Ongoing neural oscillations predict the post-stimulus outcome of closed loop auditory stimulation during slow-wave sleep

Abstract

The large slow oscillation (SO, 0.5-2Hz) that characterises slow-wave sleep is crucial to memory consolidation and other physiological functions. Manipulating slow oscillations can enhance sleep and memory, as well as benefitting the immune system. Closed-loop auditory stimulation (CLAS) has been demonstrated to increase the SO amplitude and to boost fast sleep spindle activity (11-16Hz). Nevertheless, not all such stimuli are effective in evoking SOs, even if they are precisely phase-locked. Here, we studied whether it is possible to use ongoing activity patterns to determine which oscillations to stimulate in order to effectively enhance SOs or SO-locked spindle activity. To this end, we trained classifiers using the morphological characteristics of the ongoing SO, as measured by electroencephalography (EEG), to predict whether stimulation would lead to a benefit in terms of the resulting SO and spindle amplitude. Separate classifiers were trained using trials from spontaneous control and stimulated datasets, and we evaluated their performance by applying them to held-out data both within and across conditions. We were able to predict both when large SOs will occur spontaneously, and whether a phase-locked auditory click will effectively enlarge them with an accuracy of ~70%. We were also able to predict when stimulation would elicit spindle activity with an accuracy of ~60%. Finally, we evaluate the importance of the various SO features used to make these predictions. Our results offer new insight into SO and spindle dynamics and provide a new method for online optimisation of stimulation.

Response of sleep slow oscillations to acoustic stimulation is evidenced by distinctive synchronization processes

“…This hypothesis further suggests the existence of some nonexplicit cortical conditions that determine cortical sensitivity to the stimulation (i.e., whether the stimulation would boost SOs dynamics, whether it would be completely ineffective, or even induce awakenings). In line with this hypothesis, recent analyses suggest that the amplitude of SO peaks may facilitate global synchronization of post-neuronal down-states, thereby enhancing the amplitudes of the resulting slow wave troughs (Navarrete et al, 2022;Torres et al, 2021;Wei et al, 2020). Congruently, we found that large and synchronous C1 and C3 events were increased by stimuli during large peaks of the SOs (with average amplitudes larger than +40 μV across all EEG channels, Figures 2e & 2f).…”

“…Presumably, CLAS might only enhance SO-SS-SWR coupling when the stimulus is able to increase the corticothalamic coordination of SW troughs which then sustain the co-occurrence of cortical down-states in the thalamus (Navarrete et al, 2020b;Todorova and Zugaro, 2020). Indeed, the capability of enhancing this corticothalamic coordination may not only lie in the effect of the stimulation, but also in the ongoing dynamics of the cortical activity during the CLAS click (Navarrete et al, 2022(Navarrete et al, , 2020a. However, currently it is not clear how the stimulus disturbs the ongoing neuronal dynamics and the characteristics of the resulting post-stimulus SW.…”