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The subcortical belly of sleep: New possibilities in neuromodulation of basal ganglia?

ABSTRACT: Early studies posited a relationship between sleep and the basal ganglia, but this relationship has received little attention recently. It is timely to revisit this relationship, given new insights into the functional anatomy of the basal ganglia and the physiology of sleep, which has been made possible by modern techniques such as chemogenetic and optogenetic mapping of neural circuits in rodents and intracranial recording, functional imaging, and a better understanding of human sleep disorders. We discuss the functional anatomy of the basal ganglia, and review evidence implicating their role in sleep. Whilst these studies are in their infancy, we suggest that the basal ganglia may play an integral role in the sleep-wake cycle, specifically by contributing to a thalamo-cortical-basal ganglia oscillatory network in slow-wave sleep which facilitates neural plasticity, and an active state during REM sleep which enables the enactment of cognitive and emotional networks. A better understanding of sleep mechanisms may pave the way for more effective neuromodulation strategies for sleep and basal ganglia disorders.

SUBMITTER: Hasegawa H

PROVIDER: S-EPMC7679363 | biostudies-literature | 2020 Aug

REPOSITORIES: biostudies-literature

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The subcortical belly of sleep: New possibilities in neuromodulation of basal ganglia?

Hasegawa Harutomo H Selway Richard R Gnoni Valentina V Beniczky Sandor S Williams Steve C R SCR Kryger Meir M Ferini-Strambi Luigi L Goadsby Peter P Leschziner Guy D GD Ashkan Keyoumars K Rosenzweig Ivana I

Sleep medicine reviews 20200422

Early studies posited a relationship between sleep and the basal ganglia, but this relationship has received little attention recently. It is timely to revisit this relationship, given new insights into the functional anatomy of the basal ganglia and the physiology of sleep, which has been made possible by modern techniques such as chemogenetic and optogenetic mapping of neural circuits in rodents and intracranial recording, functional imaging, and a better understanding of human sleep disorders ...[more]

PMID: 32446196

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Project description:ObjectivesThe aim was to describe the contribution of basal ganglia (BG) thalamo-cortical circuitry to the whole-brain functional connectivity in focal epilepsies.MethodsInterictal resting-state fMRI recordings were acquired in 46 persons with focal epilepsies. Of these 46, 22 had temporal lobe epilepsy: 9 left temporal (LTLE), 13 right temporal (RTLE); 15 had frontal lobe epilepsy (FLE); and 9 had parietal/occipital lobe epilepsy (POLE). There were 20 healthy controls. The complete weighted network was analyzed based on correlation matrices of 90 and 194 regions. The network topology was quantified on a global and regional level by measures based on graph theory, and connection-level changes were analyzed by the partial least square method.ResultsIn all patient groups except RTLE, the shift of the functional network topology away from random was observed (normalized clustering coefficient and characteristic path length were higher in patient groups than in controls). Links contributing to this change were found in the cortico-subcortical connections. Weak connections (low correlations) consistently contributed to this modification of the network. The importance of regions changed: decreases in the subcortical areas and both decreases and increases in the cortical areas were observed in node strength, clustering coefficient and eigenvector centrality in patient groups when compared to controls. Node strength decreases of the basal ganglia, i.e. the putamen, caudate, and pallidum, were displayed in LTLE, FLE, and POLE. The connectivity within the basal ganglia-thalamus circuitry was not disturbed; the disturbance concerned the connectivity between the circuitry and the cortex.SignificanceFocal epilepsies affect large-scale brain networks beyond the epileptogenic zones. Cortico-subcortical functional connectivity disturbance was displayed in LTLE, FLE, and POLE. Significant changes in the resting-state functional connectivity between cortical and subcortical structures suggest an important role of the BG and thalamus in focal epilepsies.

Dataset Information

The subcortical belly of sleep: New possibilities in neuromodulation of basal ganglia?

Publications

The subcortical belly of sleep: New possibilities in neuromodulation of basal ganglia?

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