Relationships between hippocampal sharp waves, ripples, and fast gamma oscillation: Influence of dentate and entorhinal cortical activity

Journal of Neuroscience

Volumn 31, Issue 23, 2011, Pages 8605-8616

  Sullivan, David ^a   Csicsvari, Jozsef ^a,b   Mizuseki, Kenji ^a   Montgomery, Sean ^a   Diba, Kamran ^a,c   Buzsáki, György ^a  

^a RUTGERS UNIVERSITY   (United States)

^b UNIVERSITY OF OXFORD   (United Kingdom)

^c UNIVERSITY OF WISCONSIN MILWAUKEE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL CELL; ARTICLE; BRAIN REGION; CONTROLLED STUDY; DENTATE GYRUS; ELECTRIC POTENTIAL; ELECTROENCEPHALOGRAM; ENTORHINAL CORTEX; FAST GAMMA OSCILLATION; GRANULE CELL; HIPPOCAMPUS; HIPPOCAMPUS SHARP WAVE; MALE; NONHUMAN; OSCILLATION; PRIORITY JOURNAL; RAT; RIPPLE OSCILLATION; STRATUM PYRAMIDALE; STRATUM RADIATUM;

ACTION POTENTIALS; ANIMALS; ELECTROPHYSIOLOGY; ENTORHINAL CORTEX; HIPPOCAMPUS; MALE; NERVE NET; NEURONS; RATS; RATS, LONG-EVANS; RATS, SPRAGUE-DAWLEY;

EID: 79958294518     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.0294-11.2011     Document Type: Article

References (113)

