Associative memory storage and retrieval: Involvement of theta oscillations in hippocampal information processing

Neural Plasticity

Volumn 2011, Issue , 2011, Pages

  Stella, Federico ^a   Treves, Alessandro ^a,b  

^a SISSA   (Italy)

^b NORWEGIAN UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Norway)

Author keywords

[No Author keywords available]

Indexed keywords

ACETYLCHOLINE;

ARTICLE; ASSOCIATIVE MEMORY; DENTATE GYRUS; ELECTRIC POTENTIAL; ENTORHINAL CORTEX; HIPPOCAMPAL CA1 REGION; HIPPOCAMPAL CA3 REGION; HIPPOCAMPUS THETA RHYTHM; INFORMATION PROCESSING; LONG TERM POTENTIATION; MEMORY CONSOLIDATION; NONHUMAN; OSCILLATION; OSCILLATOR; PERFORANT NERVE TRACT; REM SLEEP; SPIKE WAVE; SYNAPTIC TRANSMISSION; ACTION POTENTIAL; ANIMAL; ASSOCIATION; BIOLOGICAL MODEL; COMPUTER SIMULATION; EXPLORATORY BEHAVIOR; HUMAN; LEARNING; MAMMAL; MEMORY; NERVE CELL; PHYSIOLOGY; PSYCHOLOGICAL MODEL; RAT; RECALL; REVIEW; THETA RHYTHM;

ACETYLCHOLINE; ACTION POTENTIALS; ANIMALS; ASSOCIATION LEARNING; CA1 REGION, HIPPOCAMPAL; CA3 REGION, HIPPOCAMPAL; COMPUTER SIMULATION; CUES; EXPLORATORY BEHAVIOR; HUMANS; MAMMALS; MEMORY; MENTAL RECALL; MODELS, NEUROLOGICAL; MODELS, PSYCHOLOGICAL; NEURONS; RATS; THETA RHYTHM;

EID: 81555213224     PISSN: 20905904     EISSN: 16875443     Source Type: Journal    
DOI: 10.1155/2011/683961     Document Type: Article

References (102)

