Memory replay in the hippocampus

Space, Time and Memory in the Hippocampal Formation

Volumn , Issue , 2014, Pages 351-371

  Jadhav, Shantanu P ^a   Frank, Loren M ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84930724339     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1007/978-3-7091-1292-2_13     Document Type: Chapter

References (120)

1. Alvarez P, Zola-Morgan S, Squire LR (1994) The animal model of human amnesia: long-term memory impaired and short-term memory intact. Proc Natl Acad Sci USA 91(12):5637-5641
2. Amaral DG, Ishizuka N, Claiborne B (1990) Neurons, numbers and the hippocampal network. Prog Brain Res 83:1-11
3. Ambrosini MV, Mariucci G, Colarieti L, Bruschelli G, Carobi C, Giuditta A (1993) The structure of sleep is related to the learning ability of rats. Eur J Neurosci 5(3):269-275
4. Bendor D, Wilson MA (2012) Biasing the content of hippocampal replay during sleep. Nat Neurosci 15(10):1439-1444. doi:10.1038/nn.3203
5. Best PJ, White AM, Minai A (2001) Spatial processing in the brain: The activity of hippocampal place cells. Annu Rev Neurosci 24:459-486
6. Bi GQ, Poo MM (1998) Synaptic modifications in cultured hippocampal neurons: dependence on spike timing, synaptic strength, and postsynaptic cell type. J Neurosci 18(24):10464-10472
7. Born J, Rasch B, Gais S (2006) Sleep to remember. Neuroscientist 12(5):410-424. doi:10.1177/ 1073858406292647
8. Bouret S, Sara SJ (2005) Network reset: A simplified overarching theory of locus coeruleus noradrenaline function. Trends Neurosci 28(11):574-582
9. Buzsaki G (1986) Hippocampal sharp waves: their origin and significance. Brain Res 398 (2):242-252
10. Buzsaki G (1989) Two-stage model of memory trace formation: A role for "noisy" brain states. Neuroscience 31(3):551-570
11. Buzsaki G (1996) The hippocampo-neocortical dialogue. Cereb Cortex 6(2):81-92
12. Carr MF, Frank LM (2012) A single microcircuit with multiple functions: state dependent information processing in the hippocampus. Curr Opin Neurobiol 22(4):704-708. doi:10.1016/j.conb.2012.03.007
13. 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, nn.2732 [pii]
14. Carr MF, Karlsson MP, Frank LM (2012) Transient slow gamma synchrony underlies hippocampal memory replay. Neuron 75(4):700-713. doi:10.1016/j.neuron.2012.06.014
15. Cheng S, Frank LM (2008) New experiences enhance coordinated neural activity in the hippocampus. Neuron 57(2):303-313
16. Chrobak JJ, Buzsaki 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
17. Chrobak JJ, Buzsaki G (1996) High-frequency oscillations in the output networks of the hippocampal-entorhinal axis of the freely behaving rat. J Neurosci 16(9):3056-3066
