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Cited by 188Transcranial Magnetic Stimulation StudiesSleep and Wakefulness ResearchNeural dynamics and brain function

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Transcranial Electrical Currents to Probe EEG Brain Rhythms and Memory Consolidation during Sleep in Humans

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Marshall, Lisa, Kirov, Roumen, Brade, Julian, Mölle, Matthias, Born, Jan·2011·PLoS ONE
DOI 10.1371/journal.pone.0016905PMC PMC3038929
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Abstract

Previously the application of a weak electric anodal current oscillating with a frequency of the sleep slow oscillation (∼0.75 Hz) during non-rapid eye movement sleep (NonREM) sleep boosted endogenous slow oscillation activity and enhanced sleep-associated memory consolidation. The slow oscillations occurring during NonREM sleep and theta oscillations present during REM sleep have been considered of critical relevance for memory formation. Here transcranial direct current stimulation (tDCS) oscillating at 5 Hz, i.e., within the theta frequency range (theta-tDCS) is applied during NonREM and REM sleep. Theta-tDCS during NonREM sleep produced a global decrease in slow oscillatory activity conjoint with a local reduction of frontal slow EEG spindle power (8-12 Hz) and a decrement in consolidation of declarative memory, underlining the relevance of these cortical oscillations for sleep-dependent memory consolidation. In contrast, during REM sleep theta-tDCS appears to increase global gamma (25-45 Hz) activity, indicating a clear brain state-dependency of theta-tDCS. More generally, results demonstrate the suitability of oscillating-tDCS as a tool to analyze functions of endogenous EEG rhythms and underlying endogenous electric fields as well as the interactions between EEG rhythms of different frequencies.

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Figure 1 Time line of the two experiments. (A) Theta-tDCS during NonREM sleep (NonREM Experiment) and (B) during REM sleep (REM Experiment). Respective upper panels show representative individual sleep profiles (W: wake, REM: REM sleep, S1–S4: NonREM sleep stages 1–4) and periods of stimulation. Lower parts indicate Learning and Retrieval periods for memory testing on declarative and procedural tasks. The horizontal gray bar indicates lights out.
Figure 1 Time line of the two experiments. (A) Theta-tDCS during NonREM sleep (NonREM Experiment) and (B) during REM sleep (REM Experiment). Respective upper panels show representative individual sleep profiles (W: wake, REM: REM sleep, S1–S4: NonREM sleep stages 1–4) and periods of stimulation. Lower parts indicate Learning and Retrieval periods for memory testing on declarative and procedural tasks. The horizontal gray bar indicates lights out.CC BY · PubMed Central
Figure 2 Topographical distribution and temporal pattern of EEG spectral power during NonREM sleep. (A and C) Topographical distribution of EEG power (± SEM) averaged across the 1-min stimulation-free intervals in the slow oscillation (0.4–1.2 Hz) (A), and slow spindle (8–12 Hz) frequency bands (C) after the five 5-min intervals of theta-tDCS or sham stimulation. (B and D) Time course of EEG spectral power for the five 1-min stimulation-free periods (S1–S5) immediately succeeding stimulation and for 0–30 and 30–60 min after termination of stimulation in the slow oscillation band (B), and slow spindle frequency band at Fz (D). ‘Ba’ refers to baseline activity prior to stimulation. **, P<0.01; *, P<0.05; for comparisons between the theta-tDCS and sham stimulation conditions by t-test (n = 25).
Figure 2 Topographical distribution and temporal pattern of EEG spectral power during NonREM sleep. (A and C) Topographical distribution of EEG power (± SEM) averaged across the 1-min stimulation-free intervals in the slow oscillation (0.4–1.2 Hz) (A), and slow spindle (8–12 Hz) frequency bands (C) after the five 5-min intervals of theta-tDCS or sham stimulation. (B and D) Time course of EEG spectral power for the five 1-min stimulation-free periods (S1–S5) immediately succeeding stimulation and for 0–30 and 30–60 min after termination of stimulation in the slow oscillation band (B), and slow spindle frequency band at Fz (D). ‘Ba’ refers to baseline activity prior to stimulation. **, P<0.01; *, P<0.05; for comparisons between the theta-tDCS and sham stimulation conditions by t-test (n = 25).CC BY · PubMed Central
Figure 3 Changes in EEG spectral power induced by theta-tDCS during REM sleep. Spectral power for theta-tDCS (black lines) and sham stimulation (gray lines) averaged across all EEG locations (A) and for submental electromyographic (EMG) activity (B). Time course of gamma band activity during the five 1-min stimulation-free periods immediately succeeding the stimulation intervals (S1–S5), averaged across all electrode sites for theta-tDCS (black bars) and sham stimulation (empty bars) (C). ‘Ba’ refers to baseline activity prior to stimulation. **, P<0.01; *, P<0.05; for comparisons between the theta-tDCS and sham stimulation conditions by t-test (n = 16).
Figure 3 Changes in EEG spectral power induced by theta-tDCS during REM sleep. Spectral power for theta-tDCS (black lines) and sham stimulation (gray lines) averaged across all EEG locations (A) and for submental electromyographic (EMG) activity (B). Time course of gamma band activity during the five 1-min stimulation-free periods immediately succeeding the stimulation intervals (S1–S5), averaged across all electrode sites for theta-tDCS (black bars) and sham stimulation (empty bars) (C). ‘Ba’ refers to baseline activity prior to stimulation. **, P<0.01; *, P<0.05; for comparisons between the theta-tDCS and sham stimulation conditions by t-test (n = 16).CC BY · PubMed Central
Figure 4 Theta-tDCS during NonREM sleep impairs declarative memory consolidation. (A) Retention performance on the declarative memory task (word paired-associates) across nocturnal sleep for the sham control and theta-tDCS conditions. Performance is expressed as difference between the number of correct words reported in a cued recall test at retrieval testing after sleep and in the end of learning before sleep. The list contained 46 word-pairs (**P<0.01). Performance across the retention interval on (B) the procedural finger sequence tapping task expressed as the difference in the number of correctly tapped sequences per 30 s between retrieval testing and learning, and on (C) the procedural mirror drawing task expressed as the corresponding difference in drawing time. Data are the means ± SEM. Times of performance testing within the experiments are depicted in Fig. 1.
Figure 4 Theta-tDCS during NonREM sleep impairs declarative memory consolidation. (A) Retention performance on the declarative memory task (word paired-associates) across nocturnal sleep for the sham control and theta-tDCS conditions. Performance is expressed as difference between the number of correct words reported in a cued recall test at retrieval testing after sleep and in the end of learning before sleep. The list contained 46 word-pairs (**P<0.01). Performance across the retention interval on (B) the procedural finger sequence tapping task expressed as the difference in the number of correctly tapped sequences per 30 s between retrieval testing and learning, and on (C) the procedural mirror drawing task expressed as the corresponding difference in drawing time. Data are the means ± SEM. Times of performance testing within the experiments are depicted in Fig. 1.CC BY · PubMed Central