1. Vinogradova O. S., Expression, control, and probable functional significance of the neuronal theta-rhythm Progress in Neurobiology 1995 45 6 523 583
2. Fries P., A mechanism for cognitive dynamics: neuronal communication through neuronal coherence Trends in Cognitive Sciences 2005 9 10 474 480 (Pubitemid 41338822)
3. Salinas E., Sejnowski T. J., Correlated neuronal activity and the flow of neural information Nature Reviews Neuroscience 2001 2 8 539 550 (Pubitemid 33679827)
4. Schroeder C. E., Lakatos P., Low-frequency neuronal oscillations as instruments of sensory selection Trends in Neurosciences 2009 32 1 9 18
5. Buehlmann A., Deco G., Optimal information transfer in the cortex through synchronization PLoS Computational Biology 2010 6 9
6. Hipp J. F., Engel A. K., Siegel M., Oscillatory synchronization in large-scale cortical networks predicts perception Neuron 2011 69 2 387 396
7. Varela F., Lachaux J. P., Rodriguez E., Martinerie J., The brainweb: phase synchronization and large-scale integration Nature Reviews Neuroscience 2001 2 4 229 239 (Pubitemid 33673064)
8. Miller R., Cortico-Hippocampal Interplay and the Representation of Contexts in the Brain 1991 New York, NY, USA Springer
9. Buzski G., Theta oscillations in the hippocampus Neuron 2002 33 3 325 340
10. Sirota A., Buzski G., Interaction between neocortical and hippocampal networks via slow oscillations Thalamus and Related Systems 2005 3 4 245 259
11. Jones M. W., Wilson M. A., Theta rhythms coordinate hippocampal- prefrontal interactions in a spatial memory task PLoS Biology 2005 3 12, article e402 1 13 (Pubitemid 41796337)
12. Siapas A. G., Lubenov E. V., Wilson M. A., Prefrontal phase locking to hippocampal theta oscillations Neuron 2005 46 1 141 151 (Pubitemid 40488318)
13. Montemurro M. A., Rasch M. J., Murayama Y., Logothetis N. K., Panzeri S., Phase-of-firing coding of natural visual stimuli in primary visual cortex Current Biology 2008 18 5 375 380
14. Belitski A., Panzeri S., Magri C., Logothetis N. K., Kayser C., Sensory information in local field potentials and spikes from visual and auditory cortices: time scales and frequency bands Journal of Computational Neuroscience 2010 29 3 533 545
15. Buzski G., Rhythms of the Brain 2006 New York, NY, USA Oxford University Press
16. Vanderwolf C. H., Hippocampal electrical activity and voluntary movement in the rat Electroencephalography and Clinical Neurophysiology 1969 26 4 407 418
17. Mizuseki K., Sirota A., Pastalkova E., Buzski G., Theta oscillations provide temporal windows for local circuit computation in the entorhinal-hippocampal loop Neuron 2009 64 2 267 280
18. Montgomery S. M., Sirota A., Buzski G., Theta and gamma coordination of hippocampal networks during waking and rapid eye movement sleep Journal of Neuroscience 2008 28 26 6731 6741
19. Montgomery S. M., Betancur M. I., Buzski G., Behavior-dependent coordination of multiple theta dipoles in the hippocampus Journal of Neuroscience 2009 29 5 1381 1394
20. Yoder R. M., Pang K. C. H., Involvement of GABAergic and cholinergic medial septal neurons in hippocampal theta rhythm Hippocampus 2005 15 3 381 392 (Pubitemid 40668357)
21. Hafting T., Fyhn M., Bonnevie T., Moser M. B., Moser E. I., Hippocampus-independent phase precession in entorhinal grid cells Nature 2008 453 7199 1248 1252 (Pubitemid 351913591)
22. Quilichini P., Sirota A., Buzski G., Intrinsic circuit organization and theta-gamma oscillation dynamics in the entorhinal cortex of the rat Journal of Neuroscience 2010 30 33 11128 11142
23. Deshmukh S. S., Yoganarasimha D., Voicu H., Knierim J. J., Theta modulation in the medial and the lateral entorhinal cortices Journal of Neurophysiology 2010 104 2 994 1006
24. Manns J. R., Zilli E. A., Ong K. C., Hasselmo M. E., Eichenbaum H., Hippocampal CA1 spiking during encoding and retrieval: relation to theta phase Neurobiology of Learning and Memory 2007 87 1 9 20 (Pubitemid 44667570)
25. Lubenov E. V., Siapas A. G., Hippocampal theta oscillations are travelling waves Nature 2009 459 7246 534 539
26. Royer S., Sirota A., Patel J., Buzski G., Distinct representations and theta dynamics in dorsal and ventral hippocampus Journal of Neuroscience 2010 30 5 1777 1787
27. Jung M. W., Wiener S. I., McNaughton B. L., Comparison of spatial firing characteristics of units in dorsal and ventral hippocampus of the rat Journal of Neuroscience 1994 14 12 7347 7356 (Pubitemid 24379745)
28. Fanselow M. S., Dong H. W., Are the dorsal and ventral hippocampus functionally distinct structures? Neuron 2010 65 1 7 19
