Abstract
The human brain faces a fundamental information storage challenge—forming useful new memories while not over-writing important old ones. Memory consolidation, and the corresponding interplay between the hippocampus and neocortex, is a protracted process to adjudicate between these two competing factors. Converging evidence from behavioral, cellular, and systems neuroscience strongly implicates a special role for sleep in stabilizing new declarative memories. In this chapter, we review evidence that during sleep the reactivation of newly acquired neuronal traces has lasting implications for memory transformation and stabilization. We first summarize relevant theoretical issues in memory research and then outline the physiological properties of sleep that may allow for this reactivation. We consider many factors that affect spontaneous memory reactivation, and we highlight research showing that memories can be selectively targeted and modified using learning-related stimuli. Ultimately, the ability to rescue otherwise fleeting episodes from oblivion plays a vital role in human life. Research elucidating this ability will also be critical for understanding how memory breaks down in aging and disease.
This is a preview of subscription content, log in via an institution.
Buying options
Tax calculation will be finalised at checkout
Purchases are for personal use only
Learn about institutional subscriptionsReferences
Adcock RA, Thangavel A, Whitfield-Gabrieli S, Knutson B, Gabrieli JDE (2006) Reward-motivated learning: mesolimbic activation precedes memory formation. Neuron 50(3):507–517. doi:10.1016/j.neuron.2006.03.036
Albouy G, King BR, Maquet P, Doyon J (2013) Hippocampus and striatum: dynamics and interaction during acquisition and sleep-related motor sequence memory consolidation. Hippocampus 23(11):985–1004. doi:10.1002/hipo.22183
Antony JW, Gobel EW, O’Hare JK, Reber PJ, Paller KA (2012) Cued memory reactivation during sleep influences skill learning. Nat Neurosci 15(8):1114–1116. doi:10.1038/nn.3152
Atherton LA, Dupret D, Mellor JR (2015) Memory trace replay: the shaping of memory consolidation by neuromodulation. Trends Neurosci 38(9):560–570. doi:10.1016/j.tins.2015.07.004
Atienza M, Cantero JL (2008) Modulatory effects of emotion and sleep on recollection and familiarity. J Sleep Res 17:285–294. doi:10.1111/j.1365-2869.2008.00661.x
Ayoub A, Mölle M, Preissl H, Born J (2012) Grouping of MEG gamma oscillations by EEG sleep spindles. NeuroImage 59(2):1491–1500. doi:10.1016/j.neuroimage.2011.08.023
Barakat M, Doyon J, Debas K, Vandewalle G, Morin A, Poirier G et al (2011) Fast and slow spindle involvement in the consolidation of a new motor sequence. Behav Brain Res 217(1):117–121
Baran B, Pace-Schott EF, Ericson C, Spencer RMC (2012) Processing of emotional reactivity and emotional memory over sleep. J Neurosci 32(3):1035–1042. doi:10.1523/JNEUROSCI.2532-11.2012
Baran B, Daniels D, Spencer RMC (2013) Sleep-dependent consolidation of value-based learning. PLoS One 8(10):e75326. doi:10.1371/journal.pone.0075326
Barnes DC, Wilson DA (2014) Slow-wave sleep-imposed replay modulates both strength and precision of memory. J Neurosci 34(15):5134–5142. doi:10.1523/JNEUROSCI.5274-13.2014
Batterink LJ, Paller KA (2015) Sleep-based memory processing facilitates grammatical generalization: evidence from targeted memory reactivation. Brain Lang. Available online Oct 3, 2015 [Epub ahead of print]. doi:10.1016/j.bandl.2015.09.003
Batterink LJ, Oudiette D, Reber PJ, Paller KA (2014) Sleep facilitates learning a new linguistic rule. Neuropsychologia 65(2014):169–179. doi:10.1016/j.neuropsychologia.2014.10.024
Behrens CJ, van den Boom LP, de Hoz L, Friedman A, Heinemann U (2005) Induction of sharp wave-ripple complexes in vitro and reorganization of hippocampal networks. Nat Neurosci 8(11):1560–1567. doi:10.1038/nn1571
Benchenane K, Peyrache A, Khamassi M, Tierney PL, Gioanni Y, Battaglia FP, Wiener SI (2010) Coherent theta oscillations and reorganization of spike timing in the hippocampal-prefrontal network upon learning. Neuron 66(6):921–936. doi:10.1016/j.neuron.2010.05.013
Bendor D, Wilson MA (2012) Biasing the content of hippocampal replay during sleep. Nat Neurosci 15(10):1439–1444. doi:10.1038/nn.3203
Bennion KA, Mickley Steinmetz KR, Kensinger EA, Payne JD (2015) Sleep and cortisol interact to support memory consolidation. Cereb Cortex 25(3):646–657
Benson K, Feinberg I (1977) The beneficial effect of sleep in an extended Jenkins and Dallenbach paradigm. Psychophysiology 14(4):375–384
Ben-Yakov A, Eshel N, Dudai Y (2013) Hippocampal immediate poststimulus activity in the encoding of consecutive naturalistic episodes. J Exp Psychol Gen 142(4):1255–1263. doi:10.1037/a0033558
Bergmann TO, Mölle M, Diedrichs J, Born J, Siebner HR (2012) Sleep spindle-related reactivation of category-specific cortical regions after learning face-scene associations. NeuroImage 59(3):2733–2742
Berry JA, Cervantes-Sandoval I, Chakraborty M, Davis RL (2015) Sleep facilitates memory by blocking dopamine neuron-mediated forgetting. Cell 161(7):1656–1667. doi:10.1016/j.cell.2015.05.027
Bethus I, Tse D, Morris RGM (2010) Dopamine and memory: modulation of the persistence of memory for novel hippocampal NMDA receptor-dependent paired associates. J Neurosci 30(5):1610–1618. doi:10.1523/JNEUROSCI.2721-09.2010
Bódizs R, Körmendi J, Rigó P, Lázár AS (2009) The individual adjustment method of sleep spindle analysis: methodological improvements and roots in the fingerprint paradigm. J Neurosci Methods 178(1):205–213
Born J, Wilhelm I (2012) System consolidation of memory during sleep. Psychol Res 76(2):192–203
Brain R (1958) The physiological basis of consciousness: a critical review. Brain 81(3):426–455. doi:10.1093/brain/81.3.426
Brawn TP, Fenn KM, Nusbaum HC, Margoliash D (2010a) Consolidating the effects of waking and sleep on motor-sequence learning. J Neurosci 30(42):13977–13982. doi:10.1523/JNEUROSCI.3295-10.2010
Brawn TP, Nusbaum HC, Margoliash D (2010b) Sleep-dependent consolidation of auditory discrimination learning in adult starlings. J Neurosci 30(2):609–613. doi:10.1523/JNEUROSCI.4237-09.2010
Brawn TP, Nusbaum HC, Margoliash D (2013) Sleep consolidation of interfering auditory memories in starlings. Psychol Sci 24(4):439–447. doi:10.1177/0956797612457391
