Sharp wave/ripple network oscillations and learning-associated hippocampal maps

Philosophical Transactions of the Royal Society B: Biological Sciences

Volumn 369, Issue 1635, 2014, Pages

  Csicsvari, Jozsef ^a   Dupret, David ^b  

^a INSTITUTE OF SCIENCE AND TECHNOLOGY AUSTRIA   (Austria)

^b UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

Cognitive map; Memory consolidation; Place cell; Sleep

Indexed keywords

BRAIN; MAPPING; MEMORY; NEUROLOGY; OSCILLATION; SPATIAL COGNITION;

ANIMAL; BIOLOGICAL RHYTHM; COGNITIVE MAP; DEPTH PERCEPTION; HIPPOCAMPUS; LEARNING; MEMORY; MEMORY CONSOLIDATION; NERVE CELL; PHYSIOLOGY; PLACE CELL; RAT; REVIEW; SLEEP;

COGNITIVE MAP; MEMORY CONSOLIDATION; PLACE CELL; SLEEP;

ANIMALS; BIOLOGICAL CLOCKS; HIPPOCAMPUS; LEARNING; MEMORY; NEURONS; RATS; SLEEP; SPACE PERCEPTION;

EID: 84903595365     PISSN: 09628436     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rstb.2012.0528     Document Type: Review

References (47)

