Replay of Specific Sequences of Neuronal Activity in the Brain and its Significance for Cognitive Processes

It has been repeatedly shown in animals that during periods of their relative motor inactivity (between runs, for example, or when the pace slows down), there is reactivation of specific sequences of activity of the same neurons and in the same order (sometimes in exactly the opposite order) as in the process of actually performing behavioral acts. Such reactivations were called “replays”. Similar neuronal reactivations in the brain are observed during periods of sleep, that is often associated with the presence of dreams and the phenomenon of “improving” memory. Initially, such “spontaneous” reactivations were demonstrated in the hippocampus for neurons specific in their activity in relation to various places. Later it turned out that the same thing is found in the cortex and in subcortical structures, for example, in the striatum. The phenomenon of neuronal replays presumably underlies the reorganization and consolidation of memory (i.e. its stabilization). “Spontaneous” reactivations are also observed immediately before the performance of a particular behavior and, apparently, underlie selection for future behavior during decision-making. The data presented in this review suggest that what is considered “spontaneous” brain activity is a natural process of continuous updating of existing elements of individual experience for future interactions in the environment. Brain activity is a continuous change of active neuronal groups, and the frequency of “spontaneous” replays, presumably, depends on the time that has elapsed since the appearance of exactly such a combination of neurons during the consolidation and reconsolidation of memory. The study of “spontaneous” brain activations is a relatively new field of neuroscience, and their nature and significance require further research.

1. Alexandrov Yu.I. Nauchenie I pamyat’: traditsionny I sistemny podkhody [Learning and memory: traditional and system approaches]. Zhurnal vysshey nervnoy deyatel’nosti [Journal of Higher Nervous Activity], 2005, no. 55, pp. 842—860. (In Russ.).
2. Aleksandrov I.O., Maksimova N.E. Zakonomernosti formirovaniya novogo komponenta struktury individualnogo znaniya [Regularities of formation of of individual knowledge new component]. Psykhologicheskii zhurnal [Psychological journal], 2003, no. 24(6), pp. 55—76. (In Russ.).
3. Alexandrov Yu.I., Svarnik O.E., Znamenskaya I.I., Kolbeneva M.G., Arutunova K.R., Krylov A.K., Bulava A.I. Regressiya kak etap razvitiya [Regression as developmental stage]. М.: Izd-vo «Institut psikhologii RAN», 2017. (In Russ.).
4. Anokhin P.K. Biologiya I neirofiziologiya uslovnogo refleksa [Biology and neurophysiology of conditioned reflex]. М.: Meditsina, 1968. (In Russ.).
5. Gorkin A.G., Shevchenko D.G. Otrazhenie istorii obucheniya v aktivnosti neironov limbicheskoi kory krolikov [Learning history reflexion in limbic cortical neuronal activity] Zhurnal vysshey nervnoy deyatel’nosti [Journal of Higher Nervous Activity], 1993, 43, no. 1, pp. 172—175. (In Russ.).
6. Popper K. Obiektivnoe znanie: Evolutsionnyi podkhod [Objective knowledge: Evolutional approach]. М.: URSS, 2002. (In Russ.).
7. Rozhdestvin A.V., Svarnik O.E., Grinchenko Yu.V., Alexandrov Yu.I. Zakonomernosti aktualizatsii elementov individualnogo opyta raznoi stepeni differentsirovannosti v protsesse organizatsii povedeniya [Regularities of variously differentiated individual experience elements actualization in the process of behavioral organization]. Psykhologicheskii zhurnal [Psychological journal], 2015, 36, no. 3, pp. 67—72. (In Russ.).
8. Svarnik O.E., Bulava A.I., Fadeeva T.A., Alexandrov Yu.I. Zakonomernosti reorganizatsii pamyati o navykakh, sformirovannykh pri odno- I mnogoetapnom obuchenii [Regularities of memory reorganization about skills formed by one- or multiple-stage learning] Eksperimentalnaya psikhologiya [Experimental psychology], 2011, 4, no. 2, pp. 5—14. (In Russ.).
