The role of phase synchronization in memory processes (original) (raw)

References

1. Buzsáki, G. Rhythms of the Brain (Oxford University Press, New York, 2006).
   Google Scholar
2. Steriade, M. Impact of network activities on neuronal properties in corticothalamic systems. J. Neurophysiol. 86, 1–39 (2001).
   CAS PubMed Google Scholar
3. Buzsáki, G. & Draguhn, A. Neuronal oscillations in cortical networks. Science 304, 1926–1929 (2004).
   PubMed Google Scholar
4. Lakatos, P. et al. An oscillatory hierarchy controlling neuronal excitability and stimulus processing in the auditory cortex. J. Neurophysiol. 94, 1904–1911 (2005).
   PubMed Google Scholar
5. Elbert, T. & Rockstroh, B. Threshold regulation — a key to the understanding of the combined dynamics of EEG and event-related potentials. J. Psychophysiol. 4, 317–333 (1987).
   Google Scholar
6. Fröhlich, F. & McCormick, D. A. Endogenous electric fields may guide neocortical network activity. Neuron 67, 129–143 (2010).
   PubMed PubMed Central Google Scholar
7. Roelfsema, P. R., Engel, A. K., König, P. & Singer, W. Visuomotor integration is associated with zero time-lag synchronization among cortical areas. Nature 385, 157–161 (1997).
   CAS PubMed Google Scholar
8. Rodriguez, E. et al. Perception's shadow, long-distance synchronization of human brain activity. Nature 397, 430–433 (1999).
   CAS PubMed Google Scholar
9. Engel, A. K., Fries, P. & Singer, W. Dynamic predictions, oscillations and synchrony in top-down processing. Nature Rev. Neurosci. 2, 704–716 (2001).
   CAS Google Scholar
10. Fries, P., Reynolds, J. H., Rorie, A. E. & Desimone, R. Modulation of oscillatory neuronal synchronization by selective visual attention. Science 291, 1560–1563 (2001).
    CAS PubMed Google Scholar
11. Cavanagh, J. F., Cohen, M. X. & Allen, J. J. Prelude to and resolution of an error, EEG phase synchrony reveals cognitive control dynamics during action monitoring. J. Neurosci. 29, 98–105 (2009).
    CAS PubMed PubMed Central Google Scholar
12. Eckhorn, R. et al. Coherent oscillations, a mechanism of feature linking in the visual cortex? Multiple electrode and correlation analyses in the cat. Biol. Cybern. 60, 121–130 (1988).
    CAS PubMed Google Scholar
13. Gray, C. M., König, P., Engel, A. K. & Singer, W. Oscillatory responses in cat visual cortex exhibit inter-columnar synchronization which reflects global stimulus properties. Nature 338, 334–337 (1989).
    CAS PubMed Google Scholar
14. Fries, P. A mechanism for cognitive dynamics, neuronal communication through neuronal coherence. Trends Cogn. Sci. 9, 474–480 (2005).
    PubMed Google Scholar
15. König, P., Engel, A. K. & Singer, W. Integrator or coincidence detector? The role of the cortical neuron revisited. Trends Neurosci. 19, 130–137 (1996).
    PubMed Google Scholar
16. Azouz, R. & Gray, C. M. Dynamic spike threshold reveals a mechanism for synaptic coincidence detection in cortical neurons in vivo. Proc. Natl Acad. Sci. USA 97, 8110–8115 (2000).
    CAS PubMed PubMed Central Google Scholar
17. Daoudal, G. & Debanne, D. Long-term plasticity of intrinsic excitability: learning rules and mechanisms. Learn. Mem. 10, 456–465 (2003).
    PubMed Google Scholar
18. Fries, P., Neuenschwader, S., Engel, A. K., Goebel, R. & Singer, W. Rapid feature selective neuronal synchronization through correlated latency shifting. Nature Neurosci. 4, 194–200 (2001).
    CAS PubMed Google Scholar
19. Jacobs, J., Kahana, M. J., Ekstrom, A. D. & Fried, I. Brain oscillations control timing of single-neuron activity in humans. J. Neurosci. 27, 3839–3844 (2007).