18. Cohen NJ, Eichenbaum H (1993) Memory, amnesia, and the hippocampal system. MIT Press, Cambridge, M.A.
19. Csicsvari J, Hirase H, Czurko A, Mamiya A, Buzsaki G (1999) Fast network oscillations in the hippocampal CA1 region of the behaving rat. J Neurosci 19(16):RC20
20. Csicsvari J, Hirase H, Mamiya A, Buzsaki G (2000) Ensemble patterns of hippocampal CA3-CA1 neurons during sharp wave-associated population events. Neuron 28(2):585-594
21. Csicsvari J, O'Neill J, Allen K, Senior T (2007) Place-selective firing contributes to the reverseorder reactivation of CA1 pyramidal cells during sharp waves in open-field exploration. Eur J Neurosci 26(3):704-716
22. Davidson TJ, Kloosterman F, Wilson MA (2009) Hippocampal replay of extended experience. Neuron 63(4):497-507
23. de Hoz L, Wood ER (2006) Dissociating the past from the present in the activity of place cells. Hippocampus 16(9):704-715
24. Diba K, Buzsaki G (2007) Forward and reverse hippocampal place-cell sequences during ripples. Nat Neurosci 10(10):1241-1242
25. Diekelmann S, Born J (2010) Slow-wave sleep takes the leading role in memory reorganization. Nat Rev Neurosci 11(3):218
26. Diekelmann S, Buchel 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
27. Dudai Y (2004) The neurobiology of consolidations, or, how stable is the engram? Annu Rev Psychol 55:51-86
28. 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
29. Ego-Stengel V, Wilson MA (2010) Disruption of ripple-associated hippocampal activity during rest impairs spatial learning in the rat. Hippocampus 20(1):1-10
30. Eichenbaum H, Cohen NJ (2001) From conditioning to conscious recollection. Oxford University Press, New York, NY
31. Eldridge LL, Knowlton BJ, Furmanski CS, Bookheimer SY, Engel SA (2000) Remembering episodes: A selective role for the hippocampus during retrieval. Nat Neurosci 3(11):1149-1152
32. 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
33. Eschenko O, Molle M, Born J, Sara SJ (2006) Elevated sleep spindle density after learning or after retrieval in rats. J Neurosci 26(50):12914-12920
34. Eschenko O, Ramadan W, Molle M, Born J, Sara SJ (2008) Sustained increase in hippocampal sharp-wave ripple activity during slow-wave sleep after learning. Learn Mem 15(4):222-228
35. Euston DR, Tatsuno M, McNaughton BL (2007) Fast-forward playback of recent memory sequences in prefrontal cortex during sleep. Science 318(5853):1147-1150
36. Fortin NJ, Wright SP, Eichenbaum H (2004) Recollection-like memory retrieval in rats is dependent on the hippocampus. Nature 431(7005):188-191
37. Foster DJ, Wilson MA (2006) Reverse replay of behavioural sequences in hippocampal place cells during the awake state. Nature 440(7084):680-683
38. Frank LM, Stanley GB, Brown EN (2004) Hippocampal plasticity across multiple days of exposure to novel environments. J Neurosci 24(35):7681-7689
39. Gais S, Born J (2004) Declarative memory consolidation: mechanisms acting during human sleep. Learn Mem 11(6):679-685. doi:10.1101/lm.80504
40. Gais S, Lucas B, Born J (2006) Sleep after learning aids memory recall. Learn Mem 13 (3):259-262. doi:10.1101/lm.132106, 13/3/259 [pii]
41. Giovannini MG, Rakovska A, Benton RS, Pazzagli M, Bianchi L, Pepeu G (2001) Effects of novelty and habituation on acetylcholine, GABA, and glutamate release from the frontal cortex and hippocampus of freely moving rats. Neuroscience 106(1):43-53
42. Girardeau G, Benchenane K, Wiener SI, Buzsaki G, Zugaro MB (2009) Selective suppression of hippocampal ripples impairs spatial memory. Nat Neurosci 12(10):1222-1223
43. Glickman SE (1961) Perseverative neural processes and consolidation of the memory trace. Psychol Bull 58:218-233
