Circadian VIPergic Neurons of the Suprachiasmatic Nuclei Sculpt the Sleep-Wake Cycle

Collins, Ben; Pierre-Ferrer, Sara; Muheim, Christine; Lukacsovich, David; Cai, Yuchen; Spinnler, Andrea; Herrera, Carolina Gutierrez; Wen, Shao'ang; Winterer, Jochen; Belle, Mino D. C.; Piggins, Hugh D.; Hastings, Michael H.; Loudon, A. S. I.; Yan, Jun; Földy, Csaba; Adamantidis, Antoine; Brown, Steven A.

doi:10.1016/j.neuron.2020.08.001

Cited by 75 publications

(50 citation statements)

References 79 publications

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“…We show how the Drosophila circadian system creates a dynamic internal reference of what environmental conditions should be. Many of the motifs we observed are conserved: Mammalian circadian clock neuron subpopulations are also active at different times (80)(81)(82)(83) and are linked by recurrent inhibition (84)(85)(86)(87)(88), suggesting that mammalian temporal estimation may operate using similar principles. The paradigm that we developed offers opportunities to understand the interface between internal models and sensory evidence.…”

Section: Discussionmentioning

confidence: 83%

Daily rewiring of a neural circuit generates a predictive model of environmental light

2021

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Behavioral responsiveness to external stimulation is shaped by context. We studied how sensory information can be contextualized, by examining light-evoked locomotor responsiveness of Drosophila relative to time of day. We found that light elicits an acute increase in locomotion (startle) that is modulated in a time-of-day–dependent manner: Startle is potentiated during the nighttime, when light is unexpected, but is suppressed during the daytime. The internal daytime-nighttime context is generated by two interconnected and functionally opposing populations of circadian neurons—LNvs generating the daytime state and DN1as generating the nighttime state. Switching between the two states requires daily remodeling of LNv and DN1a axons such that the maximum presynaptic area in one population coincides with the minimum in the other. We propose that a dynamic model of environmental light resides in the shifting connectivities of the LNv-DN1a circuit, which helps animals evaluate ongoing conditions and choose a behavioral response.

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Section: Discussionmentioning

confidence: 83%

Daily rewiring of a neural circuit generates a predictive model of environmental light

2021

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“…Action potentials are a key output of neural circuits and SCN neuronal firing is used to communicate circadian timekeeping information to the rest of the brain 38 – 40 . To assess how baseline firing was altered by the absence of VPAC 2 receptor signaling, we used a microelectrode array (MEA) platform to record and compare spontaneous multi-unit spiking activity in the dSCN and vSCN of brain slices from WT and Vipr2 −/− mice (Fig.…”

Section: Resultsmentioning

confidence: 99%

Timed daily exercise remodels circadian rhythms in mice

et al. 2021

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Regular exercise is important for physical and mental health. An underexplored and intriguing property of exercise is its actions on the body’s 24 h or circadian rhythms. Molecular clock cells in the brain’s suprachiasmatic nuclei (SCN) use electrical and chemical signals to orchestrate their activity and convey time of day information to the rest of the brain and body. To date, the long-lasting effects of regular physical exercise on SCN clock cell coordination and communication remain unresolved. Utilizing mouse models in which SCN intercellular neuropeptide signaling is impaired as well as those with intact SCN neurochemical signaling, we examined how daily scheduled voluntary exercise (SVE) influenced behavioral rhythms and SCN molecular and neuronal activities. We show that in mice with disrupted neuropeptide signaling, SVE promotes SCN clock cell synchrony and robust 24 h rhythms in behavior. Interestingly, in both intact and neuropeptide signaling deficient animals, SVE reduces SCN neural activity and alters GABAergic signaling. These findings illustrate the potential utility of regular exercise as a long-lasting and effective non-invasive intervention in the elderly or mentally ill where circadian rhythms can be blunted and poorly aligned to the external world.

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“…We found that inhibition of SCN VIP neurons during the daytime did not delay locomotor activity offset (Fig. S3C), indicating that simple activation or inhibition of SCN VIP neurons during daytime cannot directly affect locomotor plasticity (Collins et al, 2020). Alternatively, SCN VIP neurons may not involve in mediating TRF-related behaviors.…”

Section: Resultsmentioning

confidence: 92%

Time-restricted feeding near dawn entrains long-term behavioral changes through the suprachiasmatic nucleus

Zhai

Zheng

et al. 2021

Preprint

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The suprachiasmatic nucleus (SCN) is a master circadian pacemaker known to integrate light intensity and seasonal information with peripheral tissues to coordinate daily rhythms of physiology and behavior. However, the contribution of food information to the regulation of the SCN network remains controversial. Here, we identified the effect induced by time-restricted feeding (TRF) at dawn, but not at another time widow, inducing a robust and long-term shift in locomotor behavior and increased wakefulness. Comparing the oscillations of intracellular Ca2+ signals in the SCN GABAergic neurons of freely moving mice, before and after TRF, revealed significant activation of these neurons in dawn-TRF mice. Moreover, RNA-seq profiling in the dawn TRF-induced behavioral changes identified altered expressed genes involved in regulating extracellular exosome, ion transporters, and ECM-receptor interaction, but not core clock genes. Furthermore, injection in the SCN of insulin-like growth factor (IGF2) inhibitor Chromeceptin, targeting the most upregulated gene in extracellular exosome, abolished the after effect induced by ZT0-4 TRF. Finally, GABAergic-neuron-specific disruption of the potassium-chloride cotransporter Kcc2 intensified the dawn TRF-induced after effect, indicating that Kcc2 encodes food intake derived signals that control SCN clock entrainment. Thus, our study functionally links SCN GABAergic neuron activity and central clock entrainment regulation to both hunger- and food-response-related behaviors in mice.

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Circadian VIPergic Neurons of the Suprachiasmatic Nuclei Sculpt the Sleep-Wake Cycle

Cited by 75 publications

References 79 publications

Daily rewiring of a neural circuit generates a predictive model of environmental light

Daily rewiring of a neural circuit generates a predictive model of environmental light

Timed daily exercise remodels circadian rhythms in mice

Time-restricted feeding near dawn entrains long-term behavioral changes through the suprachiasmatic nucleus

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