Oscillatory power decreases and long-term memory: The information via desynchronization hypothesis

Frontiers in Human Neuroscience

Volumn , Issue MARCH 2012, 2012, Pages 1-20

  Hanslmayr, Simon ^a   Staudigl, Tobias ^a   Fellner, Marie Christin ^a  

^a UNIVERSITY OF KONSTANZ   (Germany)

Author keywords

Alpha; Beta; Desynchronization; Eeg; Long term memory; Meg; Oscillations; Synchronization

Indexed keywords

ALPHA RHYTHM; BETA RHYTHM; BOLD SIGNAL; BRAIN FUNCTION; CORRELATIONAL STUDY; ELECTROENCEPHALOGRAPHY; EVOKED RESPONSE; FREQUENCY MODULATION; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HUMAN; LONG TERM MEMORY; MATHEMATICAL MODEL; MEMORY CONSOLIDATION; MEMORY DISORDER; OSCILLATION; PREDICTIVE VALUE; RECALL; REVIEW; TASK PERFORMANCE; THEORETICAL STUDY;

EID: 84859017702     PISSN: 16625161     EISSN: 16625161     Source Type: Journal    
DOI: 10.3389/fnhum.2012.00074     Document Type: Review

References (80)

1. Addante, R.J., Watrous, A.J., Yonelinas, A.P., Ekstrom, A.D., Ranganath, C. (2011). Prestimulus theta activity predicts correct source memory retrieval. Proc. Natl. Acad. Sci. U.S.A., 108, 10702-10707.
2. Alvarez, P. and Squire, L.R. (1994). Memory consolidation and the medial temporal lobe: a simple network model. Proc. Natl. Acad. Sci. U.S.A., 91, 7041-7045.
3. Anderson, M.C., Bjork, R.A. and Bjork, E.L. (1994). Remembering can cause forgetting: retrieval dynamics in long-term memory. J. Exp. Psychol. Learn. Mem. Cogn., 20, 1063-1087.
4. Anderson, M.C. and Green, C. (2001). Suppressing unwanted memories by executive control. Nature, 410, 366-369.
5. Axmacher, N., Mormann, F., Fernández, G., Elger, C.E. and Fell, J. (2006). Memory formation by neuronal synchronization. Brain Res. Rev, 52, 170-182.
6. Barlow, H.B. (1961). "The coding of sensory messages," in Current Problems in Animal Behaviour, eds. W.H. Thorpe, and O.L. Zangwill (Cambridge, UK: Cambridge University Press), 331-360.
7. Barlow, H. (2001). Redundancy reduction revisited. Comput Neural Syst, 12, 241-253.
8. Bialek, W., Rieke, F., van Ruyter Steveninck, R.R. de and Warland, D. (1991). Reading a neural code. Science, 252, 1854-1857.
9. Burgess, A.P. and Gruzelier, J.H. (2000). Short duration power changes in the EEG during recognition memory for words and faces. Psychophysiology, 37, 596-606.
10. Buzsáki, G. and Draguhn, A. (2004). Neuronal oscillations in cortical networks. Science, 304, 1926-1929.
11. Chalk, M., Herrero, J.L., Gieselmann, M.A., Delicato, L.S., Gotthardt, S. and Thiele, A. (2010). Attention reduces stimulus-driven gamma frequency oscillations and spike field coherence in V1. Neuron, 66, 114-125.
12. Craik, F.I.M. (2002). Levels of processing: past, present and future? Memory, 10, 305-318.
13. Dujardin, K., Bourriez, J.L. and Guieu, J.D. (1994). Event-Related Desynchronization (ERD) patterns during verbal memory tasks: effect of age. Int. J. Psychophysiol., 16, 17-27.
14. Düzel, E., Habib, R., Schott, B., Schoenfeld, A., Lobaugh, N., McIntosh, A.R., Scholz, M. and Heinze, H.J. (2003). A multivariate, spatiotemporal analysis of electromagnetic time-frequency data of recognition memory. Neuroimage, 18, 185-197.
15. Düzel, E., Penny, W.D. and Burgess, N. (2010). Brain oscillations and memory. Curr. Opin. Neurobiol., 20, 143-149.
16. Fell, J., Klaver, P., Lehnertz, K., Grunwald, T., Schaller, C., Elger, C.E. and Fernández, G. (2001). Human memory formation is accompanied by rhinal-hippocampal coupling and decoupling. Nat. Neurosci., 4, 1259-1264.
17. Fell, J. and Axmacher, N. (2011). The role of phase synchronization in memory processes. Nat. Rev. Neurosci., 12, 105-118.
18. Fell, J., Ludowig, E., Staresina, B.P., Wagner, T., Kranz, T., Elger, C.E. and Axmacher, N. (2011). Medial temporal theta/alpha power enhancement precedes successful memory encoding: evidence based on intracranial EEG. J. Neurosci., 31, 5392-5397.
