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A Novel Approach to Estimating the Cortical Sources of Sleep Spindles Using Simultaneous EEG/MEG.

ABSTRACT: Sleep spindles, defining oscillations of stage II non-rapid eye movement sleep (N2), mediate sleep-dependent memory consolidation. Spindles are disrupted in several neurodevelopmental, neuropsychiatric, and neurodegenerative disorders characterized by cognitive impairment. Increasing spindles can improve memory suggesting spindles as a promising physiological target for the development of cognitive enhancing therapies. This effort would benefit from more comprehensive and spatially precise methods to characterize spindles. Spindles, as detected with electroencephalography (EEG), are often widespread across electrodes. Available evidence, however, suggests that they act locally to enhance cortical plasticity in the service of memory consolidation. Here, we present a novel method to enhance the spatial specificity of cortical source estimates of spindles using combined EEG and magnetoencephalography (MEG) data constrained to the cortex based on structural MRI. To illustrate this method, we used simultaneous EEG and MEG recordings from 25 healthy adults during a daytime nap. We first validated source space spindle detection using only EEG data by demonstrating strong temporal correspondence with sensor space EEG spindle detection (gold standard). We then demonstrated that spindle source estimates using EEG alone, MEG alone and combined EEG/MEG are stable across nap sessions. EEG detected more source space spindles than MEG and each modality detected non-overlapping spindles that had distinct cortical source distributions. Source space EEG was more sensitive to spindles in medial frontal and lateral prefrontal cortex, while MEG was more sensitive to spindles in somatosensory and motor cortices. By combining EEG and MEG data this method leverages the differential spatial sensitivities of the two modalities to obtain a more comprehensive and spatially specific source estimation of spindles than possible with either modality alone.

SUBMITTER: Mylonas D

PROVIDER: S-EPMC9243385 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Sleep spindles are approximately 1-second bursts of 10-15 Hz activity, occurring during normal stage 2 sleep. In animals, sleep spindles can be synchronous across multiple cortical and thalamic locations, suggesting a distributed stable phase-locked generating system. The high synchrony of spindles across scalp EEG sites suggests that this may also be true in humans. However, prior MEG studies suggest multiple and varying generators.We recorded 306 channels of MEG simultaneously with 60 channels of EEG during naturally occurring spindles of stage 2 sleep in 7 healthy subjects. High-resolution structural MRI was obtained in each subject, to define the shells for a boundary element forward solution and to reconstruct the cortex providing the solution space for a noise-normalized minimum norm source estimation procedure. Integrated across the entire duration of all spindles, sources estimated from EEG and MEG are similar, diffuse and widespread, including all lobes from both hemispheres. However, the locations, phase and amplitude of sources simultaneously estimated from MEG versus EEG are highly distinct during the same spindles. Specifically, the sources estimated from EEG are highly synchronous across the cortex, whereas those from MEG rapidly shift in phase, hemisphere, and the location within the hemisphere.The heterogeneity of MEG sources implies that multiple generators are active during human sleep spindles. If the source modeling is correct, then EEG spindles are generated by a different, diffusely synchronous system. Animal studies have identified two thalamo-cortical systems, core and matrix, that produce focal or diffuse activation and thus could underlie MEG and EEG spindles, respectively. Alternatively, EEG spindles could reflect overlap at the sensors of the same sources as are seen from the MEG. Although our results generally match human intracranial recordings, additional improvements are possible and simultaneous intra- and extra-cranial measures are needed to test their accuracy.

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A Novel Approach to Estimating the Cortical Sources of Sleep Spindles Using Simultaneous EEG/MEG.

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