    CAS PubMed PubMed Central Google Scholar
20. Womelsdorf, T. et al. Modulation of neuronal interactions through neuronal synchronization. Science 316, 1609–1612 (2007). A pivotal empirical study supporting the hypothesis that phase synchronization facilitates neuronal communication ('communication through coherence').
    CAS PubMed Google Scholar
21. Vinck, M. et al. Gamma-phase shifting in awake monkey visual cortex. J. Neurosci. 30, 1250–1257 (2010).
    CAS PubMed PubMed Central Google Scholar
22. Llinas, R. R., Leznik, E. & Urbano, F. J. Temporal binding via cortical coincidence detection of specific and nonspecific thalamocortical inputs: a voltage-dependent dye-imaging study in mouse brain slices. Proc. Natl Acad. Sci. USA 99, 449–454 (2002).
    CAS PubMed PubMed Central Google Scholar
23. Volgushev, M., Chistiakova, M. & Singer, W. Modification of discharge patterns of neocortical neurons by induced oscillations of the membrane potential. Neuroscience 83, 15–25 (1998).
    CAS PubMed Google Scholar
24. Miltner, W. H., Braun, C., Arnold, M., Witte, H. & Taub, E. Coherence of gamma-band EEG activity as a basis for associative learning. Nature 397, 434–436 (1999). One of the first studies describing the role of neural synchronization (in this case EEG coherence) in long-term memory processes.
    CAS PubMed Google Scholar
25. Weiss, S. & Rappelsberger, P. Long-range EEG synchronization during word encoding correlates with successful memory performance. Brain Res. Cogn. Brain Res. 9, 299–312 (2000).
    CAS PubMed Google Scholar
26. Fell, J. et al. Human memory formation is accompanied by rhinal-hippocampal coupling and decoupling. Nature Neurosci. 4, 1259–1264 (2001).
    CAS PubMed Google Scholar
27. Summerfield, C. & Mangels, J. A. Coherent theta-band EEG activity predicts item-context binding during encoding. Neuroimage 24, 692–703 (2005).
    PubMed Google Scholar
28. Fell, J. et al. Rhinal-hippocampal connectivity determines memory formation during sleep. Brain 129, 108–114 (2006).
    PubMed Google Scholar
29. Sato, N. & Yamaguchi, Y. Theta synchronization networks emerge during human object-place memory encoding. Neuroreport 18, 419–424 (2007).
    PubMed Google Scholar
30. Fell, J., Ludowig, E., Rosburg, T., Axmacher, N. & Elger, C. E. Phase-locking within human mediotemporal lobe predicts memory formation. Neuroimage 43, 410–419 (2008). The first study to directly compare the predictive power of different medial temporal EEG measures for long-term memory formation — namely, phase synchronization, inter-trial phase locking and spectral power changes.
    PubMed Google Scholar
31. Babiloni, C. et al. Hippocampal, amygdala, and neocortical synchronization of theta rhythms is related to an immediate recall during Rey auditory verbal learning test. Hum. Brain Mapp. 30, 2077–2089 (2009).
    PubMed Google Scholar
32. Benchenane, K. et al. Coherent theta oscillations and reorganization of spike timing in the hippocampal-prefrontal network upon learning. Neuron 66, 921–936 (2010).
    CAS PubMed Google Scholar
33. Axmacher, N., Mormann, F., Fernández, G., Elger, C. E. & Fell, J. Memory formation by neuronal synchronization. Brain Res. Rev. 52, 170–182 (2006).
    PubMed Google Scholar
34. Jutras, M. J. & Buffalo, E. A. Synchronous neural activity and memory formation. Curr. Opin. Neurobiol. 20, 150–155 (2010).
    CAS PubMed PubMed Central Google Scholar
35. Markram, H., Lübke, J., Frotscher, M. & Sakmann, B. Regulation of synaptic efficacy by coincidence of postsynaptic APs and EPSPs. Science 275, 213–215 (1997).
    CAS PubMed Google Scholar
36. Abbott, L. F. & Nelson, S. B. Synaptic plasticity: taming the beast. Nature Neurosci. 3, 1178–1183 (2000).
    CAS PubMed Google Scholar
37. Caporale, N. & Dan, Y. Spike timing-dependent plasticity, a Hebbian learning rule. Annu. Rev. Neurosci. 31, 25–46 (2008).
