009) Task-dependent organization of brain regions active during rest. Proc Natl Acad Sci USA 106:10841-10846.
16. Stevens WD, Buckner RL, Schacter DL (2010) Correlated low-frequency BOLD fluctuations in the resting human brain are modulated by recent experience in categorypreferential visual regions. Cereb Cortex 20:1997-2006.
17. Tambini A, Ketz N, Davachi L (2010) Enhanced brain correlations during rest are related to memory for recent experiences. Neuron 65:280-290.
18. van Dongen EV, Takashima A, Barth M, Fernández G (2011) Functional connectivity during light sleep is correlated with memory performance for face-location associations. Neuroimage 57:262-270.
19. Steriade M, Llinás RR (1988) The functional states of the thalamus and the associated neuronal interplay. Physiol Rev 68:649-742.
20. Briggs F, Usrey WM (2008) Emerging views of corticothalamic function. Curr Opin Neurobiol 18:403-407.
21. Steriade M (2003) The corticothalamic system in sleep. Front Biosci 8:d878-d899.
22. Sirota A, Csicsvari J, Buhl D, Buzsáki G (2003) Communication between neocortex and hippocampus during sleep in rodents. Proc Natl Acad Sci USA 100:2065-2069. (Pubitemid 36254574)
23. Steriade M, Timofeev I (2003) Neuronal plasticity in thalamocortical networks during sleep and waking oscillations. Neuron 37:563-576. (Pubitemid 36262979)
24. Marshall L, Born J (2007) The contribution of sleep to hippocampus-dependent memory consolidation. Trends Cogn Sci 11:442-450. (Pubitemid 47588990)
25. Mölle M, Born J (2009) Hippocampus whispering in deep sleep to prefrontal cortex -for good memories? Neuron 61:496-498.
26. Dinges DF, Powell JW (1985) Microcomputer analyses of performance on a portable, simple visual RT task during sustained operations. Behav Res Methods Instrum Comput 17:652-655.
27. Issa EB, Wang X (2008) Sensory responses during sleep in primate primary and secondary auditory cortex. J Neurosci 28:14467-14480.
28. Issa EB, Wang X (2011) Altered neural responses to sounds in primate primary auditory cortex during slow-wave sleep. J Neurosci 31:2965-2973.
29. Steele CJ, Penhune VB (2010) Specific increases within global decreases: A functional magnetic resonance imaging investigation of five days of motor sequence learning. J Neurosci 30:8332-8341.
30. Debas K, et al. (2010) Brain plasticity related to the consolidation of motor sequence learning and motor adaptation. Proc Natl Acad Sci USA 107:17839-17844.
31. Lewis PA, Couch TJ, Walker MP (2011) Keeping time in your sleep: Overnight consolidation of temporal rhythm. Neuropsychologia 49:115-123.
32. Clark RE (2011) Eyeblink conditioning and systems consolidation: An ironic yet powerful pairing. Neurobiol Learn Mem 95:118-124.
33. Takashima A, et al. (2007) Memory trace stabilization leads to large-scale changes in the retrieval network: A functional MRI study on associative memory. Learn Mem 14:472-479. (Pubitemid 47204845)
34. Sterpenich V, et al. (2009) Sleep promotes the neural reorganization of remote emotional memory. J Neurosci 29:5143-5152.
35. Cavanna AE, Trimble MR (2006) The precuneus: A review of its functional anatomy and behavioural correlates. Brain 129:564-583. (Pubitemid 43278220)
36. Takashima A, et al. (2006) Declarative memory consolidation in humans: A prospective functional magnetic resonance imaging study. Proc Natl Acad Sci USA 103:756-761. (Pubitemid 43153098)
37. Restivo L, Vetere G, Bontempi B, Ammassari-Teule M (2009) The formation of recent and remote memory is associated with time-dependent formation of dendritic spines in the hippocampus and anterior cingulate cortex. J Neurosci 29:8206-8214.
38. van Kesteren MT, Fernández G, Norris DG, Hermans EJ (2010) Persistent schema-dependent hippocampal-neocortical connectivity during memory encoding and postencoding rest in humans. Proc Natl Acad Sci USA 107:7550-7555.
39. Leon WC, Bruno MA, Allard S, Nader K, Cuello AC (2010) Engagement of the PFC in consolidation and recall of recent spatial memory. Learn Mem 17:297-305.
40. Tse D, et al. (2011) Schema-dependent gene activation and memory encoding in neocortex. Science 333:891-895.
41. Steriade M (1991) Alertness, quiet sleep, dreaming. Cerebral Cortex ed Peters AJ, (Plenum, New York), Vol 9, pp 279-357.
42. Dang-Vu TT, McKinney SM, Buxton OM, Solet JM, Ellenbogen JM (2010) Spontaneous brain rhythms predict sleep stability in the face of noise. Curr Biol 20:R626-R627.
43. Dang-Vu TT, et al. (2011) Interplay between spontaneous and induced brain activity during human non-rapid eye movement sleep. Proc Natl Acad Sci USA 108:15438-15443.
44. Schmitter S, et al. (2008) Silent echo-planar imaging for auditory FMRI. MAGMA 21:317-325.
45. Iber C, Ancoli-Israel S, Chesson A, Quan SF (2007) The AASM Manual for the Scoring of Sleep and Associated Events: Rules, Terminology and Technical Specifications (Am Acad Sleep Med, Westchester, IL).