Bremer F (1954) The neurophysiological problem of sleep. In: Adrian E, Bremer F, Japser H (eds) Brain mechanisms and consciousness. Blackwell, Oxford, pp 137–162
Buchegger J, Meier-Koll A (1988) Motor learning and ultradian sleep cycle: an electroencephalographic study of trampoliners. Percept Mot Skills 67(1972):635–645
Buchsbaum BR, Lemire-Rodger S, Fang C, Abdi H (2012) The neural basis of vivid memory is patterned on perception. J Cogn Neurosci 24(9):1867–1883
Buzsaki G (1984) Long-term changes of hippocampal sharp-waves following high frequency afferent activation. Brain Res 300(1):179–182. doi:10.1016/0006-8993(84)91356-8
Buzsaki G (1986) Hippocampal sharp waves: their origin and significance. Brain Res 398:242–252
Buzsaki G (1989) Two-stage model of memory trace formation: a role for “noisy” brain states. Neuroscience 31(3):551–570
Buzsáki G, Lai-Wo SL, Vanderwolf CH (1983) Cellular bases of hippocampal EEG in the behaving rat. Brain Res Rev 6(2):139–171. doi:10.1016/0165-0173(83)90037-1
Buzsáki G, Logothetis N, Singer W (2013) Scaling brain size, keeping timing: evolutionary preservation of brain rhythms. Neuron 80(3):751–764. doi:10.1016/j.neuron.2013.10.002
Cahill L, Haiert RJ, Fallon J, Alkirei MT, Tangii C, Keatorii D et al (1996) Amygdala activity at encoding correlated with long-term, free recall of emotional information. Proc Natl Acad Sci USA 93:8016–8021
Cai DJ, Mednick SA, Harrison EM, Kanady JC, Mednick SC (2009) REM, not incubation, improves creativity by priming associative networks. Proc Natl Acad Sci 106(25):10130–10134
Cairney SA, Durrant SJ, Power R, Lewis PA (2015) Complementary roles of slow-wave sleep and rapid eye movement sleep in emotional memory consolidation. Cereb Cortex 25(6):1565–1575. doi:10.1093/cercor/bht349
Canli T, Zhao Z, Brewer J, Gabrieli JD, Cahill L (2000) Event-related activation in the human amygdala associates with later memory for individual emotional experience. J Neurosci 20(19):RC99 20004570 [pii]
Carr MF, Jadhav SP, Frank LM (2011) Hippocampal replay in the awake state: a potential substrate for memory consolidation and retrieval. Nat Neurosci 14(2):147–153. doi:10.1038/nn.2732
Cash SS, Halgren E, Dehghani N, Rossetti AO, Thesen T, Wang C et al (2009) The human K-complex represents an isolated cortical down-state. Science 324(5930):1084–1087. doi:10.1126/science.1169626
Chrobak JJ, Buzsáki G (1994) Selective activation of deep layer (V-VI) retrohippocampal cortical neurons during hippocampal sharp waves in the behaving rat. J Neurosci 14(10):6160–6170
Cirelli C, Tononi G (2008) Is sleep essential? PLoS Biol 6(8):1605–1611
Clemens Z, Fabó D, Halász P (2005) Overnight verbal memory retention correlates with the number of sleep spindles. Neuroscience 132(2):529–535
Clemens Z, Fabó D, Halász P (2006) Twenty-four hours retention of visuospatial memory correlates with the number of parietal sleep spindles. Neurosci Lett 403(1-2):52–56
Clemens Z, Mölle M, Eross L, Barsi P, Halász P, Born J (2007) Temporal coupling of parahippocampal ripples, sleep spindles and slow oscillations in humans. Brain 130:2868–2878
Cohen DA, Pascual-Leone A, Press DZ, Robertson EM (2005) Off-line learning of motor skill memory: a double dissociation of goal and movement. Proc Natl Acad Sci USA 102(50):18237–18241. doi:10.1073/pnas.0506072102
Corkin S (2013) Permanent present tense. Basic Books, New York, NY
Cote K, Epps T, Campbell K (2000) The role of the spindle in human information processing of high-intensity stimuli during sleep. J Sleep Res 9:19–26
Cousins JN, El-Deredy W, Parkes LM, Hennies N, Lewis PA (2014) Cued memory reactivation during slow-wave sleep promotes explicit knowledge of a motor sequence. J Neurosci 34(48):15870–15876. doi:10.1523/JNEUROSCI.1011-14.2014
Cox R, Hofman WF, Talamini LM (2012) Involvement of spindles in memory consolidation is slow wave sleep-specific. Learn Mem 19(7):264–267
Cox R, Hofman WF, de Boer M, Talamini LM (2014) Local sleep spindle modulations in relation to specific memory cues. NeuroImage 99:103–110 Retrieved from http://www.ncbi.nlm.nih.gov/pubmed/24852461
Craig M, Dewar M, Della Sala S, Wolbers T (2015a) Rest boosts the long-term retention of spatial associative and temporal order information. Hippocampus 25:1017–1027. doi:10.1002/hipo.22424
Craig M, Dewar M, Harris MA, Della Sala S, Wolbers T (2015b) Wakeful rest promotes the integration of spatial memories into accurate cognitive maps. Hippocampus. doi:10.1002/hipo.22502
Creery JD, Oudiette D, Antony JW, Paller KA (2014) Targeted memory reactivation during sleep depends on prior learning. Sleep 38(5):755–763 Retrieved from http://www.ncbi.nlm.nih.gov/pubmed/25515103
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(15):R626–R627
Dang-Vu TT, Bonjean M, Schabus M, Boly M, Darsaud A, Desseilles M et al (2011) Interplay between spontaneous and induced brain activity during human non-rapid eye movement sleep. Proc Natl Acad Sci USA 108(37):15438–15443
Dave A, Margoliash D (2000) Song replay during sleep and computational rules for sensorimotor vocal learning. Science 290(5492):812–816. doi:10.1126/science.290.5492.812
Davidson TJ, Kloosterman F, Wilson MA (2009) Hippocampal replay of extended experience. Neuron 63(4):497–507. doi:10.1016/j.neuron.2009.07.027
de Gennaro L, Ferrara M (2003) Sleep spindles: an overview. Sleep Med Rev 7(5):423–440
de Lavilléon G, Lacroix MM (2015) Explicit memory creation during sleep demonstrates a causal role of place cells in navigation. Nat Neurosci 18:493–495. doi:10.1038/nn.3970
Dement W (1960) The effect of dream deprivation. Science 131(3415):1705–1707. doi:10.1126/science.131.3415.1705
Deuker L, Olligs J, Fell J, Kranz TA, Mormann F, Montag C et al (2013) Memory consolidation by replay of stimulus-specific neural activity. J Neurosci 33(49):19373–19383. doi:10.1523/JNEUROSCI.0414-13.2013
Dewar M, Alber J, Butler C, Cowan N, Della Sala S (2012) Brief wakeful resting boosts new memories over the long term. Psychol Sci 23(9):955–960. doi:10.1177/0956797612441220
Diba K, Buzsáki G (2007) Forward and reverse hippocampal place-cell sequences during ripples. Nat Neurosci 10(10):1241–1242. doi:10.1038/nn1961