1. O'Keefe J, Nadel L. 1978 The hippocampus as a cognitive map. Oxford, UK: Oxford University Press.
2. Buzsaki G, Horvath Z, Urioste R, Hetke J, Wise K. 1992 High-frequency network oscillation in the hippocampus. Science 256, 1025-1027. (doi:10. 1126/science.1589772)
3. 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, RC20.
4. Buzsaki G, Leung LW, Vanderwolf CH. 1983 Cellular bases of hippocampal EEG in the behaving rat. Brain Res. 287, 139-171.
5. 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, 143-155. (doi:10.1016/j.neuron. 2005.10.037)
6. Marr D. 1971 Simple memory: a theory for archicortex. Phil. Trans. R. Soc. Lond. B 262, 23-81. (doi:10.1098/rstb.1971.0078)
7. Buzsaki G. 1989 Two-stage model of memory trace formation: a role for 'noisy' brain states. Neuroscience 31, 551-570. (doi:10.1016/0306-4522(89)90423-5)
8. 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. (doi:10.1037/0033-295X.102.3.419)
9. Wilson MA, McNaughton BL. 1994 Reactivation of hippocampal ensemble memories during sleep. Science 265, 676-679. (doi:10.1126/science. 8036517)
10. 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, 9497-9507.
11. Kudrimoti HS, Barnes CA, McNaughton BL. 1999 Reactivation of hippocampal cell assemblies: effects of behavioral state, experience, and EEG dynamics. J. Neurosci. 19, 4090-4101.
12. Lee AK, Wilson MA. 2002 Memory of sequential experience in the hippocampus during slow wave sleep. Neuron 36, 1183-1194. (doi:10.1016/S0896-6273(02)01096-6)
13. Girardeau G, Benchenane K, Wiener SI, Buzsaki G, Zugaro MB. 2009 Selective suppression of hippocampal ripples impairs spatial memory. Nat. Neurosci. 12, 1222-1223. (doi:10.1038/ nn.2384)
14. Ego-Stengel V, Wilson MA. 2010 Disruption of ripple-associated hippocampal activity during rest impairs spatial learning in the rat. Hippocampus 20, 1-10. (doi:10.1002/hipo.20707)
15. Jadhav SP, Kemere C, German PW, Frank LM. 2012 Awake hippocampal sharp-wave ripples support spatial memory. Science 336, 1454-1458. (doi:10. 1126/science.1217230)
16. Lisman JE, Otmakhova NA. 2001 Storage, recall, and novelty detection of sequences by the hippocampus: elaborating on the SOCRATIC model to account for normal and aberrant effects of dopamine. Hippocampus 11, 551-568. (doi:10. 1002/hipo.1071)
17. Vinogradova OS. 2001 Hippocampus as comparator: role of the two input and two output systems of the hippocampus in selection and registration of information. Hippocampus 11, 578-598. (doi:10.1002/hipo.1073)
18. Dere E, Huston JP, Souza Silva MA. 2007 The pharmacology, neuroanatomy and neurogenetics of one-trial object recognition in rodents. Neurosci. Biobehav. Rev. 31, 673-704. (doi:10.1016/j. neubiorev.2007.01.005)
19. Muller R. 1996 A quarter of a century of place cells. Neuron 17, 813-822. (doi:10.1016/S0896-6273 (00)80214-7)
20. Agnihotri NT, Hawkins RD, Kandel ER, Kentros C. 2004 The long-term stability of new hippocampal place fields requires new protein synthesis. Proc. Natl Acad. Sci. USA 101, 3656-3661. (doi:10.1073/ pnas.0400385101)
21. Kentros C, Hargreaves E, Hawkins RD, Kandel ER, Shapiro M, Muller RV. 1998 Abolition of long-term stability of new hippocampal place cell maps by NMDA receptor blockade. Science 280, 2121-2126. (doi:10.1126/science.280.5372.2121)
22. Dragoi G, Harris KD, Buzsaki G. 2003 Place representation within hippocampal networks is modified by long-term potentiation. Neuron 39, 843-853. (doi:10.1016/S0896-6273(03)00465-3)
23. Stickgold R, Hobson JA, Fosse R, Fosse M. 2001 Sleep, learning, and dreams: off-line memory reprocessing. Science 294, 1052-1057. (doi:10. 1126/science.1063530)
24. Diekelmann S, Born J. 2010 SLEEP: the memory function of sleep. Nat. Rev. Neurosci. 11, 114-126. (doi:10.1038/nrn2762-c2)
25. 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, 209-215. (doi:10.1038/nn2037)
26. Frank LM, Stanley GB, Brown EN. 2004 Hippocampal plasticity across multiple days of exposure to novel environments. J. Neurosci. 24, 7681-7689. (doi:10.1523/JNEUROSCI.1958-04.2004)
27. King C, Henze DA, Leinekugel X, Buzsaki G. 1999 Hebbian modification of a hippocampal population pattern in the rat. J. Physiol. 521, 159-167. (doi:10.1111/j.1469-7793.1999.00159.x)
28. Lever C, Wills T, Cacucci F, Burgess N, O'Keefe J. 2002 Long-term plasticity in hippocampal place-cell representation of environmental geometry. Nature 416, 90-94. (doi:10.1038/416090a)
29. Leutgeb JK, Leutgeb S, Treves A, Meyer R, Barnes CA, McNaughton BL, Moser MB, Moser EI. 2005 Progressive transformation of hippocampal neuronal representations in 'morphed' environments. Neuron 48, 345-358. (doi:10.1016/j.neuron.2005.09.007)
30. Dragoi G, Tonegawa S. 2011 Preplay of future place cell sequences by hippocampal cellular assemblies. Nature 469, 397. (doi:10.1038/nature09633)
31. Bonnevie T, Dunn B, Fyhn M, Hafting T, Derdikman D, Kubie JL, Roudi Y, Moser EI, Moser MB. 2013 Grid cells require excitatory drive from the hippocampus. Nat. Neurosci. 16, 309-317. (doi:10.1038/nn.3311)
32. Barry C, Ginzberg LL, O'Keefe J, Burgess N. 2012 Grid cell firing patterns signal environmental novelty by expansion. Proc. Natl Acad. Sci. USA 109, 17 687-17 692. (doi:10.1073/pnas.1209918109)
33. Carr MF, Jadhav SP, Frank LM. 2011 Hippocampal replay in the awake state: a potential substrate for memory consolidation and retrieval. Nat. Neurosci. 14, 147-153. (doi:10.1038/nn.2732)
34. O'Neill J, Pleydell-Bouverie B, Dupret D, Csicsvari J. 2010 Play it again: reactivation of waking experience and memory. Trends Neurosci. 33, 220-229. (doi:10.1016/j.tins.2010.01.006)
35. Cheng S, Frank LM. 2008 New experiences enhance coordinated neural activity in the hippocampus. Neuron 57, 303-313. (doi:10.1016/j.neuron. 2007.11.035)
36. Skaggs WE, McNaughton BL. 1996 Replay of neuronal firing sequences in rat hippocampus during sleep following spatial experience. Science 271, 1870-1873. (doi:10.1126/science.271.5257.1870)
37. Foster DJ, Wilson MA. 2006 Reverse replay of behavioural sequences in hippocampal place cells during the awake state. Nature 440, 680-683. (doi:10.1038/nature04587)
38. Hollup SA, Molden S, Donnett JG, Moser MB, Moser EI. 2001 Accumulation of hippocampal place fields at the goal location in an annular watermaze task. J. Neurosci. 21, 1635-1644.
39. 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, 995-1002. (doi:10. 1038/nn.2599)
40. McKenzie S, Robinson NTM, Herrera L, Churchill JC, Eichenbaum H. 2013 Learning causes reorganization of neuronal firing patterns to represent related experiences within a hippocampal schema. J. Neurosci. 33, 10 243-10 256. (doi:10.1523/ JNEUROSCI.0879-13.2013)
41. Dupret D, O'Neill J, Csicsvari J. 2013 Dynamic reconfiguration of hippocampal interneuron circuits during spatial learning. Neuron 78, 166-180. (doi:10.1016/j.neuron.2013.01.033)
42. Singer AC, Frank LM. 2009 Rewarded outcomes enhance reactivation of experience in the hippocampus. Neuron 64, 910-921. (doi:10.1016/j. neuron.2009.11.016)
43. 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, 1163-1173. (doi:10.1016/j.neuron. 2013.01.027)
44. Pfeiffer BE, Foster DJ. 2013 Hippocampal place-cell sequences depict future paths to remembered goals. Nature 497, 74. (doi:10.1038/nature12112)
45. Moscovitch M et al. 2005 Functional neuroanatomy of remote episodic, semantic and spatial memory: a unified account based on multiple trace theory. J. Anat. 207, 35-66. (doi:10.1111/j.1469-7580. 2005.00421.x)
46. Ji DY, Wilson MA. 2007 Coordinated memory replay in the visual cortex and hippocampus during sleep. Nat. Neurosci. 10, 100-107. (doi:10.1038/nn1825)
47. Lansink CS, Goltstein PM, Lankelma JV, McNaughton BL, Pennartz CM. 2009 Hippocampus leads ventral striatum in replay of place-reward information. PLoS Biol. 7, e1000173. (doi:10.1371/journal.pbio. 1000173)