44. Gupta AS, van der Meer MA, Touretzky DS, Redish AD (2010) Hippocampal replay is not a simple function of experience. Neuron 65(5):695-705
45. Haist F, Bowden GJ, Mao H (2001) Consolidation of human memory over decades revealed by functional magnetic resonance imaging. Nat Neurosci 4(11):1139-1145
46. Hebb DO (1949) The organization of behavior. Wiley, New York, NY
47. Hoffman KL, McNaughton BL (2002) Coordinated reactivation of distributed memory traces in primate neocortex. Science 297(5589):2070-2073
48. Jackson JC, Johnson A, Redish AD (2006) Hippocampal sharp waves and reactivation during awake states depend on repeated sequential experience. J Neurosci 26(48):12415-12426
49. 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
50. Jarrard LE (2001) Retrograde amnesia and consolidation: anatomical and lesion considerations. Hippocampus 11(1):43-49
51. Ji D, Wilson MA (2007) Coordinated memory replay in the visual cortex and hippocampus during sleep. Nat Neurosci 10(1):100-107
52. Johnson A, Redish AD (2007) Neural ensembles in CA3 transiently encode paths forward of the animal at a decision point. J Neurosci 27(45):12176-12189
53. Karlsson MP, Frank LM (2008) Network dynamics underlying the formation of sparse, informative representations in the hippocampus. J Neurosci 28(52):14271-14281
54. Karlsson MP, Frank LM (2009) Awake replay of remote experiences in the hippocampus. Nat Neurosci 12(7):913-918
55. Kim JJ, Fanselow MS (1992) Modality-specific retrograde amnesia of fear. Science 256 (5057):675-677
56. Kim SM, Frank LM (2009) Hippocampal lesions impair rapid learning of a continuous spatial alternation task. PLoS One 4(5):e5494
57. 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
58. Lansink CS, Goltstein PM, Lankelma JV, Joosten RN, McNaughton BL, Pennartz CM (2008) Preferential reactivation of motivationally relevant information in the ventral striatum. J Neurosci 28(25):6372-6382
59. Lansink CS, Goltstein PM, Lankelma JV, McNaughton BL, Pennartz CM (2009) Hippocampus leads ventral striatum in replay of place-reward information. PLoS Biol 7(8):e1000173
60. Lee AK, Wilson MA (2002) Memory of sequential experience in the hippocampus during slow wave sleep. Neuron 36(6):1183-1194
61. Leutgeb JK, Leutgeb S, Moser MB, Moser EI (2007) Pattern separation in the dentate gyrus and CA3 of the hippocampus. Science 315(5814):961-966
62. Logothetis NK, Eschenko O, Murayama Y, Augath M, Steudel T, Evrard HC, Besserve M, Oeltermann A (2012) Hippocampal-cortical interaction during periods of subcortical silence. Nature 491(7425):547-553. doi:10.1038/nature11618
63. Louie K, Wilson MA (2001) Temporally structured replay of awake hippocampal ensemble activity during rapid eye movement sleep. Neuron 29(1):145-156
64. Lubenov EV, Siapas AG (2008) Decoupling through synchrony in neuronal circuits with propagation delays. Neuron 58(1):118-131
65. Maquet P (2001) The role of sleep in learning and memory. Science 294(5544):1048-1052. doi:10.1126/science.1062856
66. Marr D (1971) Simple memory: A theory for archicortex. Philos Trans R Soc Lond 262(841):23-81
67. Marshall L, Born J (2007) The contribution of sleep to hippocampus-dependent memory consolidation. Trends Cogn Sci 11(10):442-450. doi:10.1016/j.tics.2007.09.001
68. 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(3):419-457
69. McGaugh JL (1966) Time-dependent processes in memory storage. Science 153 (3742):1351-1358
70. McKenzie S, Eichenbaum H (2011) Consolidation and reconsolidation: two lives of memories? Neuron 71(2):224-233. doi:10.1016/j.neuron.2011.06.037
71. McNaughton BL, Morris RG (1987) Hippocampal synaptic enhancement and information storage within a distributed memory system. Trends Neurosci 10:408-415
