Alizadeh Zahra, Azimi Amin, Ghorbani Maryam
Department of Electrical Engineering, Ferdowsi University of Mashhad, Mashhad, 91779-48974, Iran.
Department of Physics, Institute for Advanced Studies in Basic Sciences, Zanjan, 45137-66731, Iran.
J Neurosci. 2022 Sep 21;42(38):7222-7243. doi: 10.1523/JNEUROSCI.2515-21.2022.
Temporal nesting of cortical slow oscillations, thalamic spindles, and hippocampal ripples indicates multiregional neuronal interactions required for memory consolidation. However, how the thalamic activity during spindles organizes hippocampal dynamics remains largely undetermined. We analyzed simultaneous recordings of anterodorsal thalamus and CA1 in male mice to determine the contribution of thalamic spindles in cross-regional synchronization. Our results indicated that temporal hippocampo-thalamocortical coupling was more enhanced during slower and longer thalamic spindles. Additionally, spindles occurring closer to slow oscillation trough were more strongly coupled to ripples. We found that the temporal association between CA1 spiking/ripples and thalamic spindles was stronger following spatial exploration compared with baseline sleep. We further developed a hippocampal-thalamocortical model to explain the mechanism underlying the duration and frequency-dependent coupling of thalamic spindles to hippocampal activity. Our findings shed light on our understanding of the functional role of thalamic activity during spindles on multiregional information transfer. The contribution of thalamic spindles with differential properties to cross-regional synchronization and information transfer still remains poorly understood. Using simultaneous anterodorsal thalamic and hippocampal recordings from naturally sleeping mice before and after exploration, we found strong coupling of CA1 units to anterodorsal thalamic spindles and increase of this coupling following spatial experience. We further showed that the temporal coupling of CA1 units and hippocampal ripples with thalamic spindles and the spindle-associated modulation of CA1 units with ripples were stronger for spindles with slower frequency of oscillations. Our experimental as well as computational findings using a hippocampal-thalamocortical model provide the first demonstration that spindle frequency and duration can provide valuable information about the underlying multiregional interactions essential for memory consolidation computations.
皮质慢振荡、丘脑纺锤波和海马涟漪在时间上的嵌套表明了记忆巩固所需的多区域神经元相互作用。然而，纺锤波期间的丘脑活动如何组织海马动力学在很大程度上仍未确定。我们分析了雄性小鼠前背侧丘脑和CA1的同步记录，以确定丘脑纺锤波在跨区域同步中的作用。我们的结果表明，在较慢且较长的丘脑纺锤波期间，海马 - 丘脑 - 皮质的时间耦合增强。此外，在更接近慢振荡波谷时出现的纺锤波与涟漪的耦合更强。我们发现，与基线睡眠相比，空间探索后CA1区的放电/涟漪与丘脑纺锤波之间的时间关联更强。我们进一步开发了一个海马 - 丘脑 - 皮质模型，以解释丘脑纺锤波与海马活动的持续时间和频率依赖性耦合的潜在机制。我们的研究结果有助于我们理解纺锤波期间丘脑活动在多区域信息传递中的功能作用。具有不同特性的丘脑纺锤波对跨区域同步和信息传递的贡献仍然知之甚少。通过记录自然睡眠小鼠在探索前后的前背侧丘脑和海马的同步活动，我们发现CA1区神经元与前背侧丘脑纺锤波有很强的耦合，并且在空间体验后这种耦合增强。我们进一步表明，CA1区神经元和海马涟漪与丘脑纺锤波的时间耦合以及CA1区神经元与涟漪的纺锤波相关调制，对于振荡频率较慢的纺锤波更强。我们使用海马 - 丘脑 - 皮质模型的实验和计算结果首次证明，纺锤波的频率和持续时间可以提供有关记忆巩固计算所需的潜在多区域相互作用的有价值信息。
