Effects of prolonged waking-auditory stimulation on electroencephalogram synchronization and cortical coherence during subsequent slow-wave sleep

Abstract

Evidence suggests that sleep homeostasis is not only dependent on duration of previous wakefulness but also on experience- and/or use-dependent processes. Such homeostatic mechanisms are reflected by selective increases in the duration of a sleep stage, modifications to electrophysiological-metabolic brain patterns in specific sleep states, and/or reactivation to neuronal ensembles in subsequent sleep periods. Use-dependent sleep changes, apparently different from those changes caused by memory consolidation processes, are thought to reflect neuronal restoration processes after the sustained exposure to stimulation during the preceding wakefulness. In the present study, we investigated changes in the brain electrical activity pattern during human sleep after 6 hr of continuous auditory stimulation during previous wakefulness. Poststimulation nights showed a widespread increase of spectral power within the alpha (8-12 Hz) and sleep spindle (12-15 Hz) frequency range during slow-wave sleep (SWS) compared with the baseline night. This effect was mainly attributable to an enhanced EEG amplitude rather than an increase of oscillations, except for temporal (within alpha and sleep spindles) and parietal regions (within sleep spindles) in which both parameters contributed equally to the increase of spectral energy. Power increments were accompanied by a strengthening of the coherence between fronto-temporal cortical regions within a broad frequency range during SWS but to the detriment of the coherence between temporal and parieto-occipital areas, suggesting underlying compensatory mechanisms between temporal and other cortical regions. In both cases, coherence was built up progressively across the night, although no changes were observed within each SWS period. No electrophysiological changes were found in rapid eye movement sleep. These results point to SWS as a critical brain period for correcting the cortical synaptic imbalance produced by the predominant use of specific neuronal populations during the preceding wakefulness, as well as for synaptic reorganization after prolonged exposure to a novel sensory experience.

Fig. 1.

Mean absolute power spectra calculated for SWS and REM. Electrodes over the same brain region were collapsed (frontal: F3, F4, and Fz; central: C3, C4, and Cz; temporal: T3a, T3, T5a, T5, T4a, T4, T6a, and T6; parietal: P3, P4, and Pz; occipital: O1 and O2). Right and left labels indicate the effects of the stimulation side on spectral power during sleep. Black bars below each SWS spectrum denote significance levels (post hoct tests) between experimental (right or left) and baseline nights only when overall rANOVA showed a main effect of the night factor. Auditory stimulation in wakefulness was followed by a power increase during SWS circumscribed to the α and spindle ranges over almost the whole scalp, whereas no differences among nights were found during REM sleep.

Fig. 2.

Mean percentage increases in the EEG spectral power, wave incidence, and wave amplitude within the α and spindle range during the SWS periods in nights after acoustic overstimulation compared with baseline night in only those cortical regions [central (C), parietal (P), occipital (O), and temporal (T)] in which overall rANOVAs revealed main effects. Asterisks indicate significant increase (p < 0.05) in both nights after auditory stimulation compared with baseline night. Note that significant increments of spectral power within α and sleep spindle band were mainly caused by an increase in wave amplitude, although enhanced spectral power was further observed to be partially attributable to a significant increase in the wave incidence over temporal regions for both frequency bands and parietal areas only for sleep spindles.

Fig. 3.

Mean EEG coherence values during SWS for those coherence pairs that showed significant differences in the overall rANOVA. right and left indicate the effects of the stimulation side on the EEG coherence during sleep.Bottom bar panels represent post hocsignificance levels for comparisons between baseline and experimental (right or left) nights. Short-range coherence over the posterior left hemisphere (P3O1–T5aT5) decreased (gray bars), whereas long-range fronto-temporal coherence (F3C3–T5aT5) increased (black bars) after auditory stimulation over a wide spectral range compared with the baseline night. A schematic topographic representation of the coherence locations is depicted on the left bottom corner of each graphic.

Fig. 4.

Mean and SE percentage of coherence change and in those coherence pairs (F3C3–T5aT5 and P3O1–T5aT5) in which the overall rANOVAs showed main effects of the night factor (baseline, right, and left stimulation) for each classic frequency band during SWS periods after either right or left acoustic overstimulation.Post hoc comparisons (baseline vs poststimulation night) for each coherence pair and frequency band are also reported (*p < 0.05; **p < 0.005). Note that significant changes in cortical coherence were restricted to the night just after the first exposure to the auditory stimulation (right session). The direction of these changes in functional coupling between cortical areas was different in each case. Right auditory stimulation significantly weakened cortical coherence between left posterior cortex (P3O1) and left posterior temporal regions (T5aT5), whereas the coherence between left fronto-central cortex (F3C3) and left posterior temporal regions (T5aT5) were strengthened compared with the baseline night.