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

根据最近的所有分子系统学，昆虫必须被认为是一个非常成功的陆地动物类群，起源于海洋甲壳类。这两个分类群对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轴突投射到大脑的初级嗅觉中心，即两侧成对的触角叶(昆虫)/嗅叶(甲壳类)。在那里，感觉嗅觉传入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)--在特殊的神经束隔室--嗅小球内--形成突触。尽管甲壳动物和昆虫肾小球内的主要连线模式有许多相似之处，但这些嗅觉核心回路也存在明显的差异。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，我们的PP第一阶段的结果强烈地表明，目前被描述为标准嗅觉系统组织的东西，例如在基准系统中，黑腹果蝇很可能是从分布式表示/组合编码进化而来的派生字符状态，并且越来越多来自甲壳类动物和昆虫内部的例子作为对该模式的偏离而出现。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。该项目汇集了甲壳类(HAR)和昆虫(RYB)嗅觉系统的功能和进化形态方面的两位专家和一位在节肢动物嗅觉系统(NAW)方面具有丰富背景的计算神经学家。在延期提案中，我们希望从PP的第一阶段开始继续我们的成功合作，并在经过充分研究的模式系统D.Blackogaster之外，对非模式昆虫和甲壳类动物的中枢嗅觉通路的神经解剖学获得更详细的见解。通过量化涉及的神经元成分(嗅觉神经元、局部嗅觉中间神经元、投射神经元、嗅小球)和分析OSN-PN-输出通路(蘑菇体)的投射特征，我们将获得更多关于节肢动物中枢嗅觉通路的发散与汇聚和进化专门化的见解。此外，通过获取超微结构数据，我们将继续了解OSN与PNS连接的进化优化。最后，通过进一步进化阶段1中发展的不同节肢动物的嗅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.