1. Anastassiou CA, Montgomery SM, Barahona M, Buzsáki G, Koch C (2010) The effect of spatially inhomogeneous extracellular electric fields on neurons. J Neurosci 30:1925-1936.
2. Axmacher N, Helmstaedter C, Elger CE, Fell J (2008) Enhancement of neocortical-medial temporal EEG correlations during non-REM sleep. Neural Plast 2008:563028.
3. Bartos M, Vida I, Jonas P (2007) Synaptic mechanisms of synchronized gamma oscillations in inhibitory interneuron networks. Nat Rev Neuro-sci 8:45-56.
4. Battaglia FP, Sutherland GR, McNaughton BL (2004) Hippocampal sharp wave bursts coincide with neocortical "up-state" transitions. Learn Mem 11:697-704.
5. 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 8:1560-1567.
6. Behrens CJ, van den Boom LP, Heinemann U (2007) Effects of the GABA(A) receptor antagonists bicuculline and gabazine on stimulus-induced sharp wave-ripple complexes in adult rat hippocampus in vitro. Eur J Neurosci 25:2170-2181.
7. Both M, Bähner F, von Bohlen Halbach O, Draguhn A (2008) Propagation of specific network patterns through the mouse hippocampus. Hippocampus 18:899-908.
8. Bragin A, Jando G, Nadasdy Z, van Landeghem M, Buzsáki G (1995) Dentate EEG spikes and associated population burstsinthe hippocampal hilar region of the rat. J Neurophysiol 73:1691-1705.
9. Bragin A, Engel J Jr, Wilson CL, Fried I, Buzsáki G (1999a) High-frequency oscillations in human brain. Hippocampus 9:137-142.
10. Bragin A, Engel J Jr, Wilson CL, Fried I, Mathern GW (1999b) Hippocampal and entorhinal cortex high-frequency oscillations (100-500 Hz) in human epileptic brain and in kainic acid-treated rats with chronic seizures. Epilepsia 40:127-137.
11. Bragin A, Wilson CL, Engel J Jr (2000) Chronic epileptogenesis requires development of a network of pathologically interconnected neuron clusters: a hypothesis. Epilepsia 41 [Suppl 6]:S144-S152.
12. Brunel N, Wang XJ (2003) What determines the frequency of fast network oscillations with irregular neural discharges? I. Synaptic dynamics and excitation-inhibition balance. J Neurophysiol 90:415-430.
13. Buhl DL, Buzsáki G (2005) Developmental emergence of hippocampal fast-field "ripple" oscillations in the behaving rat pups. Neuroscience 134:1423-1430.
14. Buzsáki G (1986) Hippocampal sharp waves: their origin and significance. Brain Res 398:242-252.
15. Buzsáki G (1989) A two-stage model of memory trace formation: A role for "noisy" brain states. Neuroscience 31:551-570.
16. Buzsáki G (1996) The hippocampo-neocortical dialogue. Cereb Cortex 6:81-92.
17. Buzsáki G (2006) Rhythms of the brain. New York: Oxford UP.
18. Buzsáki G, Leung LW, Vanderwolf CH (1983) Cellular bases of hippocam-pal EEG in the behaving rat. Brain Res Rev 287:139-171.
19. Buzsáki G, Horvath Z, Urioste R, Hetke J, Wise K (1992) High-frequency network oscillation in the hippocampus. Science 256:1025-1027.
20. Buzsáki G, Buhl DL, Harris KD, Csicsvari J, Czeh B, Morozov A (2003a) Hippocampal network patterns of activity in the mouse. Neuroscience 116:201-211.
21. Buzsáki G, Carpi D, Csicsvari J, Dragoi G, Harris KD, Henze DA, Hirase H (2003b) Maintenance and modification of firing rates and sequences in the hippocampus: does sleep play a role? In: Sleep and plasticity (Maquet P, Smith C, Stickgold R, eds), pp 247-270. Oxford: Oxford UP.
22. Canolty RT, Edwards E, Dalal SS, Soltani M, Nagarajan SS, Kirsch HE, Berger MS, Barbaro NM, Knight RT (2006) High gamma power is phase-locked to theta oscillations in human neocortex. Science 313:1626-1628.
23. Chrobak JJ, Buzsáki G (1996) High-frequency oscillationsinthe output networks of the hippocampal-entorhinal axis of the freely behaving rat. J Neurosci 16:3056-3066.
24. Clemens Z, Mölle M, Eröss, L, Jakus R, Rásonyi G, Halász P, Born J (2010) Fine-tuned coupling between human parahippocampal ripples and sleep spindles. Eur J Neurosci 33:511-520.
25. Colgin LL, Kubota D, Brucher FA, Jia Y, Branyan E, Gall CM, Lynch G (2004) Spontaneous waves in the dentate gyrus of slices from the ventral hippocampus. J Neurophysiol 92:3385-3398.
26. Colgin LL, Jia Y, Sabatier JM, Lynch G (2005) Blockade of NMDA receptors enhances spontaneous sharp waves in rat hippocampal slices. Neurosci Lett 385:46-51.
27. Colgin LL, Denninger T, Fyhn M, Hafting T, Bonnevie T, Jensen O, Moser MB, Moser EI (2009) Frequency of gamma oscillations routes flow of information in the hippocampus. Nature 462:353-357.
28. Csicsvari J, Hirase H, Czurko A, Mamiya A, Buzsáki G (1999a) Oscillatory coupling of hippocampal pyramidal cells and interneurons in the behaving rat. J Neurosci 19:274-287.