Diekelmann S, Born J (2010) The memory function of sleep. Nat Rev Neurosci 11(2):114–126
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(3):381–386. doi:10.1038/nn.2744
Diekelmann S, Biggel S, Rasch B, Born J (2012) Offline consolidation of memory varies with time in slow wave sleep and can be accelerated by cuing memory reactivations. Neurobiol Learn Mem 98(2):103–111. doi:10.1016/j.nlm.2012.07.002
Djonlagic I, Rosenfeld A, Shohamy D, Djonlagic I, Rosenfeld A, Shohamy D, Myers C, Gluck M, Stickgold R (2009) Sleep enhances category learning. Learn Mem 16:751–755
Dolcos F, Labar KS, Cabeza R (2004) Interaction between the amygdala and the medial temporal lobe memory system predicts better memory for emotional events. Neuron 42:855–863
Dunsmoor JE, Murty VP, Davachi L, Phelps EA (2015) Emotional learning selectively and retroactively strengthens memories for related events. Nature 520:345–348. doi:10.1038/nature14106
Dupret D, O’Neill J, Pleydell-Bouverie B, Csicsvari J (2010) The reorganization and reactivation of hippocampal maps predict spatial memory performance. Nat Neurosci 13(8):995–1002. doi:10.1038/nn.2599
Durrant SJ, Taylor C, Cairney S, Lewis PA (2011) Sleep-dependent consolidation of statistical learning. Neuropsychologia 49(5):1322–1331. doi:10.1016/j.neuropsychologia.2011.02.015
Ebbinghaus H (1885) Memory: a contribution to experimental psychology. Columbia University Press, New York
Ego-Stengel V, Wilson MA (2009) Disruption of ripple-associated hippocampal activity during rest impairs spatial learning in the rat. Hippocampus 20(1):1–10. doi:10.1002/hipo.20707
Ellenbogen JM, Hulbert JC, Stickgold R, Dinges DF, Thompson-Schill SL (2006) Interfering with theories of sleep and memory: sleep, declarative memory, and associative interference. Curr Biol 16(13):1290–1294. doi:10.1016/j.cub.2006.05.024
Empson J, Clarke P (1970) Rapid eye movements and remembering. Nature 227:287–288
Eschenko O, Mölle M, Born J, Sara SJ (2006) Elevated sleep spindle density after learning or after retrieval in rats. J Neurosci 26(50):12914–12920
Eschenko O, Ramadan W, Mölle M, Born J, Sara S (2008) Sustained increase in hippocampal sharp-wave ripple activity during slow-wave sleep after learning. Learn Mem 15:222–228
Euston DR, Tatsuno M, McNaughton BL (2007) Fast-forward playback of recent memory sequences in prefrontal cortex during sleep. Science 318(5853):1147–1150. doi:10.1126/science.1148979
Feld GB, Besedovsky L, Kaida K, Münte TF, Born J (2014) Dopamine D2-like receptor activation wipes out preferential consolidation of high over low reward memories during human sleep. J Cogn Neurosci 26(10):2310–2320. doi:10.1162/jocn
Fenn KM, Hambrick DZ (2012) Individual differences in working memory capacity predict sleep-dependent memory consolidation. J Exp Psychol Gen 141(3):404–410. doi:10.1037/a0025268
Fenn KM, Hambrick DZ (2015) General intelligence predicts memory change across sleep. Psychon Bull Rev 22(3):791–799. doi:10.3758/s13423-014-0731-1
Fenn KM, Nusbaum HC, Margoliash D (2003) Consolidation during sleep of perceptual learning of spoken language. Nature 425:614–616. doi:10.1038/nature01971.1
Fischer S, Born J (2009) Anticipated reward enhances offline learning during sleep. J Exp Psychol Learn Mem Cogn 35(6):1586–1593. doi:10.1037/a0017256
Fischer S, Hallschmid M, Elsner AL, Born J (2002) Sleep forms memory for finger skills. Proc Natl Acad Sci USA 99(18):11987–11991
Fischer S, Diekelmann S, Born J (2011) Sleep’s role in the processing of unwanted memories. J Sleep Res 20(2):267–274. doi:10.1111/j.1365-2869.2010.00881.x
Fishbein W (1971) Disruptive effects of rapid eye movement sleep deprivation on long-term memory. Physiol Behav 6(1):279–282
Fogel SM, Smith CT (2006) Learning-dependent changes in sleep spindles and Stage 2 sleep. J Sleep Res 15:250–255
Fosse R, Stickgold R, Hobson JA (2001) The mind in REM sleep: reports of emotional experience. Sleep 24(8):947–955 Retrieved from http://www.ncbi.nlm.nih.gov/pubmed/11766165
Frank MG, Issa NP, Stryker MP (2001) Sleep enhances plasticity in the developing visual cortex. Neuron 30:275–287
Freud S (1913) The interpretation of dreams. Macmillan, New York, NY
Fuentemilla L, Miró J, Ripollés P, Vilà-Balló A, Juncadella M, Castañer S et al (2013) Hippocampus-dependent strengthening of targeted memories via reactivation during sleep in humans. Curr Biol 23(18):1769–1775. doi:10.1016/j.cub.2013.07.006
Gaab N, Paetzold M, Becker M, Walker MP, Schlaug G (2004) The influence of sleep on auditory learning: a behavioral study. NeuroReport 15(4):731–734. doi:10.1097/01.wnr.0000113532.32218.d6
Gais S, Born J (2004) Declarative memory consolidation: mechanisms acting during human sleep. Learn Mem 11(6):679–685. doi:10.1101/lm.80504
Gais S, Plihal W, Wagner U, Born J (2000) Early sleep triggers memory for early visual discrimination skills. Nat Neurosci 3(12):1335–1339
Gais S, Mo M, Helms K, Born J (2002) Learning-dependent increases in sleep spindle density. J Neurosci 22(15):6830–6834
Gais S, Lucas B, Born J (2006) Sleep after learning aids memory recall. Learn Mem 13(3):259–262. doi:10.1101/lm.132106
Gelbard-Sagiv H, Mukamel R, Harel M, Malach R, Fried I (2008) Internally generated reactivation of single neurons in human hippocampus during free recall. Science 322(5898):96–101. doi:10.1126/science.1164685
Genzel L, Kroes MCW, Dresler M, Battaglia FP (2013) Light sleep versus slow wave sleep in memory consolidation: a question of global versus local processes? Trends Neurosci 37(1):1–10. doi:10.1016/j.tins.2013.10.002
Girardeau G, Benchenane K, Wiener SI, Buzsáki G, Zugaro MB (2009) Selective suppression of hippocampal ripples impairs spatial memory. Nat Neurosci 12(10):1222–1223. doi:10.1038/nn.2384
Godden D, Baddeley A (1975) Context-dependent memory in two natural environments: on land and underwater. Br J Psychol 66(3):325–331
Gómez RL, Bootzin RR, Nadel L (2006) Naps promote abstraction in language-learning infants. Psychol Sci 17(8):670–674. doi:10.1111/j.1467-9280.2006.01764.x
Guerrien A, Dujardin K, Mandai O, Sockeel P, Leconte P (1989) Enhancement of memory by auditory stimulation during postlearning REM sleep in humans. Physiol Behav 45:947–950