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Research works printed but not linked: 1

  1. MS Doran, 2003, The Dynamic Topography of Individual Sleep Spindles., Sleep Research Online, 5, 133

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Metadata

Authors
Marshall, L., Kirov, R., Brade, J., Mölle, M., & Born, J.
Affiliations
  • University of Lübeck (DE)
  • Bulgarian Academy of Sciences (BG)
Corresponding author
Marshall, Lisa
ORCID
Venue
PLoS ONE
Publisher
Public Library of Science (PLoS)
Published
2011-02-14
Volume
6
Issue
2
Pages
e16905
ISSN
1932-6203 (ISSN-L)
DOI
10.1371/journal.pone.0016905
PMC
PMC3038929
OpenAlex
W1966385969
Cited by
188
References
63
Citations by year
2026: 3 · 2025: 7 · 2024: 4 · 2023: 7 · 2022: 8 · 2021: 13 · 2020: 14 · 2019: 12 · 2018: 11 · 2017: 16 · 2016: 22 · 2015: 18 · 2014: 16 · 2013: 18 · 2012: 12
FWCI
9.37
Type
journal article
Language
en
Open access
Licence
Locations
  • PLoS ONE (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Funders
  • Deutsche Forschungsgemeinschaft (SFB654)
  • Universität zu Lübeck
Topics
  • Life Sciences › Neuroscience › Neurology › Transcranial Magnetic Stimulation Studies
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Sleep and Wakefulness Research
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
Keywords
transcranial direct current stimulation, sleep slow oscillations, REM sleep, NREM sleep, memory consolidation, declarative memory, theta oscillations, gamma oscillations, EEG spindles, endogenous electric fields, sleep-dependent memory
MeSH terms
Adolescent, Adult, Biological Clocks, Brain, Electric Stimulation, Electroencephalography, Female, Humans, Male, Memory, Neuropsychological Tests, Sleep, Task Performance and Analysis, Deep Brain Stimulation, Young Adult

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