Department of Cell Biology, Faculty of Biology, University Complutense, 28040, Madrid, Spain.
Brain Struct Funct. 2020 Sep;225(7):2239-2269. doi: 10.1007/s00429-020-02123-5. Epub 2020 Aug 2.
The organization of the pallial derivatives across vertebrates follows a comparable elementary arrangement, although not all of them possess a layered cortical structure as sophisticated as the cerebral cortex of mammals. However, its expansion along evolution has only been possible by the development and coevolution of the cellular networks formed by excitatory neurons and inhibitory interneurons. Thus, the comparative analysis of interneuron types in vertebrate models of key evolutionary significance will provide important information, due to the extraordinary anatomical sophistication of their interneuron systems with simpler behavioral implications. Particularly in mammals, the main consensus for classifying interneuron types is based on non-overlapping markers, which do not form a single population, but consist of several distinct classes of inhibitory cells showing co-expression of other markers. In our study, we analyzed immunohistochemically the expression of the main markers like somatostatin (SOM), parvalbumin (PV), calretinin (CR), calbindin (CB), neuropeptide Y (NPY) and/or nitric oxide synthase (NOS) at the pallial regions of three different models of Osteichthyes. First, we selected two tetrapods, one amniote from the genus Pseudemys belonging to the order Testudine, at the base of the amniote diversification and with a three-layered simple cortex, and the Anuran Xenopus laevis, an anamniote tetrapod with a non-layered evaginated pallium, and finally the order Polypteriform, a small fish group at the base of the actinopterygian diversification with an everted telencephalon. SOM was the most conserved interneuron type in terms of its distribution and co-expression with other markers such as CR, in contrast to PV, which showed a different pattern between the models analyzed. In addition, the SOM expression supports a homological relationship between the medial pallial derivatives in all the models. CR and CB expressions in the tetrapods were observed, particularly, CR expressing cells were detected in the medial and the dorsal pallial derivatives, in contrast to CB, which appeared only in discrete scattered populations. However, the pallium of Polypteriforms fishes was almost devoid of CR cells, in contrast to the important number of CB cells observed in all the pallial regions. The NPY immunoreactivity was detected in all the pallial domains of all the models, as well as cells coexpressing CR. Finally, the pallial nitrergic expression was also conserved, which allows to postulate the homological relationships between the ventropallial and the amygdaloid derivatives. In summary, even in basal pallial models the neurochemically characterized interneurons indicate that their first appearance took place before the common ancestor of amniotes. Thus, our results suggest a shared pattern of interneuron types in the pallium of all Osteichthyes.
神经嵴衍生物在脊椎动物中的组织排列遵循类似的基本模式,尽管并非所有脊椎动物都具有像哺乳动物大脑皮层那样复杂的分层皮质结构。然而,其沿着进化的扩展仅通过兴奋性神经元和抑制性中间神经元组成的细胞网络的发展和共同进化才成为可能。因此,对关键进化意义的脊椎动物模型中的中间神经元类型进行比较分析将提供重要信息,因为其中间神经元系统具有更简单的行为影响,但具有非凡的解剖复杂性。特别是在哺乳动物中,中间神经元类型的主要分类共识基于不重叠的标志物,这些标志物不形成单一群体,而是由几个不同类别的抑制性细胞组成,这些细胞表现出其他标志物的共表达。在我们的研究中,我们分析了三种不同的硬骨鱼类脑区的主要标志物的免疫组织化学表达,如生长抑素(SOM)、副甲状腺素(PV)、钙调蛋白(CR)、钙结合蛋白(CB)、神经肽 Y(NPY)和/或一氧化氮合酶(NOS)。首先,我们选择了两种四足动物,一种是来自龟鳖目属的羊膜动物,属于龟鳖目,是羊膜动物多样化的基础,具有三层简单的皮质,另一种是无羊膜的非洲爪蟾,一种具有非分层外生脑区的四足动物,最后是多鳍鱼目,一种位于肉鳍鱼多样化基础的小鱼群,具有外向的端脑。SOM 是分布最保守的中间神经元类型,与其他标志物如 CR 共表达,而 PV 则表现出分析模型之间的不同模式。此外,SOM 的表达支持所有模型中内侧脑区衍生物之间的同源关系。在四足动物中观察到 CR 和 CB 的表达,特别是在背侧和内侧脑区衍生物中检测到表达 CR 的细胞,而 CB 仅出现在离散的散在群体中。然而,多鳍鱼的脑区几乎没有 CR 细胞,而在所有脑区都观察到大量的 CB 细胞。所有模型的所有脑区都检测到 NPY 免疫反应性,以及共表达 CR 的细胞。最后,脑区的硝化表达也得到了保留,这使得可以假设在腹侧脑区和杏仁核衍生物之间存在同源关系。总之,即使在基础脑区模型中,神经化学特征化的中间神经元也表明它们的首次出现发生在羊膜动物的共同祖先之前。因此,我们的结果表明,所有硬骨鱼类的脑区都具有共享的中间神经元类型模式。