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Journal Club
Editor’s Note: These short reviews of recent JNeurosci articles, written exclusively by students or postdoctoral fellows,
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Sleep is essential for the formation of An element common to these two period” of visual system development,
long-term memory (Diekelmann and hypotheses is the modification of synaptic occlusion of one eye causes the represen-
Born, 2010). Two major hypotheses have strengths within cortical networks. In the tation of the spared eye to expand rapidly
emerged linking the memory functions of cortex and elsewhere in the mammalian in the visual cortex (Wiesel and Hubel,
sleep to cortical excitability and plasticity. brain, synapses undergo two major forms 1963). This sensory-driven remapping de-
The synaptic homeostasis hypothesis of long-lasting plasticity, LTP and LTD, pends on the transient suppression of PV
(Tononi and Cirelli, 2003) states that characterized by a persistent increase or interneurons and the consequent disinhi-
sleep renormalizes the net increase in decrease in synaptic efficacy, respectively. bition of pyramidal cell somata (Kuhlman
synaptic strength that accrues during Both processes are involved in memory et al., 2013). Disinhibition also underlies
wakefulness. In this framework, learn- (Malenka and Bear, 2004); and impor- enhanced plasticity in adulthood, although
ing during waking experience leads to tantly, both processes depend on the acti- this involves primarily dendritic disinhibi-
a cumulative potentiation of synapses. vation of postsynaptic NMDARs and the tion through suppression of SST activity
To avoid excessive potentiation and main- resulting Ca21 influx (Collingridge et al., or increased VIP activity (Fu et al., 2015).
tain homeostatic equilibrium, sleep resets 2010). Whether LTP or LTD occurs can Conversely, increased SST action blocks
the excitability of neurons by facilitating a depend on whether the postsynaptic cell somatosensory plasticity associated with
net downscaling of synapses (Tononi and spikes (Bi and Poo, 1998), which is deter- neuropathic pain (Cichon et al., 2017).
Cirelli, 2003). The two-stage theory pos- mined partly by inhibitory input. Together, these findings indicate that
tulates that sleep consolidates memory The principal projection neurons of PV, SST, and VIP interneurons control
through hippocampo-cortical transmis- the cortex (i.e., pyramidal cells) receive cortical plasticity in addition to control-
sion (Frankland and Bontempi, 2005). inhibitory inputs at specific somatoden- ling pyramidal cell output.
According to this theory, waking experi- dritic regions from different interneuron The role of inhibitory interneurons in
ence is initially encoded as a labile, short- subtypes, including parvalbumin (PV)-, sleep-dependent plasticity is only begin-
term representation in the hippocampus. somatostatin (SST)-, and vasoactive intes- ning to be understood (Aime et al., 2022).
In subsequent sleep, neuronal replay of tinal polypeptide (VIP)-expressing neu- A recent study by Brécier et al. (2022)
hippocampal activity that occurred in rons (Tremblay et al., 2016). PVs inhibit examined how the activity of PV, SST, and
prior wakefulness drives the strengthen- the soma and proximal dendrites of py- VIP interneurons evolves over the sleep/
ing of corticocortical connections, con- ramidal cells, whereas SSTs inhibit distal wake cycle. Using transgenic mice injected
solidating the labile memory into stable, dendrites. VIP interneurons, in contrast, with a genetically encoded Ca21 indicator,
long-term storage in the cortex. inhibit SST cells, causing disinhibition the authors selectively targeted PV, SST,
of pyramidal-cell distal dendrites (Fig. or VIP interneurons and measured Ca21-
1). The combinatorial input from differ- driven fluorescence changes over wake,
ent interneuron subtypes can generate rapid-eye movement (REM) sleep and
Received Aug. 24, 2022; revised Oct. 19, 2022; accepted Oct. 26, 2022.
Publication costs were supported by Natural Sciences and distinct spatiotemporal patterns of inhi- non-REM (NREM) sleep. The Ca21 sig-
Engineering Research Council (NSERC) Grant 298475 awarded to bition over the pyramidal cell, allowing nal is commonly used as a measure of
Dr. Igor Timofeev. precise control of cortical output. neuronal activity; and although it does
The authors declare no competing financial interests. Much evidence points to inhibition not resolve fast events such as action
Correspondence should be addressed to Diellor Basha at diellor.
[email protected].
as a key mediator of cortical plasticity potentials, it enables the simultaneous
https://doi.org/10.1523/JNEUROSCI.1631-22.2022 (Maffei et al., 2010; Kuhlman et al., monitoring of multiple cells in vivo.
Copyright © 2023 the authors 2013). During the highly plastic “critical Using mice that were trained to sleep
524 • J. Neurosci., January 25, 2023 • 43(4):523–525 Desrosiers and Basha · Cortical Inhibition, Plasticity, and Sleep
REM sleep, the threshold for synaptic REM activity patterns, this brief spindle- Frankland PW, Bontempi B (2005) The organiza-
plasticity is raised along the entire py- related somatodendritic decoupling (Seibt tion of recent and remote memories. Nat Rev
ramidal neuron, an assertion that sup- et al., 2017) likely facilitates corticocortical Neurosci 6:119–130.
Fu Y, Kaneko M, Tang Y, Alvarez-Buylla A,
ports the synaptic downscaling claim of integration precisely during the reactiva-
Stryker MP (2015) A cortical disinhibitory
the synaptic homeostasis hypothesis. tion of memory traces related to hippo- circuit for enhancing adult plasticity. Elife 4:
However, dendritic disinhibition and the campal replay in spindle-sharp wave ripple e05558.
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can occur at the distal dendrites of the demonstrate that the pattern of inhibition circuit initiates critical-period plasticity in the
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