Binini Noemi, Talpo Francesca, Spaiardi Paolo, Maniezzi Claudia, Pedrazzoli Matteo, Raffin Francesca, Mattiello Niccolò, Castagno Antonio N, Masetto Sergio, Yanagawa Yuchio, Dickson Clayton T, Ramat Stefano, Toselli Mauro, Biella Gerardo Rosario
Department of Biology and Biotechnology Lazzaro Spallanzani, University of Pavia, Pavia, Italy.
Department of Brain and Behavioral Sciences, University of Pavia, Pavia, Italy.
Front Cell Neurosci. 2021 Jul 22;15:703407. doi: 10.3389/fncel.2021.703407. eCollection 2021.
The perirhinal cortex (PRC) is a polymodal associative region of the temporal lobe that works as a gateway between cortical areas and hippocampus. In recent years, an increasing interest arose in the role played by the PRC in learning and memory processes, such as object recognition memory, in contrast with certain forms of hippocampus-dependent spatial and episodic memory. The integrative properties of the PRC should provide all necessary resources to select and enhance the information to be propagated to and from the hippocampus. Among these properties, we explore in this paper the ability of the PRC neurons to amplify the output voltage to current input at selected frequencies, known as membrane resonance. Within cerebral circuits the resonance of a neuron operates as a filter toward inputs signals at certain frequencies to coordinate network activity in the brain by affecting the rate of neuronal firing and the precision of spike timing. Furthermore, the ability of the PRC neurons to resonate could have a fundamental role in generating subthreshold oscillations and in the selection of cortical inputs directed to the hippocampus. Here, performing whole-cell patch-clamp recordings from perirhinal pyramidal neurons and GABAergic interneurons of GAD67-GFP mice, we found, for the first time, that the majority of PRC neurons are resonant at their resting potential, with a resonance frequency of 0.5-1.5 Hz at 23°C and of 1.5-2.8 Hz at 36°C. In the presence of ZD7288 (blocker of HCN channels) resonance was abolished in both pyramidal neurons and interneurons, suggesting that I current is critically involved in resonance generation. Otherwise, application of TTx (voltage-dependent Na channel blocker) attenuates the resonance in pyramidal neurons but not in interneurons, suggesting that only in pyramidal neurons the persistent sodium current has an amplifying effect. These experimental results have also been confirmed by a computational model. From a functional point of view, the resonance in the PRC would affect the reverberating activity between neocortex and hippocampus, especially during slow wave sleep, and could be involved in the redistribution and strengthening of memory representation in cortical regions.
嗅周皮质(PRC)是颞叶的一个多模态联合区域,充当皮质区域与海马体之间的通道。近年来,人们对PRC在学习和记忆过程(如物体识别记忆)中所起的作用越来越感兴趣,这与某些形式的依赖海马体的空间和情景记忆形成对比。PRC的整合特性应提供所有必要资源,以选择和增强要在海马体之间传播的信息。在这些特性中,我们在本文中探讨了PRC神经元在选定频率下将输出电压放大为电流输入的能力,即膜共振。在大脑回路中,神经元的共振作为对特定频率输入信号的滤波器,通过影响神经元放电速率和尖峰时间精度来协调大脑中的网络活动。此外,PRC神经元的共振能力可能在产生阈下振荡以及选择导向海马体的皮质输入方面发挥重要作用。在这里,通过对GAD67-GFP小鼠的嗅周锥体神经元和GABA能中间神经元进行全细胞膜片钳记录,我们首次发现,大多数PRC神经元在静息电位时具有共振特性,在23°C时共振频率为0.5 - 1.5 Hz,在36°C时为1.5 - 2.8 Hz。在存在ZD7288(HCN通道阻滞剂)的情况下,锥体神经元和中间神经元的共振均被消除,这表明I电流在共振产生中起关键作用。否则,应用TTX(电压依赖性Na通道阻滞剂)会减弱锥体神经元的共振,但不会减弱中间神经元的共振,这表明只有在锥体神经元中,持续性钠电流具有放大作用。这些实验结果也得到了计算模型的证实。从功能角度来看,PRC中的共振会影响新皮质和海马体之间的回响活动,尤其是在慢波睡眠期间,并且可能参与皮质区域记忆表征的重新分配和强化。