Motosada Iwase, Kamran Diba, Eva Pastalkova, Kenji Mizuseki
{"title":"海马和内视网膜皮层主细胞和中间神经元之间的尖峰传递和抑制动态。","authors":"Motosada Iwase, Kamran Diba, Eva Pastalkova, Kenji Mizuseki","doi":"10.1002/hipo.23612","DOIUrl":null,"url":null,"abstract":"<p>Synaptic excitation and inhibition are essential for neuronal communication. However, the variables that regulate synaptic excitation and inhibition in the intact brain remain largely unknown. Here, we examined how spike transmission and suppression between principal cells (PCs) and interneurons (INTs) are modulated by activity history, brain state, cell type, and somatic distance between presynaptic and postsynaptic neurons by applying cross-correlogram analyses to datasets recorded from the dorsal hippocampus and medial entorhinal cortex (MEC) of 11 male behaving and sleeping Long Evans rats. The strength, temporal delay, and brain-state dependency of the spike transmission and suppression depended on the subregions/layers. The spike transmission probability of PC–INT excitatory pairs that showed short-term depression versus short-term facilitation was higher in CA1 and lower in CA3. Likewise, the intersomatic distance affected the proportion of PC–INT excitatory pairs that showed short-term depression and facilitation in the opposite manner in CA1 compared with CA3. The time constant of depression was longer, while that of facilitation was shorter in MEC than in CA1 and CA3. During sharp-wave ripples, spike transmission showed a larger gain in the MEC than in CA1 and CA3. The intersomatic distance affected the spike transmission gain during sharp-wave ripples differently in CA1 versus CA3. A subgroup of MEC layer 3 (EC3) INTs preferentially received excitatory inputs from and inhibited MEC layer 2 (EC2) PCs. The EC2 PC–EC3 INT excitatory pairs, most of which showed short-term depression, exhibited higher spike transmission probabilities than the EC2 PC–EC2 INT and EC3 PC–EC3 INT excitatory pairs. EC2 putative stellate cells exhibited stronger spike transmission to and received weaker spike suppression from EC3 INTs than EC2 putative pyramidal cells. This study provides detailed comparisons of monosynaptic interaction dynamics in the hippocampal–entorhinal loop, which may help to elucidate circuit operations.</p>","PeriodicalId":13171,"journal":{"name":"Hippocampus","volume":"34 8","pages":"393-421"},"PeriodicalIF":2.4000,"publicationDate":"2024-06-14","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://onlinelibrary.wiley.com/doi/epdf/10.1002/hipo.23612","citationCount":"0","resultStr":"{\"title\":\"Dynamics of spike transmission and suppression between principal cells and interneurons in the hippocampus and entorhinal cortex\",\"authors\":\"Motosada Iwase, Kamran Diba, Eva Pastalkova, Kenji Mizuseki\",\"doi\":\"10.1002/hipo.23612\",\"DOIUrl\":null,\"url\":null,\"abstract\":\"<p>Synaptic excitation and inhibition are essential for neuronal communication. However, the variables that regulate synaptic excitation and inhibition in the intact brain remain largely unknown. Here, we examined how spike transmission and suppression between principal cells (PCs) and interneurons (INTs) are modulated by activity history, brain state, cell type, and somatic distance between presynaptic and postsynaptic neurons by applying cross-correlogram analyses to datasets recorded from the dorsal hippocampus and medial entorhinal cortex (MEC) of 11 male behaving and sleeping Long Evans rats. The strength, temporal delay, and brain-state dependency of the spike transmission and suppression depended on the subregions/layers. The spike transmission probability of PC–INT excitatory pairs that showed short-term depression versus short-term facilitation was higher in CA1 and lower in CA3. Likewise, the intersomatic distance affected the proportion of PC–INT excitatory pairs that showed short-term depression and facilitation in the opposite manner in CA1 compared with CA3. The time constant of depression was longer, while that of facilitation was shorter in MEC than in CA1 and CA3. During sharp-wave ripples, spike transmission showed a larger gain in the MEC than in CA1 and CA3. The intersomatic distance affected the spike transmission gain during sharp-wave ripples differently in CA1 versus CA3. A subgroup of MEC layer 3 (EC3) INTs preferentially received excitatory inputs from and inhibited MEC layer 2 (EC2) PCs. The EC2 PC–EC3 INT excitatory pairs, most of which showed short-term depression, exhibited higher spike transmission probabilities than the EC2 PC–EC2 INT and EC3 PC–EC3 INT excitatory pairs. EC2 putative stellate cells exhibited stronger spike transmission to and received weaker spike suppression from EC3 INTs than EC2 putative pyramidal cells. This study provides detailed comparisons of monosynaptic interaction dynamics in the hippocampal–entorhinal loop, which may help to elucidate circuit operations.