72. Molle M, Eschenko O, Gais S, Sara SJ, Born J (2009) The influence of learning on sleep slow oscillations and associated spindles and ripples in humans and rats. Eur J Neurosci 29 (5):1071-1081
73. Muller RU, Kubie JL (1987) The effects of changes in the environment on the spatial firing of hippocampal complex-spike cells. J Neurosci 7(7):1951-1968
74. Nadasdy Z, Hirase H, Czurko A, Csicsvari J, Buzsaki G (1999) Replay and time compression of recurring spike sequences in the hippocampus. J Neurosci 19(21):9497-9507
75. Nadel L, Moscovitch M (2001) The hippocampal complex and long-term memory revisited. Trends Cogn Sci 5(6):228-230
76. Nader K, Hardt O (2009) A single standard for memory: The case for reconsolidation. Nat Rev Neurosci 10(3):224-234. doi:10.1038/nrn2590
77. Nakashiba T, Buhl DL, McHugh TJ, Tonegawa S (2009) Hippocampal CA3 output is crucial for ripple-associated reactivation and consolidation of memory. Neuron 62(6):781-787
78. Navratilova Z, Hoang LT, Schwindel CD, Tatsuno M, McNaughton BL (2012) Experiencedependent firing rate remapping generates directional selectivity in hippocampal place cells. Front Neural Circuits 6:6. doi:10.3389/fncir.2012.00006
79. Nokia MS, Mikkonen JE, Penttonen M, Wikgren J (2012) Disrupting neural activity related to awake-state sharp wave-ripple complexes prevents hippocampal learning. Front Behav Neurosci 6:84. doi:10.3389/fnbeh.2012.00084
80. O'Keefe J, Dostrovsky J (1971) The hippocampus as a spatial map. Preliminary evidence from unit activity in the freely-moving rat. Brain Res 34(1):171-175
81. O'Keefe J, Nadel L (1978) The hippocampus as a cognitive map. Oxford University Press, London
82. 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
83. 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
84. 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
85. Peigneux P, Laureys S, Fuchs S, Collette F, Perrin F, Reggers J, Phillips C, Degueldre C, Del Fiore G, Aerts J, Luxen A, Maquet P (2004) Are spatial memories strengthened in the human hippocampus during slow wave sleep? Neuron 44(3):535-545
86. 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
87. Peyrache A, Battaglia FP, Destexhe A (2011) Inhibition recruitment in prefrontal cortex during sleep spindles and gating of hippocampal inputs. Proc Natl Acad Sci USA 108 (41):17207-17212. doi:10.1073/pnas.1103612108
88. Pfeiffer BE, Foster DJ (2013) Hippocampal place-cell sequences depict future paths to remembered goals. Nature 497(7447):74-79. doi:10.1038/nature12112
89. Phillips KG, Bartsch U, McCarthy AP, Edgar DM, Tricklebank MD, Wafford KA, Jones MW (2012) Decoupling of sleep-dependent cortical and hippocampal interactions in a neurodevelopmental model of schizophrenia. Neuron 76(3):526-533. doi:10.1016/j.neuron.2012.09.016
90. Rasch B, Buchel C, Gais S, Born J (2007) Odor cues during slow-wave sleep prompt declarative memory consolidation. Science 315(5817):1426-1429
91. Ribeiro S, Gervasoni D, Soares ES, Zhou Y, Lin SC, Pantoja J, Lavine M, Nicolelis MA (2004) Long-lasting novelty-induced neuronal reverberation during slow-wave sleep in multiple forebrain areas. PLoS Biol 2(1):E24
92. Riedel G, Micheau J, Lam AG, Roloff EL, Martin SJ, Bridge H, de Hoz L, Poeschel B, McCulloch J, Morris RG (1999) Reversible neural inactivation reveals hippocampal participation in several memory processes. Nat Neurosci 2(10):898-905
93. Rudoy JD, Voss JL, Westerberg CE, Paller KA (2009) Strengthening individual memories by reactivating them during sleep. Science 326(5956):1079. doi:10.1126/science.1179013