9. Svarnik O.E., Anokhin K.V., Alexandrov Yu.I. Opyt pervogo, vibrissnogo, navyka vliyaet na induktsiyu ekspressii c-Fos v neironakh bochonkovogo polya somatosensornoi kory pri obuchenii vtoromu, nevibrissnomu navyku [Experience of a first, “whisker-dependent,” skill affects the induction of c-fos expression in somatosensory cortex barrel field neurons in rats on training to a second skill]. Zhurnal vyssheĭ nervnoĭ deyatel’nosti [Journal of Higher Nervous Activity], 2014, 63, no. 6, pp. 77—81. (In Russ.).
10. Sozinov A.A., Krylov A.K., Aleksandrov YU.I. Effekt interferentsii v izuchenii psikhologicheskikh struktur [The effect of interference in the study of psychological structures]// Eksperim. psikhol. [Journal of Experimental Psychology], 2013. 6. no. 1. pp. 5—47. (In Russ.).
11. Shvyrkov V.B. Izuchenie aktivnosti neironov kak metod psikhofiziologicheskogo issledovaniya povedeniya [Neuronal activity study as a method of psychophysiological research of behavior] // Neirony v povedenii: sistemnye aspekty [Neurons in behavior: systemic aspects]. М.: Nauka, 1986. (In Russ.).
12. Addis D.R., Wong A.T., Schacter D.L. Remembering the past and imagining the future: common and distinct neural substrates during event construction and elaboration // Neuropsychologia. 2007. V. 45. No. 7. P. 1363—1377. DOI: 10.1016/j.neuropsychologia.2006.10.016
13. Akers K.G., Martinez-Canabal A., Restivo L., Yiu A.P., De Cristofaro A., Hsiang H.L., Wheeler A.L., Guskjolen A., Niibori Y., Shoji H., Ohira K., Richards B.A., Miyakawa T., Josselyn S.A., Frankland P.W. Hippocampal neurogenesis regulates forgetting during adulthood and infancy // Science. 2014. V. 344. No. 6184. P. 598— 602. DOI: 10.1126/science.1248903
14. Alving B.O. Spontaneous activity in isolated somata of Aplysia pacemaker neurons // J. Gen. Physiol. 1968. V. 51. No. 1. P. 29—45. DOI: 10.1085/jgp.51.1.29
15. Barnes D.C., Wilson D.A. Slow-wave sleep-imposed replay modulates both strength and precision of memory // J. Neurosci. 2014. V. 34 (15). P. 5134—5142. DOI: 10.1523/JNEUROSCI.5274-13.2014
16. Barrett L.F., Simmons W.K. Interoceptive predictions in the brain // Nat Rev Neurosci. 2015. V. 16(7). P. 419—429. DOI: 10.1038/nrn3950
17. Bartsch T., Butler C. Transient amnesic syndromes // Nat. Rev. Neurol. 2013. V. 9 (2). P. 86—97. DOI: 10.1038/nrneurol.2012.264
18. Bendor D., Wilson M.A. Biasing the content of hippocampal replay during sleep // Nat. Neurosci. 2012. V. 15 (10). P. 1439—1444. DOI: 10.1038/nn.3203
19. Bermudez Contreras E.J., Schjetnan A.G., Muhammad A., Bartho P., McNaughton B.L., Kolb B., Gruber A.J., Luczak A. Formation and reverberation of sequential neural activity patterns evoked by sensory stimulation are enhanced during cortical desynchronization // Neuron. 2013. V. 79 (3). P. 555—566. DOI: 10.1016/j. neuron.2013.06.013
20. Bisley J.W., Zaksas D., Droll J.A., Pasternak T. Activity of neurons in cortical area MT during a memory for motion task // J. Neurophysiol. 2004. V. 91 (1). P. 286—300. DOI: 10.1152/jn.00870.2003
21. Blagrove M., Henley-Einion J., Barnett A., Edwards D., Heidi Seage C. A replication of the 5—7 day dream-lag effect with comparison of dreams to future events as control for baseline matching // Conscious Cogn. 2011. V. 20 (2). P. 384—391. DOI: 10.1016/j.concog.2010.07.006
22. Buhry L., Azizi A. H., Cheng S. Reactivation, replay, and preplay: how it might all fit together // Neural Plast. 2011. P. 203462. DOI: 10.1155/2011/203462
