Arai Mary, Osanai Hisayuki, Snell Chris C, Gawf Kaylea E, Kitamura Takashi, Ogawa Sachie K
Department of Psychiatry, University of Texas Southwestern Medical Center, Dallas, Texas, USA.
Peter O'Donnell Jr. Brain Institute, University of Texas Southwestern Medical Center, Dallas, Texas, USA.
Hippocampus. 2025 Sep;35(5):e70030. doi: 10.1002/hipo.70030.
Expression of immediate early genes (IEGs) is critical for memory formation and has been widely used to identify the neural substrate of memory traces, termed memory engram cells. Functions of IEGs have been known to be different depending on their types. However, there is limited knowledge about the extent to which different types of IEGs are selectively or concurrently involved in the formation of memory engram. To address this question, we investigated the combinative expression of c-Fos, Arc, and Npas4 proteins using immunohistochemistry following aversive and rewarding experiences across subregions in the prefrontal cortex (PFC), basolateral amygdala (BLA), hippocampal dentate gyrus (DG), and retrosplenial cortex (RSC). Using an automated cell detection algorithm, we found that expression patterns of c-Fos, Npas4, and Arc varied across different brain areas, with a higher increase of IEG expressing cells in the PFC and posterior BLA than in the DG. The combinative expression patterns, along with their experience-induced changes, also differed across brain areas; the co-expression of IEGs increased in the PFC and BLA following experience, whereas the increase was less pronounced in the DG and RSC. Furthermore, we demonstrate that different area-to-area functional connectivity networks were extracted by different IEGs. These findings provide insights into how different IEGs and their combinations identify engram cells, which will contribute to a deeper understanding of the functional significance of IEG-tagged memory engram cells.
即刻早期基因(IEGs)的表达对记忆形成至关重要,并且已被广泛用于识别记忆痕迹的神经基质,即记忆印迹细胞。已知IEGs的功能因其类型而异。然而,关于不同类型的IEGs在多大程度上选择性或同时参与记忆印迹形成的了解有限。为了解决这个问题,我们在经历厌恶和奖赏体验后,通过免疫组织化学研究了前额叶皮质(PFC)、基底外侧杏仁核(BLA)、海马齿状回(DG)和压后皮质(RSC)各亚区域中c-Fos、Arc和Npas4蛋白的联合表达。使用自动细胞检测算法,我们发现c-Fos、Npas4和Arc的表达模式在不同脑区有所不同,PFC和BLA中表达IEG的细胞增加幅度高于DG。联合表达模式及其经验诱导的变化在不同脑区也存在差异;经历后PFC和BLA中IEGs的共表达增加,而DG和RSC中的增加不太明显。此外,我们证明不同的IEGs提取了不同的区域间功能连接网络。这些发现为不同的IEGs及其组合如何识别印迹细胞提供了见解,这将有助于更深入地理解IEG标记的记忆印迹细胞的功能意义。