Medina Loreta, Abellán Antonio, Vicario Alba, Desfilis Ester
Laboratory of Brain Development and Evolution, Department of Experimental Medicine, Faculty of Medicine, University of Lleida, Institute of Biomedical Research of Lleida (IRBLleida), Lleida, Spain.
Brain Behav Evol. 2014;83(2):112-25. doi: 10.1159/000357832. Epub 2014 Apr 24.
Herein we take advantage of the evolutionary developmental biology approach in order to improve our understanding of both the functional organization and the evolution of the basal ganglia, with a particular focus on the globus pallidus. Therefore, we review data on the expression of developmental regulatory genes (that play key roles in patterning, regional specification and/or morphogenesis), gene function and fate mapping available in different vertebrate species, which are useful to (a) understand the embryonic origin and basic features of each neuron subtype of the basal ganglia (including neurotransmitter/neuropeptide expression and connectivity patterns); (b) identify the same (homologous) subpopulations in different species and the degree of variation or conservation throughout phylogeny, and (c) identify possible mechanisms that may explain the evolution of the basal ganglia. These data show that the globus pallidus of rodents contains two major subpopulations of GABAergic projection neurons: (1) neurons containing parvalbumin and neurotensin-related hexapetide (LANT6), with descending projections to the subthalamus and substantia nigra, which originate from progenitors expressing Nkx2.1, primarily located in the pallidal embryonic domain (medial ganglionic eminence), and (2) neurons containing preproenkephalin (and possibly calbindin), with ascending projections to the striatum, which appear to originate from progenitors expressing Islet1 in the striatal embryonic domain (lateral ganglionic eminence). Based on data on Nkx2.1, Islet1, LANT6 and proenkephalin, it appears that both cell types are also present in the globus pallidus/dorsal pallidum of chicken, frog and lungfish. In chicken, the globus pallidus also contains neurons expressing substance P (SP), perhaps originating in the striatal embryonic domain. In ray-finned and cartilaginous fishes, the pallidum contains at least the Nkx2.1 lineage cell population (likely representing the neurons containing LANT6). Based on the presence of neurons containing enkephalin or SP, it is possible that the pallidum of these animals also includes the Islet1 lineage cell subpopulation, and both neuron subtypes were likely present in the pallidum of the first jawed vertebrates. In contrast, lampreys (jawless fishes) appear to lack the pallidal embryonic domain and the Nkx2.1 lineage cell population that mainly characterize the pallidum in jawed vertebrates. In the absence of data in other jawless fishes, the ancestral condition in vertebrates remains to be elucidated. Perhaps, a major event in telencephalic evolution was the novel expression of Nkx2.1 in the subpallium, which has been related to Hedgehog expression and changes in the regulatory region of Nkx2.1.
在此，我们利用进化发育生物学方法，以增进对基底神经节功能组织和进化的理解，特别关注苍白球。因此，我们回顾了不同脊椎动物物种中有关发育调控基因（在模式形成、区域特化和/或形态发生中起关键作用）表达、基因功能和命运图谱的数据，这些数据有助于：（a）了解基底神经节各神经元亚型的胚胎起源和基本特征（包括神经递质/神经肽表达和连接模式）；（b）识别不同物种中相同（同源）的亚群以及整个系统发育过程中的变异或保守程度；（c）识别可能解释基底神经节进化的机制。这些数据表明，啮齿动物的苍白球包含两个主要的γ-氨基丁酸能投射神经元亚群：（1）含有小白蛋白和神经降压素相关六肽（LANT6）的神经元，其向下投射至丘脑底核和黑质，起源于表达Nkx2.1的祖细胞，主要位于苍白球胚胎区域（内侧神经节隆起）；（2）含有前脑啡肽原（可能还有钙结合蛋白）的神经元，其向上投射至纹状体，似乎起源于纹状体胚胎区域（外侧神经节隆起）中表达Islet1的祖细胞。基于有关Nkx2.1、Islet1、LANT6和脑啡肽原的数据，鸡、青蛙和肺鱼的苍白球/背侧苍白球中似乎也存在这两种细胞类型。在鸡中，苍白球还含有表达P物质（SP）的神经元，可能起源于纹状体胚胎区域。在硬骨鱼和软骨鱼中，苍白球至少包含Nkx2.1谱系细胞群（可能代表含有LANT6的神经元）。基于含有脑啡肽或SP的神经元的存在，这些动物的苍白球也可能包括Islet1谱系细胞亚群，并且这两种神经元亚型可能在第一批有颌脊椎动物的苍白球中就已存在。相比之下，七鳃鳗（无颌鱼类）似乎缺乏主要表征有颌脊椎动物苍白球的苍白球胚胎区域和Nkx2.1谱系细胞群。由于缺乏其他无颌鱼类的数据，脊椎动物的原始状态仍有待阐明。也许，端脑进化中的一个重大事件是Nkx2.1在大脑皮质下的新表达，这与刺猬蛋白表达以及Nkx2.1调控区域的变化有关。