23. Buzsaki G. The Brain from Inside Out. New York: Oxford University Press, 2019.
24. Cerf M., Thiruvengadam N., Mormann F., Kraskov A., Quiroga R.Q., Koch C., Fried I. On-line, voluntary control of human temporal lobe neurons // Nature. 2010. V. 467 (7319). P. 1104—1108. DOI: 10.1038/ nature09510
25. Cisek P., Kalaska J. F. Neural correlates of mental rehearsal in dorsal premotor cortex // Nature. 2004. V. 431 (7011). P. 993—996. DOI: 10.1038/nature03005
26. Clark A. Whatever next? Predictive brains, situated agents, and the future of cognitive science // Behav Brain Sci. 2013. V. 36(3). P. 181—204. DOI: 10.1017/S0140525X12000477
27. Csicsvari J., O’Neill J., Allen K., Senior T. Place-selective firing contributes to the reverse-order reactivation of CA1 pyramidal cells during sharp waves in open-field exploration // Eur J. Neurosci. 2007. V. 26 (3). P. 704—716. DOI: 10.1111/j.1460-9568.2007.05684.x
28. Dave A.S., Margoliash D. Song replay during sleep and computational rules for sensorimotor vocal learning // Science. 2000. V. 290 (5492). P. 812—816. DOI: 10.1126/science.290.5492.812
29. Davidson T. J., Kloosterman F., Wilson M. A. Hippocampal replay of extended experience // Neuron. 2009. V. 63 (4). P. 497—507. DOI: 10.1016/j.neuron.2009.07.027
30. Denny C.A., Kheirbek M.A., Alba E.L., Tanaka K.F., Brachman R.A., Laughman K.B., Tomm N.K., Turi G.F., Losonczy A., Hen R. Hippocampal memory traces are differentially modulated by experience, time and adult neurogenesis // Neuron. 2014. V. 83 (1). P. 189—201. DOI: 10.1016/j.neuron.2014.05.018
31. Derdikman D., Moser M.B. A dual role for hippocampal replay // Neuron. 2010. V. 65(5). P. 582—584. DOI: 10.1016/j.neuron.2010.02.022
32. Diba K., Buzsaki G. Forward and reverse hippocampal place-cell sequences during ripples // Nat. Neurosci. 2007. V. 10 (10). P. 1241—1242. DOI: 10.1038/nn1961
33. Diekelmann S., Landolt H. P., Lahl O., Born J., Wagner U. Sleep loss produces false memories // PLoS One. 2008. V. 3 (10). e3512. DOI: 10.1371/journal.pone.0003512
34. Dragoi G., Tonegawa S. Preplay of future place cell sequences by hippocampal cellular assemblies // Nature. 2011. V. 469 (7330). P. 397—401. DOI: 10.1038/nature09633
35. Drosopoulos S., Wagner U., Born J. Sleep enhances explicit recollection in recognition memory // Learn Mem. 2005. V. 12 (1). P. 44—51. DOI: 10.1101/lm.83805
36. Dudai Y. The Restless Engram: Consolidations Never End // Annu. Rev. Neurosci. 2012. V. 35. P. 227— 247. DOI: 10.1146/annurev-neuro-062111-150500
37. Dupret D., O’Neill J., Pleydell-Bouverie B., Csicsvari J. The reorganization and reactivation of hippocampal maps predict spatial memory performance // Nat. Neurosci. 2010. V. 13 (8). P. 995—1002. DOI: 10.1038/ nn.2599
38. Ekstrom A.D., Kahana M.J., Caplan J.B., Fields T.A., Isham E.A., Newman E.L., Fried I. Cellular networks underlying human spatial navigation // Nature. 2003. V. 425. P. 184—188. DOI: 10.1038/nature01964
39. Eldar E., Lievre G., Dayan P., Dolan R.J. The roles of online and offline replay in planning // eLife. 2020. V. 9. P. e56911. DOI: 10.7554/eLife.56911.
