Department of Animal Physiology and Molecular Biomedicine, University of Giessen, Giessen, Germany.
Departamento de Biodiversidad y Biología Experimental, IBBEA-CONICET, Universidad de Buenos Aires, Buenos Aires, Argentina.
J Comp Neurol. 2020 Sep 1;528(13):2239-2253. doi: 10.1002/cne.24887. Epub 2020 Feb 27.
Individual receptor neurons in the peripheral olfactory organ extend long axons into the olfactory bulb forming synapses with projection neurons in spherical neuropil regions, called glomeruli. Generally, odor map formation and odor processing in all vertebrates is based on the assumption that receptor neuron axons exclusively connect to a single glomerulus without any axonal branching. We comparatively tested this hypothesis in multiple fish and amphibian species (both sexes) by applying sparse cell electroporation to trace single olfactory receptor neuron axons. Sea lamprey (jawless fish) and zebrafish (bony fish) support the unbranched axon concept, with 94% of axons terminating in single glomeruli. Contrastingly, axonal projections of the axolotl (salamander) branch extensively before entering up to six distinct glomeruli. Receptor neuron axons labeled in frog species (Pipidae, Bufonidae, Hylidae, and Dendrobatidae) predominantly bifurcate before entering a glomerulus and 59 and 50% connect to multiple glomeruli in larval and postmetamorphotic animals, respectively. Independent of developmental stage, lifestyle, and adaptations to specific habitats, it seems to be a common feature of amphibian olfactory receptor neuron axons to frequently bifurcate and connect to multiple glomeruli. Our study challenges the unbranched axon concept as a universal vertebrate feature and it is conceivable that also later diverging vertebrates deviate from it. We propose that this unusual wiring logic evolved around the divergence of the terrestrial tetrapod lineage from its aquatic ancestors and could be the basis of an alternative way of odor processing.
在周围嗅觉器官中的单个受体神经元将长轴突延伸到嗅球中，与球形神经胶区域（称为肾小球）中的投射神经元形成突触。通常，所有脊椎动物的气味图形成和气味处理都是基于这样的假设，即受体神经元轴突仅与单个肾小球连接，而没有任何轴突分支。我们通过对多种鱼类和两栖类物种（雌雄两性）进行稀疏细胞电穿孔来追踪单个嗅觉受体神经元轴突，从而比较性地检验了这一假说。海鳗（无颚鱼）和斑马鱼（硬骨鱼）支持无分支轴突概念，其中 94%的轴突终止于单个肾小球。相比之下，蝾螈（蝾螈）的轴突投射在进入多达六个不同的肾小球之前广泛分支。在青蛙物种（Piidae、Bufonidae、Hylidae 和 Dendrobatidae）中标记的受体神经元轴突在进入肾小球之前主要分叉，并且在幼虫和变态后动物中分别有 59%和 50%的轴突与多个肾小球连接。独立于发育阶段、生活方式和对特定栖息地的适应，两栖动物嗅觉受体神经元轴突经常分叉并与多个肾小球连接似乎是一个共同特征。我们的研究挑战了无分支轴突概念作为普遍的脊椎动物特征，并且可以想象，后来分化的脊椎动物也偏离了它。我们提出，这种不寻常的布线逻辑是围绕着陆地四足动物谱系与其水生祖先的分化而进化的，并且可能是另一种气味处理方式的基础。
