Evolutionary specialization of neuronal core circuits in arthropod olfactory systems: structure and function of convergence/divergence in crustaceans versus insects

根据最近所有的分子系统发育学，昆虫必须被认为是起源于海洋甲壳类的一个非常成功的陆生动物群体。这两个类群用于远距离嗅觉的主要化学感觉器官是最前面的一对头部附属物，即中脑触角。与触角上的感受器相关的嗅觉感觉神经元将其轴突投射到大脑的主要嗅觉中心，即两侧成对的触角叶（昆虫）/嗅觉叶（甲壳类动物）。在那里，感觉嗅觉传入事件与两类嗅觉中间神经元（OSNs），局部嗅觉中间神经元（LNs）和嗅觉投射神经元（PNs）在专门的神经隔室嗅觉肾小球内发生突触。尽管甲壳类动物和昆虫的肾小球内的主要线路模式有许多相似之处，但这些嗅觉核心回路也存在着明显的差异。因此，对于那些对分析神经元核心电路的进化多样化感兴趣的人来说，这个系统可以被视为一个理想的游乐场。例如，我们在PP阶段1的结果强烈表明，目前被描述为“典型嗅觉系统组织”的东西，例如在基准系统中，黑腹果蝇可能是从分布式表示/组合编码进化而来的衍生特征状态，并且越来越多的甲壳类动物和昆虫内部的例子出现了偏离这种模式。通过比较昆虫和甲壳类动物，我们可以研究过去进化优化过程的终点。该项目汇集了两位甲壳类动物（HAR）和昆虫（RYB）嗅觉系统的功能和进化形态学专家以及一位在节肢动物嗅觉系统（NAW）方面具有强大背景的计算神经科学家。在延长提案中，我们希望继续我们在PP第一阶段的成功合作，并在非模式昆虫和甲壳类动物的中枢嗅觉通路的神经解剖学方面获得更详细的见解，而不是已经研究得很好的模式系统D. melanogaster。通过量化所涉及的神经元元素（嗅觉感觉神经元、局部嗅觉中间神经元、投射神经元、嗅觉肾小球）的数量，并通过分析从OSN到PN到输出通路（蘑菇体）的投射学特征，我们将进一步了解节肢动物谱系中中枢嗅觉通路的分化与趋同和进化专门化。此外，通过获得超微结构数据，我们将继续了解osn与pn连通性的进化优化。最后，通过进一步进化不同节肢动物谱系嗅觉肾小球内信息处理的数学模型，我们希望进一步了解昆虫和甲壳类动物嗅觉编码机制的现有差异。

According to all recent molecular phylogenies, insects must be regarded as a highly successful terrestrial animal group that originated from marine crustaceans. The main chemosensory organ of both taxa for distance olfaction is the most anterior pair of head appendages, the deutocerebral antennae. Olfactory sensory neurons associated with sensilla on the antennae project their axons into the brain’s primary olfactory centres, the bilaterally paired antennal lobes (insects)/olfactory lobes (crustaceans). There, sensory olfactory afferents synapse with two classes of olfactory interneurons (OSNs), the local olfactory interneurons (LNs) and the olfactory projection neurons (PNs), within specialized neuropil compartments, the olfactory glomeruli. Although the principle wiring pattern within the glomeruli of crustaceans and insects share many similarities, nevertheless there also exist pronounced difference of these olfactory core circuits. Therefore, this system can be seen as an ideal playground for those interested in analysing evolutionary diversification of neuronal core circuits. For example, our results from phase 1 of the PP strongly suggest that what is currently described as „canonical olfactory system organization” e.g. in the benchmark system Drosophila melanogaster likely is a derived character state that evolved from a distributed representation / combinatorial coding, and more and more examples from crustaceans and from within the insects emerge as deviations from this pattern. By comparing insects and crustaceans we can study the end point of past evolutionary optimization processes. This project brings together two experts on the functional and evolutionary morphology of crustacean (HAR) and insect (RYB) olfactory system and a computational neuroscientist with a strong background in arthropod olfactory systems (NAW). In the prolongation proposal, we want to continue our successful collaboration from phase 1 of the PP and gain more detailed insights into the neuroanatomy of the central olfactory pathway in non-model insects and crustaceans beyond the well studied model system D. melanogaster. By quantifying the numbers of the involved neuronal elements (olfactory sensory neurons, local olfactory interneurons, projection neurons, olfactory glomeruli) and by analysing projectomic characteristics of the OSN to PN to output pathway (mushroom bodies) we will gain additional insights into divergence versus convergence and evolutionary specialization of the central olfactory pathways in arthropod lineages. Furthermore, by obtaining ultrastructural data we will continue to understand the evolutionary optimization of the connectivity of OSNs to PNs. Finally, by further evolving a mathematical model of information processing within olfactory glomeruli of different arthropod lineages as developed in phase 1, we want to further understand the existing differences of olfactory coding mechanisms in insects versus crustaceans.