19. Freunberger, R., Fellinger, R., Sauseng, P., Gruber, W., and Klimesch, W. (2009). Dissociation between phase-locked and nonphase-locked alpha oscillations in a working memory task. Hum Brain Mapp., 30, 3417-3425.
20. Fries, P., Reynolds, J.H., Rorie, A.E. and Desimone, R. (2001). Modulation of oscillatory neuronal synchronization by selective visual attention. Science, 291, 1560-1563.
21. Friston, K. (2010). The free-energy principle: a unified brain theory? Nat Rev Neurosci, 11, 127-138.
22. Gabrieli, J.D., Poldrack, R.A. and Desmond, J.E. (1998). The role of left prefrontal cortex in language and memory. Proc. Natl. Acad. Sci. U.S.A., 95, 906-913.
23. Goard, M. and Dan, Y. (2009). Basal forebrain activation enhances cortical coding of natural scenes. Nat. Neurosci., 12, 1444-1449.
24. Guderian, S., Schott, B.H., Richardson-Klavehn, A. and Düzel, E. (2009). Medial temporal theta state before an event predicts episodic encoding success in humans. Proc. Natl. Acad. Sci. U.S.A., 106, 5365-5370.
25. Haegens, S., Nácher, V., Luna, R., Romo, R. and Jensen, O. (2011). α-Oscillations in the monkey sensorimotor network influence discrimination performance by rhythmical inhibition of neuronal spiking. Proc. Natl. Acad. Sci. U.S.A., 108, 19377-19382.
26. Hämäläinen, M., Hari, R., Illmoniemi, R.J., Knuutila, J., and Lounasmaa, O.V. (1993). Magnetoencephalography - theory, instrumentation, and applications to noninvasive studies of the working human brain. Rev Mod Phys, 65, 413-497.
27. Hanslmayr, S., Gross, J., Klimesch, W. and Shapiro, K.L. (2011a). The role of alpha oscillations in temporal attention. Brain Res. Rev., 67, 331-343.
28. Hanslmayr, S., Leipold, P., Passtötter, B., and Bäuml, K.-H. (2009b). Anticipatory signatures during voluntary memory suppression. J. Neurosci., 29, 2742-2747.
29. Hanslmayr, S., Spitzer, B. and Bäuml, K.-H. (2009a). Brain oscillations dissociate between semantic and nonsemantic encoding of episodic memories. Cereb. Cortex, 19, 1631-1640.
30. Hanslmayr, S., Staudigl, T., Aslan, A. and Bäuml, K.-H. (2010). Theta oscillations predict the detrimental effects of memory retrieval. Cogn. Affect. Behav. Neurosci., 10, 329-338.
31. Hanslmayr, S., Volberg, G., Wimber, M., Raabe, M., Greenlee, M.W. and Bäuml, K.-H.T. (2011b). The Relationship between Brain Oscillations and BOLD Signal during Memory Formation: A Combined EEG-fMRI Study. J. Neurosci., 31, 15674-15680.
32. Hebb, D.O. (2002). The Organization of Behavior: a Neuropsychological Theory. Mahwah, NJ: Erlbaum.
33. Henson, R.N., Gagnepain, P. (2010). Predictive, interactive multiple memory systems. Hippocampus, 20, 1315-1326.
34. Innocenti, I., Giovanelli, F., Cincotta, M., Feurra, M., Polizzotto, N.R., Bianco, G., Cappa, S.F., Rossi, S. (2010). Event-related rTMS at encoding affects differently deep and shallow memory traces. Neuroimage, 53, 325-330.
35. Jacobs, J., Kahana, M.J., Ekstrom, A.D. and Fried, I. (2007). Brain oscillations control timing of single-neuron activity in humans. J. Neurosci., 27, 3839-3844. doi:10.1523/JNEUROSCI.4636-06.2007.
36. Jensen, O., Gelfand, J., Kounios, J. and Lisman, J.E. (2002). Oscillations in the alpha band (9-12 Hz) increase with memory load during retention in a short-term memory task. Cereb. Cortex, 12, 877-882.
37. Jensen, O. and Mazaheri, A. (2010). Shaping functional architecture by oscillatory alpha activity: gating by inhibition. Front. Hum. Neurosci., 4, 186.
38. Khader, P.H., Jost, K., Ranganath, C. and Rösler, F. (2010). Theta and alpha oscillations during working-memory maintenance predict successful long-term memory encoding. Neurosci. Lett., 468, 339-343.
39. Khader, P.H. and Rösler, F. (2011). EEG power changes reflect distinct mechanisms during long-term memory retrieval. Psychophysiology, 48, 362-369.