29. Geisler C., Diba K., Pastalkova E., Mizuseki K., Royer S., Buzski G., Temporal delays among place cells determine the frequency of population theta oscillations in the hippocampus Proceedings of the National Academy of Sciences of the United States of America 2010 107 17 7957 7962
30. Freund T. F., Buzski G., Interneurons of the hippocampus Hippocampus 1998 6 347 470 (Pubitemid 126682925)
31. Klausberger T., Somogyi P., Neuronal diversity and temporal dynamics: the unity of hippocampal circuit operations Science 2008 321 5885 53 57 (Pubitemid 351956237)
32. Klausberger T., Magill P. J., Mrton L. F., Roberts J. D. B., Cobden P. M., Buzski G., Somogyi P., Brain-state- and cell-type-specific firing of hippocampal interneurons in vivo Nature 2003 421 6925 844 848 (Pubitemid 36254143)
33. Somogyi P., Klausberger T., Defined types of cortical interneurone structure space and spike timing in the hippocampus Journal of Physiology 2005 562 1 9 26 (Pubitemid 40207780)
34. Klausberger T., Mrton L. F., Baude A., Roberts J. D. B., Magill P. J., Somogyi P., Spike timing of dendrite-targeting bistratified cells during hippocampal network oscillations in vivo Nature Neuroscience 2004 7 1 41 47 (Pubitemid 38032166)
35. Halasy K., Buhl E. H., Lrinczi Z., Tams G., Somogyi P., Synaptic target selectivity and input of GABAergic basket and bistratified interneurons in the CA1 area of the rat hippocampus Hippocampus 1996 6 3 306 329 (Pubitemid 26275790)
36. Czurk A., Huxter J., Li Y., Hangya B., Muller R. U., Theta phase classification of interneurons in the hippocampal formation of freely moving rats Journal of Neuroscience 2011 31 8 2938 2947
37. Miles R., Tth K., Gulys A. I., Hjos N., Freund T. F., Differences between somatic and dendritic inhibition in the hippocampus Neuron 1996 16 4 815 823 (Pubitemid 26124058)
38. Lengyel M., Huhn Z., rdi P., Computational theories on the function of theta oscillations Biological Cybernetics 2005 92 6 393 408 (Pubitemid 40834169)
39. Orr G., Rao G., Houston F. P., McNaughton B. L., Barnes C. A., Hippocampal synaptic plasticity is modulated by theta rhythm in the fascia dentata of adult and aged freely behaving rats Hippocampus 2001 11 6 647 654 (Pubitemid 34065493)
40. Villarreal D. M., Gross A. L., Derrick B. E., Modulation of CA3 afferent inputs by novelty and theta rhythm Journal of Neuroscience 2007 27 49 13457 13467 (Pubitemid 350255337)
41. Hyman J. M., Wyble B. P., Goyal V., Rossi C. A., Hasselmo M. E., Stimulation in hippocampal region CA1 in behaving rats yields long-term potentiation when delivered to the peak of theta and long-term depression when delivered to the trough Journal of Neuroscience 2003 23 37 11725 11731 (Pubitemid 38021299)
42. Lisman J. E., Idiart M. A. P., Storage of 7 2 short-term memories in oscillatory subcycles Science 1995 267 5203 1512 1515
43. Skaggs W. E., McNaughton B. L., Wilson M. A., Barnes C. A., Theta phase precession in hippocampal neuronal populations and the compression of temporal sequences Hippocampus 1996 6 2 149 172 (Pubitemid 26232443)
44. O'Keefe J., Recce M. L., Phase relationship between hippocampal place units and the EEG theta rhythm Hippocampus 1993 3 3 317 330 (Pubitemid 23231466)
45. van der Meer M. A. A., Redish A. D., Theta phase precession in rat ventral striatum links place and reward information Journal of Neuroscience 2011 31 8 2843 2854
46. Huxter J. R., Senior T. J., Allen K., Csicsvari J., Theta phase-specific codes for two-dimensional position, trajectory and heading in the hippocampus Nature Neuroscience 2008 11 5 587 594 (Pubitemid 351595200)
47. Mehta M. R., Lee A. K., Wilson M. A., Role of experience and oscillations in transforming a rate code into a temporal code Nature 2002 417 6890 741 746 (Pubitemid 34640627)
48. Hasselmo M. E., Schnell E., Barkai E., Dynamics of learning and recall at excitatory recurrent synapses and cholinergic modulation in rat hippocampal region CA3 Journal of Neuroscience 1995 15 7 5249 5262
49. Hasselmo M. E., Wyble B. P., Wallenstein G. V., Encoding and retrieval of episodic memories: role of cholinergic and GABAergic modulation in the hippocampus Hippocampus 1996 6 6 693 708 (Pubitemid 27084755)
50. Hasselmo M. E., Schnell E., Laminar selectivity of the cholinergic suppression of synaptic transmission in rat hippocampal region CA1: computational modeling and brain slice physiology Journal of Neuroscience 1994 14 6 3898 3914 (Pubitemid 24174132)
51. Hasselmo M. E., Fehlau B. P., Differences in time course of ACh and GABA modulation of excitatory synaptic potentials in slices of rat hippocampus Journal of Neurophysiology 2001 86 4 1792 1802 (Pubitemid 32953228)