40. Engle-Friedman M. The effects of sleep loss on capacity and effort // Sleep Science. 2014. V. 7. P. 213— 224. DOI: 10.1016/j.slsci.2014.11.001
41. Euston D.R., Tatsuno M., McNaughton B.L. Fast-forward playback of recent memory sequences in prefrontal cortex during sleep // Science. 2007. V. 318 (5853). P. 1147—1150. DOI: 10.1126/science.1148979
42. Fares J., Bou Diab Z., Nabha S., Fares Y. Neurogenesis in the adult hippocampus: history, regulation, and prospective roles // Int J Neurosci. 2019. V. 129(6). P. 598—611. DOI: 10.1080/00207454.2018.1545771.
43. Foster D.J., Wilson M.A. Reverse replay of behavioural sequences in hippocampal place cells during the awake state // Nature. 2006. V. 440 (7084). P. 680—683. DOI: 10.1038/nature04587
44. Furman O., Mendelsohn A., Dudai Y. The episodic engram transformed: Time reduces retrieval-related brain activity but correlates it with memory accuracy // Learn Mem. 2012. V. 19 (12). P. 575—587. DOI: 10.1101/lm.025965.112
45. Gelbard-Sagiv H., Mukamel R., Harel M., Malach R., Fried I. Internally gener- ated reactivation of single neurons in human hippocampus during free recall // Science. 2008. V. 322. P. 96—101. DOI: 10.1126/ science.1164685
46. Gerrard J.L., Burke S.N., McNaughton B.L., Barnes C.A. Sequence reactivation in the hippocampus is impaired in aged rats // J. Neurosci. 2008. V. 28 (31). P. 7883—7890. DOI: 10.1523/JNEUROSCI.1265-08.2008
47. Getting P.A. Emerging principles governing the operation of neural networks // Annu Rev Neurosci. 1989. V. 12. P. 185—204. DOI: 10.1146/annurev.ne.12.030189.001153
48. Girardeau G., Benchenane K., Wiener S.I., Buzsaki G., Zugaro M.B. Selective suppression of hippocampal ripples impairs spatial memory //Nat.Neurosci. 2009. V. 12 (10). P. 1222—1223. DOI: 10.1038/nn.2384
49. Grosmark A.D., Buzsáki G. Diversity in neural firing dynamics supports both rigid and learned hippocampal sequences // Science. 2016. V. 351(6280). P. 1440—3. DOI: 10.1126/science.aad1935
50. Gupta A.S., van der Meer M.A., Touretzky D.S., Redish A.D. Hippocampal replay is not a simple function of experience // Neuron. 2010. V. 65(5). P. 695—705. DOI: 10.1016/j.neuron.2010.01.034
51. Harris J.A., Petersen R.S., Diamond M.E. Distribution of tactile learning and its neural basis // Proc. Natl. Acad. Sci. USA. 1999. V. 96. P. 7587—7591. DOI: 10.1073/pnas.96.13.7587
52. Harvey C.D., Coen P., Tank D.W. Choice-specific sequences in parietal cortex during a virtual-navigation decision task // Nature. 2012. V. 484(7392). P. 62—8. DOI: 10.1038/nature10918
53. Hassabis D., Kumaran D., Vann S. D., Maguire E. A. Patients with hippocampal amnesia cannot imagine new experiences // Proc. Natl Acad. Sci. USA. 2007. V. 104. P. 1726—1731. DOI: 10.1073/ pnas.0610561104
54. Hausser M., Raman I. M., Otis T., Smith S. L., Nelson A., du Lac S., Loewenstein Y., Mahon S., Pennartz C., Cohen I., Yarom Y. The beat goes on: spontaneous firing in mammalian neuronal microcircuits // J. Neurosci. 2004. V. 24 (42). P. 9215—9219. DOI: 10.1523/JNEUROSCI.3375-04.2004
55. Hobson J.A., Pace-Schott E.F. The cognitive neuroscience of sleep: neuronal systems, consciousness and learning // Nat. Rev. Neurosci. 2002. V. 3 (9). P. 679—693. DOI: 10.1038/nrn915
56. Jackson J.C., Johnson A., Redish A.D. Hippocampal sharp waves and reactivation during awake states depend on repeated sequential experience // J. Neurosci. 2006. V. 26 (48). P. 12415—12426. DOI: 10.1523/ JNEUROSCI.4118-06.2006
