Abstract
The aim of this study is to detect changes in a functional state during the performance of monotonous psychomotor test. We propose that these changes represent the repeated episodes of short sleep and spontaneous awakenings from them. We also argue that spontaneous awakenings from sleep stage 2 are accompanied by high-amplitude slow oscillations (SO). 20 subjects participated in 27 experiments during daytime. They performed continuous psychomotor test in a supine position with eyes closed for 1 h. Expert scoring of SOs in the EEG, including K-complexes and other single slow waves, was performed in sleep episodes reaching sleep stage 2, defined as pauses in task performance longer than 3 s. 248 episodes with SOs occurred in time intervals without activity lasting from 3 s to 10 min. In 195 cases, at least one SO was recorded before the test performance was resumed. 248 sleep episodes with 1255 SOs were taken into analysis. It was shown that SOs occur much more frequently just before awakenings (SO1, 12 or less seconds before awakening) than within sleep episodes (12 of more seconds before awakening, SO2). Some SOs were recorded within a few seconds after behavioral awakening (SO3), which has not been previously reported. We propose the hypothesis that SOs which occurred just before resuming performance (SO1) are associated with the unconscious episodic memory that triggers awakening followed by recovery of conscious activity performed prior to falling asleep. We also describe the novel type of SO (SO3) which occurs just after awakening.
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1140%2Fepjs%2Fs11734-023-01075-1/MediaObjects/11734_2023_1075_Fig1_HTML.png)
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1140%2Fepjs%2Fs11734-023-01075-1/MediaObjects/11734_2023_1075_Fig2_HTML.png)
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1140%2Fepjs%2Fs11734-023-01075-1/MediaObjects/11734_2023_1075_Fig3_HTML.png)
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1140%2Fepjs%2Fs11734-023-01075-1/MediaObjects/11734_2023_1075_Fig4_HTML.png)
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1140%2Fepjs%2Fs11734-023-01075-1/MediaObjects/11734_2023_1075_Fig5_HTML.png)
Similar content being viewed by others
Data availability
The data sets generated during the current study are available from the corresponding author on reasonable request.
References
J. Hesse, T. Gross, Self-organized criticality as a fundamental property of neural systems. Front. Syst. Neurosci. 23(8), 166 (2014). https://doi.org/10.3389/fnsys.2014.00166
C.C. Lo, T. Chou, T. Penzel, T.E. Scammell, R.E. Strecker, H.E. Stanley, PCh. Ivanov, Common scale-invariant patterns of sleep-wake transitions across mammalian species. Proc. Natl. Acad. Sci. U.S.A. 101(50), 17545–17548 (2004). https://doi.org/10.1073/pnas.0408242101
V.B. Dorokhov, Alpha-bursts and K-complex: phasic activation pattern during spontaneous recovery of correct psychomotor performance at difference stages of drowsiness. Zh. Vyssh. Nerv. Deiat. Im. I P Pavlova 53(4), 503–512 (2003)
V.B. Dorokhov, A. Runnova, O.N. Tkachenko, A.O. Taranov, G.N. Arseniev, A. Kiselev, A. Selskii, A. Orlova, M. Zhuravlev, Analysis two types of K complexes on the human EEG based on classical continuous wavelet transform. Chaos 33(3), 031102 (2023). https://doi.org/10.1063/5.0143284
F. Siclari, G. Bernardi, B.A. Riedner, J.J. LaRocque, R.M. Benca, G. Tononi, Two distinct synchronization processes in the transition to sleep: a high-density electroencephalographic study. Sleep 37(10), 1621–1637 (2014). https://doi.org/10.5665/sleep.4070
G. Bernardi, F. Siclari, G. Handjaras, B.A. Riedner, G. Tononi, Local and widespread slow waves in stable nrem sleep: evidence for distinct regulation mechanisms. Front. Hum. Neurosci. 19(12), 248 (2018). https://doi.org/10.3389/fnhum.2018.00248
Q. Lu, U. Hasson, K.A. Norman, A neural network model of when to retrieve and encode episodic memories. Elife 10(11), e74445 (2022). https://doi.org/10.7554/eLife.74445
S. Sonkusare, M. Breakspear, C. Guo, Naturalistic stimuli in neuroscience: critically acclaimed. Trends Cogn. Sci. 23(8), 699–714 (2019). https://doi.org/10.1016/j.tics.2019.05.004
T. Schreiner, T. Staudigl, Electrophysiological signatures of memory reactivation in humans. Philos. Trans. R. Soc. Lond. B Biol. Sci. 375(1799), 20190293 (2020). https://doi.org/10.1098/rstb.2019.0293