Gulati T, Ramanathan DS, Wong CC, Ganguly K (2014) Reactivation of emergent task-related ensembles during slow-wave sleep after neuroprosthetic learning. Nat Neurosci 17(8):1107–1113. doi:10.1038/nn.3759
Hars B, Hennevin E (1990) Reactivation of an old memory during sleep and wakefulness. Anim Learn Behav 18(4):365–376
Hars B, Hennevin E, Pasques P (1985) Improvement of learning by cueing during postlearning paradoxical sleep. Behav Brain Res 18:241–250
Hartse KM, Eisenhart SF, Bergmann BM, Rechtschaffen A (1979) Ventral hippocampus spikes during sleep, wakefulness, and arousal in the cat. Sleep 1(3):231–246
Hasselmo ME, McGaughy J (2004) High acetylcholine levels set circuit dynamics for attention and encoding and low acetylcholine levels set dynamics for consolidation. Prog Brain Res 145:207–231. doi:10.1016/S0079-6123(03)45015-2
Hauner KK, Howard JD, Zelano C, Gottfried JA (2013) Stimulus-specific enhancement of fear extinction during slow-wave sleep. Nat Neurosci 16(11):1553–1555. doi:10.1038/nn.3527
Heib DPJ, Hoedlmoser K, Anderer P, Gruber G, Zeitlhofer J, Schabus M (2015) Oscillatory theta activity during memory formation and its impact on overnight consolidation: a missing link? J Cogn Neurosci 27(8):1648–1658. doi:10.1162/jocn
Hennevin E, Hars B (1987) Is increase in post-learning paradoxical sleep modified by cueing? Behav Brain Res 24(3):243–249
Hoffman K, McNaughton B (2002) Coordinated reactivation of distributed memory traces in primate neocortex. Science 297:2070–2073
Hu P, Stylos-Allan M, Walker MP (2006) Sleep facilitates consolidation of emotional declarative memory. Psychol Sci 17(10):891–898
Hu X, Antony JW, Creery JD, Vargas IM, Bodenhausen GV, Paller KA (2015) Unlearning implicit social biases during sleep. Science 348(6238):1013–1015
Huber R, Ghilardi MF, Massimini M, Tononi G (2004) Local sleep and learning. Nature 430:78–81
Jadhav SP, Kemere C, German PW, Frank LM (2012) Awake hippocampal sharp-wave ripples support spatial memory. Science 336(6087):1454–1458. doi:10.1126/science.1217230
Jenkins J, Dallenbach K (1924) Obliviscence during sleep and waking. Am J Psychol 35(4):605–612
Jensen LC, Harris K, Anderson DC (1971) Retention following a change in ambient contextual stimuli for six age groups. Dev Psychol 4(3):394–399. doi:10.1037/h0030957
Ji D, Wilson MA (2007) Coordinated memory replay in the visual cortex and hippocampus during sleep. Nat Neurosci 10(1):100–107. doi:10.1038/nn1825
Johnson JD, Rugg MD (2007) Recollection and the reinstatement of encoding-related cortical activity. Cereb Cortex 17(11):2507–2515. doi:10.1093/cercor/bhl156
Johnson JD, McDuff SGR, Rugg MD, Norman KA (2009) Recollection, familiarity, and cortical reinstatement: a multivoxel pattern analysis. Neuron 63(5):697–708. doi:10.1016/j.neuron.2009.08.011
Johnson L, Blakely T, Hermes D, Hakimian S, Ramsey N, Ojemann J (2012) Sleep spindles are locally modulated by training on a brain-computer interface. Proc Natl Acad Sci USA 109(45):18583–18588
Kaestner EJ, Wixted JT, Mednick SC (2013) Pharmacologically increasing sleep spindles enhances recognition for negative and high-arousal memories. J Cogn Neurosci 25(10):1597–1610
Karlsson MP, Frank LM (2009) Awake replay of remote experiences in the hippocampus. Nat Neurosci 12(7):913–918. doi:10.1038/nn.2344
Karlsson Wirebring L, Wiklund-Hornqvist C, Eriksson J, Andersson M, Jonsson B, Nyberg L (2015) Lesser neural pattern similarity across repeated tests is associated with better long-term memory retention. J Neurosci 35(26):9595–9602. doi:10.1523/JNEUROSCI.3550-14.2015
Karni A, Tanne D, Rubenstein B, Askenasy J, Sagi D (1994) Dependence on REM sleep of overnight improvement of a perceptual skill. Science 265:679–682
Korman M, Doyon J, Doljansky J, Carrier J, Dagan Y, Karni A (2007) Daytime sleep condenses the time course of motor memory consolidation. Nat Neurosci 10(9):1206–1213. doi:10.1038/nn1959
Kudrimoti HS, Barnes CA, Mcnaughton BL (1999) Reactivation of hippocampal cell assemblies: effects of behavioral state, experience, and EEG dynamics. J Neurosci 19(10):4090–4101
Kuhl BA, Shah AT, DuBrow S, Wagner AD (2010) Resistance to forgetting associated with hippocampus-mediated reactivation during new learning. Nat Neurosci 13(4):501–506. doi:10.1038/nn.2498
Kuhl BA, Bainbridge WA, Chun MM (2012a) Neural reactivation reveals mechanisms for updating memory. J Neurosci 32(10):3453–3461. doi:10.1523/JNEUROSCI.5846-11.2012
Kuhl BA, Rissman J, Wagner AD (2012b) Multi-voxel patterns of visual category representation during episodic encoding are predictive of subsequent memory. Neuropsychologia 50(4):458–469. doi:10.1016/j.neuropsychologia.2011.09.002
Kurdziel L, Duclos K, Spencer RMC (2013) Sleep spindles in midday naps enhance learning in preschool children. Proc Natl Acad Sci USA 110(43):17267–17272. doi:10.1073/pnas.1306418110
Kuriyama K, Stickgold R, Walker MP (2004) Sleep-dependent learning and motor-skill complexity. Learn Mem 11:705–713. doi:10.1101/lm.76304.appears
LaBar KS, Cabeza R (2006) Cognitive neuroscience of emotional memory. Nat Rev Neurosci 7(1):54–64. doi:10.1038/nrn1825
Landsness EC, Crupi D, Hulse BK, Peterson MJ, Huber R, Ansari H et al (2009) Sleep-dependent improvement in visuomotor learning: a causal role for slow waves. Sleep 32(10):1273–1284
Lansink CS, Goltstein PM, Lankelma JV, Joosten RNJMA, McNaughton BL, Pennartz CMA (2008) Preferential reactivation of motivationally relevant information in the ventral striatum. J Neurosci 28(25):6372–6382. doi:10.1523/JNEUROSCI.1054-08.2008
Lansink CS, Goltstein PM, Lankelma JV, McNaughton BL, Pennartz CMA (2009) Hippocampus leads ventral striatum in replay of place-reward information. PLoS Biol 7(8):e1000173. doi:10.1371/journal.pbio.1000173
Lany J, Gómez RL (2008) Twelve-month-old infants benefit from prior experience in statistical learning. Psychol Sci 19(12):1247–1252. doi:10.1111/j.1467-9280.2008.02233.x
Lechner H, Squire L, Byrne J (1999) 100 years of consolidation—remembering Müller and Pilzecker. Learn Mem 6:77–88
Lehmann H, McNamara KC (2011) Repeatedly reactivated memories become more resistant to hippocampal damage. Learn Mem 18(3):132–135. doi:10.1101/lm.2000811
Lehmann H, Sparks FT, Spanswick SC, Hadikin C, McDonald RJ, Sutherland RJ (2009) Making context memories independent of the hippocampus. Learn Mem 16(7):417–420. doi:10.1101/lm.1385409