57. Jasnow A.M., Cullen P.K., Riccio D.C. Remembering another aspect of forgetting // Front Psychol. 2012. V. 3. P. 175. DOI: 10.3389/fpsyg.2012.00175
58. Jeannerod M., Decety J. Mental motor imagery: a window into the representational stages of action // Curr Opin Neurobiol. 1995. V. 5 (6). P. 727—732. DOI: 10.1016/0959-4388(95)80099-9
59. Jiang X., Shamie I., Doyle W., Friedman D., Dugan P., Devinsky O., Eskandar E., Cash S.S., Thesen T., Halgren E. Replay of large-scale spatio-temporal patterns from waking during subsequent NREM sleep in human cortex // Sci Rep. 2017. V. 7(1). P. 17380. DOI: 10.1038/s41598-017-17469-w
60. Karlsson M.P., Frank L.M. Awake replay of remote experiences in the hippocampus // Nat. Neurosci. 2009. V. 12 (7). P. 913—918. DOI: 10.1038/nn.2344
61. Killingsworth M.A., Gilbert D.T. A wandering mind is an unhappy mind // Science. 2010. V. 330 (6006). DOI: 10.1126/science.1192439
62. Konishi Y., Lindholm K., Yang L.B., Li R., Shen Y. Isolation of living neurons from human elderly brains using the immunomagnetic sorting DNA-linker system // Am. J. Pathol. 2002. V. 161 (5). P. 1567—1576. DOI: 10.1016/S0002-9440(10)64435-5
63. Kudrimoti H.S., Barnes C.A., McNaughton B.L. Reactivation of hippocampal cell assemblies: effects of behavioral state, experience, and EEG dynamics // J. Neurosci. 1999. V. 19 (10). P. 4090—4101. DOI: 10.1523/JNEUROSCI.19-10-04090.1999
64. Kumar D., Koyanagi I., Carrier-Ruiz A., Vergara P., Srinivasan S., Sugaya Y., Kasuya M., Yu T.S., Vogt K.E., Muratani M., Ohnishi T., Singh S., Teixeira C.M., Chérasse Y., Naoi T., Wang S.H., Nondhalee P., Osman B.A.H., Kaneko N., Sawamoto K., Kernie S.G., Sakurai T., McHugh T.J., Kano M., Yanagisawa M., Sakaguchi M. Sparse Activity of Hippocampal Adult-Born Neurons during REM Sleep Is Necessary for Memory Consolidation // Neuron. 2020. V. 107(3). P. 552—565.e10. DOI: 10.1016/j.neuron.2020.05.008
65. Kuriyama K., Stickgold R., Walker M. P. Sleep-dependent learning and motor- skill complexity // Learn Mem. 2004. V. 11 (6). P. 705—713. DOI: 10.1101/lm.76304
66. Lee A.K., Wilson M.A. Memory of sequential experience in the hippocampus during slow wave sleep // Neuron. 2002. V. 36 (6). P. 1183—1194. DOI: 10.1016/s0896-6273(02)01096-6
67. Louie K., Wilson M.A. Temporally structured replay of awake hippocampal ensemble activity during rapid eye movement sleep // Neuron. 2001. V. 29 (1). P. 145—156. DOI: 10.1016/s0896-6273(01)00186-6
68. MacDonald C.J., Carrow S., Place R., Eichenbaum H. Distinct hippocampal time cell sequences represent odor memories in immobilized rats // J. Neurosci. 2013. V. 33 (36). P. 14607—14616. DOI: 10.1523/ JNEUROSCI.1537-13.2013
69. MacDonald C.J., Lepage K.Q, Eden U.T., Eichenbaum H. Hippocampal “time cells” bridge the gap in memory for discontiguous events // Neuron. 2011. V. 71 (4). P. 737—749. DOI: 10.1016/j.neuron.2011.07.012
70. Maguire E.A., Frackowiak R.S., Frith C.D. Recalling routes around London: activation of the right hippocampus in taxi drivers // J. Neurosci. 1997. V. 17 (18). P. 7103—7110. DOI: 10.1523/ JNEUROSCI.17-18-07103.1997
71. Maquet P., Laureys S., Peigneux P., Fuchs S., Petiau C., Phillips C., Aerts J., Del Fiore G., Degueldre C., Meulemans T., Luxen A., Franck G., Van Der Lin- den M., Smith C., Cleeremans A. Experience-dependent changes in cerebral activation during human REM sleep // Nat. Neurosci. 2000. V. 3 (8). P. 831—836. DOI: 10.1038/77744