</p>\",\"PeriodicalId\":13171,\"journal\":{\"name\":\"Hippocampus\",\"volume\":\"34 8\",\"pages\":\"393-421\"},\"PeriodicalIF\":2.4000,\"publicationDate\":\"2024-06-14\",\"publicationTypes\":\"Journal Article\",\"fieldsOfStudy\":null,\"isOpenAccess\":false,\"openAccessPdf\":\"https://onlinelibrary.wiley.com/doi/epdf/10.1002/hipo.23612\",\"citationCount\":\"0\",\"resultStr\":null,\"platform\":\"Semanticscholar\",\"paperid\":null,\"PeriodicalName\":\"Hippocampus\",\"FirstCategoryId\":\"3\",\"ListUrlMain\":\"https://onlinelibrary.wiley.com/doi/10.1002/hipo.23612\",\"RegionNum\":3,\"RegionCategory\":\"医学\",\"ArticlePicture\":[],\"TitleCN\":null,\"AbstractTextCN\":null,\"PMCID\":null,\"EPubDate\":\"\",\"PubModel\":\"\",\"JCR\":\"Q3\",\"JCRName\":\"NEUROSCIENCES\",\"Score\":null,\"Total\":0}","platform":"Semanticscholar","paperid":null,"PeriodicalName":"Hippocampus","FirstCategoryId":"3","ListUrlMain":"https://onlinelibrary.wiley.com/doi/10.1002/hipo.23612","RegionNum":3,"RegionCategory":"医学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q3","JCRName":"NEUROSCIENCES","Score":null,"Total":0}
引用次数: 0
摘要
突触兴奋和抑制是神经元交流的基本要素。然而,调节完整大脑中突触兴奋和抑制的变量在很大程度上仍是未知的。在这里,我们通过对 11 只雄性行为和睡眠 Long Evans 大鼠的海马背侧和内侧内耳皮层(MEC)记录的数据集进行交叉相关图分析,研究了主细胞(PCs)和中间神经元(INTs)之间的尖峰传递和抑制如何受活动历史、大脑状态、细胞类型以及突触前和突触后神经元之间的体细胞距离的调节。尖峰传递和抑制的强度、时间延迟和脑状态依赖性取决于亚区/层。表现出短期抑制与短期促进的PC-IN兴奋对的尖峰传递概率在CA1较高,在CA3较低。同样,与 CA3 相比,CA1 中出现短期抑制和短期促进的 PC-INT 兴奋剂对的比例受腔间距离的影响恰恰相反。与 CA1 和 CA3 相比,MEC 中抑制的时间常数更长,而促进的时间常数更短。在尖波波纹过程中,尖峰传递在MEC比在CA1和CA3表现出更大的增益。在CA1和CA3中,节间距离对尖峰传递增益的影响不同。MEC第3层(EC3)INT的一个亚群优先接收来自MEC第2层(EC2)PC的兴奋性输入,并抑制MEC第2层(EC2)PC。与 EC2 PC-EC2 INT 和 EC3 PC-EC3 INT 的兴奋对相比,EC2 PC-EC3 INT 的兴奋对(其中大部分表现出短期抑制)表现出更高的尖峰传递概率。与 EC2 拟锥体细胞相比,EC2 拟星状细胞对 EC3 INT 的尖峰传递更强,而从 EC3 INT 受到的尖峰抑制更弱。这项研究提供了海马-大脑环路中单突触相互作用动态的详细比较,可能有助于阐明环路的运作。
Dynamics of spike transmission and suppression between principal cells and interneurons in the hippocampus and entorhinal cortex
Synaptic excitation and inhibition are essential for neuronal communication. However, the variables that regulate synaptic excitation and inhibition in the intact brain remain largely unknown. Here, we examined how spike transmission and suppression between principal cells (PCs) and interneurons (INTs) are modulated by activity history, brain state, cell type, and somatic distance between presynaptic and postsynaptic neurons by applying cross-correlogram analyses to datasets recorded from the dorsal hippocampus and medial entorhinal cortex (MEC) of 11 male behaving and sleeping Long Evans rats. The strength, temporal delay, and brain-state dependency of the spike transmission and suppression depended on the subregions/layers. The spike transmission probability of PC–INT excitatory pairs that showed short-term depression versus short-term facilitation was higher in CA1 and lower in CA3. Likewise, the intersomatic distance affected the proportion of PC–INT excitatory pairs that showed short-term depression and facilitation in the opposite manner in CA1 compared with CA3. The time constant of depression was longer, while that of facilitation was shorter in MEC than in CA1 and CA3. During sharp-wave ripples, spike transmission showed a larger gain in the MEC than in CA1 and CA3. The intersomatic distance affected the spike transmission gain during sharp-wave ripples differently in CA1 versus CA3. A subgroup of MEC layer 3 (EC3) INTs preferentially received excitatory inputs from and inhibited MEC layer 2 (EC2) PCs. The EC2 PC–EC3 INT excitatory pairs, most of which showed short-term depression, exhibited higher spike transmission probabilities than the EC2 PC–EC2 INT and EC3 PC–EC3 INT excitatory pairs. EC2 putative stellate cells exhibited stronger spike transmission to and received weaker spike suppression from EC3 INTs than EC2 putative pyramidal cells. This study provides detailed comparisons of monosynaptic interaction dynamics in the hippocampal–entorhinal loop, which may help to elucidate circuit operations.
期刊介绍:
Hippocampus provides a forum for the exchange of current information between investigators interested in the neurobiology of the hippocampal formation and related structures. While the relationships of submitted papers to the hippocampal formation will be evaluated liberally, the substance of appropriate papers should deal with the hippocampal formation per se or with the interaction between the hippocampal formation and other brain regions. The scope of Hippocampus is wide: single and multidisciplinary experimental studies from all fields of basic science, theoretical papers, papers dealing with hippocampal preparations as models for understanding the central nervous system, and clinical studies will be considered for publication. The Editor especially encourages the submission of papers that contribute to a functional understanding of the hippocampal formation.