    CAS PubMed Google Scholar
38. Buzsáki, G., Leung, L. W. & Vanderwolf, C. H. Cellular bases of hippocampal EEG in the behaving rat. Brain Res. 287, 139–171 (1983).
    PubMed Google Scholar
39. Maurer, A. P. & McNaughton, B. L. Network and intrinsic cellular mechanisms underlying theta phase precession of hippocampal neurons. Trends Neurosci. 30, 325–333 (2007).
    CAS PubMed Google Scholar
40. Bragin, A. et al. Gamma (40–100 Hz) oscillation in the hippocampus of the behaving rat. J. Neurosci. 15, 47–60 (1995).
    CAS PubMed PubMed Central Google Scholar
41. Sarnthein, J., Petsche, H., Rappelsberger, P., Shaw, G. L. & von Stein, A. Synchronization between prefrontal and posterior association cortex during human working memory. Proc. Natl Acad. Sci. USA 95, 7092–7096 (1998).
    CAS PubMed PubMed Central Google Scholar
42. Fell, J. et al. Rhinal-hippocampal theta coherence during declarative memory formation, interaction with gamma synchronization? Eur. J. Neurosci. 17, 1082–1088 (2003).
    PubMed Google Scholar
43. Sauseng, P. et al. Theta coupling in the human electroencephalogram during a working memory task. Neurosci. Lett. 354, 123–126 (2004).
    CAS PubMed Google Scholar
44. Serrien, D. J., Pogosyan, A. H. & Brown, P. Influence of working memory on patterns of motor related cortico-cortical coupling. Exp. Brain Res. 155, 204–210 (2004).
    PubMed Google Scholar
45. Sauseng, P., Klimesch, W., Schabus, M. & Doppelmayr, M. Fronto-parietal EEG coherence in theta and upper alpha reflect central executive functions of working memory. Int. J. Psychophysiol. 57, 97–103 (2005).
    PubMed Google Scholar
46. Kopp, F., Schröger, E. & Lipka, S. Synchronized brain activity during rehearsal and short-term memory disruption by irrelevant speech is affected by recall mode. Int. J. Psychophysiol. 61, 188–203 (2006).
    PubMed Google Scholar
47. Payne, L. & Kounios, J. Coherent oscillatory networks supporting short-term memory retention. Brain Res. 1247, 126–132 (2009).
    CAS PubMed Google Scholar
48. Wittenberg, G. M. & Wang, S. S. Malleability of spike-timing-dependent plasticity at the CA3–CA1 synapse. J. Neurosci. 26, 6610–6617 (2006).
    CAS PubMed PubMed Central Google Scholar
49. Spruston, N. & Cang, J. Timing isn't everything. Nature Neurosci. 13, 277–279 (2010).
    CAS PubMed Google Scholar
50. Mehta, M. R., Lee, A. K. & Wilson, M. A. Role of experience and oscillations in transforming a rate code into a temporal code. Nature 417, 741–746 (2002).
    CAS PubMed Google Scholar
51. Pavlides, C., Greenstein, Y. J., Grudman, M. & Winson, J. Long-term potentiation in the dentate gyrus is induced preferentially on the positive phase of theta-rhythm. Brain Res. 439, 383–387 (1988).
    CAS PubMed Google Scholar
52. Huerta, P. T. & Lisman, J. E. Heightened synaptic plasticity of hippocampal CA1 neurons during a cholinergically induced rhythmic state. Nature 364, 723–725 (1993).
    CAS PubMed Google Scholar
53. Hasselmo, M. E., Bodelón, C. & Wyble, B. P. A proposed function for hippocampal theta rhythm, separate phases of encoding and retrieval enhance reversal of prior learning. Neural Comput. 14, 793–817 (2002).
    PubMed Google Scholar
54. Baddeley, A. D. Working Memory (Oxford University Press, Oxford,1986).
    Google Scholar
55. Marr, D. A theory for cerebral neocortex. Proc. R. Soc. Lond. B Biol. Sci. 176, 161–234 (1970).
    CAS PubMed Google Scholar
56. Bliss, T. V. & Lomo, T. Long-lasting potentiation of synaptic transmission in the dentate area of the anaesthetized rabbit following stimulation of the perforant path. J. Physiol. 232, 331–356 (1973).