40. Khayat, P.S., Niebergall, R. and Martinez-Trujillo, J.C. (2010). Frequency-dependent attentional modulation of local field potential signals in macaque area MT. J. Neurosci., 30, 7037-7048.
41. Kilner, J.M., Mattout, J., Henson, R. and Friston, K.J. (2005). Hemodynamic correlates of EEG: a heuristic. Neuroimage, 28, 280-286.
42. Kim, H. (2011). Neural activity that predicts subsequent memory and forgetting: a meta analysis of 74 fMRI studies. Neuroimage, 54, 2446-2461.
43. Klimesch, W. (1999). EEG 749 alpha and theta oscillations reflect cognitive and memory performance: a review and analysis. Brain Res. Brain Res. Rev., 29, 169-195.
44. Klimesch, W., Doppelmayr, M., Schimke, H. and Ripper, B. (1997). Theta synchronization and alpha desynchronization in a memory task. Psychophysiology, 34, 169-176.
45. Klimesch, W., Doppelmayr, M., Stadler, W., Pöllhuber, D., Sauseng, P. and Röhm, D. (2001). Episodic retrieval is reflected by a process specific increase in human electroencephalographic theta activity. Neurosci. Lett., 302, 49-52.
46. Klimesch, W., Schimke, H., Doppelmayr, M., Ripper, B., Schwaiger, J. and Pfurtscheller, G. (1996). Event-related desynchronization (ERD) and the Dm effect: does alpha desynchronization during encoding predict later recall performance? Int. J. Psychophysiol., 24, 47-60.
47. Klimesch, W., Sauseng, P. and Hanslmayr, S. (2007). EEG alpha oscillations: the inhibition timing hypothesis. Brain Res Rev, 53, 63-88.
48. Kurimoto, R., Ishii, R., Canuet, L., Ikezawa, K., Iwase, M., Azechi, M., Aoki, Y., Ikeda, S., Yoshida, T., Takahashi, H., Nakahachi, T., Kazui, H., and Takeda, M. (2012). Induced oscillatory responses during the Sternberg's visual memory task in patients with Alzheimer's disease and mild cognitive impairment. Neuroimage, 59, 4132-4140.
49. Laufs, H., Krakow, K., Sterzer, P., Eger, E., Beyerle, A., Salek-Haddadi, A. and Kleinschmidt, A. (2003). Electroencephalographic signatures of attentional and cognitive default modes in spontaneous brain activity fluctuations at rest. Proc. Natl. Acad. Sci. U.S.A., 100, 11053-11058.
50. Lee, H., Simpson, G.V., Logothetis, N.K. and Rainer, G. (2005). Phase locking of single neuron activity to theta oscillations during working memory in monkey extrastriate visual cortex. Neuron, 45, 147-156.
51. Mantini, D., Perrucci, M.G., Del Gratta, C., Romani, G.L. and Corbetta, M. (2007). Electrophysiological signatures of resting state networks in the human brain. Proc. Natl. Acad. Sci. U.S.A., 104, 13170-13175.
52. Markram, H., Lübke, J., Frotscher, M. and Sakmann, B. (1997). Regulation of synaptic efficacy by coincidence of postsynaptic APs and EPSPs. Science, 275, 213-215.
53. Marr, D. (1971). Simple memory: a theory for archicortex. Philos. Trans. R. Soc. Lond., B, Biol. Sci., 262, 23-81.
54. Meeuwissen, E.B., Takashima, A., Fernández, G. and Jensen, O. (2011a). Increase in posterior alpha activity during rehearsal predicts successful long-term memory formation of word sequences. Hum Brain Mapp, 32, 2045-2053.
55. Meeuwissen, E.B., Takashima, A., Fernández, G. and Jensen, O. (2011b). Evidence for human fronto-central gamma activity during long-term memory encoding of word sequences. PLoS ONE, 6, e21356.
56. Moosmann, M., Ritter, P., Krastel, I., Brink, A., Thees, S., Blankenburg, F., Taskin, B., Obrig, H. and Villringer, A. (2003). Correlates of alpha rhythm in functional magnetic resonance imaging and near infrared spectroscopy. Neuroimage, 20, 145-158.
57. Norman, K.A. (2010). How hippocampus and cortex contribute to recognition memory: revisiting the complementary learning systems model. Hippocampus, 20, 1217-1227.
58. Nyhus, E. and Curran, T. (2010). Functional role of gamma and theta oscillations in episodic memory. Neurosci. Biobehav. Rev., 34, 1023-1035. doi:10.1016/j.neubiorev.2009.12.014.