Lesburguères E, Gobbo OL, Alaux-Cantin S, Hambucken A, Trifilieff P, Bontempi B (2011) Early tagging of cortical networks is required for the formation of enduring associative memory. Science 331(6019):924–928. doi:10.1126/science.1196164
Lewis PA, Cairney S, Manning L, Critchley HD (2011) The impact of overnight consolidation upon memory for emotional and neutral encoding contexts. Neuropsychologia 49:2619–2629. doi:10.1016/j.neuropsychologia.2011.05.009
Lisman JE, Grace AA (2005) The hippocampal-VTA loop: controlling the entry of information into long-term memory. Neuron 46(5):703–713. doi:10.1016/j.neuron.2005.05.002
Louie K, Wilson MA (2001) Temporally structured replay of awake hippocampal ensemble activity during rapid eye movement sleep. Neuron 29(1):145–156. doi:10.1016/S0896-6273(01)00186-6
Mandai O, Guerrien A, Sockeel P, Dujardin K, Leconte P (1989) REM sleep modifications following a Morse code learning session in humans. Physiol Behav 46(4):639–642. doi:10.1016/0031-9384(89)90344-2
Mander BA, Santhanam S, Saletin JM, Walker MP (2011) Wake deterioration and sleep restoration of human learning. Curr Biol 21(5):R183–R184. doi:10.1016/j.cub.2011.01.019
Manning JR, Sperling MR, Sharan A, Rosenberg EA, Kahana MJ (2012) Spontaneously reactivated patterns in frontal and temporal lobe predict semantic clustering during memory search. J Neurosci 32(26):8871–8878. doi:10.1523/JNEUROSCI.5321-11.2012
Manoach DS, Thakkar KN, Stroynowski E, Ely A, McKinley SK, Wamsley E et al (2009) Reduced overnight consolidation of procedural learning in chronic medicated schizophrenia is related to specific sleep stages. J Psychiatr Res 44(2):112–120. doi:10.1016/j.jpsychires.2009.06.011
Maquet P, Péters J, Aerts J, Delfiore G, Degueldre C, Luxen A, Franck G (1996) Functional neuroanatomy of human rapid-eye-movement sleep and dreaming. Nature 383(6596):163–166. doi:10.1038/383163a0
Maquet P, Laureys S, Peigneux P, Fuchs S, Petiau C, Phillips C et al (2000) Experience-dependent changes in cerebral activation during human REM sleep. Nat Neurosci 3(8):831–836
Marshall L, Helgadóttir H, Mölle M, Born J (2006) Boosting slow oscillations during sleep potentiates memory. Nature 444(7119):610–613
Mather M, Sutherland MR (2011) Arousal-biased competition in -perception and memory. Perspect Psychol Sci 6:114–133. doi:10.1177/1745691611400234
Maviel T, Durkin TP, Menzaghi F, Bontempi B (2004) Sites of neocortical reorganization critical for remote spatial memory. Science 305(5680):96–99. doi:10.1126/science.1098180
McGaugh JL (2000) Memory—a century of consolidation. Science 287(5451):248–251. doi:10.1126/science.287.5451.248
McNamara CG, Tejero-Cantero Á, Trouche S, Campo-Urriza N, Dupret D (2014) Dopaminergic neurons promote hippocampal reactivation and spatial memory persistence. Nat Neurosci 17:1658–1660. doi:10.1038/nn.3843
Mednick SC, Nakayama K, Cantero JL, Atienza M, Levin AA, Pathak N, Stickgold R (2002) The restorative effect of naps on perceptual deterioration. Nat Neurosci 5(7):677–681
Mednick S, Nakayama K, Stickgold R (2003) Sleep-dependent learning: a nap is as good as a night. Nat Neurosci 6(7):697–698
Mednick SC, Drummond SPA, Arman AC, Boynton GM (2008) Perceptual deterioration is reflected in the neural response: fMRI study of nappers and non-nappers. Perception 37(7):1086–1097. doi:10.1068/p5998
Mednick S, McDevitt E, Walsh J, Wamsley E, Paulus M, Kanady J, Drummond S (2013) The critical role of sleep spindles in hippocampal-dependent memory: a pharmacology study. J Neurosci 33(10):4494–4504
Mölle M, Born J (2011) Slow oscillations orchestrating fast oscillations and memory consolidation. Prog Brain Res 193:93–110
Mölle M, Yeshenko O, Marshall L, Sara S, Born J (2006) Hippocampal sharp wave-ripples linked to slow oscillations in rat slow-wave sleep. J Neurophysiol 96(1):62–70
Mölle M, Bergmann T, Marshall L, Born J (2011) Fast and slow spindles during the sleep slow oscillation: disparate coalescence and engagement in memory processing. Sleep 34(10):1411–1421
Morin A, Doyon J, Dostie V, Barakat M, Tahar AH, Korman M et al (2008) Motor sequence learning increases sleep spindles and fast frequencies in post-training sleep. Sleep 31(8):1149–1156
Morison R, Bassett D (1945) Electrical activity of the thalamus and basal ganglia in decorticate cats. J Neurophysiol 8(5):309–314
Morris RGM (2006) Elements of a neurobiological theory of hippocampal function: the role of synaptic plasticity, synaptic tagging and schemas. Eur J Neurosci 23(11):2829–2846. doi:10.1111/j.1460-9568.2006.04888.x
Moscovitch M, Rosenbaum RS, Gilboa A, Addis DR, Westmacott R, Grady C et al (2005) Functional neuroanatomy of remote episodic, semantic and spatial memory: a unified account based on multiple trace theory. J Anat 207(1):35–66. doi:10.1111/j.1469-7580.2005.00421.x
Müller G, Pilzecker A (1900) Experimental contributions to the theory of memory. Z Psychol Ergänzungsband 1:1–300
Newman EL, Norman KA (2010) Moderate excitation leads to weakening of perceptual representations. Cereb Cortex 20(11):2760–2770. doi:10.1093/cercor/bhq021
Ngo HV, Martinetz T, Born J, Mölle M (2013) Auditory closed-loop stimulation of the sleep slow oscillation enhances memory. Neuron 78(3):545–553
Ngo H, Miedema A, Faude I, Martinetz T, Molle M, Born J (2015) Driving sleep slow oscillations by auditory closed-loop stimulation—a self-limiting process. J Neurosci 35(17):6630–6638. doi:10.1523/JNEUROSCI.3133-14.2015
Nir Y, Tononi G (2010) Dreaming and the brain: from phenomenology to neurophysiology. Trends Cogn Sci 14(2):88–100. doi:10.1016/j.tics.2009.12.001
Nir Y, Staba RJ, Andrillon T, Vyazovskiy VV, Cirelli C, Fried I, Tononi G (2011) Regional slow waves and spindles in human sleep. Neuron 70(1):153–169
Nishida M, Walker MP (2007) Daytime naps, motor memory consolidation and regionally specific sleep spindles. PLoS One 2(4):e341
Nishida M, Pearsall J, Buckner RL, Walker MP (2009) REM sleep, prefrontal theta, and the consolidation of human emotional memory. Cereb Cortex 19:1158–1166. doi:10.1093/cercor/bhn155
Nyberg L, Habib R, McIntosh AR, Tulving E (2000) Reactivation of encoding-related brain activity during memory retrieval. Proc Natl Acad Sci USA 97(20):11120–11124. doi:10.1073/pnas.97.20.11120
