Alpha reactivity to complex sounds differs during REM sleep and wakefulness

Abstract

We aimed at better understanding the brain mechanisms involved in the processing of alerting meaningful sounds during sleep, investigating alpha activity. During EEG acquisition, subjects were presented with a passive auditory oddball paradigm including rare complex sounds called Novels (the own first name - OWN, and an unfamiliar first name - OTHER) while they were watching a silent movie in the evening or sleeping at night. During the experimental night, the subjects' quality of sleep was generally preserved. During wakefulness, the decrease in alpha power (8-12 Hz) induced by Novels was significantly larger for OWN than for OTHER at parietal electrodes, between 600 and 900 ms after stimulus onset. Conversely, during REM sleep, Novels induced an increase in alpha power (from 0 to 1200 ms at all electrodes), significantly larger for OWN than for OTHER at several parietal electrodes between 700 and 1200 ms after stimulus onset. These results show that complex sounds have a different effect on the alpha power during wakefulness (decrease) and during REM sleep (increase) and that OWN induce a specific effect in these two states. The increased alpha power induced by Novels during REM sleep may 1) correspond to a short and transient increase in arousal; in this case, our study provides an objective measure of the greater arousing power of OWN over OTHER, 2) indicate a cortical inhibition associated with sleep protection. These results suggest that alpha modulation could participate in the selection of stimuli to be further processed during sleep.

Figure 1. Alpha activity induced by novel stimuli during wakefulness.

Left panel. Time-frequency analysis (TF) plots for OWN and OTHER at the electrode Pz, after baseline correction (baseline defined from −300 to −100 ms). x-axis : time, y-axis : frequency, the vertical white line indicates stimulus onset and the gray lines indicate the 8–12 Hz frequency band. Right panel. Scalp topographies (back-top views) of alpha power are presented in each tested 200 ms time window. The color scale represents in red (negative values) a decrease in oscillatory power compared to the baseline level, and in yellow (positive values) an increase. Black dots on the topographies indicate electrodes showing a significant alpha increase or decrease compared to baseline. In the bottom right corner, the arrow indicates the view angle used to generate the back-top topographies.

Figure 2. Alpha activity induced by OWN during sleep stages N2 and N3.

Time-frequency analysis (TF) plots for OWN at electrode Pz, after baseline correction (baseline defined from −300 to −100 ms). x-axis: time, y-axis: frequency, the vertical white line indicates stimulus onset and the horizontal gray lines delineate the alpha frequency band (8–12 Hz).

Figure 3. Alpha activity induced by novel stimuli during REM sleep.

Left panel. Time-frequency analysis (TF) plots for OWN and OTHER at the electrode Pz, after baseline correction (baseline defined from −300 to −100 ms). x-axis : time, y-axis : frequency, the vertical white line indicates stimulus onset and the gray lines indicate the 8–12 Hz frequency band. Right panel. Scalp topographies (back-top views) of alpha power are presented in each tested 200 ms time window. The color scale represents in red (negative values) a decrease in oscillatory power compared to the baseline level, and in yellow (positive values) an increase. Black dots on the topographies indicate electrodes showing a significant alpha increase or decrease compared to baseline.

Figure 4. Alpha activity induced by novel stimuli.

Upper panel. Time-Frequency (TF) plots for OWN, OTHER and OWN minus OTHER in the wakefulness and REM sleep conditions at the electrode Pz, after baseline correction (baseline defined from −300 to −100 ms). x-axis: time, y-axis: frequency, the vertical white line indicates stimulus onset and the horizontal gray lines indicate the time windows showing a significant difference between OWN and OTHER in the 8–12 Hz frequency band. Scalp topographies (back-top views) of alpha power are presented in the 700–900 ms time window during wakefulness and in the 1000–1200 ms time window during REM sleep. The color scale represents in red (negative values) a decrease in oscillatory power compared to the baseline level, and in yellow (positives values) an increase. The scalp topographies with a gray scale indicate electrodes showing a significantly different alpha power for OWN vs OTHER (p<0.05). Lower panel. Time profiles of TF power in the 8–12 Hz frequency band at the electrode Pz for OWN (bold continuous line), OTHER (thin continuous line) and OWN minus OTHER (dotted line) in the wakefulness (red) and in the REM sleep condition (green). Colored areas indicate the time windows with a significant difference in alpha power between OWN and OTHER during wakefulness (in red) and REM sleep (in green). The next stimulus (a standard tone) is presented 1260 ms after the first names onsets.