29. Csicsvari J, Hirase H, Czurkó A, Mamiya A, Buzsáki G (1999b) Fast network oscillationsinthe hippocampal CA1 regionofthe behaving rat. J Neurosci 19:RC20.
30. Csicsvari J, Hirase H, Mamiya A, Buzsáki G (2000) Ensemble patterns of hippocampal CA3-CA1 neurons during sharp wave-associated population events. Neuron 28:585-594.
31. Csicsvari J, Jameison B, Wise KD, Buzsáki G (2003) Mechanisms of gamma oscillations in the hippocampus of the behaving rat. Neuron 37:311-322.
32. Diba K, Buzsáki G (2007) Forward and reverse hippocampal place-cell sequences during ripples. Nat Neurosci 10:1241-1242.
33. Diba K, Montgomery SM, Harris KD, Buzsáki G (2005) Identification of silicon probe irregularities using analysis of in vivo recordings. Soc Neu-rosci Abstr 31:275.10.
34. Draguhn A, Traub RD, Schmitz D, Jefferys JG (1998) Electrical coupling underlies high-frequency oscillations in the hippocampus in vitro. Nature 394:189-192.
35. 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.
36. Dzhala VI, Staley KJ (2004) Mechanisms of fast ripplesinthe hippocampus. J Neurosci 24:8896-8906.
37. Ego-Stengel V, Wilson MA (2010) Disruption of ripple-associated hip-pocampal activity during rest impairs spatial learning in the rat. Hippocampus 20:1-10.
38. Ellender TJ, Nissen W, Colgin LL, Mann EO, Paulsen O (2010) Priming of hippocampal population bursts by individual perisomatic-targeting in-terneurons. J Neurosci 30:5979-5991.
39. Eschenko O, Ramadan W, Mölle M, Born J, Sara SJ (2008) Sustained increase in hippocampal sharp-wave ripple activity during slow-wave sleep after learning. Learn Mem 15:222-228.
40. Foffani G, Uzcategui YG, Gal B, Menendez de la Prida L (2007) Reduced spike-timing reliability correlates with the emergence of fast ripples in the rat epileptic hippocampus. Neuron 55:930-941.
41. Foster DJ, Wilson MA (2006) Reverse replay of behavioural sequences in hippocampal place cells during the awake state. Nature 440:680-683.
42. Girardeau G, Benchenane K, Wiener SI, Buzsáki G, Zugaro MB (2009) Selective suppression of hippocampal ripples impairs spatial memory. Nat Neurosci 12:1222-1223.
43. Hafting T, Fyhn M, Molden S, Moser MB, Moser EI (2005) Microstructure of a spatial map in the entorhinal cortex. Nature 436:801-806.
44. Hahn TT, Sakmann B, Mehta MR (2007) Differential responses of hip-pocampal subfields to cortical up-down states. Proc Natl Acad Sci U S A 104:5169-5174.
45. Hasselmo ME, Bower JM (1993) Acetylcholine and memory. Trends Neu-rosci 16:218-222.
46. Hazan L, Zugaro M, Buzsáki G (2006) Klusters, Neuro Scope, ND Manager: A free software suite neurophysiological data processing and visualization. J Neurosci Methods 155:207-216.
47. Ibarz JM, Foffani G, Cid E, Inostroza M, Menendez de la Prida L (2010) Emergent dynamics of fast ripples in the epileptic hippocampus. J Neu-rosci 30:16249-16261.
48. Ishizuka N, Weber J, Amaral DG (1990) Organization of intrahippocampal projections originating from CA3 pyramidal cells in the rat. J Comp Neu-rol 295:580-623.
49. Isomura Y, Sirota A, Ozen S, Montgomery S, Mizuseki K, Henze DA, Buzsáki G (2006) Integration and segregation of activity in entorhinal-hippocampal subregions by neocortical slow oscillations. Neuron 52:871-882.
50. Ji D, Wilson MA (2007) Coordinated memory replay in the visual cortex and hippocampus during sleep. Nat Neurosci 10:100-107.
51. Jiruska P, Finnerty GT, Powell AD, Lofti N, Cmejla R, Jefferys JG (2010) Epileptic high-frequency network activity in a model of nonlesional temporal lobe epilepsy. Brain. 133:1380-1390.
52. Karlsson MP, Frank LM (2008) Network dynamics underlying the formation of sparse, informative representations in the hippocampus. J Neuro-sci 28:14271-14281.
53. Karlsson MP, Frank LM (2009) Awake replay of remote experiences in the hippocampus. Nat Neurosci 12:913-918.
54. Klausberger T, Somogyi P (2008) Neuronal diversity and temporal dynamics: the unity of hippocampal circuit operations. Science 321:53-57.
55. Klausberger T, Magill PJ, Marton LF, Roberts JD, Cobden PM, Buzsáki G, Somogyi P (2003) Brain-state- and cell-type-specific firing of hip-pocampal interneurons in vivo. Nature 421:844-848.
56. Kubota D, Colgin LL, Casale M, Brucher FA, Lynch G (2003) Endogenous waves in hippocampal slices. J Neurophysiol 89:81-89.
57. Kudrimoti HS, Barnes CA, McNaughton BL (1999) Reactivation of hip-pocampal cell assemblies: effects of behavioral state, experience, and EEG dynamics. J Neurosci 19:4090-4101.
