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Niethard, N.* ; Brodt, S.* ; Born, J.

Cell-type specific dynamics of calcium activity in cortical circuits over the course of slow wave sleep and rapid eye movement sleep.

J. Neurosci. 41, 4212-4222 (2021)
Verlagsversion DOI PMC
Open Access Gold (Paid Option)
Creative Commons Lizenzvertrag
Sleep shapes cortical network activity, fostering global homeostatic down-regulation of excitability while maintaining or even up-regulating excitability in selected networks in a manner that supports memory consolidation. Here we used two-photon calcium imaging of cortical layer 2/3 neurons in sleeping male mice to examine how these seemingly opposing dynamics are balanced in cortical networks. During slow-wave sleep (SWS) episodes, mean calcium activity of excitatory pyramidal (Pyr) cells decreased. Simultaneously, however, variance in Pyr population calcium activity increased, contradicting the notion of a homogenous down-regulation of network activity. Indeed, we identified a subpopulation of Pyr cells distinctly up-regulating calcium activity during SWS, which were highly active during sleep spindles known to support mnemonic processing. REM episodes following SWS were associated with a general down-regulation of Pyr cells - including the subpopulation of Pyr cells active during spindles - which persisted into following stages of sleep and wakefulness. Parvalbumin-positive inhibitory interneurons (PV-In) showed an increase in calcium activity during SWS episodes, while activity remained unchanged during REM sleep episodes. This supports the view that down-regulation of Pyr calcium activity during SWS results from increased somatic inhibition via PV-In, whereas down-regulation during REM sleep is achieved independently of such inhibitory activity. Overall, our findings show that SWS enables up-regulation of select cortical circuits (likely those which were involved in mnemonic processing) through a spindle-related process, whereas REM sleep mediates general down-regulation, possibly through synaptic re-normalization.SIGNIFICANCE STATEMENTSleep is thought to globally down-regulate cortical excitability and, concurrently, to up-regulate synaptic connections in neuron ensembles with newly encoded memory, with up-regulation representing a function of sleep spindles. Using in-vivo two-photon calcium imaging in combination with surface EEG recordings, we classified cells based on their calcium activity during sleep spindles. Spindle-active pyramidal cells persistently increased calcium activity during slow wave sleep (SWS) episodes while spindle-inactive cells decreased calcium activity. Subsequent rapid-eye movement (REM) sleep episodes profoundly reduced calcium activity in both cell clusters. Results indicate that SWS allows for a spindle-related differential up-regulation of ensembles whereas REM sleep functions to globally down-regulate networks.
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Publikationstyp Artikel: Journalartikel
Dokumenttyp Wissenschaftlicher Artikel
Korrespondenzautor
Schlagwörter Calcium Imaging ; Rem ; Sleep ; Slow Oscillation ; Slow-wave Sleep ; Spindle; Rem; Oscillations; Spindles; Interneurons; Inhibition; Plasticity; Synapses; Promotes; Induce; Waking
ISSN (print) / ISBN 0270-6474
e-ISSN 1529-2401
Zeitschrift Journal of Neuroscience
Quellenangaben Band: 41, Heft: 19, Seiten: 4212-4222 Artikelnummer: , Supplement: ,
Verlag Society for Neuroscience
Verlagsort 11 Dupont Circle, Nw, Ste 500, Washington, Dc 20036 Usa
Nichtpatentliteratur Publikationen
Begutachtungsstatus Peer reviewed
Institut(e) Institute of Diabetes Research and Metabolic Diseases (IDM)
Förderungen German Excellence Initiative
Deutsche Forschungsgemeinschaft