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  • Print publication year: 2013
  • Online publication date: March 2013

Chapter 22 - Memory systems, sleep, and neuroimaging

from Section 4 - Sleep and memory


Although the neurophysiological origin of the functional magnetic resonance imaging (fMRI) blood oxygen level-dependent (BOLD) signal is still poorly understood, spontaneous fMRI signal fluctuations show consistent spatial correlations in functionally related networks. Large-scale functional brain networks as derived from fMRI time-series can be examined by graph theoretical analysis; such analysis has revealed a small-world organization of human functional brain networks during wakefulness, with high local clustering and short path length. A hierarchical cluster analysis indeed illustrated that frontoparietal clusters could be detected in wakefulness but not in deeper non-rapid eye movement (NREM) sleep stages. Functional connectivity of phasic events allows further spatial and temporal refinement of vigilance-state dependent connectivity patterns, and may be of special interest for phasic electroencephalography (EEG) events during sleep. Finally, although functional connectivity appears to overlap to a considerable extent with brain metabolism, these measures seem to represent correlated but different dimensions.


1. DiekelmannS, BornJ. The memory function of sleep. Nat Rev Neurosci. 2010;11:114–26.
2. WalkerMP. A refined model of sleep and the time course of memory formation. Behav Brain Sci. 2005;28:51–64.
3. RotenbergVS. Sleep and memory. II: Investigations on humans. Neurosci Biobehav Rev. 1992;16:503–5.
4. KarniA, TanneD, RubensteinBS, et al. Dependence on REM sleep of overnight improvement of a perceptual skill. Science. 1994;265:679–82.
5. WalkerMP, StickgoldR.Sleep, memory, and plasticity. Annu Rev Psychol. 2006;57:139–66.
6. HeineR.Über wiedererkennen und rückwirkende hemmung. Z Psychol. 1914;68:161–236.
7. Van OrmerEB. Retention after intervals of sleep and waking. Arch Psychol. 1932; 21:1–49.
8. EkstrandBR, BarrettTR, WestJN, et al. The effect of sleep on human long-term memory. In: Drucker-ColinRR, McGaughJL, eds. Neurobiology of Sleep and Memory. New York, Academic Press. 1977;419–38.
9. MaquetP. The role of sleep in learning and memory. Science. 2001;294:1048–52.
10. BuzsákiG.Two-stage model of memory trace formation: a role for “noisy” brain states. Neuroscience. 1989;31:551–70.
11. McClellandJL, McNaughtonBL, O’ReillyRC. 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. 1995;102:419–57.
12. EustonDR, TatsunoM, McNaughtonBL. Fast-forward playback of recent memory sequences in prefrontal cortex during sleep. Science. 2007;318:1147–50.
13. PavlidesC, WinsonJ.Influences of hippocampal place cell firing in the awake state on the activity of these cells during subsequent sleep episodes. J Neurosci. 1989;9:2907–18.
14. MaquetP, LaureysS, PeigneuxP, et al. Experience-dependent changes in cerebral activation during human REM sleep. Nat Neurosci. 2000;3:831–6.
15. PeigneuxP, LaureysS, FuchsS, et al. Learned material content and acquisition level modulate cerebral reactivation during posttraining rapid-eye-movements sleep. Neuroimage. 2003;20:125–34.
16. MaquetP, SchwartzS, PassinghamR, et al. Sleep-related consolidation of a visuomotor skill: brain mechanisms as assessed by functional magnetic resonance imaging. J Neurosci. 2003;23:1432–40.
17. SchwartzS, MaquetP, FrithC.Neural correlates of perceptual learning: a functional MRI study of visual texture discrimination. Proc Natl Acad Sci U S A. 2002;99:17137–42.
18. StickgoldR, JamesL, HobsonJA. Visual discrimination learning requires sleep after training. Nat Neurosci. 2000;3:1237–8.
19. WalkerMP, StickgoldR, JoleszFA, et al. The functional anatomy of sleep-dependent visual skill learning. Cereb Cortex. 2005;15:1666–75.
20. MednickSC, ArmanAC, BoyntonGM. The time course and specificity of perceptual deterioration. Proc Natl Acad Sci U S A. 2005;102:3881–5.
