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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)

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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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