EEG slow waves, the hallmarks of NREM sleep are thought to be crucial for the regulation of several important processes, including learning, sensory disconnection and the removal of brain metabolic wastes. Animal research indicates that slow waves may involve complex interactions within and between cortical and subcortical structures. Conventional EEG in humans, however, has a low spatial resolution and is unable to accurately describe changes in the activity of subcortical and deep cortical structures. To overcome these limitations, here we took advantage of simultaneous EEG-fMRI recordings to map cortical and subcortical hemodynamic (BOLD) fluctuations time-locked to slow waves of light sleep. Recordings were performed in twenty healthy adults during an afternoon nap. Slow waves were associated with BOLD-signal increases in the posterior brainstem and in portions of thalamus and cerebellum characterized by preferential functional connectivity with limbic and somatomotor areas, respectively. At the cortical level, significant BOLD-signal decreases were instead found in several areas, including insula and somatomotor cortex. Specifically, a slow signal increase preceded slow-wave onset and was followed by a delayed, stronger signal decrease. Similar hemodynamic changes were found to occur at different delays across most cortical brain areas, mirroring the propagation of electrophysiological slow waves, from centro-frontal to inferior temporo-occipital cortices. Finally, we found that the amplitude of electrophysiological slow waves was positively related to the magnitude and inversely related to the delay of cortical and subcortical BOLD-signal changes. These regional patterns of brain activity are consistent with theoretical accounts of the functions of sleep slow waves.

Cortical and subcortical hemodynamic changes during sleep slow waves in human light sleep / Betta, Monica; Handjaras, Giacomo; Leo, Andrea; Federici, Alessandra; Farinelli, Valentina; Ricciardi, Emiliano; Siclari, Francesca; Meletti, Stefano; Ballotta, Daniela; Benuzzi, Francesca; Bernardi, Giulio. - In: NEUROIMAGE. - ISSN 1053-8119. - 236:(2021), pp. 118117_1-118117_17. [10.1016/j.neuroimage.2021.118117]

Cortical and subcortical hemodynamic changes during sleep slow waves in human light sleep

Meletti, Stefano;Ballotta, Daniela;Benuzzi, Francesca;
2021

Abstract

EEG slow waves, the hallmarks of NREM sleep are thought to be crucial for the regulation of several important processes, including learning, sensory disconnection and the removal of brain metabolic wastes. Animal research indicates that slow waves may involve complex interactions within and between cortical and subcortical structures. Conventional EEG in humans, however, has a low spatial resolution and is unable to accurately describe changes in the activity of subcortical and deep cortical structures. To overcome these limitations, here we took advantage of simultaneous EEG-fMRI recordings to map cortical and subcortical hemodynamic (BOLD) fluctuations time-locked to slow waves of light sleep. Recordings were performed in twenty healthy adults during an afternoon nap. Slow waves were associated with BOLD-signal increases in the posterior brainstem and in portions of thalamus and cerebellum characterized by preferential functional connectivity with limbic and somatomotor areas, respectively. At the cortical level, significant BOLD-signal decreases were instead found in several areas, including insula and somatomotor cortex. Specifically, a slow signal increase preceded slow-wave onset and was followed by a delayed, stronger signal decrease. Similar hemodynamic changes were found to occur at different delays across most cortical brain areas, mirroring the propagation of electrophysiological slow waves, from centro-frontal to inferior temporo-occipital cortices. Finally, we found that the amplitude of electrophysiological slow waves was positively related to the magnitude and inversely related to the delay of cortical and subcortical BOLD-signal changes. These regional patterns of brain activity are consistent with theoretical accounts of the functions of sleep slow waves.
2021
236
118117_1
118117_17
Cortical and subcortical hemodynamic changes during sleep slow waves in human light sleep / Betta, Monica; Handjaras, Giacomo; Leo, Andrea; Federici, Alessandra; Farinelli, Valentina; Ricciardi, Emiliano; Siclari, Francesca; Meletti, Stefano; Ballotta, Daniela; Benuzzi, Francesca; Bernardi, Giulio. - In: NEUROIMAGE. - ISSN 1053-8119. - 236:(2021), pp. 118117_1-118117_17. [10.1016/j.neuroimage.2021.118117]
Betta, Monica; Handjaras, Giacomo; Leo, Andrea; Federici, Alessandra; Farinelli, Valentina; Ricciardi, Emiliano; Siclari, Francesca; Meletti, Stefano;...espandi
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