    CAS PubMed PubMed Central Google Scholar
57. Muzzio, I. A., Kentros, C. & Kandel, E. What is remembered? Role of attention on the encoding and retrieval of hippocampal representations. J. Physiol. 587, 2837–2854 (2009).
    CAS PubMed PubMed Central Google Scholar
58. Buzsáki, G. The hippocampo-neocortical dialogue. Cereb. Cortex 6, 81–92 (1996).
    PubMed Google Scholar
59. Gazzaniga, M. S., Ivry, R. M. & Mangun, G. R. Cognitive Neuroscience: The Biology of the Mind 2nd edn, p311 (Norton & Company, New York, 2002).
    Google Scholar
60. Fuster, J. M. Memory in the Cerebral Cortex (MIT Press, Cambridge, Massachusetts, 1995).
    Google Scholar
61. Ruchkin, D. S., Grafman, J., Cameron, K. & Berndt, R. S. Working memory retention systems, a state of activated long-term memory. Behav. Brain Sci. 26, 709–728 (2003).
    PubMed Google Scholar
62. D'Esposito, M. From cognitive to neural models of working memory. Philos. Trans. R. Soc. Lond. B Biol. Sci. 362, 761–772 (2007).
    PubMed PubMed Central Google Scholar
63. Harrison, S. A. & Tong, F. Decoding reveals the contents of visual working memory in early visual areas. Nature 458, 632–635 (2009).
    CAS PubMed PubMed Central Google Scholar
64. Cohen, J. D. et al. Temporal dynamics of brain activation during a working memory task. Nature 386, 604–608 (1997).
    CAS PubMed Google Scholar
65. Lutzenberger, W., Ripper, B., Busse, L., Birbaumer, N. & Kaiser, J. Dynamics of gamma-band activity during an audiospatial working memory task in humans. J. Neurosci. 22, 5630–5638 (2002).
    CAS PubMed PubMed Central Google Scholar
66. Babiloni, C. et al. Functional frontoparietal connectivity during short-term memory as revealed by high-resolution EEG coherence analysis. Behav. Neurosci. 118, 687–697 (2004).
    PubMed Google Scholar
67. Tallon-Baudry, C., Bertrand, O. & Fischer, C. Oscillatory synchrony between human extrastriate areas during visual short-term memory maintenance. J. Neurosci. 21, RC177 (2001).
    CAS PubMed PubMed Central Google Scholar
68. Axmacher, N., Schmitz, D. P., Wagner, T., Elger, C. E. & Fell, J. Interactions between medial temporal lobe, prefrontal cortex, and inferior temporal regions during visual working memory, a combined intracranial EEG and functional magnetic resonance imaging study. J. Neurosci. 28, 7304–7312 (2008).
    CAS PubMed PubMed Central Google Scholar
69. Siegel, M., Warden, M. R. & Miller, E. K. Phase-dependent neuronal coding of objects in short-term memory. Proc. Natl Acad. Sci. USA 106, 21341–21346 (2009).
    CAS PubMed PubMed Central Google Scholar
70. Axmacher, N. et al. Cross-frequency coupling supports multi-item working memory in the human hippocampus. Proc. Natl Acad. Sci. USA 107, 3228–3233 (2010). The first direct empirical evidence that multi-item working memory relies on cross-frequency coupling between the amplitude of high-frequency and the phase of low-frequency oscillations in the human hippocampus.
    CAS PubMed PubMed Central Google Scholar
71. Engel, A. K. & Fries, P. Beta-band oscillations — signalling the status quo? Curr. Opin. Neurobiol. 20, 156–165 (2010).
    CAS PubMed Google Scholar
72. Huijbers, W., Pennartz, C. M. & Daselaar S. M. Dissociating the “retrieval success” regions of the brain: effects of retrieval delay. Neuropsychologia 48, 491–497 (2010).
    CAS PubMed Google Scholar
73. Gruber, T., Keil, A. & Müller, M. M. Modulation of induced gamma band responses and phase synchrony in a paired associate learning task in the human EEG. Neurosci. Lett. 316, 29–32 (2001).