T. Schreiner, M. Petzka, T. Staudigl, B.P. Staresina, Endogenous memory reactivation during sleep in humans is clocked by slow oscillation-spindle complexes. Nat. Commun. 12(1), 3112 (2021). https://doi.org/10.1038/s41467-021-23520-2
Y. Norman, E.M. Yeagle, S. Khuvis, M. Harel, A.D. Mehta, R. Malach, Hippocampal sharp-wave ripples linked to visual episodic recollection in humans. Science 365(6454), eaax1030 (2019). https://doi.org/10.1126/science.aax1030
S. Berres, E. Erdfelder, The sleep benefit in episodic memory: an integrative review and a meta-analysis. Psychol. Bull. 147(12), 1309–1353 (2021). https://doi.org/10.1037/bul0000350
T. Andrillon, A. Burns, T. Mackay, J. Windt, N. Tsuchiya, Predicting lapses of attention with sleep-like slow waves. Nat. Commun. 12(1), 3657 (2021). https://doi.org/10.1038/s41467-021-23890-7
M.H. Zaky, R. Shoorangiz, G.R. Poudel, L. Yang, C.R.H. Innes, R.D. Jones, Increased cerebral activity during microsleeps reflects an unconscious drive to re-establish consciousness. Int. J. Psychophysiol. S0167–8760(23), 00429–00434 (2023). https://doi.org/10.1016/j.ijpsycho.2023.05.349
G.R. Poudel, C.R. Innes, P.J. Bones, R. Watts, R.D. Jones, Losing the struggle to stay awake: divergent thalamic and cortical activity during microsleeps. Hum. Brain Mapp. 35(1), 257–269 (2014). https://doi.org/10.1002/hbm.22178
W. Moorcroft, J.L. Breitenstein, Awareness of time during sleep. Ann. Med. 32(4), 236–238 (2000)
S. Malloggi, F. Conte, B. Albinni, G. Gronchi, G. Ficca, F. Giganti, Sleep and psychological characteristics in habitual self-awakeners and forced awakeners. Chronobiol. Int. 39(4), 547–556 (2022). https://doi.org/10.1080/07420528.2021.2003375
K. Christoff, Z.C. Irving, K.C. Fox, R.N. Spreng, J.R. Andrews-Hanna, Mind-wandering as spontaneous thought: a dynamic framework. Nat. Rev. Neurosci. 17(11), 718–731 (2016). https://doi.org/10.1038/nrn.2016.113
E.M. Robertson, L. Genzel, Memories replayed: reactivating past successes and new dilemmas. Philos. Trans. R. Soc. Lond. B Biol. Sci. 375(1799), 20190226 (2020). https://doi.org/10.1098/rstb.2019.0226
P. Halász, R. Bódizs, L. Parrino, M. Terzano, Two features of sleep slow waves: homeostatic and reactive aspects–from long term to instant sleep homeostasis. Sleep Med. 15(10), 1184–1195 (2014). https://doi.org/10.1016/j.sleep.2014.06.006
T. Andrillon, S. Kouider, The vigilant sleeper: neural mechanisms of sensory (de) coupling during sleep. Curr. Opin. Phys. 15, 47–59 (2020). https://doi.org/10.1016/j.cophys.2019.12.002
A. Destexhe, S.W. Hughes, M. Rudolph, V. Crunelli, Are corticothalamic “up” states fragments of wakefulness? Trends Neurosci. 30(7), 334–342 (2007). https://doi.org/10.1016/j.tins.2007.04.006
J. Feldman, The neural binding problem(s). Cogn. Neurodyn. 7(1), 1–11 (2013). https://doi.org/10.1007/s11571-012-9219-8
R. Jerath, C. Beveridge, Multimodal integration and phenomenal spatiotemporal binding: a perspective from the default space theory. Front. Integr. Neurosci. 5(13), 2 (2019). https://doi.org/10.3389/fnint.2019.00002
A.P. Yonelinas, C. Ranganath, A.D. Ekstrom, B.J. Wiltgen, A contextual binding theory of episodic memory: systems consolidation reconsidered. Nat. Rev. Neurosci. 20(6), 364–375 (2019)
V.B. Dorokhov, V.V. Dementienko, L.G. Koreneva, A.G. Markov, V.M. Shakhnorovich, The electrodermal indices of the subjective perception of performance errors during drowsy changes in consciousness. Zh. Vyssh. Nerv. Deiat. Im. I P Pavlova 50(2), 206–218 (2000)
P. Tassi, A. Bonnefond, O. Engasser et al., EEG spectral power and cognitive performance during sleep inertia: the effect of normal sleep duration and partial sleep deprivation. Physiol. Behav. 87(1), 177–184 (2006). https://doi.org/10.1016/j.physbeh.2005.09.017
R. Vallat, D. Meunier, A. Nicolas, P. Ruby, Hard to wake up? The cerebral correlates of sleep inertia assessed using combined behavioral, EEG and fMRI measures. Neuroimage 184, 266–278 (2019). https://doi.org/10.1016/j.neuroimage.2018.09.033
V. Dorokhov, S. Gruzdeva, O. Tkachenko, E. Cheremushkin, N. Petrenko, Experimental model of consciousness in the sleep-wake paradigm: determining consciousness activation using behavioral and Electromyographic indicators. Proc. Comput. Sci. 169, 840–844 (2020). https://doi.org/10.1007/978-3-030-71637-0_49
I.M. Colrain, The K-complex: a 7-decade history. Sleep 28(2), 255–273 (2005). https://doi.org/10.1093/sleep/28.2.255