94. Rudy JW, Sutherland RJ (1995) Configural association theory and the hippocampal formation: an appraisal and reconfiguration. Hippocampus 5(5):375-389
95. Sara SJ (2000) Retrieval and reconsolidation: toward a neurobiology of remembering. Learn Mem 7(2):73-84
96. Schultz W (1998) Predictive reward signal of dopamine neurons. J Neurophysiol 80(1):1-27
97. Scoville WB, Milner B (1957) Loss of recent memory after bilateral hippocampal lesions. J Neurol Neurosurg Psychiatry 20:11-21
98. Siapas AG, Wilson MA (1998) Coordinated interactions between hippocampal ripples and cortical spindles during slow-wave sleep. Neuron 21(5):1123-1128
99. Singer AC, Frank LM (2009) Rewarded outcomes enhance reactivation of experience in the hippocampus. Neuron 64(6):910-921
100. Singer AC, Carr MF, Karlsson MP, Frank LM (2013) Hippocampal SWR activity predicts correct decisions during the initial learning of an alternation task. Neuron 77(6):1163-1173. doi:10.1016/j.neuron.2013.01.027
101. Sirota A, Csicsvari J, Buhl D, Buzsaki G (2003) Communication between neocortex and hippocampus during sleep in rodents. Proc Natl Acad Sci USA 100(4):2065-2069
102. Skaggs WE, McNaughton BL (1996) Replay of neuronal firing sequences in rat hippocampus during sleep following spatial experience. Science 271(5257):1870-1873
103. Squire LR (1982) The neuropsychology of human memory. Annu Rev Neurosci 5 (241-73):241-273
104. Squire LR, Zola SM (1996) Structure and function of declarative and nondeclarative memory systems. Proc Natl Acad Sci USA 93(24):13515-13522
105. Squire LR, Zola-Morgan S (1991) The medial temporal lobe memory system. Science 253 (5026):1380-1386
106. Squire LR, Clark RE, Knowlton BJ (2001) Retrograde amnesia. Hippocampus 11(1):50-55
107. Stickgold R (2005) Sleep-dependent memory consolidation. Nature 437(7063):1272-1278
108. Sutherland GR, McNaughton B (2000) Memory trace reactivation in hippocampal and neocortical neuronal ensembles. Curr Opin Neurobiol 10(2):180-186
109. Takehara-Nishiuchi K, McNaughton BL (2008) Spontaneous changes of neocortical code for associative memory during consolidation. Science 322(5903):960-963. doi:10.1126/science. 1161299
110. Tononi G, Cirelli C (2006) Sleep function and synaptic homeostasis. Sleep Med Rev 10(1):49-62
111. Tse D, Langston RF, Kakeyama M, Bethus I, Spooner PA, Wood ER, Witter MP, Morris RG (2007) Schemas and memory consolidation. Science 316(5821):76-82
112. Tulving E (1987) Multiple memory systems and consciousness. Hum Neurobiol 6(2):67-80
113. Tulving E, Markowitsch HJ (1998) Episodic and declarative memory: role of the hippocampus. Hippocampus 8(3):198-204
114. Walker MP, Stickgold R (2004) Sleep-dependent learning and memory consolidation. Neuron 44 (1):121-133. doi:10.1016/j.neuron.2004.08.031
115. Walker MP, Brakefield T, Hobson JA, Stickgold R (2003) Dissociable stages of human memory consolidation and reconsolidation. Nature 425(6958):616-620
116. Wierzynski CM, Lubenov EV, Gu M, Siapas AG (2009) State-dependent spike-timing relationships between hippocampal and prefrontal circuits during sleep. Neuron 61(4):587-596
117. Wilson MA, McNaughton BL (1993) Dynamics of the hippocampal ensemble code for space. Science 261(5124):1055-1058
118. Wilson MA, McNaughton BL (1994) Reactivation of hippocampal ensemble memories during sleep. Science 265(5172):676-679
119. Ylinen A, Bragin A, Nadasdy Z, Jando G, Szabo I, Sik A, Buzsaki G (1995) Sharp wave-associated high-frequency oscillation (200 Hz) in the intact hippocampus: network and intracellular mechanisms. J Neurosci 15(1 Pt 1):30-46
120. Zola-Morgan SM, Squire LR (1990) The primate hippocampal formation: evidence for a timelimited role in memory storage. Science 250(4978):288-290