O’Neill J, Senior T, Csicsvari J (2006) Place-selective firing of CA1 pyramidal cells during sharp wave/ripple network patterns in exploratory behavior. Neuron 49(1):143–155. doi:10.1016/j.neuron.2005.10.037
O’Neill J, Senior TJ, Allen K, Huxter JR, Csicsvari J (2008) Reactivation of experience-dependent cell assembly patterns in the hippocampus. Nat Neurosci 11(2):209–215. doi:10.1038/nn2037
Ong JL, Lo JC, Chee NIYN, Santostasi G, Paller KA, Zee PC, Chee MWL (2016) Effects of phase-locked acoustic stimulation during a nap on EEG spectra and declarative memory consolidation. Sleep Med 20:88–97
Oswald I, Taylor A, Treisman M (1960) Discriminative responses to stimuli during human sleep. Brain 83(3):440–453. doi:10.1093/brain/83.3.440
Oudiette D, Antony JW, Creery JD, Paller KA (2013) The role of memory reactivation during wakefulness and sleep in determining which memories endure. J Neurosci 33(15):6672–6678. doi:10.1523/JNEUROSCI.5497-12.2013
Pavlides C, Winson J (1989) Influences of hippocampal place cell firing in the awake state on the activity of these cells during subsequent sleep episodes. J Neurosci 9(8):2907–2918
Payne JD, Kensinger EA (2011) Sleep leads to changes in the emotional memory trace: evidence from fMRI. J Cogn Neurosci 23(6):1285–1297. doi:10.1162/jocn.2010.21526
Payne JD, Stickgold R, Swanberg K, Kensinger EA (2008) Sleep preferentially enhances memory for emotional components of scenes. Psychol Sci 19(8):781–788. doi:10.1111/j.1467-9280.2008.02157.x
Payne JD, Chambers AM, Kensinger EA (2012) Sleep promotes lasting changes in selective memory for emotional scenes. Front Integr Neurosci 6:108. doi:10.3389/fnint.2012.00108
Payne JD, Kensinger EA, Wamsley EJ, Spreng RN, Alger SE, Gibler K et al (2015) Napping and the selective consolidation of negative aspects of scenes. Emotion 15(2):176–186. doi:10.1037/a0038683
Peigneux P, Laureys S, Fuchs S, Collette F, Perrin F, Reggers J et al (2004) Are spatial memories strengthened in the human hippocampus during slow wave sleep? Neuron 44:535–545
Peigneux P, Orban P, Balteau E, Degueldre C, Luxen A, Laureys S, Maquet P (2006) Offline persistence of memory-related cerebral activity during active wakefulness. PLoS Biol 4(4):e100. doi:10.1371/journal.pbio.0040100
Pennartz CMA, Lee E, Verheul J, Lipa P, Barnes CA, McNaughton BL (2004) The ventral striatum in off-line processing: ensemble reactivation during sleep and modulation by hippocampal ripples. J Neurosci 24(29):6446–6456. doi:10.1523/JNEUROSCI.0575-04.2004
Peyrache A, Khamassi M, Benchenane K, Wiener SI, Battaglia FP (2009) Replay of rule-learning related neural patterns in the prefrontal cortex during sleep. Nat Neurosci 12(7):919–926. doi:10.1038/nn.2337
Plihal W, Born J (1997) Effects of early and late nocturnal sleep on declarative and procedural memory. J Cogn Neurosci 9(4):534–547
Polyn SM, Natu VS, Cohen JD, Norman KA (2005) Category-specific cortical activity precedes retrieval during memory search. Science 310(5756):1963–1966. doi:10.1126/science.1117645
Ramadan W, Eschenko O, Sara SJ (2009) Hippocampal sharp wave/ripples during sleep for consolidation of associative memory. PLoS One 4(8):1–9. doi:10.1371/journal.pone.0006697
Rasch B, Büchel C, Gais S, Born J (2007) Odor cues during slow-wave sleep prompt declarative memory consolidation. Science:1426–1429
Rasch B, Pommer J, Diekelmann S, Born J (2009) Pharmacological REM sleep suppression paradoxically improves rather than impairs skill memory. Nat Neurosci 12(4):396–397. doi:10.1038/nn.2206
Rauchs G, Feyers D, Landeau B, Bastin C, Luxen A, Maquet P, Collette F (2011) Sleep contributes to the strengthening of some memories over others, depending on hippocampal activity at learning. J Neurosci 31(7):2563–2568. doi:10.1523/JNEUROSCI.3972-10.2011
Rechtschaffen A, Kales A (1968) A manual of standardized terminology, techniques and scoring system of sleep stages in human subjects. University of California, Los Angele
Redondo RL, Morris RGM (2011) Making memories last: the synaptic tagging and capture hypothesis. Nat Rev Neurosci 12(1):17–30. doi:10.1038/nrn2963
Richter-Levin G, Akirav I (2003) Emotional tagging of memory formation—in the search for neural mechanisms. Brain Res Rev 43:247–256. doi:10.1016/j.brainresrev.2003.08.005
Rihm JS, Diekelmann S, Born J, Rasch B (2014) Reactivating memories during sleep by odors: odor specificity and associated changes in sleep oscillations. J Cogn Neurosci 26(8):1806–1818. doi:10.1162/jocn_a_00579
Ritter SM, Strick M, Bos MW, van Baaren RB, Dijksterhuis A (2012) Good morning creativity: task reactivation during sleep enhances beneficial effect of sleep on creative performance. J Sleep Res 21(6):643–647. doi:10.1111/j.1365-2869.2012.01006.x
Robertson EM, Pascual-Leone A, Press DZ (2004) Awareness modifies the skill-learning benefits of sleep. Curr Biol 14(3):208–212. doi:10.1016/j.cub.2004.01.027
Roediger HL, Karpicke JD (2006) The power of testing memory: basic research and implications for educational practice. Perspect Psychol Sci 1(3):181–210
Rolls A, Makam M, Kroeger D, Colas D, de Lecea L, Heller HC (2013) Sleep to forget: interference of fear memories during sleep. Mol Psychiatry 18(11):1166–1170. doi:10.1038/mp.2013.121
Rosanova M, Ulrich D (2005) Pattern-specific associative long-term potentiation induced by a sleep spindle-related spike train. J Neurosci 25(41):9398–9405
Routtenberg A, Rekart JL (2005) Post-translational protein modification as the substrate for long-lasting memory. Trends Neurosci 28(1):12–19. doi:10.1016/j.tins.2004.11.006
Rudoy J, Voss J, Westerberg C, Paller K (2009) Strengthening individual memories by reactivating them during sleep. Science 326:1079
Saletin JM, Goldstein AN, Walker MP (2011) The role of sleep in directed forgetting and remembering of human memories. Cereb Cortex 21(11):2534–2541
Sato Y, Fukuoka Y, Minamitani H, Honda K (2007) Sensory stimulation triggers spindles during sleep Stage 2. Sleep 30(4):511–518
Schabus M, Gruber G, Parapatics S, Sauter C, Klösch G, Anderer P et al (2004) Sleep spindles and their significance for declarative memory consolidation. Sleep 27(8):1479–1485
Schabus M, Hödlmoser K, Gruber G, Sauter C, Anderer P, Klösch G et al (2006) Sleep spindle-related activity in the human EEG and its relation to general cognitive and learning abilities. Eur J Neurosci 23(7):1738–1746
