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Heterogenous electrophysiological responses of functionally distinct striatal subregions to circadian and sleep-related homeostatic processes.

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Basal Ganglia (BG) are a set of subcortical nuclei that are involved in the control of a wide variety of motor, cognitive and affective behaviors. Although many behavioral abnormalities associated… Click to show full abstract

Basal Ganglia (BG) are a set of subcortical nuclei that are involved in the control of a wide variety of motor, cognitive and affective behaviors. Although many behavioral abnormalities associated with BG dysfunction overlap with the clinical picture precipitated by the lack of sleep, the impact of sleep alterations on neuronal activity in BG is unknown. Using wildtype C57BI mice, we investigated the circadian and sleep-related homeostatic modulation of neuronal activity in the 3 functional subdivisions of the striatum (i.e. sensorimotor, associative and limbic striatum). We found no circadian modulation of activity in both ventral and dorso-medial striatum while the dorso-lateral striatum displayed a significant circadian rhythm with increased firing rates during the subjective dark, active phase. By combining neuronal activity recordings with electroencephalogram (EEG) recordings, we found a strong modulation of neuronal activity by the nature of vigilance states with increased activity during wakefulness and rapid eye movement sleep relative to non-rapid eye movement sleep in all striatal subregions. Depriving animals of sleep for 6 hours induced significant, but heterogenous alterations in the neuronal activity across striatal subregions. Notably, these alterations lasted for up to 48 hours in the sensorimotor striatum and persisted even after the normalization of cortical EEG power densities. Our results show that vigilance and sleep states as well as their disturbances significantly affect neuronal activity within the striatum. We propose that these changes in neuronal activity underlie both the well-established links between sleep alterations and several disorders involving BG dysfunction as well as the maladaptive changes in behavior induced in healthy subjects following sleep loss.

Keywords: neuronal activity; striatal subregions; circadian sleep; striatum; sleep related; activity

Journal Title: Sleep
Year Published: 2021

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