I. Duman, I.S. Ehmann, A.R. Gonsalves, Z. Gültekin, J. Van den Berckt, C. van Leeuwen, The no-report paradigm: a revolution in consciousness research? Front. Hum. Neurosci. 11(16), 861517 (2022). https://doi.org/10.3389/fnhum.2022.861517
N. Tsuchiya, M. Wilke, S. Frässle, V.A.F. Lamme, No-report paradigms: extracting the true neural correlates of consciousness. Trends Cogn. Sci. 19(12), 757–770 (2015). https://doi.org/10.1016/j.tics.2015.10.002
E. Tulving, Episodic memory: from mind to brain. Annu. Rev. Psychol. 53, 1–25 (2002). https://doi.org/10.1146/annurev.psych.53.100901.135114
N.J. Cohen, H. Eichenbaum, Memory, amnesia, and the hippocampal system (MIT press, Cambridge, 1993)
K. Henke, A model for memory systems based on processing modes rather than consciousness. Nat. Rev. Neurosci. 11(7), 523–532 (2010). https://doi.org/10.1038/nrn2850
J.D. Gabrieli, Cognitive neuroscience of human memory. Annu. Rev. Psychol. 49, 87–115 (1998). https://doi.org/10.1146/annurev.psych.49.1.87
M. Moscovitch, The hippocampus as a “stupid,” domain-specific module: Implications for theories of recent and remote memory, and of imagination. Can. J. Exp. Psychol. 62(1), 62–79 (2008). https://doi.org/10.1037/1196-1961.62.1.62
S.B. Duss, T.P. Reber, J. Hänggi, S. Schwab, R. Wiest, R.M. Müri, P. Brugger, K. Gutbrod, K. Henke, Unconscious relational encoding depends on hippocampus. Brain 137(Pt 12), 3355–3370 (2014). https://doi.org/10.1093/brain/awu270
T.P. Reber, K. Henke, Integrating unseen events over time. Conscious. Cogn. 21(2), 953–960 (2012). https://doi.org/10.1016/j.concog.2012.02.013
L. Pacozzi, L. Knüsel, S. Ruch, K. Henke, Inverse forgetting in unconscious episodic memory. Sci. Rep. 12(1), 20595 (2022). https://doi.org/10.1038/s41598-022-25100-w
I. Lerner, P.K. Pilly, A.A. Moustafa, Editorial: mechanisms contributing to sleep-dependent memory generalization. Front. Neurosci. 20(16), 1106577 (2022). https://doi.org/10.3389/fnins.2022.1106577
S.A. Hall, D.C. Rubin, A. Miles, S.W. Davis, E.A. Wing, R. Cabeza, D. Berntsen, The neural basis of involuntary episodic memories. J. Cogn. Neurosci. 26(10), 2385–2399 (2014). https://doi.org/10.1162/jocn_a_00633
E. van der Helm, N. Gujar, M. Nishida, M.P. Walker, Sleep-dependent facilitation of episodic memory details. PLoS ONE 6(11), e27421 (2011). https://doi.org/10.1371/journal.pone.002742
L. Peter-Derex, M. Magnin, H. Bastuji, Heterogeneity of arousals in human sleep: a stereo-electroencephalographic study. Neuroimage 123, 229–244 (2015). https://doi.org/10.1016/j.neuroimage.2015.07.057
P. Ruby, M. Eskinazi, R. Bouet, S. Rheims, L. Peter-Derex, Dynamics of hippocampus and orbitofrontal cortex activity during arousing reactions from sleep: an intracranial electroencephalographic study. Hum. Brain Mapp. 42(16), 5188–5203 (2021). https://doi.org/10.1002/hbm.25609
U. Voss, Change in EEG pre and post awakening. Int. Rev. Neuribiol. 93, 23–55 (2010). https://doi.org/10.1016/S0074-7742(10)93002-X
J.M. Windt, How deep is the rift between conscious states in sleep and wakefulness? Spontaneous experience over the sleep-wake cycle. Philos. Trans. R. Soc. Lond. B Biol. Sci. 376(1817), 20190696 (2021). https://doi.org/10.1098/rstb.2019.0696
Funding
This study was funded by Russian Science Foundation (Grant #22–28-01769).
Author information
Authors and Affiliations
Contributions
Conceptualization VBD; funding acquisition VBD and ONT; data curation VBD and ONT; resources VBD, AOT, GNT, EOG and NVL; supervision VBD; software ONT and VBD; investigation VBD, and ONT; methodology VBD, and ONT; sleep scoring AOT, GNT and EOG; spectra calculation AOT, GNT and EOG; validation VBD; visualization VBD and ONT; writing—review and editing VBD, ONT, AOT, GNT, EOG and NVL.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare no competing interests. The funders had no role in the design of the study, the collection, analyses, or interpretation of data, the writing of the manuscript, and the decision to publish the results.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Dorokhov, V.B., Tkachenko, O.N., Taranov, A.O. et al. Episodic memory causes a slow oscillation of EEG, awakening and performance recovery from sleep episodes during monotonous psychomotor test. Eur. Phys. J. Spec. Top. 233, 589–599 (2024). https://doi.org/10.1140/epjs/s11734-023-01075-1
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1140/epjs/s11734-023-01075-1