Schabus M, Kerstin H, Thomas P, Anderer P, Gruber G, Parapatics S et al (2008) Interindividual sleep spindle differences and their relation to learning-related enhancements. Brain Res 29:127–135
Schabus M, Dang-Vu T, Heib D, Boly M, Desseilles M, Vandewalle G et al (2012) The fate of incoming stimuli during NREM sleep is determined by spindles and the phase of the slow oscillation. Front Neurol 3:40
Schmidt C, Peigneux P, Muto V, Schenkel M, Knoblauch V, Münch M et al (2006) Encoding difficulty promotes postlearning changes in sleep spindle activity during napping. J Neurosci 26(35):8976–8982. doi:10.1523/JNEUROSCI.2464-06.2006
Schönauer M, Geisler T, Gais S (2014) Strengthening procedural memories by reactivation in sleep. J Cogn Neurosci 26(1):143–153. doi:10.1162/jocn_a_00471
Schreiner T, Rasch B (2014) Boosting vocabulary learning by verbal cueing during sleep. Cereb Cortex 25(11):4169–4179. doi:10.1093/cercor/bhu139
Schreiner T, Göldi M, Rasch B (2015) Cueing vocabulary during sleep increases theta activity during later recognition testing. Psychophysiology 52(11):1538–1543. doi:10.1111/psyp.12505
Scoville WB, Milner B (1957) Loss of recent memory after bilateral hippocampal lesions. J Neurol Neurosurg Psychiatry 20:11–21
Scrima L (1982) Isolated REM sleep facilitates recall of complex associative information. Psychophysiology 19(3):252–259. doi:10.1111/j.1469-8986.1982.tb02556.x
Shank SS, Margoliash D (2009) Sleep and sensorimotor integration during early vocal learning in a songbird. Nature 458(7234):73–77. doi:10.1038/nature07615
Siapas AG, Wilson MA (1998) Coordinated interactions between hippocampal ripples and cortical spindles during slow-wave sleep. Neuron 21:1123–1128
Silva RH, Abílio VC, Takatsu AL, Kameda SR, Grassl C, Chehin AB et al (2004) Role of hippocampal oxidative stress in memory deficits induced by sleep deprivation in mice. Neuropharmacol 46(6):895–903
Skaggs WE, McNaughton BL (1996) Replay of neuronal firing sequences in rat hippocampus during sleep following spatial experience. Science 271(5257):1870–1873. doi:10.1126/science.271.5257.1870
Smith C (1995) Sleep states and memory processes. Behav Brain Res 69:137–145
Smith C (2001) Sleep states and memory processes in humans: procedural versus declarative memory systems. Sleep Med Rev 5(6):491–506. doi:10.1053/smrv.2001.0164
Smith C, MacNeill C (1994) Impaired motor memory for a pursuit rotor task following stage 2 sleep loss in college students. J Sleep Res 3:206–213
Smith CT, Smith D (2003) Ingestion of ethanol just prior to sleep onset impairs memory for procedural but not declarative tasks. Sleep 26(2):185–191
Smith C, Weeden K (1990) Post training REMs coincident auditory stimulation enhances memory in humans. Psychiatr J Univ Ott 15(2):85–90
Smith C, Wong PT (1991) Paradoxical sleep increases predict successful learning in a complex operant task. Behav Neurosci 105(2):282–288. doi:10.1037//0735-7044.105.2.282
Smith C, Young J, Young W (1980) Prolonged increases in paradoxical sleep during and after avoidance-task acquisition. Sleep 3(1):67–81
Smith C, Aubrey J, Peters K (2004) Different roles for REM and Stage-2 sleep in motor learning: a proposed model. Psychol Belg 44:79–102
Song S, Cohen LG (2014) Practice and sleep form different aspects of skill. Nat Commun 5:3407. doi:10.1038/ncomms4407
Squire LR, Bayley PJ (2007) The neuroscience of remote memory. Curr Opin Neurobiol 17(2):185–196. doi:10.1016/j.conb.2007.02.006
Squire LR, Genzel L, Wixted JT, Morris RG (2015) Memory consolidation. Cold Spring Harb Perspect Biol 7(8):a021766
Staresina BP, Alink A, Kriegeskorte N, Henson RN (2013) Awake reactivation predicts memory in humans. Proc Natl Acad Sci USA 110(52):21159–21164. doi:10.1073/pnas.1311989110
Staresina BP, Bergmann TO, Bonnefond M, van der Meij R, Jensen O, Deuker L et al (2015) Hierarchical nesting of slow oscillations, spindles and ripples in the human hippocampus during sleep. Nat Neurosci 18:1679–1686. doi:10.1038/nn.4119
Stickgold R, Walker MP (2013) Sleep-dependent memory triage: evolving generalization through selective processing. Nat Neurosci 16(2):139–145. doi:10.1038/nn.3303
Stickgold R, Whidbee D, Schirmer B, Patel V, Hobson JA (2000) Visual discrimination task improvement: a multi-step process occurring during sleep. J Cogn Neurosci 12(2):246–254
St-Laurent M, Abdi H, Buchsbaum BR (2014) Distributed patterns of reactivation predict vividness of recollection. J Cogn Neurosci 27(10):2000–2018. doi:10.1162/jocn
Studte S, Bridger E, Mecklinger A (2015) Nap sleep preserves associative but not item memory performance. Neurobiol Learn Mem 120:84–93. doi:10.1016/j.nlm.2015.02.012
Takashima A, Nieuwenhuis ILC, Jensen O, Talamini LM, Rijpkema M, Fernández G (2009) Shift from hippocampal to neocortical centered retrieval network with consolidation. J Neurosci 29(32):10087–10093. doi:10.1523/JNEUROSCI.0799-09.2009
Takeuchi T, Duszkiewicz AJ, Morris RGM (2014) The synaptic plasticity and memory hypothesis: encoding, storage and persistence. Philos Trans R Soc Lond B Biol Sci 369(1633):20130288. doi:10.1098/rstb.2013.0288
Talamini LM, Nieuwenhuis ILC, Takashima A, Jensen O (2008) Sleep directly following learning benefits consolidation of spatial associative memory. Learn Mem 15(4):233–237. doi:10.1101/lm.771608
Tamaki M, Matsuoka T, Nittono H, Hori T (2008) Fast sleep spindle (13–15 Hz) activity correlates with sleep-dependent improvement in visuomotor performance. Sleep 31(2):204–211
Tambini A, Ketz N, Davachi L (2010) Enhanced brain correlations during rest are related to memory for recent experiences. Neuron 65(2):280–290. doi:10.1016/j.neuron.2010.01.001
Tilley A, Empson J (1978) REM sleep and memory consolidation. Biol Psychol 6(4):293–300. doi:10.1016/0301-0511(78)90031-5
Tononi G, Cirelli C (2014) Sleep and the price of plasticity: from synaptic and cellular homeostasis to memory consolidation and integration. Neuron 81(1):12–34. doi:10.1016/j.neuron.2013.12.025
Torres M, Giraldez F (1998) The development of the vertebrate inner ear. Mech Dev 71:5–21
Tse D, Takeuchi T, Kakeyama M, Kajii Y, Okuno H, Tohyama C et al (2011) Schema-dependent gene activation and memory encoding in neocortex. Science 333:891–895