    CAS PubMed Google Scholar
74. Eichenbaum, H. A cortical-hippocampal system for declarative memory. Nature Rev. Neurosci. 1, 41–50 (2000).
    CAS Google Scholar
75. Fernández, G. & Tendolkar, I. The rhinal cortex, 'gatekeeper' of the declarative memory system. Trends Cogn. Sci. 10, 358–362 (2006).
    PubMed Google Scholar
76. Jutras, M. J., Fries, P. & Buffalo, E. A. Gamma-band synchronization in the macaque hippocampus and memory formation. J. Neurosci. 29, 12521–12531 (2009).
    CAS PubMed PubMed Central Google Scholar
77. Seidenbecher, T., Laxmi, T. R., Stork, O. & Pape, H. C. Amygdalar and hippocampal theta rhythm synchronization during fear memory retrieval. Science 301, 846–850 (2003). This study showed that amygdala–hippocampal coherence is increased in rodents after fear conditioning, suggesting that phase synchronization is also relevant for non-declarative long-term memory processes.
    CAS PubMed Google Scholar
78. Narayanan, R. T. et al. Dissociated theta phase synchronization in amygdalo-hippocampal circuits during various stages of fear memory. Eur. J. Neurosci. 25, 1823–1831 (2007).
    PubMed Google Scholar
79. Reymann, K. G. & Frey, J. U. The late maintenance of hippocampal LTP: requirements, phases, 'synaptic tagging', 'late-associativity' and implications. Neuropharmacology 52, 24–40 (2007).
    CAS PubMed Google Scholar
80. Jones, M. W. & Wilson, M. A. Theta rhythms coordinate hippocampal-prefrontal interactions in a spatial memory task. PLoS Biol. 3, e402 (2005).
    PubMed PubMed Central Google Scholar
81. Montgomery, S. M. & Buzsáki, G. Gamma oscillations dynamically couple hippocampal CA3 and CA1 regions during memory task performance. Proc. Natl Acad. Sci. USA 104, 14495–14500 (2007). In this study, intrahippocampal phase synchronization between areas CA1 and CA3 was shown to increase during retrieval of information in a delayed spatial alternation task.
    CAS PubMed PubMed Central Google Scholar
82. Paré, D. Role of the basolateral amygdala in memory consolidation. Prog. Neurobiol. 70, 409–420 (2003).
    PubMed Google Scholar
83. Cave, C. B. & Squire, L. R. Intact verbal and nonverbal short-term memory following damage to the human hippocampus. Hippocampus 2, 151–163 (1992).
    CAS PubMed Google Scholar
84. Gaffan, D. & Murray, E. A. Monkeys (Macaca fascicularis) with rhinal cortex ablations succeed in object discrimination learning despite 24-hr intertrial intervals and fail at matching to sample despite double sample presentations. Behav. Neurosci. 106, 30–38 (1992).
    CAS PubMed Google Scholar
85. Young B. J., Otto T., Fox G. D. & Eichenbaum H. Memory representation within the parahippocampal region. J. Neurosci. 17, 5183–5195 (1997).
    CAS PubMed PubMed Central Google Scholar
86. Axmacher, N. et al. Sustained neural activity patterns during working memory in the human medial temporal lobe. J. Neurosci. 27, 7807–7816 (2007).
    CAS PubMed PubMed Central Google Scholar
87. Nichols, E. A., Kao, Y. C., Verfaellie, M. & Gabrieli, J. D. Hippocampus, working memory and long-term memory for faces: evidence from fMRI and global amnesia for involvement of the medial temporal lobes. Hippocampus 16, 604–616 (2006).
    PubMed PubMed Central Google Scholar
88. Schon, K., Hasselmo, M. E., Lopresti, M. L., Tricarico, M. D. & Stern, C. E. Persistence of parahippocampal representation in the absence of stimulus input enhances long-term encoding, a functional magnetic resonance imaging study of subsequent memory after a delayed match-to-sample task. J. Neurosci. 24, 11088–11097 (2004).
    CAS PubMed PubMed Central Google Scholar
89. Ranganath, C. & D'Esposito, M. Medial temporal lobe activity associated with active maintenance of novel information. Neuron 31, 865–873 (2001).
