Basal ganglia beta oscillations during sleep underlie Parkinsonian insomnia.

Aviv D Mizrahi-Kliger, Alexander Kaplan, Zvi Israel, Marc Deffains, Hagai Bergman

Proceedings of the National Academy of Sciences of the United States of America 2020 Jul 21

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Sleep disorders are among the most debilitating comorbidities of Parkinson's disease (PD) and affect the majority of patients. Of these, the most common is insomnia, the difficulty to initiate and maintain sleep. The degree of insomnia correlates with PD severity and it responds to treatments that decrease pathological basal ganglia (BG) beta oscillations (10-17 Hz in primates), suggesting that beta activity in the BG may contribute to insomnia. We used multiple electrodes to record BG spiking and field potentials during normal sleep and in 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine (MPTP)-induced Parkinsonism in nonhuman primates. MPTP intoxication resulted in severe insomnia with delayed sleep onset, sleep fragmentation, and increased wakefulness. Insomnia was accompanied by the onset of nonrapid eye movement (NREM) sleep beta oscillations that were synchronized across the BG and cerebral cortex. The BG beta oscillatory activity was associated with a decrease in slow oscillations (0.1-2 Hz) throughout the cortex, and spontaneous awakenings were preceded by an increase in BG beta activity and cortico-BG beta coherence. Finally, the increase in beta oscillations in the basal ganglia during sleep paralleled decreased NREM sleep, increased wakefulness, and more frequent awakenings. These results identify NREM sleep beta oscillation in the BG as a neural correlate of PD insomnia and suggest a mechanism by which this disorder could emerge.

Citation

Aviv D Mizrahi-Kliger, Alexander Kaplan, Zvi Israel, Marc Deffains, Hagai Bergman. Basal ganglia beta oscillations during sleep underlie Parkinsonian insomnia. Proceedings of the National Academy of Sciences of the United States of America. 2020 Jul 21;117(29):17359-17368