Blackiston Douglas, Dromiack Hannah, Grasso Caitlin, Varley Thomas F, Moore Douglas G, Srinivasan Krishna Kannan, Sporns Olaf, Bongard Joshua, Levin Michael, Walker Sara I
Allen Discovery Center, Tufts University, Medford, Massachusetts, United States of America.
Wyss Institute for Biologically Inspired Engineering, Harvard University, Boston, Massachusetts, United States of America.
PLoS Comput Biol. 2025 Apr 14;21(4):e1012149. doi: 10.1371/journal.pcbi.1012149. eCollection 2025 Apr.
A central challenge in the progression of a variety of open questions in biology, such as morphogenesis, wound healing, and development, is learning from empirical data how information is integrated to support tissue-level function and behavior. Information-theoretic approaches provide a quantitative framework for extracting patterns from data, but so far have been predominantly applied to neuronal systems at the tissue-level. Here, we demonstrate how time series of Ca2+ dynamics can be used to identify the structure and information dynamics of other biological tissues. To this end, we expressed the calcium reporter GCaMP6s in an organoid system of explanted amphibian epidermis derived from the African clawed frog Xenopus laevis, and imaged calcium activity pre- and post- a puncture injury, for six replicate organoids. We constructed functional connectivity networks by computing mutual information between cells from time series derived using medical imaging techniques to track intracellular Ca2+. We analyzed network properties including degree distribution, spatial embedding, and modular structure. We find organoid networks exhibit potential evidence for more connectivity than null models, with our models displaying high degree hubs and mesoscale community structure with spatial clustering. Utilizing functional connectivity networks, our model suggests the tissue retains non-random features after injury, displays long range correlations and structure, and non-trivial clustering that is not necessarily spatially dependent. In the context of this reconstruction method our results suggest increased integration after injury, possible cellular coordination in response to injury, and some type of generative structure of the anatomy. While we study Ca2+ in Xenopus epidermal cells, our computational approach and analyses highlight how methods developed to analyze functional connectivity in neuronal tissues can be generalized to any tissue and fluorescent signal type. We discuss expanded methods of analyses to improve models of non-neuronal information processing highlighting the potential of our framework to provide a bridge between neuroscience and more basal modes of information processing.
在生物学中诸多开放性问题(如形态发生、伤口愈合和发育)的研究进程中,一个核心挑战是从经验数据中了解信息是如何整合以支持组织水平的功能和行为的。信息论方法提供了一个从数据中提取模式的定量框架,但迄今为止主要应用于组织水平的神经元系统。在这里,我们展示了如何利用Ca2+动态的时间序列来识别其他生物组织的结构和信息动态。为此,我们在源自非洲爪蟾非洲爪蟾的外植体两栖类表皮类器官系统中表达了钙报告基因GCaMP6s,并对六个重复的类器官在穿刺损伤前后的钙活性进行了成像。我们通过计算使用医学成像技术跟踪细胞内Ca2+得到的时间序列中细胞之间的互信息,构建了功能连接网络。我们分析了网络属性,包括度分布、空间嵌入和模块结构。我们发现类器官网络显示出比空模型具有更多连接性的潜在证据,我们的模型显示出高度中心节点和具有空间聚类的中尺度群落结构。利用功能连接网络,我们的模型表明组织在损伤后保留了非随机特征,显示出长程相关性和结构,以及不一定依赖空间的非平凡聚类。在这种重建方法的背景下,我们的结果表明损伤后整合增加,可能存在对损伤的细胞协调,以及某种类型的解剖学生成结构。虽然我们研究的是非洲爪蟾表皮细胞中的Ca2+,但我们的计算方法和分析突出了为分析神经元组织中的功能连接而开发的方法如何能够推广到任何组织和荧光信号类型。我们讨论了扩展的分析方法以改进非神经元信息处理模型,强调了我们的框架为神经科学和更基础的信息处理模式之间搭建桥梁的潜力。