72. McKenzie S., Eichenbaum H. Consolidation and reconsolidation: two lives of memories? // Neuron. 2011. V. 71 (2). P. 224—233. DOI: 10.1016/j.neuron.2011.06.037
73. Miller J.F., Neufang M., Solway A., Brandt A., Trippel M., Mader I., Hefft S., Merkow M., Polyn S.M., Jacobs J., Kahana M.J., Schulze-Bonhage A. Neural activity in human hippocampal formation reveals the spatial context of retrieved memories // Science. 2013. V. 342(6162). P. 1111—4. DOI: 10.1126/ science.1244056
74. 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. V. 62 (6). P. 781—787. DOI: 10.1016/j.neuron.2009.05.013
75. O’Keefe J. Place units in the hippocampus of the freely moving rat // Exp. Neurol. 1976. V. 51. P. 78— 109. DOI: 10.1016/0014-4886(76)90055-8
76. O’Keefe J., Dostrovsky J. The hippocampus as a spatial map: Preliminary evi- dence from unit activity in the freely-moving rat // Brain Research. 1971. V. 34. P. 171—175. DOI: 10.1016/0006-8993(71)90358-1
77. Olafsdottir H.F., Barry C., Saleem A.B., Hassabis D., Spiers H.J. Hippocampal place cells construct reward related sequences through unexplored space // Elife. 2015. V. 4. P. e06063. DOI: 10.7554/eLife.06063
78. Olafsdottir H.F., Bush D., Barry C. The Role of Hippocampal Replay in Memory and Planning // Curr Biol. 2018. V. 28(1). P. R37—R50. DOI: 10.1016/j.cub.2017.10.073
79. O’Neill J., Senior T.J., Allen K., Huxter J.R., Csicsvari J. Reactivation of experience-dependent cell assembly patterns in the hippocampus // Nat. Neurosci. 2008. V. 11 (2). P. 209—215. DOI: 10.1038/nn2037
80. Pastalkova E., Itskov V., Amarasingham A., Buzsaki G. Internally generated cell assembly sequences in the rat hippocampus // Science. 2008. V. 321. P. 1322—1327. DOI: 10.1126/science.1159775
81. Pavlides C., Winson J. Influences of hippocampal place cell firing in the awake state on the activity of these cells during subsequent sleep episodes // J. Neurosci. 1989. V. 9 (8). P. 2907—2918. DOI: 10.1523/ JNEUROSCI.09-08-02907.1989
82. Peigneux P., Laureys S., Fuchs S., Destrebecqz A., Collette F., Delbeuck X., Phillips C., Aerts J., Del Fiore G., Degueldre C. et al. Learned material content and acquisition level modulate cerebral reactivation during posttraining rapid-eye-movements sleep // Neuroimage. 2003. V. 20. P. 125—134. DOI: 10.1016/s1053- 8119(03)00278-7
83. Peigneux P., Laureys S., Fuchs S., Collette F., Perrin F., Reggers J., Phillips C., Degueldre C., Del Fiore G., Aerts J., Luxen A., Maquet P. Are spatial memories strengthened in the human hippocampus during slow wave sleep? // Neuron. 2004. V. 44 (3). P. 535—545. DOI: 10.1016/j.neuron.2004.10.007
84. Peyrache A., Khamassi M., Benchenane K., Wiener S.I., Battaglia F.P. Replay of rule-learning related neural patterns in the prefrontal cortex during sleep // Nat. Neurosci. 2009. V. 12 (7). P. 919—926. DOI: 10.1038/nn.2337
85. Quiroga R.Q., Reddy L., Kreiman G., Koch C., Fried I. Invariant visual representation by single neurons in the human brain // Nature. 2005. V. 435 (7045). P. 1102—1107. DOI: 10.1038/nature03687
86. Ranck J.B. Studies on single neurons in dorsal hippocampal formation and septum in unrestrained rats. I. Behavioural correlates and firing repertoires // Exp Neurol. 1973. V. 41. P. 461—531. DOI: 10.1016/0014- 4886(73)90290-2. DOI: 10.1016/0014-4886(73)90290-2