    CAS PubMed Google Scholar
90. Stern, C. E., Sherman, S. J., Kirchhoff, B. A. & Hasselmo, M. E. Medial temporal and prefrontal contributions to working memory tasks with novel and familiar stimuli. Hippocampus 11, 337–346 (2001).
    CAS PubMed Google Scholar
91. Olson, I. R., Moore, K. S., Stark, M. & Chatterjee, A. Visual working memory is impaired when the medial temporal lobe is damaged. J. Cogn. Neurosci. 18, 1087–1097 (2006).
    PubMed Google Scholar
92. Cohen, N. J. & Eichenbaum, H. Memory, Amnesia, and the Hippocampal System (The MIT Press, Cambridge, Massachusetts,1993).
    Google Scholar
93. Henke, K. A model for memory systems based on processing modes rather than consciousness. Nature Rev. Neurosci. 11, 523–532 (2010).
    CAS Google Scholar
94. Piekema, C., Kessels, R. P., Mars, R. B., Petersson, K. M. & Fernandez, G. The right hippocampus participates in short-term memory maintenance of object-location associations. Neuroimage 33, 374–382 (2006).
    PubMed Google Scholar
95. Aggleton, J. P., Shaw, C. & Gaffan, E. A. The performance of postencephalitic amnesic subjects on two behavioural tests of memory, concurrent discrimination learning and delayed matching-to-sample. Cortex 28, 359–372 (1992).
    CAS PubMed Google Scholar
96. Hannula, D. E., Tranel, D. & Cohen, N. J. The long and the short of it, relational memory impairments in amnesia, even at short lags. J. Neurosci. 262, 8352–8359 (2006).
    Google Scholar
97. Olson, I. R., Page, K., Moore, K. S., Chatterjee, A. & Verfaellie, M. Working memory for conjunctions relies on the medial temporal lobe. J. Neurosci. 26, 4596–4601 (2006).
    CAS PubMed PubMed Central Google Scholar
98. Shrager, Y., Levy, D. A., Hopkins, R. O. & Squire, L. R. Working memory and the organization of brain systems. J. Neurosci. 28, 4818–4822 (2008).
    CAS PubMed PubMed Central Google Scholar
99. Ranganath, C., Cohen, M. X. & Brozinsky, C. J. Working memory maintenance contributes to long-term memory formation, neural and behavioral evidence. J. Cogn. Neurosci. 17, 994–1010 (2005).
    PubMed Google Scholar
100. Sauseng, P. et al. Brain oscillatory substrates of visual short-term memory capacity. Curr. Biol. 19, 1846–1852 (2009). This elegant study separated the neural mechanisms underlying maintenance of relevant and suppression of irrelevant items during working memory, and shows that the former relies on cross-frequency phase–phase and phase–amplitude coupling of theta and gamma oscillations.
     CAS PubMed Google Scholar
101. Demiralp, T. et al. Gamma amplitudes are coupled to theta phase in human EEG during visual perception. Int. J. Psychophysiol. 64, 24–30 (2007).
     PubMed Google Scholar
102. Mormann, F. et al. Phase/amplitude reset and theta-gamma interaction in the human medial temporal lobe during a continuous word recognition memory task. Hippocampus 15, 890–900 (2005).
     PubMed Google Scholar
103. Canolty, R. T. et al. High gamma power is phase-locked to theta oscillations in human neocortex. Science 313, 1626–1628 (2006).
     CAS PubMed PubMed Central Google Scholar
104. Lisman, J. E. & Idiart, M. A. Storage of 7 ± 2 short-term memories in oscillatory subcycles. Science 267, 1512–1515 (1995).
     CAS PubMed Google Scholar
105. Jensen, O. & Lisman, J. E. Hippocampal sequence-encoding driven by a cortical multi-item working memory buffer. Trends Neurosci. 28, 67–72 (2005). A groundbreaking theoretical work suggesting that cross-frequency coupling underlies both the representation of multiple items in a working memory buffer and the encoding of these items into long-term memory.
     CAS PubMed Google Scholar
106. Jensen, O. & Colgin, L. L. Cross-frequency coupling between neuronal oscillations. Trends Cogn. Sci. 11, 267–269 (2007).
