The amygdala, a complex array of nuclei in the forebrain, controls emotions and emotion-related behaviors in vertebrates. Current research aims to understand the amygdala’s evolution in ray-finned fish such as zebrafish because of the region’s relevance for social behavior and human psychiatric disorders. Clear-cut molecular definitions of the amygdala and its evolutionary-developmental relationship to the one of mammals are critical for zebrafish models of affective disorders and autism. In this review, I argue that the prosomeric model and a focus on the olfactory system’s organization provide ideal tools for discovering deep ancestral relationships between the emotional systems of zebrafish and mammals. The review’s focus is on the “extended amygdala,” which refers to subpallial amygdaloid territories including the central (autonomic) and the medial (olfactory) amygdala required for reproductive and social behaviors. Amphibians, sauropsids, and lungfish share many characteristics with the basic amygdala ground plan of mammals, as molecular and hodological studies have shown. Further exploration of the evolution of the amygdala in basally derived fish vertebrates requires researchers to test these “tetrapod-based” concepts. Historically, this has been a daunting task because the forebrains of basally derived fish vertebrates look very different from those of more familiar tetrapod ones. An extreme case are ray-finned fish (Actinopterygii) like zebrafish, because their telencephalon develops through a distinct outward-growing process called eversion. To this day, scientists have struggled to determine how the everted telencephalon compares to non-actinopterygian vertebrates. Using the teleost zebrafish as a genetic model, comparative neurologists began to establish quantifiable molecular definitions that allow direct comparisons between ray-finned fish and tetrapods. In this review, I discuss how the most recent discovery of the zebrafish amygdala ground plan offers an opportunity to identify the developmental constraints of amygdala evolution and function. In addition, I explain how the zebrafish prethalamic eminence (PThE) topologically relates to the medial amygdala proper and the nucleus of the lateral olfactory tract (nLOT). In fact, I consider these previously misinterpreted olfactory structures the most critical missing evolutionary links between actinopterygian and tetrapod amygdalae. In this context, I will also explain why recognizing both the PThE and the nLOT is crucial to understanding the telencephalon eversion. Recognizing these anatomical hallmarks allows direct comparisons of the amygdalae of zebrafish and mammals. Ultimately, the new concepts of the zebrafish amygdala will overcome current dogmas and reach a holistic understanding of amygdala circuits of cognition and emotion in actinopterygians.


中文翻译：

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辐鳍鱼外翻的杏仁核——斑马鱼就是一个例子

杏仁核是前脑中的一组复杂核，控制着脊椎动物的情绪和与情绪相关的行为。目前的研究旨在了解斑马鱼等射线鳍鱼的杏仁核进化，因为该区域与社会行为和人类精神疾病相关。杏仁核的明确分子定义及其与哺乳动物之一的进化-发育关系对于斑马鱼情感障碍和自闭症模型至关重要。在这篇综述中，我认为前体模型和对嗅觉系统组织的关注为发现斑马鱼和哺乳动物情感系统之间深厚的祖先关系提供了理想的工具。审查的重点是“扩展的杏仁核，”指的是亚杏仁核区域，包括生殖和社会行为所需的中央（自主神经）和内侧（嗅觉）杏仁核。分子和动物学研究表明，两栖动物、蜥脚类动物和肺鱼与哺乳动物的基本杏仁核平面图有许多共同特征。进一步探索基底来源的鱼类脊椎动物杏仁核的进化需要研究人员测试这些“基于四足动物”的概念。从历史上看，这是一项艰巨的任务，因为基底来源的鱼类脊椎动物的前脑看起来与更熟悉的四足动物的前脑非常不同。一个极端的例子是像斑马鱼这样的辐鳍鱼 (Actinopterygii)，因为它们的端脑通过一种称为外翻的独特向外生长过程发育。到今天，科学家们一直在努力确定外翻端脑与非放线鳍脊椎动物的比较。使用硬骨鱼斑马鱼作为遗传模型，比较神经学家开始建立可量化的分子定义，以便直接比较射线鳍鱼和四足动物。在这篇综述中，我讨论了斑马鱼杏仁核平面图的最新发现如何为确定杏仁核进化和功能的发育限制提供了机会。此外，我还解释了斑马鱼前丘脑隆起 (PThE) 在拓扑学上如何与内侧杏仁核和外侧嗅束核 (nLOT) 相关。事实上，我认为这些以前被误解的嗅觉结构是放线纲和四足类杏仁核之间最关键的缺失进化联系。在这种情况下，我还将解释为什么识别 PThE 和 nLOT 对于理解端脑外翻至关重要。认识到这些解剖学特征可以直接比较斑马鱼和哺乳动物的杏仁核。最终，斑马鱼杏仁核的新概念将克服当前的教条，并全面了解放线纲动物的杏仁核认知和情感回路。