Kinoshita Fukuaki L, Yamada Rikuhiro G, Ode Koji L, Ueda Hiroki R
Department of Neurology, Graduate School of Medicine, Osaka University, Osaka, Japan.
Laboratory for Synthetic Biology, RIKEN Center for Biosystems Dynamics Research, Osaka, Japan.
PLoS Biol. 2025 Jun 12;23(6):e3003198. doi: 10.1371/journal.pbio.3003198. eCollection 2025 Jun.
Understanding synaptic dynamics during the sleep-wake cycle in the cortex is crucial yet remains controversial. The synaptic homeostasis hypothesis (SHY) suggests synaptic depression during non-rapid eye movement (NREM) sleep, while other studies report synaptic potentiation or synaptic changes during NREM sleep depending on activities in wakefulness. To find boundary conditions between these contradictory observations, we focused on learning rules and firing patterns that contribute to the synaptic dynamics. Using computational models considering mammalian cortical neurons, we found that under Hebbian and spike-timing dependent plasticity (STDP), wake-like firing patterns decrease synaptic weights, while sleep-like patterns strengthen synaptic weights. We refer to this tendency as Wake Inhibition and Sleep Excitation (WISE). Conversely, under Anti-Hebbian and Anti-STDP, synaptic depression during NREM sleep was observed, aligning with the conventional synaptic homeostasis hypothesis. Moreover, synaptic changes depended on firing rate differences between NREM sleep and wakefulness. We provide a unified framework that could explain synaptic homeodynamics under the sleep-wake cycle.
了解皮质中睡眠-觉醒周期期间的突触动力学至关重要，但仍存在争议。突触稳态假说（SHY）表明在非快速眼动（NREM）睡眠期间突触会发生抑制，而其他研究报告称，根据清醒时的活动情况，NREM睡眠期间会出现突触增强或突触变化。为了找出这些相互矛盾的观察结果之间的边界条件，我们专注于有助于突触动力学的学习规则和放电模式。使用考虑哺乳动物皮质神经元的计算模型，我们发现，在赫布型和尖峰时间依赖可塑性（STDP）条件下，类似清醒的放电模式会降低突触权重，而类似睡眠的模式会增强突触权重。我们将这种趋势称为清醒抑制和睡眠兴奋（WISE）。相反，在反赫布型和反STDP条件下，观察到NREM睡眠期间的突触抑制，这与传统的突触稳态假说一致。此外，突触变化取决于NREM睡眠和清醒之间的放电率差异。我们提供了一个统一的框架，可以解释睡眠-觉醒周期下的突触动态平衡。
