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Structure and function of the gap junctional network of photoreceptive ganglion cells
Visual Neuroscience ( IF 1.1 ) Pub Date : 2021-09-16 , DOI: 10.1017/s0952523821000134
Xiwu Zhao 1 , Kwoon Y Wong 1, 2
Affiliation  

Intrinsically photosensitive retinal ganglion cells (ipRGCs) signal not only anterogradely to drive behavioral responses, but also retrogradely to some amacrine interneurons to modulate retinal physiology. We previously found that all displaced amacrine cells with spiking, tonic excitatory photoresponses receive gap-junction input from ipRGCs, but the connectivity patterns and functional roles of ipRGC-amacrine coupling remained largely unknown. Here, we injected PoPro1 fluorescent tracer into all six types of mouse ipRGCs to identify coupled amacrine cells, and analyzed the latter’s morphological and electrophysiological properties. We also examined how genetically disrupting ipRGC-amacrine coupling affected ipRGC photoresponses. Results showed that ipRGCs couple with not just ON- and ON/OFF-stratified amacrine cells in the ganglion-cell layer as previously reported, but also OFF-stratified amacrine cells in both ganglion-cell and inner nuclear layers. M1- and M3-type ipRGCs couple mainly with ON/OFF-stratified amacrine cells, whereas the other ipRGC types couple almost exclusively with ON-stratified ones. ipRGCs transmit melanopsin-based light responses to at least 93% of the coupled amacrine cells. Some of the ON-stratifying ipRGC-coupled amacrine cells exhibit transient hyperpolarizing light responses. We detected bidirectional electrical transmission between an ipRGC and a coupled amacrine cell, although transmission was asymmetric for this particular cell pair, favoring the ipRGC-to-amacrine direction. We also observed electrical transmission between two amacrine cells coupled to the same ipRGC. In both scenarios of coupling, the coupled cells often spiked synchronously. While ipRGC-amacrine coupling somewhat reduces the peak firing rates of ipRGCs’ intrinsic melanopsin-based photoresponses, it renders these responses more sustained and longer-lasting. In summary, ipRGCs’ gap junctional network involves more amacrine cell types and plays more roles than previously appreciated.

中文翻译:

感光神经节细胞间隙连接网络的结构与功能

本质上光敏性视网膜神经节细胞 (ipRGC) 不仅顺行发出信号以驱动行为反应,而且还逆行向一些无长突中间神经元发出信号以调节视网膜生理。我们之前发现所有具有尖峰、强直兴奋性光反应的移位无长突细胞都从 ipRGCs 接收间隙连接输入,但 ipRGC-无长突偶联的连接模式和功能作用在很大程度上仍然未知。在这里,我们将 PoPro1 荧光示踪剂注射到所有六种类型的小鼠 ipRGC 中,以识别偶联的无长突细胞,并分析后者的形态学和电生理学特性。我们还研究了基因破坏 ipRGC-无长突偶联如何影响 ipRGC 光反应。结果表明,ipRGC 不仅与先前报道的神经节细胞层中的 ON 和 ON/OFF 分层无长突细胞结合,而且还与神经节细胞层和内核层中的 OFF 分层无长突细胞结合。M1 和 M3 型 ipRGC 主要与 ON/OFF 分层无长突细胞耦合,而其他 ipRGC 类型几乎只与 ON 分层细胞耦合。ipRGC 将基于黑视蛋白的光响应传递给至少 93% 的偶联无长突细胞。一些 ON 分层 ipRGC 耦合的无长突细胞表现出瞬态超极化光反应。我们检测到 ipRGC 和耦合的无长突细胞之间的双向电传输,尽管传输对于这个特定的细胞对是不对称的,有利于 ipRGC 到无长突的方向。我们还观察到与同一 ipRGC 耦合的两个无长突细胞之间的电传输。在这两种耦合情况下,耦合的细胞通常同步出现峰值。虽然 ipRGC-无长突偶联在一定程度上降低了 ipRGC 内在的基于黑视蛋白的光反应的峰值放电率,但它使这些反应更加持久和持久。总之,ipRGC 的缝隙连接网络涉及更多的无长突细胞类型,并且发挥的作用比以前所认识的更多。
更新日期:2021-09-16
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