A common hub for sleep and motor control in the substantia nigra

Liu, Danqian; Li, Weifu; Ma, Chenyan; Zheng, Weitong; Yao, Yunpeng; Tso, Chak Foon; Zhong, Peng; Chen, Xi; Song, Jun; Choi, Woochul; Paik, Se-Bum; Han, Hua; Dan, Yang

doi:10.1126/science.aaz0956

Cited by 97 publications

(97 citation statements)

References 39 publications

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“…Remarkably, STN DBS, which has been shown to reduce beta oscillation (51), is associated with an improvement in subjective sleep quality (27) and reductions in insomnia and sleep fragmentation in PD (27,28). Finally, a dual BG involvement in sleep homeostasis and motor control was recently supported by a work showing that GAD2 neurons in the SNr promote sleep generation, possibly through their projections to various monoaminergic nuclei orchestrating the vigilance cycle (52).…”

Section: Discussionmentioning

confidence: 98%

Basal ganglia beta oscillations during sleep underlie Parkinsonian insomnia

Mizrahi-Kliger

Kaplan

Israel

et al. 2020

Proc. Natl. Acad. Sci. U.S.A.

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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.

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Section: Discussionmentioning

confidence: 98%

Basal ganglia beta oscillations during sleep underlie Parkinsonian insomnia

Mizrahi-Kliger

Kaplan

Israel

et al. 2020

Proc. Natl. Acad. Sci. U.S.A.

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“…These data can be continuous body parts trajectories that comprehensively capture the motion of the animal's limbs and torso. Theoretically, the natural characteristics of animal movement involve locomotion and non-locomotor movement (NM) [34][35][36]. Locomotion can be represented by velocitybased parameters.…”

Section: Framework Of the Unsupervised Animal Movement Analysismentioning

confidence: 99%

A Hierarchical 3D-motion Learning Framework for Animal Spontaneous Behavior Mapping

Huang

Han

Chen

et al. 2020

Preprint

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Objective quantification of animal behavior is crucial to understanding the relationship between brain activity and behavior. For rodents, this has remained a challenge due to the high-dimensionality and large temporal variability of their behavioral features. Inspired by the natural structure of animal behavior, the present study uses a parallel, multi-stage approach to decompose motion features and generate an objective metric for mapping rodent behavior into the animal's feature space. Incorporating a three-dimensional (3D) motion-capture system and unsupervised clustering into this approach, we developed a framework that can automatically identify animal behavioral phenotypes from experimental monitoring. We demonstrate the efficacy of our framework by generating an "autistic-like behavior space" that can robustly characterize a transgenic mouse disease model based on motor activity without human supervision. Our results suggest that our framework features a broad range of applications, including animal disease model phenotyping and the modeling of relationships between neural circuits and behavior.

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“…To guarantee rest, however, the output of both BB and GDB had to be paralyzed (Nicolau et al, 2000;Rial et al, 2010). BB was paralyzed after developing a group of inhibitory cells in the substantia nigra, pars reticulata, that in modern mammals is responsible of blocking the NREM behavioral output (Liu et al, 2020), while a group of glycinergic-GABAergic neurons of the rostroventral medulla were developed to provoke the REM muscular atonia (Sakai et al, 1979;Lai & Siegel, 1988;Morales et al, 2006;Vetrivelan et al, 2009). So, NREM and REM are paralyzed versions of BB and GDB, respectively (Nicolau et al, 2000;Rial et al, 2007Rial et al, , 2010Rial et al, , 2018.…”

Section: The Birth Of the Mammalian Sleepmentioning

confidence: 99%

How The Mammalian Sleep Was Born

Rial¹,

Cañellas²,

Gamundı́³

et al. 2020

Preprint

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The Nocturnal Bottleneck explains how mammals evolved from their reptilian ancestors after inverting the chronotype, form diurnal to nocturnal. Pre-mammals traded-off the excellent visual system of their ancestors for improvements in audition and in olfactory telencephalon, needed for efficient orientation in the dark. This was how the mammalian nocturnal telencephalic wakefulness was born. However, the modified visual system of those pre-mammals became sensitive to the dangerous diurnal light and the exposure would involve a high risk of blindness and death. Therefore, pre-mammals had to remain immobile with closed eyes hidden in lightproof burrows during light time. This was the birth of the mammalian sleep. Typical reptiles distribute their wake time cycling between Basking Behavior, to attain the preferred body temperature, and poikilothermic Goal Directed Behavior, to perform life sustaining tasks. These cycles persisted during the new mammalian sleep. However, as the behavioral output had to be blocked during light time, the paralyzed reptilian Basking Behavior and Goal Directed Behavior cycles became the NREM and REM cycles, respectively. This was how NREM and REM cycles remained incorporated within the mammalian sleep. After the Cretaceous-Paleogene extinction, the environmental pressure for nocturnal life was softened, allowing high variability in chronotype and sleeping patterns. This permitted some mammalian groups, e.g., primates, to begin the quest for diurnal wake.Concluding, sleep constituted an additional bottleneck in the mammalian evolution. The reduced population of pre-mammals that was able to develop sleep during light time, including NREM and REM, became full mammals and survived; the remainder perished.

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A common hub for sleep and motor control in the substantia nigra

Cited by 97 publications

References 39 publications

Basal ganglia beta oscillations during sleep underlie Parkinsonian insomnia

Basal ganglia beta oscillations during sleep underlie Parkinsonian insomnia

A Hierarchical 3D-motion Learning Framework for Animal Spontaneous Behavior Mapping

How The Mammalian Sleep Was Born

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