58. Le Van Quyen M, Staba R, Bragin A, Dickson C, Valderrama M, Fried I, Engel J (2010) Large-scale microelectrode recordings of high-frequency gamma oscillations in human cortex during sleep. J Neurosci 30:7770-7782.
59. Lee AK, Wilson MA (2002) Memory of sequential experience in the hippocampus during slow wave sleep. Neuron 36:1183-1194.
60. Leinekuge lX, Khazipov R, Cannon R, Hirase H, Ben-Ari Y, Buzsáki G (2002) Correlated bursts of activity in the neonatal hippocampus in vivo. Science 296:2049-2052.
61. Leopold DA, Murayama Y, Logothetis NK (2003) Very slow activity fluctu-ationsin monkey visual cortex: implications for functional brain imaging. Cereb Cortex 13:422-433.
62. Li XG, Somogyi P, Ylinen A, Buzsáki G (1994) The hippocampal CA3 network: aninvivo intracellular labeling study. J Comp Neurol 339:181-208.
63. Liotta A, Caliskan G, Haq RU, Hollnagel JO, Roesler A, Heinemann U, Behrens CJ (2011) Partial disinhibition is required for transition of stimulus-induced sharp wave-ripple complexes to recurrent epilepti-form discharges in rat hippocampal slices. J Neurophysiol 105:172-187.
64. Lubenov EV, Siapas AG (2008) Decoupling through synchrony in neuronal circuits with propagation delays. Neuron 58:118-131.
65. Maier N, Nimmrich V, Draguhn A (2003) Cellular and network mechanisms underlying spontaneous sharp wave-ripple complexes in mouse hippocampal slices. J Physiol 550:873-887.
66. Mann EO, Suckling JM, Hajos N, Greenfield SA, Paulsen O (2005) Periso-matic feedback inhibition underlies cholinergically induced fast network oscillations in the rat hippocampus in vitro. Neuron 45:105-117.
67. 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.
68. Memmesheimer RM (2010) Quantitative prediction of intermittent high-frequency oscillations in neural networks with supralinear dendritic interactions. Proc Natl Acad Sci U S A 107:11092-11097.
69. Mitra PP, Bokil H (2007) Observed brain dynamics. Cambridge, UK: Oxford UP.
70. Mitra PP, Pesaran B (1999) Analysis of dynamic brain imaging data. Bio-phys J 1999 76:691-708.
71. Mitzdorf U (1985) Current source-density method and application in cat cerebral cortex: investigation of evoked potentials and EEG phenomena. Physiol Rev 65:37-100.
72. Mizuseki K, Sirota A, Pastalkova E, Buzsáki G (2009) Theta oscillations provide temporal windows for local circuit computation in the entorhinal-hippocampal loop. Neuron 64:267-280.
73. Mölle M, Yeshenko O, Marshall L, Sara SJ, Born J (2006) Hippocampal sharp wave-ripples linked to slow oscillations in rat slow-wave sleep. J Neurophysiol 96:62-70.
74. Mölle 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 29:1071-1081.
75. Montgomery SM, Buzsáki G (2007) Gamma oscillations dynamically couple hippocampal CA3 and CA1 regions during memory task performance. Proc Natl Acad Sci U S A 104:14495-14500.
76. Montgomery SM, Sirota A, Buzsaki G (2008) Theta and gamma coordination of hippocampal networks during waking and rapid eye movement sleep. J Neurosci 28:6731-6741.
77. Montgomery SM, Betancur MI, Buzsáki G (2009) Behavior-dependent coordination of multiple theta dipoles in the hippocampus. J Neurosci 29:1381-1394.
78. Mukovski M, Chauvette S, Timofeev I, Volgushev M (2007) Detection of active and silent states in neocortical neurons from the field potential signal during slow-wave sleep. Cereb Cortex 17:400-414.
79. Nadasdy Z, Hirase H, Czurko A, Csicsvari J, Buzsáki G (1999) Replay and time compression of recurring spike sequences in the hippocampus. J Neurosci 19:9497-9507.
80. Nakashiba T, Buhl DL, McHugh TJ, Tonegawa S (2009) Hippocampal CA3 output is crucial for ripple-associated reactivation and consolidation of memory. Neuron 62:781-787.
81. Nguyen DP, Kloosterman F, Barbieri R, Brown EN, Wilson MA (2009) Characterizing the dynamic frequency structure of fast oscillations in the rodent hippocampus. Front Integr Neurosci 3:11.
82. Nokia MS, Penttonen M, Wikgren J (2010) Hippocampal ripple-contingent training accelerates trace eyeblink conditioning and retards extinction in rabbits. J Neurosci 30:11486-11492.
83. O'Keefe J and Nadel L (1978) The hippocampus as a cognitive map. Cambridge, UK: Oxford UP.
84. 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.
85. 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.
86. Pais I, Hormuzdi SG, Monyer H, Traub RD, Wood IC, Buhl EH, Whittington MA, LeBeau FE (2003) Sharp wave-like activity in the hippocampus in vitroin mice lacking the gap junction protein connexin 36. JNeurophysiol 89:2046-2054.