     PubMed Google Scholar
107. Tort, A. B. et al. Dynamic cross-frequency couplings of local field potential oscillations in rat striatum and hippocampus during performance of a T-maze task. Proc. Natl. Acad. Sci. USA 105, 20517–20522 (2008).
     CAS PubMed PubMed Central Google Scholar
108. Tort, A. B., Komorowski, R. W., Manns, J. R., Kopell, N. J. & Eichenbaum, H. Theta-gamma coupling increases during the learning of item-context associations. Proc. Natl Acad. Sci. USA 106, 20942–20947 (2009).
     CAS PubMed PubMed Central Google Scholar
109. O'Keefe, J. & Recce, M. L. Phase relationship between hippocampal place units and the EEG theta rhythm. Hippocampus 3, 317–330 (1993).
     CAS PubMed Google Scholar
110. Senior, T. J., Huxter, J. R., Allen, K., O'Neill, J. & Csicsvari, J. Gamma oscillatory firing reveals distinct populations of pyramidal cells in the CA1 region of the hippocampus. J. Neurosci. 28, 2274–2286 (2008).
     CAS PubMed PubMed Central Google Scholar
111. Jensen, O. & Lisman, J. E. Hippocampal CA3 region predicts memory sequences: accounting for the phase precession of place cells. Learn. Mem. 3, 279–287 (1996).
     CAS PubMed Google Scholar
112. Lisman, J. & Buzsáki, G. A neural coding scheme formed by the combined function of gamma and theta oscillations. Schizophr. Bull. 34, 974–980 (2008).
     PubMed PubMed Central Google Scholar
113. Harris, K. D., Csicsvari, J., Hirase, H., Dragoi, G. & Buzsaki, G. Organization of cell assemblies in the hippocampus. Nature 424, 552–556 (2003).
     CAS PubMed Google Scholar
114. Hasselmo, M. E. & Eichenbaum, H. Hippocampal mechanisms for the context-dependent retrieval of episodes. Neural Netw. 18, 1172–1190 (2005).
     PubMed PubMed Central Google Scholar
115. Lisman, J. E., Talamini, L. M. & Raffone, A. Recall of memory sequences by interaction of the dentate and CA3, a revised model of the phase precession. Neural Netw. 18, 1191–1201 (2005).
     PubMed Google Scholar
116. Tass, P. et al. Detection of n:m phase locking from noisy data: application to magnetoencephalography. Phys. Rev. Lett. 81, 3291–3294 (1998).
     CAS Google Scholar
117. Schack, B., Klimesch, W. & Sauseng, P. Phase synchronization between theta and upper alpha oscillations in a working memory task. Int. J. Psychophysiol. 57, 105–114 (2005).
     CAS PubMed Google Scholar
118. Palva, J. M., Palva, S. & Kaila, K. Phase synchrony among neuronal oscillations in the human cortex. J. Neurosci. 25, 3962–3972 (2005). One of the first studies highlighting the relevance of m:n phase–phase coupling for working memory processes.
     CAS PubMed PubMed Central Google Scholar
119. James, W. The Principles of Psychology (Holt, Rinehard & Winston, New York,1890).
     Google Scholar
120. Craik, F. I. M. & Lockhart, R. S. Levels of processing: a framework for memory research. J. Verb. Learn. Verb. Behav. 11, 671–684 (1972).
     Google Scholar
121. Axmacher, N., Elger, C. E. & Fell, J. Working memory-related hippocampal deactivation interferes with long-term memory formation. J. Neurosci. 29, 1052–1060 (2009).
     CAS PubMed PubMed Central Google Scholar
122. Hebb, D. O. in Brain Mechanisms and Learning (ed. Delafresnaye, J. F.) 37–51 (Oxford University Press, London, 1961).
     Google Scholar
123. Hulme, C., Maughan, S., Brown & G. D. A. Memory for familiar and unfamiliar words, evidence for a long-term memory contribution to short-term memory span. J. Mem. Language 30, 685–701 (1991).
     Google Scholar
124. Jensen, O. & Lisman, J. E. Theta/gamma networks with slow NMDA channels learn sequences and encode episodic memory: role of NMDA channels in recall. Learn. Mem. 3, 264–278 (1996).