87. Rasch B., Buchel C., Gais S., Born J. Odor cues during slow-wave sleep prompt declarative memory consolidation // Science. 2007. V. 315. P. 1426—1429. DOI: 10.1126/science.1138581
88. Schacter D.L., Slotnick S.D. The cognitive neuroscience of memory distortion // Neuron. 2004. V. 44(1). P. 149—160. DOI: 10.1016/j.neuron.2004.08.017
89. Singer A.C., Carr M.F., Karlsson M.P., Frank L.M. Hippocampal SWR activity predicts correct decisions during the initial learning of an alternation task // Neuron. 2013. V. 77 (6). P. 1163—1173. DOI: 10.1016/j. neuron.2013.01.027
90. Sterpenich V., Schmidt C., Albouy G., Matarazzo L., Vanhaudenhuyse A., Bover oux P., Degueldre C., Leclercq Y., Balteau E., Collette F., Luxen A., Phillips C., Maquet P. Memory reactivation during rapid eye movement sleep promotes its generalization and integration in cortical stores // Sleep. 2014. V. 37 (6). P. 1061—1075, 1075A-1075B. DOI: 10.5665/sleep.3762
91. Stickgold R., Malia A., Maguire D., Roddenberry D., O’Connor M. Replaying the game: hypnagogic images in normals and amnesics // Science. 2000a. V. 290 (5490). P. 350—353. DOI: 10.1126/science.290.5490.350
92. Stickgold R., Whidbee D., Schirmer B., Patel V., Hobson J.A. Visual discrimination task improvement: A multistep process occurring during sleep // J. Cogn. Neurosci. 2000b. V. 12 (2). P. 246—254. DOI: 10.1162/089892900562075
93. Tyler A.L., Mahoney J.M., Richard G.R., Holmes G.L., Lenck-Santini P.P., Scott R.C. Functional network changes in hippocampal CA1 after status epilepticus predict spatial memory deficits in rats // J. Neurosci. 2012. V. 32 (33). P. 11365—11376. DOI: 10.1523/JNEUROSCI.1516-12.2012
94. van der Meer M.A., Redish A.D. Expectancies in decision making, reinforcement learning and ventral striatum // Front Neurosci. 2010. V. 4. P. 6. DOI: 10.3389/neuro.01.006.2010
95. Wegner D.M., Schneider D.J., Carter S.R. 3rd, White T.L. Paradoxical effects of thought suppression // J Pers Soc Psychol. 1987. V. 53(1). P. 5—13. DOI: 10.1037//0022-3514.53.1.5. DOI: 10.1037//0022- 3514.53.1.5
96. Wilson D.A. Single-unit activity in piriform cortex during slow-wave state is shaped by recent odor experience // J Neurosci. 2010. V. 30(5). P. 1760—1765. DOI: 10.1523/JNEUROSCI.5636-09.2010
97. Wilson M.A., McNaughton B.L. Reactivation of hippocampal ensemble memories during sleep // Science. 1994. V. 265 (5172). P. 676—679. DOI: 10.1126/science.8036517
98. Wimmer G.E., Liu Y., Vehar N., Behrens T.E.J., Dolan R.J. Episodic memory retrieval success is associated with rapid replay of episode content // Nat Neurosci. 2020. V. 23(8). P. 1025—1033. DOI: 10.1038/s41593- 020-0649-z
99. Wood E.R., Dudchenko P.A., Robitsek R.J., Eichenbaum H. Hippocampal neurons encode information about different types of memory episodes occurring in the same location // Neuron. 2000. V. 27(3). P. 623— 33. DOI: 10.1016/s0896-6273(00)00071-4
100. Yuste R., MacLean J.N., Smith J., Lansner A. The cortex as a central pattern generator // Nat Rev Neurosci. 2005. V. 6(6). P. 477—83. DOI: 10.1038/nrn1686.
101. Zhang K., Ginzburg I., McNaughton B.L., Sejnowski T.J. Interpreting neuronal population activity by reconstruction: unified framework with application to hippocampal place cells // J. Neurophysiol. 1998. V. 79 (2). P. 1017—1044. DOI: 10.1152/jn.1998.79.2.1017