Sleep-Dependent Plasticity Requires Cortical Activity

Jha, Sushil K.; Jones, Brian E.; Coleman, Tammi; Steinmetz, Nicholas A.; Law, Chi-Tat; Griffin, Gerald D.; Hawk, Joshua D.; Dabbish, Nooreen; Kalatsky, Valery A.; Frank, Marcos G.

doi:10.1523/jneurosci.2722-05.2005

Cited by 95 publications

(129 citation statements)

References 40 publications

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“…A dependency of this form of plasticity on glutamatergic activity on the one hand and sleep on the other has been shown previously (Frank et al, 2001;Ramoa et al, 2001). Previously, it was demonstrated in addition that neuronal activity was necessary during sleep for plastic changes to occur (Jha et al, 2005). Although plasticity in the developing and adult visual cortex are not identical (Carmignoto and Vicini, 1992), our results show that also in the adult human, learning based on very simple processes of synaptic plasticity requires glutamate receptor reactivation during the following hours.…”

Section: Discussionsupporting

confidence: 77%

Visual–Procedural Memory Consolidation during Sleep Blocked by Glutamatergic Receptor Antagonists

Gais¹,

Rasch²,

Wagner³

et al. 2008

J. Neurosci.

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Visual cortex plasticity is enhanced by sleep. It is hypothesized that a reactivation of glutamatergic synapses is essential for this form of plasticity to occur after learning. To test this hypothesis, human subjects practiced a visual texture discrimination skill known to require post-training sleep for improvements to occur. During sleep, glutamatergic transmission was inhibited by administration of the two glutamate antagonists, caroverine and ketamine, targeting the ionotropic NMDA and AMPA receptors. Both substances given during consolidation sleep in a placebo controlled crossover design were able to prevent improvement of the skill measured the next morning. An off-line activation of glutamatergic synapses therefore seems to play a critical part in the consolidation of plastic changes in the visual cortex.

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Section: Discussionsupporting

confidence: 77%

Visual–Procedural Memory Consolidation during Sleep Blocked by Glutamatergic Receptor Antagonists

Gais¹,

Rasch²,

Wagner³

et al. 2008

J. Neurosci.

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“…Specifically, we confirmed that the diffusion of the dye Pontamine blue (2%) was confined to the frontal area surrounding the electrode. Also, the injection of a solution of 20% lidocaine, a sodium channel blocker that causes a temporary inhibition of neuronal activity (Amzica and Steriade, 1995;Jha et al, 2005), suppressed EEG activity only at the corresponding (frontal) LFP, and did not affect either the contralateral frontal LFP, or the parietal LFPs. All solutions were infused through polyethylene tubing (5 l/injection delivered over 10 min) connected to a Hamilton syringe controlled by a microinfusion pump (CMA 400 Syringe Pump; CMA Microdialysis, Solna, Sweden).…”

Section: Methodsmentioning

confidence: 99%

A Causal Role for Brain-Derived Neurotrophic Factor in the Homeostatic Regulation of Sleep

Faraguna¹,

Vyazovskiy²,

Nelson³

et al. 2008

J. Neurosci.

250

186

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Slow-wave activity (SWA), the EEG power between 0.5 and 4 Hz during non-rapid eye movement (NREM) sleep, is one of the best characterized markers of sleep need, because it increases as a function of preceding waking duration and decreases during sleep, but the underlying mechanisms remain unknown. We hypothesized that SWA is high at sleep onset because it reflects the occurrence, during the previous waking period, of widespread synaptic potentiation in cortical and subcortical areas. Consistent with this hypothesis, we recently showed that the more rats explore, the stronger is the cortical expression of BDNF during wakefulness, and the larger is the increase in SWA during the subsequent sleep period. There is compelling evidence that BDNF plays a causal role in synaptic potentiation, and exogenous application of BDNF in vivo is sufficient to induce long-term increases in synaptic strength. We therefore performed cortical unilateral microinjections of BDNF in awake rats and measured SWA during the subsequent sleep period. SWA during NREM sleep was higher in the injected hemisphere relative to the contralateral one. The effect was reversible within 2 h, and did not occur during wakefulness or rapid eye movement sleep. Asymmetries in NREM SWA did not occur after vehicle injections. Furthermore, microinjections, during wakefulness, of a polyclonal anti-BDNF antibody or K252a, an inhibitor of BDNF TrkB receptors, led to a local SWA decrease during the following sleep period. These effects were also reversible and specific for NREM sleep. These results show a causal link between BDNF expression during wakefulness and subsequent sleep regulation.

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“…Increased potentiation of cortical electrophysiological responses during sleep was observed in adult mice (Aton & et al, 2014) and cats (Chauvette, Seigneur, & Timofeev, 2012). In kittens, the early development of the visual cortex depends on plasticity mechanisms triggered during sleep (Jha et al, 2005;Seibt et al, 2012), including an upregulation of Arc and BDNF translation (Jha et al, 2005;Seibt et al, 2012). In the rat dorsal hippocampus, REM deprivation has been shown to decrease long-term potentiation (LTP), synaptic transmission, glutamate receptor protein levels, and ERK/MAPK activation (Ravassard & et al, 2009).…”

Section: Introductionmentioning

confidence: 99%

Experience-dependent upregulation of multiple plasticity factors in the hippocampus during early REM sleep

Calais

Ojopi

Morya

et al. 2015

Neurobiology of Learning and Memory

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Sleep is beneficial to learning, but the underlying mechanisms remain controversial. The synaptic homeostasis hypothesis (SHY) proposes that the cognitive function of sleep is related to a generalized rescaling of synaptic weights to intermediate levels, due to a passive downregulation of plasticity mechanisms. A competing hypothesis proposes that the active upscaling and downscaling of synaptic weights during sleep embosses memories in circuits respectively activated or deactivated during prior waking experience, leading to memory changes beyond rescaling. Both theories have empirical support but the experimental designs underlying the conflicting studies are not congruent, therefore a consensus is yet to be reached. To advance this issue, we used real-time PCR and electrophysiological recordings to assess gene expression related to synaptic plasticity in the hippocampus and primary somatosensory cortex of rats exposed to novel objects, then kept awake (WK) for 60 min and finally killed after a 30 min period rich in WK, slow-wave sleep (SWS) or rapid-eye-movement sleep (REM). Animals similarly treated but not exposed to novel objects were used as controls. We found that the mRNA levels of Arc, Egr1, Fos, Ppp2ca and Ppp2r2d were significantly increased in the hippocampus of exposed animals allowed to enter REM, in comparison with control animals. Experience-dependent changes during sleep were not significant in the hippocampus for Bdnf, Camk4, Creb1, and Nr4a1, and no differences were detected between exposed and control SWS groups for any of the genes tested. No significant changes in gene expression were detected in the primary somatosensory cortex during sleep, in contrast with previous studies using longer post-stimulation intervals (>180 min). The experience-dependent induction of multiple plasticity-related genes in the hippocampus during early REM adds experimental support to the synaptic embossing theory.

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Sleep-Dependent Plasticity Requires Cortical Activity

Cited by 95 publications

References 40 publications

Visual–Procedural Memory Consolidation during Sleep Blocked by Glutamatergic Receptor Antagonists

Visual–Procedural Memory Consolidation during Sleep Blocked by Glutamatergic Receptor Antagonists

A Causal Role for Brain-Derived Neurotrophic Factor in the Homeostatic Regulation of Sleep

Experience-dependent upregulation of multiple plasticity factors in the hippocampus during early REM sleep

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