Abstract
Recent findings link fronto-temporal gamma electroencephalographic (EEG) activity to conscious awareness in dreams, but a causal relationship has not yet been established. We found that current stimulation in the lower gamma band during REM sleep influences ongoing brain activity and induces self-reflective awareness in dreams. Other stimulation frequencies were not effective, suggesting that higher order consciousness is indeed related to synchronous oscillations around 25 and 40 Hz.
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Acknowledgements
We thank A. Antal and C. Stephani for technical advice, S. Weyn Banningh for data collection, J. Windt for helpful discussions, K. Schermelleh-Engel for advice on statistical procedures, C. Frenzel for technical assistance during preliminary work, and A. Melnikova and C. Naefgen for help with data acquisition of pilot data. This work was supported by the German Science Foundation (DFG Vo 650/5-1).
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U.V., W.P. and M.A.N. designed the study. R.H. developed the filter algorithms and conducted the analyses. J.K.-G. and U.V. collected the data, U.V., R.H., M.A.N., W.P., A.K. and A.H. wrote the manuscript. All of the authors discussed the results and commented on the manuscript.
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Integrated supplementary information
Supplementary Figure 1 Study Design
Double-blind repeated measures tACS stimulation (30 s duration, each) in REM sleep over 4 non-consecutive nights. Frequency of stimulation (sham, 2, 6, 12, 25, 40, 70, and 100 Hz) was counterbalanced across subjects and across nights. The experimenter operating the tACS device did not interact with the subjects. The experimenter conducting the interview stayed outside the monitoring room during stimulation, unable to identify the stimulation condition (for sham stimulation, the push button on the tACS device was activated but current was not applied). Extensive exploration gave no indication of subjective discomfort or awareness of stimulation in any subject.
Supplementary Figure 2 Montage and Stimulation Potentials
a) Montage of 22-channel EEG (bandpass filtered: 0.3 – 120 Hz, sampling rate: 512 Hz) and sites of tACS electrode placement (a, b, c, d). tACS electrodes a and b, as well as c and d were connected pair-wise. The AC current flowed mainly sagitally between a and c, respectively b and d. The combined impedances of the paired tACS electrodes were kept below 5 kΩ. EEG electrodes were referenced to Cz instead of mastoids because of the close proximity of the latter to the tACS electrodes c and d. b) Measured scalp surface potentials applied during one arbitrarily chosen maximum of a 40 Hz sinusoidal tACS stimulation in a single subject, with all polarities reverting every 12.5 milliseconds (voltage scale given in relative units). See Online Methods for details. c) Mathematically derived dura potential (CSD estimate). The dura potential indicates the effect of the stimulation current entering the skull, spreading from fronto-temporal to parieto-occipital regions, as well.
Supplementary Figure 3 Empirical Model of Dream Consciousness
Positions on the indicated primary-to-secondary consciousness axis are based on the logarithm of ratios of mean scores in lucid and non-lucid dreams. All factors have been identified as components of dream consciousness. Lucid dreams, which are thought to add elements of secondary consciousness, are characterized by increased ratings in reflective INSIGHT, CONTROL, and DISSOCIATION; and, to a lesser extent, by access to MEMORY, as well as NEGATIVE and POSITIVE EMOTIONS. THOUGHT and REALISM do not differentiate between lucid and non-lucid dreams. The graph is based on the laboratory scores shown in Fig. 4 of Voss et al.9 (LuCiD scale). For validation purposes, mean scores of the dream reports under sham condition in the current sample were compared to those of the original study on the basis of which these factors were constructed9. Scores of both studies compared well, suggesting reliable subjective ratings in the current study (INSIGHT: t = 0.91, p = 0.366; CONTROL: t = 0.46, p = 0.647; THOUGHT: t = 1.20, p = 0.231; REALISM: t = 1.08, p = 0.283; MEMORY: t = 1.59, p = 0.133; DISSOCIATION: t = 0.73, p = 0.470; NEGATIVE EMOTION: t = 1.49, p = 0.139; POSITIVE EMOTION: t = 0.39, p = 0.700, df = 106, all n.s.).
Supplementary Figure 4 Sample EEG Recordings During tACS
EEG and EMG data recorded during sham condition (top) and with tACS stimulation of 12 Hz (center), respectively 40 Hz (bottom). The EEG at site Fpz is shown unfiltered while the EMG is filtered to demonstrate that subject remained in REM sleep throughout stimulation; awakening (sham: t = 220 s, 12 Hz: t = 195 s, 40 Hz: t = 215 s) is signaled by a marked change in the EMG. Note also that the EEG samples shown are not corrected for ocular artefacts. The horizontal accolades schematically indicate the phases defined in the main text, namely, before stimulation (I), during stimulation (II), as well as after forced awakening (IV). During phase II, the tACS current is applied for 30 s generating the very large amplitudes indicated as a solid blue block in the unfiltered EEG (center and bottom frames). Phases I, II, and III (not indicated here) cover REM sleep, and phase IV corresponds to wakefulness
Supplementary Figure 5 Grand Average EEG Power vs. Frequency
Grand average FFT power was computed as a function of the EEG frequency (resolution = 1 Hz) for indicated stimulation conditions: sham (N = 30), 2 Hz (N = 31), 6 Hz (N = 19), 12 Hz (N = 18), 25 Hz (N = 26), 40 Hz (N = 44), 70 Hz (N = 21), and 100 Hz (N = 18). Averaging took place over frontal and temporal electrode sites (Fp1, Fp2, Fpz, F3, F4, Fz, F7, F8, T3, T4, T5, and T6), over stimulation sequences, and over subjects. The dips in power mark those frequencies for which a notch filter was applied. Phases I & II correspond to REM sleep, phase IV to wakefulness.
Supplementary Figure 6 Additional Mean LuCiD Scores vs. Stimulus
Mean scores (±1 s.e.) are shown for the LuCiD factors THOUGHT, REALISM, MEMORY, NEGATIVE EMOTION, and POSITIVE EMOTION. Significant contrasts from MANOVA (N = 207) exist only for REALISM (sham vs. 2 Hz: p = 0.032, 2 Hz vs. 100 Hz: p = 0.0097) and for MEMORY (sham vs. 70 Hz: p = 0.035, 40 Hz vs. 70 Hz: p = 0.009). In accordance with previous laboratory data9, THOUGHT and REALISM are reported in a similar pattern across all stimulation conditions. Albeit not reaching statistical significance, ratings for both NEGATIVE and POSITIVE EMOTION appear to decrease linearly with increasing stimulus frequency (as indicated by dashed lines).
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Supplementary Figures 1–6 and Supplementary Tables 1–4 (PDF 753 kb)
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Voss, U., Holzmann, R., Hobson, A. et al. Induction of self awareness in dreams through frontal low current stimulation of gamma activity. Nat Neurosci 17, 810–812 (2014). https://doi.org/10.1038/nn.3719
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DOI: https://doi.org/10.1038/nn.3719
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