59. Otten, L.J. and Rugg, M.D. (2001). Task-dependency of the neural correlates of episodic encoding as measured by fMRI. Cereb. Cortex, 11, 1150-1160.
60. Paller, K.A. and Wagner, A.D. (2002). Observing the transformation of experience into memory. Trends Cogn. Sci., 6, 93-102.
61. Palva, J.M., Monto, S., Kulashekhar, S., and Palva, S. (2010). Neuronal synchrony reveals working memory networks and predicts individual memory capacity. Proc Natl Acad Sci U S A., 107, 7580-7585.
62. Palva, S., and Palva, J.M. (2011). Functional role 800 s of alpha-band phase synchronization in local and large-scale cortical networks. Front Psychol., 2, 204.
63. Palva, S., and Palva, J.M. (2007). New vistas for alpha-frequency band oscillations. Trends Neurosci. 30, 150-158.
64. Pfurtscheller, G. and Aranibar, A. (1977). Event-related cortical desynchronization detected by power measurements of scalp EEG. Electroencephalogr Clin Neurophysiol, 42, 817-826.
65. Pfurtscheller, G., Neuper, C., Andrew, C. and Edlinger, G. (1997). Foot and hand area mu rhythms. Int. J. Psychophysiol., 26, 121-135.
66. Rossi, S., Innocenti, I., Polozzotto, N.R., Feurra, M., De Capua, A., Ulivelli, M., Bartalini, S., and Cappa, S.F. (2011). Temporal dynamics of memory trace formation in the human prefrontal cortex. Cereb. Cortex, 21, 368-373.
67. Scheeringa, R., Fries, P., Petersson, K.-M., Oostenveld, R., Grothe, I., Norris, D.G., Hagoort, P. and Bastiaansen, M.C.M. (2011). Neuronal dynamics underlying high- and low-frequency EEG oscillations contribute independently to the human BOLD signal. Neuron, 69, 572-583.
68. Schneidman, E., Puchalla, J.L., Segev, R., Harris, R.A., Bialek, W. and Berry, M.J. (2011). Synergy from silence in a combinatorial neural code. J. Neurosci., 31, 15732-15741.
69. Sederberg, P.B., Gauthier, L.V., Terushkin, V., Miller, J.F., Barnathan, J.A. and Kahana, M.J. (2006). Oscillatory correlates of the primacy effect in episodic memory. Neuroimage, 32, 1422-1431.
70. Sederberg, P.B., Kahana, M.J., Howard, M.W., Donner, E.J. and Madsen, J.R. (2003). Theta and gamma oscillations during encoding predict subsequent recall. J. Neurosci., 23, 10809-10814.
71. Sederberg, P.B., Schulze-Bonhage, A., Madsen, J.R., Bromfield, E.B., McCarthy, D.C., Brandt, A., Tully, M.S. and Kahana, M.J. (2007). Hippocampal and neocortical gamma oscillations predict memory formation in humans. Cereb. Cortex, 17, 1190-1196.
72. Shannon, C.E. and Weaver, W. (1949). The mathematical theory of communication. Urbana, IL: University of Illinois Press.
73. Spitzer, B., Hanslmayr, S., Opitz, B., Mecklinger, A. and Bäuml, K.-H. (2009). Oscillatory correlates of retrieval-induced forgetting in recognition memory. J. Cogn. Neurosci., 21, 976-990.
74. Staudigl, T., Hanslmayr, S. and Bäuml, K.-H.T. (2010). Theta oscillations reflect the dynamics of interference in episodic memory retrieval. J. Neurosci., 30, 11356-11362.
75. Tulving, E. (1972) Episodic and semantic memory. In Tulving, E. and Donaldson, W. (eds), Organization of Memory. Academic Press, Inc., New York, pp. 382-402.
76. Tulving, E. and Thomson, D.M. (1973). Encoding specificity and retrieval processes in episodic memory. Psych. Rev., 80, 352-373.
77. Waldhauser, G., Johansson, M., Hanslmayr, S. (in press). Alpha/beta oscillations indicate inhibition of interfering visual memories. J. Neurosci.
78. Weiss, S. and Rappelsberger, P. (2000). Long-range EEG synchronization during word encoding correlates with successful memory performance. Brain Res. Cogn. Brain Res., 9, 299-312.
79. Wyart, V. and Tallon-Baudry, C. (2008). Neural dissociation between visual awareness and spatial attention. J. Neurosci., 28, 2667-2679.
80. Zion-Golumbic, E., Kutas, M. and Bentin, S. (2010). Neural dynamics associated with semantic and episodic memory for faces: evidence from multiple frequency bands. J. Cogn. Neurosci., 22, 263-277.