87. Papatheodoropoulos C, Koniaris E (2010) a5GABA(A) receptors regulate hippocampal sharp wave-ripple activity in vitro. Neuropharmacology 60:662-673.
88. Papatheodoropoulos C, Kostopoulos G (2002) Spontaneous, low frequency (approximately 2-3 Hz) field activity generated in rat ventral hippocam-pal slices perfused with normal medium. Brain Res Bull 57:187-193.
89. Pikovsky A, Rosenblum M, Kurths J (2001) Synchronization: a universal concept in nonlinear sciences. Cambridge, UK: Cambridge UP.
90. Ponomarenko AA, Li JS, Korotkova TM, Huston JP, Haas HL (2008) Frequency of network synchronization in the hippocampus marks learning. Eur J Neurosci 27:3035-3042.
91. Ramadan W, Eschenko O, Sara SJ (2009) Hippocampal sharp wave/ripples during sleep for consolidation of associative memory. PloS One 4:e6697.
92. Reichinnek S, Künsting T, Draguhn A, Both M (2010) Field potential signature of distinct multicellular activity patterns in the mouse hippocampus. J Neurosci 30:15441-15449.
93. Sakata S, Harris KD (2009) Laminar structure of spontaneous and sensory-evoked population activity in auditory cortex. Neuron 64:404-418.
94. Schmitz D, Schuchmann S, Fisahn A, Draguhn A, Buhl EH, Petrasch-Parwez E, Dermietzel R, Heinemann U, Traub RD (2001) Axo-axonal coupling. a novel mechanism for ultrafast neuronal communication. Neuron 31:831-840.
95. Siapas AG, Wilson MA (1998) Coordinated interactions between hippocampal ripples and cortical spindles during slow-wave sleep. Neuron 21:1123-1128.
96. Singer AC, Frank LM (2009) Rewarded outcomes enhance reactivation of experience in the hippocampus. Neuron 64:910-921.
97. Sirota A, Csicsvari, J., Buhl D, Buzsaki G (2003) Communication between neocortex and hippocampus during sleep in rats and mice. Proc Natl Acad Sci USA 100:2065-2069.
98. Skaggs WE, McNaughton BL (1996) Replay of neuronal firing sequences in rat hippocampus during sleep following spatial experience. Science 271:1870-1873.
99. Staba RJ, Wilson CL, Bragin A, Fried I, Engel J Jr (2002) Quantitative analysis of high-frequency oscillations (80-500 Hz) recorded in human epileptic hippocampus and entorhinal cortex. J Neurophysiol 88:1743-1752.
100. Steriade M, Nunez A, Amzica F (1993) A novel slow (<1 Hz) oscillation of neocortical neurons in vivo: depolarizing and hyperpolarizing components. J Neurosci 13:3252-3265.
101. Suzuki SS, Smith GK (1987) Spontaneous EEG spikes in the normal hippocampus. I. Behavioral correlates, laminar profiles and bilateral synchrony. Electroencephalogr Clin Neurophysiol 67:348-359.
102. Tass P, Rosenblum MG, Weule J, Kurths J, Pikovsky AS, Volkmann J, Schnit-zler A, Freund HJ (1998) Detection of n:m phase locking from noise data: application to magnetoencephalography. Phys Rev Lett 81: 3291-3294.
103. Taxidis J, Coombes S, Mason R, Owen MR (2011) Modeling sharp wave-ripple complexes through a CA3-CA1 network model with chemical synapses. Hippocampus. Advance online publication. Retrieved March 30, 2011. doi:10.1002/hip.20930.
104. Traub R, Bibbig A (2000) A model of high frequency ripples in the hippocampus based on synaptic coupling plus axon-axon gap junctions between pyramidal neurons. J Neurosci 20:2086-2093.
105. Traub RD (2003) Fast Oscillations and Epilepsy. Epilepsy Curr 3:77-79.
106. Traub RD, Draguhn A, Whittington MA, Baldeweg T, Bibbig A, Buhl EH, Schmitz D (2002) Axonal gap junctions between principal neurons: a novel source of network oscillations, and perhaps epileptogenesis. Rev Neurosci 13:1-30.
107. Wang XJ (2010) Neurophysiological and computational principles of cortical rhythms in cognition. Physiol Rev 90:1195-1268.
108. Whittington MA, Cunningham MO, LeBeau FE, Racca C, Traub RD (2011) Multiple origins of the cortical gamma rhythm. Dev Neurobiol 71:92-106.
109. Wilson MA, McNaughton BL (1994) Reactivation of hippocampal ensemble memories during sleep. Science 265:676-679.
110. Wittner L, Henze DA, Zaborszky L, Buzsaki G (2007) Three-dimensional reconstruction of the axon arbor of a CA3 pyramidal cell recorded and filled in vivo. Brain Struct Funct 212:75-83.
111. Wolansky T, Clement EA, Peters SR, Palczak MA, Dickson CT (2006) Hippocampal slow oscillation: a novel EEG state and its coordination with ongoing neocortical activity. J Neurosci 26:6213-6229.
112. Wu C, Asl MN, Gillis J, Skinner FK, Zhang L (2005) An in vitro model of hippocampal sharp waves: regional initiation and intracellular correlates. J Neurophysiol 94:e741-e753.
113. 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 15:30-46.