Ichijo Hiroyuki, Nakamura Tomoya, Kawaguchi Masahumi, Takeuchi Yuichi
Department of Anatomy and Neuroscience, Graduate School of Medicine and Pharmaceutical Sciences, University of Toyama Toyama, Japan.
Front Neurosci. 2017 Jan 4;10:595. doi: 10.3389/fnins.2016.00595. eCollection 2016.
Many vertebrates have asymmetrical circuits in the nervous system. There are two types of circuit asymmetry. Asymmetrical circuits in sensory and/or motor systems are usually related to lateralized behaviors. It has been hypothesized that spatial asymmetry in the environment and/or social interactions has led to the evolution of asymmetrical circuits by natural selection. There are also asymmetrical circuits that are not related to lateralized behaviors. These circuits lie outside of the sensory and motor systems. A typical example is found in the habenula (Hb), which has long been known to be asymmetrical in many vertebrates, but has no remarkable relationship to lateralized behaviors. Instead, the Hb is a hub wherein information conveyed to the unilateral Hb is relayed to diverging bilateral nuclei, which is unlikely to lead to lateralized behavior. Until now, there has been no hypothesis regarding the evolution of Hb asymmetry. Here, we propose a new hypothesis that binary opposition in functional incompatibility applies selection pressure on the habenular circuit and leads to asymmetry. Segregation of the incompatible functions on either side of the habenula is likely to enhance information processing ability via creating shorter circuits and reducing the cost of circuit duplication, resulting in benefits for survival. In zebrafish and mice, different evolutionary strategies are thought to be involved in Hb asymmetry. In zebrafish, which use a strategy of structurally fixed asymmetry, the asymmetrical dorsal Hb leads to constant behavioral choices in binary opposition. In contrast, in mice, which use a strategy of functionally flexible lateralization, the symmetrical lateral Hb is functionally lateralized. This makes it possible to process complicated information and to come to variable behavioral choices, depending on the specific situation. These strategies are thought to be selected for and preserved by evolution under selection pressures of rigidity and flexibility of sociability in zebrafish and mice, respectively, as they are beneficial for survival. This hypothesis is highly valuable because it explains how the Hb evolved differently in terms of asymmetry and lateralization among different species. In addition, one can propose possible experiments for the verification of this hypothesis in future research.
许多脊椎动物的神经系统中存在不对称回路。回路不对称有两种类型。感觉和/或运动系统中的不对称回路通常与偏侧化行为有关。据推测，环境和/或社会互动中的空间不对称通过自然选择导致了不对称回路的进化。也存在与偏侧化行为无关的不对称回路。这些回路位于感觉和运动系统之外。一个典型的例子是缰核（Hb），长期以来人们已知在许多脊椎动物中它是不对称的，但与偏侧化行为没有显著关系。相反，Hb是一个枢纽，其中传递到单侧Hb的信息被中继到不同的双侧核团，这不太可能导致偏侧化行为。到目前为止，还没有关于Hb不对称进化的假说。在这里，我们提出一个新的假说，即功能不相容中的二元对立对缰核回路施加选择压力并导致不对称。在缰核两侧分离不相容的功能可能通过创建更短的回路和降低回路复制成本来提高信息处理能力，从而带来生存优势。在斑马鱼和小鼠中，不同的进化策略被认为与Hb不对称有关。在斑马鱼中，它采用结构固定不对称的策略，不对称的背侧Hb导致在二元对立中做出恒定的行为选择。相比之下，在小鼠中，它采用功能灵活偏侧化的策略，对称的外侧Hb在功能上发生偏侧化。这使得根据具体情况处理复杂信息并做出可变的行为选择成为可能。这些策略被认为分别在斑马鱼和小鼠社交性的刚性和灵活性的选择压力下通过进化被选择和保留，因为它们有利于生存。这个假说非常有价值，因为它解释了Hb在不同物种之间如何在不对称和偏侧化方面以不同方式进化。此外，人们可以在未来的研究中提出可能的实验来验证这个假说。