Tulving E, Thomson D (1973) Encoding specificity and retrieval processes in episodic memory. Psychol Rev 80(5):352–373
van der Helm E, Gujar N, Nishida M, Walker MP (2011) Sleep-dependent facilitation of episodic memory details. PLoS One 6(11):e27421. doi:10.1371/journal.pone.0027421
van Dongen EV, Takashima A, Barth M, Zapp J, Schad LR, Paller KA, Fernández G (2012a) Memory stabilization with targeted reactivation during human slow-wave sleep. Proc Natl Acad Sci USA 109(26):10575–10580. doi:10.1073/pnas.1201072109
van Dongen EV, Thielen J-W, Takashima A, Barth M, Fernández G (2012b) Sleep supports selective retention of associative memories based on relevance for future utilization. PLoS One 7(8):e43426. doi:10.1371/journal.pone.0043426
van Stegeren AH, Goekoop R, Everaerd W, Scheltens P, Barkhof F, Kuijer JPA, Rombouts SARB (2005) Noradrenaline mediates amygdala activation in men and women during encoding of emotional material. NeuroImage 24:898–909. doi:10.1016/j.neuroimage.2004.09.011
Vilberg KL, Davachi L (2013) Perirhinal-hippocampal connectivity during reactivation is a marker for object-based memory consolidation. Neuron 79(6):1232–1242. doi:10.1016/j.neuron.2013.07.013
Vyazovskiy VV, Harris KD (2013) Sleep and the single neuron: the role of global slow oscillations in individual cell rest. Nat Rev Neurosci 14(6):443–451
Vyazovskiy VV, Cirelli C, Pfister-Genskow M, Faraguna U, Tononi G (2008) Molecular and electrophysiological evidence for net synaptic potentiation in wake and depression in sleep. Nat Neurosci 11(2):200–208
Vyazovskiy VV, Olcese U, Lazimy YM, Faraguna U, Esser SK, Williams JC et al (2009) Cortical firing and sleep homeostasis. Neuron 63(6):865–878
Vyazovskiy VV, Olcese U, Hanlon EC, Nir Y, Cirelli C, Tononi G (2011) Local sleep in awake rats. Nature 472(7344):443–447
Wagner U, Gais S, Born J (2001) Emotional memory formation is enhanced across sleep intervals with high amounts of rapid eye movement sleep. Learn Mem 8:112–119. doi:10.1101/lm.36801.sleep
Wagner U, Gais S, Haider H, Verleger R, Born J (2004) Sleep inspires insight. Nature 427(22):352–355
Wagner U, Hallschmid M, Rasch B, Born J (2006) Brief sleep after learning keeps emotional memories alive for years. Biol Psychiatry 60:788–790. doi:10.1016/j.biopsych.2006.03.061
Walker MP, Brakefield T, Morgan A, Hobson JA, Stickgold R (2002a) Practice with sleep makes perfect: sleep-dependent motor skill learning. Neuron 35:205–211
Walker MP, Liston C, Hobson JA, Stickgold R (2002b) Cognitive flexibility across the sleep–wake cycle: REM-sleep enhancement of anagram problem solving. Cogn Brain Res 14(3):317–324. doi:10.1016/S0926-6410(02)00134-9
Walker MP, Brakefield T, Hobson JA (2003) Dissociable stages of human memory consolidation and reconsolidation. Nature 425:616–620. doi:10.1038/nature01951.1
Walker MP, Stickgold R, Alsop D, Gaab N, Schlaug G (2005) Sleep-dependent motor memory plasticity in the human brain. Neuroscience 133(4):911–917. doi:10.1016/j.neuroscience.2005.04.007
Wamsley EJ, Tucker MA, Shinn AK, Ono KE, McKinley SK, Ely AV et al (2012) Reduced sleep spindles and spindle coherence in schizophrenia: mechanisms of impaired memory consolidation? Biol Psychiatry 71(2):154–161. doi:10.1016/j.biopsych.2011.08.008
Wang S-H, Redondo RL, Morris RGM (2010) Relevance of synaptic tagging and capture to the persistence of long-term potentiation and everyday spatial memory. Proc Natl Acad Sci 107(45):19537–19542
Wiesel TN, Hubel DH (1963) Effects of visual deprivation on morphology and physiology of cells in the cat’s lateral geniculate body. J Neurophysiol 26:978–993 Retrieved from http://hubel.med.harvard.edu/papers/HubelWiesel1963Jneurophysiol3.pdf. http://www.ncbi.nlm.nih.gov/pubmed/14084170
Wilhelm I, Diekelmann S, Molzow I, Ayoub A, Mölle M, Born J (2011) Sleep selectively enhances memory expected to be of future relevance. J Neurosci 31(5):1563–1569. doi:10.1523/JNEUROSCI.3575-10.2011
Wilson M, McNaughton B (1994) Reactivation of hippocampal ensemble memories during sleep. Science 265:676–679
Wing EA, Ritchey M, Cabeza R (2015) Reinstatement of individual past events revealed by the similarity of distributed activation patterns during encoding and retrieval. J Cogn Neurosci 27(4):679–691. doi:10.1162/jocn
Wittmann BC, Schott BH, Guderian S, Frey JU, Heinze HJ, Düzel E (2005) Reward-related fMRI activation of dopaminergic midbrain is associated with enhanced hippocampus-dependent long-term memory formation. Neuron 45:459–467. doi:10.1016/j.neuron.2005.01.010
Xie L, Kang H, Xu Q, Chen MJ, Liao Y, Thiyagarajan M et al (2013) Sleep drives metabolite clearance from the adult brain. Science 342:373–377
Xue G, Dong Q, Chen C, Lu Z, Mumford JA, Poldrack RA (2010) Greater neural pattern similarity across repetitions is associated with better memory. Science 330(6000):97–101. doi:10.1126/science.1193125
Yaroush R, Sullivan MJ, Ekstrand BR (1971) Effect of sleep on memory: II. Differential effect of the first and second half of the night. J Exp Psychol 88(3):361–366. doi:10.1037/h0030914
Yordanova J, Kolev V, Wagner U, Born J, Verleger R (2012) Increased alpha (8–12 Hz) activity during slow wave sleep as a marker for the transition from implicit knowledge to explicit insight. J Cogn Neurosci 24(1):119–132
Acknowledgements
Parts of this chapter were adapted from James Antony’s Ph.D. thesis. We offer special thanks to Paul Reber for his insightful comments and Aryeh Routtenberg for his willingness to discuss these topics in detail. This work was supported by NIMH grant F31MH100958 and Princeton University’s C.V. Starr Fellowship to JWA and NSF grants NSF BCS-1461088 and BCS-1533512 to KAP.
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2017 Springer International Publishing AG
About this chapter
Cite this chapter
Antony, J.W., Paller, K.A. (2017). Hippocampal Contributions to Declarative Memory Consolidation During Sleep. In: Hannula, D., Duff, M. (eds) The Hippocampus from Cells to Systems. Springer, Cham. https://doi.org/10.1007/978-3-319-50406-3_9
Download citation
DOI: https://doi.org/10.1007/978-3-319-50406-3_9
Published:
Publisher Name: Springer, Cham
Print ISBN: 978-3-319-50405-6
Online ISBN: 978-3-319-50406-3
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)