52. Hasselmo M. E., Bodeln C., Wyble B. P., A proposed function for hippocampal theta rhythm: separate phases of encoding and retrieval enhance reversal of prior learning Neural Computation 2002 14 4 793 817
53. Hasselmo M. E., What is the function of hippocampal theta rhythm?linking bahavioral data to phasic properties of field potential and unit recording data Hippocampus 2005 15 7 936 949 (Pubitemid 41556423)
54. Hasselmo M. E., Eichenbaum H., Hippocampal mechanisms for the context-dependent retrieval of episodes Neural Networks 2005 18 9 1172 1190 (Pubitemid 41642602)
55. Golding N. L., Staff N. P., Spruston N., Dendritic spikes as a mechanism for cooperative long-term potentiation Nature 2002 418 6895 326 331 (Pubitemid 34790683)
56. Hasselmo M. E., Hay J., Ilyn M., Gorchetchnikov A., Neuromodulation, theta rhythm and rat spatial navigation Neural Networks 2002 15 46 689 707 (Pubitemid 34947468)
57. Lee I., Rao G., Knierim J. J., A double dissociation between hippocampal subfields: differential time course of CA3 and CA1 place cells for processing changed environments Neuron 2004 42 5 803 815 (Pubitemid 38748793)
58. Leutgeb S., Leutgeb J. K., Treves A., Moser M. B., Moser E. I., Distinct ensemble codes in hippocampal areas CA3 and CA1 Science 2004 305 5688 1295 1298 (Pubitemid 39129235)
59. Guzowski J. F., Knierim J. J., Moser E. I., Ensemble dynamics of hippocampal regions CA3 and CA1 Neuron 2004 44 4 581 584 (Pubitemid 39531222)
60. Treves A., Computational constraints between retrieving the past and predicting the future, and the CA3-CA1 differentiation Hippocampus 2004 14 5 539 556 (Pubitemid 39107010)
61. Treves A., Quantitative estimation of the information relayed by the schaffer collaterals Journal of Computational Neuroscience 1995 2 3 259 272
62. Colgin L. L., Denninger T., Fyhn M., Hafting T., Bonnevie T., Jensen O., Moser M. B., Moser E. I., Frequency of gamma oscillations routes flow of information in the hippocampus Nature 2009 462 7271 353 357
63. Dupret D., O'Neill J., Pleydell-Bouverie B., Csicsvari J., The reorganization and reactivation of hippocampal maps predict spatial memory performance Nature Neuroscience 2010 13 8 995 1002
64. Nakashiba T., Young J. Z., McHugh T. J., Buhl D. L., Tonegawa S., Transgenic inhibition of synaptic transmission reveals role of CA3 output in hippocampal learning Science 2008 319 5867 1260 1264 (Pubitemid 351323025)
65. Nakashiba T., Buhl D. L., McHugh T. J., Tonegawa S., Hippocampal CA3 output is crucial for ripple-associated reactivation and consolidation of memory Neuron 2009 62 6 781 787
66. Treves A., Tashiro A., Witter M. E., Moser E. I., What is the mammalian dentate gyrus good for? Neuroscience 2008 154 4 1155 1172
67. Marr D., Simple memory: a theory for archicortex Philosophical transactions of the Royal Society of London. Series B 1971 262 841 23 81
68. McNaughton B. L., Morris R. G. M., Hippocampal synaptic enhancement and information storage within a distributed memory system Trends in Neurosciences 1987 10 10 408 415 (Pubitemid 17149102)
69. Treves A., Rolls E. T., Computational constraints suggest the need for two distinct input systems to the hippocampal CA3 network Hippocampus 1992 2 2 189 199
70. Cerasti E., Treves A., How informative are spatial CA3 representations established by the dentate gyrus? PLoS Computational Biology 2010 6 4
71. Leutgeb J. K., Leutgeb S., Moser M. B., Moser E. I., Pattern separation in the dentate gyrus and CA3 of the hippocampus Science 2007 315 5814 961 966 (Pubitemid 46281178)
72. Henze D. A., Wittner L., Buzski G., Single granule cells reliably discharge targets in the hippocampal CA3 network in vivo Nature Neuroscience 2002 5 8 790 795 (Pubitemid 34827598)
73. Jezek K., Henriksen E. J., Treves A., Moser E. I., Moser M.-B., Theta-paced flickering between place-cell maps in the hippocampus Nature. 2011. In press
74. Scarpetta S., Zhaoping L., Hertz J., Hebbian imprinting and retrieval in oscillatory neural networks Neural Computation 2002 14 10 2371 2396
75. Harris K. D., Csicsvari J., Hirase H., Dragoi G., Buzski G., Organization of cell assemblies in the hippocampus Nature 2003 424 6948 552 556 (Pubitemid 36975776)
76. Akrami A., Liu Y., Treves A., Jagadeesh B., Converging neuronal activity in inferior temporal cortex during the classification of morphed stimuli Cerebral Cortex 2009 19 4 760 776
77. Zugaro M. B., Arleo A., Berthoz A., Wiener S. I., Rapid spatial reorientation and head direction cells Journal of Neuroscience 2003 23 8 3478 3482 (Pubitemid 36531990)
78. Samsonovich A., McNaughton B. L., Path integration and cognitive mapping in a continuous attractor neural network model Journal of Neuroscience 1997 17 15 5900 5920 (Pubitemid 27310504)
