Evolution of Neural Circuits for Locomotion

不同种类的动物表现出不同的行为，这些行为是由每种动物大脑中潜在的神经回路产生的。为了理解不同的行为是如何进化的，有必要比较近亲物种的神经回路是如何不同的。这个项目的目标是解决三个关于神经回路进化的基本问题：1)相似的神经系统如何产生不同的行为？2)不同动物的行为不同，但相同的神经元是否具有相似的功能？3)不同谱系动物的神经系统是如何产生相同行为的？本研究通过检查裸鳃软体动物（也称为海蛞蝓）中已鉴定的同源神经元的系统发育变化来解决这些问题。裸鳃动物有简单的神经系统，具有可单独识别的神经元，这些神经元构成了三种不同类型的运动行为：爬行和两种类型的游泳：一些海蛞蝓通过身体侧向弯曲游泳，而其他海蛞蝓通过身体背侧/腹侧弯曲游泳。不同的游泳行为在不同裸鳃动物谱系中多次独立出现。研究运动中已识别神经元的功能和特性的系统发育差异将有助于确定这些海蛞蝓在进化史中行为是如何变化的，也将有助于理解任何生物中与行为相关的神经回路是如何变化的。密切相关的裸枝可以表现出不同的行为，这些行为通常与神经元的性质和连接的物种差异有关。本项目比较了四种密切相关的物种：Tritonia diomedea（背/腹侧游泳者）、Melibe leonina和Dendronotus iris（均为侧游泳者）和Tochuina tetraquetra（非游泳者）产生不同行为的同源神经元的神经生理特性和突触连接。该项目的这一部分将把神经生理学与行为联系起来，以确定神经元的哪些特征或它们的回路连接在功能上是重要的。然后，神经生理特性的功能将直接使用一种称为动态钳的电生理技术来人工改变同源神经元的膜和突触特性。如果神经元的特性可以被电转化，使它们的活动更接近于其他物种的同源神经元，并产生该物种的典型游泳行为，那么这些神经特性在行为的产生中起因果作用将是强有力的证据。尽管一些密切相关的裸支动物在行为上存在很大差异，但在已识别的神经元功能上可能存在潜在的相似性。该项目的第二个目标是寻找具有不同行为的物种中同源神经元的保守行为功能。这将为理解神经回路的共享组织提供一个基础，这构成了衍生行为建立的基础。远亲裸鳃也可以表现出类似的行为。游泳行为的系统发育分布表明，它们是多次独立出现的。该项目的第三个目的是测试相同运动行为的独立进化是由收敛进化还是平行进化引起的。我们将对具有相同游泳行为的不同谱系裸鳃动物的同源神经元的功能进行测试。拟研究的物种对为背/腹侧游远亲的Aphelodoris antillensis和Tritonia diomedea，以及侧侧游远亲的Flabellina iodinea和Melibe leonina。如果同源神经元在不同的谱系中以同样的方式、为了同样的目的被独立地使用，那么这将表明游泳行为的相似性是通过平行进化产生的。这表明，神经回路的组成部分就像积木一样，可以以同样的方式拆卸和重新组装。或者，如果发现由于趋同进化导致行为彼此相似，则表明存在多种神经系统配置可以产生相同的行为输出。该项目旨在让本科生参与研究计划。已经建立了具体机制，以加强历史上代表性不足的族裔群体的参与。计划将这个项目作为一种工具，利用佐治亚州立大学的生物巴士在中学教授动物多样性和进化，并在亚特兰大的新佐治亚水族馆举办关于海蛞蝓的公共展览。

Award AbstractDifferent species of animals display disparate behaviors that are produced by underlying neural circuits in the brains of each animal. To understand how different behaviors may have evolved, it is necessary to compare how the neural circuits in closely related species differ. The objective of this project is to address three fundamental questions about the evolution of neural circuits underlying behavior: 1) How do similar nervous systems produce different behaviors? 2) Can the same neurons in different species have similar functions even though the behaviors of the animals differ? 3) How do nervous systems in animals of different lineages produce the same behavior? This study addresses these questions by examining phylogenetic changes in identified homologous neurons in nudibranch mollusks, also known as sea slugs. Nudibranchs have simple nervous systems with individually identifiable neurons that underly three different types of locomotor behavior: crawling and two types of swimming: some sea slugs swim by lateral body flexions and others swim by dorsal/ventral body flexions. The divergent swimming behaviors arose independently multiple times in different nudibranch lineages. Studying phylogenetic differences in the functions and properties of identified neurons underlying locomotion will help determine how the behaviors changed during the evolutionary history of these sea slugs and will also provide understanding of how behaviorally relevant neural circuits can change in any creature.Closely-related nudibranchs can exhibit divergent behaviors that are often associated with species-differences in the properties and connections of the underlying neurons. This project compares the neurophysiological properties and synaptic connections of homologous neurons that produce different behaviors in four closely-related species: Tritonia diomedea (a dorsal/ventral swimmer), Melibe leonina and Dendronotus iris (both lateral swimmers), and Tochuina tetraquetra (a non-swimmer). This part of the project will correlate neurophysiology with behavior to determine which features of the neurons or their circuit connections are functionally important. The functions of the neurophysiological properties then will be tested directly using an electrophysiological technique called dynamic clamp to artificially transform the membrane and synaptic properties of homologous neurons. If the properties of neurons can be electrically transformed so their activity more closely resembles that of the homologous neurons in other species and swim behavior typical of that species is produced, then it would be strong evidence that those neural properties play a causal role in the production of behavior.Despite large differences in the behaviors of some closely-related nudibranchs, there likely will be underlying similarities in the functions of identified neurons. The second aim of the project is to look for conserved behavioral functions of homologous neurons in species with divergent behaviors. This will provide a basis for understanding the shared organization of the neural circuits, which forms the foundation upon which the derived behaviors are built.Distantly-related nudibranchs can also display similar behaviors. The phylogenetic distribution of swim behaviors suggests that they arose independently multiple times. The third aim of this project is to test whether independent evolution of the same motor behavior was caused by convergent or parallel evolution. The functions of homologous neurons in nudibranchs of different lineages that exhibit the same swimming behavior will be tested. The species pairs to be examined are Aphelodoris antillensis and Tritonia diomedea, distantly related dorsal /ventral swimmers, and Flabellina iodinea and Melibe leonina, distantly related lateral swimmers. If homologous neurons came to be used in the same way, for the same purpose, independently in different lineages, then it would indicate that the similarity in the swimming behavior arose through parallel evolution. This would suggest that components of neural circuits are like building blocks that can be taken apart and reassembled in the same way. Alternatively, if it is found that the behaviors resemble each other because of convergent evolution, then it would indicate that there are multiple configurations of nervous systems that can produce the same behavioral output. The project is designed to involve undergraduate students in the research plan. Specific mechanisms are in place to enhance the participation of historically under-represented ethnic groups. Plans have been made to use this project as a tool to teach about animal diversity and evolution in secondary schools using Georgia State University's Bio-Bus and to develop public exhibits on sea slugs at the new Georgia Aquarium in Atlanta.