     CAS PubMed Google Scholar
125. Schack, B. & Weiss, S. Quantification of phase synchronization phenomena and their importance for verbal memory processes. Biol. Cybern. 92, 275–287 (2005). One of the first studies to show simultaneous effects of theta and gamma phase synchronization and m:n phase–phase coupling between these frequencies during memory formation.
     PubMed Google Scholar
126. Colgin, L. L. et al. Frequency of gamma oscillations routes flow of information in the hippocampus. Nature 462, 353–357 (2009).
     CAS PubMed Google Scholar
127. Palva, J. M., Monto, S., Kulashekhar, S. & Palva, S. Neuronal synchrony reveals working memory networks and predicts individual memory capacity. Proc. Natl Acad. Sci. USA 107, 7580–7585 (2010).
     CAS PubMed PubMed Central Google Scholar
128. Gelbard-Sagiv, H., Mukamel, R., Harel, M., Malach, R. & Fried, I. Internally generated reactivation of single neurons in human hippocampus during free recall. Science 322, 96–101 (2008).
     CAS PubMed PubMed Central Google Scholar
129. Lisman, J. E. & Grace, A. A. The hippocampal–VTA loop, controlling the entry of information into long-term memory. Neuron 46, 703–713 (2005).
     CAS PubMed Google Scholar
130. Wittmann, B. C. et al. Reward-related fMRI activation of dopaminergic midbrain is associated with enhanced hippocampus-dependent long-term memory formation. Neuron 45, 459–467 (2005).
     CAS PubMed Google Scholar
131. Mecklinger, A. The control of long-term memory, brain systems and cognitive processes. Neurosci. Biobehav. Rev. 34, 1055–1065 (2010).
     PubMed Google Scholar
132. Nunez, P. L. Neocortical Dynamics and Human EEG Rhythms (Oxford University Press, New York, 1995).
     Google Scholar
133. Pfurtscheller, G. & Aranibar, A. Event-related cortical desynchronization detected by power measurements of scalp EEG. Electroencephalogr. Clin. Neurophysiol. 42, 817–826 (1977).
     CAS PubMed Google Scholar
134. Heinzle, J., König, P. & Salazar, R. F. Modulation of synchrony without changes in firing rates. Cogn. Neurodyn. 1, 225–235 (2007).
     PubMed PubMed Central Google Scholar
135. Gregoriou, G. G., Gotts, S. J., Zhou, H. & Desimone, R. High-frequency, long-range coupling between prefrontal and visual cortex during attention. Science 324, 1207–1210 (2009).
     CAS PubMed PubMed Central Google Scholar
136. Frien, A., Eckhorn, R., Bauer, R., Woelbern, T. & Kehr, H. Stimulus-specific fast oscillations at zero phase between visual areas V1 and V2 of awake monkey. Neuroreport 5, 2273–2277 (1994).
     CAS PubMed Google Scholar
137. König, P. & Schillen, T. B. Stimulus-dependent assembly formation of oscillatory responses: I. synchronization. Neural Comput. 3, 155–166 (1991).
     PubMed Google Scholar
138. Traub, R. D., Whittington, M. A., Stanford, I. M. & Jefferys, J.G. A mechanism for generation of long-range synchronous fast oscillations in the cortex. Nature 383, 621–624 (1996).
     CAS PubMed Google Scholar
139. Bibbig, A., Traub, R. D. & Whittington, M. A. Long-range synchronization of gamma and beta oscillations and the plasticity of excitatory and inhibitory synapses, a network model. J. Neurophysiol. 88, 1634–1654 (2002).
     PubMed Google Scholar
140. Vicente, R., Gollo, L. L., Mirasso, C. R., Fischer, I. & Pipa, G. Dynamical relaying can yield zero time lag neuronal synchrony despite long conduction delays. Proc. Natl Acad. Sci. USA 105, 17157–17162 (2008).
     CAS PubMed PubMed Central Google Scholar
141. 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 6, 149–172 (1996).
     CAS PubMed Google Scholar
142. Lachaux, J. P., Rodriguez, E., Martinerie, J. & Varela, F. J. Measuring phase synchrony in brain signals. Hum. Brain Mapp. 8, 194–208 (1999).
     CAS PubMed PubMed Central Google Scholar

Download references