79. Johnson A., Redish A. D., Neural ensembles in CA3 transiently encode paths forward of the animal at a decision point Journal of Neuroscience 2007 27 45 12176 12189 (Pubitemid 350085471)
80. Maurer A. P., Cowen S. L., Burke S. N., Barnes C. A., McNaughton B. L., Phase precession in hippocampal interneurons showing strong functional coupling to individual pyramidal cells Journal of Neuroscience 2006 26 52 13485 13492 (Pubitemid 46026480)
81. Csicsvari J., Hirase H., Czurk A., Mamiya A., Buzski G., Oscillatory coupling of hippocampal pyramidal cells and interneurons in the behaving rat Journal of Neuroscience 1999 19 1 274 287 (Pubitemid 29028968)
82. Torborg C. L., Nakashiba T., Tonegawa S., McBain C. J., Control of CA3 output by feedforward inhibition despite developmental changes in the excitation-inhibition balance Journal of Neuroscience 2010 30 46 15628 15637
83. Pouille F., Scanziani M., Enforcement of temporal fidelity in pyramidal cells by somatic feed-forward inhibition Science 2001 293 5532 1159 1163 (Pubitemid 32758100)
84. Szabadics J., Soltesz I., Functional specificity of mossy fiber innervation of GAB aergic cells in the hippocampus Journal of Neuroscience 2009 29 13 4239 4251
85. Acsdy L., Kamondi A., Sk A., Freund T., Buzski G., GABAergic cells are the major postsynaptic targets of mossy fibers in the rat hippocampus Journal of Neuroscience 1998 18 9 3386 3403 (Pubitemid 28186030)
86. Lawrence J. J., McBain C. J., Interneuron Diversity series: containing the detonationfeedforward inhibition in the CA3 hippocampus Trends in Neurosciences 2003 26 11 631 640 (Pubitemid 37338372)
87. Freund T. F., Interneuron Diversity series: rhythm and mood in perisomatic inhibition Trends in Neurosciences 2003 26 9 489 495 (Pubitemid 37025787)
88. Pouille F., Scanziani M., Routing of spike series by dynamic circuits in the hippocampus Nature 2004 429 6993 717 723 (Pubitemid 38833116)
89. Remondes M., Schuman E. M., Direct cortical input modulates plasticity and spiking in CA1 pyramidal neurons Nature 2002 416 6882 736 740 (Pubitemid 34429149)
90. Banks M. I., White J. A., Pearce R. A., Interactions between distinct GABA(A) circuits in hippocampus Neuron 2000 25 2 449 457
91. Ang C. W., Carlson G. C., Coulter D. A., Hippocampal CA1 circuitry dynamically gates direct cortical inputs preferentially at theta frequencies Journal of Neuroscience 2005 25 42 9567 9580 (Pubitemid 41510898)
92. Dragoi G., Buzski G., Temporal encoding of place sequences by hippocampal cell assemblies Neuron 2006 50 1 145 157
93. McNaughton B. L., Barnes C. A., Meltzer J., Sutherland R. J., Hippocampal granule cells are necessary for normal spatial learning but not for spatially-selective pyramidal cell discharge Experimental Brain Research 1989 76 3 485 496 (Pubitemid 19203600)
94. Lassalle J. M., Bataille T., Halley H., Reversible inactivation of the hippocampal mossy fiber synapses in mice impairs spatial learning, but neither consolidation nor memory retrieval, in the Morris navigation task Neurobiology of Learning and Memory 2000 73 3 243 257 (Pubitemid 30250104)
95. Lee I., Kesner R. P., Encoding versus retrieval of spatial memory: double dissociation between the dentate gyrus and the perforant path inputs into CA3 in the dorsal hippocampus Hippocampus 2004 14 1 66 76 (Pubitemid 38351173)
96. Buzski G., Hippocampal sharp waves: their origin and significance Brain Research 1986 398 2 242 252
97. Csicsvari J., Hirase H., Mamiya A., Buzski G., Ensemble patterns of hippocampal CA3-CA1 neurons during sharp wave-associated population events Neuron 2000 28 2 585 594
98. Isomura Y., Sirota A., zen S., Montgomery S., Mizuseki K., Henze D. A., Buzski G., Integration and segregation of activity in entorhinal-hippocampal subregions by neocortical slow oscillations Neuron 2006 52 5 871 882 (Pubitemid 44828448)
99. Karlsson M. P., Frank L. M., Awake replay of remote experiences in the hippocampus Nature Neuroscience 2009 12 7 913 918
100. Cheng S., Frank L. M., New experiences enhance coordinated neural activity in the hippocampus Neuron 2008 57 2 303 313
101. Sullivan D., Csicsvari J., Mizuseki K., Montgomery S., Diba K., Buzski G., Relationships between hippocampal sharp waves, ripples, and fast gamma oscillation: influence of dentate and entorhinal cortical activity Journal of Neuroscience 2011 31 23 8605 8616
102. Tsodyks M. V., Skaggs W. E., Sejnowski T. J., McNaughton B. L., Population dynamics and theta rhythm phase precession of hippocampal place cell firing: a spiking neuron model Hippocampus 1996 6 3 271 280 (Pubitemid 26275787)