Synaptic Mechanisms of Memory Consolidation during Sleep Slow Oscillations

By Yina Wei, Giri Panamoottil Krishnan, Maxim Bazhenov. 2016

92 citations recorded by the source corpus.

Sleep is critical for regulation of synaptic efficacy, memories, and learning. However, the underlying mechanisms of how sleep rhythms contribute to consolidating memories acquired during wakefulness remain unclear. Here we studied the role of slow oscillations, 0.2–1 Hz rhythmic transitions between Up and Down states during stage 3/4 sleep, on dynamics of synaptic connectivity in the thalamocortical network model implementing spike-timing-dependent synaptic plasticity. We found that the spatiotemporal pattern of Up-state propagation determines the changes of synaptic strengths between neurons. Furthermore, an external input, mimicking hippocampal ripples, delivered to the cortical network results in input-specific changes of synaptic weights, which persisted after stimulation was removed. These synaptic changes promoted replay of specific firing sequences of the cortical neurons. Our study proposes a neuronal mechanism on how an interaction between hippocampal input, such as mediated by sharp wave-ripple events, cortical slow oscillations, and synaptic plasticity, may lead to consolidation of memories through preferential replay of cortical cell spike sequences during slow-wave sleep. SIGNIFICANCE STATEMENT Sleep is critical for memory and learning. Replay during sleep of temporally ordered spike sequences related to a recent experience was proposed to be a neuronal substrate of memory consolidation. However, specific mechanisms of replay or how spike sequence replay leads to synaptic changes that underlie memory consolidation are still poorly understood. Here we used a detailed computational model of the thalamocortical system to report that interaction between slow cortical oscillations and synaptic plasticity during deep sleep can underlie mapping hippocampal memory traces to persistent cortical representation. This study provided, for the first time, a mechanistic explanation of how slow-wave sleep may promote consolidation of recent memory events.

Subfields: Cognitive Neuroscience

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Citations in the corpus

Replay in Deep Learning: Current Approaches and Missing Biological Elements (2021, neutral): “Both spindles and slow oscillations demonstrate characteristic spatiotemporal dynamics (Muller et al., 2016), and its properties determine synaptic changes during sleep (Wei et al., 2016).”
Biologically inspired sleep algorithm for artificial neural networks (2019, methodology): “However, our approach signiﬁcantly differs from these previous attempts, in that we used conversion method from ANN to SNN and implemented sleep at the SNN level which is relatively well understood from the neuroscience perspective [15, 16, 33, 30].”
Can sleep protect memories from catastrophic forgetting? (2019, unknown): “…variety of sleep functions remains to be understood, there is growing evidence for the role of sleep in consolidation of newly encoded memories (Oudiette and Paller, 2013; Paller and Voss, 2004; Rasch and Born, 2013; Stickgold, 2013; Walker and Stickgold, 2004; Wei et al., 2016; Wei et al., 2018).”
Sleep prevents catastrophic forgetting in spiking neural networks by forming a joint synaptic weight representation (2022, background): “We previously showed that sleep replay improves memory in a thalamocortical network [38–40] and when a network was trained to learn interfering tasks sequentially, sleep prevented the old task memory from catastrophic forgetting [41].”
Cellular and neurochemical basis of sleep stages in the thalamocortical network (2016, methodology): “The model included populations of pyramidal (PY) cells and inhibitory interneurons (IN) in the cortex, and thalamic relay (TC) and reticular nucleus (RE) neurons in the thalamus (Figure 1A); it was designed based on our previous studies of sleep slow oscillations and sleep spindles (Bazhenov et al.,”
Bidirectional Interaction of Hippocampal Ripples and Cortical Slow Waves Leads to Coordinated Spiking Activity During NREM Sleep. (2020, methodology): “This was likely because the network slow wave activity has some refractoriness (Wei et al. 2016), so a single ripple event could not instantly trigger global”
How can memories last for days, years, or a lifetime? Proposed mechanisms for maintaining synaptic potentiation and memory (2019, background): “In particular, replay of recently learned engrams during sleep is frequent and is likely to contribute to engram consolidation (Giri et al. 2019; Wei et al. 2016).”