21. WalkerMP, BrakefieldT, MorganA, et al. Practice with sleep makes perfect: sleep-dependent motor skill learning. Neuron. 2002;35:205–11.
22. WalkerMP, StickgoldR, AlsopD, et al. Sleep-dependent motor memory plasticity in the human brain. Neuroscience. 2005;133:911–17.
23. RaschB, BüchelC, GaisS, et al. Odor cues during slow-wave sleep prompt declarative memory consolidation. Science. 2007;315:1426–9.
24. PeigneuxP, LaureysS, FuchsS, et al. Are spatial memories strengthened in the human hippocampus during slow wave sleep?Neuron. 2004;44:535–45.
25. BergmannTO, MolleM, DiedrichsJ, et al. Sleep spindle-related reactivation of category-specific cortical regions after learning face-scene associations. Neuroimage. 2012;59:2733–42.
26. GaisS, MölleM, HelmsK, et al. Learning-dependent increases in sleep spindle density. J Neurosci. 2002;22:6830–4.
27. ClemensZ, MolleM, ErossL, et al. Fine-tuned coupling between human parahippocampal ripples and sleep spindles. Eur J Neurosci. 2011;33:511–20.
28. GirardeauG, ZugaroM.Hippocampal ripples and memory consolidation. Curr Opin Neurobiol. 2011;21:452–9.
29. TakashimaA, PeterssonKM, RuttersF, et al. Declarative memory consolidation in humans: a prospective functional magnetic resonance imaging study. Proc Natl Acad Sci U S A. 2006;103:756–61.
30. FranklandPW, BontempiB.The organization of recent and remote memories. Nat Rev Neurosci. 2005;6:119–30.
31. BosshardtS, DegondaN, SchmidtCF, et al. One month of human memory consolidation enhances retrieval-related hippocampal activity. Hippocampus. 2005;15:1026–40.
32. GaisS, AlbouyG, BolyM, et al. Sleep transforms the cerebral trace of declarative memories. Proc Natl Acad Sci U S A. 2007;104:18778–83.
33. TakashimaA, NieuwenhuisIL, JensenO, et al. Shift from hippocampal to neocortical centered retrieval network with consolidation. J Neurosci. 2009;29:10087–93.
34. van DongenEV, TakashimaA, BarthM, et al. Functional connectivity during light sleep is correlated with memory performance for face-location associations. Neuroimage. 2011;57:262–70.
35. AndradeKC, Spoormaker VI, DreslerM, et al. Sleep spindles and hippocampal functional connectivity in human NREM sleep. J Neurosci. 2011;31:10331–9.
36. OrbanP, RauchsG, BalteauE, et al. Sleep after spatial learning promotes covert reorganization of brain activity. Proc Natl Acad Sci U S A. 2006;103:7124–9.
37. RauchsG, OrbanP, SchmidtC, et al. Sleep modulates the neural substrates of both spatial and contextual memory consolidation. PLoS One. 2008;3:e2949.
38. SterpenichV, AlbouyG, BolyM, et al. Sleep-related hippocampo-cortical interplay during emotional memory recollection. PLoS Biol. 2007;5:e282.
39. SterpenichV, AlbouyG, DarsaudA, et al. Sleep promotes the neural reorganization of remote emotional memory. J Neurosci. 2009;29:5143–52.
40. PayneJD, KensingerEA. Sleep leads to changes in the emotional memory trace: evidence from FMRI. J Cogn Neurosci. 2011;23:1285–97.
41. LoftusE.Our changeable memories: legal and practical implications. Nat Rev Neurosci. 2003;4:231–4.
42. SaletinJM, GoldsteinAN, WalkerMP. The role of sleep in directed forgetting and remembering of human memories. Cereb Cortex. 2011;21:2534–41.
43. RauchsG, FeyersD, LandeauB, et al. Sleep contributes to the strengthening of some memories over others, depending on hippocampal activity at learning. J Neurosci. 2011;31:2563–8.
44. WagnerU, GaisS, HaiderH, et al. Sleep inspires insight. Nature. 2004;427:352–5.
45. DarsaudA, WagnerU, BalteauE, et al. Neural precursors of delayed insight. J Cogn Neurosci. 2011;23:1900–10.
46. CarrMF, JadhavSP, FrankLM. Hippocampal replay in the awake state: a potential substrate for memory consolidation and retrieval. Nat Neurosci. 2011;14:147–53.
47. PeigneuxP, OrbanP, BalteauE, et al. Offline persistence of memory-related cerebral activity during active wakefulness. PLoS Biol. 2006;4:e100.