The Nobel Institute for Neurophysiology, Department of Neuroscience, Karolinska Institutet, SE-171 77 Stockholm, Sweden.
Curr Biol. 2011 Jul 12;21(13):1081-91. doi: 10.1016/j.cub.2011.05.001. Epub 2011 Jun 23.
Although the basal ganglia are thought to play a key role in action selection in mammals, it is unknown whether this mammalian circuitry is present in lower vertebrates as a conserved selection mechanism. We aim here, using lamprey, to elucidate the basal ganglia circuitry in the phylogenetically oldest group of vertebrates (cyclostomes) and determine how this selection architecture evolved to accommodate the increased behavioral repertoires of advanced vertebrates.
We show, using immunohistochemistry, tract tracing, and whole-cell recordings, that all parts of the mammalian basal ganglia (striatum, globus pallidus interna [GPi] and externa [GPe], and subthalamic nucleus [STN]) are present in the lamprey forebrain. In addition, the circuit features, molecular markers, and physiological activity patterns are conserved. Thus, GABAergic striatal neurons expressing substance P project directly to the pallidal output layer, whereas enkephalin-expressing striatal neurons project indirectly via nuclei homologous to the GPe and STN. Moreover, pallidal output neurons tonically inhibit tectum, mesencephalic, and diencephalic motor regions.
These results show that the detailed basal ganglia circuitry is present in the phylogenetically oldest vertebrates and has been conserved, most likely as a mechanism for action selection used by all vertebrates, for over 560 million years. Our data also suggest that the mammalian basal ganglia evolved through a process of exaptation, where the ancestral core unit has been co-opted for multiple functions, allowing them to process cognitive, emotional, and motor information in parallel and control a broader range of behaviors.
尽管基底神经节被认为在哺乳动物的动作选择中起着关键作用，但尚不清楚这种哺乳动物的回路是否存在于更低等的脊椎动物中，作为一种保守的选择机制。我们的目的是使用七鳃鳗来阐明在进化上最古老的脊椎动物（圆口类）中的基底神经节回路，并确定这种选择结构是如何进化以适应高级脊椎动物不断增加的行为范围的。
我们通过免疫组织化学、轨迹追踪和全细胞记录显示，哺乳动物基底神经节的所有部分（纹状体、苍白球内（GPi）和外（GPe）部以及丘脑下核（STN））都存在于七鳃鳗的前脑中。此外，回路特征、分子标记和生理活动模式都是保守的。因此，表达 P 物质的 GABA 能纹状体神经元直接投射到苍白球的输出层，而表达脑啡肽的纹状体神经元则通过与 GPe 和 STN 同源的核间接投射。此外，苍白球的输出神经元对顶盖、中脑和间脑的运动区进行紧张性抑制。
这些结果表明，详细的基底神经节回路存在于进化上最古老的脊椎动物中，并得到了保守，很可能作为所有脊椎动物使用的动作选择机制，已经存在超过 5.6 亿年了。我们的数据还表明，哺乳动物的基底神经节是通过适应化的过程进化而来的，其中祖先的核心单元被用于多种功能，使它们能够并行处理认知、情感和运动信息，并控制更广泛的行为。
