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Review
. 2017 Sep 15;11:65.
doi: 10.3389/fncir.2017.00065. eCollection 2017.

Plasticity During Sleep Is Linked to Specific Regulation of Cortical Circuit Activity

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Free PMC article
Review

Plasticity During Sleep Is Linked to Specific Regulation of Cortical Circuit Activity

Niels Niethard et al. Front Neural Circuits. .
Free PMC article

Abstract

Sleep is thought to be involved in the regulation of synaptic plasticity in two ways: by enhancing local plastic processes underlying the consolidation of specific memories and by supporting global synaptic homeostasis. Here, we briefly summarize recent structural and functional studies examining sleep-associated changes in synaptic morphology and neural excitability. These studies point to a global down-scaling of synaptic strength across sleep while a subset of synapses increases in strength. Similarly, neuronal excitability on average decreases across sleep, whereas subsets of neurons increase firing rates across sleep. Whether synapse formation and excitability is down or upregulated across sleep appears to partly depend on the cell's activity level during wakefulness. Processes of memory-specific upregulation of synapse formation and excitability are observed during slow wave sleep (SWS), whereas global downregulation resulting in elimination of synapses and decreased neural firing is linked to rapid eye movement sleep (REM sleep). Studies of the excitation/inhibition balance in cortical circuits suggest that both processes are connected to a specific inhibitory regulation of cortical principal neurons, characterized by an enhanced perisomatic inhibition via parvalbumin positive (PV+) cells, together with a release from dendritic inhibition by somatostatin positive (SOM+) cells. Such shift towards increased perisomatic inhibition of principal cells appears to be a general motif which underlies the plastic synaptic changes observed during sleep, regardless of whether towards up or downregulation.

Keywords: REM; SWS; excitation; inhibition; plasticity; sleep.

Figures

Figure 1
Figure 1
In vivo two-photon Ca2+ imaging during sleep. (A) Mean (±SEM) activity of pyramidal cells during the first and second half of all slow wave sleep (SWS) and rapid eye movement (REM) sleep episodes. Note, during REM sleep activity is overall lower than during SWS. Activity decreases within REM sleep epochs, but remains at the same level during SWS epochs. **p < 0.01 for pairwise comparisons. (B) In vivo two-photon imaging was performed on head-fixed mice (expressing GCaMP6f, while parvalbumin positive (PV+) or somatostatin positive (SOM+) cells are labeled with tdTomato, for recording of putative Pyr, PV+ and SOM+ cells respectively) which repeatedly went through periods of wake, SWS and REM sleep during one imaging session. Sleep stages were identified by EEG and EMG. (C) Example recordings of activity in 110 putative pyramidal cells and 17 PV+ cells that were imaged simultaneously. Note, activity of pyramidal cells, but not PV+ cells, is substantially decreased during REM sleep (with permission from Elsevier adapted from Niethard et al., 2016).
Figure 2
Figure 2
(A) Mean (±SEM) activity during epochs of wakefulness, SWS and REM sleep is shown for pyramidal-like cells (top), PV+ cells (middle) and SOM+ cells (bottom). Black lines—activity across all cells, gray lines—activity of the 20% cells most active during the wake phases. Note, compared with SWS, REM sleep is characterized by distinctly increased PV+ cell activity while SOM+ cell activity reaches minimum levels. This dynamics is particularly pronounced in the wake active cells (data are from Niethard et al., , with permission from Elsevier). (B) Mean (±SEM) activity during the slow oscillation upstate (with reference to activity during a baseline interval −3 to −2 s before the event) for slow oscillations (SO), spindles (Spindle), and spindles that nested in a slow oscillation upstate (SO+ Spindle). ##p < 0.01, for comparisons against baseline activity; **p < 0.01, *p < 0.05, for pairwise comparisons. Note, spindles and spindles nesting in a slow oscillation upstates are characterized by high PV+ cell activity in the presence of low SOM+ cell activity. Spindles co-occuring with SO are additionally associated with increased pyramidal cell activity (Niethard et al., unpublished).

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